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Stress
The International Journal on the Biology of Stress
Volume 26, 2023 - Issue 1
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Research Article

Multiple brain regions are involved in reaction to acute restraint stress in CYLD-knockout mice

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Article: 2228925 | Received 07 Jan 2023, Accepted 19 Jun 2023, Published online: 03 Jul 2023

References

  • Aguayo, F. I., Tejos-Bravo, M., Díaz-Véliz, G., Pacheco, A., García-Rojo, G., Corrales, W., Olave, F. A., Aliaga, E., Ulloa, J. L., Avalos, A. M., Román-Albasini, L., Rojas, P. S., & Fiedler, J. L. (2018). Hippocampal memory recovery after acute stress: A behavioral, morphological and molecular study. Frontiers in Molecular Neuroscience, 11, 1. https://doi.org/10.3389/fnmol.2018.00283
  • Assad, N., Luz, W. L., Santos-Silva, M., Carvalho, T., Moraes, S., Picanço-Diniz, D. L. W., Bahia, C. P., Oliveira Batista, E. d J., da Conceição Passos, A., Oliveira, K. R. H. M., & Herculano, A. M. (2020). Acute restraint stress evokes anxiety-like behavior mediated by telencephalic inactivation and GabAergic dysfunction in zebrafish brains. Scientific Reports, 10(1), 5551. https://doi.org/10.1038/s41598-020-62077-w
  • Azevedo, E. P., Tan, B., Pomeranz, L. E., Ivan, V., Fetcho, R., Schneeberger, M., Doerig, K. R., Liston, C., Friedman, J. M., & Stern, S. A. (2020). A limbic circuit selectively links active escape to food suppression. ELife, 9, e58894. https://doi.org/10.7554/eLife.58894
  • Barbas, H. (2000). Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Research Bulletin, 52(5), 319–12. https://doi.org/10.1016/s0361-9230(99)00245-2
  • Bi, L.-L., Wang, J., Luo, Z.-Y., Chen, S.-P., Geng, F., Chen, Y-h., Li, S.-J., Yuan, C-h., Lin, S., & Gao, T.-M. (2013). Enhanced excitability in the infralimbic cortex produces anxiety-like behaviors. Neuropharmacology, 72, 148–156. https://doi.org/10.1016/j.neuropharm.2013.04.048
  • Bignell, G. R., Warren, W., Seal, S., Takahashi, M., Rapley, E., Barfoot, R., Green, H., Brown, C., Biggs, P. J., Lakhani, S. R., Jones, C., Hansen, J., Blair, E., Hofmann, B., Siebert, R., Turner, G., Evans, D. G., Schrander-Stumpel, C., Beemer, F. A., … Rasmussen, S. (2000). Identification of the familial cylindromatosis tumour-suppressor gene. Nature Genetics, 25(2), 160–165. https://doi.org/10.1038/76006
  • Bullitt, E. (1990). Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. The Journal of Comparative Neurology, 296(4), 517–530. https://doi.org/10.1002/cne.902960402
  • Burton, A. C., Nakamura, K., & Roesch, M. R. (2015). From ventral-medial to dorsal-lateral striatum: neural correlates of reward-guided decision-making. Neurobiology of Learning and Memory, 117, 51–59. https://doi.org/10.1016/j.nlm.2014.05.003
  • Calhoon, G. G., & Tye, K. M. (2015). Resolving the neural circuits of anxiety. Nature Neuroscience, 18(10), 1394–1404. https://doi.org/10.1038/nn.4101
  • Chen, S.-Y., Liu, K.-F., Tan, S.-Y., Chen, X.-S., Li, H.-D., Li, J.-J., Zhou, J.-W., Yang, L., & Long, C. (2023). Deubiquitinase CYLD regulates excitatory synaptic transmission and short-term plasticity in the hippocampus. Brain Research, 1806, 148313. https://doi.org/10.1016/j.brainres.2023.148313
