Permanent and plastic epigenesis in neuroendocrine systems

Frontiers in Neuroendocrinology

Volumn 34, Issue 3, 2013, Pages 190-197

  Auger, Catherine J ^a   Auger, Anthony P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Brain; Coactivators; Epigenetic; Histones; MeCP2; Methylation; Sex difference; Sexual differentiation; Steroid hormones; Vasopressin

Indexed keywords

DNA METHYLTRANSFERASE; METHYL CPG BINDING PROTEIN;

BINDING AFFINITY; BINDING SITE; BRAIN DEVELOPMENT; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GENE CONTROL; GENETIC EPIGENESIS; HISTONE MODIFICATION; HUMAN; MOLECULAR DYNAMICS; NEUROENDOCRINE SYSTEM; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN STABILITY; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION;

EID: 84881316191     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2013.05.003     Document Type: Review

References (86)

1. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999, 23:185-188.
2. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
3. Auger A.P., Auger C.J. Epigenetic turn ons and turn offs: chromatin reorganization and brain differentiation. Endocrinology 2011, 152:349-353.
4. Auger A.P., Olesen K.M. Brain sex differences and the organisation of juvenile social play behaviour. J. Neuroendocrinol. 2009, 21:519-525.
5. Auger A.P., Tetel M.J., McCarthy M.M. Steroid receptor coactivator-1 (SRC-1) mediates the development of sex-specific brain morphology and behavior. Proc. Natl. Acad. Sci. USA 2000, 97:7551-7555.
6. Auger A.P., Perrot-Sinal T.S., Auger C.J., Ekas L.A., Tetel M.J., McCarthy M.M. Expression of the nuclear receptor coactivator, cAMP response element-binding protein, is sexually dimorphic and modulates sexual differentiation of neonatal rat brain. Endocrinology 2002, 143:3009-3016.
7. Auger A.P., Jessen H.M., Edelmann M.N. Epigenetic organization of brain sex differences and juvenile social play behavior. Horm. Behav. 2010, 3:358-363.
8. Auger C.J., Coss D., Auger A.P., Forbes-Lorman R.M. Epigenetic control of vasopressin expression is maintained by steroid hormones in the adult male rat brain. Proc. Natl. Acad. Sci. USA 2011, 108:4242-4247.
9. Ballas N., Lioy D.T., Grunseich C., Mandel G. Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat. Neurosci. 2009, 12:311-317.
10. Barreto G., Schafer A., Marhold J., Stach D., Swaminathan S.K., Handa V., Doderlein G., Maltry N., Wu W., Lyko F., Niehrs C. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445:671-675.
11. Bielsky I.F., Young L.J. Oxytocin, vasopressin, and social recognition in mammals. Peptides 2004, 25:1565-1574.
12. Bielsky I.F., Hu S.B., Ren X., Terwilliger E.F., Young L.J. The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 2005, 47:503-513.
13. Bonthuis P.J., Patteson J.K., Rissman E.F. Acquisition of sexual receptivity: roles of chromatin acetylation, estrogen receptor-alpha, and ovarian hormones. Endocrinology 2011, 152:3172-3181.
14. Caldwell H.K., Lee H.J., Macbeth A.H., Young W.S. Vasopressin: behavioral roles of an "original" neuropeptide. Prog. Neurobiol. 2008, 84:1-24.
15. Carouge D., Host L., Aunis D., Zwiller J., Anglard P. CDKL5 is a brain MeCP2 target gene regulated by DNA methylation. Neurobiol. Dis. 2010, 38:414-424.
16. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
17. Champagne F.A. Interplay between social experiences and the genome: epigenetic consequences for behavior. Adv. Genet. 2012, 77:33-57.
18. Champagne F.A., Weaver I.C., Diorio J., Dymov S., Szyf M., Meaney M.J. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 2006, 147:2909-2915.
