Cited by 144Birth, Development, and HealthEpigenetics and DNA MethylationNutrition, Genetics, and Disease

Considering Maternal Dietary Modulators for Epigenetic Regulation and Programming of the Fetal Epigenome

Open access
Chango, Abalo, Pogribny, Igor·2015·Nutrients

Abstract

Fetal life is characterized by a tremendous plasticity and ability to respond to various environmental and lifestyle factors, including maternal nutrition. Identification of the role of dietary factors that can modulate and reshape the cellular epigenome during development, including methyl group donors (e.g., folate, choline) and bioactive compounds (e.g., polyphenols) is of great importance; however, there is insufficient knowledge of a particular effect of each type of modulator and/or their combination on fetal life. To enhance the quality and safety of food products for proper fetal health and disease prevention in later life, a better understanding of the underlying mechanisms of dietary epigenetic modulators during the critical prenatal period is necessary. This review focuses on the influence of maternal dietary components on DNA methylation, histone modification, and microRNAs, and summarizes current knowledge of the effect and importance of dietary components on epigenetic mechanisms that control the proper expression of genetic information. Evidence reveals that some components in the maternal diet can directly or indirectly affect epigenetic mechanisms. Understanding the underlying mechanisms of how early-life nutritional environment affects the epigenome during development is of great importance for the successful prevention of adult chronic diseases through optimal maternal nutrition.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/nu7042748

Cites

12 of 12 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • These micronutrient deficiencies contribute not only to immediate pregnancy complications but also to persistent alterations in fetal growth, neurodevelopment, and metabolic programming, often mediated through epigenetic mechanisms.

    “These deficiencies contribute not only to immediate pregnancy complications but also to persistent alterations in fetal growth, neurodevelopment, and metabolic programming, often mediated through epigenetic mechanisms [89,90].”

    From Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences (2026) · cites this paper as [89]

    Section 1 (Introduction) says deficiencies in methyl-group donors can cause lasting epigenetic and phenotypic changes, and §3.4 links methyl-donor restriction to adverse offspring phenotypes and altered DNA methylation. Section 6 also links dietary components to metabolic programming. The copy does not establish that micronutrient deficiencies cause the cited pregnancy complications or persistent neurodevelopmental changes; §3.4 discusses growth restriction and preeclampsia in relation to placental maladaptation, not specifically deficiency. Page numbers are unavailable in the indexed passages. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 132

  1. [2]Rodenhiser D. Mann M. Epigenetics and human disease: Translating basic biology into clinical applications CMAJ 2006 174 341 348 10.1503/cmaj.050774 16446478 PMC1373719 · DOI
  2. [3]Hewagama A. Richardson B. The genetics and epigenetics of autoimmune diseases J. Autoimmun. 2009 33 3 11 10.1016/j.jaut.2009.03.007 19349147 PMC2819418 · DOI
  3. [4]Lopez-Pedrera C. Perez-Sanchez C. Ramos-Casals M. Santos-Gonzalez M. Rodriguez-Ariza A. Cuadrado M.J. Cardiovascular risk in systemic autoimmune diseases: Epigenetic mechanisms of immune regulatory functions Clin. Dev. Immunol. 2012 2012 10.1155/2012/974648 PMC3173726 21941583 · DOI
  4. [6]Brookes E. Shi Y. Diverse epigenetic mechanisms of human disease Annu. Rev. Genet. 2014 48 237 268 10.1146/annurev-genet-120213-092518 25195505 · DOI
  5. [8]Reik W. Dean W. Walter J. Epigenetic reprogramming in mammalian development Science 2001 293 1089 1093 10.1126/science.1063443 11498579 · DOI · Paper page
  6. [9]Smith Z.D. Meissner A. DNA methylation: Roles in mammalian development Nat. Rev. Genet. 2013 14 204 220 10.1038/nrg3354 23400093 · DOI · Paper page
  7. [10]Saffery R. Novakovic B. Epigenetics as the mediator of fetal programming of adult onset disease: What is the evidence? Acta Obstet. Gynecol. Scand. 2014 93 1090 1098 10.1111/aogs.12431 24835110 · DOI
