Advanced search
Publication Cover
Stress
The International Journal on the Biology of Stress
Volume 24, 2021 - Issue 2: Commemorating the 2nd Munich Stress Conference
Submit an article Journal homepage
1,266
Views
11
CrossRef citations to date
0
Altmetric
Reviews

Experience and activity-dependent control of glucocorticoid receptors during the stress response in large-scale brain networks

Damien Huzarda Department of Neuroscience and Physiology, University of Montpellier, CNRS, INSERM, Institut de Génomique Fonctionnelle, Montpellier, FranceORCID Iconhttps://orcid.org/0000-0003-4820-7951View further author information
ORCID Icon,
Virginie Rappeneaub Department of Behavioural Biology, University of Osnabrück, Osnabrück, GermanyORCID Iconhttps://orcid.org/0000-0001-5773-1275View further author information
ORCID Icon,
Onno C. Meijerc Division of Endocrinology, Department of Internal Medicine, Leiden University Medical Center, Leiden University, Leiden, The NetherlandsORCID Iconhttps://orcid.org/0000-0002-8394-6859View further author information
ORCID Icon,
Chadi Toumab Department of Behavioural Biology, University of Osnabrück, Osnabrück, GermanyView further author information
,
Margarita Arango-Lievanoa Department of Neuroscience and Physiology, University of Montpellier, CNRS, INSERM, Institut de Génomique Fonctionnelle, Montpellier, FranceORCID Iconhttps://orcid.org/0000-0002-9611-8032View further author information
ORCID Icon,
Michael J. Garabediand New York University Langone Medical Center, New York, NY, USAORCID Iconhttps://orcid.org/0000-0001-8915-7378View further author information
ORCID Icon &
Freddy Jeanneteaua Department of Neuroscience and Physiology, University of Montpellier, CNRS, INSERM, Institut de Génomique Fonctionnelle, Montpellier, FranceCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-9606-2892View further author information
ORCID Icon show all
Pages 130-153 | Received 30 Nov 2019, Accepted 02 Aug 2020, Published online: 26 Aug 2020

References

  • Adzic, M., Djordjevic, J., Djordjevic, A., Niciforovic, A., Demonacos, C., Radojcic, M., & Krstic-Demonacos, M. (2009). Acute or chronic stress induce cell compartment-specific phosphorylation of glucocorticoid receptor and alter its transcriptional activity in Wistar rat brain. The Journal of Endocrinology, 202(1), 87–97. https://doi.org/10.1677/JOE-08-0509
  • Akimoto, H., Oshima, S., Sugiyama, T., Negishi, A., Nemoto, T., & Kobayashi, D. (2019). Changes in brain metabolites related to stress resilience: Metabolomic analysis of the hippocampus in a rat model of depression. Behavioural Brain Research, 359, 342–352. https://doi.org/10.1016/j.bbr.2018.11.017
  • Alt, S. R., Turner, J. D., Klok, M. D., Meijer, O. C., Lakke, E. A., Derijk, R. H., & Muller, C. P. (2010). Differential expression of glucocorticoid receptor transcripts in major depressive disorder is not epigenetically programmed. Psychoneuroendocrinology, 35(4), 544–556. https://doi.org/10.1016/j.psyneuen.2009.09.001
  • Altarejos, J. Y., & Montminy, M. (2011). CREB and the CRTC co-activators: Sensors for hormonal and metabolic signals. Nature Reviews. Molecular Cell Biology, 12(3), 141–151. https://doi.org/10.1038/nrm3072
  • Altemus, M. (2006). Sex differences in depression and anxiety disorders: Potential biological determinants. Hormones and Behavior, 50(4), 534–538. https://doi.org/10.1016/j.yhbeh.2006.06.031
  • Ambroggi, F., Turiault, M., Milet, A., Deroche-Gamonet, V., Parnaudeau, S., Balado, E., Barik, J., van der Veen, R., Maroteaux, G., Lemberger, T., Schütz, G., Lazar, M., Marinelli, M., Piazza, P. V., & Tronche, F. (2009). Stress and addiction: Glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nature Neuroscience, 12(3), 247–249. https://doi.org/10.1038/nn.2282
  • Arango-Lievano, M., Borie, A. M., Dromard, Y., Murat, M., Desarmenien, M. G., Garabedian, M. J., & Jeanneteau, F. (2019). Persistence of learning-induced synapses depends on neurotrophic priming of glucocorticoid receptors. Proceedings of the National Academy of Sciences of the United States of America, 116(26), 13097–13106. https://doi.org/10.1073/pnas.1903203116
  • Arango-Lievano, M., & Jeanneteau, F. (2016). Timing and crosstalk of glucocorticoid signaling with cytokines, neurotransmitters and growth factors. Pharmacological Research, 113(Pt A), 1–17. https://doi.org/10.1016/j.phrs.2016.08.005
  • Arango-Lievano, M., Lambert, W. M., & Jeanneteau, F. (2015b). Molecular biology of glucocorticoid signaling. Advances in Experimental Medicine and Biology, 872, 33–57. https://doi.org/10.1007/978-1-4939-2895-8_2
  • Arango-Lievano, M., Lambert, W. M., Bath, K. G., Garabedian, M. J., Chao, M. V., & Jeanneteau, F. (2015a). Neurotrophic-priming of glucocorticoid receptor signaling is essential for neuronal plasticity to stress and antidepressant treatment. Proceedings of the National Academy of Sciences of the United States of America, 112(51), 15737–15742. https://doi.org/10.1073/pnas.1509045112
  • Arango-Lievano, M., Peguet, C., Catteau, M., Parmentier, M. L., Wu, S., Chao, M. V., Ginsberg, S. D., & Jeanneteau, F. (2016). Deletion of neurotrophin signaling through the glucocorticoid receptor pathway causes tau neuropathology. Scientific Reports, 6, 37231. https://doi.org/10.1038/srep37231
  • Arnett, M. G., Muglia, L. M., Laryea, G., & Muglia, L. J. (2016). Genetic approaches to hypothalamic-pituitary-adrenal axis regulation. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 41(1), 245–260. https://doi.org/10.1038/npp.2015.215
  • Autry, A. E., & Monteggia, L. M. (2012). Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacological Reviews, 64(2), 238–258. https://doi.org/10.1124/pr.111.005108
  • Avey, D., Sankararaman, S., Yim, A. K. Y., Barve, R., Milbrandt, J., & Mitra, R. D. (2018). Single-cell RNA-Seq uncovers a robust transcriptional response to morphine by glia. Cell Reports, 24(13), 3619–3629.e4. https://doi.org/10.1016/j.celrep.2018.08.080
  • Bangasser, D. A., & Valentino, R. J. (2014). Sex differences in stress-related psychiatric disorders: Neurobiological perspectives. Frontiers in Neuroendocrinology, 35(3), 303–319. https://doi.org/10.1016/j.yfrne.2014.03.008
  • Bangasser, D. A., & Wiersielis, K. R. (2018). Sex differences in stress responses: A critical role for corticotropin-releasing factor. Hormones (Athens, Greece), 17(1), 5–13. https://doi.org/10.1007/s42000-018-0002-z
  • Barfield, E. T., & Gourley, S. L. (2018). Prefrontal cortical trkB, glucocorticoids, and their interactions in stress and developmental contexts. Neuroscience & Biobehavioral Reviews, 95, 535–558. https://doi.org/10.1016/j.neubiorev.2018.10.015
  • Barford, K., Deppmann, C., & Winckler, B. (2017). The neurotrophin receptor signaling endosome: Where trafficking meets signaling. Developmental Neurobiology, 77(4), 405–418. https://doi.org/10.1002/dneu.22427
  • Barik, J., Marti, F., Morel, C., Fernandez, S. P., Lanteri, C., Godeheu, G., Tassin, J. P., Mombereau, C., Faure, P., & Tronche, F. (2013). Chronic stress triggers social aversion via glucocorticoid receptor in dopaminoceptive neurons. Science (New York, N.Y.), 339(6117), 332–335. https://doi.org/10.1126/science.1226767
  • Barnes, P. J. (2009). Role of HDAC2 in the pathophysiology of COPD. Annual Review of Physiology, 71, 451–464. https://doi.org/10.1146/annurev.physiol.010908.163257
  • Barnes, P. J. (2013). Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. The Journal of Allergy and Clinical Immunology, 131(3), 636–645. https://doi.org/10.1016/j.jaci.2012.12.1564
  • Bartlett, A., Lapp, H., & Hunter, R. (2019). Epigenetic mechanisms of the glucocorticoid receptor. Trends in Endocrinology & Metabolism, 30(11), 807–818. https://doi.org/10.1016/j.tem.2019.07.003
  • Bergstrom, A., Jayatissa, M. N., Mork, A., & Wiborg, O. (2008). Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study. Brain Research, 1196, 41–52. https://doi.org/10.1016/j.brainres.2007.12.025
  • Biggio, F., Mostallino, M. C., Talani, G., Locci, V., Mostallino, R., Calandra, G., Sanna, E., & Biggio, G. (2019). Social enrichment reverses the isolation-induced deficits of neuronal plasticity in the hippocampus of male rats. Neuropharmacology, 151, 45–54. https://doi.org/10.1016/j.neuropharm.2019.03.030
  • Binder, E. B. (2009). The role of FKBP5, a co-chaperone of the glucocorticoid receptor in the pathogenesis and therapy of affective and anxiety disorders. Psychoneuroendocrinology, 34 Suppl 1, S186–S195. https://doi.org/10.1016/j.psyneuen.2009.05.021
  • Binder, E. B., Salyakina, D., Lichtner, P., Wochnik, G. M., Ising, M., Pütz, B., Papiol, S., Seaman, S., Lucae, S., Kohli, M. A., Nickel, T., Künzel, H. E., Fuchs, B., Majer, M., Pfennig, A., Kern, N., Brunner, J., Modell, S., Baghai, T., … Muller-Myhsok, B. (2004). Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nature Genetics, 36(12), 1319–1325. https://doi.org/10.1038/ng1479
  • Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes & Development, 16(1), 6–21. https://doi.org/10.1101/gad.947102
  • Bjorkholm, C., & Monteggia, L. M. (2016). BDNF – A key transducer of antidepressant effects. Neuropharmacology, 102, 72–79. https://doi.org/10.1016/j.neuropharm.2015.10.034
  • Bledsoe, R. K., Montana, V. G., Stanley, T. B., Delves, C. J., Apolito, C. J., McKee, D. D., Consler, T. G., Parks, D. J., Stewart, E. L., Willson, T. M., Lambert, M. H., Moore, J. T., Pearce, K. H., & Xu, H. E. (2002). Crystal structure of the glucocorticoid receptor ligand binding domain reveals a novel mode of receptor dimerization and coactivator recognition. Cell, 110(1), 93–105. https://doi.org/10.1016/S0092-8674(02)00817-6
  • Blugeot, A., Rivat, C., Bouvier, E., Molet, J., Mouchard, A., Zeau, B., Bernard, C., Benoliel, J. J., & Becker, C. (2011). Vulnerability to depression: From brain neuroplasticity to identification of biomarkers. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 31(36), 12889–12899. https://doi.org/10.1523/JNEUROSCI.1309-11.2011
  • Boivin, J. R., & Nedivi, E. (2018). Functional implications of inhibitory synapse placement on signal processing in pyramidal neuron dendrites. Current Opinion in Neurobiology, 51, 16–22. https://doi.org/10.1016/j.conb.2018.01.013
  • Bourke, C. H., Harrell, C. S., & Neigh, G. N. (2012). Stress-induced sex differences: Adaptations mediated by the glucocorticoid receptor. Hormones and Behavior, 62(3), 210–218. https://doi.org/10.1016/j.yhbeh.2012.02.024
  • Bousiges, O., Neidl, R., Majchrzak, M., Muller, M. A., Barbelivien, A., Pereira de Vasconcelos, A., Schneider, A., Loeffler, J. P., Cassel, J. C., & Boutillier, A. L. (2013). Detection of histone acetylation levels in the dorsal hippocampus reveals early tagging on specific residues of H2B and H4 histones in response to learning. PLoS One, 8(3), e57816. https://doi.org/10.1371/journal.pone.0057816
  • Boyle, M. P., Brewer, J. A., Funatsu, M., Wozniak, D. F., Tsien, J. Z., Izumi, Y., & Muglia, L. J. (2005). Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proceedings of the National Academy of Sciences of the United States of America, 102(2), 473–478. https://doi.org/10.1073/pnas.0406458102
  • Boyle, M. P., Kolber, B. J., Vogt, S. K., Wozniak, D. F., & Muglia, L. J. (2006). Forebrain glucocorticoid receptors modulate anxiety-associated locomotor activation and adrenal responsiveness. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 26(7), 1971–1978. https://doi.org/10.1523/JNEUROSCI.2173-05.2006
  • Breen, M. S., Bierer, L. M., Daskalakis, N. P., Bader, H. N., Makotkine, I., Chattopadhyay, M., Xu, C., Buxbaum Grice, A., Tocheva, A. S., Flory, J. D., Buxbaum, J. D., Meaney, M. J., Brennand, K., & Yehuda, R. (2019). Differential transcriptional response following glucocorticoid activation in cultured blood immune cells: A novel approach to PTSD biomarker development. Translational Psychiatry, 9(1), 201. https://doi.org/10.1038/s41398-019-0539-x
  • Brivio, E., Lopez, J. P., & Chen, A. (2020). Sex differences: Transcriptional signatures of stress exposure in male and female brains. Genes, Brain, and Behavior, 19, e12643.