  • Colombo, E., Horta, G., Roesler, M. K., et al. (2021). The K63 deubiquitinase CYLD modulates autism-like behaviors and hippocampal plasticity by regulating autophagy and mTOR signaling. Proceedings of the National Academy of Sciences of the United States of America, 118(47), e2110755118. https://doi.org/10.1073/pnas.2110755118
  • Craske, M. G., & Stein, M. B. (2016). Anxiety. Lancet, 388(10063), 3048–3059. https://doi.org/10.1016/S0140-6736(16)30381-6
  • Dobson-Stone, C., Hallupp, M., Shahheydari, H., Ragagnin, A. M. G., Chatterton, Z., Carew-Jones, F., Shepherd, C. E., Stefen, H., Paric, E., Fath, T., Thompson, E. M., Blumbergs, P., Short, C. L., Field, C. D., Panegyres, P. K., Hecker, J., Nicholson, G., Shaw, A. D., Fullerton, J. M., … Kwok, J. B. (2020). CYLD is a causative gene for frontotemporal dementia - amyotrophic lateral sclerosis. Brain, 143(3), 783–799. https://doi.org/10.1093/brain/awaa039
  • Dosemeci, A., Thein, S., Yang, Y., Reese, T. S., & Tao-Cheng, J.-H. (2013). CYLD, a deubiquitinase specific for lysine63-linked polyubiquitins, accumulates at the postsynaptic density in an activity-dependent manner. Biochemical and Biophysical Research Communications, 430(1), 245–249. https://doi.org/10.1016/j.bbrc.2012.10.131
  • Duncan, L. E., Pollastri, A. R., & Smoller, J. W. (2014). Mind the gap: why many geneticists and psychological scientists have discrepant views about gene-environment interaction (G × E) research. The American Psychologist, 69(3), 249–268. https://doi.org/10.1037/a0036320
  • Friedman, A., Homma, D., Bloem, B., Gibb, L. G., Amemori, K.-I., Hu, D., Delcasso, S., Truong, T. F., Yang, J., Hood, A. S., Mikofalvy, K. A., Beck, D. W., Nguyen, N., Nelson, E. D., Toro Arana, S. E., Vorder Bruegge, R. H., Goosens, K. A., & Graybiel, A. M. (2017). Chronic stress alters striosome-circuit dynamics, leading to aberrant decision-making. Cell, 171(5), 1191–1205 e1128. https://doi.org/10.1016/j.cell.2017.10.017
  • Godar, S. C., Bortolato, M., Richards, S. E., et al. (2015). Monoamine oxidase A is required for rapid dendritic remodeling in response to stress. The International Journal of Neuropsychopharmacology, 18(9), pyv035. https://doi.org/10.1093/ijnp/pyv035
  • Gomes, F. V., Zhu, X., & Grace, A. A. (2019). Stress during critical periods of development and risk for schizophrenia. Schizophrenia Research, 213, 107–113. https://doi.org/10.1016/j.schres.2019.01.030
  • Haller, J., & Alicki, M. (2012). Current animal models of anxiety, anxiety disorders, and anxiolytic drugs. Current Opinion in Psychiatry, 25(1), 59–64. https://doi.org/10.1097/YCO.0b013e32834de34f
  • Haller, J., Aliczki, M., & Gyimesine Pelczer, K. (2013). Classical and novel approaches to the preclinical testing of anxiolytics: A critical evaluation. Neuroscience and Biobehavioral Reviews, 37(10 Pt 1), 2318–2330. https://doi.org/10.1016/j.neubiorev.2012.09.001
  • Han, Y.-Y., Jin, K., Pan, Q.-S., Li, B., Wu, Z.-Q., Gan, L., Yang, L., & Long, C. (2020). Microglial activation in the dorsal striatum participates in anxiety-like behavior in Cyld knockout mice. Brain, Behavior, and Immunity, 89, 326–338. https://doi.org/10.1016/j.bbi.2020.07.011
