Advertisement

The AAPS Journal

, Volume 16, Issue 1, pp 27–36 | Cite as

Impact of Epigenetic Dietary Compounds on Transgenerational Prevention of Human Diseases

  • Yuanyuan LiEmail author
  • Sabita N. Saldanha
  • Trygve O. Tollefsbol
Review Article Theme: Natural Products Drug Discovery in Cancer Prevention

Abstract

The etiology of most human diseases involves complicated interactions of multiple environmental factors with individual genetic background which is initially generated early in human life, for example, during the processes of embryogenesis and fetal development in utero. Early embryogenesis includes a series of programming processes involving extremely accurate time-controlled gene activation/silencing expressions, and epigenetic control is believed to play a key role in regulating early embryonic development. Certain dietary components with properties in influencing epigenetic processes are believed to have preventive effects on many human diseases such as cancer. Evidence shows that in utero exposure to certain epigenetic diets may lead to reprogramming of primary epigenetic profiles such as DNA methylation and histone modifications on the key coding genes of the fetal genome, leading to different susceptibility to diseases later in life. In this review, we assess the current advances in dietary epigenetic intervention on transgenerational human disease control. Enhanced understanding of the important role of early life epigenetics control may lead to cost-effective translational chemopreventive potential by appropriate administration of prenatal and/or postnatal dietary supplements leading to early disease prevention.

KEY WORDS

diet embryogenesis epigenetic human diseases prevention transgenerational 

Abbreviations

DNMT

DNA methyltransferase

HDACs

Histone deacetylases

HATs

Histone acetyltransferases

SFN

Sulforaphane

EGCG

(−)-Epigallocatechin-3-gallate

SAM

S-adenosylmethionine

NTDs

Neural tube defects

ER

Estrogen receptor

NCDs

Noncommunicable diseases

Notes

ACKNOWLEDGMENTS

This work was supported by grants from the American Institute for Cancer Research.

Conflict of Interest

The authors declare that they have no competing interests.