19. Charlier T.D., Ball G.F., Balthazart J. Inhibition of steroid receptor coactivator-1 blocks estrogen and androgen action on male sex behavior and associated brain plasticity. J. Neurosci. 2005, 25:906-913.
20. Collingwood T.N., Urnov F.D., Wolffe A.P. Nuclear receptors: coactivators, corepressors and chromatin remodeling in the control of transcription. J. Mol. Endocrinol. 1999, 23:255-275.
21. De Vries G.J., Simerly R.B. Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain. Hormones, Brain and Behavior 2002, 137-191. Academic Press, San Diego. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
22. De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 2002, 22:9005-9014.
23. DonCarlos L.L., Handa R.J. Developmental profile of estrogen receptor mRNA in the preoptic area of male and female neonatal rats. Brain Res. Dev. Brain Res. 1994, 79:283-289.
24. Edelmann M.N., Auger A.P. Epigenetic impact of simulated maternal grooming on estrogen receptor alpha within the developing amygdala. Brain Behav. Immun. 2011, 7:1299-1304.
25. Forbes-Lorman R.M., Rautio J.J., Kurian J.R., Auger A.P., Auger C.J. Neonatal MeCP2 is important for the organization of sex differences in vasopressin expression. Epigenetics 2012, 7:230-238.
26. Fraga M.F., Ballestar E., Paz M.F., Ropero S., Setien F., Ballestar M.L., Heine-Suner D., Cigudosa J.C., Urioste M., Benitez J., Boix-Chornet M., Sanchez-Aguilera A., Ling C., Carlsson E., Poulsen P., Vaag A., Stephan Z., Spector T.D., Wu Y.Z., Plass C., Esteller M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. USA 2005, 102:10604-10609.
27. Grafstrom R.H., Yuan R., Hamilton D.L. The characteristics of DNA methylation in an in vitro DNA synthesizing system from mouse fibroblasts. Nucl. Acids Res. 1985, 13:2827-2842.
28. 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. 2001, 27:322-326.
29. Guy J., Gan J., Selfridge J., Cobb S., Bird A. Reversal of neurological defects in a mouse model of Rett syndrome. Science 2007, 315:1143-1147.
30. He Y.F., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., Ding J., Jia Y., Chen Z., Li L., Sun Y., Li X., Dai Q., Song C.X., Zhang K., He C., Xu G.L. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011, 333:1303-1307.
31. Hendrich B., Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol. Cell Biol. 1998, 18:6538-6547.
32. Hochberg Z., Feil R., Constancia M., Fraga M., Junien C., Carel J.C., Boileau P., Le B.Y., Deal C.L., Lillycrop K., Scharfmann R., Sheppard A., Skinner M., Szyf M., Waterland R.A., Waxman D.J., Whitelaw E., Ong K., Albertsson-Wikland K. Child health, developmental plasticity, and epigenetic programming. Endocr. Rev. 2011, 32:159-224.
33. Howlett S.K., Reik W. Methylation levels of maternal and paternal genomes during preimplantation development. Development 1991, 113:119-127.
34. Hsieh C.L. In vivo activity of murine de novo methyltransferases, Dnmt3a and Dnmt3b. Mol. Cell Biol. 1999, 19:8211-8218.
35. Ito S., Shen L., Dai Q., Wu S.C., Collins L.B., Swenberg J.A., He C., Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
36. Jessen H.M., Auger A.P. Sex differences in epigenetic mechanisms may underlie risk and resilience for mental health disorders. Epigenetics 2011, 6:857-861.
37. Klose R.J., Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 2006, 31:89-97.
38. Kolodkin M.H., Auger A.P. Sex difference in the expression of DNA methyltransferase 3a (DNMT3a) in the rat amygdala during development. J. Neuroendocrinol. 2011, 7:577-583.
39. Kurian J.R., Forbes-Lorman R.M., Auger A.P. Sex difference in mecp2 expression during a critical period of rat brain development. Epigenetics 2007, 2:173-178.
