The epigenetics of sex differences in the brain

Journal of Neuroscience

Volumn 29, Issue 41, 2009, Pages 12815-12823

  McCarthy, Margaret M ^a   Auger, Anthony P ^b   Bale, Tracy L ^c   De Vries, Geert J ^d   Dunn, Gregory A ^c   Forger, Nancy G ^d   Murray, Elaine K ^d   Nugent, Bridget M ^a   Schwarz, Jaclyn M ^e   Wilson, Melinda E ^f  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

^e DUKE UNIVERSITY   (United States)

^f UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; DNA METHYLTRANSFERASE; ESTROGEN RECEPTOR; HISTONE; PROGESTERONE RECEPTOR; STEROID HORMONE; STEROID RECEPTOR; TRANSCRIPTION FACTOR;

ACETYLATION; ADULT; BEHAVIOR; BRAIN; CONFERENCE PAPER; CPG ISLAND; DIET; DNA METHYLATION; ENZYME ACTIVITY; EPIGENETICS; EXPOSURE; GENE REPRESSION; HORMONAL REGULATION; HUMAN; INJURY; LIFESPAN; MEMORY; METHYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MODIFICATION; SEX CHROMOSOME; SEX DIFFERENCE; ANIMAL; BIOLOGICAL MODEL; FEMALE; GENETIC EPIGENESIS; GENETICS; MALE; METABOLISM; PHYSIOLOGY; REVIEW; SEXUAL DEVELOPMENT;

ANIMALS; BRAIN; DNA MODIFICATION METHYLASES; EPIGENESIS, GENETIC; FEMALE; HISTONES; HUMANS; MALE; MODELS, BIOLOGICAL; SEX CHARACTERISTICS;

EID: 70350433239     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3331-09.2009     Document Type: Conference Paper

References (82)

