Early growth response 2 in the mPFC regulates mouse social and cooperative behaviors.


Journal

Lab animal
ISSN: 1548-4475
Titre abrégé: Lab Anim (NY)
Pays: United States
ID NLM: 0417737

Informations de publication

Date de publication:
02 2023
Historique:
received: 28 09 2021
accepted: 14 11 2022
pubmed: 17 1 2023
medline: 7 2 2023
entrez: 16 1 2023
Statut: ppublish

Résumé

Adolescent social neglect impairs social performance, but the underlying molecular mechanisms remain unclear. Here we report that isolation rearing of juvenile mice caused cooperation defects that were rescued by immediate social reintroduction. We also identified the transcription factor early growth response 2 (Egr2) in the medial prefrontal cortex (mPFC) as a major target of social isolation and resocialization. Isolation rearing increased corticosteroid production, which reduced the expression of Egr2 in the mPFC, including in oligodendrocytes. Overexpressing Egr2 ubiquitously in the mPFC, but not specifically in neurons nor in oligodendroglia, protected mice from the isolation rearing-induced cooperation defect. In addition to synapse integrity, Egr2 also regulated the development of oligodendroglia, specifically the transition from undifferentiated oligodendrocyte precursor cells to premyelinating oligodendrocytes. In conclusion, this study reveals the importance of mPFC Egr2 in the cooperative behavior that is modulated by social experience, and its unexpected role in oligodendrocyte development.

Identifiants

pubmed: 36646797
doi: 10.1038/s41684-022-01090-0
pii: 10.1038/s41684-022-01090-0
doi:

Substances chimiques

Egr2 protein, mouse 0
Early Growth Response Protein 2 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

37-50

Subventions

Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 81871117
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 81801378

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.

