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Epigenetic effects of paternal diet on offspring: emphasis on obesity

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Abstract

Overnutrition, obesity, and the rise in associated comorbidities are widely recognized as preventable challenges to global health. Behavioral, metabolic, and epigenetic influences that alter the epigenome, when passed on to offspring, can increase their risk of developing an altered metabolic profile. This review is focused on the role of paternal inheritance as demonstrated by clinical, epidemiological, and experimental models. Development of additional experimental models that resemble the specific epigenetic sensitive situations in human studies will be essential to explore paternally induced trans-generational effects that are mediated, primarily, by epigenetic effects. Further elucidation of epigenetic marks will help identify preventive and therapeutic targets, which in combination with healthy lifestyle choices, can diminish the growing tide of obesity, type 2 diabetes, and other related disorders.

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References

  1. C.L. Ogden, M.D. Carroll, B.K. Kit, K.M. Flegal, Prevalence of obesity in the United States, 2009–2010. NCHS Data Br. 82, 1–8 (2012)

    Google Scholar 

  2. C.L. Ogden, M.D. Carroll, B.K. Kit, K.M. Flegal, Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA, J. Am. Med. Assoc. 307, 483–490 (2012)

    Article  Google Scholar 

  3. K.M. Flegal, M.D. Carroll, B.K. Kit, C.L. Ogden, Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA, J. Am. Med. Assoc. 307, 491–497 (2012)

    Article  Google Scholar 

  4. C. Bouchard, Childhood obesity: are genetic differences involved? Am. J. Clin. Nutr. 89, 1494S–1501S (2009)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. R.A. Waterland, Epigenetic epidemiology of obesity: application of epigenomic technology. Nutr. Rev. 66(Suppl 1), S21–23 (2008)

    Article  PubMed  Google Scholar 

  6. R.C. Whitaker, J.A. Wright, M.S. Pepe, K.D. Seidel, W.H. Dietz, Predicting obesity in young adulthood from childhood and parental obesity. New Engl. J. Med. 337, 869–873 (1997)

    Article  CAS  PubMed  Google Scholar 

  7. M.E. Pembrey, L.O. Bygren, G. Kaati, S. Edvinsson, K. Northstone, M. Sjostrom, J. Golding, A.S. Team, Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 14, 159–166 (2006)

    Article  PubMed  Google Scholar 

  8. C. Bouchard, A. Tremblay, J.P. Despres, A. Nadeau, P.J. Lupien, G. Theriault, J. Dussault, S. Moorjani, S. Pinault, G. Fournier, The response to long-term overfeeding in identical twins. New Engl. J. Med. 322, 1477–1482 (1990)

    Article  CAS  PubMed  Google Scholar 

  9. J. Wardle, S. Carnell, C.M. Haworth, R. Plomin, Evidence for a strong genetic influence on childhood adiposity despite the force of the obesogenic environment. Am. J. Clin. Nutr. 87, 398–404 (2008)

    CAS  PubMed  Google Scholar 

  10. A.P. Wolffe, D. Guschin, Review: chromatin structural features and targets that regulate transcription. J. Struct. Biol. 129, 102–122 (2000)

    Article  CAS  PubMed  Google Scholar 

  11. A.F. Fleisch, R.O. Wright, A.A. Baccarelli, Environmental epigenetics: a role in endocrine disease? J. Mol. Endocrinol. 49(2), R61–R67 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. J.K. Kim, M. Samaranayake, S. Pradhan, Epigenetic mechanisms in mammals. Cell. Mol. Life Sci. 66, 596–612 (2009)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. S. Sharma, T.K. Kelly, P.A. Jones, Epigenetics in cancer. Carcinogenesis 31, 27–36 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. F.I. Milagro, M.L. Mansego, C. De Miguel, J.A. Martinez, Dietary factors, epigenetic modifications and obesity outcomes: progresses and perspectives. Mol. Asp. Med. 34(4), 782–812 (2013)

    Article  CAS  Google Scholar 

  15. J.C. Jimenez-Chillaron, R. Diaz, D. Martinez, T. Pentinat, M. Ramon-Krauel, S. Ribo, T. Plosch, The role of nutrition on epigenetic modifications and their implications on health. Biochimie 94(11), 2242–2263 (2012)

