Epigenetics meets endocrinology.

Although genetics determines endocrine phenotypes, it cannot fully explain the great variability and reversibility of the system in response to environmental changes. Evidence now suggests that epigenetics, i.e. heritable but reversible changes in gene function without changes in nucleotide sequence, links genetics and environment in shaping endocrine function. Epigenetic mechanisms, including DNA methylation, histone modification, and microRNA, partition the genome into active and inactive domains based on endogenous and exogenous environmental changes and developmental stages, creating phenotype plasticity that can explain interindividual and population endocrine variability. We will review the current understanding of epigenetics in endocrinology, specifically, the regulation by epigenetics of the three levels of hormone action (synthesis and release, circulating and target tissue levels, and target-organ responsiveness) and the epigenetic action of endocrine disruptors. We will also discuss the impacts of hormones on epigenetics. We propose a three-dimensional model (genetics, environment, and developmental stage) to explain the phenomena related to progressive changes in endocrine functions with age, the early origin of endocrine disorders, phenotype discordance between monozygotic twins, rapid shifts in disease patterns among populations experiencing major lifestyle changes such as immigration, and the many endocrine disruptions in contemporary life. We emphasize that the key for understanding epigenetics in endocrinology is the identification, through advanced high-throughput screening technologies, of plasticity genes or loci that respond directly to a specific environmental stimulus. Investigations to determine whether epigenetic changes induced by today's lifestyles or environmental 'exposures' can be inherited and are reversible should open doors for applying epigenetics to the prevention and treatment of endocrine disorders.

[1]  Xiaowei Wang,et al.  Systematic identification of microRNA functions by combining target prediction and expression profiling , 2006, Nucleic acids research.

[2]  G. Reaven Role of insulin resistance in human disease (syndrome X): an expanded definition. , 1993, Annual review of medicine.

[3]  T. Rauch,et al.  Insulin Gene Expression Is Regulated by DNA Methylation , 2009, PloS one.

[4]  H. Tournaye,et al.  [Genetics and male infertility]. , 2009, Verhandelingen - Koninklijke Academie voor Geneeskunde van Belgie.

[5]  A. B. Reddy,et al.  Genetic and molecular analysis of the central and peripheral circadian clockwork of mice. , 2007, Cold Spring Harbor symposia on quantitative biology.

[6]  Long-Cheng Li,et al.  MethPrimer: designing primers for methylation PCRs , 2002, Bioinform..

[7]  Polybrominated Diphenyl Ethers ( PBDEs ) Fall 2004 , 2022 .

[8]  D. Iliopoulos,et al.  Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention , 2007, Annals of the rheumatic diseases.

[9]  J. W. Thornton Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[10]  G. Lal,et al.  Epigenetic mechanisms of regulation of Foxp3 expression. , 2009, Blood.

[11]  M. Reis-Henriques,et al.  Polycyclic aromatic hydrocarbons inhibit in vitro ovarian steroidogenesis in the flounder (Platichthys flesus L.). , 2000, Aquatic toxicology.

[12]  A. Pang,et al.  Aberrant promoter methylation of the retinoic acid receptor alpha gene in acute promyelocytic leukemia , 2005, Leukemia.

[13]  J. Vanselow,et al.  DNA methylation of placenta-specific Cyp19 promoters of cattle and sheep. , 2008, Experimental and clinical endocrinology & diabetes : official journal, German Society of Endocrinology [and] German Diabetes Association.

[14]  J. Stockman Inheritance of a Cancer-Associated MLH1 Germ-Line Epimutation , 2008 .

[15]  J. Newell-Price Proopiomelanocortin gene expression and DNA methylation: implications for Cushing's syndrome and beyond. , 2003, The Journal of endocrinology.

[16]  Guangcun Huang,et al.  Over‐expressed microRNA‐27a and 27b influence fat accumulation and cell proliferation during rat hepatic stellate cell activation , 2009, FEBS letters.

[17]  P. Bennett,et al.  Excessive obesity in offspring of Pima Indian women with diabetes during pregnancy. , 1983, The New England journal of medicine.

[18]  N. Sugino,et al.  DNA methyltransferase expression in the human endometrium: down-regulation by progesterone and estrogen. , 2009, Human reproduction.

[19]  C. Kuzawa,et al.  Developmental Origins of Adult Function and Health: Evolutionary Hypotheses , 2009 .

[20]  A. Gilman,et al.  G proteins: transducers of receptor-generated signals. , 1987, Annual review of biochemistry.

[21]  Leena Peltonen,et al.  Global Transcript Profiles of Fat in Monozygotic Twins Discordant for BMI: Pathways behind Acquired Obesity , 2008, PLoS medicine.

