Review article: Epigenetic control of fetal gene expression

Each differentiated cell type has its own epigenetic signature, which reflects its genotype, developmental history, and environmental influences, and is ultimately reflected in the phenotype of the cell and organism. Some cells undergo major epigenetic ‘reprogramming’ during fetal development. The proper, or improper, handling of these highly sensitive periods may have significant short‐term and long‐term effects on the newborn and his/her progeny. This review highlights the impact of environmental and nutritional factors on the epigenome and the potential effect of epigenetic dysregulation on maternal and fetal pregnancy outcomes, as well as possible long‐term implications.

[1]  J. Byrd,et al.  M6P/IGF2R imprinting evolution in mammals. , 2000, Molecular cell.

[2]  Wendy Dean,et al.  Regulation of supply and demand for maternal nutrients in mammals by imprinted genes , 2003, The Journal of physiology.

[3]  Tsung-Teh Wu,et al.  Frequent CpG island methylation in sporadic and syndromic gastric fundic gland polyps. , 2004, American journal of clinical pathology.

[4]  Carolyn J. Brown,et al.  Extremely skewed X-chromosome inactivation is increased in women with recurrent spontaneous abortion. , 1999, American journal of human genetics.

[5]  T. Bestor,et al.  The DNA methyltransferases of mammals. , 2000, Human molecular genetics.

[6]  S. Tilghman.  The Sins of the Fathers and Mothers Genomic Imprinting in Mammalian Development , 1999, Cell.

[7]  J. Herman,et al.  A gene hypermethylation profile of human cancer. , 2001, Cancer research.

[8]  Y. Matsui,et al.  Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. , 2005, Developmental biology.

[9]  I. Gut,et al.  Expressional and Epigenetic Alterations of Placental Serine Protease Inhibitors: SERPINA3 Is a Potential Marker of Preeclampsia , 2007, Hypertension.

[10]  R. Waterland,et al.  Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. , 2004, Nutrition.

[11]  M. Toyota,et al.  The role of DNA hypermethylation in human neoplasia , 2000, Electrophoresis.

[12]  Robert A. Waterland,et al.  Transposable Elements: Targets for Early Nutritional Effects on Epigenetic Gene Regulation , 2003, Molecular and Cellular Biology.

[13]  H. Hashimoto,et al.  DNA methylation in systemic lupus erythematosus , 2003, Lupus.

[14]  T. Haaf,et al.  Spatial Separation of Parental Genomes in Preimplantation Mouse Embryos , 2000, The Journal of cell biology.

[15]  W. Reik,et al.  Imprinted Genes, Placental Development and Fetal Growth , 2006, Hormone Research in Paediatrics.

[16]  R. Grant-Downton,et al.  Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. , 2005, Annals of botany.

[17]  P. Gluckman,et al.  The Consequences of Being Born Small – An Adaptive Perspective , 2006, Hormone Research in Paediatrics.

[18]  C. Walsh,et al.  Transcription of IAP endogenous retroviruses is constrained by cytosine methylation , 1998, Nature Genetics.

[19]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[20]  I. Pogribny,et al.  DNA methylation in Folbp1 knockout mice supplemented with folic acid during gestation. , 2002, The Journal of nutrition.

[21]  R. Ward,et al.  Colorectal cancer: a model for epigenetic tumorigenesis , 2006, Gut.

[22]  J. D. Vries,et al.  Underlying disorders associated with severe early-onset preeclampsia. , 1995, American journal of obstetrics and gynecology.

[23]  W. Reik,et al.  Epigenetic Reprogramming in Mammalian Development , 2001, Science.

[24]  T. Kouzarides,et al.  The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. , 2003, Nucleic acids research.

[25]  M. Azim Surani,et al.  Reprogramming of genome function through epigenetic inheritance , 2001, Nature.

[26]  Wendy Dean,et al.  Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. , 2003, Seminars in cell & developmental biology.

[27]  E. Rimm,et al.  Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. , 1996, Circulation.

[28]  A. Bird,et al.  Genomic DNA methylation: the mark and its mediators. , 2006, Trends in biochemical sciences.

[29]  W Dean,et al.  Conservation of methylation reprogramming in mammalian development: Aberrant reprogramming in cloned embryos , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[30]  A. Ferguson-Smith,et al.  Genomic imprinting: Mother maintains methylation marks , 2001, Current Biology.

[31]  C. Khoo,et al.  Dietary and serum folate: their influence on the outcome of pregnancy. , 1996, The American journal of clinical nutrition.

[32]  Wendy Dean,et al.  Dynamic reprogramming of DNA methylation in the early mouse embryo. , 2002, Developmental biology.

