Developmental and adult stress: effects of steroids and neurosteroids

References

• Abbink, M. R., Kotah, J. M., Hoeijmakers, L., Mak, A., Yvon-Durocher, G., van der Gaag, B., Lucassen, P. J., & Korosi, A. (2020). Characterization of astrocytes throughout life in wildtype and APP/PS1 mice after early-life stress exposure. Journal of Neuroinflammation, 17(1), 1. https://doi.org/10.1186/s12974-020-01762-z
   PubMed Web of Science ®Google Scholar
• Agis-Balboa, R. C., Guidotti, A., & Pinna, G. (2014). 5α-reductase type I expression is downregulated in the prefrontal cortex/Brodmann’s area 9 (BA9) of depressed patients. Psychopharmacology, 231(17), 3569–18. https://doi.org/10.1007/s00213-014-3567-5
   PubMed Web of Science ®Google Scholar
• Agís-Balboa, R. C., Pinna, G., Zhubi, A., Maloku, E., Veldic, M., Costa, E., & Guidotti, A. (2006). Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proceedings of the National Academy of Sciences, 103(39), 14602–14607. https://doi.org/10.1073/pnas.0606544103
   PubMed Web of Science ®Google Scholar
• Alaiyed, S., McCann, M., Mahajan, G., Rajkowska, G., Stockmeier, C. A., Kellar, K. J., Wu, J. Y., & Conant, K. (2020). Venlafaxine stimulates an MMP-9-dependent increase in excitatory/inhibitory balance in a stress model of depression. The Journal of Neuroscience., 40(22), 4418–4431. https://doi.org/10.1523/JNEUROSCI.2387-19.2020
   PubMed Web of Science ®Google Scholar
• Altshuler, L. L., Abulseoud, O. A., Foland-Ross, L., Bartzokis, G., Chang, S., Mintz, J., Hellemann, G., & Vinters, H. V. (2010). Amygdala astrocyte reduction in subjects with major depressive disorder but not bipolar disorder. Bipolar Disorders, Banqueri, M., Méndez, M2(5), 541–549. https://doi.org/10.1111/j.1399-5618.2010.00838.x
   Google Scholar
• Amateau, S. K., Alt, J. J., Stamps, C. L., & McCarthy, M. M. (2004). Brain estradiol content in newborn rats: Sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology, 145(6), 2906–2917. https://doi.org/10.1210/en.2003-1363
   PubMed Web of Science ®Google Scholar
• Baldy, C., Fournier, S., Boisjoly-Villeneuve, S., Tremblay, M.-È., & Kinkead, R. (2018). The influence of sex and neonatal stress on medullary microglia in rat pups. Experimental Physiology, 103(9), 1192–1199. https://doi.org/10.1113/EP087088
   PubMed Web of Science ®Google Scholar
• Banasr, M., Chowdhury, G. M. I., Terwilliger, R., Newton, S. S., Duman, R. S., Behar, K. L., & Sanacora, G. (2010). Glial pathology in an animal model of depression: Reversal of stress- induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Molecular Psychiatry, 15(5), 501–511. https://doi.org/10.1038/mp.2008.106
   PubMed Web of Science ®Google Scholar
• Bangasser, D. A., & Wicks, B. (2017). Sex-specific mechanisms for responding to stress. Journal of Neuroscience Research, 95(1-2), 75–82. https://doi.org/10.1002/jnr.23812
   PubMed Web of Science ®Google Scholar
• Banqueri, M., Méndez, M., Gómez-Lázaro, E., & Arias, J. L. (2019). Early life stress by repeated maternal separation induces long-term neuroinflammatory response in glial cells of male rats. Stress, 22(5), 563–570. https://doi.org/10.1080/10253890.2019.1604666
   PubMed Web of Science ®Google Scholar
• Barbaccia, M. L. (2004). Neurosteroidogenesis: Relevance to neurosteroid actions in brain and modulation by psychotropic drugs. Critical Reviews in Neurobiology, 16(1–2), 67–74. https://doi.org/10.1615/critrevneurobiol.v16.i12.70
   Google Scholar
• Barbaccia, M. L., Roscetti, G., Trabucchi, M., Mostallino, M. C., Concas, A., Purdy, R. H., & Biggio, G. (1996). Time-dependent changes in rat brain neuroactive steroid concentrations and GABAA receptor function after acute stress. Neuroendocrinology, 63(2), 166–172. https://doi.org/10.1159/000126953
   PubMed Web of Science ®Google Scholar
• Barbaccia, M. L., Roscetti, G., Trabucchi, M., Purdy, R. H., Mostallino, M. C., Concas, A., & Biggio, G. (1997). The effects of inhibitors of GABAergic transmission and stress on brain and plasma allopregnanolone concentrations. British Journal of Pharmacology, 120(8), 1582–1588. https://doi.org/10.1038/sj.bjp.0701046
   PubMed Web of Science ®Google Scholar
• Barreto-Cordero, L. M., Ríos-Carrillo, J., Roldán-Roldán, G., Rasia-Filho, A. A., Flores, G., Bringas, M. E., Briones-Aranda, A., & Picazo, O. (2020). Cyclic changes and actions of progesterone and allopregnanolone on cognition and hippocampal basal (stratum oriens) dendritic spines of female rats. Behavioural Brain Research, 379, 112355. https://doi.org/10.1016/j.bbr.2019.112355
   PubMed Web of Science ®Google Scholar
• Baulieu, E. E., Robel, P., & Schumacher, M. (2001). Neurosteroids: Beginning of the story. International Review of Neurobiology, 46, 1–32. https://doi.org/10.1016/s0074-7742(01)46057-0
   PubMed Web of Science ®Google Scholar
• Beato, M., Herrlich, P., & Schütz, G. (1995). Steroid hormone receptors: Many actors in search of a plot. Cell, 83(6), 851–857. https://doi.org/10.1016/0092-8674(95)90201-5
   PubMed Web of Science ®Google Scholar
• Belelli, D., Casula, A., Ling, A., & Lambert, J. J. (2002). The influence of subunit composition on the interaction of neurosteroids with GABA(A) receptors. Neuropharmacology, 43(4), 651–661. https://doi.org/10.1016/s0028-3908(02)00172-7
   PubMed Web of Science ®Google Scholar
• Bian, Y., Pan, Z., Hou, Z., Huang, C., Li, W., & Zhao, B. (2012). Learning, memory, and glial cell changes following recovery from chronic unpredictable stress. Brain Research Bulletin, 88(5), 471–476. https://doi.org/10.1016/j.brainresbull.2012.04.008
   PubMed Web of Science ®Google Scholar
• Bitran, D., Hilvers, R. J., & Kellogg, C. K. (1991). Anxiolytic effects of 3 alpha-hydroxy-5 alpha[beta]-pregnan-20-one: Endogenous metabolites of progesterone that are active at the GABAA receptor. Brain Research, 561(1), 157–161. https://doi.org/10.1016/0006-8993(91)90761-j
   PubMed Web of Science ®Google Scholar
• Black, P. H. (2003). The inflammatory response is an integral part of the stress response: Implications for atherosclerosis, insulin resistance, type II diabetes and metabolic syndrome X. Brain, Behavior, and Immunity, 17(5), 350–364. https://doi.org/10.1016/s0889-1591(03)00048-5
   PubMed Web of Science ®Google Scholar
• Bortolato, M., Devoto, P., Roncada, P., Frau, R., Flore, G., Saba, P., Pistritto, G., Soggiu, A., Pisanu, S., Zappala, A., Ristaldi, M. S., Tattoli, M., Cuomo, V., Marrosu, F., & Barbaccia, M. L. (2011). Isolation rearing-induced reduction of brain 5α-reductase expression: Relevance to dopaminergic impairments. Neuropharmacology, 60(7-8), 1301–1308. https://doi.org/10.1016/j.neuropharm.2011.01.013
   PubMed Web of Science ®Google Scholar
• Calcia, M. A., Bonsall, D. R., Bloomfield, P. S., Selvaraj, S., Barichello, T., & Howes, O. D. (2016). Stress and neuroinflammation: A systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology, 233(9), 1637–1650. https://doi.org/10.1007/s00213-016-4218-9
   PubMed Web of Science ®Google Scholar
• Caruso, D., Pesaresi, M., Maschi, O., Giatti, S., Garcia-Segura, L. M., & Melcangi, R. C. (2010). Effect of short-and long-term gonadectomy on neuroactive steroid levels in the central and peripheral nervous system of male and female rats. Journal of Neuroendocrinology, 22(11), 1137–1147. https://doi.org/10.1111/j.1365-2826.2010.02064.x
   PubMed Web of Science ®Google Scholar
• Catale, C., Martini, A., Piscitelli, R. M., Senzasono, B., Iacono, L. L., Mercuri, N. B., Guatteo, E., & Carola, V. (2022). Early-life social stress induces permanent alterations in plasticity and perineuronal nets in the mouse anterior cingulate cortex. The European Journal of Neuroscience, 56(10), 5763–5783. https://doi.org/10.1111/ejn.15825
   PubMed Web of Science ®Google Scholar