REFERENCES

  1. 1.
    Jablonka A, Raz G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Quart Rev Biol. 2009;84(2):131–76.PubMedCrossRefGoogle Scholar
  2. 2.
    Cantone I, Fisher AG. Epigenetic programming and reprogramming during development. Nat Struct Mol Biol. 2013;20(3):282–9.PubMedCrossRefGoogle Scholar
  3. 3.
    Ho L, Crabtree GR. Chromatin remodeling during development. Nature. 2010;463(7280):474–84.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Gopalakrishnan S, Van Emburgh BO, Robertson KD. DNA methylation in development and human disease. Mutat Res. 2008;647(1–2):30–8.PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Avner P, Heard E. X-chromosome inactivation: counting, choice and initiation. Nat Rev Genet. 2001;2(1):59–67.PubMedCrossRefGoogle Scholar
  6. 6.
    Lee JT, Bartolomei MS. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell. 2013;152(6):1308–23.PubMedCrossRefGoogle Scholar
  7. 7.
    Tomizawa S, Sasaki H. Genomic imprinting and its relevance to congenital disease, infertility, molar pregnancy and induced pluripotent stem cell. J Hum Genet. 2012;57(2):84–91.PubMedCrossRefGoogle Scholar
  8. 8.
    Meeran SM, Ahmed A, Tollefsbol TO. Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clin Epigenetics. 2010;1(3–4):101–16.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Hardy TM, Tollefsbol TO. Epigenetic diet: impact on the epigenome and cancer. Epigenomics. 2011;3(4):503–18.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Messina MJ, Persky V, Setchell KD, Barnes S. Soy intake and cancer risk: a review of the in vitro and in vivo data. Nutr Cancer. 1994;21(2):113–31.PubMedCrossRefGoogle Scholar
  11. 11.
    Cheung KL, Kong AN. Molecular targets of dietary phenethyl isothiocyanate and sulforaphane for cancer chemoprevention. AAPS J. 2010;12(1):87–97.PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Singh BN, Shankar S, Srivastava RK. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem Pharmacol. 2011;82(12):1807–21.PubMedCrossRefGoogle Scholar
  13. 13.
    Li Y, Liu L, Andrews L, Tollefsbol T. Genistein depletes telomerase activity through cross-talk between genetic and epigenetic mechanisms. Int J Cancer. 2009;125(2):286–96.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Berghe WV. Epigenetic impact of dietary polyphenols in cancer chemoprevention: lifelong remodeling of our epigenomes. Pharmacol Res. 2012;65:565–76.CrossRefGoogle Scholar
  15. 15.
    Canani RB, Di Costanzo M, Leone L, Bedogni G, Brambilla P, Cianfarani S, et al. Epigenetic mechanisms elicited by nutrition in early life. Nutr Res Rev. 2011;24:198–205.PubMedCrossRefGoogle Scholar
  16. 16.
    Ordovás JM, Smith CE. Epigenetics and cardiovascular disease. Nat Rev Cardiol. 2010;7(9):510–9.PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Vanhees K, Coort S, Ruijters EJ, Godschalk RW, van Schooten FJ, van Waalwijk B, et al. Epigenetics: prenatal exposure to genistein leaves a permanent signature on the hematopoietic lineage. FASEB J. 2011;25(2):797–807.PubMedCrossRefGoogle Scholar
  18. 18.
    Nelson NJ. Migrant studies aid the search for factors linked to breast cancer risk. J Natl Cancer Inst. 2006;98(7):436–8.PubMedCrossRefGoogle Scholar
  19. 19.
    Mosley BS, Cleves MA, Siega-Riz AM, Shaw GM, Canfield MA, Waller DK, et al. Neural tube defects and maternal folate intake among pregnancies conceived after folic acid fortification in the United States. Am J Epidemiol. 2009;169(1):9–17.PubMedCrossRefGoogle Scholar
  20. 20.
    Strogantsev R, Ferguson-Smith AC. Proteins involved in establishment and maintenance of imprinted methylation marks. Brief Funct Genomics. 2012;11(3):227–39.PubMedCrossRefGoogle Scholar
  21. 21.
    Robertson KD. DNA methylation and chromatin—unraveling the tangled web. Oncogene. 2002;21(35):5361–79.PubMedCrossRefGoogle Scholar
  22. 22.
    Deaton A, Bird A. CpG islands and the regulation of transcription. Genes and Dev. 2011;25:1010–22.PubMedCrossRefGoogle Scholar
  23. 23.
    Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet. 2005;14(1):R47–58.PubMedCrossRefGoogle Scholar
  24. 24.
    Haaf T. Methylation dynamics in the early mammalian embryo: implications of genome reprogramming defects for development. Curr Top Microbiol Immunol. 2006;310:13–22.PubMedGoogle Scholar
  25. 25.
    Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem. 2005;74:481–514.PubMedCrossRefGoogle Scholar
  26. 26.
    Chen T, Tsujimoto N, Li E. The PWWP domain of Dnmt3a and Dnmt3b is required for directing DNA methylation to the major satellite repeats at pericentric heterochromatin. Mol Cell Biol. 2004;24(20):9048–58.PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Okano M, Bell D, Haber D, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999;99(3):247–57.PubMedCrossRefGoogle Scholar
  28. 28.
    Okano M, Takebayashi S, Okumura K, Li E. Assignment of cytosine-5 DNA methyltransferases Dnmt3a and Dnmt3b to mouse chromosome bands 12A2-A3 and 2H1 by in situ hybridization. Cytogenet Cell Genet. 1999;86(3–4):333–4.PubMedCrossRefGoogle Scholar
  29. 29.
    Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet. 1998;19(3):219–20.PubMedCrossRefGoogle Scholar
  30. 30.
    Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science. 2001;294(5551):2536–9.PubMedCrossRefGoogle Scholar
  31. 31.
    Hata K, Okano M, Lei H, Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development. 2002;129(8):1983–93.PubMedGoogle Scholar
  32. 32.
    Berger SL. Histone modifications in transcriptional regulation. Curr Opin Genet Dev. 2002;12(2):142–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Rugg-Gunn PJ, Cox BJ, Ralston A, Rossant J. Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc Natl Acad Sci U S A. 2010;107(24):10783–90.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature. 2007;445(7124):214–8.PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Bedford MT. Arginine methylation at a glance. J Cell Sci. 2007;120(Pt 24):4243–6.PubMedCrossRefGoogle Scholar
  36. 36.
    Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, et al. Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science. 2002;298(5595):1039–43.PubMedCrossRefGoogle Scholar
  37. 37.
    Byrd KN, Shearn A. ASH1, a Drosophila trithorax group protein, is required for methylation of lysine 4 residues on histone H3. Proc Natl Acad Sci U S A. 2003;100(20):11535–40.PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Schnerch A, Lee JB, Graham M, Guezguez B, Bhatia M. Human embryonic stem cell-derived hematopoietic cells maintain core epigenetic machinery of the polycomb group/trithorax group complexes distinctly from functional adult hematopoietic stem cells. Stem Cells Dev. 2013;22(1):73–89.PubMedCrossRefGoogle Scholar
  39. 39.
    Hochedlinger K, Plath K. Epigenetic reprogramming and induced pluripotency. Development. 2009;136(4):509–23.PubMedCrossRefGoogle Scholar
  40. 40.
    Lindeman LC, Winata CL, Aanes H, Mathavan S, Alestrom P, Collas P. Chromatin states of developmentally-regulated genes revealed by DNA and histone methylation patterns in zebrafish embryos. Int J Dev Biol. 2010;54(5):803–13.PubMedCrossRefGoogle Scholar
  41. 41.
    Tachibana M, Sugimoto K, Nozaki M, Ueda J, Ohta T, Ohki M, et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 2002;16(14):1779–91.PubMedCrossRefGoogle Scholar
  42. 42.
    Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125(2):315–26.PubMedCrossRefGoogle Scholar
  43. 43.
    Aranda P, Agirre X, Ballestar E, Andreu EJ, Román-Gómez J, Prieto I, et al. Epigenetic signatures associated with different levels of differentiation potential in human stem cells. PLoS One. 2009;4(11):e7809.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, et al. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell. 2009;4(1):80–93.PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Li Y, Tollefsbol TO. Impact on DNA methylation in cancer prevention and therapy by bioactive dietary components. Curr Med Chem. 2010;17(20):2141–51.PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Waterland RA, Jirtle RL. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition. 2004;20(1):63–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Lucock M. Folic acid: nutritional biochemistry, molecular biology, and role in disease processes. Mol Genet Metab. 2000;71(1–2):121–38.PubMedCrossRefGoogle Scholar