  • Broekema, M. F., Hollman, D. A. A., Koppen, A., van den Ham, H. J., Melchers, D., Pijnenburg, D., Ruijtenbeek, R., van Mil, S. W. C., Houtman, R., & Kalkhoven, E. (2018). Profiling of 3696 nuclear receptor-coregulator interactions: A resource for biological and clinical discovery. Endocrinology, 159(6), 2397–2407. https://doi.org/10.1210/en.2018-00149
  • Burd, C. J., Ward, J. M., Crusselle-Davis, V. J., Kissling, G. E., Phadke, D., Shah, R. R., & Archer, T. K. (2012). Analysis of chromatin dynamics during glucocorticoid receptor activation. Molecular and Cellular Biology, 32(10), 1805–1817. https://doi.org/10.1128/MCB.06206-11
  • Castren, E., & Antila, H. (2017). Neuronal plasticity and neurotrophic factors in drug responses. Molecular Psychiatry, 22(8), 1085–1095. https://doi.org/10.1038/mp.2017.61
  • Castren, E., & Rantamaki, T. (2010). The role of BDNF and its receptors in depression and antidepressant drug action: Reactivation of developmental plasticity. Developmental Neurobiology, 70, 289–297.
  • Chameau, P., Qin, Y., Spijker, S., Smit, A. B., Smit, G., & Joëls, M. (2007). Glucocorticoids specifically enhance L-type calcium current amplitude and affect calcium channel subunit expression in the mouse hippocampus. Journal of Neurophysiology, 97(1), 5–14. https://doi.org/10.1152/jn.00821.2006
  • Charney, D. S. (2004). Psychobiological mechanisms of resilience and vulnerability: Implications for successful adaptation to extreme stress. The American Journal of Psychiatry, 161(2), 195–216. https://doi.org/10.1176/appi.ajp.161.2.195
  • Chater, T. E., & Goda, Y. (2014). The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity. Frontiers in Cellular Neuroscience, 8, 401. https://doi.org/10.3389/fncel.2014.00401
  • Chattarji, S., Tomar, A., Suvrathan, A., Ghosh, S., & Rahman, M. M. (2015). Neighborhood matters: Divergent patterns of stress-induced plasticity across the brain. Nature Neuroscience, 18(10), 1364–1375. https://doi.org/10.1038/nn.4115
  • Chen, C. C., Lu, J., Yang, R., Ding, J. B., & Zuo, Y. (2018). Selective activation of parvalbumin interneurons prevents stress-induced synapse loss and perceptual defects. Molecular Psychiatry, 23(7), 1614–1625. https://doi.org/10.1038/mp.2017.159
  • Chen, D. Y., Bambah-Mukku, D., Pollonini, G., & Alberini, C. M. (2012a). Glucocorticoid receptors recruit the CaMKIIα-BDNF-CREB pathways to mediate memory consolidation. Nature Neuroscience, 15(12), 1707–1714. https://doi.org/10.1038/nn.3266
  • Chen, J. L., Villa, K. L., Cha, J. W., So, P. T., Kubota, Y., & Nedivi, E. (2012b). Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron, 74(2), 361–373. https://doi.org/10.1016/j.neuron.2012.02.030
  • Chen, K., Zhang, L., Tan, M., Lai, C. S., Li, A., Ren, C., & So, K. F. (2017). Treadmill exercise suppressed stress-induced dendritic spine elimination in mouse barrel cortex and improved working memory via BDNF/TrkB pathway. Translational Psychiatry, 7(3), e1069. https://doi.org/10.1038/tp.2017.41
  • Chen, Z.-Y., Jing, D., Bath, K. G., Ieraci, A., Khan, T., Siao, C.-J., Herrera, D. G., Toth, M., Yang, C., McEwen, B. S., Hempstead, B. L., & Lee, F. S. (2006). Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science (New York, N.Y.), 314(5796), 140–143. https://doi.org/10.1126/science.1129663
  • Choi, G. E., Oh, J. Y., Lee, H. J., Chae, C. W., Kim, J. S., Jung, Y. H., & Han, H. J. (2018). Glucocorticoid-mediated ER-mitochondria contacts reduce AMPA receptor and mitochondria trafficking into cell terminus via microtubule destabilization. Cell Death Dis, 9(11), 1137. https://doi.org/10.1038/s41419-018-1172-y
  • Cichon, J., & Gan, W. B. (2015). Branch-specific dendritic Ca(2+) spikes cause persistent synaptic plasticity. Nature, 520(7546), 180–185. https://doi.org/10.1038/nature14251
  • Clayton, D. F., Anreiter, I., Aristizabal, M., Frankland, P. W., Binder, E. B., & Citri, A. (2019). The role of the genome in experience-dependent plasticity: Extending the analogy of the genomic action potential. Proc Natl Acad Sci U S A,
  • Clemens, B., Wagels, L., Bauchmuller, M., Bergs, R., Habel, U., & Kohn, N. (2017). Alerted default mode: Functional connectivity changes in the aftermath of social stress. Scientific Reports, 7, 40180. https://doi.org/10.1038/srep40180
  • Conboy, L., & Sandi, C. (2010). Stress at learning facilitates memory formation by regulating AMPA receptor trafficking through a glucocorticoid action. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 35(3), 674–685. https://doi.org/10.1038/npp.2009.172
  • Conway-Campbell, B. L., McKenna, M. A., Wiles, C. C., Atkinson, H. C., de Kloet, E. R., & Lightman, S. L. (2007). Proteasome-dependent down-regulation of activated nuclear hippocampal glucocorticoid receptors determines dynamic responses to corticosterone. Endocrinology, 148(11), 5470–5477. https://doi.org/10.1210/en.2007-0585
  • Conway-Campbell, B. L., Pooley, J. R., Hager, G. L., & Lightman, S. L. (2012). Molecular dynamics of ultradian glucocorticoid receptor action. Molecular and Cellular Endocrinology, 348(2), 383–393. https://doi.org/10.1016/j.mce.2011.08.014
  • Crosio, C., Heitz, E., Allis, C. D., Borrelli, E., & Sassone-Corsi, P. (2003). Chromatin remodeling and neuronal response: Multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. Journal of Cell Science, 116(Pt 24), 4905–4914. https://doi.org/10.1242/jcs.00804
  • Crow, M., Lim, N., Ballouz, S., Pavlidis, P., & Gillis, J. (2019). Predictability of human differential gene expression. Proceedings of the National Academy of Sciences of the United States of America, 116(13), 6491–6500. https://doi.org/10.1073/pnas.1802973116
  • Dalla, C., Antoniou, K., Kokras, N., Drossopoulou, G., Papathanasiou, G., Bekris, S., Daskas, S., & Papadopoulou-Daifoti, Z. (2008a). Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiology & Behavior, 93(3), 595–605. https://doi.org/10.1016/j.physbeh.2007.10.020
  • Dalla, C., Edgecomb, C., Whetstone, A. S., & Shors, T. J. (2008b). Females do not express learned helplessness like males do. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 33(7), 1559–1569. https://doi.org/10.1038/sj.npp.1301533
  • Dalla, C., Whetstone, A. S., Hodes, G. E., & Shors, T. J. (2009). Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neuroscience Letters, 449(1), 52–56. https://doi.org/10.1016/j.neulet.2008.10.051
  • Datson, N. A., Polman, J. A., de Jonge, R. T., van Boheemen, P. T., van Maanen, E. M., Welten, J., McEwen, B. S., Meiland, H. C., & Meijer, O. C. (2011). Specific regulatory motifs predict glucocorticoid responsiveness of hippocampal gene expression. Endocrinology, 152(10), 3749–3757. https://doi.org/10.1210/en.2011-0287
  • de Assis, G. G., & Gasanov, E. V. (2019). BDNF and Cortisol integrative system – Plasticity vs. degeneration: Implications of the Val66Met polymorphism. Frontiers in Neuroendocrinology, 55, 100784. https://doi.org/10.1016/j.yfrne.2019.100784
  • de Boer, S. F., Buwalda, B., & Koolhaas, J. M. (2017). Untangling the neurobiology of coping styles in rodents: Towards neural mechanisms underlying individual differences in disease susceptibility. Neuroscience and Biobehavioral Reviews, 74(Pt B), 401–422. https://doi.org/10.1016/j.neubiorev.2016.07.008
  • de Kloet, E. R., Otte, C., Kumsta, R., Kok, L., Hillegers, M. H., Hasselmann, H., Kliegel, D., & Joels, M. (2016). Stress and depression: A crucial role of the mineralocorticoid receptor. Journal of Neuroendocrinology, 28(8). https://doi.org/10.1111/jne.12379
  • De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joels, M. (1998). Brain corticosteroid receptor balance in health and disease. Endocrine Reviews, 19(3), 269–301. https://doi.org/10.1210/er.19.3.269
  • Deinhardt, K., & Jeanneteau, F. (2012). More than just an OFF-switch: The essential role of protein dephosphorylation in the modulation of BDNF signaling events. In C. Huang (Ed.), Protein phosphorylation in human health. InTechOpen.