1. Akbarian S, Huang HS (2009) Epigenetic regulation in human brain-focus on histone lysine methylation. Biol Psychiatry 65:198-203.
2. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185-188. (Pubitemid 29455390)
3. Anderson LM, Riffle L, Wilson R, Travlos GS, Lubomirski MS, Alvord WG (2006) Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 22:327-331. (Pubitemid 43261531)
4. Avner P, Heard E (2001) X-chromosome inactivation: counting, choice and initiation. Nat Rev Genet 2:59-67. (Pubitemid 33674770)
5. Bale TL (2006) Stress sensitivity and the development of affective disorders. Horm Behav 50:529-533.
6. Brown TJ, Hochberg RB, Zielinski JE, MacLusky NJ (1988) Regional sex differences in cell nuclear estrogen-binding capacity in the rat hypothalamus and preoptic area. Endocrinology 123:1761-1770.
7. Cameron N, Del Corpo A, Diorio J, McAllister K, Sharma S, Meaney MJ (2008) Maternal programming of sexual behavior and hypothalamic-pituitary- gonadal function in the female rat. PLoS ONE 3:e2210.
8. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ (2006) Maternal care associated with methylation of the estrogen receptoralpha 1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 147:2909-2915. (Pubitemid 43764626)
9. Chen X, Grisham W, Arnold AP (2009) X chromosome number causes sex differences in gene expression in adult mouse striatum. Eur J Neurosci 29:768-776.
10. Choi DC, Furay AR, Evanson NK, Ostrander MM, Ulrich-Lai YM, Herman JP (2007) Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J Neurosci 27:2025-2034.
11. Choi DC, Evanson NK, Furay AR, Ulrich-Lai YM, Ostrander MM, Herman JP (2008) The anteroventral bed nucleus of the stria terminalis differentially regulates hypothalamic-pituitary-adrenocortical axis responses to acute and chronic stress. Endocrinology 149:818-826.
12. Chung WC, Swaab DF, De Vries GJ (2000) Apoptosis during sexual differentiation of the bed nucleus of the stria terminalis in the rat brain. J Neurobiol 43:234-243.
13. Connor CM, Akbarian S (2008) DNA methylation changes in schizophrenia and bipolar disorder. Epigenetics 3:55-58.
14. Crews D (2008) Epigenetics and its implications for behavioral neuroendocrinology. Front Neuroendocrinol 29:344-357.
15. Cukier HN, Perez AM, Collins AL, Zhou Z, Zoghbi HY, Botas J (2008) Genetic modifiers of MeCP2 function in Drosophila. PLoS Genet 4: e1000179.
16. Davies W, Lynn PM, Relkovic D, Wilkinson LS (2008) Imprinted genes and neuroendocrine function. Front Neuroendocrinol 29:413-427.
17. De Vries GJ, Panzica GC (2006) Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138:947-955.
18. DonCarlos LL (1996) Developmental profile and regulation of estrogen receptor (ER) mRNA expression in the preoptic area of prenatal rats. Brain Res Dev Brain Res 94:224-233. (Pubitemid 26292266)
19. DonCarlos LL, Handa RJ (1994) Developmental profile of estrogen receptor mRNA in the preoptic area of male and female neonatal rats. Brain Res Dev Brain Res 79:283-289.
20. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I, Kindy MS, Wise PM (2001) Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci U S A 98:1952-1957. (Pubitemid 32165604)
21. Dubal DB, Rau SW, Shughrue PJ, Zhu H, Yu J, Cashion AB, Suzuki S, Gerhold LM, Bottner MB, Dubal SB, Merchanthaler I, Kindy MS, Wise PM (2006) Differential modulation of estrogen receptors (ERs) in ischemic brain injury: a role for ERalpha in estradiol-mediated protection against delayed cell death. Endocrinology 147:3076-3084. (Pubitemid 43764643)
22. Ellis L, Atadja PW, Johnstone RW (2009) Epigenetics in cancer: targeting chromatin modifications. Mol Cancer Ther 8:1409-1420.
23. Férézou-Viala J, Roy AF, Sérougne C, Gripois D, Parquet M, Bailleux V, Gertler A, Delplanque B, Djiane J, Riottot M, Taouis M (2007) Longterm consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 293:R1056-R1062. (Pubitemid 47358924)
24. Forger NG, Rosen GJ, Waters EM, Jacob D, Simerly RB, de Vries GJ (2004) Deletion of Bax eliminates sex differences in the mouse forebrain. Proc Natl Acad Sci U S A 101:13666-13671. (Pubitemid 39238460)
25. Glaser KB, Staver MJ, Waring JF, Stender J, Ulrich RG, Davidsen SK (2003) Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol Cancer Ther 2:151-163.
26. Gniuli D, Calcagno A, Caristo ME, Mancuso A, Macchi V, Mingrone G, Vettor R (2008) Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res 49:1936-1945.
27. Goldberg AD, Allis CD, Bernstein E (2007) Epigenetics: a landscape takes shape. Cell 128:635-638.
28. Gore AC (2008) Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front Neuroendocrinol 29:358-374.
29. Gotsiridze T, Kang N, Jacob D, Forger NG (2007) Development of sex differences in the principal nucleus of the bed nucleus of the stria terminalis of mice: role of Bax-dependent cell death. Dev Neurobiol 67:355-362. (Pubitemid 46319024)