    Article  CAS  PubMed  Google Scholar 

  16. S.U. Devaskar, S. Raychaudhuri, Epigenetics–a science of heritable biological adaptation. Pediatr. Res. 61, 1R–4R (2007)

    Article  PubMed  Google Scholar 

  17. A. Marti, J. Ordovas, Epigenetics lights up the obesity field. Obes. Facts 4, 187–190 (2011)

    Article  PubMed  Google Scholar 

  18. A.C. Ferguson-Smith, M.E. Patti, You are what your dad ate. Cell Metab. 13, 115–117 (2011)

    Article  CAS  PubMed  Google Scholar 

  19. B.R. Carone, L. Fauquier, N. Habib, J.M. Shea, C.E. Hart, R. Li, C. Bock, C. Li, H. Gu, P.D. Zamore, A. Meissner, Z. Weng, H.A. Hofmann, N. Friedman, O.J. Rando, Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084–1096 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. A. Ferguson-Smith, S.P. Lin, C.E. Tsai, N. Youngson, M. Tevendale, Genomic imprinting–insights from studies in mice. Semin. Cell Dev. Biol. 14, 43–49 (2003)

    Article  CAS  PubMed  Google Scholar 

  21. A. Soubry, J.M. Schildkraut, A. Murtha, F. Wang, Z. Huang, A. Bernal, J. Kurtzberg, R.L. Jirtle, S.K. Murphy, C. Hoyo, Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a newborn epigenetics study (NEST) cohort. BMC Med. 11, 29 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. M.J. Luteijn, R.F. Ketting, PIWI-interacting RNAs: from generation to transgenerational epigenetics. Nat. Rev. Genet. 14, 523–534 (2013)

    Article  CAS  PubMed  Google Scholar 

  23. C. Gallou-Kabani, C. Junien, Nutritional epigenomics of metabolic syndrome: new perspective against the epidemic. Diabetes 54, 1899–1906 (2005)

    Article  CAS  PubMed  Google Scholar 

  24. E.L. Sullivan, K.L. Grove, Metabolic imprinting in obesity. Forum Nutr. 63, 186–194 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. F. Perera, J. Herbstman, Prenatal environmental exposures, epigenetics, and disease. Reprod. Toxicol. 31, 363–373 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  26. W. Reik, W. Dean, J. Walter, Epigenetic reprogramming in mammalian development. Science 293, 1089–1093 (2001)

    Article  CAS  PubMed  Google Scholar 

  27. L. Shi, J. Wu, Epigenetic regulation in mammalian preimplantation embryo development. Reprod. Biol. Endocrinol. 7, 59 (2009)

    Article  PubMed Central  PubMed  Google Scholar 

  28. B.T. Heijmans, E.W. Tobi, A.D. Stein, H. Putter, G.J. Blauw, E.S. Susser, P.E. Slagboom, L.H. Lumey, Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. USA 105, 17046–17049 (2008)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. H.T. Bjornsson, M.I. Sigurdsson, M.D. Fallin, R.A. Irizarry, T. Aspelund, H. Cui, W. Yu, M.A. Rongione, T.J. Ekstrom, T.B. Harris, L.J. Launer, G. Eiriksdottir, M.F. Leppert, C. Sapienza, V. Gudnason, A.P. Feinberg, Intra-individual change over time in DNA methylation with familial clustering. JAMA, J. Am. Med. Assoc. 299, 2877–2883 (2008)

    Article  CAS  Google Scholar 

  30. M.K. Skinner, Metabolic disorders: Fathers’ nutritional legacy. Nature 467, 922–923 (2010)

    Article  CAS  PubMed  Google Scholar 

  31. N.A. Youngson, E. Whitelaw, The effects of acquired paternal obesity on the next generation. Asian J. Androl. 13, 195–196 (2011)

    Article  PubMed Central  PubMed  Google Scholar 

  32. S.S. Hammoud, D.A. Nix, H. Zhang, J. Purwar, D.T. Carrell, B.R. Cairns, Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473–478 (2009)

    PubMed Central  CAS  PubMed  Google Scholar 

  33. K.D. Wagner, N. Wagner, H. Ghanbarian, V. Grandjean, P. Gounon, F. Cuzin, M. Rassoulzadegan, RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev. Cell 14, 962–969 (2008)