  • Deisseroth, K., Mermelstein, P. G., Xia, H., & Tsien, R. W. (2003). Signaling from synapse to nucleus: The logic behind the mechanisms. Current Opinion in Neurobiology, 13(3), 354–365. https://doi.org/10.1016/S0959-4388(03)00076-X
  • Deng, J.-H., Yan, W., Han, Y., Chen, C., Meng, S.-Q., Sun, C.-Y., Xu, L.-Z., Xue, Y.-X., Gao, X.-J., Chen, N., Zhang, F.-L., Wang, Y.-M., Shi, J., & Lu, L. (2017). Predictable chronic mild stress during adolescence promotes fear memory extinction in adulthood. Scientific Reports, 7(1), 7857. https://doi.org/10.1038/s41598-017-08017-7
  • Der-Avakian, A., Mazei-Robison, M. S., Kesby, J. P., Nestler, E. J., & Markou, A. (2014). Enduring deficits in brain reward function after chronic social defeat in rats: Susceptibility, resilience, and antidepressant response. Biological Psychiatry, 76(7), 542–549. https://doi.org/10.1016/j.biopsych.2014.01.013
  • Derijk, R. H. (2009). Single nucleotide polymorphisms related to HPA axis reactivity. Neuroimmunomodulation, 16(5), 340–352. https://doi.org/10.1159/000216192
  • Deroche, V., Marinelli, M., Maccari, S., Le Moal, M., Simon, H., & Piazza, P. V. (1995). Stress-induced sensitization and glucocorticoids. I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 15(11), 7181–7188. https://doi.org/10.1523/JNEUROSCI.15-11-07181.1995
  • Deroche-Gamonet, V., Sillaber, I., Aouizerate, B., Izawa, R., Jaber, M., Ghozland, S., Kellendonk, C., Le Moal, M., Spanagel, R., Schütz, G., Tronche, F., & Piazza, P. V. (2003). The glucocorticoid receptor as a potential target to reduce cocaine abuse. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 23(11), 4785–4790. https://doi.org/10.1523/JNEUROSCI.23-11-04785.2003
  • Di, S., Maxson, M. M., Franco, A., & Tasker, J. G. (2009). Glucocorticoids regulate glutamate and GABA synapse-specific retrograde transmission via divergent nongenomic signaling pathways. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 29(2), 393–401. https://doi.org/10.1523/JNEUROSCI.4546-08.2009
  • Dias-Ferreira, E., Sousa, J. C., Melo, I., Morgado, P., Mesquita, A. R., Cerqueira, J. J., Costa, R. M., & Sousa, N. (2009). Chronic stress causes frontostriatal reorganization and affects decision-making. Science (New York, N.Y.), 325(5940), 621–625. https://doi.org/10.1126/science.1171203
  • Douma, E. H., & de Kloet, E. R. (2020). Stress-induced plasticity and functioning of ventral tegmental dopamine neurons. Neuroscience and Biobehavioral Reviews, 108, 48–77. https://doi.org/10.1016/j.neubiorev.2019.10.015
  • Doya, K., Ishii, S., Pouget, A., & Rao, R. (2007). Bayesian brain probabilistic approaches to neural coding. The MIT Press.
  • Du, J., Wang, Y., Hunter, R., Wei, Y., Blumenthal, R., Falke, C., Khairova, R., Zhou, R., Yuan, P., Machado-Vieira, R., McEwen, B. S., & Manji, H. K. (2009). Dynamic regulation of mitochondrial function by glucocorticoids. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3543–3548. https://doi.org/10.1073/pnas.0812671106
  • Duman, R. S., Aghajanian, G. K., Sanacora, G., & Krystal, J. H. (2016). Synaptic plasticity and depression: New insights from stress and rapid-acting antidepressants. Nature Medicine, 22(3), 238–249. https://doi.org/10.1038/nm.4050
  • Ebner, K., & Singewald, N. (2017). Individual differences in stress susceptibility and stress inhibitory mechanisms. Current Opinion in Behavioral Sciences, 14, 54–64. https://doi.org/10.1016/j.cobeha.2016.11.016
  • Egan, M. F., Kojima, M., Callicott, J. H., Goldberg, T. E., Kolachana, B. S., Bertolino, A., Zaitsev, E., Gold, B., Goldman, D., Dean, M., Lu, B., & Weinberger, D. R. (2003). The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell, 112(2), 257–269. https://doi.org/10.1016/S0092-8674(03)00035-7
  • Ernst, M., Pine, D. S., & Hardin, M. (2006). Triadic model of the neurobiology of motivated behavior in adolescence. Psychological Medicine, 36(3), 299–312. https://doi.org/10.1017/S0033291705005891
  • Faraji, J., Soltanpour, N., Lotfi, H., Moeeini, R., Moharreri, A.-R., Roudaki, S., Hosseini, S. A., Olson, D. M., Abdollahi, A.-A., Soltanpour, N., Mohajerani, M. H., & Metz, G. A. S. (2017). Lack of social support raises stress vulnerability in rats with a history of ancestral stress. Scientific Reports, 7(1), 5277. https://doi.org/10.1038/s41598-017-05440-8
  • Faresse, N. (2014). Post-translational modifications of the mineralocorticoid receptor: How to dress the receptor according to the circumstances? Journal of Steroid Biochemistry and Molecular Biology, 143, 334–342. https://doi.org/10.1016/j.jsbmb.2014.04.015
  • Farhang, S., Barar, J., Fakhari, A., Mesgariabbasi, M., Khani, S., Omidi, Y., & Farnam, A. (2014). Asymmetrical expression of BDNF and NTRK3 genes in frontoparietal cortex of stress-resilient rats in an animal model of depression. Synapse (New York, N.Y.), 68(9), 387–393. https://doi.org/10.1002/syn.21746
  • Fenzl, T., Touma, C., Romanowski, C. P., Ruschel, J., Holsboer, F., Landgraf, R., Kimura, M., & Yassouridis, A. (2011). Sleep disturbances in highly stress reactive mice: Modeling endophenotypes of major depression. BMC Neuroscience, 12, 29. https://doi.org/10.1186/1471-2202-12-29
  • Franco, L. M., Gadkari, M., Howe, K. N., Sun, J., Kardava, L., Kumar, P., Kumari, S., Hu, Z., Fraser, I. D. C., Moir, S., Tsang, J. S., & Germain, R. N. (2019). Immune regulation by glucocorticoids can be linked to cell type-dependent transcriptional responses. The Journal of Experimental Medicine, 216(2), 384–406. https://doi.org/10.1084/jem.20180595
  • Franklin, T. B., Russig, H., Weiss, I. C., Graff, J., Linder, N., Michalon, A., Vizi, S., & Mansuy, I. M. (2010). Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68(5), 408–415. https://doi.org/10.1016/j.biopsych.2010.05.036
  • Frey, U., & Morris, R. G. (1997). Synaptic tagging and long-term potentiation. Nature, 385(6616), 533–536. https://doi.org/10.1038/385533a0
  • Fries, G. R., Gassen, N. C., Schmidt, U., & Rein, T. (2015). The FKBP51-glucocorticoid receptor balance in stress-related mental disorders. Current Molecular Pharmacology, 9(2), 126–140. https://doi.org/10.2174/1874467208666150519114435
  • Fukumoto, K., Morita, T., Mayanagi, T., Tanokashira, D., Yoshida, T., Sakai, A., & Sobue, K. (2009). Detrimental effects of glucocorticoids on neuronal migration during brain development. Molecular Psychiatry, 14(12), 1119–1131. https://doi.org/10.1038/mp.2009.60
  • Galigniana, N. M., Ballmer, L. T., Toneatto, J., Erlejman, A. G., Lagadari, M., & Galigniana, M. D. (2012). Regulation of the glucocorticoid response to stress-related disorders by the Hsp90-binding immunophilin FKBP51. Journal of Neurochemistry, 122(1), 4–18. https://doi.org/10.1111/j.1471-4159.2012.07775.x
  • Galliher-Beckley, A. J., & Cidlowski, J. A. (2009). Emerging roles of glucocorticoid receptor phosphorylation in modulating glucocorticoid hormone action in health and disease. IUBMB Life, 61(10), 979–986. https://doi.org/10.1002/iub.245
  • Galliher-Beckley, A. J., Williams, J. G., & Cidlowski, J. A. (2011). Ligand-independent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling. Molecular and Cellular Biology, 31(23), 4663–4675. https://doi.org/10.1128/MCB.05866-11
  • Garabedian, M. J., Harris, C. A., & Jeanneteau, F. (2017). Glucocorticoid receptor action in metabolic and neuronal function. F1000Research, 6, 1208. https://doi.org/10.12688/f1000research.11375.1
  • Gertz, J., Savic, D., Varley, K. E., Partridge, E. C., Safi, A., Jain, P., Cooper, G. M., Reddy, T. E., Crawford, G. E., & Myers, R. M. (2013). Distinct properties of cell-type-specific and shared transcription factor binding sites. Molecular Cell, 52(1), 25–36. https://doi.org/10.1016/j.molcel.2013.08.037
  • Goel, N., Workman, J. L., Lee, T. T., Innala, L., & Viau, V. (2014). Sex differences in the HPA axis. Comprehensive Physiology, 4(3), 1121–1155. https://doi.org/10.1002/cphy.c130054
  • Gourley, S. L., Swanson, A. M., Jacobs, A. M., Howell, J. L., Mo, M., Dileone, R. J., Koleske, A. J., & Taylor, J. R. (2012). Action control is mediated by prefrontal BDNF and glucocorticoid receptor binding. Proceedings of the National Academy of Sciences of the United States of America, 109(50), 20714–20719. https://doi.org/10.1073/pnas.1208342109
  • Groc, L., Choquet, D., & Chaouloff, F. (2008). The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nature Neuroscience, 11(8), 868–870. https://doi.org/10.1038/nn.2150
  • Groeneweg, F. L., Karst, H., de Kloet, E. R., & Joels, M. (2011). Rapid non-genomic effects of corticosteroids and their role in the central stress response. The Journal of Endocrinology, 209(2), 153–167. https://doi.org/10.1530/JOE-10-0472
  • Grontved, L., John, S., Baek, S., Liu, Y., Buckley, J. R., Vinson, C., Aguilera, G., & Hager, G. L. (2013). C/EBP maintains chromatin accessibility in liver and facilitates glucocorticoid receptor recruitment to steroid response elements. The EMBO Journal, 32(11), 1568–1583. https://doi.org/10.1038/emboj.2013.106
  • Gutierrez-Mecinas, M., Trollope, A. F., Collins, A., Morfett, H., Hesketh, S. A., Kersante, F., & Reul, J. M. (2011). Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proceedings of the National Academy of Sciences of the United States of America, 108(33), 13806–13811. https://doi.org/10.1073/pnas.1104383108
  • Hagenston, A. M., & Bading, H. (2011). Calcium signaling in synapse-to-nucleus communication. Cold Spring Harbor Perspectives in Medicine, 3(11), a004564. https://doi.org/10.1101/cshperspect.a004564
  • Hapgood, J. P., Avenant, C., & Moliki, J. M. (2016). Glucocorticoid-independent modulation of GR activity: Implications for immunotherapy. Pharmacology & Therapeutics, 165, 93–113. https://doi.org/10.1016/j.pharmthera.2016.06.002
  • Harris, C., Weiss, G. L., Di, S., & Tasker, J. G. (2019). Cell signaling dependence of rapid glucocorticoid-induced endocannabinoid synthesis in hypothalamic neuroendocrine cells. Neurobiology of Stress, 10, 100158. https://doi.org/10.1016/j.ynstr.2019.100158
  • Hartmann, J., Dedic, N., Pöhlmann, M. L., Häusl, A., Karst, H., Engelhardt, C., Westerholz, S., Wagner, K. V., Labermaier, C., Hoeijmakers, L., Kertokarijo, M., Chen, A., Joëls, M., Deussing, J. M., & Schmidt, M. V. (2017). Forebrain glutamatergic, but not GABAergic, neurons mediate anxiogenic effects of the glucocorticoid receptor. Molecular Psychiatry, 22(3), 466–475. https://doi.org/10.1038/mp.2016.87
  • Heim, C., & Binder, E. B. (2012). Current research trends in early life stress and depression: Review of human studies on sensitive periods, gene-environment interactions, and epigenetics. Experimental Neurology, 233(1), 102–111. https://doi.org/10.1016/j.expneurol.2011.10.032
