Sex differences in epigenetic mechanisms may underlie risk and resilience for mental health disorders

References

• Métivier R, Gallais R, Tiffoche C, Le Péron C, Jurkowska RZ, Carmouche RP, et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008; 452:45 - 50
   PubMed Web of Science ®Google Scholar
• Grafstrom RH, Yuan R, Hamilton DL. The characteristics of DNA methylation in an in vitro DNA synthesizing system from mouse fibroblasts. Nucleic Acids Res 1985; 13:2827 - 2842
   PubMed Web of Science ®Google Scholar
• Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, 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
   PubMed Web of Science ®Google Scholar
• Pradhan S, Bacolla A, Wells RD, Roberts RJ. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification and comparison of de novo and maintenance methylation. J Biol Chem 1999; 274:33002 - 33010
   PubMed Web of Science ®Google Scholar
• Yoder JA, Soman NS, Verdine GL, Bestor TH. DNA (cytosine-5)-methyltransferases in mouse cells and tissues. Studies with a mechanism-based probe. J Mol Biol 1997; 270:385 - 395
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Hsieh CL. In vivo activity of murine de novo methyltransferases, Dnmt3a and Dnmt3b. Mol Cell Biol 1999; 19:8211 - 8218
   PubMed Web of Science ®Google Scholar
• Feng J, Chang H, Li E, Fan G. Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J Neurosci Res 2005; 79:734 - 746
   PubMed Web of Science ®Google Scholar
• Kolodkin MH, Auger AP. Sex difference in the expression of DNA methyltransferase 3a (DNMT3a) in the rat amygdala during development. J Neuroendocrinol 2011; In press
   PubMed Web of Science ®Google Scholar
• Meaney MJ, Dodge AM, Beatty WW. Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats. Physiol Behav 1981; 26:467 - 472
   PubMed Web of Science ®Google Scholar
• Pinel JP, Treit D, Rovner LI. Temporal lobe aggression in rats. Science 1977; 197:1088 - 1089
   PubMed Web of Science ®Google Scholar
• Hitchcock J, Davis M. Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav Neurosci 1986; 100:11 - 22
   PubMed Web of Science ®Google Scholar
• Shibata K, Kataoka Y, Yamashita K, Ueki S. An important role of the central amygdaloid nucleus and mammillary body in the mediation of conflict behavior in rats. Brain Res 1986; 372:159 - 162
   PubMed Web of Science ®Google Scholar
• LaPlant Q, Vialou V, Covington HE 3rd, Dumitriu D, Feng J, Warren BL, et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 2010; 13:1137 - 1143
   Google Scholar
• Feng J, Zhou Y, Campbell SL, Le T, Li E, Sweatt JD, et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 2010; 13:423 - 430
   PubMed Web of Science ®Google Scholar
• Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ. 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
   PubMed Web of Science ®Google Scholar
• Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7:847 - 854
   PubMed Web of Science ®Google Scholar
• Moore CL, Morelli GA. Mother rats interact differently with male and female offspring. J Comp Physiol Psychol 1979; 93:677 - 684
   PubMed Web of Science ®Google Scholar
• Moore CL. Maternal contributions to the development of masculine sexual behavior in laboratory rats. Dev Psychobiol 1984; 17:347 - 356
   PubMed Web of Science ®Google Scholar
• Kurian JR, Olesen KM, Auger AP. Sex differences in epigenetic regulation of the estrogen receptor-alpha promoter within the developing preoptic area. Endocrinology 2010; 151:2297 - 2305
   PubMed Web of Science ®Google Scholar
• Edelmann MN, Auger AP. Epigenetic impact of simulated maternal grooming on estrogen receptor alpha within the developing amygdala. Brain Behav Immun 2011; In press
   PubMed Web of Science ®Google Scholar
• DonCarlos LL, Handa RJ. 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
   PubMedGoogle Scholar
• Yamamoto Y, Carter CS, Cushing BS. Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha. Neuroscience 2006; 137:157 - 164