[22]  H. Shibuya,et al.  DNA demethylation in hormone-induced transcriptional derepression , 2009, Nature.

[23]  G. Latini,et al.  Influence of environment on insulin sensitivity. , 2009, Environment international.

[24]  Piero Carninci,et al.  Molecular mechanisms of pituitary organogenesis: In search of novel regulatory genes , 2010, Molecular and Cellular Endocrinology.

[25]  S. Patra,et al.  Epigenetic DNA(Cytosine5Carbon) Modifications: 5Aza2 'deoxycytidine and DNADemethylation , 2009 .

[26]  C. Peterson,et al.  Histones and histone modifications , 2004, Current Biology.

[27]  I. Leav,et al.  Dynamic regulation of estrogen receptor-beta expression by DNA methylation during prostate cancer development and metastasis. , 2004, The American journal of pathology.

[28]  M. Tusié-Luna,et al.  Mutation Analysis in Patients with Congenital Adrenal Hyperplasia in the Spanish Population: Identification of Putative Novel Steroid 21-Hydroxylase Deficiency Alleles Associated with the Classic Form of the Disease , 1999, Human Heredity.

[29]  P. Laird,et al.  Widespread Epigenetic Abnormalities Suggest a Broad DNA Methylation Erasure Defect in Abnormal Human Sperm , 2007, PloS one.

[30]  M. Fang,et al.  Hypermethylation-associated inactivation of retinoic acid receptor beta in human esophageal squamous cell carcinoma. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[31]  H. Haisma,et al.  Histone acetyl transferases as emerging drug targets. , 2009, Drug discovery today.

[32]  C. Klinge Estrogen Regulation of MicroRNA Expression , 2009, Current genomics.

[33]  David Crews,et al.  Resurrecting the Ancestral Steroid Receptor: Ancient Origin of Estrogen Signaling , 2003, Science.

[34]  X. Zhang,et al.  AP-2 regulates the transcription of estrogen receptor (ER)-β by acting through a methylation hotspot of the 0N promoter in prostate cancer cells , 2007, Oncogene.

[35]  Richard J Jackson,et al.  How Do MicroRNAs Regulate Gene Expression? , 2007, Science's STKE.

[36]  G. Vassart,et al.  Possible non-Mendelian mechanisms of thyroid dysgenesis. , 2007, Endocrine development.

[37]  I. Weaver,et al.  Reversal of Maternal Programming of Stress Responses in Adult Offspring through Methyl Supplementation: Altering Epigenetic Marking Later in Life , 2005, The Journal of Neuroscience.

[38]  P. Georgel,et al.  Genetic and epigenetic regulations of prostate cancer by genistein. , 2009, Drug news & perspectives.

[39]  H. Morris,et al.  Hydroxylase enzymes of the vitamin D pathway: expression, function, and regulation. , 2002, Annual review of nutrition.

[40]  R. Jansen Endocrine response in the fallopian tube. , 1984, Endocrine reviews.

[41]  O. Kirak,et al.  Regulation of progenitor cell proliferation and granulocyte function by microRNA-223 , 2008, Nature.

[42]  A. Bradley,et al.  Identification of mammalian microRNA host genes and transcription units. , 2004, Genome research.

[43]  Tatjana Buklijas,et al.  Epigenetic mechanisms that underpin metabolic and cardiovascular diseases , 2009, Nature Reviews Endocrinology.

[44]  I. Kourides,et al.  Expression of Chorionic Gonadotropin α- and β-Genes in Normal and Neoplastic Human Tissues: Relationship to Deoxyribonucleic Acid Structure* , 1985 .

[45]  L. Ekström,et al.  Regulation and expression of human CYP7B1 in prostate: Overexpression of CYP7B1 during progression of prostatic adenocarcinoma , 2007, The Prostate.

[46]  Wei-wen Sun,et al.  Assessment of the neurotoxic mechanisms of decabrominated diphenyl ether (PBDE-209) in primary cultured neonatal rat hippocampal neurons includes alterations in second messenger signaling and oxidative stress. , 2010, Toxicology letters.

[47]  L. Groop,et al.  Epigenetics: A Molecular Link Between Environmental Factors and Type 2 Diabetes , 2009, Diabetes.

[48]  M. Tonacchera,et al.  Genetics and phenomics of hypothyroidism and thyroid dys- and agenesis due to PAX8 and TTF1 mutations , 2010, Molecular and Cellular Endocrinology.

[49]  T. Clarkson,et al.  Environmental contaminants in the food chain. , 1995, The American journal of clinical nutrition.

[50]  M. Bieda,et al.  Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes , 2007, Proceedings of the National Academy of Sciences.