[33]  C. Plass,et al.  Quantitative assessment of DNA methylation: potential applications for disease diagnosis, classification, and prognosis in clinical settings , 2006, Journal of Molecular Medicine.

[34]  B. Richardson.  Impact of aging on DNA methylation , 2003, Ageing Research Reviews.

[35]  W. Hay,et al.  Placental transport of nutrients and its implications for fetal growth. , 2019, Journal of reproduction and fertility. Supplement.

[36]  Nathalie Beaujean,et al.  Reprogrammation et épigenèse , 2005 .

[37]  Pinchas Cohen,et al.  The role of the insulin-like growth factor system in prenatal growth. , 2005, Molecular genetics and metabolism.

[38]  I. Wilmut,et al.  Effect of Limited DNA Methylation Reprogramming in the Normal Sheep Embryo on Somatic Cell Nuclear Transfer1 , 2004, Biology of reproduction.

[39]  J. Granger,et al.  Pathophysiology of hypertension during preeclampsia linking placental ischemia with endothelial dysfunction. , 2001, Hypertension.

[40]  J. Renard,et al.  [Reprogramming and epigenesis]. , 2005, Medecine sciences : M/S.

[41]  M. D'Esposito,et al.  Folate treatment and unbalanced methylation and changes of allelic expression induced by hyperhomocysteinaemia in patients with uraemia , 2003, The Lancet.

[42]  S. Edvinsson,et al.  Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period , 2002, European Journal of Human Genetics.

[43]  J. Granger,et al.  Pathophysiology of hypertension during preeclampsia: linking placental ischemia with endothelial dysfunction. , 2008, American journal of physiology. Heart and circulatory physiology.

[44]  Rajiv P. Sharma.  Schizophrenia, epigenetics and ligand-activated nuclear receptors: a framework for chromatin therapeutics , 2004, Schizophrenia Research.

[45]  H. Blom,et al.  Is mutated serine hydroxymethyltransferase (SHMT) involved in the etiology of neural tube defects? , 2001, Molecular genetics and metabolism.

[46]  R. Feil,et al.  Epigenetic regulation of mammalian genomic imprinting. , 2004, Current opinion in genetics & development.

[47]  Gavin Kelsey,et al.  Resourceful imprinting : Fertility , 2004 .

[48]  F. Muskiet.  The importance of (early) folate status to primary and secondary coronary artery disease prevention. , 2005, Reproductive toxicology.

[49]  P. Gluckman,et al.  Predictive adaptive responses and human evolution. , 2005, Trends in ecology & evolution.

[50]  C. Brown,et al.  Skewed X-chromosome inactivation is associated with trisomy in women ascertained on the basis of recurrent spontaneous abortion or chromosomally abnormal pregnancies. , 2003, American journal of human genetics.

[51]  M. Lizano,et al.  Epigenetics of cervical cancer. An overview and therapeutic perspectives , 2005, Molecular Cancer.

[52]  Satoshi Tanaka,et al.  DNA Methylation-dependent Epigenetic Regulation of Dimethylarginine Dimethylaminohydrolase 2 Gene in Trophoblast Cell Lineage* , 2006, Journal of Biological Chemistry.

[53]  A. Ferguson-Smith,et al.  Roles for genomic imprinting and the zygotic genome in placental development , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[54]  H. Blom,et al.  Hyperhomocysteinemia: a risk factor for placental abruption or infarction. , 1996, European journal of obstetrics, gynecology, and reproductive biology.

[55]  L. Joss-Moore,et al.  The developmental origins of adult disease , 2009, Current opinion in pediatrics.

[56]  W. Rees,et al.  Gene-nutrient interactions during fetal development. , 2005, Reproduction.

[57]  D. Wieczorek,et al.  Histone acetylation dependent allelic expression imbalance of BAPX1 in patients with the oculo-auriculo-vertebral spectrum. , 2006, Human molecular genetics.

[58]  B M Turner,et al.  Histone acetylation and an epigenetic code. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[59]  Peter W. Laird,et al.  DNA Hypomethylation and Ovarian Cancer Biology , 2004, Cancer Research.

[60]  W. Reik,et al.  Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse , 2003, Genesis.

[61]  W. Farrell,et al.  Molecular Pathogenesis of Pituitary Tumors , 2000, Frontiers in Neuroendocrinology.

[62]  Carolyn J. Brown,et al.  Skewed X Inactivation and Recurrent Spontaneous Abortion , 2001, Seminars in reproductive medicine.