  8. [11]Jiang X. West A.A. Caudill M.A. Maternal choline supplementation: A nutritional approach for improving offspring health? Trends Endocrinol. Metab. 2014 25 263 273 10.1016/j.tem.2014.02.001 24680198 · DOI
  9. [12]Masuyama H. Hiramatsu Y. Effects of a high-fat diet exposure in utero on the metabolic syndrome-like phenomenon in mouse offspring through epigenetic changes in adipocytokine gene expression Endocrinology 2012 153 2823 2830 10.1210/en.2011-2161 22434078 · DOI · Paper page
  10. [13]Thornburg K.L. Shannon J. Thuillier P. Turker M.S. In utero life and epigenetic predisposition for disease Adv. Genet. 2010 71 57 78 20933126 PMC3923648
  11. [14]Hogg K. Price E.M. Hanna C.W. Robinson W.P. Prenatal and perinatal environmental influences on the human fetal and placental epigenome Clin. Pharmacol. Ther. 2012 92 716 726 10.1038/clpt.2012.141 23047650 · DOI
  12. [15]Mathers J.C. Early nutrition: Impact on epigenetics Forum Nutr. 2007 60 42 48 17684400
  13. [16]Szyf M. The early life environment and the epigenome Biochim. Biophys. Acta 2009 1790 878 885 10.1016/j.bbagen.2009.01.009 19364482 · DOI
  14. [17]Sharma S. Kelly T.K. Jones P.A. Epigenetics in cancer Carcinogenesis 2010 31 27 36 10.1093/carcin/bgp220 19752007 PMC2802667 · DOI · Paper page
  15. [18]Bell J.T. Pai A.A. Pickrell J.K. Gaffney D.J. Pique-Regi R. Degner J.F. Gilad Y. Pritchard J.K. DNA methylation patterns associated with genetic and gene expression variation in HapMap cell lines Genome Biol. 2011 12 10.1186/gb-2011-12-1-r10 21251332 PMC3091299 · DOI · Paper page
  16. [19]Pogribny I.P. Rusyn I. Environmental toxicants, epigenetics, and cancer Adv. Exp. Med. Biol. 2013 754 215 232 22956504 PMC4281087
  17. [20]Fraga M.F. Ballestar E. Paz M.F. Ropero S. Setien F. Ballestar M.L. Heine-Suñer D. Cigudosa J.C. Urioste M. Benitez J. Epigenetic differences arise during the lifetime of monozygotic twins Proc. Natl. Acad. Sci. USA 2005 102 10604 10609 10.1073/pnas.0500398102 16009939 PMC1174919 · DOI · Paper page
  18. [21]Talens R.P. Boomsma D.I. Tobi E.W. Kremer D. Jukema J.W. Willemsen G. Putter H. Slagboom P.E. Heijmans B.T. Variation, patterns, and temporal stability of DNA methylation: Considerations for epigenetic epidemiology FASEB J. 2010 24 3135 3144 10.1096/fj.09-150490 20385621 · DOI
  19. [22]Ooi S.K. O’Donnell A.H. Bestor T.H. Mammalian cytosine methylation at a glance J. Cell Sci. 2009 122 2787 2791 10.1242/jcs.015123 19657014 PMC2724605 · DOI
  20. [23]Das R. Dimitrova N. Xuan Z. Rollins R.A. Haghighi F. Edwards J.R. Ju J. Bestor T.H. Zhang M.Q. Computational prediction of methylation status in human genomic sequences Proc. Natl. Acad. Sci. USA 2006 103 10713 10716 10.1073/pnas.0602949103 16818882 PMC1502297 · DOI
  21. [24]Rollins R.A. Haghighi F. Edwards J.R. Das R. Zhang M.Q. Ju J. Bestor T.H. Large-scale structure of genomic methylation patterns Genome Res. 2006 16 157 163 10.1101/gr.4362006 16365381 PMC1361710 · DOI
  22. [25]Mikkelsen T.S. Ku M. Jaffe D.B. Issac B. Lieberman E. Giannoukos G. Alvarez P. Brockman W. Kim T.K. Koche R.P. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells Nature 2007 448 553 560 10.1038/nature06008 17603471 PMC2921165 · DOI · Paper page
  23. [26]Kouzarides T. Chromatin modifications and their function Cell 2007 128 693 705 10.1016/j.cell.2007.02.005 17320507 · DOI · Paper page
  24. [27]Ropero S. Esteller M. The role of histone deacetylases (HDACs) in human cancer Mol. Oncol. 2007 1 19 25 10.1016/j.molonc.2007.01.001 19383284 PMC5543853 · DOI
  25. [28]Iizuka M. Smith M.M. Functional consequences of histone modifications Curr. Opin. Genet. Dev. 2003 13 154 160 10.1016/S0959-437X(03)00020-0 12672492 · DOI
  26. [29]Butler J.S. Koutelou E. Schibler A.C. Dent S.Y. Histone-modifying enzymes: Regulators of developmental decisions and drivers of human disease Epigenomics 2012 4 163 177 10.2217/epi.12.3 22449188 PMC3382990 · DOI
  27. [32]Denis H. Ndlovu M.N. Fuks F. Regulation of mammalian DNA methyltransferases: A route to new mechanisms EMBO Rep. 2011 12 647 656 10.1038/embor.2011.110 21660058 PMC3128952 · DOI
  28. [33]Waterland R.A. Assessing the effects of high methionine intake on DNA methylation J. Nutr. 2006 136 1706S 1710S 16702343