[51]  D. Barlow,et al.  Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal , 1993, Cell.

[52]  K. Knudsen,et al.  Partners in crime: deregulation of AR activity and androgen synthesis in prostate cancer , 2010, Trends in Endocrinology & Metabolism.

[53]  Kathleen M. Scully,et al.  Pituitary Development: Regulatory Codes in Mammalian Organogenesis , 2002, Science.

[54]  Xiangyin Kong,et al.  Hypomethylation in the promoter region of POMC gene correlates with ectopic overexpression in thymic carcinoids. , 2005, The Journal of endocrinology.

[55]  S. Safe,et al.  Inhibitory aryl hydrocarbon receptor-estrogen receptor alpha cross-talk and mechanisms of action. , 2003, Chemical research in toxicology.

[56]  C. Tohyama,et al.  Exposure of Mouse Preimplantation Embryos to 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) Alters the Methylation Status of Imprinted Genes H19 and Igf21 , 2004, Biology of reproduction.

[57]  C. Wijmenga,et al.  The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[58]  J. Vanselow,et al.  DNA Methylation Is Not Involved in Preovulatory Down-Regulation of CYP11A1, HSD3B1, and CYP19A1 in Bovine Follicles but May Have a Role in Permanent Silencing of CYP19A1 in Large Granulosa Lutein Cells1 , 2010, Biology of reproduction.

[59]  Dan J Stein Oxytocin and Vasopressin: Social Neuropeptides , 2009, CNS Spectrums.

[60]  A. Sehgal,et al.  Regulation of CLOCK and MOP4 by Nuclear Hormone Receptors in the Vasculature A Humoral Mechanism to Reset a Peripheral Clock , 2001, Cell.

[61]  S. Sikka,et al.  Endocrine disruptors and estrogenic effects on male reproductive axis. , 2008, Asian journal of andrology.

[62]  A. Bird,et al.  Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals , 2003, Nature Genetics.

[63]  M. Widschwendter,et al.  MeCP2 and MBD2 expression in human neoplastic and non-neoplastic breast tissue and its association with oestrogen receptor status , 2003, British Journal of Cancer.

[64]  C. Naughton,et al.  Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility , 2006 .

[65]  B. Jégou,et al.  Role of DNA methylation in the tissue-specific expression of the CYP17A1 gene for steroidogenesis in rodents. , 2009, The Journal of endocrinology.

[66]  J. Craigon,et al.  DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status , 2007, Proceedings of the National Academy of Sciences.

[67]  R. Jirtle,et al.  Environmental epigenomics and disease susceptibility , 2007, Nature Reviews Genetics.

[68]  C. Allis,et al.  Epigenetics: A Landscape Takes Shape , 2007, Cell.

[69]  Johannes Kornhuber,et al.  Epigenetic regulation and gene expression of vasopressin and atrial natriuretic peptide in alcohol withdrawal , 2009, Psychoneuroendocrinology.

[70]  P. Bingley,et al.  Reanalysis of twin studies suggests that diabetes is mainly genetic , 2001, BMJ : British Medical Journal.

[71]  G. Abecasis,et al.  A Genome-Wide Association Study of Type 2 Diabetes in Finns Detects Multiple Susceptibility Variants , 2007, Science.

[72]  Xiaoqing Tang,et al.  Identification of glucose-regulated miRNAs from pancreatic {beta} cells reveals a role for miR-30d in insulin transcription. , 2009, RNA.

[73]  S. Kato,et al.  RETRACTED: 1α,25(OH)2D3-induced DNA methylation suppresses the human CYP27B1 gene , 2007, Molecular and Cellular Endocrinology.

[74]  J. Millam,et al.  Phytoestrogens and avian reproduction: Exploring the evolution and function of phytoestrogens and possible role of plant compounds in the breeding ecology of wild birds. , 2009, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[75]  Jef D Boeke,et al.  Regulated nucleosome mobility and the histone code , 2004, Nature Structural &Molecular Biology.

[76]  N. Yang,et al.  Polynuclear Aromatic Hydrocarbons, Steroids and Carcinogenesis , 1961, Science.

[77]  A. Baccarelli,et al.  Global DNA Hypomethylation Is Associated with High Serum-Persistent Organic Pollutants in Greenlandic Inuit , 2008, Environmental health perspectives.

[78]  C. Tepper,et al.  microRNAs and prostate cancer , 2008, Journal of cellular and molecular medicine.

[79]  P. Ladenson,et al.  Methylation of the thyroid-stimulating hormone receptor gene in epithelial thyroid tumors: a marker of malignancy and a cause of gene silencing. , 2003, Cancer research.