Références

Ioannou, C. C., Guttal, V. & Couzin, I. D. Predatory fish select for coordinated collective motion in virtual prey. Science 337, 1212–1215 (2012).
doi: 10.1126/science.1218919
Kanter, J. W., Manos, R. C., Busch, A. M. & Rusch, L. C. Making behavioral activation more behavioral. Behav. Modif. 32, 780–803 (2008).
doi: 10.1177/0145445508317265
Segrin, C. Social skills deficits associated with depression. Clin. Psychol. Rev. 20, 379–403 (2000).
doi: 10.1016/S0272-7358(98)00104-4
Lai, M. C., Lombardo, M. V. & Baron-Cohen, S. Autism. Lancet 383, 896–910 (2014).
doi: 10.1016/S0140-6736(13)61539-1
Lahera, G. et al. Hostile attributions in bipolar disorder and schizophrenia contribute to poor social functioning. Acta Psychiatr. Scand. 131, 472–482 (2015).
doi: 10.1111/acps.12399
Thaler, N. S., Allen, D. N., Sutton, G. P., Vertinski, M. & Ringdahl, E. N. Differential impairment of social cognition factors in bipolar disorder with and without psychotic features and schizophrenia. J. Psychiatr. Res. 47, 2004–2010 (2013).
doi: 10.1016/j.jpsychires.2013.09.010
Strikwerda-Brown, C. et al. The interplay of emotional and social conceptual processes during moral reasoning in frontotemporal dementia. Brain 144, 938–952 (2021).
doi: 10.1093/brain/awaa435
Ko, J. Neuroanatomical substrates of rodent social behavior: the medial prefrontal cortex and its projection patterns. Front. Neural Circuits https://doi.org/10.3389/fncir.2017.00041 (2017).
Chugani, H. T. et al. Local brain functional activity following early deprivation: a study of postinstitutionalized romanian orphans. NeuroImage 14, 1290–1301 (2001).
doi: 10.1006/nimg.2001.0917
Eluvathingal, T. J. et al. Abnormal brain connectivity in children after early severe socioemotional deprivation: a diffusion tensor imaging study. Pediatrics 117, 2093–2100 (2006).
doi: 10.1542/peds.2005-1727
Xin, W. & Chan, J. R. Myelin plasticity: sculpting circuits in learning and memory. Nat. Rev. Neurosci. 21, 682–694 (2020).
doi: 10.1038/s41583-020-00379-8
Etxeberria, A. et al. Dynamic modulation of myelination in response to visual stimuli alters optic nerve conduction velocity. J. Neurosci. 36, 6937–6948 (2016).
doi: 10.1523/JNEUROSCI.0908-16.2016
Mount, C. W. & Monje, M. Wrapped to adapt: experience-dependent myelination. Neuron 95, 743–756 (2017).
doi: 10.1016/j.neuron.2017.07.009
Makinodan, M., Rosen, K. M., Ito, S. & Corfas, G. A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337, 1357–1360 (2012).
doi: 10.1126/science.1220845
Liu, J. et al. Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat. Neurosci. 15, 1621–1623 (2012).
doi: 10.1038/nn.3263
Liu, J. et al. Clemastine enhances myelination in the prefrontal cortex and rescues behavioral changes in socially isolated mice. J. Neurosci. 36, 957–962 (2016).
doi: 10.1523/JNEUROSCI.3608-15.2016
Noë, R. Cooperation experiments: coordination through communication versus acting apart together. Anim. Behav. 71, 1–18 (2006).
doi: 10.1016/j.anbehav.2005.03.037
Sokolowski, M. B. Social interactions in ‘simple’ model systems. Neuron 65, 780–794 (2010).
doi: 10.1016/j.neuron.2010.03.007
Martinez-Moreno, M. et al. Regulation of peripheral myelination through transcriptional buffering of Egr2 by an antisense long non-coding RNA. Cell Rep. 20, 1950–1963 (2017).
doi: 10.1016/j.celrep.2017.07.068
Feng, W., et al. A water-reward task assay for evaluating mouse mutualistic cooperative behavior. Preprint at bioRxiv https://doi.org/10.1101/2021.02.06.430037 (2021).
Skelly, M. J., Chappell, A. E., Carter, E. & Weiner, J. L. Adolescent social isolation increases anxiety-like behavior and ethanol intake and impairs fear extinction in adulthood: possible role of disrupted noradrenergic signaling. Neuropharmacology 97, 149–159 (2015).
doi: 10.1016/j.neuropharm.2015.05.025
Quan, M. N., Tian, Y. T., Xu, K. H., Zhang, T. & Yang, Z. Post weaning social isolation influences spatial cognition, prefrontal cortical synaptic plasticity and hippocampal potassium ion channels in Wistar rats. Neuroscience 169, 214–222 (2010).
doi: 10.1016/j.neuroscience.2010.04.048
Cao, M. et al. Early enriched physical environment reverses impairments of the hippocampus, but not medial prefrontal cortex, of socially-isolated mice. Brain Behav. Immun. 64, 232–243 (2017).
doi: 10.1016/j.bbi.2017.04.009
Karasek, M., Swiltoslawski, J. & Zieliniska, A. Ultrastructure of the central nervous system: the basics. Folia Neuropathol. 42, 1–9 (2004).
De, S. & Turman, J. E. Jr. Krox-20 gene expression: influencing hindbrain–craniofacial developmental interactions. Arch. Histol. Cytol. 68, 227–234 (2005).
doi: 10.1679/aohc.68.227
Svaren, J. & Meijer, D. The molecular machinery of myelin gene transcription in Schwann cells. Glia 56, 1541–1551 (2008).
doi: 10.1002/glia.20767
Zeisel, A. et al. Molecular architecture of the mouse nervous system. Cell 174, 999–1014.e1022 (2018).
doi: 10.1016/j.cell.2018.06.021
Floriddia, E. M. et al. Distinct oligodendrocyte populations have spatial preference and different responses to spinal cord injury. Nat. Commun. 11, 5860 (2020).
doi: 10.1038/s41467-020-19453-x
Marques, S. et al. Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science 352, 1326–1329 (2016).
doi: 10.1126/science.aaf6463
Mittelstadt, P. R. & Ashwell, J. D. Inhibition of AP-1 by the glucocorticoid-inducible protein GILZ *. J. Biol. Chem. 276, 29603–29610 (2001).
doi: 10.1074/jbc.M101522200
Snyder, J. S., Soumier, A., Brewer, M., Pickel, J. & Cameron, H. A. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476, 458–461 (2011).
doi: 10.1038/nature10287
Choi, G. E. et al. BNIP3L/NIX-mediated mitophagy protects against glucocorticoid-induced synapse defects. Nat. Commun. 12, 487 (2021).
doi: 10.1038/s41467-020-20679-y
Wang, Z., Frederick, J. & Garabedian, M. J. Deciphering the phosphorylation ‘code’ of the glucocorticoid receptor in vivo. J. Biol. Chem. 277, 26573–26580 (2002).
doi: 10.1074/jbc.M110530200
Marin-Husstege, M. et al. Multiple roles of Id4 in developmental myelination: predicted outcomes and unexpected findings. Glia 54, 285–296 (2006).
doi: 10.1002/glia.20385
Qi, Y. C. et al. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 128, 2723–2733 (2001).
doi: 10.1242/dev.128.14.2723
Bujalka, H., et al. MYRF is a membrane-associated transcription factor that autoproteolytically cleaves to directly activate myelin genes. PLoS Biol. https://doi.org/10.1371/journal.pbio.1001625 (2013).
Shin, J. & Ko, J. Protocol for quantitative assessment of social cooperation in mice. STAR Protoc. 2, 100305 (2021).
doi: 10.1016/j.xpro.2021.100305
