MeCP2 and histone deacetylases 1 and 2 in dorsal striatum collectively suppress repetitive behaviors

Nature Neuroscience

Volumn 19, Issue 11, 2016, Pages 1506-1512

  Mahgoub, Melissa ^a   Adachi, Megumi ^a   Suzuki, Kanzo ^a   Liu, Xihui ^a   Kavalali, Ege T ^a   Chahrour, Maria H ^a,b   Monteggia, Lisa M ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; METHYL CPG BINDING PROTEIN 2; POSTSYNAPTIC DENSITY PROTEIN 95; HDAC1 PROTEIN, MOUSE; HDAC2 PROTEIN, MOUSE; MECP2 PROTEIN, MOUSE; NERVE PROTEIN; SAPAP3 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; COMPULSION; CONTROLLED STUDY; DORSAL STRIATUM; FOREBRAIN; GENE DELETION; GENE EXPRESSION; GROOMING; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; ANIMAL BEHAVIOR; CENTRAL NERVOUS SYSTEM; CORPUS STRIATUM; GENETICS; METABOLISM; PHYSIOLOGY; RETT SYNDROME; TRANSGENIC MOUSE;

ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM; CORPUS STRIATUM; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; METHYL-CPG-BINDING PROTEIN 2; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PHENOTYPE; RETT SYNDROME;

EID: 84988714343     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4395     Document Type: Article

References (45)