[80]  E. Rimm,et al.  Retrospective analysis of birth weight and prostate cancer in the Health Professionals Follow-up Study. , 1998, American journal of epidemiology.

[81]  François Fuks,et al.  DNA methylation and histone modifications: teaming up to silence genes. , 2005, Current opinion in genetics & development.

[82]  C. Hughes,et al.  Phytochemical mimicry of reproductive hormones and modulation of herbivore fertility by phytoestrogens. , 1988, Environmental health perspectives.

[83]  J. McLachlan,et al.  Epigenetics, evolution, endocrine disruption, health, and disease. , 2006, Endocrinology.

[84]  R. Dahiya,et al.  Inactivation of the human androgen receptor gene is associated with CpG hypermethylation in uterine endometrial cancer , 2000, Molecular carcinogenesis.

[85]  M. Webber,et al.  Tumor Suppressor Gene Inactivation during Cadmium-Induced Malignant Transformation of Human Prostate Cells Correlates with Overexpression of de Novo DNA Methyltransferase , 2007, Environmental health perspectives.

[86]  Yiliang Zhang,et al.  Allele-specific targeting of hsa-miR-657 to human IGF2R creates a potential mechanism underlying the association of ACAA-insertion/deletion polymorphism with type 2 diabetes. , 2008, Biochemical and biophysical research communications.

[87]  M. Uzumcu,et al.  Fetal and neonatal exposure to the endocrine disruptor methoxychlor causes epigenetic alterations in adult ovarian genes. , 2009, Endocrinology.

[88]  S. Ehrlich,et al.  Promoter specific DNA methylation and gene expression of POMC in acutely underweight and recovered patients with anorexia nervosa. , 2010, Journal of psychiatric research.

[89]  C. Lintas,et al.  Neocortical RELN promoter methylation increases significantly after puberty , 2010, Neuroreport.

[90]  Ghazala Begum,et al.  Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. , 2010, Endocrinology.

[91]  P. Zielenkiewicz,et al.  Mammalian DNA methyltransferases. , 2006, Acta biochimica Polonica.

[92]  Luke O Dannenberg,et al.  Epigenetics of gene expression in human hepatoma cells: expression profiling the response to inhibition of DNA methylation and histone deacetylation , 2006, BMC Genomics.

[93]  M. Yatin,et al.  Restoration of iodide uptake in dedifferentiated thyroid carcinoma: relationship to human Na+/I-symporter gene methylation status. , 1999, The Journal of clinical endocrinology and metabolism.

[94]  N. Terakawa,et al.  An epigenetic disorder may cause aberrant expression of aromatase gene in endometriotic stromal cells. , 2008, Fertility and sterility.

[95]  W. Miller Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. , 2007, Biochimica et biophysica acta.

[96]  Shizhen Song,et al.  Effects of long-term low-dose cadmium exposure on genomic DNA methylation in human embryo lung fibroblast cells. , 2008, Toxicology.

[97]  M. Esteller Aberrant DNA methylation as a cancer-inducing mechanism. , 2005, Annual review of pharmacology and toxicology.

[98]  Adrian Bird,et al.  Perceptions of epigenetics , 2007, Nature.

[99]  T. Zacharewski,et al.  Dioxin Induces an Estrogen-Like, Estrogen Receptor-Dependent Gene Expression Response in the Murine Uterus , 2006, Molecular Pharmacology.

[100]  A. Jeltsch,et al.  Biochemistry and biology of mammalian DNA methyltransferases , 2004, Cellular and Molecular Life Sciences CMLS.

[101]  Zhongli Yang,et al.  Estrogen regulates DNA methyltransferase 3B expression in Ishikawa endometrial adenocarcinoma cells , 2009, Molecular Biology Reports.

[102]  T. Tollefsbol,et al.  Genistein depletes telomerase activity through cross‐talk between genetic and epigenetic mechanisms , 2009, International journal of cancer.

[103]  R. Evans,et al.  The steroid and thyroid hormone receptor superfamily. , 1988, Science.

[104]  D. Haber,et al.  DNA Methyltransferases Dnmt3a and Dnmt3b Are Essential for De Novo Methylation and Mammalian Development , 1999, Cell.

[105]  R. Lotan,et al.  Inactivation of retinoic acid receptor beta by promoter CpG hypermethylation in gastric cancer. , 2001, Differentiation; research in biological diversity.

[106]  H. Grönberg,et al.  Birth Characteristics and Risk of Prostate Cancer: the Contribution of Genetic Factors , 2009, Cancer Epidemiology, Biomarkers & Prevention.