  • Heinzmann, J. M., Kloiber, S., Ebling-Mattos, G., Bielohuby, M., Schmidt, M. V., Palme, R., Holsboer, F., Uhr, M., Ising, M., & Touma, C. (2014). Mice selected for extremes in stress reactivity reveal key endophenotypes of major depression: A translational approach. Psychoneuroendocrinology, 49, 229–243. https://doi.org/10.1016/j.psyneuen.2014.07.008
  • Herman, J. P. (2013). Neural control of chronic stress adaptation. Frontiers in Behavioral Neuroscience, 7, 61. https://doi.org/10.3389/fnbeh.2013.00061
  • Herman, J. P., Figueiredo, H., Mueller, N. K., Ulrich-Lai, Y., Ostrander, M. M., Choi, D. C., & Cullinan, W. E. (2003). Central mechanisms of stress integration: Hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Frontiers in Neuroendocrinology, 24(3), 151–180. https://doi.org/10.1016/j.yfrne.2003.07.001
  • Herman, J. P., McKlveen, J. M., Ghosal, S., Kopp, B., Wulsin, A., Makinson, R., Scheimann, J., & Myers, B. (2016). Regulation of the hypothalamic-pituitary-adrenocortical stress response. Comprehensive Physiology, 6(2), 603–621. https://doi.org/10.1002/cphy.c150015
  • Heshmati, M., & Russo, S. J. (2013). Learning to deal with life’s ups and downs. Nature Neuroscience, 16(6), 658–659. https://doi.org/10.1038/nn.3400
  • Hill, M. J., Suzuki, S., Segars, J. H., & Kino, T. (2016). CRTC2 is a coactivator of GR and couples GR and CREB in the regulation of hepatic gluconeogenesis. Molecular Endocrinology (Baltimore, Md.), 30(1), 104–117. https://doi.org/10.1210/me.2015-1237
  • Hillerer, K. M., Slattery, D. A., & Pletzer, B. (2019). Neurobiological mechanisms underlying sex-related differences in stress-related disorders: Effects of neuroactive steroids on the hippocampus. Frontiers in Neuroendocrinology, 55, 100796. https://doi.org/10.1016/j.yfrne.2019.100796
  • Holsboer, F., & Ising, M. (2010). Stress hormone regulation: Biological role and translation into therapy. Annual Review of Psychology, 61, 81–109. C101–111. https://doi.org/10.1146/annurev.psych.093008.100321
  • Hudson, W. H., Youn, C., & Ortlund, E. A. (2013). The structural basis of direct glucocorticoid-mediated transrepression. Nature Structural & Molecular Biology, 20(1), 53–58. https://doi.org/10.1038/nsmb.2456
  • Huzard, D., Vouros, A., Monari, S., Astori, S., Vasilaki, E., & Sandi, C. (2020). Constitutive differences in glucocorticoid responsiveness are related to divergent spatial information processing abilities. Stress (Amsterdam, Netherlands), 23(1), 37–13. https://doi.org/10.1080/10253890.2019.1625885
  • Ishmael, F. T., Fang, X., Houser, K. R., Pearce, K., Abdelmohsen, K., Zhan, M., Gorospe, M., & Stellato, C. (2011). The human glucocorticoid receptor as an RNA-binding protein: Global analysis of glucocorticoid receptor-associated transcripts and identification of a target RNA motif. Journal of Immunology (Baltimore, Md. : 1950), 186(2), 1189–1198. https://doi.org/10.4049/jimmunol.1001794
  • Ismaili, N., & Garabedian, M. J. (2004). Modulation of glucocorticoid receptor function via phosphorylation. Annals of the New York Academy of Sciences, 1024, 86–101. https://doi.org/10.1196/annals.1321.007
  • Ito, K., Yamamura, S., Essilfie-Quaye, S., Cosio, B., Ito, M., Barnes, P. J., & Adcock, I. M. (2006). Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kappaB suppression. The Journal of Experimental Medicine, 203(1), 7–13. https://doi.org/10.1084/jem.20050466
  • Jawaid, A., Roszkowski, M., & Mansuy, I. M. (2018). Transgenerational epigenetics of traumatic stress. Progress in Molecular Biology and Translational Science, 158, 273–298. https://doi.org/10.1016/bs.pmbts.2018.03.003
  • Jeanneteau, F., Barrère, C., Vos, M., De Vries, C. J. M., Rouillard, C., Levesque, D., Dromard, Y., Moisan, M.-P., Duric, V., Franklin, T. C., Duman, R. S., Lewis, D. A., Ginsberg, S. D., & Arango-Lievano, M. (2018). The stress-induced transcription factor NR4A1 adjusts mitochondrial function and synapse number in prefrontal cortex. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 38(6), 1335–1350. https://doi.org/10.1523/JNEUROSCI.2793-17.2017
  • Jeanneteau, F., Borie, A., Chao, M., & Garabedian, M. (2019). Bridging the gap between BDNF and glucocorticoid effects on brain networks. Neuroendocrinology, 109(3), 277–284. https://doi.org/10.1159/000496392
  • Jeanneteau, F., & Chao, M. V. (2013). Are BDNF and glucocorticoid activities calibrated? Neuroscience, 239, 173–195. https://doi.org/10.1016/j.neuroscience.2012.09.017
  • Jeanneteau, F., & Deinhardt, K. (2011). Fine-tuning MAPK signaling in the brain: The role of MKP-1. Communicative and Integrative Biology, 4, 1–3.
  • Jeanneteau, F., Lambert, W. M., Ismaili, N., Bath, K. G., Lee, F. S., Garabedian, M. J., & Chao, M. V. (2012). BDNF and glucocorticoids regulate corticotrophin-releasing hormone (CRH) homeostasis in the hypothalamus . Proceedings of the National Academy of Sciences of the United States of America, 109(4), 1305–1310. https://doi.org/10.1073/pnas.1114122109
  • Joels, M. (2008). Functional actions of corticosteroids in the hippocampus. European Journal of Pharmacology, 583, 312–321.
  • Joels, M., & Baram, T. Z. (2009). The neuro-symphony of stress. Nature Reviews. Neuroscience, 10(6), 459–466. https://doi.org/10.1038/nrn2632
  • Joels, M., & de Kloet, E. R. (1990). Mineralocorticoid receptor-mediated changes in membrane properties of rat CA1 pyramidal neurons in vitro. Proceedings of the National Academy of Sciences of the United States of America, 87(12), 4495–4498. https://doi.org/10.1073/pnas.87.12.4495
  • Joels, M., & de Kloet, E. R. (1994). Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems. Progress in Neurobiology, 43, 1–36.
  • Joels, M., Pasricha, N., & Karst, H. (2013). The interplay between rapid and slow corticosteroid actions in brain. European Journal of Pharmacology, 719(1-3), 44–52. https://doi.org/10.1016/j.ejphar.2013.07.015
  • Joels, M., Pu, Z., Wiegert, O., Oitzl, M. S., & Krugers, H. J. (2006). Learning under stress: How does it work? Trends in Cognitive Sciences, 10(4), 152–158. https://doi.org/10.1016/j.tics.2006.02.002
  • John, S., Sabo, P. J., Thurman, R. E., Sung, M. H., Biddie, S. C., Johnson, T. A., Hager, G. L., & Stamatoyannopoulos, J. A. (2011). Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nature Genetics, 43(3), 264–268. https://doi.org/10.1038/ng.759
  • Johnson, L. R., Farb, C., Morrison, J. H., McEwen, B. S., & LeDoux, J. E. (2005). Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience, 136(1), 289–299. https://doi.org/10.1016/j.neuroscience.2005.06.050
  • Kalafatakis, K., Russell, G. M., Zarros, A., & Lightman, S. L. (2016). Temporal control of glucocorticoid neurodynamics and its relevance for brain homeostasis, neuropathology and glucocorticoid-based therapeutics. Neuroscience and Biobehavioral Reviews, 61, 12–25. https://doi.org/10.1016/j.neubiorev.2015.11.009
  • Kan, M., Shumyatcher, M., Diwadkar, A., Soliman, G., & Himes, B. E. (2018). Integration of transcriptomic data identifies global and cell-specific asthma-related gene expression signatures. AMIA. Annual Symposium Proceedings. AMIA Symposium, 2018, 1338–1347.
  • Kanatsou, S., Joels, M., & Krugers, H. (2019). Brain mineralocorticoid receptors and resilience to stress. Vitamins and Hormones, 109, 341–359. https://doi.org/10.1016/bs.vh.2018.11.001
  • Karatsoreos, I. N., & McEwen, B. S. (2011). Psychobiological allostasis: Resistance, resilience and vulnerability. Trends in Cognitive Sciences, 15(12), 576–584. https://doi.org/10.1016/j.tics.2011.10.005
  • Karssen, A. M., Meijer, O. C., Berry, A., Sanjuan Pinol, R., & de Kloet, E. R. (2005). Low doses of dexamethasone can produce a hypocorticosteroid state in the brain. Endocrinology, 146(12), 5587–5595. https://doi.org/10.1210/en.2005-0501
  • Karst, H., Berger, S., Erdmann, G., Schutz, G., & Joels, M. (2010). Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proceedings of the National Academy of Sciences of the United States of America, 107(32), 14449–14454. https://doi.org/10.1073/pnas.0914381107
  • Karst, H., de Kloet, E. R., & Joels, M. (1999). Episodic corticosterone treatment accelerates kindling epileptogenesis and triggers long-term changes in hippocampal CA1 cells, in the fully kindled state. The European Journal of Neuroscience, 11(3), 889–898. https://doi.org/10.1046/j.1460-9568.1999.00495.x
  • Kellendonk, C., Gass, P., Kretz, O., Schutz, G., & Tronche, F. (2002). Corticosteroid receptors in the brain: Gene targeting studies. Brain Research Bulletin, 57(1), 73–83. https://doi.org/10.1016/S0361-9230(01)00638-4
  • Kent, M., Bardi, M., Hazelgrove, A., Sewell, K., Kirk, E., Thompson, B., Trexler, K., Terhune-Cotter, B., & Lambert, K. (2017). Profiling coping strategies in male and female rats: Potential neurobehavioral markers of increased resilience to depressive symptoms. Hormones and Behavior, 95, 33–43. https://doi.org/10.1016/j.yhbeh.2017.07.011
  • Khan, S. H., McLaughlin, W. A., & Kumar, R. (2017). Site-specific phosphorylation regulates the structure and function of an intrinsically disordered domain of the glucocorticoid receptor. Scientific Reports, 7(1), 15440. https://doi.org/10.1038/s41598-017-15549-5
  • Kitagawa, H., Sugo, N., Morimatsu, M., Arai, Y., Yanagida, T., & Yamamoto, N. (2017). Activity-dependent dynamics of the transcription factor of cAMP-response element binding protein in cortical neurons revealed by single-molecule imaging. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 37(1), 1–10. https://doi.org/10.1523/JNEUROSCI.0943-16.2016
  • Klein, L. C., Popke, E. J., & Grunberg, N. E. (1998). Sex differences in effects of opioid blockade on stress-induced freezing behavior. Pharmacology, Biochemistry, and Behavior, 61(4), 413–417. https://doi.org/10.1016/S0091-3057(98)00135-X
  • Klemm, S., Shipony, Z., & Greenleaf, W. (2019). Chromatin accessibility and the regulatory epigenome. Nature Reviews. Genetics, 20(4), 207–220. https://doi.org/10.1038/s41576-018-0089-8
  • Klok, M. D., Alt, S. R., Irurzun Lafitte, A. J., Turner, J. D., Lakke, E. A., Huitinga, I., Muller, C. P., Zitman, F. G., de Kloet, E. R., & Derijk, R. H. (2011a). Decreased expression of mineralocorticoid receptor mRNA and its splice variants in postmortem brain regions of patients with major depressive disorder. Journal of Psychiatric Research, 45(7), 871–878. https://doi.org/10.1016/j.jpsychires.2010.12.002
  • Klok, M. D., Giltay, E. J., Van der Does, A. J. W., Geleijnse, J. M., Antypa, N., Penninx, B. W. J. H., de Geus, E. J. C., Willemsen, G., Boomsma, D. I., van Leeuwen, N., Zitman, F. G., de Kloet, E. R., & DeRijk, R. H. (2011b). A common and functional mineralocorticoid receptor haplotype enhances optimism and protects against depression in females. Translational Psychiatry, 1, e62. https://doi.org/10.1038/tp.2011.59