Conde-Moro, A. R., Rocha-Almeida, F., Sánchez-Campusano, R., Delgado-García, J. M. & Gruart, A. The activity of the prelimbic cortex in rats is enhanced during the cooperative acquisition of an instrumental learning task. Prog. Neurobiol. 183, 101692 (2019).
doi: 10.1016/j.pneurobio.2019.101692
Zhang, Y. et al. miR-124 regulates early isolation-induced social abnormalities via inhibiting myelinogenesis in the medial prefrontal cortex. Cell. Mol. Life Sci. 79, 507 (2022).
doi: 10.1007/s00018-022-04533-6
Wang, Z. et al. Miconazole promotes cooperative ability of a mouse model of Alzheimer’s disease. Int. J. Neuropsychopharmacol. https://doi.org/10.1093/ijnp/pyac061 (2022).
Sock, E. & Wegner, M. Transcriptional control of myelination and remyelination. Glia 67, 2153–2165 (2019).
doi: 10.1002/glia.23636
Nagarajan, R. et al. EGR2 mutations in inherited neuropathies dominant-negatively inhibit myelin gene expression. Neuron 30, 355–368 (2001).
doi: 10.1016/S0896-6273(01)00282-3
Parkinson, D. B. et al. Krox-20 inhibits Jun-NH2-terminal kinase/c-Jun to control Schwann cell proliferation and death. J. Cell Biol. 164, 385–394 (2004).
doi: 10.1083/jcb.200307132
Zawadzka, M. et al. CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6, 578–590 (2010).
doi: 10.1016/j.stem.2010.04.002
Xie, X.-M. et al. Co-transplantation of MRF-overexpressing oligodendrocyte precursor cells and Schwann cells promotes recovery in rat after spinal cord injury. Neurobiol. Dis. 94, 196–204 (2016).
doi: 10.1016/j.nbd.2016.06.016
Dubois, J. et al. The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276, 48–71 (2014).
doi: 10.1016/j.neuroscience.2013.12.044
Lee, S. L., Tourtellotte, L. C., Wesselschmidt, R. L. & Milbrandt, J. Growth and differentiation proceeds normally in cells deficient in the immediate early gene NGFI-A. J. Biol. Chem. 270, 9971–9977 (1995).
doi: 10.1074/jbc.270.17.9971
Williams, J. et al. Krox20 may play a key role in the stabilization of long-term potentiation. Brain Res. Mol. Brain Res. 28, 87–93 (1995).
doi: 10.1016/0169-328X(94)00187-J
Raffety, B. D., Smith, R. E. & Ptacek, J. T. Facilitating and debilitating trait anxiety, situational anxiety, and coping with an anticipated stressor: a process analysis. J. Pers. Soc. Psychol. 72, 892–906 (1997).
doi: 10.1037/0022-3514.72.4.892
Schneier, F. R. Social anxiety disorder. Brit. Med. J. 327, 515–516 (2003).
doi: 10.1136/bmj.327.7414.515
Stein, M. B. & Kean, Y. M. Disability and quality of life in social phobia: epidemiologic findings. Am. J. Psychiatry 157, 1606–1613 (2000).
doi: 10.1176/appi.ajp.157.10.1606
Doremus-Fitzwater, T. L., Varlinskaya, E. I. & Spear, L. P. Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol. Behav. 97, 484–494 (2009).
doi: 10.1016/j.physbeh.2009.03.025
Leclerc, N. et al. Opposing effects of glucocorticoids and Wnt signaling on Krox20 and mineral deposition in osteoblast cultures. J. Cell. Biochem. 103, 1938–1951 (2008).
doi: 10.1002/jcb.21587
Zalewska, K., et al. Corticosterone administration alters white matter tract structure and reduces gliosis in the sub-acute phase of experimental stroke. Int. J. Mol. Sci. https://doi.org/10.3390/ijms22136693 (2021).
Alonso, G. Prolonged corticosterone treatment of adult rats inhibits the proliferation of oligodendrocyte progenitors present throughout white and gray matter regions of the brain. Glia 31, 219–231 (2000).
doi: 10.1002/1098-1136(200009)31:3<219::AID-GLIA30>3.0.CO;2-R
Bhat, R. V., Worley, P. F., Cole, A. J. & Baraban, J. M. Activation of the zinc finger encoding gene krox-20 in adult rat brain: comparison with zif268. Brain Res. Mol. Brain Res. 13, 263–266 (1992).
doi: 10.1016/0169-328X(92)90034-9
Beckmann, A. M., Davidson, M. S., Goodenough, S. & Wilce, P. A. Differential expression of Egr-1-like DNA-binding activities in the naive rat brain and after excitatory stimulation. J. Neurochem. 69, 2227–2237 (1997).
doi: 10.1046/j.1471-4159.1997.69062227.x
Zelikowsky, M. et al. The neuropeptide Tac2 controls a distributed brain state induced by chronic social isolation stress. Cell 173, 1265–1279 e1219 (2018).
doi: 10.1016/j.cell.2018.03.037
Felix-Ortiz, A. C. & Tye, K. M. Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J. Neurosci. 34, 586–595 (2014).
doi: 10.1523/JNEUROSCI.4257-13.2014
Leung, C., Kim, J. C. & Jia, Z. Three-chamber social approach task with optogenetic stimulation (mice). Bio Protoc. 8, e3120 (2018).
doi: 10.21769/BioProtoc.3120
Wang, L. et al. Deep cervical lymph node ligation aggravates AD-like pathology of APP/PS1 mice. Brain Pathol. 29, 176–192 (2019).
doi: 10.1111/bpa.12656
Gao, J. et al. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466, 1105–1109 (2010).
doi: 10.1038/nature09271
Lei, Y. et al. SIRT1 in forebrain excitatory neurons produces sexually dimorphic effects on depression-related behaviors and modulates neuronal excitability and synaptic transmission in the medial prefrontal cortex. Mol. Psychiatry 25, 1094–1111 (2020).
doi: 10.1038/s41380-019-0352-1
Flores-Obando, R. E., Freidin, M. M. & Abrams, C. K. Rapid and specific immunomagnetic isolation of mouse primary oligodendrocytes. J. Vis. Exp. https://doi.org/10.3791/57543 (2018).
Kinn Rod, A. M., Harkestad, N., Jellestad, F. K. & Murison, R. Comparison of commercial ELISA assays for quantification of corticosterone in serum. Sci Rep. 7, 6748 (2017).
doi: 10.1038/s41598-017-06006-4
Xu, Z. et al. Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Aβ accumulation and memory deficits. Mol. Neurodegener. 10, 58 (2015).
doi: 10.1186/s13024-015-0056-1
Castejon, O.J. Low resolution scanning electron microscopy of cerebellar neurons and neuroglial cells of the granular layer. Scan Electron Microsc. 1391–1400 (1984).
Castejon, O. J., Castejon, H. V. & Castellano, A. Oligodendroglial cell damage and demyelination in infant hydrocephalus. An electron microscopic study. J. Submicrosc. Cytol. Pathol. 33, 33–40 (2001).
Garcia-Cabezas, M.A., John, Y.J., Barbas, H. & Zikopoulos, B. Distinction of neurons, glia and endothelial cells in the cerebral cortex: an algorithm based on cytological features. Front. Neuroanat. https://doi.org/10.3389/fnana.2016.00107 (2016).
Jones, D. G. & Devon, R. M. An ultrastructural study into the effects of pentobarbitone on synaptic organization. Brain Res. 147, 47–63 (1978).
doi: 10.1016/0006-8993(78)90771-0
Flygt, J. et al. Neutralization of interleukin-1β following diffuse traumatic brain injury in the mouse attenuates the loss of mature oligodendrocytes. J. Neurotrauma 35, 2837–2849 (2018).
doi: 10.1089/neu.2018.5660