[63]  Nutrient Supplements during Pregnancy,et al.  Nutrition During Pregnancy: Part I, Weight Gain; Part II, Nutrient Supplements , 1991 .

[64]  I M Morison,et al.  The imprinted gene and parent-of-origin effect database , 2001, Nucleic Acids Res..

[65]  B. Sibai,et al.  Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia. , 2006, American journal of obstetrics and gynecology.

[66]  Sang-Woon Choi,et al.  Gene-nutrient interactions in one-carbon metabolism. , 2005, Current drug metabolism.

[67]  A. Bird.  DNA methylation patterns and epigenetic memory. , 2002, Genes & development.

[68]  A. Madan,et al.  Epigenetic regulation of maspin expression in the human placenta. , 2006, Molecular human reproduction.

[69]  G. Shaw,et al.  Occurrence of Low Birthweight and Preterm Delivery among California Infants before and after Compulsory Food Fortification with Folic Acid , 2004, Public health reports.

[70]  K. Robertson.  DNA methylation and human disease , 2005, Nature Reviews Genetics.

[71]  P. Gluckman,et al.  The fetal, neonatal, and infant environments-the long-term consequences for disease risk. , 2005, Early human development.

[72]  Jian-xin Wu,et al.  [DNA methylation: an epigenetic mechanism for tumorigenesis]. , 2006, Yi chuan = Hereditas.

[73]  R. Yuen,et al.  Hypermethylation of RASSF1A in human and rhesus placentas. , 2007, The American journal of pathology.

[74]  D. Leon,et al.  Fetal growth and adult disease. , 1998, European journal of clinical nutrition.

[75]  R. Feil,et al.  Environmental and nutritional effects on the epigenetic regulation of genes. , 2006, Mutation research.

[76]  M. Surani,et al.  Epigenetic reprogramming in mouse primordial germ cells , 2002, Mechanisms of Development.

[77]  S. Baylin,et al.  Epigenetic gene silencing in cancer – a mechanism for early oncogenic pathway addiction? , 2006, Nature Reviews Cancer.

[78]  F. O'Malley,et al.  CpG methylation within the 5′ regulatory region of the BRCA1 gene is tumor specific and includes a putative CREB binding site , 1998, Oncogene.

[79]  T. Ozcelik,et al.  Extremely skewed X‐chromosome inactivation patterns in women with recurrent spontaneous abortion , 2006, The Australian & New Zealand journal of obstetrics & gynaecology.

[80]  J. Cavaille,et al.  Differential regulation of imprinting in the murine embryo and placenta by the Dlk1-Dio3 imprinting control region , 2007, Development.

[81]  L. Myatt.  Placental adaptive responses and fetal programming , 2006, The Journal of physiology.

[82]  W. Reik,et al.  Placental-specific IGF-II is a major modulator of placental and fetal growth , 2002, Nature.

[83]  M. Menon,et al.  ACCIDENTAL HAEMORRHAGE AND FOLIC ACID DEFICIENCY , 1966, The Journal of obstetrics and gynaecology of the British Commonwealth.

[84]  W. Reik,et al.  Imprinting in clusters: lessons from Beckwith-Wiedemann syndrome. , 1997, Trends in genetics : TIG.

[85]  J. Trasler.  Gamete imprinting: setting epigenetic patterns for the next generation. , 2006, Reproduction, fertility, and development.

[86]  G. Poirier,et al.  Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. , 1999, The Biochemical journal.

[87]  H. Blom,et al.  Hyperhomocysteinemia: a risk factor in women with unexplained recurrent early pregnancy loss. , 1993, Fertility and sterility.

[88]  L. D. Croce,et al.  Chromatin structure and epigenetics. , 2006, Biochemical pharmacology.

[89]  W. Reik,et al.  Imprinting mechanisms in mammals. , 1998, Current opinion in genetics & development.

[90]  Shiva M. Singh,et al.  Involvement of gene–diet/drug interaction in DNA methylation and its contribution to complex diseases: from cancer to schizophrenia , 2003, Clinical genetics.

[91]  M. Stephenson.  Frequency of factors associated with habitual abortion in 197 couples. , 1996, Fertility and sterility.

[92]  Y. Matsui,et al.  Erasure of methylation imprinting of Igf2r during mouse primordial germ‐cell development , 2003, Molecular reproduction and development.

[93]  Chunming Ding,et al.  Detection of the placental epigenetic signature of the maspin gene in maternal plasma. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[94]  W. Johnson,et al.  Folic acid: influence on the outcome of pregnancy. , 2000, The American journal of clinical nutrition.

[95]  J. Mathers,et al.  Folate and DNA methylation during in utero development and aging. , 2004, Biochemical Society transactions.