    Article  CAS  PubMed  Google Scholar 

  34. L. Siggens, K. Ekwall, Epigenetics, chromatin and genome organisation: recent advances from the ENCODE project. J. Int. Med. (2014). doi:10.1111/joim.12231

    Google Scholar 

  35. U. Brykczynska, M. Hisano, S. Erkek, L. Ramos, E.J. Oakeley, T.C. Roloff, C. Beisel, D. Schubeler, M.B. Stadler, A.H. Peters, Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679–687 (2010)

    Article  CAS  PubMed  Google Scholar 

  36. S. Erkek, M. Hisano, C.Y. Liang, M. Gill, R. Murr, J. Dieker, D. Schubeler, J. van der Vlag, M.B. Stadler, A.H. Peters, Molecular determinants of nucleosome retention at CpG-rich sequences in mouse spermatozoa. Nat. Struct. Mol. Biol. 20, 868–875 (2013)

    Article  CAS  PubMed  Google Scholar 

  37. A. Arpanahi, M. Brinkworth, D. Iles, S.A. Krawetz, A. Paradowska, A.E. Platts, M. Saida, K. Steger, P. Tedder, D. Miller, Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res. 19, 1338–1349 (2009)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. S.S. Hammoud, D.A. Nix, A.O. Hammoud, M. Gibson, B.R. Cairns, D.T. Carrell, Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum. Reprod. 26, 2558–2569 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. A.M. Roccaro, A. Sacco, X. Jia, A.K. Azab, P. Maiso, H.T. Ngo, F. Azab, J. Runnels, P. Quang, I.M. Ghobrial, microRNA-dependent modulation of histone acetylation in Waldenstrom macroglobulinemia. Blood 116, 1506–1514 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. H. Denis, M.N. Ndlovu, F. Fuks, Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep. 12, 647–656 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. F.J. Ortega, J.M. Mercader, V. Catalan, J.M. Moreno-Navarrete, N. Pueyo, M. Sabater, J. Gomez-Ambrosi, R. Anglada, J.A. Fernandez-Formoso, W. Ricart, G. Fruhbeck, J.M. Fernandez-Real, Targeting the circulating microRNA signature of obesity. Clin. Chem. 59, 781–792 (2013)

    Article  CAS  PubMed  Google Scholar 

  42. H.W. Bakos, M. Mitchell, B.P. Setchell, M. Lane, The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int. J. Androl. 34, 402–410 (2011)

    Article  CAS  PubMed  Google Scholar 

  43. M. Mitchell, H.W. Bakos, M. Lane, Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil. Steril. 95, 1349–1353 (2011)

    Article  PubMed  Google Scholar 

  44. B.I. Ghanayem, R. Bai, G.E. Kissling, G. Travlos, U. Hoffler, Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol. Reprod. 82, 96–104 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. N.K. Binder, N.J. Hannan, D.K. Gardner, Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 7, e52304 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. T. Fullston, E.M. Ohlsson Teague, N.O. Palmer, M.J. Deblasio, M. Mitchell, M. Corbett, C.G. Print, J.A. Owens, M. Lane, Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 27, 4226–4243 (2013)

    Article  CAS  PubMed  Google Scholar 

  47. T. Fullston, N.O. Palmer, J.A. Owens, M. Mitchell, H.W. Bakos, M. Lane, Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum. Reprod. 27, 1391–1400 (2012)

    Article  CAS  PubMed  Google Scholar 

  48. N.O. McPherson, T. Fullston, H.W. Bakos, B.P. Setchell, M. Lane, Obese father’s metabolic state, adiposity, and reproductive capacity indicate son’s reproductive health. Fertil. Steril. 101, 865–873 (2014)

    Article  PubMed  Google Scholar 

  49. N.O. Palmer, H.W. Bakos, J.A. Owens, B.P. Setchell, M. Lane, Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am. J. Physiol. Endocrinol. Metab. 302, E768–780 (2012)