  29. [34]Niculescu M.D. Zeisel S.H. Diet, methyl donors and DNA methylation: Interactions between dietary folate, methionine and choline J. Nutr. 2002 132 2333S 2335S 12163687
  30. [35]Hardy T.M. Tollefsbol T.O. Epigenetic diet: Impact on the epigenome and cancer Epigenomics 2011 3 503 518 10.2217/epi.11.71 22022340 PMC3197720 · DOI
  31. [36]Stone N. Pangilinan F. Molloy A.M. Shane B. Scott J.M. Ueland P.M. Mills J.L. Kirke P.N. Sethupathy P. Brody L.C. Bioinformatic and genetic association analysis of microrna target sites in one-carbon metabolism genes PLoS ONE 2011 6 e21851 10.1371/journal.pone.0021851 21765920 PMC3134459 · DOI
  32. [37]Wolff G.L. Kodell R.L. Moore S.R. Cooney C.A. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice FASEB J. 1998 12 949 957 9707167
  33. [38]Cooney C.A. Dave A.A. Wolff G.L. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring J. Nutr. 2002 132 2393S 2400S 12163699
  34. [40]Waterland R.A. Travisano M. Tahiliani K.G. Rached M.T. Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity Int. J. Obes. (Lond.) 2008 32 1373 1379 10.1038/ijo.2008.100 18626486 PMC2574783 · DOI
  35. [41]Cropley J.E. Suter C.M. Beckman K.B. Martin D.I. Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation Proc. Natl. Acad. Sci. USA 2006 103 17308 17312 10.1073/pnas.0607090103 17101998 PMC1838538 · DOI
  36. [42]Elango N. Hunt B.G. Goodisman M.A. Yi S.V. DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera Proc. Natl. Acad. Sci. USA 2009 106 11206 11211 10.1073/pnas.0900301106 19556545 PMC2708677 · DOI
  37. [43]Hunt B.G. Brisson J.A. Yi S.V. Goodisman M.A. Functional conservation of DNA methylation in the pea aphid and the honeybee Genome Biol. Evol. 2010 2 719 728 20855427 PMC2962555
  38. [44]Ghoshal K. Li X. Datta J. Bai S. Pogribny I. Pogribny M. Huang Y. Young D. Jacob S.T. A folate- and methyl-deficient diet alters the expression of DNA methyltransferases and methyl CpG binding proteins involved in epigenetic gene silencing in livers of F344 rats J. Nutr. 2006 136 1522 1527 16702315 PMC2237890
  39. [45]Padmanabhan N. Jia D. Geary-Joo C. Wu X. Ferguson-Smith A.C. Fung E. Bieda M.C. Snyder F.F. Gravel R.A. Cross J.C. Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development Cell 2013 155 81 93 10.1016/j.cell.2013.09.002 24074862 PMC3844871 · DOI
  40. [46]Pogribny I.P. Tryndyak V.P. Muskhelishvili L. Rusyn I. Ross S.A. Methyl deficiency, alterations in global histone modifications, and carcinogenesis J. Nutr. 2007 137 216S 222S 17182829
  41. [47]Zhou W. Alonso S. Takai D. Lu S.C. Yamamoto F. Perucho M. Huang S. Requirement of RIZ1 for cancer prevention by methyl-balanced diet PLoS ONE 2008 3 e3390 10.1371/journal.pone.0003390 18852888 PMC2559864 · DOI
  42. [48]Luka Z. Moss F. Loukachevitch L.V. Bornhop D.J. Wagner C. Histone demethylase LSD1 is a folate-binding protein Biochemistry 2011 50 4750 4756 10.1021/bi200247b 21510664 PMC3111596 · DOI
  43. [49]Franchina T. Amodeo V. Bronte G. Savio G. Ricciardi G.R. Picciotto M. Russo A. Giordano A. Adamo V. Circulating miR-22, miR-24 and miR-34a as novel predictive biomarkers to pemetrexed-based chemotherapy in advanced non-small cell lung cancer J. Cell Physiol. 2014 229 97 99 23794259
  44. [50]Koturbash I. Melnyk S. James S.J. Beland F.A. Pogribny I.P. Role of epigenetic and miR-22 and miR-29b alterations in the downregulation of Mat1a and Mthfr genes in early preneoplastic livers in rats induced by 2-acetylaminofluorene Mol. Carcinog. 2013 52 318 327 10.1002/mc.21861 22213190 · DOI
  45. [51]Novakovic B. Saffery R. The ever growing complexity of placental epigenetics—Role in adverse pregnancy outcomes and fetal programming Placenta 2012 33 959 970 10.1016/j.placenta.2012.10.003 23102655 · DOI
  46. [52]Yajnik C.S. Deshmukh U.S. Fetal programming: Maternal nutrition and role of one-carbon metabolism Rev. Endocr. Metab. Disord. 2012 13 121 127 10.1007/s11154-012-9214-8 22415298 · DOI
  47. [53]Longtine M.S. Nelson D.M. Placental dysfunction and fetal programming: The importance of placental size, shape, histopathology, and molecular composition Semin. Reprod. Med. 2011 29 187 196 10.1055/s-0031-1275515 21710395 PMC3682832 · DOI
  48. [54]Fryer A.A. Nafee T.M. Ismail K.M. Carroll W.D. Emes R.D. Farrell W.E. LINE-1 DNA methylation is inversely correlated with cord plasma homocysteine in man: A preliminary study Epigenetics 2009 4 394 398 10.4161/epi.4.6.9766 19755846 · DOI