  • Knapman, A., Heinzmann, J. M., Hellweg, R., Holsboer, F., Landgraf, R., & Touma, C. (2010). Increased stress reactivity is associated with cognitive deficits and decreased hippocampal brain-derived neurotrophic factor in a mouse model of affective disorders. Journal of Psychiatric Research, 44(9), 566–575. https://doi.org/10.1016/j.jpsychires.2009.11.014
  • Koning, A., Buurstede, J. C., van Weert, L., & Meijer, O. C. (2019). Glucocorticoid and mineralocorticoid receptors in the brain: A transcriptional perspective. Journal of the Endocrine Society, 3(10), 1917–1930. https://doi.org/10.1210/js.2019-00158
  • Koob, G. F., & Le Moal, M. (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 24(2), 97–129. https://doi.org/10.1016/S0893-133X(00)00195-0
  • Koolhaas, J. M., de Boer, S. F., Buwalda, B., & Meerlo, P. (2017). Social stress models in rodents: Towards enhanced validity. Neurobiology of Stress, 6, 104–112. https://doi.org/10.1016/j.ynstr.2016.09.003
  • Krishnan, V., Han, M.-H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., Laplant, Q., Graham, A., Lutter, M., Lagace, D. C., Ghose, S., Reister, R., Tannous, P., Green, T. A., Neve, R. L., Chakravarty, S., Kumar, A., Eisch, A. J., Self, D. W., … Nestler, E. J. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell, 131(2), 391–404. https://doi.org/10.1016/j.cell.2007.09.018
  • Kudielka, B. M., & Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress: A review. Biological Psychology, 69(1), 113–132. https://doi.org/10.1016/j.biopsycho.2004.11.009
  • Labonté, B., Engmann, O., Purushothaman, I., Menard, C., Wang, J., Tan, C., Scarpa, J. R., Moy, G., Loh, Y.-H E., Cahill, M., Lorsch, Z. S., Hamilton, P. J., Calipari, E. S., Hodes, G. E., Issler, O., Kronman, H., Pfau, M., Obradovic, A. L. J., Dong, Y., … Nestler, E. J. (2017). Sex-specific transcriptional signatures in human depression. Nature Medicine, 23(9), 1102–1111. https://doi.org/10.1038/nm.4386
  • Lambert, W. M., Xu, C.-F., Neubert, T. A., Chao, M. V., Garabedian, M. J., & Jeanneteau, F. (2013). Brain-derived neurotrophic factor signaling rewrites the glucocorticoid transcriptome via glucocorticoid receptor phosphorylation . Molecular and Cellular Biology, 33(18), 3700–3714. https://doi.org/10.1128/MCB.00150-13
  • Lapp, H. E., Bartlett, A. A., & Hunter, R. G. (2019). Stress and glucocorticoid receptor regulation of mitochondrial gene expression. Journal of Molecular Endocrinology, 62(2), R121–R128. https://doi.org/10.1530/JME-18-0152
  • Laryea, G., Schutz, G., & Muglia, L. J. (2013). Disrupting hypothalamic glucocorticoid receptors causes HPA axis hyperactivity and excess adiposity. Molecular Endocrinology (Baltimore, Md.), 27(10), 1655–1665. https://doi.org/10.1210/me.2013-1187
  • Lazarus, R., & Folkman, S. (1984). Stress, Appraisal, and Coping. Springer.
  • Lee, M.-S., Kim, Y.-H., Park, W.-S., Park, O.-K., Kwon, S.-H., Hong, K. S., Rhim, H., Shim, I., Morita, K., Wong, D. L., Patel, P. D., Lyons, D. M., Schatzberg, A. F., & Her, S. (2016). Temporal variability of glucocorticoid receptor activity is functionally important for the therapeutic action of fluoxetine in the hippocampus. Molecular Psychiatry, 21(2), 252–260. https://doi.org/10.1038/mp.2014.137
  • Li, Y., Suino, K., Daugherty, J., & Xu, H. E. (2005). Structural and biochemical mechanisms for the specificity of hormone binding and coactivator assembly by mineralocorticoid receptor. Molecular Cell, 19(3), 367–380. https://doi.org/10.1016/j.molcel.2005.06.026
  • Liberman, A. C., Antunica-Noguerol, M., & Arzt, E. (2014). Modulation of the glucocorticoid receptor activity by post-translational modifications. Nuclear Receptor Research, 1, 1–15. https://doi.org/10.11131/2014/101086
  • Liston, C., Cichon, J. M., Jeanneteau, F., Jia, Z., Chao, M. V., & Gan, W.-B. (2013). Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance. Nature Neuroscience, 16(6), 698–705. https://doi.org/10.1038/nn.3387
  • Liston, C., & Gan, W. B. (2011). Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proceedings of the National Academy of Sciences of the United States of America, 108(38), 16074–16079. https://doi.org/10.1073/pnas.1110444108
  • Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S., Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science (New York, N.Y.), 277(5332), 1659–1662. https://doi.org/10.1126/science.277.5332.1659
  • Liu, W., Wang, J., Sauter, N. K., & Pearce, D. (1995). Steroid receptor heterodimerization demonstrated in vitro and in vivo. Proceedings of the National Academy of Sciences of the United States of America, 92(26), 12480–12484. https://doi.org/10.1073/pnas.92.26.12480
  • Liu, W., Xue, X., Xia, J., Liu, J., & Qi, Z. (2018). Swimming exercise reverses CUMS-induced changes in depression-like behaviors and hippocampal plasticity-related proteins. Journal of Affective Disorders, 227, 126–135. https://doi.org/10.1016/j.jad.2017.10.019
  • Lu, Y., Ji, Y., Ganesan, S., Schloesser, R., Martinowich, K., Sun, M., Mei, F., Chao, M. V., & Lu, B. (2011). TrkB as a potential synaptic and behavioral tag. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 31(33), 11762–11771. https://doi.org/10.1523/JNEUROSCI.2707-11.2011
  • Mahfouz, A., Lelieveldt, B. P., Grefhorst, A., van Weert, L. T., Mol, I. M., Sips, H. C., van den Heuvel, J. K., Datson, N. A., Visser, J. A., Reinders, M. J., & Meijer, O. C. (2016). Genome-wide coexpression of steroid receptors in the mouse brain: Identifying signaling pathways and functionally coordinated regions. Proceedings of the National Academy of Sciences of the United States of America, 113(10), 2738–2743. https://doi.org/10.1073/pnas.1520376113
  • Mallei, A., Ieraci, A., & Popoli, M. (2019). Chronic social defeat stress differentially regulates the expression of BDNF transcripts and epigenetic modifying enzymes in susceptible and resilient mice. The World Journal of Biological Psychiatry : The Official Journal of the World Federation of Societies of Biological Psychiatry, 20(7), 555–566. https://doi.org/10.1080/15622975.2018.1500029
  • Mayanagi, T., Morita, T., Hayashi, K., Fukumoto, K., & Sobue, K. (2008). Glucocorticoid receptor-mediated expression of caldesmon regulates cell migration via the reorganization of the actin cytoskeleton. The Journal of Biological Chemistry, 283(45), 31183–31196. https://doi.org/10.1074/jbc.M801606200
  • McEwen, B. S. (1998). Stress, adaptation, and disease. Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 33–44. https://doi.org/10.1111/j.1749-6632.1998.tb09546.x
  • McEwen, B. S. (2006). Protective and damaging effects of stress mediators: Central role of the brain. Dialogues in Clinical Neuroscience, 8(4), 367–381.
  • McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiological Reviews, 87(3), 873–904. https://doi.org/10.1152/physrev.00041.2006
  • McEwen, B. S. (2015). Preserving neuroplasticity: Role of glucocorticoids and neurotrophins via phosphorylation. Proceedings of the National Academy of Sciences of the United States of America, 112(51), 15544–15545. https://doi.org/10.1073/pnas.1521416112
  • McEwen, B. S., Bowles, N. P., Gray, J. D., Hill, M. N., Hunter, R. G., Karatsoreos, I. N., & Nasca, C. (2015). Mechanisms of stress in the brain. Nature Neuroscience, 18(10), 1353–1363. https://doi.org/10.1038/nn.4086
  • McEwen, B. S., Nasca, C., & Gray, J. D. (2016). Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 41(1), 3–23. https://doi.org/10.1038/npp.2015.171
  • McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonte, B., Szyf, M., Turecki, G., & Meaney, M. J. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience, 12(3), 342–348. https://doi.org/10.1038/nn.2270
  • McIlwrick, S., Pohl, T., Chen, A., & Touma, C. (2017). Late-onset cognitive impairments after early-life stress are shaped by inherited differences in stress reactivity. Frontiers in Cellular Neuroscience, 11, 9. https://doi.org/10.3389/fncel.2017.00009
  • McIlwrick, S., Rechenberg, A., Matthes, M., Burgstaller, J., Schwarzbauer, T., Chen, A., & Touma, C. (2016). Genetic predisposition for high stress reactivity amplifies effects of early-life adversity. Psychoneuroendocrinology, 70, 85–97. https://doi.org/10.1016/j.psyneuen.2016.04.023
  • Meijer, O. C., Buurstede, J. C., & Schaaf, M. J. M. (2019). Corticosteroid receptors in the brain: Transcriptional mechanisms for specificity and context-dependent effects. Cellular and molecular neurobiology, 39(4), 539–549. https://doi.org/10.1007/s10571-018-0625-2
  • Meijer, O. C., Kalkhoven, E., van der Laan, S., Steenbergen, P. J., Houtman, S. H., Dijkmans, T. F., Pearce, D., & de Kloet, E. R. (2005). Steroid receptor coactivator-1 splice variants differentially affect corticosteroid receptor signaling. Endocrinology, 146(3), 1438–1448. https://doi.org/10.1210/en.2004-0411
  • Meijsing, S. H., Pufall, M. A., So, A. Y., Bates, D. L., Chen, L., & Yamamoto, K. R. (2009). DNA binding site sequence directs glucocorticoid receptor structure and activity. Science (New York, N.Y.), 324(5925), 407–410. https://doi.org/10.1126/science.1164265
  • Menke, A., Arloth, J., Pütz, B., Weber, P., Klengel, T., Mehta, D., Gonik, M., Rex-Haffner, M., Rubel, J., Uhr, M., Lucae, S., Deussing, J. M., Müller-Myhsok, B., Holsboer, F., & Binder, E. B. (2012). Dexamethasone stimulated gene expression in peripheral blood is a sensitive marker for glucocorticoid receptor resistance in depressed patients. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 37(6), 1455–1464. https://doi.org/10.1038/npp.2011.331
  • Mifsud, K. R., & Reul, J. (2018). Mineralocorticoid and glucocorticoid receptor-mediated control of genomic responses to stress in the brain. Stress (Amsterdam, Netherlands), 21(5), 389–402. https://doi.org/10.1080/10253890.2018.1456526
  • Mifsud, K. R., & Reul, J. M. (2016). Acute stress enhances heterodimerization and binding of corticosteroid receptors at glucocorticoid target genes in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 113(40), 11336–11341. https://doi.org/10.1073/pnas.1605246113
  • Mitic, M., Simic, I., Djordjevic, J., Radojcic, M. B., & Adzic, M. (2013). Gender-specific effects of fluoxetine on hippocampal glucocorticoid receptor phosphorylation and behavior in chronically stressed rats. Neuropharmacology, 70, 100–111. https://doi.org/10.1016/j.neuropharm.2012.12.012
  • Mitre, M., Mariga, A., & Chao, M. V. (2017). Neurotrophin signalling: Novel insights into mechanisms and pathophysiology. Clinical Science (London, England : 1979), 131(1), 13–23. https://doi.org/10.1042/CS20160044
  • Moda-Sava, R. N., Murdock, M. H., Parekh, P. K., Fetcho, R. N., Huang, B. S., Huynh, T. N., Witztum, J., Shaver, D. C., Rosenthal, D. L., & Alway, E. J. (2019). Sustained rescue of prefrontal circuit dysfunction by antidepressant-induced spine formation. Science, 364(6436), eaat8078.
