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3 - The Social Environment and the Epigenome

Published online by Cambridge University Press:  26 May 2010

Carol M. Worthman
Affiliation:
Emory University, Atlanta
Paul M. Plotsky
Affiliation:
Emory University, Atlanta
Daniel S. Schechter
Affiliation:
Hôpitaux Universitaires de Genève
Constance A. Cummings
Affiliation:
Foundation for Psychocultural Research, California
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Summary

Early life events both before and after birth have a long-lasting impact on physical and mental health trajectories later in life. Several lines of evidence point to the early origin of adult-onset diseases and psychiatric disorders. For example, nutritional restriction or maternal stress during pregnancy has been correlated with an increased risk of developing obesity, type 2 diabetes, and coronary heart disease (Ozanne & Constancia, 2007). Postnatally, adverse socioeconomic status during early childhood has been firmly linked to a susceptibility to the same conditions, as well as autoimmune disease, whereas childhood abuse is a major risk factor in the development of mood and anxiety disorders (Heim & Nemeroff, 2001; Kendler, Kuhn, & Prescott, 2004; see also Seraphin et al.; Nater & Heim, this volume). The critical question is, what are the mechanisms that mediate the effects of the early environment on our health and mental well-being, producing stable, long-lasting changes? It is now widely believed that epigenetics may constitute the mechanism that binds nurture and nature. “Epigenetics” is a polysemous term that in the present context refers to various mechanisms in the cell's nucleus that control genetic activity without altering the DNA sequence. The “epigenome” refers to the configuration of epigenetic modifiers of gene activation around the genome. Recent data suggest that epigenetic programming of gene expression profiles represented in the epigenome is sensitive to the early-life environment and that both the chemical and social environment early in life could affect the manner by which the genome is programmed by the epigenome.

Type
Chapter
Information
Formative Experiences
The Interaction of Caregiving, Culture, and Developmental Psychobiology
, pp. 53 - 81
Publisher: Cambridge University Press
Print publication year: 2010

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References

Barreto, G., Schafer, A., Marhold, J., Stach, D., Swaminathan, S. K., Handa, V., et al. (2007). Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature, 445(7128), 671–675.CrossRefGoogle ScholarPubMed
Baylin, S. B., Esteller, M., Rountree, M. R., Bachman, K. E., Schuebel, K., & Herman, J. G. (2001). Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Human Molecular Genetics, 10(7), 68–692.CrossRefGoogle Scholar
Beck, S., Olek, A., & Walter, J. (1999). From genomics to epigenomics: A loftier view of life. Nature Biotechnology, 17(12), 1144.CrossRefGoogle ScholarPubMed
Bergmann, A., & Lane, M. E. (2003). HIDden targets of microRNAs for growth control. Trends in Biochemical Sciences, 28(9), 461–463.CrossRefGoogle ScholarPubMed
Bhattacharya, S. K., Ramchandani, S., Cervoni, N., & Szyf, M. (1999). A mammalian protein with specific demethylase activity for mCpG DNA [See comments]. Nature, 397(6720), 579–583.CrossRefGoogle Scholar
Bourc'his, D., Xu, G. L., Lin, C. S., Bollman, B., & Bestor, T. H. (2001). Dnmt3L and the establishment of maternal genomic imprints. Science, 294(5551), 2536–2539.CrossRefGoogle ScholarPubMed
Bowcock, A. M. (1993). Molecular cloning of BRCA1: A gene for early onset familial breast and ovarian cancer. Breast Cancer Research and Treatment, 28(2), 121–135.CrossRefGoogle ScholarPubMed