• Chang, C., Saltzman, A., Yeh, S., Young, W., Keller, E., Lee, H. J., Wang, C., & Mizokami, A. (1995). Androgen receptor: An overview. Critical Reviews in Eukaryotic Gene Expression, 5(2), 97–125. https://doi.org/10.1615/critreveukargeneexpr.v5.i2.10
   PubMed Web of Science ®Google Scholar
• Compagnone, N. A., & Mellon, S. H. (2000). Neurosteroids: Biosynthesis and function of these novel neuromodulators. Frontiers in Neuroendocrinology, 21(1), 1–56. https://doi.org/10.1006/frne.1999.0188
   PubMed Web of Science ®Google Scholar
• Crawley, J. N., Glowa, J. R., Majewska, M. D., & Paul, S. M. (1986). Anxiolytic activity of an endogenous adrenal steroid. Brain Research, 398(2), 382–385. https://doi.org/10.1016/0006-8993(86)91500-3
   PubMed Web of Science ®Google Scholar
• Czéh, B., Simon, M., Schmelting, B., Hiemke, C., & Fuchs, E. (2006). Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology, 31(8), 1616–1626. https://doi.org/10.1038/sj.npp.1300982
   PubMed Web of Science ®Google Scholar
• De Kloet, E. R., Rots, N. Y., & Cools, A. R. (1996). Jun Brain-corticosteroid hormone dialogue: Slow and persistent. Cellular and Molecular Neurobiology, 16(3), 345–356. https://doi.org/10.1007/BF02088100
   PubMed Web of Science ®Google Scholar
• Delpech, J. C., Wei, L., Hao, J., Yu, X., Madore, C., Butovsky, O., & Kaffman, A. (2016). Early life stress perturbs the maturation of microglia in the developing hippocampus. Brain, Behavior, and Immunity, 57, 79–93. https://doi.org/10.1016/j.bbi.2016.06.006
   PubMed Web of Science ®Google Scholar
• Dimatelis, J. J., Hendricks, S., Hsieh, J., Vlok, N. M., Bugarith, K., Daniels, W. M. U., & Russell, V. A. (2013). Exercise partly reverses the effect of maternal separation on hippocampal proteins in 6-hydroxydopamine-lesioned rat brain. Experimental Physiology, 98(1), 233–244. https://doi.org/10.1113/expphysiol.2012.066720
   PubMed Web of Science ®Google Scholar
• Dong, E., Matsumoto, K., Uzunova, V., Sugaya, I., Takahata, H., Nomura, H., Watanabe, H., Costa, E., & Guidotti, A. (2001). Brain 5alpha-dihydroprogesterone and allopregnanolone synthesis in a mouse model of protracted social isolation. Proceedings of the National Academy of Sciences, 98(5), 2849–2854. https://doi.org/10.1073/pnas.051628598
   PubMed Web of Science ®Google Scholar
• Drzewiecki, C. M., Willing, J., & Juraska, J. M. (2020). Influences of age and pubertal status on number and intensity of perineuronal nets in the rat medial prefrontal cortex. Brain Structure & Function, 225(8), 2495–2507. https://doi.org/10.1007/s00429-020-02137-z
   PubMed Web of Science ®Google Scholar
• Dufau, M. L., Catt, K. J., & Tsuruhara, T. (1971). Gonadotrophin stimulation of testosterone production by the rat testis in vitro. Biochimica et Biophysica Acta, 252(3), 574–579. https://doi.org/10.1016/0304-4165(71)90161-9
   PubMedGoogle Scholar
• Eck, S. R., Ardekani, C. S., Salvatore, M., Luz, S., Kim, E. D., Rogers, C. M., Hall, A., Lee, D. E., Famularo, S. T., Bhatnagar, S., & Bangasser, D. A. (2020). The effects of early life adversity on growth, maturation, and steroid hormones in male and female rats. The European Journal of Neuroscience, 52(1), 2664–2680. https://doi.org/10.1111/ejn.14609
   PubMed Web of Science ®Google Scholar
• Eck, S. R., Palmer, J. L., Bavley, C. C., Karbalaei, R., Ordoñes Sanchez, E., Flowers, J., Holley, A., Wimmer, M. E., & Bangasser, D. A. (2022). Effects of early life adversity on male reproductive behavior and the medial preoptic area transcriptome. Neuropsychopharmacology, 47(6), 1231–1239. https://doi.org/10.1038/s41386-022-01282-9
   PubMed Web of Science ®Google Scholar
• Eicheler, W., Tuohimaa, P., Vilja, P., Adermann, K., Forssmann, W. G., & Aumüller, G. (1994). Immunocytochemical localization of human 5 alpha-reductase 2 with polyclonal antibodies in androgen target and non-target human tissues. The Journal of Histochemistry and Cytochemistry, 42(5), 667–675. https://doi.org/10.1177/42.5.8157936
   PubMed Web of Science ®Google Scholar
• Evans, A., Terstege, D. J., Scott, G. A., Tsutsui, M., & Epp, J. R. (2022). Neurogenesis mediated plasticity is associated with reduced neuronal activity in CA1 during context fear memory retrieval. Scientific Reports, 12(1), 7016. https://doi.org/10.1038/s41598-022-10947-w
   PubMed Web of Science ®Google Scholar
• Faturi, C. B., Tiba, P. A., Kawakami, S. E., Catallani, B., Kerstens, M., & Suchecki, D. (2010). Disruptions of the mother-infant relationship and stress-related behaviours: Altered corticosterone secretion does not explain everything. Neuroscience and Biobehavioral Reviews, 34(6), 821–834. https://doi.org/10.1016/j.neubiorev.2009.09.002
   PubMed Web of Science ®Google Scholar
• Fevold, H. R., Lorence, M. C., McCarthy, J. L., Trant, J. M., Kagimoto, M., Waterman, M. R., & Mason, J. I. (1989). Rat P450(17 alpha) from testis: Characterization of a full-length cDNA encoding a unique steroid hydroxylase capable of catalyzing both delta 4- and delta 5-steroid-17,20-lyase reactions. Molecular Endocrinology, 3(6), 968–975. https://doi.org/10.1210/mend-3-6-968
   PubMedGoogle Scholar
• Filipović, D., Zlatković, J., Gass, P., & Inta, D. (2013). The differential effects of acute vs. chronic stress and their combination on hippocampal parvalbumin and inducible heat shock protein 70 expression. Neuroscience, 236, 47–54. https://doi.org/10.1016/j.neuroscience.2013.01.033
   PubMed Web of Science ®Google Scholar
• Fonken, L. K., Frank, M. G., Gaudet, A. D., D’Angelo, H. M., Daut, R. A., Hampson, E. C., Ayala, M. T., Watkins, L. R., & Maier, S. F. (2018). Neuroinflammatory priming to stress is differentially regulated in male and female rats. Brain, Behavior, and Immunity, 70, 257–267. https://doi.org/10.1016/j.bbi.2018.03.005
   PubMed Web of Science ®Google Scholar
• Frank, M. G., Baratta, M. V., Sprunger, D. B., Watkins, L. R., & Maier, S. F. (2007). Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain, Behavior, and Immunity, 21(1), 47–59. https://doi.org/10.1016/j.bbi.2006.03.005
   PubMed Web of Science ®Google Scholar
• Frank, M. G., Fonken, L. K., Watkins, L. R., & Maier, S. F. (2019). Microglia: Neuroimmune-sensors of stress. Seminars in Cell & Developmental Biology, 94, 176–185. https://doi.org/10.1016/j.semcdb.2019.01.001
   PubMed Web of Science ®Google Scholar
• Frye, C., Edinger, K., Lephart, E., & Walf, A. (2010). 3α-androstanediol, but not testosterone, attenuates age-related decrements in cognitive, anxiety, and depressive behavior of male rats. Frontiers in Aging Neuroscience, 2, 15. https://doi.org/10.3389/fnagi.2010.00015
   PubMed Web of Science ®Google Scholar
• Ganguly, P., Thompson, V., Gildawie, K., & Brenhouse, H. C. (2018). Adolescent food restriction in rats alters prefrontal cortex microglia in an experience-dependent manner. Stress (Amsterdam, Netherlands), 21(2), 162–168. https://doi.org/10.1080/10253890.2017.1423054
   PubMed Web of Science ®Google Scholar
• Gao, L., Zhao, F., Zhang, Y., Wang, W., & Cao, Q. (2020). Diminished ovarian reserve induced by chronic unpredictable stress in C57BL/6 mice. Gynecological Endocrinology, 36(1), 49–54. https://doi.org/10.1080/09513590.2019.1631274
   PubMed Web of Science ®Google Scholar
• Giatti, S., Diviccaro, S., Serafini, M. M., Caruso, D., Garcia-Segura, L. M., Viviani, B., & Melcangi, R. C. (2020). Sex differences in steroid levels and steroidogenesis in the nervous system: Physiopathological role. Frontiers in Neuroendocrinology, 56, 100804. https://doi.org/10.1016/j.yfrne.2019.100804
   PubMed Web of Science ®Google Scholar
• Gildawie KR, Ryll LM, Hexter JC, Peterzell S, Valentine AA, Brenhouse HC. (2021). A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior. Dev Cogn Neurosci. 48:100924. https://doi.org/10.1016/j.dcn.2021.100924.