[107]  H. Taylor,et al.  Hypermethylation of homeobox A10 by in utero diethylstilbestrol exposure: an epigenetic mechanism for altered developmental programming. , 2009, Endocrinology.

[108]  J. Veldhuis,et al.  Three-peptide control of pulsatile and entropic feedback-sensitive modes of growth hormone secretion: modulation by estrogen and aromatizable androgen. , 2003, Journal of pediatric endocrinology & metabolism : JPEM.

[109]  M. Mascini,et al.  Heavy Metals , 2019, Biomedical Journal of Scientific & Technical Research.

[110]  R. Dahiya,et al.  Hypermethylation can selectively silence multiple promoters of steroid receptors in cancers , 2003, Molecular and Cellular Endocrinology.

[111]  C. Caldas,et al.  Cancer genetics of epigenetic genes. , 2007, Human molecular genetics.

[112]  W L Miller,et al.  Molecular biology of steroid hormone synthesis. , 1988, Endocrine reviews.

[113]  M. Kokoska,et al.  Methylation status of genes in papillary thyroid carcinoma. , 2006, Archives of otolaryngology--head & neck surgery.

[114]  M. Schlumpf,et al.  Gene expression and estrogen sensitivity in rat uterus after developmental exposure to the polybrominated diphenylether PBDE 99 and PCB. , 2006, Toxicology.

[115]  Susan C. Tilton,et al.  Genomic Profiling Reveals an Alternate Mechanism for Hepatic Tumor Promotion by Perfluorooctanoic Acid in Rainbow Trout , 2008, Environmental health perspectives.

[116]  H. Putter,et al.  DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. , 2009, Human molecular genetics.

[117]  L. Gray,et al.  Persistent DDT metabolite p,p'–DDE is a potent androgen receptor antagonist , 1995, Nature.

[118]  H. Kung,et al.  Interleukin-6 Regulates Androgen Synthesis in Prostate Cancer Cells , 2009, Clinical Cancer Research.

[119]  R. Sharpe,et al.  Bisphenol a and metabolic syndrome. , 2010, Endocrinology.

[120]  T. Wolfsberg Using the NCBI Map Viewer to Browse Genomic Sequence Data , 2003, Current protocols in human genetics.

[121]  M. Metzker Sequencing technologies — the next generation , 2010, Nature Reviews Genetics.

[122]  S. Schreiber,et al.  Significance of HDAC6 regulation via estrogen signaling for cell motility and prognosis in estrogen receptor-positive breast cancer , 2005, Oncogene.

[123]  G. Neri,et al.  Defective oxytocin function: a clue to understanding the cause of autism? , 2009, BMC medicine.

[124]  E. Rampersaud,et al.  Investigating parent of origin effects in studies of type 2 diabetes and obesity. , 2008, Current Diabetes Reviews.

[125]  K. Michels,et al.  Role of birthweight in the etiology of breast cancer , 2006, International journal of cancer.

[126]  M. Griswold,et al.  Site-Specific Methylation of the Promoter Alters Deoxyribonucleic Acid-Protein Interactions and Prevents Follicle-Stimulating Hormone Receptor Gene Transcription1 , 2001, Biology of reproduction.

[127]  K. Docherty,et al.  Insulin Gene Expression , 1999 .

[128]  E. Wilson,et al.  PERSISTENT DDT METABOLITE P, P'-DDE IS A POTENT ANDROGEN RECEPTOR ANTAGONIST , 1996 .

[129]  R. Holliday Mutations and epimutations in mammalian cells. , 1991, Mutation research.

[130]  Shuk-Mei Ho,et al.  4 Epigenetically Regulates Phosphodiesterase Type 4 Variant Increases Susceptibility to Prostate Carcinogenesis and Developmental Exposure to Estradiol and Bisphenol A , 2006 .

[131]  P. Boutros,et al.  microRNAs in adult rodent liver are refractory to dioxin treatment. , 2007, Toxicological sciences : an official journal of the Society of Toxicology.

[132]  Reid F. Thompson,et al.  Epigenetic basis for fetal origins of age-related disease. , 2010, Journal of women's health.

[133]  M. Medvedovic,et al.  Persistent hypomethylation in the promoter of nucleosomal binding protein 1 (Nsbp1) correlates with overexpression of Nsbp1 in mouse uteri neonatally exposed to diethylstilbestrol or genistein. , 2008, Endocrinology.

[134]  William Kong,et al.  Strategies for profiling MicroRNA expression , 2009, Journal of cellular physiology.

[135]  Tony Kouzarides,et al.  Reversing histone methylation , 2005, Nature.

[136]  P. Visscher,et al.  DNA methylation profiles in monozygotic and dizygotic twins , 2009, Nature Genetics.