30. Guillamón A, Segovia S, del Abril A (1988) Early effects of gonadal steroids on the neuron number in the medial posterior region and the lateral division of the bed nucleus of the stria terminalis in the rat. Brain Res Dev Brain Res 44:281-290. (Pubitemid 18277520)
31. Hines M, Davis FC, Coquelin A, Goy RW, Gorski RA (1985) Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain: a description and an investigation of their relationship to gonadal steroids in adulthood. J Neurosci 5:40-47. (Pubitemid 15155668)
32. Hines M, Allen LS, Gorski RA (1992) Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res 579:321-326.
33. Hisasue S, Seney ML, Immerman E, Forger NG (2007) Cell death and the development of sex differences in the bed nucleus of the stria terminalis in mice. Soc Neurosci Abstr 33:294.23.
34. Hörlein AJ, Näär AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Söderström M, Glass CK, Rosenfeld MG (1995) Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377:397-404.
35. Issa JP, Ottaviano YL, Celano P, Hamilton SR, Davidson NE, Baylin SB (1994) Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon. Nat Genet 7:536-540. (Pubitemid 24308343)
36. James WP (2008) The epidemiology of obesity: the size of the problem. J Intern Med 263:336-352.
37. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat- Pelegrin T, Faucette RR, Otis JP, Chow A, Diaz R, Ferguson-Smith A, Patti ME (2009) Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 58:460-468.
38. Kaati G, Bygren LO, Edvinsson S (2002) Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet 10:682-688. (Pubitemid 35460575)
39. Keverne EB, Curley JP (2008) Epigenetics, brain evolution and behaviour. Front Neuroendocrinol 29:398-412.
40. Kininis M, Chen BS, Diehl AG, Isaacs GD, Zhang T, Siepel AC, Clark AG, Kraus WL (2007) Genomic analyses of transcription factor binding, histone acetylation, and gene expression reveal mechanistically distinct classes of estrogen-regulated promoters. Mol Cell Biol 27:5090-5104. (Pubitemid 47068284)
41. Kishimoto M, Fujiki R, Takezawa S, Sasaki Y, Nakamura T, Yamaoka K, Kitagawa H, Kato S (2006) Nuclear receptor mediated gene regulation through chromatin remodeling and histone modifications. Endocr J 53:157-172.
42. Kokura K, Kaul SC, Wadhwa R, Nomura T, Khan MM, Shinagawa T, Yasukawa T, Colmenares C, Ishii S (2001) The Ski protein family is required for MeCP2-mediated transcriptional repression. J Biol Chem 276:34115-34121. (Pubitemid 37384641)
43. Kudwa AE, Bodo C, Gustafsson JA, Rissman EF (2005) A previously uncharacterized role for estrogen receptor beta: defeminization of male brain and behavior. Proc Natl Acad Sci U S A 102:4608-4612. (Pubitemid 40397159)
44. Kurian JR, Bychowski ME, Forbes-Lorman RM, Auger CJ, Auger AP (2008) Mecp2 organizes juvenile social behavior in a sex-specific manner. J Neurosci 28:7137-7142.
45. Lauber AH, Mobbs CV, Muramatsu M, Pfaff DW (1991) Estrogen receptor messenger RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology 129:3180-3186.
46. Lavinsky RM, Jepsen K, Heinzel T, Torchia J, Mullen TM, Schiff R, Del-Rio AL, Ricote M, Ngo S, Gemsch J, Hilsenbeck SG, Osborne CK, Glass CK, Rosenfeld MG, Rose DW (1998) Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc Natl Acad Sci U S A 95:2920-2925. (Pubitemid 28135830)
47. Li E (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 3:662-673. (Pubitemid 34984255)
48. Lubin FD, Roth TL, Sweatt JD (2008) Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J Neurosci 28: 10576-10586.
49. Maerkel K, Durrer S, Henseler M, Schlumpf M, Lichtensteiger W (2007) Sexually dimorphic gene regulation in brain as a target for endocrine disrupters: developmental exposure of rats to 4-methyl benzylidene camphor. Toxicol Appl Pharmacol 218:152-165. (Pubitemid 46177168)
50. McCarthy MM (2008) Estradiol and the developing brain. Physiol Rev 88: 91-124.
51. McCarthy MM, de Vries GJ, Forger NG (2009) Sexual differentiation of the brain: mode, mechanisms, and meaning. In: Hormones, brain and behavior, Vol 3, Ed 2 (Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds), pp 1707-1744. San Diego: Academic.
52. McGowan PO, Sasaki A, D'Alessio AC, Dymov S, Labonté B, Szyf M, Turecki G, Meaney MJ (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12:342-348.
53. Menegola J, Steppe M, Schapoval EE (2007) Dissolution test for citalopram in tablets and comparison of in vitro dissolution profiles. Eur J Pharm Biopharm 67:524-530. (Pubitemid 47211896)
54. Moore CL (1992) The role of maternal stimulation in the development of sexual behavior and its neural basis. Ann N Y Acad Sci 662:160-177.