  • Han, A., Yeo, H., Park, M.-J., Kim, S. H., Choi, H. J., Hong, C.-W., & Kwon, M.-S. (2015). IL-4/10 prevents stress vulnerability following imipramine discontinuation. Journal of Neuroinflammation, 12, 197. https://doi.org/10.1186/s12974-015-0416-3
  • Hikida, T., Kimura, K., Wada, N., Funabiki, K., & Nakanishi, S. (2010). Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron, 66(6), 896–907. https://doi.org/10.1016/j.neuron.2010.05.011
  • Jimenez, J. C., Su, K., Goldberg, A. R., Luna, V. M., Biane, J. S., Ordek, G., Zhou, P., Ong, S. K., Wright, M. A., Zweifel, L., Paninski, L., Hen, R., & Kheirbek, M. A. (2018). Anxiety cells in a hippocampal-hypothalamic circuit. Neuron, 97(3), 670–683 e676. https://doi.org/10.1016/j.neuron.2018.01.016
  • Jin, Y., Kanno, T., & Nishizaki, T. (2015). Acute restraint stress impairs induction of long-term potentiation by activating GSK-3beta. Neurochemical Research, 40(1), 36–40. https://doi.org/10.1007/s11064-014-1462-4
  • Jin, C., Kim, S., Kang, H., Yun, K. N., Lee, Y., Zhang, Y., Kim, Y., Kim, J. Y., & Han, K. (2019). Shank3 regulates striatal synaptic abundance of Cyld, a deubiquitinase specific for Lys63-linked polyubiquitin chains. Journal of Neurochemistry, 150(6), 776–786. https://doi.org/10.1111/jnc.14796
  • Joffe, M. E., Maksymetz, J., Luschinger, J. R., Dogra, S., Ferranti, A. S., Luessen, D. J., Gallinger, I. M., Xiang, Z., Branthwaite, H., Melugin, P. R., Williford, K. M., Centanni, S. W., Shields, B. C., Lindsley, C. W., Calipari, E. S., Siciliano, C. A., Niswender, C. M., Tadross, M. R., Winder, D. G., & Conn, P. J. (2022). Acute restraint stress redirects prefrontal cortex circuit function through mGlu5 receptor plasticity on somatostatin-expressing interneurons. Neuron, 110(6), 1068–1083 e1065. https://doi.org/10.1016/j.neuron.2021.12.027
  • Kinlein, S. A., Wilson, C. D., & Karatsoreos, I. N. (2015). Dysregulated hypothalamic–pituitary–adrenal axis function contributes to altered endocrine and neurobehavioral responses to acute stress. Frontiers in Psychiatry, 6, 31. https://doi.org/10.3389/fpsyt.2015.00031
  • Kinlein, S. A., Wallace, N. K., Savenkova, M. I., & Karatsoreos, I. N. (2022). Chronic hypothalamic-pituitary-adrenal axis disruption alters glutamate homeostasis and neural responses to stress in male C57Bl6/N mice. Neurobiology of Stress, 19, 100466.https://doi.org/10.1016/j.ynstr.2022.100466
  • Kovács, L. Á., Schiessl, J. A., Nafz, A. E., Csernus, V., & Gaszner, B. (2018). Both basal and acute restraint stress-induced c-Fos expression is influenced by age in the extended amygdala and brainstem stress centers in male rats. Frontiers in Aging Neuroscience, 10, 248. https://doi.org/10.3389/fnagi.2018.00248
  • Kovalenko, A., Chable-Bessia, C., Cantarella, G., Israël, A., Wallach, D., & Courtois, G. (2003). The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature, 424(6950), 801–805. https://doi.org/10.1038/nature01802
  • Krabbe, S., Gründemann, J., & Lüthi, A. (2018). Amygdala inhibitory circuits regulate associative fear conditioning. Biological Psychiatry, 83(10), 800–809. https://doi.org/10.1016/j.biopsych.2017.10.006