[96]  A. Czeizel,et al.  Can terathanasia explain the protective effect of folic-acid supplementation on birth defects? , 1997, The Lancet.

[97]  P. Geyer,et al.  The role of insulator elements in defining domains of gene expression. , 1997, Current opinion in genetics & development.

[98]  M. Bartolomei,et al.  Epigenetic reprogramming in the mammalian embryo: struggle of the clones , 2002, Genome Biology.

[99]  P. Gluckman,et al.  Living with the Past: Evolution, Development, and Patterns of Disease , 2004, Science.

[100]  S. Baylin,et al.  Methylation of the oestrogen receptor CpG island links ageing and neoplasia in human colon , 1994, Nature Genetics.

[101]  H. Zoghbi,et al.  Rett syndrome: methyl-CpG-binding protein 2 mutations and phenotype-genotype correlations. , 2000, American journal of medical genetics.

[102]  A. Wagschal,et al.  Genomic imprinting in the placenta , 2006, Cytogenetic and Genome Research.

[103]  U. Surti,et al.  Familial skewed X inactivation: a molecular trait associated with high spontaneous-abortion rate maps to Xq28. , 1997, American journal of human genetics.

[104]  Rappold,et al.  Human Molecular Genetics , 1996, Nature Medicine.

[105]  A. Hamilton,et al.  RNA–DNA Interactions and DNA Methylation in Post-Transcriptional Gene Silencing , 1999, Plant Cell.

[106]  W. Farrell,et al.  Epigenetic Mechanisms of Tumorigenesis , 2005, Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme.

[107]  C. Iacobuzio-Donahue,et al.  Frequent hypomethylation of multiple genes overexpressed in pancreatic ductal adenocarcinoma. , 2003, Cancer research.

[108]  R. Waterland,et al.  Potential mechanisms of metabolic imprinting that lead to chronic disease. , 1999, The American journal of clinical nutrition.

[109]  M. Ehrlich.  The ICF syndrome, a DNA methyltransferase 3B deficiency and immunodeficiency disease. , 2003, Clinical immunology.

[110]  D. Higgs,et al.  Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation , 2000, Nature Genetics.

[111]  H. Spencer,et al.  A census of mammalian imprinting. , 2005, Trends in genetics : TIG.

[112]  Allan Vaag,et al.  Intrauterine Growth Retardation and Consequences for Endocrine and Cardiovascular Diseases in Adult Life: Does Insulin-Like Growth Factor-I Play a Role? , 2003, Hormone Research in Paediatrics.

[113]  J. Gris,et al.  A woman with five consecutive fetal deaths: case report and retrospective analysis of hyperhomocysteinemia prevalence in 100 consecutive women with recurrent miscarriages. , 1998, Fertility and sterility.

[114]  B. Tycko,et al.  Physiological functions of imprinted genes , 2002, Journal of cellular physiology.

[115]  Mark A. Hanson,et al.  The developmental origins of the metabolic syndrome , 2004, Trends in Endocrinology & Metabolism.

[116]  T. Tamura,et al.  Folate and human reproduction. , 2006, The American journal of clinical nutrition.

[117]  A. Mclaren,et al.  Primordial germ cells in the mouse embryo during gastrulation. , 1990, Development.

[118]  Rob Willemsen,et al.  The fragile X syndrome: from molecular genetics to neurobiology. , 2004, Mental retardation and developmental disabilities research reviews.

[119]  Wolf Reik,et al.  Resourceful imprinting , 2004, Nature.

[120]  David I. K. Martin,et al.  Epigenetic inheritance at the agouti locus in the mouse , 1999, Nature Genetics.

[121]  R. Jirtle,et al.  Epigenetic Gene Regulation: Linking Early Developmental Environment to Adult Disease , 2006 .

[122]  B. Su,et al.  Hypermethylation of the RASSF1A gene in gliomas. , 2004, Clinica chimica acta; international journal of clinical chemistry.

[123]  N. Spears,et al.  Genomic imprinting and reproduction. , 2005, Reproduction.

[124]  W. Reik,et al.  Epigenetic reprogramming in mammals. , 2005, Human molecular genetics.

[125]  S. Liebhaber,et al.  Epigenetic modifications at the human growth hormone locus predict distinct roles for histone acetylation and methylation in placental gene activation. , 2004, Molecular endocrinology.

[126]  M. Susser,et al.  Obesity in young men after famine exposure in utero and early infancy. , 1976, The New England journal of medicine.

[127]  I. Sandovici,et al.  Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. , 2005, Proceedings of the National Academy of Sciences of the United States of America.