  • Monczor, F., Chatzopoulou, A., Zappia, C. D., Houtman, R., Meijer, O. C., & Fitzsimons, C. P. (2019). A model of glucocorticoid receptor interaction with coregulators predicts transcriptional regulation of target genes. Frontiers in Pharmacology, 10, 214.
  • Morsink, M. C., Steenbergen, P. J., Vos, J. B., Karst, H., Joels, M., De Kloet, E. R., & Datson, N. A. (2006). Acute activation of hippocampal glucocorticoid receptors results in different waves of gene expression throughout time. Journal of Neuroendocrinology, 18(4), 239–252. https://doi.org/10.1111/j.1365-2826.2006.01413.x
  • Mukherjee, D., Ignatowska-Jankowska, B. M., Itskovits, E., Gonzales, B. J., Turm, H., Izakson, L., Haritan, D., Bleistein, N., Cohen, C., Amit, I., Shay, T., Grueter, B., Zaslaver, A., & Citri, A. (2018). Salient experiences are represented by unique transcriptional signatures in the mouse brain. eLife, 7, e31220. https://doi.org/10.7554/eLife.31220
  • Muto, A., Taylor, M. R., Suzawa, M., Korenbrot, J. I., & Baier, H. (2013). Glucocorticoid receptor activity regulates light adaptation in the zebrafish retina. Frontiers in Neural Circuits, 7, 145. https://doi.org/10.3389/fncir.2013.00145
  • Myers, B., McKlveen, J. M., & Herman, J. P. (2014). Glucocorticoid actions on synapses, circuits, and behavior: Implications for the energetics of stress. Frontiers in Neuroendocrinology, 35(2), 180–196. https://doi.org/10.1016/j.yfrne.2013.12.003
  • Nasca, C., Zelli, D., Bigio, B., Piccinin, S., Scaccianoce, S., Nistico, R., & McEwen, B. S. (2015). Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Proceedings of the National Academy of Sciences of the United States of America, 112(48), 14960–14965. https://doi.org/10.1073/pnas.1516016112
  • Nasrallah, P., Haidar, E. A., Stephan, J. S., El Hayek, L., Karnib, N., Khalifeh, M., Barmo, N., Jabre, V., Houbeika, R., Ghanem, A., Nasser, J., Zeeni, N., Bassil, M., & Sleiman, S. F. (2019). Branched-chain amino acids mediate resilience to chronic social defeat stress by activating BDNF/TRKB signaling. Neurobiology of Stress, 11, 100170. https://doi.org/10.1016/j.ynstr.2019.100170
  • Nestler, E. J. (2016). Transgenerational epigenetic contributions to stress responses: Fact or fiction? PLoS Biology, 14(3), e1002426. https://doi.org/10.1371/journal.pbio.1002426
  • Ng, L. H. L., Huang, Y., Han, L., Chang, R. C., Chan, Y. S., & Lai, C. S. W. (2018). Ketamine and selective activation of parvalbumin interneurons inhibit stress-induced dendritic spine elimination. Translational Psychiatry, 8(1), 272. https://doi.org/10.1038/s41398-018-0321-5
  • Notaras, M., Du, X., Gogos, J., van den Buuse, M., & Hill, R. A. (2017). The BDNF Val66Met polymorphism regulates glucocorticoid-induced corticohippocampal remodeling and behavioral despair. Translational Psychiatry, 7(9), e1233. https://doi.org/10.1038/tp.2017.205
  • Notaras, M., Hill, R., Gogos, J. A., & van den Buuse, M. (2016). BDNF Val66Met genotype determines hippocampus-dependent behavior via sensitivity to glucocorticoid signaling. Molecular Psychiatry, 21(6), 730–732. https://doi.org/10.1038/mp.2015.152
  • Nott, A., Watson, P. M., Robinson, J. D., Crepaldi, L., & Riccio, A. (2008). S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature, 455(7211), 411–415. https://doi.org/10.1038/nature07238
  • Numakawa, T., Kumamaru, E., Adachi, N., Yagasaki, Y., Izumi, A., & Kunugi, H. (2009). Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-gamma signaling for glutamate release via a glutamate transporter. Proceedings of the National Academy of Sciences of the United States of America, 106(2), 647–652. https://doi.org/10.1073/pnas.0800888106
  • Paakinaho, V., Johnson, T. A., Presman, D. M., & Hager, G. L. (2019). Glucocorticoid receptor quaternary structure drives chromatin occupancy and transcriptional outcome. Genome Research, 29(8), 1223–1234. https://doi.org/10.1101/gr.244814.118
  • Parnaudeau, S., Dongelmans, M. L., Turiault, M., Ambroggi, F., Delbes, A. S., Cansell, C., Luquet, S., Piazza, P. V., Tronche, F., & Barik, J. (2014). Glucocorticoid receptor gene inactivation in dopamine-innervated areas selectively decreases behavioral responses to amphetamine. Frontiers in Behavioral Neuroscience, 8, 35. https://doi.org/10.3389/fnbeh.2014.00035
  • Paugh, S. W., Bonten, E. J., Savic, D., Ramsey, L. B., Thierfelder, W. E., Gurung, P., Malireddi, R. K. S., Actis, M., Mayasundari, A., Min, J., Coss, D. R., Laudermilk, L. T., Panetta, J. C., McCorkle, J. R., Fan, Y., Crews, K. R., Stocco, G., Wilkinson, M. R., Ferreira, A. M., … Evans, W. E. (2015). NALP3 inflammasome upregulation and CASP1 cleavage of the glucocorticoid receptor cause glucocorticoid resistance in leukemia cells. Nature Genetics, 47(6), 607–614. https://doi.org/10.1038/ng.3283
  • Pearce, D. (1994). A mechanistic basis for distinct mineralocorticoid and glucocorticoid receptor transcriptional specificities. Steroids, 59(2), 153–159. https://doi.org/10.1016/0039-128X(94)90094-9
  • Peters, A., McEwen, B. S., & Friston, K. (2017). Uncertainty and stress: Why it causes diseases and how it is mastered by the brain. Progress in Neurobiology, 156, 164–188. https://doi.org/10.1016/j.pneurobio.2017.05.004
  • Petta, I., Dejager, L., Ballegeer, M., Lievens, S., Tavernier, J., De Bosscher, K., & Libert, C. (2016). The interactome of the glucocorticoid receptor and its influence on the actions of glucocorticoids in combatting inflammatory and infectious diseases. Microbiology and Molecular Biology Reviews : MMBR, 80(2), 495–522. https://doi.org/10.1128/MMBR.00064-15
  • Piazza, P. V., & Le Moal, M. L. (1996). Pathophysiological basis of vulnerability to drug abuse: Role of an interaction between stress, glucocorticoids, and dopaminergic neurons. Annual Review of Pharmacology and Toxicology, 36, 359–378. https://doi.org/10.1146/annurev.pa.36.040196.002043
  • Picard, M., Juster, R. P., & McEwen, B. S. (2014). Mitochondrial allostatic load puts the ‘gluc’ back in glucocorticoids. Nature Reviews. Endocrinology, 10(5), 303–310. https://doi.org/10.1038/nrendo.2014.22
  • Pittenger, C., & Duman, R. S. (2008). Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology : Official Publication of the American College of Neuropsychopharmacology, 33(1), 88–109. https://doi.org/10.1038/sj.npp.1301574
  • Polman, J. A., de Kloet, E. R., & Datson, N. A. (2013). Two populations of glucocorticoid receptor-binding sites in the male rat hippocampal genome. Endocrinology, 154(5), 1832–1844. https://doi.org/10.1210/en.2012-2187
  • Pooley, J. R., Flynn, B. P., Grøntved, L., Baek, S., Guertin, M. J., Kershaw, Y. M., Birnie, M. T., Pellatt, A., Rivers, C. A., Schiltz, R. L., Hager, G. L., Lightman, S. L., & Conway-Campbell, B. L. (2017). Genome-wide identification of basic helix-loop-helix and NF-1 motifs underlying GR binding sites in male rat hippocampus. Endocrinology, 158(5), 1486–1501. https://doi.org/10.1210/en.2016-1929
  • Pooley, J. R., Rivers, C. A., Kilcooley, M. T., Paul, S. N., Cavga, A. D., Kershaw, Y. M., Muratcioglu, S., Gursoy, A., Keskin, O., & Lightman, S. L. (2020). Beyond the heterodimer model for mineralocorticoid and glucocorticoid receptor interactions in nuclei and at DNA. PLoS One, 15(1), e0227520. https://doi.org/10.1371/journal.pone.0227520
  • Poolman, T. M., Farrow, S. N., Matthews, L., Loudon, A. S., & Ray, D. W. (2013). Pin1 promotes GR transactivation by enhancing recruitment to target genes. Nucleic Acids Research, 41(18), 8515–8525. https://doi.org/10.1093/nar/gkt624
  • Prager, E. M., Brielmaier, J., Bergstrom, H. C., McGuire, J., & Johnson, L. R. (2010). Localization of mineralocorticoid receptors at mammalian synapses. PLoS One, 5(12), e14344. https://doi.org/10.1371/journal.pone.0014344
  • Provencal, N., Arloth, J., Cattaneo, A., Anacker, C., Cattane, N., Wiechmann, T., Roh, S., Kodel, M., Klengel, T., & Czamara, D. (2019). Glucocorticoid exposure during hippocampal neurogenesis primes future stress response by inducing changes in DNA methylation. Proceedings of the National Academy of Sciences of the United States of America. https://doi.org/10.1073/pnas.1820842116
  • Quinn, D. P., Kolar, A., Harris, S. A., Wigerius, M., Fawcett, J. P., & Krueger, S. R. (2019). The stability of glutamatergic synapses is independent of activity level, but predicted by synapse size. Frontiers in Cellular Neuroscience, 13, 291. https://doi.org/10.3389/fncel.2019.00291
  • Ramamoorthy, S., & Cidlowski, J. A. (2013). Exploring the molecular mechanisms of glucocorticoid receptor action from sensitivity to resistance. Endocrine Development, 24, 41–56. https://doi.org/10.1159/000342502
  • Rao-Ruiz, P., Couey, J. J., Marcelo, I. M., Bouwkamp, C. G., Slump, D. E., Matos, M. R., van der Loo, R. J., Martins, G. J., van den Hout, M., van IJcken, W. F., Costa, R. M., van den Oever, M. C., & Kushner, S. A. (2019). Engram-specific transcriptome profiling of contextual memory consolidation. Nature Communications, 10(1), 2232. https://doi.org/10.1038/s41467-019-09960-x
  • Rapicavoli, N. A., Qu, K., Zhang, J., Mikhail, M., Laberge, R. M., & Chang, H. Y. (2013). A mammalian pseudogene lncRNA at the interface of inflammation and anti-inflammatory therapeutics. eLife, 2, e00762. https://doi.org/10.7554/eLife.00762
  • Ratajczak, T., Cluning, C., & Ward, B. K. (2015). Steroid receptor-associated immunophilins: A gateway to steroid signalling. The Clinical Biochemist. Reviews, 36(2), 31–52.