  49. [55]Sinclair K.D. Lea R.G. Rees W.D. Young L.E. The developmental origins of health and disease: Current theories and epigenetic mechanisms Soc. Reprod. Fertil. Suppl. 2007 64 425 443 17491163
  50. [56]Probst A.V. Dunleavy E. Almouzni G. Epigenetic inheritance during the cell cycle Nat. Rev. Mol. Cell Biol. 2009 10 192 206 10.1038/nrm2640 19234478 · DOI
  51. [57]Jirtle R.L. Skinner M.K. Environmental epigenomics and disease susceptibility Nat. Rev. Genet. 2007 8 253 262 10.1038/nrg2045 17363974 PMC5940010 · DOI · Paper page
  52. [58]Sinclair K.D. Singh R. Modelling the developmental origins of health and disease in the early embryo Theriogenology 2007 67 43 53 10.1016/j.theriogenology.2006.09.017 17049592 · DOI
  53. [59]Shenderov B.A. Midtvedt T. Epigenomic programing: A future way to health? Microb. Ecol. Health Dis. 2014 25 10.3402/mehd.v25.24145 PMC4016746 24829553 · DOI
  54. [60]Wilkinson J. High maternal choline intake may prevent the development of stress-related disorders through epigenetic mechanisms Epigenomics 2012 4 479 480 10.2217/epi.12.54 23275980 · DOI
  55. [61]Jiang X. Yan J. West A.A. Perry C.A. Malysheva O.V. Devapatla S. Pressman E. Vermeylen F. Caudill M.A. Maternal choline intake alters the epigenetic state of fetal cortisol-regulating genes in humans FASEB J. 2012 26 3563 3574 10.1096/fj.12-207894 22549509 · DOI
  56. [62]Zeisel S.H. Dietary choline deficiency causes DNA strand breaks and alters epigenetic marks on DNA and histones Mutat. Res. 2012 733 34 38 10.1016/j.mrfmmm.2011.10.008 22041500 PMC3319504 · DOI
  57. [63]Oliva J. Bardag-Gorce F. Li J. French B.A. Nguyen S.K. Lu S.C. French S.W. Betaine prevents Mallory-Denk body formation in drug-primed mice by epigenetic mechanisms Exp. Mol. Pathol. 2009 86 77 86 10.1016/j.yexmp.2008.11.002 19073172 PMC3319154 · DOI
  58. [64]Wei L.N. Non-canonical activity of retinoic acid in epigenetic control of embryonic stem cell Transcription 2013 4 10.4161/trns.25395 PMC3977914 23863198 · DOI
  59. [65]Cheong H.S. Lee H.C. Park B.L. Kim H. Jang M.J. Han Y.M. Kim S.Y. Kim Y.S. Shin H.D. Epigenetic modification of retinoic acid-treated human embryonic stem cells BMB Rep. 2010 43 830 835 10.5483/BMBRep.2010.43.12.830 21189161 · DOI
  60. [66]Loewy A.D. Niles K.M. Anastasio N. Watkins D. Lavoie J. Lerner-Ellis J.P. Pastinen T. Trasler J.M. Rosenblatt D.S. Epigenetic modification of the gene for the vitamin B(12) chaperone MMACHC can result in increased tumorigenicity and methionine dependence Mol. Genet. Metab. 2009 96 261 267 10.1016/j.ymgme.2008.12.011 19200761 · DOI
  61. [67]Karlic H. Varga F. Impact of vitamin D metabolism on clinical epigenetics Clin. Epigenet. 2011 2 55 61 10.1007/s13148-011-0021-y PMC3365599 22704269 · DOI
  62. [68]Tian X. Diaz F.J. Acute dietary zinc deficiency before conception compromises oocyte epigenetic programming and disrupts embryonic development Dev. Biol. 2013 376 51 61 10.1016/j.ydbio.2013.01.015 23348678 PMC3601821 · DOI
  63. [70]Hu Y. McIntosh G.H. Le Leu R.K. Nyskohus L.S. Woodman R.J. Young G.P. Combination of selenium and green tea improves the efficacy of chemoprevention in a rat colorectal cancer model by modulating genetic and epigenetic biomarkers PLoS ONE 2013 8 e64362 10.1371/journal.pone.0064362 23717604 PMC3662759 · DOI
  64. [71]Shankar S. Kumar D. Srivastava R.K. Epigenetic modifications by dietary phytochemicals: Implications for personalized nutrition Pharmacol. Ther. 2013 138 1 17 10.1016/j.pharmthera.2012.11.002 23159372 PMC4153856 · DOI
  65. [72]Parasramka M.A. Ho E. Williams D.E. Dashwood R.H. MicroRNAs, diet, and cancer: New mechanistic insights on the epigenetic actions of phytochemicals Mol. Carcinog. 2012 51 213 230 10.1002/mc.20822 21739482 PMC3196802 · DOI
  66. [74]Lambert J.D. Yang C.S. Cancer chemopreventive activity and bioavailability of tea and tea polyphenols Mutat. Res. 2003 523 201 208 10.1016/S0027-5107(02)00336-6 12628518 · DOI
  67. [75]Wolfram S. Raederstorff D. Preller M. Wang Y. Teixeira S.R. Riegger C. Weber P. Epigallocatechin gallate supplementation alleviates diabetes in rodents J. Nutr. 2006 136 2512 2518 16988119