55. Murray EK, Hien A, de Vries GJ, Forger NG (2009a) Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis. Endocrinology 150:4241-4247.
56. Murray EK, Fernandez JL, Forger NG, De Vries GJ (2009b) Effect of perinatal HDAC inhibitor administration on sexual differentiation of the vasopressin innervation in the mouse brain. Soc Neurosci Abstr 35:666.3.
57. Naftolin F, Ryan KJ, Davies IJ, Reddy VV, Flores F, Petro Z, Kuhn M, White RJ, Takaoka Y, Wolin L (1975) The formation of estrogens by central neuroendocrine tissues. Recent Prog Horm Res 31:295-319.
58. Nagarajan RP, Hogart AR, Gwye Y, Martin MR, LaSalle JM (2006) Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics 1:e1-e11.
59. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389. (Pubitemid 28269714)
60. Olioff M, Stewart J (1978) Sex differences in the play behavior of prepubescent rats. Physiol Behav 20:113-115. (Pubitemid 8298884)
61. Ottaviano YL, Issa JP, Parl FF, Smith HS, Baylin SB, Davidson NE (1994) Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 54:2552-2555. (Pubitemid 24173735)
62. Parente LB, Aguila MB, Mandarim-de-Lacerda CA (2008) Deleterious effects of high-fat diet on perinatal and postweaning periods in adult rat offspring. Clin Nutr 27:623-634.
63. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjöström M, Golding J (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14:159-166. (Pubitemid 43135858)
64. Pfaff D, Keiner M (1973) Atlas of estradiol concentrating cells in the central nervous system of the female rat. J Comp Neurol 151:121-158.
65. Pfaff DW, Brooks PJ, Funabashi T, Pfaus JG, Mobbs CV (1992) Gene memory in neuroendocrine and behavioural systems. Ciba Found Symp 168: 165-183; discussion 183-186.
66. Pinheiro AR, Salvucci ID, Aguila MB, Mandarim-de-Lacerda CA (2008) Protein restriction during gestation and/or lactation causes adverse transgenerational effects on biometry and glucose metabolism in F1 and F2 progenies of rats. Clin Sci (Lond) 114:381-392.
67. Prewitt AK, Wilson ME (2007) Changes in estrogen receptor-alpha mRNA in the mouse cortex during development. Brain Res 1134:62-69.
68. Rhees RW, Lephart ED, Eliason D (2001) Effects of maternal separation during early postnatal development on male sexual behavior and female reproductive function. Behav Brain Res 123:1-10.
69. Sasaki M, Tanaka Y, Perinchery G, Dharia A, Kotcherguina I, Fujimoto S, Dahiya R (2002) Methylation and inactivation of estrogen, progesterone, and androgen receptors in prostate cancer. J Natl Cancer Inst 94:384-390. (Pubitemid 34257482)
70. Shughrue PJ, Lane MV, Merchenthaler I (1997) Comparative distribution of estrogen receptor-alpha and beta mRNA in the rat central nervous system. J Comp Neurol 388:507-525. (Pubitemid 27481288)
71. Skinner MK, Anway MD, Savenkova MI, Gore AC, Crews D (2008) Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS One 3:e3745.
72. Speert DB, Konkle AT, Zup SL, Schwarz JM, Shiroor C, Taylor ME, McCarthy MM (2007) Focal adhesion kinase and paxillin: novel regulators of brain sexual differentiation? Endocrinology 148:3391-3401.
73. Spencer TE, Jenster G, Burcin MM, Allis CD, Zhou J, Mizzen CA, McKenna NJ, Onate SA, Tsai SY, Tsai MJ, O'Malley BW (1997) Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389:194-198. (Pubitemid 27400603)
74. Thamotharan M, Garg M, Oak S, Rogers LM, Pan G, Sangiorgi F, Lee PW, Devaskar SU (2007) Transgenerational inheritance of the insulinresistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab 292:E1270-1279. (Pubitemid 46684594)
75. Tsai MJ, O'Malley BW (1994) Molecular mechanisms of action of steroid/ thyroid receptor superfamily members. Annu Rev Biochem 63:451-486. (Pubitemid 24218640)
76. Tsai HW, Grant PA, Rissman EF (2009) Sex differences in histone modifications in the neonatal mouse brain. Epigenetics 4:47-53.
77. Westberry JM, Prewitt AK, Wilson ME (2008) Epigenetic regulation of the estrogen receptor alpha promoter in the cerebral cortex following ischemia in male and female rats. Neuroscience 152:982-989.
78. Yamamoto Y, Carter CS, Cushing BS (2006) Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha. Neuroscience 137:157-164. (Pubitemid 43031483)
79. Yokosuka M, Okamura H, Hayashi S (1997) 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 389:81-93. (Pubitemid 27476202)
80. Yoon HG, Wong J (2006) 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 20:1048-1060.
81. Yoon HG, Chan DW, Reynolds AB, Qin J, Wong J (2003) N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso. Mol Cell 12:723-734. (Pubitemid 37222492)
82. Zambrano E, Martínez-Samayoa PM, Bautista CJ, Deás M, Guillén L, Rodríguez-González GL, Guzmán C, Larrea F, Nathanielsz PW (2005) Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol 566:225-236.