Auteurs

Yanli Zhang (Y)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Brain Institute, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, China.

Weixi Feng (W)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Center for Global Haealth, Nanjing Medical University, Nanjing, China.

Ze Wang (Z)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Brain Institute, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, China.

Yingting Pang (Y)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Center for Global Haealth, Nanjing Medical University, Nanjing, China.

Yuxi Jin (Y)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Brain Institute, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, China.

Sijia Chen (S)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Brain Institute, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, China.

Shixin Ding (S)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Brain Institute, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, China.

Tianqi Wang (T)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Center for Global Haealth, Nanjing Medical University, Nanjing, China.

Ying Zou (Y)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Center for Global Haealth, Nanjing Medical University, Nanjing, China.

Peng Sun (P)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Center for Global Haealth, Nanjing Medical University, Nanjing, China.

Yan Chen (Y)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Brain Institute, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, China.

Hu Feng (H)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China.
Center for Global Haealth, Nanjing Medical University, Nanjing, China.

Huang Huang (H)

Department of Neurology, Sir Run Run Hospital, Nanjing Medical University, Nanjing, China.

Chengyu Sheng (C)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China. cysheng@njmu.edu.cn.

Ming Xiao (M)

Jiangsu Key Laboratory of Neurodegeneration, Nanjing Medical University, Nanjing, China. mingx@njmu.edu.cn.
Brain Institute, Nanjing Brain Hospital, Nanjing Medical University, Nanjing, China. mingx@njmu.edu.cn.
Center for Global Haealth, Nanjing Medical University, Nanjing, China. mingx@njmu.edu.cn.

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