  68. [76]Wolfram S. Wang Y. Thielecke F. Anti-obesity effects of green tea: From bedside to bench Mol. Nutr. Food Res. 2006 50 176 187 10.1002/mnfr.200500102 16470636 · DOI
  69. [77]Kopelovich L. Crowell J.A. Fay J.R. The epigenome as a target for cancer chemoprevention J. Natl. Cancer Inst. 2003 95 1747 1757 10.1093/jnci/dig109 14652236 · DOI
  70. [78]Huang J. Plass C. Gerhauser C. Cancer chemoprevention by targeting the epigenome Curr. Drug Targets 2011 12 1925 1956 10.2174/138945011798184155 21158707 · DOI
  71. [79]Lu H. Meng X. Yang C.S. Enzymology of methylation of tea catechins and inhibition of catechol-O-methyltransferase by (−)-epigallocatechin gallate Drug Metab. Dispos. 2003 31 572 579 10.1124/dmd.31.5.572 12695345 · DOI
  72. [81]Liu A.G. Erdman J.W. Jr. Lycopene and apo-10ʹ-lycopenal do not alter DNA methylation of GSTP1 in LNCaP cells Biochem. Biophys. Res. Commun. 2011 412 479 482 10.1016/j.bbrc.2011.07.124 21839064 PMC3167003 · DOI
  73. [82]Yu J. Peng Y. Wu L.C. Xie Z. Deng Y. Hughes T. He S. Mo X. Chiu M. Wang Q.E. Curcumin down-regulates DNA methyltransferase 1 and plays an anti-leukemic role in acute myeloid leukemia PLoS ONE 2013 8 e55934 10.1371/journal.pone.0055934 23457487 PMC3572185 · DOI
  74. [83]Vanhees K. Coort S. Ruijters E.J. Godschalk R.W. van Schooten F.J. Barjesteh van Waalwijk van Doorn-Khosrovani S. Epigenetics: Prenatal exposure to genistein leaves a permanent signature on the hematopoietic lineage FASEB J. 2011 25 797 807 10.1096/fj.10-172155 21048042 · DOI
  75. [84]Hsu A. Wong C.P. Yu Z. Williams D.E. Dashwood R.H. Ho E. Promoter de-methylation of Cyclin D2 by sulforaphane in prostate cancer cells Clin. Epigenet. 2011 3 10.1186/1868-7083-3-3 PMC3257546 22303414 · DOI
  76. [85]Wang L.G. Beklemisheva A. Liu X.M. Ferrari A.C. Feng J. Chiao J.W. Dual action on promoter demethylation and chromatin by an isothiocyanate restored GSTP1 silenced in prostate cancer Mol. Carcinog. 2007 46 24 31 10.1002/mc.20258 16921492 · DOI
  77. [86]Stefanska B. Rudnicka K. Bednarek A. Fabianowska-Majewska K. Hypomethylation and induction of retinoic acid receptor beta 2 by concurrent action of adenosine analogues and natural compounds in breast cancer cells Eur. J. Pharmacol. 2010 638 47 53 10.1016/j.ejphar.2010.04.032 20447390 · DOI
  78. [87]Link A. Balaguer F. Goel A. Cancer chemoprevention by dietary polyphenols: Promising role for epigenetics Biochem. Pharmacol. 2010 80 1771 1792 10.1016/j.bcp.2010.06.036 20599773 PMC2974019 · DOI
  79. [88]Lee Y.H. Kwak J. Choi H.K. Choi K.C. Kim S. Lee J. Jun W. Park H.J. Yoon H.G. EGCG suppresses prostate cancer cell growth modulating acetylation of androgen receptor by anti-histone acetyltransferase activity Int. J. Mol. Med. 2012 30 69 74 22505206
  80. [89]Lee W.J. Chen Y.R. Tseng T.H. Quercetin induces FASL-related apoptosis, in part, through promotion of histone H3 acetylation in human leukemia HL-60 cells Oncol. Rep. 2011 25 583 591 21165570
  81. [90]Ross S.A. Davis C.D. The emerging role of microRNAs and nutrition in modulating health and disease Annu. Rev. Nutr. 2014 34 305 336 10.1146/annurev-nutr-071813-105729 25033062 · DOI
  82. [91]Wang Y. Li Y. Liu X. Cho W.C. Genetic and epigenetic studies for determining molecular targets of natural product anticancer agents Curr. Cancer Drug Targets 2013 13 506 518 10.2174/15680096113139990033 23597195 · DOI
  83. [92]Williams S.R. Yang Q. Chen F. Liu X. Keene K.L. Jacques P. Chen W.M. Weinstein G. Hsu F.C. Beiser A. Genome-wide meta-analysis of homocysteine and methionine metabolism identifies five one carbon metabolism loci and a novel association of ALDH1L1 with ischemic stroke PLoS Genet. 2014 10 e1004214 10.1371/journal.pgen.1004214 24651765 PMC3961178 · DOI
  84. [93]Shea T.B. Rogers E. Lifetime requirement of the methionine cycle for neuronal development and maintenance Curr. Opin. Psychiatry 2014 27 138 142 10.1097/YCO.0000000000000046 24445402 · DOI
  85. [94]Lillycrop K.A. Slater-Jefferies J.L. Hanson M.A. Godfrey K.M. Jackson A.A. Burdge G.C. Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications Br. J. Nutr. 2007 97 1064 1073 10.1017/S000711450769196X 17433129 PMC2211425 · DOI
  86. [95]Sene Lde B. Mesquita F.F. de Moraes L.N. Santos D.C. Carvalho R. Gontijo J.A. Boer P.A. Involvement of renal corpuscle microRNA expression on epithelial-to-mesenchymal transition in maternal low protein diet in adult programmed rats PLoS ONE 2013 8 e71310 23977013 PMC3747155