  • Ratman, D., Vanden Berghe, W., Dejager, L., Libert, C., Tavernier, J., Beck, I. M., & De Bosscher, K. (2013). How glucocorticoid receptors modulate the activity of other transcription factors: A scope beyond tethering. Molecular and Cellular Endocrinology, 380(1-2), 41–54. https://doi.org/10.1016/j.mce.2012.12.014
  • Rattiner, L. M., Davis, M., French, C. T., & Ressler, K. J. (2004a). Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 24(20), 4796–4806. https://doi.org/10.1523/JNEUROSCI.5654-03.2004
  • Rattiner, L. M., Davis, M., & Ressler, K. J. (2004b). Differential regulation of brain-derived neurotrophic factor transcripts during the consolidation of fear learning. Learning & Memory (Cold Spring Harbor, N.Y.), 11(6), 727–731. https://doi.org/10.1101/lm.83304
  • Reul, J. M., & de Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology, 117(6), 2505–2511. https://doi.org/10.1210/endo-117-6-2505
  • Revest, J. M., Le Roux, A., Roullot-Lacarriere, V., Kaouane, N., Vallee, M., Kasanetz, F., Rouge-Pont, F., Tronche, F., Desmedt, A., & Piazza, P. V. (2014). BDNF-TrkB signaling through Erk1/2 phosphorylation mediates the enhancement of fear memory induced by glucocorticoids. Molecular Psychiatry, 19(9), 1001–1009. https://doi.org/10.1038/mp.2013.134
  • Rincon-Cortes, M., Herman, J. P., Lupien, S., Maguire, J., & Shansky, R. M. (2019). Stress: Influence of sex, reproductive status and gender. Neurobiology of Stress, 10, 100155. https://doi.org/10.1016/j.ynstr.2019.100155
  • Rivers, C. A., Rogers, M. F., Stubbs, F. E., Conway-Campbell, B. L., Lightman, S. L., & Pooley, J. R. (2019). Glucocorticoid receptor-tethered mineralocorticoid receptors increase glucocorticoid-induced transcriptional responses. Endocrinology, 160(5), 1044–1056. https://doi.org/10.1210/en.2018-00819
  • Rollins, D. A., Kharlyngdoh, J. B., Coppo, M., Tharmalingam, B., Mimouna, S., Guo, Z., Sacta, M. A., Pufall, M. A., Fisher, R. P., Hu, X., Chinenov, Y., & Rogatsky, I. (2017). Glucocorticoid-induced phosphorylation by CDK9 modulates the coactivator functions of transcriptional cofactor GRIP1 in macrophages. Nature Communications, 8(1), 1739. https://doi.org/10.1038/s41467-017-01569-2
  • Rothman, S. M., & Mattson, M. P. (2013). Activity-dependent, stress-responsive BDNF signaling and the quest for optimal brain health and resilience throughout the lifespan. Neuroscience, 239, 228–240. https://doi.org/10.1016/j.neuroscience.2012.10.014
  • Russell, G. M., Kalafatakis, K., & Lightman, S. L. (2015). The importance of biological oscillators for hypothalamic-pituitary-adrenal activity and tissue glucocorticoid response: Coordinating stress and neurobehavioural adaptation. Journal of Neuroendocrinology, 27(6), 378–388. https://doi.org/10.1111/jne.12247
  • Russo, M. F., Ah Loy, S. R., Battle, A. R., & Johnson, L. R. (2016). Membrane associated synaptic mineralocorticoid and glucocorticoid receptors are rapid regulators of dendritic spines. Frontiers in Cellular Neuroscience, 10, 161. https://doi.org/10.3389/fncel.2016.00161
  • Saaltink, D. J., & Vreugdenhil, E. (2014). Stress, glucocorticoid receptors, and adult neurogenesis: A balance between excitation and inhibition? Cellular and Molecular Life Sciences : CMLS, 71(13), 2499–2515. https://doi.org/10.1007/s00018-014-1568-5
  • Sacta, M. A., Chinenov, Y., & Rogatsky, I. (2016). Glucocorticoid signaling: An update from a genomic perspective. Annual Review of Physiology, 78, 155–180. https://doi.org/10.1146/annurev-physiol-021115-105323
  • Sarabdjitsingh, R. A., Conway-Campbell, B. L., Leggett, J. D., Waite, E. J., Meijer, O. C., de Kloet, E. R., & Lightman, S. L. (2010a). Stress responsiveness varies over the ultradian glucocorticoid cycle in a brain-region-specific manner. Endocrinology, 151(11), 5369–5379. https://doi.org/10.1210/en.2010-0832
  • Sarabdjitsingh, R. A., Isenia, S., Polman, A., Mijalkovic, J., Lachize, S., Datson, N., de Kloet, E. R., & Meijer, O. C. (2010b). Disrupted corticosterone pulsatile patterns attenuate responsiveness to glucocorticoid signaling in rat brain. Endocrinology, 151(3), 1177–1186. https://doi.org/10.1210/en.2009-1119
  • Sarabdjitsingh, R. A., Jezequel, J., Pasricha, N., Mikasova, L., Kerkhofs, A., Karst, H., Groc, L., & Joels, M. (2014). Ultradian corticosterone pulses balance glutamatergic transmission and synaptic plasticity. Proceedings of the National Academy of Sciences of the United States of America, 111(39), 14265–14270. https://doi.org/10.1073/pnas.1411216111
  • Sarabdjitsingh, R. A., Spiga, F., Oitzl, M. S., Kershaw, Y., Meijer, O. C., Lightman, S. L., & de Kloet, E. R. (2010c). Recovery from disrupted ultradian glucocorticoid rhythmicity reveals a dissociation between hormonal and behavioural stress responsiveness. Journal of Neuroendocrinology, 22(8), 862–871. https://doi.org/10.1111/j.1365-2826.2010.02004.x
  • Scheimann, J. R., Mahbod, P., Morano, R., Frantz, L., Packard, B., Campbell, K., & Herman, J. P. (2018). Deletion of glucocorticoid receptors in forebrain GABAergic neurons alters acute stress responding and passive avoidance behavior in female mice. Frontiers in Behavioral Neuroscience, 12, 325. https://doi.org/10.3389/fnbeh.2018.00325
  • Scheimann, J. R., Moloney, R. D., Mahbod, P., Morano, R. L., Fitzgerald, M., Hoskins, O., Packard, B. A., Cotella, E. M., Hu, Y. C., & Herman, J. P. (2019). Conditional deletion of glucocorticoid receptors in rat brain results in sex-specific deficits in fear and coping behaviors. eLife, 8, e44672. https://doi.org/10.7554/eLife.44672
  • Schiller, B. J., Chodankar, R., Watson, L. C., Stallcup, M. R., & Yamamoto, K. R. (2014). Glucocorticoid receptor binds half sites as a monomer and regulates specific target genes. Genome Biology, 15(7), 418. https://doi.org/10.1186/s13059-014-0418-y
  • Schouten, M., Bielefeld, P., Garcia-Corzo, L., Passchier, E. M. J., Gradari, S., Jungenitz, T., Pons-Espinal, M., Gebara, E., Martín-Suárez, S., Lucassen, P. J., De Vries, H. E., Trejo, J. L., Schwarzacher, S. W., De Pietri Tonelli, D., Toni, N., Mira, H., Encinas, J. M., & Fitzsimons, C. P. (2020). Circadian glucocorticoid oscillations preserve a population of adult hippocampal neural stem cells in the aging brain. Molecular Psychiatry, 25(7), 1382–1405. https://doi.org/10.1038/s41380-019-0440-2
  • Schwabe, L., Joels, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012). Stress effects on memory: An update and integration. Neurosci Biobehav Rev, 36(7), 1740–1749. https://doi.org/10.1016/j.neubiorev.2011.07.002
  • Selye, H. (1956). The stress of life. McGrawHill.
  • Shalev, I., Lerer, E., Israel, S., Uzefovsky, F., Gritsenko, I., Mankuta, D., Ebstein, R. P., & Kaitz, M. (2009). BDNF Val66Met polymorphism is associated with HPA axis reactivity to psychological stress characterized by genotype and gender interactions. Psychoneuroendocrinology, 34(3), 382–388. https://doi.org/10.1016/j.psyneuen.2008.09.017
  • Simard, M., Couldwell, W. T., Zhang, W., Song, H., Liu, S., Cotrina, M. L., Goldman, S., & Nedergaard, M. (1999). Glucocorticoids-potent modulators of astrocytic calcium signaling. Glia, 28(1), 1–12. https://doi.org/10.1002/(SICI)1098-1136(199910)28:1<1::AID-GLIA1>3.0.CO;2-4
  • Snyder-Mackler, N., Sanz, J., Kohn, J. N., Voyles, T., Pique-Regi, R., Wilson, M. E., Barreiro, L. B., & Tung, J. (2019). Social status alters chromatin accessibility and the gene regulatory response to glucocorticoid stimulation in rhesus macaques. Proceedings of the National Academy of Sciences of the United States of America, 116(4), 1219–1228. https://doi.org/10.1073/pnas.1811758115
  • Soares, J. M., Sampaio, A., Ferreira, L. M., Santos, N. C., Marques, P., Marques, F., Palha, J. A., Cerqueira, J. J., & Sousa, N. (2013). Stress impact on resting state brain networks. PLoS One, 8(6), e66500. https://doi.org/10.1371/journal.pone.0066500
  • Soliman, F., Glatt, C. E., Bath, K. G., Levita, L., Jones, R. M., Pattwell, S. S., Jing, D., Tottenham, N., Amso, D., Somerville, L. H., Voss, H. U., Glover, G., Ballon, D. J., Liston, C., Teslovich, T., Van Kempen, T., Lee, F. S., & Casey, B. J. (2010). A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science (New York, N.Y.), 327(5967), 863–866. https://doi.org/10.1126/science.1181886
  • Solomon, M. B., & Herman, J. P. (2009). Sex differences in psychopathology: Of gonads, adrenals and mental illness. Physiology & Behavior, 97(2), 250–258. https://doi.org/10.1016/j.physbeh.2009.02.033
  • Stepanichev, M., Manolova, A., Peregud, D., Onufriev, M., Freiman, S., Aniol, V., Moiseeva, Y., Novikova, M., Lazareva, N., & Gulyaeva, N. (2018). Specific activity features in the forced swim test: Brain neurotrophins and development of stress-induced depressive-like behavior in rats. Neuroscience, 375, 49–61. https://doi.org/10.1016/j.neuroscience.2018.02.007
  • Stournaras, C., Gravanis, A., Margioris, A. N., & Lang, F. (2014). The actin cytoskeleton in rapid steroid hormone actions. Cytoskeleton (Hoboken, N.J.), 71(5), 285–293. https://doi.org/10.1002/cm.21172
  • Suderman, M., McGowan, P. O., Sasaki, A., Huang, T. C., Hallett, M. T., Meaney, M. J., Turecki, G., & Szyf, M. (2012). Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 109 Suppl 2, 17266–17272. https://doi.org/10.1073/pnas.1121260109
  • Swanson, A. M., Shapiro, L. P., Whyte, A. J., & Gourley, S. L. (2013). Glucocorticoid receptor regulation of action selection and prefrontal cortical dendritic spines. Communicative & Integrative Biology, 6(6), e26068. https://doi.org/10.4161/cib.26068
  • Taliaz, D., Loya, A., Gersner, R., Haramati, S., Chen, A., & Zangen, A. (2011). Resilience to chronic stress is mediated by hippocampal brain-derived neurotrophic factor. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 31(12), 4475–4483. https://doi.org/10.1523/JNEUROSCI.5725-10.2011
  • Tasker, J. G. (2006). Rapid glucocorticoid actions in the hypothalamus as a mechanism of homeostatic integration. Obesity (Silver Spring, Md.), 14 Suppl 5, 259S–265S. https://doi.org/10.1038/oby.2006.320
  • Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A., & Updegraff, J. A. (2000). Biobehavioral responses to stress in females: Tend-and-befriend, not fight-or-flight. Psychological Review, 107(3), 411–429. https://doi.org/10.1037/0033-295x.107.3.411
  • Tornese, P., Sala, N., Bonini, D., Bonifacino, T., La Via, L., Milanese, M., Treccani, G., Seguini, M., Ieraci, A., Mingardi, J., Nyengaard, J. R., Calza, S., Bonanno, G., Wegener, G., Barbon, A., Popoli, M., & Musazzi, L. (2019). Chronic mild stress induces anhedonic behavior and changes in glutamate release, BDNF trafficking and dendrite morphology only in stress vulnerable rats. The rapid restorative action of ketamine. Neurobiology of Stress, 10, 100160. https://doi.org/10.1016/j.ynstr.2019.100160
  • Touma, C., Bunck, M., Glasl, L., Nussbaumer, M., Palme, R., Stein, H., Wolferstatter, M., Zeh, R., Zimbelmann, M., Holsboer, F., & Landgraf, R. (2008). Mice selected for high versus low stress reactivity: A new animal model for affective disorders. Psychoneuroendocrinology, 33(6), 839–862. https://doi.org/10.1016/j.psyneuen.2008.03.013
  • Touma, C., Fenzl, T., Ruschel, J., Palme, R., Holsboer, F., Kimura, M., & Landgraf, R. (2009). Rhythmicity in mice selected for extremes in stress reactivity: Behavioural, endocrine and sleep changes resembling endophenotypes of major depression. PLoS One, 4(1), e4325. https://doi.org/10.1371/journal.pone.0004325
  • Trapp, T., Rupprecht, R., Castren, M., Reul, J. M., & Holsboer, F. (1994). Heterodimerization between mineralocorticoid and glucocorticoid receptor: A new principle of glucocorticoid action in the CNS. Neuron, 13(6), 1457–1462. https://doi.org/10.1016/0896-6273(94)90431-6
  • Tronche, F., Kellendonk, C., Kretz, O., Gass, P., Anlag, K., Orban, P. C., Bock, R., Klein, R., & Schutz, G. (1999). Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nature Genetics, 23(1), 99–103. https://doi.org/10.1038/12703
  • Ulrich-Lai, Y. M., & Herman, J. P. (2009). Neural regulation of endocrine and autonomic stress responses. Nature reviews. Neuroscience, 10(6), 397–409. https://doi.org/10.1038/nrn2647
  • van der Laan, S., de Kloet, E. R., & Meijer, O. C. (2009). Timing is critical for effective glucocorticoid receptor mediated repression of the cAMP-induced CRH gene. PLoS One, 4(1), e4327. https://doi.org/10.1371/journal.pone.0004327
  • van Weert, L., Buurstede, J. C., Mahfouz, A., Braakhuis, P. S. M., Polman, J. A. E., Sips, H. C. M., Roozendaal, B., Balog, J., de Kloet, E. R., Datson, N. A., & Meijer, O. C. (2017). NeuroD factors discriminate mineralocorticoid from glucocorticoid receptor DNA binding in the male rat brain. Endocrinology, 158(5), 1511–1522. https://doi.org/10.1210/en.2016-1422
  • van Weert, L. T. C. M., Buurstede, J. C., Sips, H. C. M., Vettorazzi, S., Mol, I. M., Hartmann, J., Prekovic, S., Zwart, W., Schmidt, M. V., Roozendaal, B., Tuckermann, J. P., Sarabdjitsingh, R. A., & Meijer, O. C. (2019). Identification of mineralocorticoid receptor target genes in the mouse hippocampus. Journal of Neuroendocrinology, 31(8), e12735. https://doi.org/10.1111/jne.12735
  • Vandevyver, S., Dejager, L., & Libert, C. (2014). Comprehensive overview of the structure and regulation of the glucocorticoid receptor. Endocrine Reviews, 35(4), 671–693. https://doi.org/10.1210/er.2014-1010
  • Veenema, A. H., Koolhaas, J. M., & de Kloet, E. R. (2004). Basal and stress-induced differences in HPA axis, 5-HT responsiveness, and hippocampal cell proliferation in two mouse lines. Annals of the New York Academy of Sciences, 1018, 255–265. https://doi.org/10.1196/annals.1296.030
  • Viho, E. M. G., Buurstede, J. C., Mahfouz, A., Koorneef, L. L., van Weert, L., Houtman, R., Hunt, H. J., Kroon, J., & Meijer, O. C. (2019). Corticosteroid action in the brain: The potential of selective receptor modulation. Neuroendocrinology, 109(3), 266–276. https://doi.org/10.1159/000499659
  • Vinckier, F., Rigoux, L., Oudiette, D., & Pessiglione, M. (2018). Neuro-computational account of how mood fluctuations arise and affect decision making. Nature Communications, 9(1), 1708. https://doi.org/10.1038/s41467-018-03774-z
  • Vinkers, C. H., Joels, M., Milaneschi, Y., Gerritsen, L., Kahn, R. S., Penninx, B. W., & Boks, M. P. (2015). Mineralocorticoid receptor haplotypes sex-dependently moderate depression susceptibility following childhood maltreatment. Psychoneuroendocrinology, 54, 90–102. https://doi.org/10.1016/j.psyneuen.2015.01.018
  • Vockley, C. M., D'Ippolito, A. M., McDowell, I. C., Majoros, W. H., Safi, A., Song, L., Crawford, G. E., & Reddy, T. E. (2016). Direct GR binding sites potentiate clusters of TF binding across the human genome. Cell, 166(5), 1269–1281.e19. https://doi.org/10.1016/j.cell.2016.07.049
  • Walker, S. E., Papilloud, A., Huzard, D., & Sandi, C. (2018). The link between aberrant hypothalamic-pituitary-adrenal axis activity during development and the emergence of aggression-Animal studies. Neuroscience and Biobehavioral Reviews, 91, 138–152. https://doi.org/10.1016/j.neubiorev.2016.10.008
  • Walker, S. E., Zanoletti, O., Guillot de Suduiraut, I., & Sandi, C. (2017). Constitutive differences in glucocorticoid responsiveness to stress are related to variation in aggression and anxiety-related behaviors. Psychoneuroendocrinology, 84, 1–10. https://doi.org/10.1016/j.psyneuen.2017.06.011
  • Wamsteeker Cusulin, J. I., Fuzesi, T., Inoue, W., & Bains, J. S. (2013). Glucocorticoid feedback uncovers retrograde opioid signaling at hypothalamic synapses. Nature Neuroscience, 16(5), 596–604. https://doi.org/10.1038/nn.3374
  • Watson, L. C., Kuchenbecker, K. M., Schiller, B. J., Gross, J. D., Pufall, M. A., & Yamamoto, K. R. (2013). The glucocorticoid receptor dimer interface allosterically transmits sequence-specific DNA signals. Nature Structural & Molecular Biology, 20(7), 876–883. https://doi.org/10.1038/nsmb.2595
  • Weikum, E. R., Knuesel, M. T., Ortlund, E. A., & Yamamoto, K. R. (2017). Glucocorticoid receptor control of transcription: Precision and plasticity via allostery. Nature Reviews. Molecular Cell Biology, 18(3), 159–174. https://doi.org/10.1038/nrm.2016.152
  • Whirledge, S., & DeFranco, D. B. (2018). Glucocorticoid signaling in health and disease: Insights from tissue-specific GR knockout mice. Endocrinology, 159(1), 46–64. https://doi.org/10.1210/en.2017-00728
  • Wild, A. R., Sinnen, B. L., Dittmer, P. J., Kennedy, M. J., Sather, W. A., & Dell'Acqua, M. L. (2019). Synapse-to-nucleus communication through NFAT is mediated by L-type Ca2+ channel Ca2+ spike propagation to the soma. Cell Reports, 26(13), 3537–3550.e4. https://doi.org/10.1016/j.celrep.2019.03.005
  • Wochnik, G. M., Ruegg, J., Abel, G. A., Schmidt, U., Holsboer, F., & Rein, T. (2005). FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. The Journal of Biological Chemistry, 280(6), 4609–4616. https://doi.org/10.1074/jbc.M407498200
  • Wood, S. K., & Bhatnagar, S. (2015). Resilience to the effects of social stress: Evidence from clinical and preclinical studies on the role of coping strategies. Neurobiology of Stress, 1, 164–173. https://doi.org/10.1016/j.ynstr.2014.11.002
  • Wook Koo, J., Labonte, B., Engmann, O., Calipari, E. S., Juarez, B., Lorsch, Z., Walsh, J. J., Friedman, A. K., Yorgason, J. T., Han, M. H., & Nestler, E. J. (2016). Essential role of mesolimbic brain-derived neurotrophic factor in chronic social stress-induced depressive behaviors. Biological Psychiatry, 80(6), 469–478. https://doi.org/10.1016/j.biopsych.2015.12.009
  • Yamashita, N., Joshi, R., Zhang, S., Zhang, Z. Y., & Kuruvilla, R. (2017). Phospho-regulation of soma-to-axon transcytosis of neurotrophin receptors. Developmental Cell, 42(6), 626–639 e625. https://doi.org/10.1016/j.devcel.2017.08.009
  • Yang, Y., Yamada, T., Hill, K. K., Hemberg, M., Reddy, N. C., Cho, H. Y., Guthrie, A. N., Oldenborg, A., Heiney, S. A., Ohmae, S., Medina, J. F., Holy, T. E., & Bonni, A. (2016). Chromatin remodeling inactivates activity genes and regulates neural coding. Science (New York, N.Y.), 353(6296), 300–305. https://doi.org/10.1126/science.aad4225
  • Yap, E. L., & Greenberg, M. E. (2018). Activity-regulated transcription: Bridging the gap between neural activity and behavior. Neuron, 100(2), 330–348. https://doi.org/10.1016/j.neuron.2018.10.013
  • Yu, H., Guo, Y., Zhao, Y., Zhou, F., Zhao, K., Li, M., Wen, J., He, Z., Zhu, X., & He, X. (2019). Both insufficient and excessive glucocorticoid receptor-mediated signaling impair neuronal migration. Journal of Endocrinology, 242(2), 103–114.
  • Yu, H., Wang, D. D., Wang, Y., Liu, T., Lee, F. S., & Chen, Z. Y. (2012). Variant brain-derived neurotrophic factor Val66Met polymorphism alters vulnerability to stress and response to antidepressants. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 32(12), 4092–4101. https://doi.org/10.1523/JNEUROSCI.5048-11.2012
  • Yu, X., & Zuo, Y. (2011). Spine plasticity in the motor cortex. Current Opinion in Neurobiology, 21(1), 169–174. https://doi.org/10.1016/j.conb.2010.07.010
  • Zalachoras, I., Verhoeve, S. L., Toonen, L. J., van Weert, L. T., van Vlodrop, A. M., Mol, I. M., Meelis, W., de Kloet, E. R., & Meijer, O. C. (2016). Isoform switching of steroid receptor co-activator-1 attenuates glucocorticoid-induced anxiogenic amygdala CRH expression. Molecular Psychiatry, 21(12), 1733–1739. https://doi.org/10.1038/mp.2016.16
  • Zhang, S. J., Zou, M., Lu, L., Lau, D., Ditzel, D. A., Delucinge-Vivier, C., Aso, Y., Descombes, P., & Bading, H. (2009). Nuclear calcium signaling controls expression of a large gene pool: Identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genetics, 5(8), e1000604. https://doi.org/10.1371/journal.pgen.1000604
  • Zhang, X., Clark, A. F., & Yorio, T. (2008). FK506-binding protein 51 regulates nuclear transport of the glucocorticoid receptor beta and glucocorticoid responsiveness. Investigative Ophthalmology & Visual Science, 49(3), 1037–1047. https://doi.org/10.1167/iovs.07-1279

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.