   Google Scholar
• Gildawie, K. R., Ryll, L. M., Hexter, J. C., Peterzell, S., Valentine, A. A., & Brenhouse, H. C. (2021). A two- hit adversity model in developing rats reveals sex-specific impacts on PFC structure and behavior. Developmental Cognitive Neuroscience, 48, 100924. https://doi.org/10.1016/j.dcn.2021.100924
   PubMed Web of Science ®Google Scholar
• Gildawie, K. R., Honeycutt, J. A., & Brenhouse, H. C. (2020). Region-specific effects of maternal separation on perineuronal net and parvalbumin-expressing interneuron formation in male and female rats. Neuroscience, 428, 23–37. https://doi.org/10.1016/j.neuroscience.2019.12.010
   PubMed Web of Science ®Google Scholar
• Gillies, G. E., & McArthur, S. (2010). Estrogen actions in the brain and the basis for differential action in men and women: A case for sex-specific medicines. Pharmacological Reviews, 62(2), 155–198. https://doi.org/10.1124/pr.109.002071
   PubMed Web of Science ®Google Scholar
• Giridharan, V. V., Réus, G. Z., Selvaraj, S., Scaini, G., Barichello, T., & Quevedo, J. (2019). Maternal deprivation increases microglial activation and neuroinflammatory markers in the PFC and hippocampus of infant rats. Journal of Psychiatric Research, 115, 13–20. https://doi.org/10.1016/j.jpsychires.2019.05.001
   PubMed Web of Science ®Google Scholar
• Gould, E., Woolley, C. S., Frankfurt, M., & McEwen, B. S. (1990). Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. The Journal of Neuroscience, 10(4), 1286–1291. https://doi.org/10.1523/JNEUROSCI.10-04-01286.1990
   PubMed Web of Science ®Google Scholar
• Guadagno, A., Verlezza, S., Long, H., Wong, T. P., & Walker, C.-D. (2020). It is all in the right amygdala: Increased synaptic plasticity and perineuronal nets in male, but not female, juvenile rat pups after exposure to early-life stress. The Journal of Neuroscience, 40(43), 8276–8291. https://doi.org/10.1523/JNEUROSCI.1029-20.2020
   PubMed Web of Science ®Google Scholar
• Guennoun, R. (2020). Progesterone in the brain: Hormone, neurosteroid and neuroprotectant. International Journal of Molecular Sciences, 21(15), 5271. https://doi.org/10.3390/ijms21155271
   PubMed Web of Science ®Google Scholar
• Hatanaka, Y., Hojo, Y., Mukai, H., Murakami, G., Komatsuzaki, Y., Kim, J., Ikeda, M., Hiragushi, A., Kimoto, T., & Kawato, S. (2015). Rapid increase of spines by dihydrotestosterone and testosterone in hippocampal neurons: Dependence on synaptic androgen receptor and kinase networks. Brain Research, 1621, 121–132. https://doi.org/10.1016/j.brainres.2014.12.011
   PubMed Web of Science ®Google Scholar
• Heitzer, M. D., Wolf, I. M., Sanchez, E. R., Witchel, S. F., & DeFranco, D. B. (2007). Glucocorticoid receptor physiology. Reviews in Endocrine & Metabolic Disorders, 8(4), 321–330. https://doi.org/10.1007/s11154-007-9059-8
   PubMed Web of Science ®Google Scholar
• Hellwig, S., Brioschi, S., Dieni, S., Frings, L., Masuch, A., Blank, T., & Biber, K. (2016). Altered microglia morphology and higher resilience to stress-induced depression-like behavior in CX3CR1-deficient mice. Brain, behavior, and immunity, 55, 126–137. https://doi.org/10.1016/j.bbi.2015.11.008
   Google Scholar
• Hernández-Vivanco, A., Cano-Adamuz, N., Sánchez-Aguilera, A., González-Alonso, A., Rodríguez-Fernández, A., Azcoitia, Í., de la Prida, L. M., & Méndez, P. (2022). Sex-specific regulation of inhibition and network activity by local aromatase in the mouse hippocampus. Nature Communications, 13(1), 3913. https://doi.org/10.1038/s41467-022-31635-3
   PubMed Web of Science ®Google Scholar
• Hiipakka, R. A., & Liao, S. (1998). Molecular mechanism of androgen action. Trends in Endocrinology and Metabolism, 9(8), 317–324. https://doi.org/10.1016/s1043-2760(98)00081-2
   PubMed Web of Science ®Google Scholar
• Hinwood, M., Morandini, J., Day, T. A., & Walker, F. R. (2012). Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial PFC. Cerebral Cortex, 22(6), 1442–1454. https://doi.org/10.1093/cercor/bhr229
   PubMed Web of Science ®Google Scholar
• Hinwood, M., Tynan, R. J., Charnley, J. L., Beynon, S. B., Day, T. A., & Walker, F. R. (2013). Chronic stress induced remodeling of the prefrontal: Structural re-organization of microglia and the inhibitory effect of minocycline. Cerebral Cortex, 23(8), 1784–1797. https://doi.org/10.1093/cercor/bhs151
   PubMed Web of Science ®Google Scholar
• Hoeijmakers, L., Ruigrok, S. R., Amelianchik, A., Ivan, D., van Dam, A.-M., Lucassen, P. J., & Korosi, A. (2017). Early-life stress lastingly alters the neuroinflammatory response to amyloid pathology in an Alzheimer’s disease mouse model. Brain, Behavior, and Immunity, 63, 160–175. https://doi.org/10.1016/j.bbi.2016.12.023
   PubMed Web of Science ®Google Scholar
• Hojo, Y., & Kawato, S. (2018). Neurosteroids in adult hippocampus of male and female rodents: Biosynthesis and actions of sex steroids. Frontiers in Endocrinology, 9, 183. https://doi.org/10.3389/fendo.2018.00183
   PubMed Web of Science ®Google Scholar
• Hokenson, R. E., Alam, Y. H., Short, A. K., Jung, S., Jang, C., & Baram, T. Z. (2022). Sex-dependent effects of multiple acute concurrent stresses on memory: A role for hippocampal estrogens. Frontiers in Behavioral Neuroscience, 16, 984494. https://doi.org/10.3389/fnbeh.2022.984494
   PubMed Web of Science ®Google Scholar
• Hokenson, R. E., Short, A. K., Chen, Y., Pham, A. L., Adams, E. T., Bolton, J. L., Swarup, V., Gall, C. M., & Baram, T. Z. (2021). Unexpected role of physiological estrogen in acute stress-induced memory deficits. The Journal of Neuroscience. 41(4), 648–662. https://doi.org/10.1523/JNEUROSCI.2146-20.2020
   PubMed Web of Science ®Google Scholar
• Holst, J. P., Soldin, O. P., Guo, T., & Soldin, S. J. (2004). Steroid hormones: Relevance and measurement in the clinical laboratory. Clinics in Laboratory Medicine, 24(1), 105–118. https://doi.org/10.1016/j.cll.2004.01.004
   PubMed Web of Science ®Google Scholar
• Horchar, M. J., & Wohleb, E. S. (2019). Glucocorticoid receptor antagonism prevents microglia-mediated neuronal remodeling and behavioral despair following chronic unpredictable stress. Brain, Behavior, and Immunity, 81, 329–340. https://doi.org/10.1016/j.bbi.2019.06.030
   PubMed Web of Science ®Google Scholar
• Im, A., & Appleman, L. J. (2010). Mifepristone: Pharmacology and clinical impact in reproductive medicine, endocrinology and oncology. Expert Opinion on Pharmacotherapy, 11(3), 481–488. https://doi.org/10.1517/14656560903535880
   PubMed Web of Science ®Google Scholar
• Jin, Y., & Penning, T. M. (2001). Steroid 5alpha-reductases and 3alpha-hydroxysteroid dehydrogenases: Key enzymes in androgen metabolism. Best Practice & Research. Clinical Endocrinology & Metabolism, 15(1), 79–94. https://doi.org/10.1053/beem.2001.0120
   PubMed Web of Science ®Google Scholar
• Jolivel, V., Brun, S., Binamé, F., Benyounes, J., Taleb, O., Bagnard, D., De Sèze, J., Patte-Mensah, C., & Mensah-Nyagan, A.-G. (2021). Microglial cell morphology and phagocytic activity are critically regulated by the neurosteroid allopregnanolone: A possible role in neuroprotection. Cells, 10(3), 698. https://doi.org/10.3390/cells10030698
   PubMed Web of Science ®Google Scholar
• Katahira, T., Miyazaki, N., & Motoyama, J. (2018). Immediate effects of maternal separation on the development of interneurons derived from medial ganglionic eminence in the neonatal mouse hippocampus. Development, Growth & Differentiation, 60(5), 278–290. https://doi.org/10.1111/dgd.12540
   PubMed Web of Science ®Google Scholar
• Kehoe, P., Mallinson, K., McCormick, C. M., & Frye, C. A. (2000). Central allopregnanolone is increased in rat pups in response to repeated, short episodes of neonatal isolation. Developmental Brain Research, 124(1-2), 133–136. https://doi.org/10.1016/S0165-3806(00)00106-1