  87. [96]Gillberg L. Jacobsen S.C. Ronn T. Brons C. Vaag A. PPARGC1A DNA methylation in subcutaneous adipose tissue in low birth weight subjects—Impact of 5 days of high-fat overfeeding Metabolism 2014 63 263 271 10.1016/j.metabol.2013.10.003 24262291 · DOI
  88. [97]Langie S.A. Achterfeldt S. Gorniak J.P. Halley-Hogg K.J. Oxley D. van Schooten F.J. Godschalk R.W. McKay J.A. Mathers J.C. Maternal folate depletion and high-fat feeding from weaning affects DNA methylation and DNA repair in brain of adult offspring FASEB J. 2013 27 3323 3334 10.1096/fj.12-224121 23603834 · DOI
  89. [98]Jacobsen S.C. Brons C. Bork-Jensen J. Ribel-Madsen R. Yang B. Lara E. Hall E. Calvanese V. Nilsson E. Jorgensen S.W. Effects of short-term high-fat overfeeding on genome-wide DNA methylation in the skeletal muscle of healthy young men Diabetologia 2012 55 3341 3349 10.1007/s00125-012-2717-8 22961225 · DOI
  90. [100]Aagaard-Tillery K.M. Grove K. Bishop J. Ke X. Fu Q. McKnight R. Lane R.H. Developmental origins of disease and determinants of chromatin structure: Maternal diet modifies the primate fetal epigenome J. Mol. Endocrinol. 2008 41 91 102 10.1677/JME-08-0025 18515302 PMC2959100 · DOI
  91. [101]Cirera S. Birck M. Busk P.K. Fredholm M. Expression profiles of miRNA-122 and its target cat1 in minipigs (Sus scrofa) fed a high-cholesterol diet Comp. Med. 2010 60 136 141 20412689 PMC2855041
  92. [102]Takanabe R. Ono K. Abe Y. Takaya T. Horie T. Wada H. Kita T. Satoh N. Shimatsu A. Hasegawa K. Up-regulated expression of microRNA-143 in association with obesity in adipose tissue of mice fed high-fat diet Biochem. Biophys. Res. Commun. 2008 376 728 732 10.1016/j.bbrc.2008.09.050 18809385 · DOI
  93. [103]Burdge G.C. Lillycrop K.A. Fatty acids and epigenetics Curr. Opin. Clin. Nutr. Metab. Care 2014 17 156 161 10.1097/MCO.0000000000000023 24322369 · DOI
  94. [104]Niculescu M.D. Craciunescu C.N. Zeisel S.H. Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains FASEB J. 2006 20 43 49 10.1096/fj.05-4707com 16394266 PMC1635129 · DOI · Paper page
  95. [105]Medici V. Shibata N.M. Kharbanda K.K. Islam M.S. Keen C.L. Kim K. Tillman B. French S.W. Halsted C.H. LaSalle J.M. Maternal choline modifies fetal liver copper, gene expression, DNA methylation, and neonatal growth in the tx-j mouse model of Wilson disease Epigenetics 2014 9 286 296 10.4161/epi.27110 24220304 PMC3962539 · DOI
  96. [107]Wang B. Majumder S. Nuovo G. Kutay H. Volinia S. Patel T. Schmittgen T.D. Croce C. Ghoshal K. Jacob S.T. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice Hepatology 2009 50 1152 1161 10.1002/hep.23100 19711427 PMC2757532 · DOI
  97. [108]Pellanda H. Betaine homocysteine methyltransferase (BHMT)-dependent remethylation pathway in human healthy and tumoral liver Clin. Chem. Lab. Med. 2013 51 617 621 10.1515/cclm-2012-0689 23449526 · DOI
  98. [109]Li M. Cao L. Yang Y. The role of epigenetic modification in glucose and lipid metabolism Yi Chuan 2014 36 200 207 24846960
  99. [110]Ferrari A. Fiorino E. Giudici M. Gilardi F. Galmozzi A. Mitro N. Cermenati G. Godio C. Caruso D. de Fabiani E. Linking epigenetics to lipid metabolism: Focus on histone deacetylases Mol. Membr. Biol. 2012 29 257 266 10.3109/09687688.2012.729094 23095054 · DOI
  100. [111]El-Osta A. Brasacchio D. Yao D. Pocai A. Jones P.L. Roeder R.G. Cooper M.E. Brownlee M. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia J. Exp. Med. 2008 205 2409 2417 10.1084/jem.20081188 18809715 PMC2556800 · DOI · Paper page
  101. [112]Mali P. Chou B.K. Yen J. Ye Z. Zou J. Dowey S. Brodsky R.A. Ohm J.E. Yu W. Baylin S.B. Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-associated genes Stem Cells 2010 28 713 720 10.1002/stem.402 20201064 PMC3015217 · DOI · Paper page
  102. [113]Martin S.L. Hardy T.M. Tollefsbol T.O. Medicinal chemistry of the epigenetic diet and caloric restriction Curr. Med. Chem. 2013 20 4050 4059 10.2174/09298673113209990189 23895687 PMC3873820 · DOI
  103. [114]Qiu X. Brown K.V. Moran Y. Chen D. Sirtuin regulation in calorie restriction Biochim. Biophys. Acta 2010 1804 1576 1583 10.1016/j.bbapap.2009.09.015 19782772 · DOI