Brown, S. E., & Szyf, M. (2007). Epigenetic programming of the rRNA promoter by MBD3. Molecular and Cellular Biology, 27(13), 4938–4952.CrossRefGoogle ScholarPubMed
Brunaud, L., Alberto, J. M., Ayav, A., Gerard, P., Namour, F., Antunes, L., et al. (2003). Effects of vitamin B12 and folate deficiencies on DNA methylation and carcinogenesis in rat liver. Clinical Chemistry and Laboratory Medicine, 41(8), 1012–1019.CrossRefGoogle ScholarPubMed
Bruniquel, D., & Schwartz, R. H. (2003). Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process. Nature Immunology, 4(3), 235–240.CrossRefGoogle ScholarPubMed
Bultman, S. J., Gebuhr, T. C., & Magnuson, T. (2005). A Brg1 mutation that uncouples ATPase activity from chromatin remodeling reveals an essential role for SWI/SNF-related complexes in beta-globin expression and erythroid development. Genes & Development, 19(23), 2849–2861.CrossRefGoogle ScholarPubMed
Cervoni, N., Detich, N., Seo, S. B., Chakravarti, D., & Szyf, M. (2002). The oncoprotein Set/TAF-1beta, an inhibitor of histone acetyltransferase, inhibits active demethylation of DNA, integrating DNA methylation and transcriptional silencing. Journal of Biological Chemistry, 277(28), 25026–25031.CrossRefGoogle ScholarPubMed
Cervoni, N., & Szyf, M. (2001). Demethylase activity is directed by histone acetylation. Journal of Biological Chemistry, 276(44), 40778–40787.CrossRefGoogle ScholarPubMed
Chamberlain, J. S., Boehnke, M., Frank, T. S., Kiousis, S., Xu, J., Guo, S. W., et al. (1993). BRCA1 maps proximal to D17S579 on chromosome 17q21 by genetic analysis. American Journal of Human Genetics, 52(4), 792–798.Google ScholarPubMed
Chen, T., Hevi, S., Gay, F., Tsujimoto, N., He, T., Zhang, B., et al. (2007). Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells [Letter]. Nature Genetics, 39(3), 391–396.CrossRefGoogle Scholar
Comb, M., & Goodman, H. M. (1990). CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2. Nucleic Acids Research, 18(13), 3975–3982.CrossRefGoogle ScholarPubMed
D'Alessio, A. C., & Szyf, M. (2006). Epigenetic tête-à-tête: The bilateral relationship between chromatin modifications and DNA methylation. Biochemistry and Cell Biology, 84(4), 463–476.Google ScholarPubMed
D'Alessio, A. C., Weaver, I. C., & Szyf, M. (2007). Acetylation-induced transcription is required for active DNA demethylation in methylation-silenced genes. Molecular and Cellular Biology, 27(21), 7462–7474.CrossRefGoogle ScholarPubMed
Detich, N., Hamm, S., Just, G., Knox, J. D., & Szyf, M. (2003). The methyl donor S-Adenosylmethionine inhibits active demethylation of DNA: A candidate novel mechanism for the pharmacological effects of S-Adenosylmethionine. Journal of Biological Chemistry, 278(23), 20812–20820.CrossRefGoogle ScholarPubMed
Di Croce, L., Raker, V. A., Corsaro, M., Fazi, F., Fanelli, M., Faretta, M., et al. (2002). Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science, 295(5557), 1079–1082.CrossRefGoogle ScholarPubMed
Eckhardt, F., Lewin, J., Cortese, R., Rakyan, V. K., Attwood, J., Burger, M., et al. (2006). DNA methylation profiling of human chromosomes 6, 20 and 22. Nature Genetics, 38(12), 1378–1385.CrossRefGoogle ScholarPubMed
Finch, J. T., Lutter, L. C., Rhodes, D., Brown, R. S., Rushton, B., Levitt, M., et al. (1977). Structure of nucleosome core particles of chromatin. Nature, 269(5623), 29–36.CrossRefGoogle ScholarPubMed
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science, 286(5442), 1155–1158.CrossRefGoogle ScholarPubMed
Fujita, N., Takebayashi, S., Okumura, K., Kudo, S., Chiba, T., Saya, H., et al. (1999). Methylation-mediated transcriptional silencing in euchromatin by methyl-CpG binding protein MBD1 isoforms. Molecular and Cellular Biology, 19(9), 6415–6426.CrossRefGoogle ScholarPubMed