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Auger CJ, Coss D, Auger AP, Forbes-Lorman RM. 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
   Google Scholar
• Hendrich B, Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 1998; 18:6538 - 6547
   PubMed Web of Science ®Google Scholar
• Meehan RR, Lewis JD, McKay S, Kleiner EL, Bird AP. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell 1989; 58:499 - 507
   PubMed Web of Science ®Google Scholar
• Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 1999; 23:185 - 188
   PubMed Web of Science ®Google Scholar
• Chen RZ, 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 2001; 27:327 - 331
   PubMed Web of Science ®Google Scholar
• Guy J, Hendrich B, Holmes M, Martin JE, Bird A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 2001; 27:322 - 326
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Nagarajan RP, Hogart AR, Gwye Y, Martin MR, LaSalle JM. Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics 2006; 1:1 - 11
   PubMed Web of Science ®Google Scholar
• Kurian JR, Forbes-Lorman RM, Auger AP. Sex difference in mecp2 expression during a critical period of rat brain development. Epigenetics 2007; 2:173 - 178
   PubMed Web of Science ®Google Scholar
• Kurian JR, Bychowski ME, Forbes-Lorman RM, Auger CJ, Auger AP. Mecp2 organizes juvenile social behavior in a sex-specific manner. J Neurosci 2008; 28:7137 - 7142
   PubMed Web of Science ®Google Scholar
• Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006; 31:89 - 97
   PubMed Web of Science ®Google Scholar
• Cunliffe VT. Eloquent silence: developmental functions of Class I histone deacetylases. Curr Opin Genet Dev 2008; 18:404 - 410
   PubMed Web of Science ®Google Scholar
• Horlein AJ, et al. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 1995; 377:397 - 404
   PubMed Web of Science ®Google Scholar
• Cheng S, Brzostek S, Lee SR, Hollenberg AN, Balk SP. Inhibition of the dihydrotestosterone-activated androgen receptor by nuclear receptor corepressor. Mol Endocrinol 2002; 16:1492 - 1501
   PubMed Web of Science ®Google Scholar
• Yoon HG, Wong J. The corepressors silencing mediator of retinoid and thyroid hormone receptor and nuclear receptor corepressor are involved in agonist- and antagonist-regulated transcription by androgen receptor. Mol Endocrinol 2006; 20:1048 - 1060
   PubMed Web of Science ®Google Scholar
• Lavinsky RM, Jepsen K, Heinzel T, Torchia J, Mullen TM, Schiff R, et al. Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc Natl Acad Sci USA 1998; 95:2920 - 2925
   PubMed Web of Science ®Google Scholar
• Liu Z, Auboeuf D, Wong J, Chen JD, Tsai SY, Tsai MJ, et al. Coactivator/corepressor ratios modulate PR-mediated transcription by the selective receptor modulator RU486. Proc Natl Acad Sci USA 2002; 99:7940 - 7944
   PubMed Web of Science ®Google Scholar
• Yoon HG, Chan DW, Reynolds AB, Qin J, Wong J. N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso. Mol Cell 2003; 12:723 - 734
   PubMed Web of Science ®Google Scholar
• Cukier HN, Perez AM, Collins AL, Zhou Z, Zoghbi HY, Botas J. Genetic modifiers of MeCP2 function in Drosophila. PLoS Genet 2008; 4:1000179
   Web of Science ®Google Scholar
• Kokura K, Kaul SC, Wadhwa R, Nomura T, Khan MM, Shinagawa T, et al. The Ski protein family is required for MeCP2-mediated transcriptional repression. J Biol Chem 2001; 276:34115 - 34121
   PubMedGoogle Scholar
• Alland L, Muhle R, Hou H Jr, Potes J, Chin L, Schreiber-Agus N, et al. Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature 1997; 387:49 - 55
   PubMed Web of Science ®Google Scholar
• Jessen HM, Kolodkin MH, Bychowski ME, Auger CJ, Auger AP. The nuclear receptor corepressor has organizational effects within the developing amygdala on juvenile social play and anxiety-like behavior. Endocrinology 2010; 151:1212 - 1220
   PubMed Web of Science ®Google Scholar