    Article  CAS  PubMed  Google Scholar 

  50. N.O. McPherson, H.W. Bakos, J.A. Owens, B.P. Setchell, M. Lane, Improving metabolic health in obese male mice via diet and exercise restores embryo development and fetal growth. PLoS One 8, e71459 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. K. Iqbal, S.G. Jin, G.P. Pfeifer, P.E. Szabo, Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc. Natl. Acad. Sci. USA 108, 3642–3647 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  52. S. Yamaguchi, L. Shen, Y. Liu, D. Sendler, Y. Zhang, Role of Tet1 in erasure of genomic imprinting. Nature 504, 460–464 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  53. H.W. Bakos, R.C. Henshaw, M. Mitchell, M. Lane, Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil. Steril. 95, 1700–1704 (2011)

    Article  PubMed  Google Scholar 

  54. O. Tunc, H.W. Bakos, K. Tremellen, Impact of body mass index on seminal oxidative stress. Andrologia 43, 121–128 (2011)

    Article  CAS  PubMed  Google Scholar 

  55. N.O. Palmer, H.W. Bakos, T. Fullston, M. Lane, Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2, 253–263 (2012)

    Article  PubMed Central  PubMed  Google Scholar 

  56. D.C. Benyshek, C.S. Johnston, J.F. Martin, Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 49, 1117–1119 (2006)

    Article  CAS  PubMed  Google Scholar 

  57. G.A. Dunn, T.L. Bale, Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152, 2228–2236 (2011)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. K.E. Rhee, S. Phelan, J. McCaffery, Early determinants of obesity: genetic, epigenetic, and in utero influences. Int. J. Pediatr. 2012, 463850 (2012)

    Article  PubMed Central  PubMed  Google Scholar 

  59. D.C. Dolinoy, R. Das, J.R. Weidman, R.L. Jirtle, Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatr. Res. 61, 30R–37R (2007)

    Article  PubMed  Google Scholar 

  60. C. Li, L.S. Balluz, E.S. Ford, C.A. Okoro, G. Zhao, C. Pierannunzi, A comparison of prevalence estimates for selected health indicators and chronic diseases or conditions from the Behavioral Risk Factor Surveillance System, the National Health Interview Survey, and the National Health and Nutrition Examination Survey, 2007–2008. Prev. Med. 54, 381–387 (2012)

    Article  PubMed  Google Scholar 

  61. G. Kaati, L.O. Bygren, S. Edvinsson, Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Eur. J. Hum. Genet. 10, 682–688 (2002)

    Article  CAS  PubMed  Google Scholar 

  62. L.O. Bygren, G. Kaati, S. Edvinsson, Longevity determined by paternal ancestors’ nutrition during their slow growth period. Acta. Biotheor. 49, 53–59 (2001)

    Article  CAS  PubMed  Google Scholar 

  63. I. Ohlund, O. Hernell, A. Hornell, H. Stenlund, T. Lind, BMI at 4 years of age is associated with previous and current protein intake and with paternal BMI. Eur. J. Clin. Nutr. 64, 138–145 (2010)

    Article  CAS  PubMed  Google Scholar 

  64. P. Magnus, H.K. Gjessing, A. Skrondal, R. Skjaerven, Paternal contribution to birth weight. J. Epidemiol. Community Health 55, 873–877 (2001)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. B. Knight, B.M. Shields, A. Hill, R.J. Powell, D. Wright, A.T. Hattersley, The impact of maternal glycemia and obesity on early postnatal growth in a nondiabetic Caucasian population. Diabetes Care 30, 777–783 (2007)

    Article  PubMed  Google Scholar 

  66. R. Cooper, E. Hypponen, D. Berry, C. Power, Associations between parental and offspring adiposity up to midlife: the contribution of adult lifestyle factors in the 1958 British birth cohort study. Am. J. Clin. Nutr. 92, 946–953 (2010)

    Article  CAS  PubMed  Google Scholar 

  67. L. Li, C. Law, R. Lo Conte, C. Power, Intergenerational influences on childhood body mass index: the effect of parental body mass index trajectories. Am. J. Clin. Nutr. 89, 551–557 (2009)

    Article  CAS  PubMed  Google Scholar 

  68. B. Linares Segovia, M. Gutierrez Tinoco, A. Izquierdo Arrizon, J.M. Guizar Mendoza, N. Amador Licona, Long-term consequences for offspring of paternal diabetes and metabolic syndrome. Exp. Diabetes Res. (2012). doi:10.1155/2012/684562