[137]  P. Nelson,et al.  Maintenance of intratumoral androgens in metastatic prostate cancer: a mechanism for castration-resistant tumor growth. , 2008, Cancer research.

[138]  D. Tindall,et al.  Androgen deprivation increases p300 expression in prostate cancer cells. , 2007, Cancer research.

[139]  R. Dahiya,et al.  Genistein reverses hypermethylation and induces active histone modifications in tumor suppressor gene B‐Cell translocation gene 3 in prostate cancer , 2009, Cancer.

[140]  D. Garabrant,et al.  Polychlorinated biphenyls and thyroid hormones in adults: a systematic review appraisal of epidemiological studies. , 2009, Chemosphere.

[141]  H. Adlercreutz Can rye intake decrease risk of human breast cancer? , 2010, Food & nutrition research.

[142]  C. Allis,et al.  Signaling to Chromatin through Histone Modifications , 2000, Cell.

[143]  A. Friedl,et al.  Methylation of the androgen receptor minimal promoter silences transcription in human prostate cancer. , 2000, Cancer research.

[144]  R. Stöger In Vivo Methylation Patterns of the Leptin Promoter in Human and Mouse , 2006, Epigenetics.

[145]  V. Papadopoulos,et al.  Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action , 2010, Steroids.

[146]  F. Sato,et al.  Hypermethylation of the somatostatin promoter is a common, early event in human esophageal carcinogenesis , 2008, Cancer.

[147]  M. Manson,et al.  Dietary Chemopreventive Phytochemicals: Too Little or Too Much? , 2009, Cancer Prevention Research.

[148]  H. Schayek,et al.  Progression to metastatic stage in a cellular model of prostate cancer is associated with methylation of the androgen receptor gene and transcriptional suppression of the insulin-like growth factor-I receptor gene. , 2010, Experimental cell research.

[149]  A. Norman,et al.  The Vitamin D Receptor Is Present in Caveolae-Enriched Plasma Membranes and Binds 1α,25(OH)2-Vitamin D3 in Vivo and in Vitro , 2004 .

[150]  S. Moon,et al.  Relationships between the insulin-like growth factor I (IGF-I) receptor gene G3174A polymorphism, serum IGF-I levels, and bone mineral density in postmenopausal Korean women , 2008, Journal of Bone and Mineral Metabolism.

[151]  S. Giannini,et al.  Secondary hyperparathyroidism is associated with vitamin D receptor polymorphism and bone density after renal transplantation. , 2005, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[152]  R. Harvey,et al.  Polycyclic Aromatic Hydrocarbons , 1997 .

[153]  S. Ojeda,et al.  New concepts on the control of the onset of puberty. , 2010, Endocrine development.

[154]  S. Woods,et al.  Perinatal exposure to bisphenol-a and the development of metabolic syndrome in CD-1 mice. , 2010, Endocrinology.

[155]  M. Wabitsch,et al.  Leptin Gene Expression in Human Preadipocytes Is Switched on by Maturation-induced Demethylation of Distinct CpGs in Its Proximal Promoter* , 2002, The Journal of Biological Chemistry.

[156]  J. Strauss,et al.  Regulation of transcription of the steroidogenic acute regulatory protein (StAR) gene: temporal and spatial changes in transcription factor binding and histone modification , 2004, Molecular and Cellular Endocrinology.

[157]  C. Franceschi,et al.  Genes involved in immune response/inflammation, IGF1/insulin pathway and response to oxidative stress play a major role in the genetics of human longevity: the lesson of centenarians , 2005, Mechanisms of Ageing and Development.

[158]  Martin Widschwendter,et al.  Association of Breast Cancer DNA Methylation Profiles with Hormone Receptor Status and Response to Tamoxifen , 2004, Cancer Research.

[159]  Thorsten Heinzel,et al.  Nuclear receptors: overview and classification. , 2004, Current drug targets. Inflammation and allergy.

[160]  B. White,et al.  The Micro-Ribonucleic Acid (miRNA) miR-206 Targets the Human Estrogen Receptor-α (ERα) and Represses ERα Messenger RNA and Protein Expression in Breast Cancer Cell Lines , 2007 .

[161]  E. Lam,et al.  Expression of estrogen receptor beta isoforms in normal breast epithelial cells and breast cancer: regulation by methylation. , 2003, Oncogene.

[162]  J. Rastad,et al.  The vitamin D receptor (VDR) start codon polymorphism in primary hyperparathyroidism and parathyroid VDR messenger ribonucleic acid levels. , 1999, The Journal of clinical endocrinology and metabolism.