  104. [115]Ganguly A. Chen Y. Shin B.C. Devaskar S.U. Prenatal caloric restriction enhances DNA methylation and MeCP2 recruitment with reduced murine placental glucose transporter isoform 3 expression J. Nutr. Biochem. 2014 25 259 266 10.1016/j.jnutbio.2013.10.015 24445052 PMC4208916 · DOI
  105. [116]Plagemann A. Harder T. Brunn M. Harder A. Roepke K. Wittrock-Staar M. Ziska T. Schellong K. Rodekamp E. Melchior K. Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: An epigenetic model of obesity and the metabolic syndrome J. Physiol. 2009 587 4963 4976 10.1113/jphysiol.2009.176156 19723777 PMC2770159 · DOI · Paper page
  106. [117]Cho C.E. Sanchez-Hernandez D. Reza-Lopez S.A. Huot P.S. Kim Y.I. Anderson G.H. High folate gestational and post-weaning diets alter hypothalamic feeding pathways by DNA methylation in Wistar rat offspring Epigenetics 2013 8 710 719 10.4161/epi.24948 23803567 PMC3781190 · DOI
  107. [118]Ly A. Hoyt L. Crowell J. Kim Y.I. Folate and DNA methylation Antioxid. Redox Signal. 2012 17 302 326 10.1089/ars.2012.4554 22332737 · DOI
  108. [119]Crider K.S. Yang T.P. Berry R.J. Bailey L.B. Folate and DNA methylation: A review of molecular mechanisms and the evidence for folate’s role Adv. Nutr. 2012 3 21 38 10.3945/an.111.000992 22332098 PMC3262611 · DOI
  109. [120]Sinclair K.D. Allegrucci C. Singh R. Gardner D.S. Sebastian S. Bispham J. Thurston A. Huntley J.F. Rees W.D. Maloney C.A. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status Proc. Natl. Acad. Sci. USA 2007 104 19351 19356 10.1073/pnas.0707258104 18042717 PMC2148293 · DOI · Paper page
  110. [121]Zhou H.R. Zhang F.F. Ma Z.Y. Huang H.W. Jiang L. Cai T. Zhu J.K. Zhang C. He X.J. Folate polyglutamylation is involved in chromatin silencing by maintaining global DNA methylation and histone H3K9 dimethylation in Arabidopsis Plant Cell 2013 25 2545 2559 10.1105/tpc.113.114678 23881414 PMC3753382 · DOI
  111. [122]Xue J. Zempleni J. Epigenetic synergies between biotin and folate in the regulation of pro-inflammatory cytokines and repeats Scand. J. Immunol. 2013 78 419 425 10.1111/sji.12108 24007195 PMC3817955 · DOI
  112. [123]Pogribny I.P. Ross S.A. Tryndyak V.P. Pogribna M. Poirier L.A. Karpinets T.V. Histone H3 lysine 9 and H4 lysine 20 trimethylation and the expression of Suv4-20h2 and Suv-39h1 histone methyltransferases in hepatocarcinogenesis induced by methyl deficiency in rats Carcinogenesis 2006 27 1180 1186 10.1093/carcin/bgi364 16497704 · DOI
  113. [124]Tryndyak V.P. Ross S.A. Beland F.A. Pogribny I.P. Down-regulation of the microRNAs miR-34a, miR-127, and miR-200b in rat liver during hepatocarcinogenesis induced by a methyl-deficient diet Mol. Carcinog. 2009 48 479 487 10.1002/mc.20484 18942116 · DOI
  114. [125]Pogribny I.P. Starlard-Davenport A. Tryndyak V.P. Han T. Ross S.A. Rusyn I. Beland F.A. Difference in expression of hepatic microRNAs miR-29c, miR-34a, miR-155, and miR-200b is associated with strain-specific susceptibility to dietary nonalcoholic steatohepatitis in mice Lab. Invest. 2010 90 1437 1446 10.1038/labinvest.2010.113 20548288 PMC4281935 · DOI
  115. [126]Minor E.A. Court B.L. Young J.I. Wang G. Ascorbate induces ten-eleven translocation (Tet) methylcytosine dioxygenase-mediated generation of 5-hydroxymethylcytosine J. Biol. Chem. 2013 288 13669 13674 10.1074/jbc.C113.464800 23548903 PMC3650403 · DOI · Paper page
  116. [127]Moison C. Senamaud-Beaufort C. Fourriere L. Champion C. Ceccaldi A. Lacomme S. Daunay A. Tost J. Arimondo P.B. Guieysse-Peugeot A.L. DNA methylation associated with polycomb repression in retinoic acid receptor beta silencing FASEB J. 2013 27 1468 1478 10.1096/fj.12-210971 23299856 · DOI
  117. [128]Kuriyama M. Udagawa A. Yoshimoto S. Ichinose M. Sato K. Yamazaki K. Matsuno Y. Shiota K. Mori C. DNA methylation changes during cleft palate formation induced by retinoic acid in mice Cleft Palate Craniofac. J. 2008 45 545 551 10.1597/07-134.1 18788878 · DOI
  118. [129]Lee E.R. Murdoch F.E. Fritsch M.K. High histone acetylation and decreased polycomb repressive complex 2 member levels regulate gene specific transcriptional changes during early embryonic stem cell differentiation induced by retinoic acid Stem Cells 2007 25 2191 2199 10.1634/stemcells.2007-0203 17525233 · DOI
  119. [130]Urvalek A.M. Gudas L.J. Retinoic acid and histone deacetylases regulate epigenetic changes in embryonic stem cells J. Biol. Chem. 2014 289 19519 19530 10.1074/jbc.M114.556555 24821725 PMC4094062 · DOI
