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The Journal of Neuroscience, October 14, 2009, 29(41):12815-12823; doi:10.1523/JNEUROSCI.3331-09.2009

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Symposia and Mini-Symposia
The Epigenetics of Sex Differences in the Brain

Margaret M. McCarthy,¹ Anthony P. Auger,² Tracy L. Bale,³ Geert J. De Vries,⁴ Gregory A. Dunn,³ Nancy G. Forger,⁴ Elaine K. Murray,⁴ Bridget M. Nugent,¹ Jaclyn M. Schwarz,⁵ and Melinda E. Wilson⁶

¹Department of Physiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201-1559, ²Department of Psychology, University of Wisconsin, Madison, Wisconsin 53706-1611, ³Department of Animal Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6009, ⁴Department of Psychology and Center for Neuroendocrine Studies, University of Massachusetts, Amherst, Massachusetts 01003, ⁵Department of Psychology and Neuroscience, Duke University, Durham, North Carolina 27708, and ⁶Department of Physiology, University of Kentucky College of Medicine, Lexington, Kentucky 40536

Correspondence should be addressed to Margaret M. McCarthy at the above address. Email: mmccarth{at}umaryland.edu

Epigenetic changes in the nervous system are emerging as a critical component of enduring effects induced by early life experience, hormonal exposure, trauma and injury, or learning and memory. Sex differences in the brain are largely determined by steroid hormone exposure during a perinatal sensitive period that alters subsequent hormonal and nonhormonal responses throughout the lifespan. Steroid receptors are members of a nuclear receptor transcription factor superfamily and recruit multiple proteins that possess enzymatic activity relevant to epigenetic changes such as acetylation and methylation. Thus steroid hormones are uniquely poised to exert epigenetic effects on the developing nervous system to dictate adult sex differences in brain and behavior. Sex differences in the methylation pattern in the promoter of estrogen and progesterone receptor genes are evident in newborns and persist in adults but with a different pattern. Changes in response to injury and in methyl-binding proteins and steroid receptor coregulatory proteins are also reported. Many steroid-induced epigenetic changes are opportunistic and restricted to a single lifespan, but new evidence suggests endocrine-disrupting compounds can exert multigenerational effects. Similarly, maternal diet also induces transgenerational effects, but the impact is sex specific. The study of epigenetics of sex differences is in its earliest stages, with needed advances in understanding of the hormonal regulation of enzymes controlling acetylation and methylation, coregulatory proteins, transient versus stable DNA methylation patterns, and sex differences across the epigenome to fully understand sex differences in brain and behavior.

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Received July 13, 2009; revised Aug. 20, 2009; accepted Sept. 2, 2009.

Correspondence should be addressed to Margaret M. McCarthy at the above address. Email: mmccarth{at}umaryland.edu

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