  48. 48.
    Hoffman DR, Cornatzer WE, Duerre JA. Relationship between tissue levels of S-adenosylmethionine, S-adenylhomocysteine, and transmethylation reactions. Can J Biochem. 1979;57(1):56–65.PubMedCrossRefGoogle Scholar
  49. 49.
    McKay JA, Williams EA, Mathers JC. Folate and DNA methylation during in utero development and aging. Biochem Soc Trans. 2004;32(Pt 6):1006–7.PubMedGoogle Scholar
  50. 50.
    Kim YI. Methylenetetrahydrofolate reductase polymorphisms, folate, and cancer risk: a paradigm of gene-nutrient interactions in carcinogenesis. Nutr Rev. 2000;58(7):205–9.PubMedCrossRefGoogle Scholar
  51. 51.
    Pitkin RM. Folate and neural tube defects. Am J Clin Nutr. 2007;85(1):285S–8S.PubMedGoogle Scholar
  52. 52.
    Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 1998;12(11):949–57.PubMedGoogle Scholar
  53. 53.
    Yen TT, Gill AM, Frigeri LG, Barsh GS, Wolff GL. Obesity, diabetes, and neoplasia in yellow A(vy)/-mice: ectopic expression of the agouti gene. FASEB J. 1994;8(8):479–88.PubMedGoogle Scholar
  54. 54.
    Kim YI. Nutritional epigenetics: impact of folate deficiency on DNA methylation and colon cancer susceptibility. J Nutr. 2005;135(11):2703–9.PubMedGoogle Scholar
  55. 55.
    Balaghi M, Wagner C. DNA methylation in folate deficiency: use of CpG methylase. Biochem Biophys Res Commun. 1993;193:1184–90.PubMedCrossRefGoogle Scholar
  56. 56.
    Thompson JR, Gerald PF, Willoughby ML, Armstrong BK. Maternal folate supplementation in pregnancy and protection against acute lymphoblastic leukaemia in childhood: a case–control study. Lancet. 2001;358(9297):1935–40.PubMedCrossRefGoogle Scholar
  57. 57.
    Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A. 2007;104(49):19351–6.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Munro IC, Harwood M, Hlywka JJ, Stephen AM, Doull J, Flamm WG, et al. Soy isoflavones: a safety review. Nutr Rev. 2003;61(1):1–33.PubMedCrossRefGoogle Scholar
  59. 59.
    Wang TT, Sathyamoorthy N, Phang JM. Molecular effects of genistein on estrogen receptor mediated pathways. Carcinogenesis. 1996;17(2):271–5.PubMedCrossRefGoogle Scholar
  60. 60.
    Barnes S. Effect of genistein on in vitro and in vivo models of cancer. J Nutr. 1995;125(3 Suppl):777S–83S.PubMedGoogle Scholar
  61. 61.
    Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect. 2006;114(4):567–72.PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Li Y, Meeran SM, Patel SN, Chen H, Hardy TM, Tollefsbol TO. Epigenetic reactivation of estrogen receptor-α (ERα) by genistein enhances hormonal therapy sensitivity in ERα-negative breast cancer. Mol Cancer. 2013;12:19.CrossRefGoogle Scholar
  63. 63.
    Wu AH, Wan P, Hankin J, Tseng CC, Yu MC, Pike MC. Adolescent and adult soy intake and risk of breast cancer in Asian-Americans. Carcinogenesis. 2002;23(9):1491–6.PubMedCrossRefGoogle Scholar
  64. 64.
    Warri A, Saarinen NM, Makela S, Hilakivi-Clarke L. The role of early life genistein exposures in modifying breast cancer risk. Br J Cancer. 2008;98(9):1485–93.PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    De Assis S, Hilakivi-Clarke L. Timing of dietary estrogenic exposures and breast cancer risk. Ann N Y Acad Sci. 2006;1089:14–35.PubMedCrossRefGoogle Scholar
  66. 66.
    Hilakivi-Clarke L, Cho E, Onojafe I, Raygada M, Clarke R. Maternal exposure to genistein during pregnancy increases carcinogen-induced mammary tumorigenesis in female rat offspring. Oncol Rep. 1999;6(5):1089–95.PubMedGoogle Scholar
  67. 67.
    Foster WG, Younglai EV, Boutross-Tadross O, Hughes CL, Wade MG. Mammary gland morphology in Sprague–Dawley rats following treatment with an organochlorine mixture in utero and neonatal genistein. Toxicol Sci. 2004;77(1):91–100.PubMedCrossRefGoogle Scholar