  • LeBlanc, K. H., London, T. D., Szczot, I., Bocarsly, M. E., Friend, D. M., Nguyen, K. P., Mengesha, M. M., Rubinstein, M., Alvarez, V. A., & Kravitz, A. V. (2020). Striatopallidal neurons control avoidance behavior in exploratory tasks. Molecular Psychiatry, 25(2), 491–505. https://doi.org/10.1038/s41380-018-0051-3
  • Li, H.-D., Li, D.-N., Yang, L., & Long, C. (2021). Deficiency of the CYLD impairs fear memory of mice and disrupts neuronal activity and synaptic transmission in the basolateral amygdala. Frontiers in Cellular Neuroscience, 15, 740165. https://doi.org/10.3389/fncel.2021.740165
  • Li, J., Sekine-Aizawa, Y., Ebrahimi, S., Tanaka, S., & Okabe, S. (2019). Tumor suppressor protein CYLD regulates morphogenesis of dendrites and spines. The European Journal of Neuroscience, 50(4), 2722–2739. https://doi.org/10.1111/ejn.14421
  • Liu, L., Liu, H., Hou, Y., Shen, J., Qu, X., & Liu, S. (2019). Temporal effect of electroacupuncture on anxiety-like behaviors and c-Fos expression in the anterior cingulate cortex in a rat model of post-traumatic stress disorder. Neuroscience Letters, 711, 134432. https://doi.org/10.1016/j.neulet.2019.134432
  • MacDowell, K. S., Caso, J. R., Martin-Hernandez, D., et al. (2014). Paliperidone prevents brain toll-like receptor 4 pathway activation and neuroinflammation in rat models of acute and chronic restraint stress. The International Journal of Neuropsychopharmacology. 18(3), pyu070.
  • Ma, Y., Matsuwaki, T., Yamanouchi, K., & Nishihara, M. (2014). Differential roles of cyclooxygenase-2-related signaling in regulating hypothalamic neuronal activity under various acute stresses. The Journal of Veterinary Medical Science, 76(2), 219–227. https://doi.org/10.1292/jvms.13-0234
  • Ma, Q., Ruan, H., Peng, L., et al. (2017). Proteasome-independent polyubiquitin linkage regulates synapse scaffolding, efficacy, and plasticity. Proceedings of the National Academy of Sciences of the United States of America, 114, E8760–E8769.
  • Mazarei, G., Neal, S. J., Becanovic, K., Luthi-Carter, R., Simpson, E. M., & Leavitt, B. R. (2010). Expression analysis of novel striatal-enriched genes in Huntington disease. Human Molecular Genetics, 19(4), 609–622. https://doi.org/10.1093/hmg/ddp527
  • Mutti, V., Bono, F., Tomasoni, Z., Bontempi, L., Guglielmi, A., Bolognin, S., Schwamborn, J. C., Missale, C., & Fiorentini, C. (2022). Structural plasticity of dopaminergic neurons requires the activation of the D3R-nAChR heteromer and the PI3K-ERK1/2/Akt-induced expression of c-Fos and p70S6K signaling pathway. Molecular Neurobiology, 59(4), 2129–2149. https://doi.org/10.1007/s12035-022-02748-z
  • Novaes, L. S., Dos Santos, N. B., Perfetto, J. G., Goosens, K. A., & Munhoz, C. D. (2018). Environmental enrichment prevents acute restraint stress-induced anxiety-related behavior but not changes in basolateral amygdala spine density. Psychoneuroendocrinology, 98, 6–10. https://doi.org/10.1016/j.psyneuen.2018.07.031
  • Pati, S., Sood, A., Mukhopadhyay, S., & Vaidya, V. A. (2018). Acute pharmacogenetic activation of medial prefrontal cortex excitatory neurons regulates anxiety-like behaviour. Journal of Biosciences, 43(1), 85–95. https://doi.org/10.1007/s12038-018-9732-y
  • Paxinos, G., Franklin, K. (2001). The mouse brain in stereotoxic coordinates. Academic Press.