40. Kurian J.R., Bychowski M.E., Forbes-Lorman R.M., Auger C.J., Auger A.P. Mecp2 organizes juvenile social behavior in a sex-specific manner. J. Neurosci. 2008, 28:7137-7142.
41. Kurian J.R., Keen K.L., Terasawa E. Epigenetic changes coincide with in vitro primate GnRH neuronal maturation. Endocrinology 2010, 151:5359-5368.
42. Kurian J.R., Olesen K.M., Auger A.P. Sex differences in epigenetic regulation of the estrogen receptor-alpha promoter within the developing preoptic area. Endocrinology 2010, 151:2297-2305.
43. Lioy D.T., Garg S.K., Monaghan C.E., Raber J., Foust K.D., Kaspar B.K., Hirrlinger P.G., Kirchhoff F., Bissonnette J.M., Ballas N., Mandel G. A role for glia in the progression of Rett's syndrome. Nature 2011, 475:497-500.
44. Lonstein J.S., Auger A.P. Perinatal gonadal hormone influences on neurobehavioral development. Handbook of Behavioral and Comparative Neuroscience 2009, 424-453. Oxford University Press, New York. M. Blumberg, J. Freeman, S. Robinson (Eds.).
45. Lubin F.D., Roth T.L., Sweatt J.D. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J. Neurosci. 2008, 28:10576-10586.
46. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 2009, 10:434-445.
47. Maddox S.A., Schafe G.E. Epigenetic alterations in the lateral amygdala are required for reconsolidation of a Pavlovian fear memory. Learn. Mem. 2011, 18:579-593.
48. Maezawa I., Jin L.W. Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J. Neurosci. 2010, 30:5346-5356.
49. Matsuda K.I., Mori H., Nugent B.M., Pfaff D.W., McCarthy M.M., Kawata M. Histone deacetylation during brain development is essential for permanent masculinization of sexual behavior. Endocrinology 2011, 152:2760-2767.
50. McCarthy M.M., Arnold A.P. Reframing sexual differentiation of the brain. Nat. Neurosci. 2011, 14:677-683.
51. McCarthy M.M., Auger A.P., Bale T.L., De Vries G.J., Dunn G.A., Forger N.G., Murray E.K., Nugent B.M., Schwarz J.M., Wilson M.E. The epigenetics of sex differences in the brain. J. Neurosci. 2009, 29:12815-12823.
52. McGraw C.M., Samaco R.C., Zoghbi H.Y. Adult neural function requires MeCP2. S c i ence 2011, 333:186.
53. Mermelstein P.G., Micevych P.E. Nervous system physiology regulated by membrane estrogen receptors. Rev. Neurosci. 2008, 19:413-424.
54. Metivier R., Gallais R., Tiffoche C., Le P.C., Jurkowska R.Z., Carmouche R.P., Ibberson D., Barath P., Demay F., Reid G., Benes V., Jeltsch A., Gannon F., Salbert G. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
55. Molenda H.A., Griffen A.L., Auger A.P., McCarthy M.M., Tetel M.J. Nuclear receptor coactivators modulate hormone-dependent gene expression in brain and female reproductive behavior in rats. Endocrinology 2002, 143:436-444.
56. Moore C.L., Morelli G.A. Mother rats interact differently with male and female offspring. J. Comp. Physiol. Psychol. 1979, 93:677-684.
57. Morgan C.P., Bale T.L. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J. Neurosci. 2011, 31:11748-11755.
58. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmuhl Y., Fischer D., Holsboer F., Wotjak C.T., Almeida O.F., Spengler D. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 2009, 12:1559-1566.
59. Murray E.K., Hien A., De Vries G.J., Forger N.G. Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis. Endocrinology 2009, 150:4241-4247.
60. Nagarajan R.P., Hogart A.R., Gwye Y., Martin M.R., LaSalle J.M. Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics. 2006, 1:e1-11.
61. Nan X., Meehan R.R., Bird A. Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucl. Acids Res. 1993, 21:4886-4892.
62. Nanney D.L. Epigenetic control systems. Proc. Natl. Acad. Sci. USA 1958, 44:712-717.
63. Okano M., Xie S., Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet. 1998, 19:219-220.