   PubMedGoogle Scholar
• Kettenmann, H., Hanisch, U.-K., Noda, M., & Verkhratsky, A. (2011). Physiology of microglia. Physiological Reviews, 91(2), 461–553. https://doi.org/10.1152/physrev.00011.2010
   PubMed Web of Science ®Google Scholar
• Kiecolt-Glaser, J. K., Glaser, R., Gravenstein, S., Malarkey, W. B., & Sheridan, J. (1996). Chronic stress alters the immune response to influenza virus vaccine in older adults. Proceedings of the National Academy of Sciences, 93(7), 3043–3047. https://doi.org/10.1073/pnas.93.7.3043
   PubMed Web of Science ®Google Scholar
• Kim, E. J., Pellman, B., & Kim, J. J. (2015). Stress effects on the hippocampus: A critical review. Learning & Memory, 22(9), 411–416. https://doi.org/10.1101/lm.037291.114
   PubMed Web of Science ®Google Scholar
• Kimoto, T, Tsurugizawa, T, Ohta, Y, Makino, J, Hojo, Y, Takata, N, Kawato, S., & Ho, S. (2001). Neurosteroid synthesis by cytochrome p450-containing systems localized in the rat brain hippocampal neurons: N-methyl-D-aspartate and calcium- dependent synthesis. Endocrinology, 142(8), 3578–3589. https://doi.org/10.1210/endo.142.8.8327
   PubMed Web of Science ®Google Scholar
• Klimczak, P., Rizzo, A., Castillo-Gómez, E., Perez-Rando, M., Gramuntell, Y., Beltran, M., & Nacher, J. (2021). Parvalbumin interneurons and perineuronal nets in the hippocampus and retrosplenial cortex of adult male mice after early social isolation stress and perinatal NMDA receptor antagonist treatment. Frontiers in Synaptic Neuroscience, 13, 733989. https://doi.org/10.3389/fnsyn.2021.733989
   PubMed Web of Science ®Google Scholar
• Kojo, A., Yamada, K., Kubo, K. Y., Yamashita, A., & Yamamoto, T. (2010). Occlusal disharmony in mice transiently activates microglia in hippocampal CA1 region but not in dentate gyrus. The Tohoku Journal of Experimental Medicine, 221(3), 237–243. https://doi.org/10.1620/tjem.221.237
   PubMed Web of Science ®Google Scholar
• Kontula, K., Paavonen, T., Luukkainen, T., & Andersson, L. C. (1983). Binding of progestins to the glucocorticoid receptor. Correlation to their glucocorticoid-like effects on in vitro functions of human mononuclear leukocytes. Biochemical Pharmacology, 32(9), 1511–1518. https://doi.org/10.1016/0006-2952(83)90474-4
   PubMed Web of Science ®Google Scholar
• Koritz, S. B., & Kumar, A. M. (1970). On the mechanism of action of the adrenocorticotrophic hormone. The stimulation of the activity of enzymes involved in pregnenolone synthesis. The Journal of Biological Chemistry, 245(1), 152–159. https://doi.org/10.1016/S0021-9258(18)63433-7
   PubMed Web of Science ®Google Scholar
• Kraus, K. L., Chordia, A. P., Drake, A. W., Herman, J. P., & Danzer, S. C. (2022). Hippocampal interneurons are direct targets for circulating glucocorticoids. The Journal of Comparative Neurology, 530(12), 2100–2112. https://doi.org/10.1002/cne.25322
   PubMed Web of Science ®Google Scholar
• Kvarta, M. D., Bradbrook, K. E., Dantrassy, H. M., Bailey, A. M., & Thompson, S. M. (2015). Corticosterone mediates the synaptic and behavioral effects of chronic stress at rat hippocampal temporoammonic synapses. Journal of Neurophysiology, 114(3), 1713–1724. https://doi.org/10.1152/jn.00359.2015
   PubMed Web of Science ®Google Scholar
• Laham, B. J., & Gould, E. (2022). How stress influences the dynamic plasticity of the brain’s extracellular matrix. Frontiers in Cellular Neuroscience, 15, 814287. https://doi.org/10.3389/fncel.2021.814287
   PubMed Web of Science ®Google Scholar
• Laham, B. J., Murthy, S. S., Hanani, M., Clappier, M., Boyer, S., Vasquez, B., & Gould, E. (2022). The estrous cycle modulates early-life adversity effects on mouse avoidance behavior through progesterone signaling. Nature Communications, 13(1), 7537. https://doi.org/10.1038/s41467-022-35068-w
   PubMed Web of Science ®Google Scholar
• Lee, J., & Lee, K. (2021). Parvalbumin-expressing GABAergic interneurons and perineuronal nets in the prelimbic and orbitofrontal cortices in association with basal anxiety-like behaviors in adult mice. Behavioural Brain Research, 398, 112915. https://doi.org/10.1016/j.bbr.2020.112915
   PubMed Web of Science ®Google Scholar
• Li, L. F., Yang, J., Ma, S. P., & Qu, R. (2013). Magnolol treatment reversed the glial pathology in an unpredictable chronic mild stress-induced rat model of depression. European Journal of Pharmacology, 711(1-3), 42–49. https://doi.org/10.1016/j.ejphar.2013.04.008
   PubMed Web of Science ®Google Scholar
• Liu, Q., Li, B., Zhu, H.-Y., Wang, Y.-Q., Yu, J., & Wu, G.-C. (2009). Clomipramine treatment reversed the glial pathology in a chronic unpredictable stress-induced rat model of depression. European Neuropsychopharmacology, 19(11), 796–805. https://doi.org/10.1016/j.euroneuro.2009.06.010
   PubMed Web of Science ®Google Scholar
• Liu, Q., Li, B., Zhu, H.-Y., Wang, Y.-Q., Yu, J., & Wu, G.-C. (2011). Glia atrophy in the hippocampus of chronic unpredictable stress-induced depression model rats is reversed by electroacupuncture treatment. Journal of Affective Disorders, 128(3), 309–313. https://doi.org/10.1016/j.jad.2010.07.007
   PubMed Web of Science ®Google Scholar
• Liu, R., Yang, X. D., Liao, X. M., Xie, X. M., Su, Y. A., Li, J. T., Wang, X. D., & Si, T. M. (2016). Early postnatal stress suppresses the developmental trajectory of hippocampal pyramidal neurons: The role of CRHR1. Brain Structure & Function, 221(9), 4525–4536. https://doi.org/10.1007/s00429-016-1182-4
   PubMed Web of Science ®Google Scholar
• Lloyd-Evans, E., & Waller-Evans, H. (2020). Biosynthesis and signalling functions of central and peripheral nervous system neurosteroids in health and disease. Essays in Biochemistry, 64(3), 591–606. https://doi.org/10.1042/EBC20200043
   PubMed Web of Science ®Google Scholar
• López-Calderón, A., Gonzaléz-Quijano, M. I., Tresguerres, J. A., & Ariznavarreta, C. (1990). Role of LHRH in the gonadotrophin response to restraint stress in intact male rats. The Journal of Endocrinology, 124(2), 241–246. https://doi.org/10.1677/joe.0.1240241
   PubMed Web of Science ®Google Scholar
• Lou, Y. X., Li, J., Wang, Z. Z., Xia, C. Y., & Chen, N. H. (2018). Glucocorticoid receptor activation induces decrease of hippocampal astrocyte number in rats. Psychopharmacology, 235(9), 2529–2540. https://doi.org/10.1007/s00213-018-4936-2
   PubMed Web of Science ®Google Scholar
• Luine, V., Villegas, M., Martinez, C., & McEwen, B. S. (1994). Repeated stress causes reversible impairments of spatial memory performance. Brain Research, 639(1), 167–170. https://doi.org/10.1016/0006-8993(94)91778-7
   PubMed Web of Science ®Google Scholar
• MacLusky, N. J., Walters, M. J., Clark, A. S., & Toran-Allerand, C. D. (1994). Aromatase in the cerebral cortex, hippocampus, and mid-brain: Ontogeny and developmental implications. Molecular and Cellular Neurosciences, 5(6), 691–698. https://doi.org/10.1006/mcne.1994.1083
   PubMed Web of Science ®Google Scholar
• Manna, P. R., Cohen-Tannoudji, J., Counis, R., Garner, C. W., Huhtaniemi, I., Kraemer, F. B., & Stocco, D. M. (2013). Mechanisms of action of hormone-sensitive lipase in mouse Leydig cells: Its role in the regulation of the steroidogenic acute regulatory protein. The Journal of Biological Chemistry, 288(12), 8505–8518. https://doi.org/10.1074/jbc.M112.417873
   PubMed Web of Science ®Google Scholar
• Mataradze, G. D., Kurabekova, R. M., & Rozen, V. B. (1992). The role of sex steroids in the formation of sex-differentiated concentrations of corticosteroid-binding globulin in rats. The Journal of Endocrinology, 132(2), 235–240. https://doi.org/10.1677/joe.0.1320235
   PubMed Web of Science ®Google Scholar