  • Qiao, Y., Wang, X., Ma, L., Li, S., & Liang, J. (2017). Functional inactivation of dorsal medial striatum alters behavioral flexibility and recognition process in mice. Physiology & Behavior, 179, 467–477. https://doi.org/10.1016/j.physbeh.2017.07.026
  • Reiley, W. W., Jin, W., Lee, A. J., Wright, A., Wu, X., Tewalt, E. F., Leonard, T. O., Norbury, C. C., Fitzpatrick, L., Zhang, M., & Sun, S.-C. (2007). Deubiquitinating enzyme CYLD negatively regulates the ubiquitin-dependent kinase Tak1 and prevents abnormal T cell responses. The Journal of Experimental Medicine, 204(6), 1475–1485. https://doi.org/10.1084/jem.20062694
  • Saitoh, A., Ohashi, M., Suzuki, S., Tsukagoshi, M., Sugiyama, A., Yamada, M., Oka, J.-I., Inagaki, M., & Yamada, M. (2014). Activation of the prelimbic medial prefrontal cortex induces anxiety-like behaviors via N-Methyl-D-aspartate receptor-mediated glutamatergic neurotransmission in mice. Journal of Neuroscience Research, 92(8), 1044–1053. https://doi.org/10.1002/jnr.23391
  • Smith, J. P., Prince, M. A., Achua, J. K., Robertson, J. M., Anderson, R. T., Ronan, P. J., & Summers, C. H. (2016). Intensity of anxiety is modified via complex integrative stress circuitries. Psychoneuroendocrinology, 63, 351–361. https://doi.org/10.1016/j.psyneuen.2015.10.016
  • Stein, D. J., Scott, K. M., de Jonge, P., & Kessler, R. C. (2017). Epidemiology of anxiety disorders: from surveys to nosology and back. Dialogues in Clinical Neuroscience, 19(2), 127–136. https://doi.org/10.31887/DCNS.2017.19.2/dstein
  • Sun, S. C. (2010). CYLD: a tumor suppressor deubiquitinase regulating NF-kappaB activation and diverse biological processes. Cell Death and Differentiation, 17(1), 25–34. https://doi.org/10.1038/cdd.2009.43
  • Tábuas-Pereira, M., Santana, I., Kun-Rodrigues, C., Bras, J., & Guerreiro, R. (2020). CYLD variants in frontotemporal dementia associated with severe memory impairment in a Portuguese cohort. Brain, 143(8), e67. https://doi.org/10.1093/brain/awaa183
  • Tan, S.-Y., Jiang, J.-X., Huang, H.-X., Mo, X.-P., Feng, J.-R., Chen, Y., Yang, L., & Long, C. (2023). Neural mechanism underlies CYLD modulation of morphology and synaptic function of medium spiny neurons in dorsolateral striatum. Frontiers in Molecular Neuroscience, 16, 1107355. https://doi.org/10.3389/fnmol.2023.1107355
  • Thein, S., Tao-Cheng, J.-H., Li, Y., Bayer, K. U., Reese, T. S., & Dosemeci, A. (2014). CaMKII mediates recruitment and activation of the deubiquitinase CYLD at the postsynaptic density. PLOS One, 9(3), e91312. https://doi.org/10.1371/journal.pone.0091312
  • Tovote, P., Fadok, J. P., & Luthi, A. (2015). Neuronal circuits for fear and anxiety. Nature Reviews Neuroscience, 16(6), 317–331. https://doi.org/10.1038/nrn3945
  • Trompouki, E., Hatzivassiliou, E., Tsichritzis, T., Farmer, H., Ashworth, A., & Mosialos, G. (2003). CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature, 424(6950), 793–796. https://doi.org/10.1038/nature01803