1. Haberland, M., Montgomery, R.L. & Olson, E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10, 32-42 (2009).
2. Levenson, J.M. et al. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 279, 40545-40559 (2004).
3. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M. & Tsai, L.H. Recovery of learning and memory is associated with chromatin remodelling. Nature 447, 178-182 (2007).
4. Vecsey, C.G. et al. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 27, 6128-6140 (2007).
5. Barrett, R.M. & Wood, M.A. Beyond transcription factors: the role of chromatin modifying enzymes in regulating transcription required for memory. Learn. Mem. 15, 460-467 (2008).
6. Morris, M.J., Karra, A.S. & Monteggia, L.M. Histone deacetylases govern cellular mechanisms underlying behavioral and synaptic plasticity in the developing and adult brain. Behav. Pharmacol. 21, 409-419 (2010).
7. Guan, J.S. et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459, 55-60 (2009).
8. Morris, M.J., Mahgoub, M., Na, E.S., Pranav, H. & Monteggia, L.M. Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. J. Neurosci. 33, 6401-6411 (2013).
9. Shahbazian, M.D. & Grunstein, M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 76, 75-100 (2007).
10. Jones, P.L. et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19, 187-191 (1998).
11. Nan, X. et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389 (1998).
12. Guy, J., Hendrich, B., Holmes, M., Martin, J.E. & Bird, A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27, 322-326 (2001).
13. Chen, R.Z., Akbarian, S., Tudor, M. & Jaenisch, R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27, 327-331 (2001).
14. Gemelli, T. et al. Postnatal loss of methyl-CpG binding protein 2 in the forebrain is sufficient to mediate behavioral aspects of Rett syndrome in mice. Biol. Psychiatry 59, 468-476 (2006).
15. Nelson, E.D., Kavalali, E.T. & Monteggia, L.M. MeCP2-dependent transcriptional repression regulates excitatory neurotransmission. Curr. Biol. 16, 710-716 (2006).
16. Chao, H.T., Zoghbi, H.Y. & Rosenmund, C. MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56, 58-65 (2007).
17. Amir, R.E. et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23, 185-188 (1999).
18. Moretti, P. & Zoghbi, H.Y. MeCP2 dysfunction in Rett syndrome and related disorders. Curr. Opin. Genet. Dev. 16, 276-281 (2006).
19. Hagberg, B., Aicardi, J., Dias, K. & Ramos, O. A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: report of 35 cases. Ann. Neurol. 14, 471-479 (1983).
20. Zoghbi, H. Genetic aspects of Rett syndrome. J. Child Neurol. 3 (Suppl.), S76-S78 (1988).
21. Adachi, M., Autry, A.E., Covington, H.E. III. & Monteggia, L.M. MeCP2-mediated transcription repression in the basolateral amygdala may underlie heightened anxiety in a mouse model of Rett syndrome. J. Neurosci. 29, 4218-4227 (2009).
22. Chao, H.T. et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468, 263-269 (2010).
23. Montgomery, R.L. et al. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev. 21, 1790-1802 (2007).
24. Fan, G. et al. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 21, 788-797 (2001).
25. Welch, J.M. et al. Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature 448, 894-900 (2007).
26. Shmelkov, S.V. et al. Slitrk5 deficiency impairs corticostriatal circuitry and leads to obsessive-compulsive-like behaviors in mice. Nat. Med. 16, 598-602 (2010).
27. McDougle, C.J. Update on pharmacologic management of OCD: agents and augmentation. J. Clin. Psychiatry 58 (Suppl. 12), 11-17 (1997).
28. Rapoport, J.L. & Inoff-Germain, G. Treatment of obsessive-compulsive disorder in children and adolescents. J. Child Psychol. Psychiatry 41, 419-431 (2000).
29. Vythilingum, B., Cartwright, C. & Hollander, E. Pharmacotherapy of obsessive-compulsive disorder: experience with the selective serotonin reuptake inhibitors. Int. Clin. Psychopharmacol. 15 (Suppl. 2), S7-S13 (2000).
30. Charney, D.S., Nestler, E.J., Sklar, P. & Buxbaum, J.D. Neurobiology of Mental Illness (Oxford University Press, 2013).
31. Berton, O. et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868 (2006).
32. Grunstein, M. Histone acetylation in chromatin structure and transcription. Nature 389, 349-352 (1997).
33. Chahrour, M. et al. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224-1229 (2008).
34. Yasui, D.H. et al. Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl. Acad. Sci. USA 104, 19416-19421 (2007).
35. Kent, W.J. et al. The human genome browser at UCSC. Genome Res. 12, 996-1006 (2002).
36. Montgomery, R.L., Hsieh, J., Barbosa, A.C., Richardson, J.A. & Olson, E.N. Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc. Natl. Acad. Sci. USA 106, 7876-7881 (2009).
37. Na, E.S. et al. A mouse model for Mecp2 duplication syndrome: MeCP2 overexpression impairs learning and memory and synaptic transmission. J. Neurosci. 32, 3109-3117 (2012).
38. Adeosun, S.O. et al. Cognitive deficits and disruption of neurogenesis in a mouse model of apolipoprotein E4 domain interaction. J. Biol. Chem. 289, 2946-2959 (2014).
39. Liu, X. et al. Interleukin 1 type 1 receptor restore: a genetic mouse model for studying interleukin 1 receptor-mediated effects in specific cell types. J. Neurosci. 35, 2860-2870 (2015).
40. Fremont, R., Tewari, A. & Khodakhah, K. Aberrant Purkinje cell activity is the cause of dystonia in a shRNA-based mouse model of rapid onset dystonia-Parkinsonism. Neurobiol. Dis. 82, 200-212 (2015).
41. Adachi, M., Barrot, M., Autry, A.E., Theobald, D. & Monteggia, L.M. Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol. Psychiatry 63, 642-649 (2008).
42. Potts, R.C. et al. CHD5, a brain-specific paralog of Mi2 chromatin remodeling enzymes, regulates expression of neuronal genes. PLoS One 6, e24515 (2011).
43. Flavell, S.W. et al. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60, 1022-1038 (2008).
44. Li, W., Calfa, G., Larimore, J. & Pozzo-Miller, L. Activity-dependent BDNF release and TRPC signaling is impaired in hippocampal neurons of Mecp2 mutant mice. Proc. Natl. Acad. Sci. USA 109, 17087-17092 (2012).
45. Autry, A.E. et al. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475, 91-95 (2011).