    PubMed Central  PubMed  Google Scholar 

  69. E.M. Perez-Pastor, B.S. Metcalf, J. Hosking, A.N. Jeffery, L.D. Voss, T.J. Wilkin, Assortative weight gain in mother-daughter and father–son pairs: an emerging source of childhood obesity. Longitudinal study of trios (Early Bird 43). Int. J. Obes. (Lond) 33, 727–735 (2009)

    Article  CAS  Google Scholar 

  70. S. Kumar, M. Raju, N. Gowda, Influence of parental obesity on school children. Indian J. Pediatr. 77, 255–258 (2010)

    Article  PubMed  Google Scholar 

  71. S. Leary, G. Davey Smith, A. Ness, No evidence of large differences in mother-daughter and father–son body mass index concordance in a large UK birth cohort. Int. J. Obes. (Lond) 34, 1191–1192 (2010)

    Article  CAS  Google Scholar 

  72. S. Danielzik, K. Langnase, M. Mast, C. Spethmann, M.J. Muller, Impact of parental BMI on the manifestation of overweight 5–7 year old children. Eur. J. Nutr. 41, 132–138 (2002)

    Article  PubMed  Google Scholar 

  73. K.L. Whitaker, M.J. Jarvis, R.J. Beeken, D. Boniface, J. Wardle, Comparing maternal and paternal intergenerational transmission of obesity risk in a large population-based sample. Am. J. Clin. Nutr. 91, 1560–1567 (2010)

    Article  CAS  PubMed  Google Scholar 

  74. R. Figueroa-Colon, R.B. Arani, M.I. Goran, R.L. Weinsier, Paternal body fat is a longitudinal predictor of changes in body fat in premenarcheal girls. Am. J. Clin. Nutr. 71, 829–834 (2000)

    CAS  PubMed  Google Scholar 

  75. V. Svensson, J.A. Jacobsson, R. Fredriksson, P. Danielsson, T. Sobko, H.B. Schioth, C. Marcus, Associations between severity of obesity in childhood and adolescence, obesity onset and parental BMI: a longitudinal cohort study. Int. J. Obes. (Lond) 35, 46–52 (2011)

    Article  CAS  Google Scholar 

  76. A.M. Linabery, R.W. Nahhas, W. Johnson, A.C. Choh, B. Towne, A.O. Odegaard, S.A. Czerwinski, E.W. Demerath, Stronger influence of maternal than paternal obesity on infant and early childhood body mass index: the Fels longitudinal study. Pediatr. Obes. 8, 159–169 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  77. Y.P. Chen, X.M. Xiao, J. Li, C. Reichetzeder, Z.N. Wang, B. Hocher, Paternal body mass index (BMI) is associated with offspring intrauterine growth in a gender dependent manner. PLoS One 7, e36329 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. C. Le Stunff, D. Fallin, P. Bougneres, Paternal transmission of the very common class I INS VNTR alleles predisposes to childhood obesity. Nat. Genet. 29, 96–99 (2001)

    Article  PubMed  Google Scholar 

  79. S.T. Bennett, A.J. Wilson, L. Esposito, N. Bouzekri, D.E. Undlien, F. Cucca, L. Nistico, R. Buzzetti, E. Bosi, F. Pociot, J. Nerup, A. Cambon-Thomsen, A. Pugliese, J.P. Shield, P.A. McKinney, S.C. Bain, C. Polychronakos, J.A. Todd, Insulin VNTR allele-specific effect in type 1 diabetes depends on identity of untransmitted paternal allele The IMDIAB Group. Nat. Genet. 17, 350–352 (1997)

    Article  CAS  PubMed  Google Scholar 

  80. S.J. Huxtable, P.J. Saker, L. Haddad, M. Walker, T.M. Frayling, J.C. Levy, G.A. Hitman, S. O’Rahilly, A.T. Hattersley, M.I. McCarthy, Analysis of parent-offspring trios provides evidence for linkage and association between the insulin gene and type 2 diabetes mediated exclusively through paternally transmitted class III variable number tandem repeat alleles. Diabetes 49, 126–130 (2000)