• McEwen, B. (2002). Estrogen actions throughout the brain. Recent Progress in Hormone Research, 57(1), 357–384. https://doi.org/10.1210/rp.57.1.357
   PubMedGoogle Scholar
• McEwen, B. S., Nasca, C., & Gray, J. D. (2016). Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41(1), 3–23. https://doi.org/10.1038/npp.2015.171
   PubMed Web of Science ®Google Scholar
• Meffre, D., Pianos, A., Liere, P., Eychenne, B., Cambourg, A., Schumacher, M., Stein, D. G., & Guennoun, R. (2007). Steroid profiling in brain and plasma of male and pseudopregnant female rats after traumatic brain injury: Analysis by gas chromatography/mass spectrometry. Endocrinology, 148(5), 2505–2517. https://doi.org/10.1210/en.2006-1678
   PubMed Web of Science ®Google Scholar
• Mellon, S. H., & Griffin, L. D. (2002). Neurosteroids: Biochemistry and clinical significance. Trends in Endocrinology and Metabolism, 13(1), 35–43. https://doi.org/10.1016/s1043-2760(01)00503-3
   PubMed Web of Science ®Google Scholar
• Miller, W. L., & Bose, H. S. (2011). Early steps in steroidogenesis: Intracellular cholesterol trafficking. Journal of Lipid Research, 52(12), 2111–2135. https://doi.org/10.1194/jlr.R016675
   PubMed Web of Science ®Google Scholar
• Mirescu, C., Peters, J. D., & Gould, E. (2004). Early life experience alters response of adult neurogenesis to stress. Nature Neuroscience, 7(8), 841–846. https://doi.org/10.1038/nn1290
   PubMed Web of Science ®Google Scholar
• Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005). Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proceedings of the National Academy of Sciences, 102(26), 9371–9376. https://doi.org/10.1073/pnas.0504011102
   PubMed Web of Science ®Google Scholar
• Miyaso, H., Nagahori, K., Takano, K., Omotehara, T., Kawata, S., Li, Z. L., Kuramasu, M., Wu, X., Ogawa, Y., & Itoh, M. (2021). Neonatal maternal separation causes decreased numbers of sertoli cell, spermatogenic cells, and sperm in mice. Toxicology Mechanisms and Methods, 31(2), 116–125. https://doi.org/10.1080/15376516.2020.1841865
   PubMed Web of Science ®Google Scholar
• Moisan, M.-P. (2021). Sexual dimorphism in glucocorticoid stress response. International Journal of Molecular Sciences, 22(6), 3139. https://doi.org/10.3390/ijms22063139
   PubMed Web of Science ®Google Scholar
• Monroy, E., Hernández-Torres, E., & Flores, G. (2010). Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. Journal of Chemical Neuroanatomy, 40(2), 93–101. https://doi.org/10.1016/j.jchemneu.2010.05.005
   PubMed Web of Science ®Google Scholar
• Murphy-Royal, C., Gordon, G. R., & Bains, J. S. (2019). Stress-induced structural and functional modifications of astrocytes—Further implicating glia in the central response to stress. Glia, 67(10), 1806–1820. https://doi.org/10.1002/glia.23610
   PubMed Web of Science ®Google Scholar
• Murthy, S., Kane, G. A., Katchur, N. J., Lara Mejia, P. S., Obiofuma, G., Buschman, T. J., McEwen, B. S., & Gould, E. (2019). Perineuronal nets, inhibitory interneurons, and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity. Biological Psychiatry, 85(12), 1011–1020. https://doi.org/10.1016/j.biopsych.2019.02.021
   PubMed Web of Science ®Google Scholar
• Musholt, K., Cirillo, G., Cavaliere, C., Rosaria Bianco, M., Bock, J., Helmeke, C., Braun, K., & Papa, M. (2009). Neonatal separation stress reduces glial fibrillary acidic protein- and S100beta-immunoreactive astrocytes in the rat medial precentral cortex. Developmental Neurobiology, 69(4), 203–211. https://doi.org/10.1002/dneu.20694
   PubMed Web of Science ®Google Scholar
• Muthu, S. J., Lakshmanan, G., Shimray, K. W., Kaliyappan, K., Sathyanathan, S. B., & Seppan, P. (2022). Testosterone influence on microtubule-associated proteins and spine density in hippocampus: Implications on learning and memory. Developmental Neuroscience, 44(6), 498–507. https://doi.org/10.1159/000525038
   PubMed Web of Science ®Google Scholar
• Nair, A., & Bonneau, R. H. (2006). Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. Journal of Neuroimmunology, 171(1-2), 72–85. https://doi.org/10.1016/j.jneuroim.2005.09.012
   PubMed Web of Science ®Google Scholar
• Nelson, L. R., & Bulun, S. E. (2001). Estrogen production and action. Journal of the American Academy of Dermatology, 45(3 Suppl), S116–S124. https://doi.org/10.1067/mjd.2001.117432
   PubMed Web of Science ®Google Scholar
• Omura, T. (2006). Mitochondrial P450s. Chemico-Biological Interactions, 163(1-2), 86–93. https://doi.org/10.1016/j.cbi.2006.06.008
   PubMed Web of Science ®Google Scholar
• Osawa, Y., Higashiyama, T., Shimizu, Y., & Yarborough, C. (1993). Multiple functions of aromatase and the active site structure; aromatase is the placental estrogen 2- hydroxylase. The Journal of Steroid Biochemistry and Molecular Biology, 44(4-6), 469–480. https://doi.org/10.1016/0960-0760(93)90252-r
   PubMed Web of Science ®Google Scholar
• Pallarès, M., Llidó, A., Mòdol, L., Vallée, M., & Darbra, S. (2015). Finasteride administration potentiates the disruption of prepulse inhibition induced by forced swim stress. Behavioural Brain Research, 289, 55–60. https://doi.org/10.1016/j.bbr.2015.04.023
   PubMed Web of Science ®Google Scholar
• Papadopoulos, V., Amri, H., Boujrad, N., Cascio, C., Culty, M., Garnier, M., Hardwick, M., Li, H., Vidic, B., Brown, A. S., Reversa, J. L., Bernassau, J. M., & Drieu, K. (1997). Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids, 62(1), 21–28. https://doi.org/10.1016/s0039-128x(96)00154-7
   PubMed Web of Science ®Google Scholar
• Paris, J. J., & Frye, C. A. (2011a). Gestational exposure to variable stressors produces decrements in cognitive and neural development of juvenile male and female rats. Current Topics in Medicinal Chemistry, 11(13), 1706–1713.
   PubMed Web of Science ®Google Scholar
• Paris, J. J., & Frye, C. A. (2011b). Juvenile offspring of rats exposed to restraint stress in late gestation have impaired cognitive performance and dysregulated progestogen formation. Stress (Amsterdam, Netherlands), 14(1), 23–32. https://doi.org/10.3109/10253890.2010.512375
   PubMed Web of Science ®Google Scholar
• Paris, J. J., Brunton, P. J., Russell, J. A., & Frye, C. A. (2011). Immune stress in late pregnant rats decreases length of gestation and fecundity, and alters later cognitive and affective behaviour of surviving pre-adolescent offspring. Stress, 14(6), 652–664. https://doi.org/10.3109/10253890.2011.628719
   PubMed Web of Science ®Google Scholar
• Park, J. H., Yoo, K.-Y., Lee, C. H., Kim, I. H., Shin, B. N., Choi, J. H., Park, J. H., Hwang, I. K., & Won, M.-H. (2011). Comparison of glucocorticoid receptor and ionized calcium-binding adapter molecule 1 immunoreactivity in the adult and aged gerbil hippocampus following repeated restraint stress. Neurochemical Research, 36(6), 1037–1045. https://doi.org/10.1007/s11064-011-0444-z
   PubMed Web of Science ®Google Scholar
• Penning, T. M., Jin, Y., Steckelbroeck, S., Lanisnik Rizner, T., & Lewis, M. (2004). Structure-function of human 3 alpha-hydroxysteroid dehydrogenases: genes and proteins. Molecular and cellular endocrinology, 215(1-2), 63–72. https://doi.org/10.1016/j.mce.2003.11.006
   Google Scholar
• Pesaresi, M., Maschi, O., Giatti, S., Garcia-Segura, L. M., Caruso, D., & Melcangi, R. C. (2010). Sex differences in neuroactive steroid levels in the nervous system of diabetic and non-diabetic rats. Hormones and Behavior, 57(1), 46–55. https://doi.org/10.1016/j.yhbeh.2009.04.008
   PubMed Web of Science ®Google Scholar
• Pinna, G., Agis-Balboa, R. C., Doueiri, M.-S., Guidotti, A., & Costa, E. (2004). Brain neurosteroids in gender-related aggression induced by social isolation. Critical Reviews in Neurobiology, 16(1-2), 75–82.