Fuks, F., Burgers, W. A., Brehm, A., Hughes-Davies, L., & Kouzarides, T. (2000). DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nature Genetics, 24(1), 88–91.CrossRefGoogle ScholarPubMed
Fuks, F., Hurd, P. J., Wolf, D., Nan, X., Bird, A. P., & Kouzarides, T. (2003). The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. Journal of Biological Chemistry, 278(6), 4035–4040.CrossRefGoogle ScholarPubMed
Goto, K., Numata, M., Komura, J. I., Ono, T., Bestor, T. H., & Kondo, H. (1994). Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice. Differentiation, 56(1–2), 39–44.CrossRefGoogle ScholarPubMed
Groop, L., & Lyssenko, V. (2008). Genes and type 2 diabetes mellitus. Current Diabetes Reports, 8(3), 192–197.CrossRefGoogle ScholarPubMed
Heim, C., & Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: Preclinical and clinical studies. Biological Psychiatry, 49, 1023–1039.CrossRefGoogle ScholarPubMed
Hendrich, B., & Bird, A. (1998). Identification and characterization of a family of mammalian methyl-CpG binding proteins. Molecular and Cellular Biology, 18(11), 6538–6547.CrossRefGoogle ScholarPubMed
Henikoff, S., McKittrick, E., & Ahmad, K. (2004). Epigenetics, histone H3 variants, and the inheritance of chromatin states. Cold Spring Harbor Symposia on Quantitative Biology, 69, 235–243.CrossRefGoogle ScholarPubMed
Inamdar, N. M., Ehrlich, K. C., & Ehrlich, M. (1991). CpG methylation inhibits binding of several sequence-specific DNA-binding proteins from pea, wheat, soybean and cauliflower. Plant Molecular Biology, 17(1), 111–123.CrossRefGoogle ScholarPubMed
Jackson, J. P., Lindroth, A. M., Cao, X., & Jacobsen, S. E. (2002). Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature, 416(6880), 556–560.CrossRefGoogle ScholarPubMed
Jenuwein, T. (2001). Re-SET-ting heterochromatin by histone methyltransferases. Trends in Cell Biology, 11(6), 266–273.CrossRefGoogle ScholarPubMed
Jenuwein, T., & Allis, C. D. (2001). Translating the histone code. Science, 293(5532), 1074–1080.CrossRefGoogle ScholarPubMed
Jost, J. P. (1993). Nuclear extracts of chicken embryos promote an active demethylation of DNA by excision repair of 5-methyldeoxycytidine. Proceedings of the National Academy of Sciences of the United States of America, 90(10), 4684–4688.CrossRefGoogle ScholarPubMed
Ke, X., Lei, Q., James, S. J., Kelleher, S. L., Melnyk, S., Jernigan, S., et al. (2006). Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiological Genomics, 25(1), 16–28.CrossRefGoogle ScholarPubMed
Kendler, K. S., Kuhn, J. W., & Prescott, C. A. (2004). Childhood sexual abuse, stressful life events and risk for major depression in women. Psychological Medicine, 34, 1475–1482.CrossRefGoogle ScholarPubMed
Kersh, E. N., Fitzpatrick, D. R., Murali-Krishna, K., Shires, J., Speck, S. H., Boss, J. M., et al. (2006). Rapid Demethylation of the IFN-{gamma} Gene Occurs in Memory but Not Naive CD8 T Cells. Journal of Immunology, 176(7), 4083–4093.CrossRefGoogle Scholar
Kramer, O. H., Gottlicher, M., & Heinzel, T. (2001). Histone deacetylase as a therapeutic target. Trends in Endocrinology and Metabolism, 12(7), 294–300.CrossRefGoogle ScholarPubMed
Kuo, M. H., & Allis, C. D. (1998). Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays, 20(8), 615–626.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., & Jenuwein, T. (2001). Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature, 410(6824), 116–120.CrossRefGoogle ScholarPubMed
Lee, D. Y., Hayes, J. J., Pruss, D., & Wolffe, A. P. (1993). A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell, 72(1), 73–84.CrossRefGoogle ScholarPubMed