[163]  E. Simpson,et al.  Epigenetic mechanisms regulating CYP19 transcription in human breast adipose fibroblasts , 2010, Molecular and Cellular Endocrinology.

[164]  D. Carrell,et al.  The human sperm epigenome and its potential role in embryonic development. , 2010, Molecular human reproduction.

[165]  Liou Y Sun,et al.  Insulin-like growth factor-I stimulates histone H3 and H4 acetylation in the brain in vivo. , 2006, Endocrinology.

[166]  O. Meijer,et al.  MicroRNA 18 and 124a down-regulate the glucocorticoid receptor: implications for glucocorticoid responsiveness in the brain. , 2009, Endocrinology.

[167]  Q. Tao,et al.  DNA methyltransferase 3 B ( DNMT 3 B ) mutations in ICF syndrome lead to altered epigenetic modifications and aberrant expression of genes regulating development , neurogenesis and immune function , 2008 .

[168]  Peter Gluckman,et al.  Developmental plasticity and human health , 2004, Nature.

[169]  S. Bulun,et al.  CpG dinucleotide methylation of the CYP19 I.3/II promoter modulates cAMP-stimulated aromatase activity , 2008, Molecular and Cellular Endocrinology.

[170]  M. Ingelman-Sundberg,et al.  Molecular genetics and epigenetics of the cytochrome P450 gene family and its relevance for cancer risk and treatment , 2009, Human Genetics.

[171]  Paul D. Jones,et al.  Polybrominated Diphenyl Ethers (PBDEs) , 2005 .

[172]  H. Adami,et al.  Duration of gestation and prostate cancer risk in offspring. , 2000, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[173]  P. Bennett,et al.  Abnormal Glucose Tolerance During Pregnancy in Pima Indian Women: Long-Term Effects on Offspring , 1991, Diabetes.

[174]  J. Blaustein The Year in Neuroendocrinology. , 2010, Molecular endocrinology.

[175]  Sandya Liyanarachchi,et al.  Xenoestrogen-induced epigenetic repression of microRNA-9-3 in breast epithelial cells. , 2009, Cancer research.

[176]  A. Feinberg Phenotypic plasticity and the epigenetics of human disease , 2007, Nature.

[177]  Kelly M. McGarvey,et al.  PcG Proteins, DNA Methylation, and Gene Repression by Chromatin Looping , 2008, PLoS biology.

[178]  W. B. Archey,et al.  Increased CpG methylation of the estrogen receptor gene in BRCA1-linked estrogen receptor-negative breast cancers , 2002, Oncogene.

[179]  Anne H. O'Donnell,et al.  Mammalian cytosine methylation at a glance , 2009, Journal of Cell Science.

[180]  M. Musri,et al.  Chromatin and chromatin-modifying proteins in adipogenesis. , 2007, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[181]  Ronald H Laessig,et al.  Polybrominated diphenyl ethers (PBDEs): new pollutants-old diseases. , 2003, Clinical medicine & research.

[182]  Tetsuo Ito,et al.  A genome-wide search identifies epigenetic silencing of somatostatin, tachykinin-1, and 5 other genes in colon cancer. , 2006, Gastroenterology.

[183]  Qian Tao,et al.  DNA methyltransferase 3B (DNMT3B) mutations in ICF syndrome lead to altered epigenetic modifications and aberrant expression of genes regulating development, neurogenesis and immune function. , 2008, Human molecular genetics.

[184]  A. Shilatifard,et al.  An operational definition of epigenetics. , 2009, Genes & development.

[185]  M. Takeda,et al.  Low dose effects of dichlorodiphenyltrichloroethane (DDT) on gene transcription and DNA methylation in the hypothalamus of young male rats: implication of hormesis-like effects. , 2009, The Journal of toxicological sciences.

[186]  G. Prins Estrogen imprinting: when your epigenetic memories come back to haunt you. , 2008, Endocrinology.

[187]  D. Smiraglia,et al.  Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. , 2007, Developmental biology.

[188]  G. Veenstra,et al.  DNA methylation and methyl-CpG binding proteins: developmental requirements and function , 2009, Chromosoma.

[189]  F. Garrido,et al.  Distinct mechanisms of loss of IFN-gamma mediated HLA class I inducibility in two melanoma cell lines , 2007, BMC Cancer.

[190]  N. Tommerup,et al.  Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene , 1999, Nature.

[191]  R. Simmons Developmental origins of adult disease. , 2009, Pediatric clinics of North America.

[192]  J. Stengård,et al.  Concordance for Type 1 (insulin-dependent) and Type 2 (non-insulin-dependent) diabetes mellitus in a population-based cohort of twins in Finland , 1992, Diabetologia.