  68. 68.
    Su Y, Eason RR, Geng Y, Till SR, Badger TM, Simmen RC. In utero exposure to maternal diets containing soy protein isolate, but not genistein alone, protects young adult rat offspring from NMU-induced mammary tumorigenesis. Carcinogenesis. 2007;28(5):1046–51.PubMedCrossRefGoogle Scholar
  69. 69.
    Parnaud G, Li P, Cassar G, Rouimi P, Tulliez J, Combaret L, et al. Mechanism of sulforaphane-induced cell cycle arrest and apoptosis in human colon cancer cells. Nutr Cancer. 2004;48(2):198–206.PubMedCrossRefGoogle Scholar
  70. 70.
    Bertl E, Bartsch H, Gerhäuser C. Inhibition of angiogenesis and endothelial cell functions are novel sulforaphane-mediated mechanisms in chemoprevention. Mol Cancer Ther. 2006;5(3):575–85.PubMedCrossRefGoogle Scholar
  71. 71.
    Myzak MC, Karplus PA, Chung FL, Dashwood RH. A novel mechanism of chemoprotection by sulforaphane: inhibition of histone deacetylase. Cancer Res. 2004;64(16):5767–74.PubMedCrossRefGoogle Scholar
  72. 72.
    Meeran SM, Patel SN, Li Y, Shukla S, Tollefsbol TO. Bioactive dietary supplements reactivate ER expression in ER-negative breast cancer cells by active chromatin modifications. PLoS One. 2012;7(5):e37748.PubMedCentralPubMedCrossRefGoogle Scholar
  73. 73.
    Ziegler RG, Hoover RN, Pike MC, Hildesheim A, Nomura AM, West DW, et al. Migration patterns and breast cancer risk in Asian-American women. J Natl Cancer Inst. 1993;85(22):1819–27.PubMedCrossRefGoogle Scholar
  74. 74.
    Kakehi Y. Epidemiology and clinical features of prostate cancer in Japan. Nihon Rinsho. 1998;56(8):1969–73.PubMedGoogle Scholar
  75. 75.
    Kerns ML, DePianto D, Dinkova-Kostova AT, Talalay P, Coulombe PA. Reprogramming of keratin biosynthesis by sulforaphane restores skin integrity in epidermolysis bullosa simplex. Proc Natl Acad Sci U S A. 2007;104(36):14460–5.PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Bushman JL. Green tea and cancer in humans: a review of the literature. Nutr Cancer. 1998;31(3):151–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Tipoe GL, Leung TM, Hung MW, Fung ML. Green tea polyphenols as an anti-oxidant and anti-inflammatory agent for cardiovascular protection. Cardiovasc Hematol Disord Drug Targets. 2007;7(2):135–44.PubMedCrossRefGoogle Scholar
  78. 78.
    Raederstorff DG, Schlachter MF, Elste V, Weber P. Effect of EGCG on lipid absorption and plasma lipid levels in rats. J Nutr Biochem. 2003;14(6):326–32.PubMedCrossRefGoogle Scholar
  79. 79.
    Berletch JB, Liu C, Love WK, Andrews LG, Katiyar SK, Tollefsbol TO. Epigenetic and genetic mechanisms contribute to telomerase inhibition by EGCG. J Cell Biochem. 2008;103(2):509–19.PubMedCentralPubMedCrossRefGoogle Scholar
  80. 80.
    Fang MZ, Wang Y, Ai N, Hou Z, Sun Y, Lu H, et al. Tea polyphenol (−)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res. 2003;63(22):7563–70.PubMedGoogle Scholar
  81. 81.
    Fang M, Chen D, Yang CS. Dietary polyphenols may affect DNA methylation. J Nutr. 2007;137(1 Suppl):223S–8S.PubMedGoogle Scholar
  82. 82.
    Castro DJ, Yu Z, Löhr CV, Pereira CB, Giovanini JN, Fischer KA, et al. Chemoprevention of dibenzo[a, l]pyrene transplacental carcinogenesis in mice born to mothers administered green tea: primary role of caffeine. Carcinogenesis. 2008;29(8):1581–6.PubMedCrossRefGoogle Scholar
  83. 83.
    Yang P, Li H. Epigallocatechin-3-gallate ameliorates hyperglycemia-induced embryonic vasculopathy and malformation by inhibition of Foxo3a activation. Am J Obstet Gynecol. 2010;203(1):75.e1–6.CrossRefGoogle Scholar
  84. 84.
    Long L, Li Y, Wang YD, He QY, Li M, Cai XD, et al. The preventive effect of oral EGCG in a fetal alcohol spectrum disorder mouse model. Alcohol Clin Exp Res. 2010;34(11):1929–36.PubMedCrossRefGoogle Scholar
  85. 85.
    Chen JR, Zhang J, Lazarenko OP, Kang P, Blackburn ML, Ronis MJ, et al. Inhibition of fetal bone development through epigenetic down-regulation of HoxA10 in obese rats fed high-fat diet. FASEB J. 2012;26(3):1131–41.PubMedCrossRefGoogle Scholar