Levenson, J. M., & Sweatt, J. D. (2005). Epigenetic mechanisms in memory formation. Nature Reveiews Neuroscience, 6, 108–118.CrossRefGoogle ScholarPubMed
Levenson, J. M., Roth, T. L., Lubin, F. D., Miller, C. A., Huang, I. C., Desai, P., et al. (2006). Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. Journal of Biological Chemistry, 281(23), 15763–15773.CrossRefGoogle ScholarPubMed
Li, E., Bestor, T. H., & Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell, 69(6), 915–926.CrossRefGoogle ScholarPubMed
Lichtenstein, M., Keini, G., Cedar, H., & Bergman, Y. (1994). B cell-specific demethylation: A novel role for the intronic kappa chain enhancer sequence. Cell, 76(5), 913–923.CrossRefGoogle ScholarPubMed
Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., et al. (1997). Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science, 277(5332), 1659–1662.CrossRefGoogle ScholarPubMed
Lucarelli, M., Fuso, A., Strom, R., & Scarpa, S. (2001). The dynamics of myogenin site-specific demethylation is strongly correlated with its expression and with muscle differentiation. Journal of Biological Chemistry, 276(10), 7500–7506.CrossRefGoogle ScholarPubMed
MacLennan, N. K., James, S. J., Melnyk, S., Piroozi, A., Jernigan, S., Hsu, J. L., et al. (2004). Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiological Genomics, 18(1), 43–50.CrossRefGoogle ScholarPubMed
McGowan, P. O., Sasaki, A., Huang, T. C., Unterberger, A., Suderman, M., Ernst, C., et al. (2008). Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain. PLoS One, 3(5), e2085.CrossRefGoogle ScholarPubMed
McGowan, P. O., Sasaki, A., D'Alessio, A. C., Dymov, S., Labonté, B., Szyf, M., et al. (2009). Epigenetic regulation of the glucocorticoid receptor in human brain associates with child abuse. Nature Neuroscience, 12, 342–348.CrossRefGoogle Scholar
Meaney, M. J., & Szyf, M. (2005). Maternal care as a model for experience-dependent chromatin plasticity?Trends in Neurosciences, 28(9), 456–463.CrossRefGoogle Scholar
Metivier, R., Gallais, R., Tiffoche, C., Le Peron, C., Jurkowska, R. Z., Carmouche, R. P., et al. (2008). Cyclical DNA methylation of a transcriptionally active promoter. Nature, 452(7183), 45–50.CrossRefGoogle ScholarPubMed
Miller, C. A., & Sweatt, J. D. (2007). Covalent modification of DNA regulates memory formation. Neuron, 53(6), 857–869.CrossRefGoogle ScholarPubMed
Nan, X., Campoy, F. J., & Bird, A. (1997). MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell, 88(4), 471–481.CrossRefGoogle ScholarPubMed
Neel, J. V., & Falls, H. F. (1951). The rate of mutation of the gene responsible for retinoblastoma in man. Science, 114(2964), 419–422.CrossRefGoogle ScholarPubMed
Ng, H. H., Zhang, Y., Hendrich, B., Johnson, C. A., Turner, B. M., Erdjument-Bromage, H., et al. (1999). MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex [See comments]. Nature Genetics, 23(1), 58–61.CrossRefGoogle Scholar
Ogryzko, V. V., Schiltz, R. L., Russanova, V., Howard, B. H., & Nakatani, Y. (1996). The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell, 87(5), 953–959.CrossRefGoogle ScholarPubMed
Okano, M., Bell, D. W., Haber, D. A., & Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell, 99(3), 247–257.CrossRefGoogle Scholar
Okano, M., Xie, S., & Li, E. (1998). Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases [Letter]. Nature Genetics, 19(3), 219–220.CrossRefGoogle Scholar
Ozanne, S. E., & Constancia, M. (2007). Mechanisms of disease: The developmental origins of disease and the role of the epigenotype. Nature Clinical Practice Endocrinology & Metabolism, 3(7), 539–546.CrossRefGoogle ScholarPubMed