[193]  A. Ganesan,et al.  Epigenetic therapy: histone acetylation, DNA methylation and anti-cancer drug discovery. , 2009, Current cancer drug targets.

[194]  N. Kondo,et al.  miR-206 Expression is down-regulated in estrogen receptor alpha-positive human breast cancer. , 2009, Cancer research.

[195]  S. Pozzi,et al.  RAR-mediated epigenetic control of the cytochrome P450 Cyp26a1 in embryocarcinoma cells , 2006, Oncogene.

[196]  L. Gudas,et al.  Epigenetic Regulatory Mechanisms Distinguish Retinoic Acid-mediated Transcriptional Responses in Stem Cells and Fibroblasts* , 2010, The Journal of Biological Chemistry.

[197]  J. Rotchell,et al.  Estrogenic activity of cadmium, copper and zinc in the yeast estrogen screen. , 2009, Toxicology in vitro : an international journal published in association with BIBRA.

[198]  Deliang Tang,et al.  Relation of DNA Methylation of 5′-CpG Island of ACSL3 to Transplacental Exposure to Airborne Polycyclic Aromatic Hydrocarbons and Childhood Asthma , 2009, PloS one.

[199]  Y. Higashi,et al.  Distinct mechanisms of loss of estrogen receptor alpha gene expression in human breast cancer: methylation of the gene and alteration of trans-acting factors. , 2000, Carcinogenesis.

[200]  F. Champagne,et al.  Maternal regulation of estrogen receptor alpha methylation. , 2008, Current opinion in pharmacology.

[201]  Y. Kondo Epigenetic Cross-Talk between DNA Methylation and Histone Modifications in Human Cancers , 2009, Yonsei medical journal.

[202]  V. Papadopoulos,et al.  In utero exposure to di-(2-ethylhexyl) phthalate decreases mineralocorticoid receptor expression in the adult testis. , 2009, Endocrinology.

[203]  P. Poulsen,et al.  Twins in metabolic and diabetes research: what do they tell us? , 2007, Current opinion in clinical nutrition and metabolic care.

[204]  J. Trasler Epigenetics in spermatogenesis , 2009, Molecular and Cellular Endocrinology.

[205]  Guorong Li,et al.  Alterations in microRNA expression in stress-induced cellular senescence , 2009, Mechanisms of Ageing and Development.

[206]  B. Chow,et al.  Regulation of the human secretin gene is controlled by the combined effects of CpG methylation, Sp1/Sp3 ratio, and the E-box element. , 2004, Molecular endocrinology.

[207]  M. Laan,et al.  MicroRNAs miR-124 and miR-135a are potential regulators of the mineralocorticoid receptor gene (NR3C2) expression , 2010, Biochemical and biophysical research communications.

[208]  S. Ho,et al.  Epigenetic reprogramming and imprinting in origins of disease , 2007, Reviews in Endocrine and Metabolic Disorders.

[209]  I. Holzman,et al.  Perinatal endocrinology: common endocrine disorders in the sick and premature newborn. , 2011, Pediatric clinics of North America.

[210]  D. Rossignol Novel and emerging treatments for autism spectrum disorders: a systematic review. , 2009, Annals of clinical psychiatry : official journal of the American Academy of Clinical Psychiatrists.

[211]  R. Jirtle,et al.  Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development , 2007, Proceedings of the National Academy of Sciences.

[212]  V. Rakyan,et al.  Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[213]  P. Collas,et al.  Stable CpG hypomethylation of adipogenic promoters in freshly isolated, cultured, and differentiated mesenchymal stem cells from adipose tissue. , 2006, Molecular biology of the cell.

[214]  J. Barrett,et al.  Interaction between genetic susceptibility and early-life environmental exposure determines tumor-suppressor-gene penetrance. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[215]  C. Tepper,et al.  Cancerous miRNAs and their regulation , 2008, Cell cycle.

[216]  V. Rakyan,et al.  Metastable epialleles in mammals. , 2002, Trends in genetics : TIG.

[217]  M. Cuccaro,et al.  Genomic and epigenetic evidence for oxytocin receptor deficiency in autism , 2009, BMC medicine.

[218]  B. Cairns,et al.  The biology of chromatin remodeling complexes. , 2009, Annual review of biochemistry.

[219]  T. Spector,et al.  Epigenetic differences arise during the lifetime of monozygotic twins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[220]  Antonia M. Calafat,et al.  Exposure of the U.S. Population to Bisphenol A and 4-tertiary-Octylphenol: 2003–2004 , 2007, Environmental health perspectives.

[221]  A. Harder,et al.  Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome , 2009, The Journal of physiology.