   PubMedGoogle Scholar
• Porcu, P., Barron, A. M., Frye, C. A., Walf, A. A., Yang, S.-Y., He, X.-Y., Morrow, A. L., Panzica, G. C., & Melcangi, R. C. (2016). Neurosteroidogenesis today: Novel targets for neuroactive steroid synthesis and action and their relevance for translational research. Journal of Neuroendocrinology, 28(2), 12351. https://doi.org/10.1111/jne.12351
   PubMed Web of Science ®Google Scholar
• Puia, G., Mienville, J. M., Matsumoto, K., Takahata, H., Watanabe, H., Costa, E., & Guidotti, A. (2003). On the putative physiological role of allopregnanolone on GABAA receptor function. Neuropharmacology, 44(1), 49–55. https://doi.org/10.1016/S0028-3908(02)00341-6
   PubMed Web of Science ®Google Scholar
• Purdy, R. H., Morrow, A. L., Moore, P. H., & Paul, S. M. (1991). Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proceedings of the National Academy of Sciences, 88(10), 4553–4557. https://doi.org/10.1073/pnas.88.10.4553
   PubMed Web of Science ®Google Scholar
• Raff, H. (2016). CORT, Cort, B, Corticosterone, and now cortistatin: Enough already!. Endocrinology, 157(9), 3307–3308. https://doi.org/10.1210/en.2016-1500
   PubMed Web of Science ®Google Scholar
• Reddy, D. S., & Jian, K. (2010). The testosterone-derived neurosteroid androstanediol is a positive allosteric modulator of GABAA receptors. The Journal of Pharmacology and Experimental Therapeutics, 334(3), 1031–1041. https://doi.org/10.1124/jpet.110.169854
   PubMed Web of Science ®Google Scholar
• Reddy, D. S., & Rogawski, M. A. (2002). Stress-induced deoxycorticosterone-derived neurosteroids modulate GABAA receptor function and seizure susceptibility. The Journal of Neuroscience, 22(9), 3795–3805. https://doi.org/10.1523/JNEUROSCI.22-09-03795.2002
   PubMed Web of Science ®Google Scholar
• Reschke-Hernández, A. E., Okerstrom, K. L., Bowles Edwards, A., & Tranel, D. (2017). Sex and stress: Men and women show different cortisol responses to psychological stress induced by the Trier social stress test and the Iowa singing social stress test. Journal of Neuroscience Research, 95(1-2), 106–114. https://doi.org/10.1002/jnr.23851
   PubMed Web of Science ®Google Scholar
• Retana-Márquez, S., Bonilla-Jaime, H., Vázquez-Palacios, G., Martínez-García, R., & Velázquez-Moctezuma, J. (2003). Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Hormones and Behavior, 44(4), 327–337. https://doi.org/10.1016/j.yhbeh.2003.04.001
   PubMed Web of Science ®Google Scholar
• Réus, G. Z., Fernandes, G. C., de Moura, A. B., Silva, R. H., Darabas, A. C., de Souza, T. G., Abelaira, H. M., Carneiro, C., Wendhausen, D., Michels, M., Pescador, B., Dal-Pizzol, F., Macêdo, D. S., & Quevedo, J. (2017). Early life experience contributes to the developmental programming of depressive-like behaviour, neuroinflammation and oxidative stress. Journal of Psychiatric Research, 95, 196–207. https://doi.org/10.1016/j.jpsychires.2017.08.020
   PubMed Web of Science ®Google Scholar
• Réus, G. Z., Giridharan, V. V., de Moura, A. B., Borba, L. A., Botelho, M. E. M., Behenck, J. P., Generoso, J. S., Selvaraj, S., Bhatti, G., Barichello, T., & Quevedo, J. (2021). The impact of early life stress and immune challenge on behavior and glia cells alteration in late adolescent rats. International Journal of Developmental Neuroscience, 81(5), 407–415. https://doi.org/10.1002/jdn.10108
   PubMed Web of Science ®Google Scholar
• Réus, G. Z., Silva, R. H., de Moura, A. B., Presa, J. F., Abelaira, H. M., Abatti, M., Vieira, A., Pescador, B., Michels, M., Ignácio, Z. M., Dal-Pizzol, F., & Quevedo, J. (2019). Early maternal deprivation induces microglial activation, alters glial fibrillary acidic protein immunoreactivity and indoleamine 2,3-dioxygenase during the development of offspring rats. Molecular Neurobiology, 56(2), 1096–1108. https://doi.org/10.1007/s12035-018-1161-2
   PubMed Web of Science ®Google Scholar
• Riga, D., Kramvis, I., Koskinen, M. K., van Bokhoven, P., van der Harst, J. E., Heistek, T. S., Jaap Timmerman, A., van Nierop, P., van der Schors, R. C., Pieneman, A. W., de Weger, A., van Mourik, Y., Schoffelmeer, A. N. M., Mansvelder, H. D., Meredith, R. M., Hoogendijk, W. J. G., Smit, A. B., & Spijker, S. (2017). Hippocampal extracellular matrix alterations contribute to cognitive impairment associated with a chronic depressive-like state in rats. Science Translational Medicine, 9(421), eaai8753. https://doi.org/10.1126/scitranslmed.aai8753
   PubMed Web of Science ®Google Scholar
• Rochefort, H., & Garcia, M. (1976). Androgen on the estrogen receptor. I—binding and in vivo nuclear translocation. Steroids, 28(4), 549–560. https://doi.org/10.1016/0039-128x(76)90023-4
   PubMed Web of Science ®Google Scholar
• Romeo, R. D., Karatsoreos, I. N., Ali, F. S., & McEwen, B. S. (2007). The effects of acute stress and pubertal development on metabolic hormones in the rat. Stress (Amsterdam, Netherlands), 10(1), 101–106. https://doi.org/10.1080/10253890701204270
   PubMed Web of Science ®Google Scholar
• Römer, B., & Gass, P. (2010). Finasteride‐induced depression: New insights into possible pathomechanisms. Journal of Cosmetic Dermatology, 9(4), 331–332. https://doi.org/10.1111/j.1473-2165.2010.00533.x
   PubMed Web of Science ®Google Scholar
• Römer, B., Pfeiffer, N., Lewicka, S., Ben-Abdallah, N., Vogt, M. A., Deuschle, M., Vollmayr, B., & Gass, P. (2010). Finasteride treatment inhibits adult hippocampal neurogenesis in male mice. Pharmacopsychiatry, 43(5), 174–178. https://doi.org/10.1055/s-0030-1249095
   PubMed Web of Science ®Google Scholar
• Rone, M. B., Fan, J., & Papadopoulos, V. (2009). Cholesterol transport in steroid biosynthesis: Role of protein-protein interactions and implications in disease states. Biochimica et Biophysica Acta, 1791(7), 646–658. https://doi.org/10.1016/j.bbalip.2009.03.001
   PubMed Web of Science ®Google Scholar
• Roque, A., Ochoa-Zarzosa, A., & Torner, L. (2016). Maternal separation activates microglial cells and induces an inflammatory response in the hippocampus of male rat pups, independently of hypothalamic and peripheral cytokine levels. Brain, Behavior, and Immunity, 55, 39–48. https://doi.org/10.1016/j.bbi.2015.09.017
   PubMed Web of Science ®Google Scholar
• Rosol, T. J., Yarrington, J. T., Latendresse, J., & Capen, C. C. (2001). Adrenal gland: Structure, function, and mechanisms of toxicity. Toxicologic Pathology, 29(1), 41–48. https://doi.org/10.1080/019262301301418847
   PubMed Web of Science ®Google Scholar
• Rubinow, K. B. (2018). An intracrine view of sex steroids, immunity, and metabolic regulation. Molecular Metabolism, 15, 92–103. https://doi.org/10.1016/j.molmet.2018.03.001
   PubMed Web of Science ®Google Scholar
• Saavedra, L. M., Fenton Navarro, B., & Torner, L. (2017). Early life stress activates glial cells in the hippocampus but attenuates cytokine secretion in response to an immune challenge in rat pups. Neuroimmunomodulation, 24(4-5), 242–255. https://doi.org/10.1159/000485383
   PubMed Web of Science ®Google Scholar
• Saldanha, C. J., Remage-Healey, L., & Schlinger, B. A. (2011). Synaptocrine signaling: Steroid synthesis and action at the synapse. Endocrine Reviews, 32(4), 532–549. https://doi.org/10.1210/er.2011-0004
   PubMed Web of Science ®Google Scholar
• Santiago, A. N., Lim, K. Y., Opendak, M., Sullivan, R. M., & Aoki, C. (2018). Early life trauma increases threat response of peri‐weaning rats, reduction of axo‐somatic synapses formed by parvalbumin cells and perineuronal net in the basolateral nucleus of amygdala. The Journal of Comparative Neurology, 526(16), 2647–2664. https://doi.org/10.1002/cne.24522
   PubMed Web of Science ®Google Scholar