Perry, M., & Chalkley, R. (1982). Histone acetylation increases the solubility of chromatin and occurs sequentially over most of the chromatin: A novel model for the biological role of histone acetylation. Journal of Biological Chemistry, 257(13), 7336–7347.Google ScholarPubMed
Pogribny, I. P., Miller, B. J., & James, S. J. (1997). Alterations in hepatic p53 gene methylation patterns during tumor progression with folate/methyl deficiency in the rat. Cancer Letters, 115(1), 31–38.CrossRefGoogle ScholarPubMed
Qiu, J. (2006). Epigenetics: Unfinished symphony. Nature, 441, 143–145.CrossRefGoogle ScholarPubMed
Ramchandani, S., Bhattacharya, S. K., Cervoni, N., & Szyf, M. (1999a). DNA methylation is a reversible biological signal. Proceedings of the National Academy of Sciences of the United States of America, 96(11), 6107–6112.CrossRefGoogle ScholarPubMed
Ramchandani, S., Bhattacharya, S. K., Cervoni, N., & Szyf, M. (1999b). DNA methylation is a reversible biological signal [See comments]. Proceedings of the National Academy of Sciences of the United States of America, 96(11), 6107–6112.CrossRefGoogle Scholar
Razin, A. (1998). CpG methylation, chromatin structure and gene silencing: A three-way connection. Embo Journal, 17(17), 4905–4908.CrossRefGoogle ScholarPubMed
Razin, A., & Cedar, H. (1977). Distribution of 5-methylcytosine in chromatin. Proceedings of the National Academy of Sciences of the United States of America, 74(7), 2725–2728.CrossRefGoogle ScholarPubMed
Razin, A., & Riggs, A. D. (1980). DNA methylation and gene function. Science, 210(4470), 604–610.CrossRefGoogle ScholarPubMed
Rountree, M. R., Bachman, K. E., & Baylin, S. B. (2000). DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nature Genetics, 25(3), 269–277.CrossRefGoogle Scholar
Sarma, K., & Reinberg, D. (2005). Histone variants meet their match. Nature Reviews Molecular Cell Biology, 6(2), 139–149.CrossRefGoogle ScholarPubMed
Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., et al. (2004). Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 119(7), 941–953.CrossRefGoogle ScholarPubMed
Shilatifard, A. (2006). Chromatin modifications by methylation and ubiquitination: Implications in the regulation of gene expression. Annual Review of Biochemistry, 75, 243–269.CrossRefGoogle ScholarPubMed
Simonini, M. V., Camargo, L. M., Dong, E., Maloku, E., Veldic, M., Costa, E., et al. (2006). The benzamide MS-275 is a potent, long-lasting brain region-selective inhibitor of histone deacetylases. Proceedings of the National Academy of Sciences of the United States of America, 103(5), 1587–1592.CrossRefGoogle ScholarPubMed
Sinclair, K. D., Allegrucci, C., Singh, R., Gardner, D. S., Sebastian, S., Bispham, J., et al. (2007). DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proceedings of the National Academy of Sciences of the United States of America, 104(49), 19351–19356.CrossRefGoogle ScholarPubMed
Sparkes, R. S., Murphree, A. L., Lingua, R. W., Sparkes, M. C., Field, L. L., Funderburk, S. J., et al. (1983). Gene for hereditary retinoblastoma assigned to human chromosome 13 by linkage to esterase D. Science, 219(4587), 971–973.CrossRefGoogle ScholarPubMed
Szyf, M. (2001). Towards a pharmacology of DNA methylation. Trends in Pharmacological Sciences, 22(7), 350–354.CrossRefGoogle ScholarPubMed
Szyf, M., McGowan, P., & Meaney, M. J. (2007). The social environment and the epigenome. Environmental and Molecular Mutagenesis, 49(1), 46–60.CrossRefGoogle Scholar
Tanzi, R. E. (1990). The Alzheimer disease-associated amyloid beta protein precursor gene and familial Alzheimer disease. Progress in Clinical Biological Research, 360, 187–199.Google ScholarPubMed
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007). Epigenetic regulation in psychiatric disorders. Nature Reviews Neuroroscience, 8, 355–376.CrossRefGoogle ScholarPubMed