  86. 86.
    Choi SW, Friso S. Epigenetics: a new bridge between nutrition and health. Adv Nutr. 2010;1(1):8–16.PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Perrine SP, Rudolph A, Faller DV, Roman C, Cohen RA, Chen SJ, et al. Butyrate infusions in the ovine fetus delay the biologic clock for globin gene switching. Proc Natl Acad Sci U S A. 1988;85(22):8540–2.PubMedCentralPubMedCrossRefGoogle Scholar
  88. 88.
    Yu Z, Mahadevan B, Löhr CV, Fischer KA, Louderback MA, Krueger SK, et al. Indole-3-carbinol in the maternal diet provides chemoprotection for the fetus against transplacental carcinogenesis by the polycyclic aromatic hydrocarbon dibenzo[a, l]pyrene. Carcinogenesis. 2006;27(10):2116–23.PubMedCrossRefGoogle Scholar
  89. 89.
    Xia X, Cai H, Qin S, Xu C. Histone acetylase inhibitor curcumin impairs mouse spermiogenesis—an in vitro study. PLoS One. 2012;7(11):e48673.PubMedCentralPubMedCrossRefGoogle Scholar
  90. 90.
    Kapusta L, Haagmans ML, Steegers EA, Cuypers MH, Blom HJ, Eskes TK. Congenital heart defects and maternal derangement of homocysteine metabolism. J Pediatr. 1999;135(6):773–4.PubMedCrossRefGoogle Scholar
  91. 91.
    Li DK, Daling JR, Mueller BA, Hickok DE, Fantel AG, Weiss NS. Periconceptional multivitamin use in relation to the risk of congenital urinary tract anomalies. Epidemiology. 1995;6(3):212–8.PubMedCrossRefGoogle Scholar
  92. 92.
    Frias AE, Grove KL. Obesity: a transgenerational problem linked to nutrition during pregnancy. Semin Reprod Med. 2012;30(6):472–8.PubMedCentralPubMedCrossRefGoogle Scholar
  93. 93.
    Dabelea D, Crume T. Maternal environment and the transgenerational cycle of obesity and diabetes. Diabetes. 2011;60(7):1849–55.PubMedCrossRefGoogle Scholar
  94. 94.
    Boqué N, de la Iglesia R, de la Garza AL, Milagro FI, Olivares M, Bañuelos O, et al. Prevention of diet-induced obesity by apple polyphenols in Wistar rats through regulation of adipocyte gene expression and DNA methylation patterns. Mol Nutr Food Res. 2013;57(8):1473–8.PubMedCrossRefGoogle Scholar
  95. 95.
    Milagro FI, Campión J, García-Díaz DF, Goyenechea E, Paternain L, Martínez JA. High fat diet-induced obesity modifies the methylation pattern of leptin promoter in rats. J Physiol Biochem. 2009;65(1):1–9.PubMedCrossRefGoogle Scholar
  96. 96.
    Takada I, Mihara M, Suzawa M, Ohtake F, Kobayashi S, Igarashi M, et al. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol. 2007;9(11):1273–85.PubMedCrossRefGoogle Scholar
  97. 97.
    Waterland RA, Travisano M, Tahiliani KG, Rached MT, Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond). 2008;32(9):1373–9.CrossRefGoogle Scholar
  98. 98.
    Ejaz A, Wu D, Kwan P, Meydani M. Curcumin inhibits adipogenesis in 3T3-L1 adipocytes and angiogenesis and obesity in C57/BL mice. J Nutr. 2009;139(5):919–25.PubMedCrossRefGoogle Scholar
  99. 99.
    Campión J, Milagro FI, Martínez JA. Individuality and epigenetics in obesity. Obes Rev. 2009;10(4):383–92.PubMedCrossRefGoogle Scholar
  100. 100.
    Li S, Tse IM, Li ET. Maternal green tea extract supplementation to rats fed a high-fat diet ameliorates insulin resistance in adult male offspring. J Nutr Biochem. 2012;23(12):1655–60.PubMedCrossRefGoogle Scholar

Copyright information

© American Association of Pharmaceutical Scientists 2013

Authors and Affiliations

  • Yuanyuan Li
    • 1
    • 6
    Email author
  • Sabita N. Saldanha
    • 1
    • 5
  • Trygve O. Tollefsbol
    • 1
    • 2
    • 3
    • 4
  1. 1.Department of BiologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Center for AgingUniversity of Alabama at BirminghamBirminghamUSA
  3. 3.Comprehensive Cancer CenterUniversity of Alabama at BirminghamBirminghamUSA
  4. 4.Nutrition Obesity Research CenterUniversity of Alabama at BirminghamBirminghamUSA
  5. 5.Department of Math and SciencesAlabama State UniversityMontgomeryUSA
  6. 6.BirminghamUSA

Personalised recommendations