• Saur, L., Baptista, P. P. A., Bagatini, P. B., Neves, L. T., de Oliveira, R. M., Vaz, S. P., Ferreira, K., Machado, S. A., Mestriner, R. G., & Xavier, L. L. (2016). Experimental post-traumatic stress disorder decreases astrocyte density and changes astrocytic polarity in the CA1 hippocampus of male rats. Neurochemical Research, 41(4), 892–904. https://doi.org/10.1007/s11064-015-1770-3
   PubMed Web of Science ®Google Scholar
• Schiavone, S., Sorce, S., Dubois-Dauphin, M., Jaquet, V., Colaianna, M., Zotti, M., Cuomo, V., Trabace, L., & Krause, K.-H. (2009). Involvement of NOX2 in the development of behavioral and pathologic alterations in isolated rats. Biological Psychiatry, 66(4), 384–392. https://doi.org/10.1016/j.biopsych.2009.04.033
   PubMed Web of Science ®Google Scholar
• Schverer, M., Lanfumey, L., Baulieu, E.-E., Froger, N., & Villey, I. (2018). Neurosteroids: Non-genomic pathways in neuroplasticity and involvement in neurological diseases. Pharmacology & Therapeutics, 191, 190–206. https://doi.org/10.1016/j.pharmthera.2018.06.011
   PubMed Web of Science ®Google Scholar
• Serra, M., Pisu, M. G., Floris, I., & Biggio, G. (2005). Social isolation-induced changes in the hypothalamic–pituitary–adrenal axis in the rat. Stress, 8(4), 259–264. https://doi.org/10.1080/10253890500495244
   PubMed Web of Science ®Google Scholar
• Serra, M., Pisu, M. G., Littera, M., Papi, G., Sanna, E., Tuveri, F., Usala, L., Purdy, R. H., & Biggio, G. (2000). Social isolation-induced decreases in both the abundance of neuroactive steroids and GABAA receptor function in rat brain. Journal of Neurochemistry, 75(2), 732–740. https://doi.org/10.1046/j.1471-4159.2000.0750732.x
   PubMed Web of Science ®Google Scholar
• Shansky, R. M., Hamo, C., Hof, P. R., Lou, W., McEwen, B. S., & Morrison, J. H. (2010). Estrogen promotes stress sensitivity in a PFC–amygdala pathway. Cerebral Cortex, 20(11), 2560–2567. https://doi.org/10.1093/cercor/bhq003
   PubMed Web of Science ®Google Scholar
• Shimizu, H., Ishizuka, Y., Yamazaki, H., & Shirao, T. (2015). Allopregnanolone increases mature excitatory synapses along dendrites via protein kinase A signaling. Neuroscience, 305, 139–145. https://doi.org/10.1016/j.neuroscience.2015.07.079
   PubMed Web of Science ®Google Scholar
• Shirayama, Y., Muneoka, K., Fukumoto, M., Tadokoro, S., Fukami, G., Hashimoto, K., & Iyo, M. (2011). Infusions of allopregnanolone into the hippocampus and amygdala, but not into the nucleus accumbens and medial PFC, produce antidepressant effects on the learned helplessness rats. Hippocampus, 21(10), 1105–1113. https://doi.org/10.1002/hipo.20824
   PubMed Web of Science ®Google Scholar
• Shors, T. J., Chua, C., & Falduto, J. (2001). Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. The Journal of neuroscience : the official journal of the Society for Neuroscience, 21(16), 6292–6297. https://doi.org/10.1523/JNEUROSCI.21-16-06292.2001
   Google Scholar
• Shors, T. J., Chua, C., & Falduto, J. (2001). Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. The Journal of Neuroscience, 21(16), 6292–6297. https://doi.org/10.1523/JNEUROSCI.21-16-06292.2001
   PubMed Web of Science ®Google Scholar
• Shors, T. J., Pickett, J., Wood, G., & Paczynski, M. (1999). Acute stress persistently enhances estrogen levels in the female rat. Stress, 3(2), 163–171. https://doi.org/10.3109/10253899909001120
   PubMedGoogle Scholar
• Simard, J., Ricketts, M.-L., Gingras, S., Soucy, P., Feltus, F. A., & Melner, M. H. (2005). Molecular biology of the 3beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase gene family. Endocrine Reviews, 26(4), 525–582. https://doi.org/10.1210/er.2002-0050
   PubMed Web of Science ®Google Scholar
• Smail, M. A., Smith, B. L., Shukla, R., Alganem, K., Eby, H. M., Bollinger, J. L., Parikh, R. K., Chambers, J. B., Reigle, J. K., Moloney, R. D., Nawreen, N., Wohleb, E. S., Pantazopoulos, H., McCullumsmith, R. E., & Herman, J. P. (2023). Molecular neurobiology of loss: A role for basolateral amygdala extracellular matrix. Molecular Psychiatry. https://doi.org/10.1038/s41380-023-02231-8
   PubMed Web of Science ®Google Scholar
• Sorg, B. A., Berretta, S., Blacktop, J. M., Fawcett, J. W., Kitagawa, H., Kwok, J. C., & Miquel, M. (2016). Casting a wide net: Role of perineuronal nets in neural plasticity. The Journal of Neuroscience, 36(45), 11459–11468. https://doi.org/10.1523/JNEUROSCI.2351-16.2016
   PubMed Web of Science ®Google Scholar
• Starling, E. H. (1905). The Croonian lectures on the chemical correlation of the functions of the body. Lancet, 166(4275), 339–341.
   Google Scholar
• Stell, B. M., Brickley, S. G., Tang, C. Y., Farrant, M., & Mody, I. (2003). Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proceedings of the National Academy of Sciences, 100(24), 14439–14444. https://doi.org/10.1073/pnas.2435457100
   PubMed Web of Science ®Google Scholar
• Stocco, D. M., Wang, X., Jo, Y., & Manna, P. R. (2005). Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: More complicated than we thought. Molecular Endocrinology, 19(11), 2647–2659. https://doi.org/10.1210/me.2004-0532
   PubMedGoogle Scholar
• Stone, D., & Hechter, O. (1955). Studies on ACTH action in perfused bovine adrenals: Aspects of progesterone as an intermediary in corticosteroidogenesis. Archives of Biochemistry and Biophysics, 54(1), 121–128. https://doi.org/10.1016/0003-9861(55)90014-x
   PubMed Web of Science ®Google Scholar
• Sugama, S., Fujita, M., Hashimoto, M., & Conti, B. (2007). Stress induced morphological microglial activation in the rodent brain: Involvement of interleukin-18. Neuroscience, 146(3), 1388–1399. https://doi.org/10.1016/j.neuroscience.2007.02.043
   PubMed Web of Science ®Google Scholar
• Sze, Y., Gill, A. C., & Brunton, P. J. (2018). Sex-dependent changes in neuroactive steroid concentrations in the rat brain following acute swim stress. Journal of Neuroendocrinology, 30(11), e12644. https://doi.org/10.1111/jne.12644
   PubMed Web of Science ®Google Scholar
• Takatsuru, Y., Nabekura, J., Ishikawa, T., Kohsaka, S., & Koibuchi, N. (2015). Early-life stress increases the motility of microglia in adulthood. The Journal of Physiological Sciences: JPS, 65(2), 187–194. https://doi.org/10.1007/s12576-015-0361-z
   PubMed Web of Science ®Google Scholar
• Tata, J. R. (2005). One hundred years of hormones: A new name sparked multidisciplinary research in endocrinology, which shed light on chemical communication in multicellular organisms. EMBO Reports, 6(6), 490–496. https://doi.org/10.1038/sj.embor.7400444
   PubMed Web of Science ®Google Scholar
• Tay, T. L., Béchade, C., D’Andrea, I., St-Pierre, M.-K., Henry, M. S., Roumier, A., & Tremblay, M.-E. (2018). Microglia gone rogue: Impacts on psychiatric disorders across the lifespan. Frontiers in Molecular Neuroscience, 10, 421. https://doi.org/10.3389/fnmol.2017.00421
   PubMed Web of Science ®Google Scholar
• Tertil, M., Skupio, U., Barut, J., Dubovyk, V., Wawrzczak-Bargiela, A., Soltys, Z., Golda, S., Kudla, L., Wiktorowska, L., Szklarczyk, K., Korostynski, M., Przewlocki, R., & Slezak, M. (2018). Glucocorticoid receptor signaling in astrocytes is required for aversive memory formation. Translational Psychiatry, 8(1), 255. https://doi.org/10.1038/s41398-018-0300-x
   PubMedGoogle Scholar
• Tsuda, M. C., Yamaguchi, N., & Ogawa, S. (2011). Early life stress disrupts peripubertal development of aggression in male mice. Neuroreport, 22(6):, 259–263. https://doi.org/10.1097/WNR.0b013e328344495a
   PubMed Web of Science ®Google Scholar
• Tyagi, V., Scordo, M., Yoon, R. S., Liporace, F. A., & Greene, L. W. (2017). Revisiting the role of testosterone: Are we missing something? Reviews in Urology, 19(1), 16–24.