  120. [131]Urvalek A. Laursen K.B. Gudas L.J. The roles of retinoic acid and retinoic acid receptors in inducing epigenetic changes Subcell. Biochem. 2014 70 129 149 24962884 PMC4199334
  121. [133]Das S. Foley N. Bryan K. Watters K.M. Bray I. Murphy D.M. Buckley P.G. Stallings R.L. MicroRNA mediates DNA demethylation events triggered by retinoic acid during neuroblastoma cell differentiation Cancer Res. 2010 70 7874 7881 10.1158/0008-5472.CAN-10-1534 20841484 PMC2955783 · DOI
  122. [134]Hassan Y.I. Zempleni J. Epigenetic regulation of chromatin structure and gene function by biotin J. Nutr. 2006 136 1763 1765 16772434 PMC1479604
  123. [135]Huang Y. Khor T.O. Shu L. Saw C.L. Wu T.Y. Suh N. Yang C.S. Kong A.N. A gamma-tocopherol-rich mixture of tocopherols maintains Nrf2 expression in prostate tumors of TRAMP mice via epigenetic inhibition of CpG methylation J. Nutr. 2012 142 818 823 10.3945/jn.111.153114 22457388 PMC3327740 · DOI
  124. [136]Cornwell D.G. Ma J. Studies in vitamin E: Biochemistry and molecular biology of tocopherol quinones Vitam. Horm. 2007 76 99 134 17628173
  125. [137]Bobrowska-Korczak B. Skrajnowska D. Tokarz A. Effect of zinc and copper supplementation on the prognostic value of urinary 5-methyl-2’-deoxycytidine in DMBA-induced carcinogenesis in rats Cancer Biomark. 2013 13 403 410 24595076 PMC12928311
  126. [138]Wang L. Bammler T.K. Beyer R.P. Gallagher E.P. Copper-induced deregulation of microRNA expression in the zebrafish olfactory system Environ. Sci. Technol. 2013 47 7466 7474 23745839 PMC4750873
  127. [139]Yang G. Zhu Y. Dong X. Duan Z. Niu X. Wei J. TLT2-ICAM1-Gadd45alpha axis mediates the epigenetic effect of selenium on DNA methylation and gene expression in Keshan disease Biol. Trace Elem. Res. 2014 159 69 80 10.1007/s12011-014-9985-8 24811888 · DOI
  128. [140]Metes-Kosik N. Luptak I. Dibello P.M. Handy D.E. Tang S.S. Zhi H. Qin F. Jacobsen D.W. Loscalzo J. Joseph J. Both selenium deficiency and modest selenium supplementation lead to myocardial fibrosis in mice via effects on redox-methylation balance Mol. Nutr. Food Res. 2012 56 1812 1824 10.1002/mnfr.201200386 23097236 PMC3546539 · DOI
  129. [141]Szarc vel Szic K. Ndlovu M.N. Haegeman G. Vanden Berghe W. Nature or nurture: Let food be your epigenetic medicine in chronic inflammatory disorders Biochem. Pharmacol. 2010 80 1816 1832 10.1016/j.bcp.2010.07.029 20688047 · DOI
  130. [142]Khan S.I. Aumsuwan P. Khan I.A. Walker L.A. Dasmahapatra A.K. Epigenetic events associated with breast cancer and their prevention by dietary components targeting the epigenome Chem. Res. Toxicol. 2012 25 61 73 10.1021/tx200378c 21992498 · DOI
  131. [143]Vanden Berghe W. Epigenetic impact of dietary polyphenols in cancer chemoprevention: Lifelong remodeling of our epigenomes Pharmacol. Res. 2012 65 565 576 10.1016/j.phrs.2012.03.007 22465217 · DOI
  132. [144]Ong T.P. Moreno F.S. Ross S.A. Targeting the epigenome with bioactive food components for cancer prevention J. Nutrigenet. Nutr. 2011 4 275 292 10.1159/000334585 PMC3388269 22353664 · DOI

Cited by

Sorted by citations

Authors
Chango, A., & Pogribny, I.
Affiliations
  • Institut polytechnique LaSalle Beauvais (FR)
  • National Center for Toxicological Research (US)
Corresponding author
Chango, Abalo
Venue
Nutrients
Publisher
MDPI AG
Published
2015-04-14
Volume
7
Issue
4
Pages
2748-2770
ISSN
2072-6643 (ISSN-L)
OpenAlex
W2127552529
Cited by
144
References
12
Citations by year
2026: 5 · 2025: 11 · 2024: 6 · 2023: 6 · 2022: 16 · 2021: 11 · 2020: 12 · 2019: 19 · 2018: 13 · 2017: 25 · 2016: 14 · 2015: 6
FWCI
2.94
Type
journal article
Language
en
Open access
Locations
  • Nutrients (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Nutrition, Genetics, and Disease
Keywords
maternal nutrition, fetal epigenome, DNA methylation, histone modifications, microRNA, folic acid, choline, polyphenols, methyl donors, prenatal programming, epigenetic regulation, early life nutrition, chronic disease prevention
MeSH terms
Energy Intake, Diet, Dietary Carbohydrates, Dietary Fats, Dietary Proteins, Female, Fetus, Humans, Pregnancy, Micronutrients, Prenatal Nutritional Physiological Phenomena, Epigenesis, Genetic, Epigenomics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review