64. Oswald J., Engemann S., Lane N., Mayer W., Olek A., Fundele R., Dean W., Reik W., Walter J. Active demethylation of the paternal genome in the mouse zygote. Curr.Biol. 2000, 10:475-478.
65. Pradhan S., Bacolla A., Wells R.D., Roberts R.J. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J. Biol. Chem. 1999, 274:33002-33010.
66. Ramsahoye B.H., Biniszkiewicz D., Lyko F., Clark V., Bird A.P., Jaenisch R. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc. Natl. Acad. Sci. USA 2000, 97:5237-5242.
67. Razin A., Riggs A.D. DNA methylation and gene function. Science 1980, 210:604-610.
68. Robison A.J., Nestler E.J. Transcriptional and epigenetic mechanisms of addiction. Nat. Rev. Neurosci. 2011, 12:623-637.
69. Schwarz J.M., Nugent B.M., McCarthy M.M. Developmental and Hormone-Induced Epigenetic Changes to Estrogen and Progesterone Receptor Genes in Brain Are Dynamic across the Life Span. Endocrinology 2010.
70. Szulwach K.E., Li X., Li Y., Song C.X., Wu H., Dai Q., Irier H., Upadhyay A.K., Gearing M., Levey A.I., Vasanthakumar A., Godley L.A., Chang Q., Cheng X., He C., Jin P. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci. 2011, 14:1607-1616.
71. Tetel M.J., Auger A.P., Charlier T.D. Who's in charge? Nuclear receptor coactivator and corepressor function in brain and behavior. Front. Neuroendocrinol. 2009, 30:328-342.
72. Tsai H.W., Grant P.A., Rissman E.F. Sex differences in histone modifications in the neonatal mouse brain. Epigenetics 2009, 4:47-53.
73. Unternaehrer E., Luers P., Mill J., Dempster E., Meyer A.H., Staehli S., Lieb R., Hellhammer D.H., Meinlschmidt G. Dynamic changes in DNA methylation of stress-associated genes (OXTR, BDNF) after acute psychosocial stress. Transl. Psychiatry 2012, 2:e150.
74. Veenema A.H., Neumann I.D. Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 2009, 34:463-467.
75. Waddington C.H. The epigenotype. Endeavour 1942, 1:18-20.
76. Walker D.M., Gore A.C. Transgenerational neuroendocrine disruption of reproduction. Nat. Rev. Endocrinol. 2011, 7:197-207.
77. Weaver I.C., Cervoni N., Champagne F.A., D'Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
78. Westberry J.M., Trout A.L., Wilson M.E. Epigenetic Regulation of Estrogen Receptor {alpha} Gene Expression in the Mouse Cortex during Early Postnatal Development. Endocrinology 2009.
79. Winslow J.T., Hastings N., Carter C.S., Harbaugh C.R., Insel T.R. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 1993, 365:545-548.
80. Yamamoto Y., Carter C.S., Cushing B.S. Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha. Neuroscience 2006, 137:157-164.
81. Yoder J.A., Soman N.S., Verdine G.L., Bestor T.H. DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J. Mol. Biol. 1997, 270:385-395.
82. Yokosuka M., Okamura H., Hayashi S. Postnatal development and sex difference in neurons containing estrogen receptor-alpha immunoreactivity in the preoptic brain, the diencephalon, and the amygdala in the rat. J. Comp. Neurol. 1997, 389:81-93.
83. Yoon H.G., Chan D.W., Reynolds A.B., Qin J., Wong J. N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso. Mol. Cell 2003, 12:723-734.
84. Zhao Z., Fan L., Frick K.M. Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation. Proc. Natl. Acad. Sci. USA 2010, 107:5605-5610.
85. Zhou Z., Hong E.J., Cohen S., Zhao W.N., Ho H.Y., Schmidt L., Chen W.G., Lin Y., Savner E., Griffith E.C., Hu L., Steen J.A., Weitz C.J., Greenberg M.E. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 2006, 52:255-269.
86. Zovkic I.B., Guzman-Karlsson M.C., Sweatt J.D. Epigenetic regulation of memory formation and maintenance. Learn. Mem. 2013, 20:61-74.