   PubMedGoogle Scholar
• Tynan, R. J., Beynon, S. B., Hinwood, M., Johnson, S. J., Nilsson, M., Woods, J. J., & Walker, F. R. (2013). Chronic stress-induced disruption of the astrocyte network is driven by structural atrophy and not loss of astrocytes. Acta Neuropathologica, 126(1), 75–91. https://doi.org/10.1007/s00401-013-1102-0
   PubMed Web of Science ®Google Scholar
• Tynan, R. J., Naicker, S., Hinwood, M., Nalivaiko, E., Buller, K. M., Pow, D. V., Day, T. A., & Walker, F. R. (2010). Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain, Behavior, and Immunity, 24(7), 1058–1068. https://doi.org/10.1016/j.bbi.2010.02.001
   PubMed Web of Science ®Google Scholar
• Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Matsumoto, Y., Okamoto, M., Aoki, S., & Ishihara, T. (2018). Juvenile stress induces behavioral change and affects perineuronal net formation in juvenile mice. BMC Neuroscience, 19(1), 41. https://doi.org/10.1186/s12868-018-0442-z
   PubMedGoogle Scholar
• Vallée, M., Rivera, J. D., Koob, G. F., Purdy, R. H., & Fitzgerald, R. L. (2000). Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ionization gas chromatography/mass spectrometry. Analytical Biochemistry, 287(1), 153–166. https://doi.org/10.1006/abio.2000.4841
   PubMed Web of Science ®Google Scholar
• Vallée, M., Vitiello, S., Bellocchio, L., Hébert-Chatelain, E., Monlezun, S., Martin-Garcia, E., Kasanetz, F., Baillie, G. L., Panin, F., Cathala, A., Roullot-Lacarrière, V., Fabre, S., Hurst, D. P., Lynch, D. L., Shore, D. M., Deroche-Gamonet, V., Spampinato, U., Revest, J. M., Maldonado, R., … Piazza, P. V. (2014). Pregnenolone can protect the brain from cannabis intoxication. Science, 343(6166), 94–98. https://doi.org/10.1126/science.1243985
   PubMed Web of Science ®Google Scholar
• Van Belle, S. (2017). Cortisol and other glucocorticoids. In Agustín Fuentes (Ed.), The international encyclopedia of primatology (pp. 1-5). Hoboken, NJ: Wiley.
   Google Scholar
• Walf, A. A., & Frye, C. A. (2012). Gestational or acute restraint in adulthood reduces levels of 5α-reduced testosterone metabolites in the hippocampus and produces behavioral inhibition of adult male rats. Frontiers in Cellular Neuroscience, 6, 40. https://doi.org/10.3389/fncel.2012.00040
   PubMed Web of Science ®Google Scholar
• Wang, M. (2011). Neurosteroids and GABA-A receptor function. Frontiers in Endocrinology, 2, 44. https://doi.org/10.3389/fendo.2011.00044
   PubMedGoogle Scholar
• Watanabe, Y., Gould, E., & McEwen, B. S. (1992). Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Research, 588(2), 341–345. https://doi.org/10.1016/0006-8993(92)91597-8
   PubMed Web of Science ®Google Scholar
• Wieland, S., Lan, N. C., Mirasedeghi, S., & Gee, K. W. (1991). Anxiolytic activity of the progesterone metabolite 5 alpha-pregnan-3 alpha-o1-20-one. Brain Research, 565(2), 263–268. https://doi.org/10.1016/0006-8993(91)91658-n
   PubMed Web of Science ®Google Scholar
• Wiktorowska, L., Bilecki, W., Tertil, M., Kudla, L., Szumiec, L., Mackowiak, M., & Przewlocki, R. (2021). Knockdown of the astrocytic glucocorticoid receptor in the central nucleus of the amygdala diminishes conditioned fear expression and anxiety. Behavioural Brain Research, 402, 113095. https://doi.org/10.1016/j.bbr.2020.113095
   PubMed Web of Science ®Google Scholar
• Wingert, J. C., & Sorg, B. A. (2021). Impact of perineuronal nets on electrophysiology of parvalbumin interneurons, principal neurons, and brain oscillations: A review. Frontiers in Synaptic Neuroscience, 13, 673210. https://doi.org/10.3389/fnsyn.2021.673210
   PubMed Web of Science ®Google Scholar
• Wohleb, E. S., Hanke, M. L., Corona, A. W., Powell, N. D., Stiner, L. M., Bailey, M. T., Nelson, R. J., Godbout, J. P., & Sheridan, J. F. (2011). β-adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. The Journal of Neuroscience, 31(17), 6277–6288. https://doi.org/10.1523/JNEUROSCI.0450-11.2011
   PubMed Web of Science ®Google Scholar
• Woolley, C. S., Gould, E., Frankfurt, M., & McEwen, B. S. (1990). Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. The Journal of Neuroscience, 10(12), 4035–4039. https://doi.org/10.1523/JNEUROSCI.10-12-04035.1990
   PubMed Web of Science ®Google Scholar
• Xia et al., 2013: Xia, L., Zhai, M., Wang, L., Miao, D., Zhu, X., & Wang, W. (2013). FGF2 blocks PTSD symptoms via an astrocyte-based mechanism. Behavioural brain research, 256, 472–480.
   Google Scholar
• Xu, B., Zhang, X., He, Y., Liu, C., Li, L., Liu, Q., Huang, Y., Chen, M., Ren, B., Guo, Y., & Chen, Y. (2022). The impacts of early-life adversity on striatal and hippocampal memory functions. Neuroscience, 490, 11–24. https://doi.org/10.1016/j.neuroscience.2022.02.029
   PubMed Web of Science ®Google Scholar
• Yamawaki, Y., Nishida, M., Harada, K., & Akagi, H. (2018). Data on the effect of maternal separation coupled with social isolation in a forced swim test and gene expression of glial fibrillary acid protein in the PFC of rats. Data in Brief, 18, 496–500. https://doi.org/10.1016/j.dib.2018.03.055
   PubMedGoogle Scholar
• Yehuda, R., Bierer, L. M., Andrew, R., Schmeidler, J., & Seckl, J. R. (2009). Enduring effects of severe developmental adversity, including nutritional deprivation, on cortisol metabolism in aging Holocaust survivors. Journal of Psychiatric Research, 43(9), 877–883. https://doi.org/10.1016/j.jpsychires.2008.12.003
   PubMed Web of Science ®Google Scholar
• Yirmiya, R., Rimmerman, N., & Reshef, R. (2015). Depression as a microglial disease. Trends in Neurosciences, 38(10), 637–658. https://doi.org/10.1016/j.tins.2015.08.001
   PubMed Web of Science ®Google Scholar
• Yoshizawa, K., Okumura, A., Nakashima, K., Sato, T., & Higashi, T. (2017). Role of allopregnanolone biosynthesis in acute stress-induced anxiety-like behaviors in mice. Synapse, 71(8), e21978. https://doi.org/10.1002/syn.21978
   Web of Science ®Google Scholar
• Yu, Z., Chen, N., Hu, D., Chen, W., Yuan, Y., Meng, S., Zhang, W., Lu, L., Han, Y., & Shi, J. (2020). Decreased density of perineuronal net in prelimbic cortex is linked to depressive-like behavior in young-aged rats. Frontiers in Molecular Neuroscience, 13, 4. https://doi.org/10.3389/fnmol.2020.00004
   PubMed Web of Science ®Google Scholar
• Zucker, T. P., Higashiura, K., Mathur, R. S., & Halushka, P. V. (1996). Androstenedione increases thromboxane A2 receptors in human erythroleukemia cells. Life Sciences, 58(8), 683–690. https://doi.org/10.1016/s0024-3205(96)80007-5
   PubMed Web of Science ®Google Scholar