Tsukada, Y., Fang, J., Erdjument-Bromage, H., Warren, M. E., Borchers, C. H., Tempst, P., et al. (2006). Histone demethylation by a family of JmjC domain-containing proteins. Nature, 439(7078), 811–816.CrossRefGoogle ScholarPubMed
Varga-Weisz, P. D., & Becker, P. B. (2006). Regulation of higher-order chromatin structures by nucleosome-remodelling factors. Current Opinion in Genetics & Development, 16(2), 151–156.CrossRefGoogle ScholarPubMed
Veldic, M., Guidotti, A., Maloku, E., Davis, J. M., & Costa, E. (2005). In psychosis, cortical interneurons overexpress DNA-methyltransferase 1. Proceedings of the National Academy of Sciences of the United States of America, 102(6), 2152–2157.CrossRefGoogle ScholarPubMed
Vilain, A., Apiou, F., Dutrillaux, B., & Malfoy, B. (1998). Assignment of candidate DNA methyltransferase gene (DNMT2) to human chromosome band 10p15.1 by in situ hybridization. Cytogenetics and Cell Genetics, 82(1–2), 120.Google ScholarPubMed
Vire, E., Brenner, C., Deplus, R., Blanchon, L., Fraga, M., Didelot, C., et al. (2005). The Polycomb group protein EZH2 directly controls DNA methylation [letter]. Nature, 439, 871–874.CrossRefGoogle Scholar
Vo, N., Klein, M. E., Varlamova, O., Keller, D. M., Yamamoto, T., Goodman, R. H., et al. (2005). A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proceedings of the National Academy of Sciences of the United States of America, 102(45), 16426–16431.CrossRefGoogle ScholarPubMed
Wade, P. A., Pruss, D., & Wolffe, A. P. (1997). Histone acetylation: Chromatin in action. Trends in Biochemical Sciences, 22(4), 128–132.CrossRefGoogle ScholarPubMed
Wainfan, E., Dizik, M., Stender, M., & Christman, J. K. (1989). Rapid appearance of hypomethylated DNA in livers of rats fed cancer-promoting, methyl-deficient diets. Cancer Research, 49(15), 4094–4097.Google ScholarPubMed
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7(8), 847–854.CrossRefGoogle ScholarPubMed
Weaver, I. C., Champagne, F. A., Brown, S. E., Dymov, S., Sharma, S., Meaney, M. J., et al. (2005). Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: Altering epigenetic marking later in life. Journal of Neuroscience, 25(47), 11045–11054.CrossRefGoogle ScholarPubMed
Weaver, I. C., D'Alessio, A. C., Brown, S. E., Hellstrom, I. C., Dymov, S., Sharma, S., et al. (2007). The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: Altering epigenetic marks by immediate-early genes. Journal of Neuroscience, 27(7), 1756–1768.CrossRefGoogle ScholarPubMed
Weaver, I. C., Meaney, M. J., & Szyf, M. (2006). Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proceedings of the National Academy of Sciences of the United States of America, 103(9), 3480–3485.CrossRefGoogle ScholarPubMed
Weidle, U. H., & Grossmann, A. (2000). Inhibition of histone deacetylases: A new strategy to target epigenetic modifications for anticancer treatment. Anticancer Research, 20(3A), 1471–1485.Google ScholarPubMed
Wolffe, A. P. (1996). Histone deacetylase: A regulator of transcription. Science, 272(5260), 371–372.CrossRefGoogle Scholar
Zhang, B., Pan, X., Cobb, G. P., & Anderson, T. A. (2007). microRNAs as oncogenes and tumor suppressors. Developmental Biology, 302(1), 1–12.CrossRefGoogle ScholarPubMed
Zhu, B., Zheng, Y., Hess, D., Angliker, H., Schwarz, S., Siegmann, M., et al. (2000). 5-methylcytosine-DNA glycosylase activity is present in a cloned G/T mismatch DNA glycosylase associated with the chicken embryo DNA demethylation complex. Proceedings of the National Academy of Sciences of the United States of America, 97(10), 5135–5139.CrossRefGoogle Scholar

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