  • Tu, B.-X., Wang, L.-F., Zhong, X.-L., Hu, Z.-L., Cao, W.-Y., Cui, Y.-H., Li, S.-J., Zou, G.-J., Liu, Y., Zhou, S.-F., Zhang, W.-J., Su, J.-Z., Yan, X.-X., Li, F., & Li, C.-Q. (2019). Acute restraint stress alters food-foraging behavior in rats: Taking the easier Way while suffered. Brain Research Bulletin, 149, 184–193. https://doi.org/10.1016/j.brainresbull.2019.04.021
  • Walf, A. A., & Frye, C. A. (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nature Protocols, 2(2), 322–328. https://doi.org/10.1038/nprot.2007.44
  • Wang, Z. (2021). Regulation of cell cycle progression by growth factor-induced cell signaling. Cells, 10(12), 3327. https://doi.org/10.3390/cells10123327
  • Xiao, Q., Xu, X., & Tu, J. (2020). Chronic optogenetic manipulation of basolateral amygdala astrocytes rescues stress-induced anxiety. Biochemical and Biophysical Research Communications, 533(4), 657–664. https://doi.org/10.1016/j.bbrc.2020.09.106
  • Xu, C., Yang, L., Yuan, Y., Du, F., Wang, S., Wang, X., Zhu, L., Zhang, B., & Weaver, D. (2016). Up-regulation of CYLD enhances Listeria monocytogenes induced apoptosis in THP-1 cells. Microbial Pathogenesis, 90, 50–54. https://doi.org/10.1016/j.micpath.2015.10.007
  • Yaeger, J. D., Krupp, K. T., Gale, J. J., & Summers, C. H. (2020). Counterbalanced microcircuits for Orx1 and Orx2 regulation of stress reactivity. Medicine in Drug Discovery, 8, 100059. https://doi.org/10.1016/j.medidd.2020.100059
  • Yaeger, J. D. W., Krupp, K. T., Summers, T. R., & Summers, C. H. (2022). Contextual generalization of social stress learning is modulated by orexin receptors in basolateral amygdala. Neuropharmacology, 215, 109168. https://doi.org/10.1016/j.neuropharm.2022.109168
  • Zajicek, A. S., Ruan, H., Dai, H., Skolfield, M. C., Phillips, H. L., Burnette, W. J., Javidfar, B., Sun, S.-C., Akbarian, S., & Yao, W.-D. (2022). Cylindromatosis drives synapse pruning and weakening by promoting macroautophagy through Akt-mTOR signaling. Molecular Psychiatry, 27(5), 2414–2424. https://doi.org/10.1038/s41380-022-01571-1
  • Zajicek, A., & Yao, W. D. (2021). Remodeling without destruction: non-proteolytic ubiquitin chains in neural function and brain disorders. Molecular Psychiatry, 26(1), 247–264. https://doi.org/10.1038/s41380-020-0849-7
  • Zhang, J., Chen, M., Li, B., Lv, B., Jin, K., Zheng, S., Yang, L., & Long, C. (2016). Altered striatal rhythmic activity in cylindromatosis knock-out mice due to enhanced GABAergic inhibition. Neuropharmacology, 110(Pt A), 260–267. https://doi.org/10.1016/j.neuropharm.2016.06.021
  • Zhang, J.-Y., Liu, T.-H., He, Y., Pan, H.-Q., Zhang, W.-H., Yin, X.-P., Tian, X.-L., Li, B.-M., Wang, X.-D., Holmes, A., Yuan, T.-F., & Pan, B.-X. (2019). Chronic stress remodels synapses in an amygdala circuit-specific manner. Biological Psychiatry, 85(3), 189–201. https://doi.org/10.1016/j.biopsych.2018.06.019
  • Zhou, H.-Y., He, J.-G., Hu, Z.-L., Xue, S.-G., Xu, J.-F., Cui, Q.-Q., Gao, S.-Q., Zhou, B., Wu, P.-F., Long, L.-H., Wang, F., & Chen, J.-G. (2019). A-kinase anchoring protein 150 and protein kinase A complex in the basolateral amygdala contributes to depressive-like behaviors induced by chronic restraint stress. Biological Psychiatry, 86(2), 131–142. https://doi.org/10.1016/j.biopsych.2019.03.967