    Article  CAS  PubMed  Google Scholar 

  81. R.S. Lindsay, D. Dabelea, J. Roumain, R.L. Hanson, P.H. Bennett, W.C. Knowler, Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes 49, 445–449 (2000)

    Article  CAS  PubMed  Google Scholar 

  82. A. Penesova, J.C. Bunt, C. Bogardus, J. Krakoff, Effect of paternal diabetes on pre-diabetic phenotypes in adult offspring. Diabetes Care 33, 1823–1828 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. A.J. Stunkard, J.R. Harris, N.L. Pedersen, G.E. McClearn, The body-mass index of twins who have been reared apart. New Engl. J. Med. 322, 1483–1487 (1990)

    Article  CAS  PubMed  Google Scholar 

  84. T.I. Sorensen, C. Holst, A.J. Stunkard, Childhood body mass index–genetic and familial environmental influences assessed in a longitudinal adoption study. Int. J. Obes. Relat. Metab. Disord. 16, 705–714 (1992)

    CAS  PubMed  Google Scholar 

  85. A.J. Stunkard, T.I. Sorensen, C. Hanis, T.W. Teasdale, R. Chakraborty, W.J. Schull, F. Schulsinger, An adoption study of human obesity. New Engl. J. Med. 314, 193–198 (1986)

    Article  CAS  PubMed  Google Scholar 

  86. V. Lecomte, N.A. Youngson, C.A. Maloney, M.J. Morris, Parental programming: How can we improve study design to discern the molecular mechanisms? BioEssays 35, 787–793 (2013)

    Article  PubMed  Google Scholar 

  87. D.K. Belyaev, A.O. Ruvinsky, L.N. Trut, Inherited activation-inactivation of the star gene in foxes: its bearing on the problem of domestication. J. Hered. 72, 267–274 (1981)

    CAS  PubMed  Google Scholar 

  88. H.D. Morgan, H.G. Sutherland, D.I. Martin, E. Whitelaw, Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23, 314–318 (1999)

    Article  CAS  PubMed  Google Scholar 

  89. V.K. Rakyan, S. Chong, M.E. Champ, P.C. Cuthbert, H.D. Morgan, K.V. Luu, E. Whitelaw, Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc. Natl. Acad. Sci. USA 100, 2538–2543 (2003)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  90. R. Lambrot, C. Xu, S. Saint-Phar, G. Chountalos, T. Cohen, M. Paquet, M. Suderman, M. Hallett, S. Kimmins, Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat. Commun. 4, 2889 (2013)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  91. L.M. Anderson, L. Riffle, R. Wilson, G.S. Travlos, M.S. Lubomirski, W.G. Alvord, Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 22, 327–331 (2006)

    Article  CAS  PubMed  Google Scholar 

  92. G.A. Dunn, T.L. Bale, Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150, 4999–5009 (2009)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  93. J.C. Jimenez-Chillaron, E. Isganaitis, M. Charalambous, S. Gesta, T. Pentinat-Pelegrin, R.R. Faucette, J.P. Otis, A. Chow, R. Diaz, A. Ferguson-Smith, M.E. Patti, Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 58, 460–468 (2009)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  94. P.J. Enriori, A.E. Evans, P. Sinnayah, E.E. Jobst, L. Tonelli-Lemos, S.K. Billes, M.M. Glavas, B.E. Grayson, M. Perello, E.A. Nillni, K.L. Grove, M.A. Cowley, Diet-induced obesity causes severe but reversible leptin resistance in arcuate melanocortin neurons. Cell Metab. 5, 181–194 (2007)

    Article  CAS  PubMed  Google Scholar 

  95. R.A. Koza, L. Nikonova, J. Hogan, J.S. Rim, T. Mendoza, C. Faulk, J. Skaf, L.P. Kozak, Changes in gene expression foreshadow diet-induced obesity in genetically identical mice. PLoS Genet. 2, e81 (2006)

    Article  PubMed Central  PubMed  Google Scholar 

  96. S.N. Yazbek, S.H. Spiezio, J.H. Nadeau, D.A. Buchner, Ancestral paternal genotype controls body weight and food intake for multiple generations. Hum. Mol. Genet. 19, 4134–4144 (2010)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  97. S.F. Ng, R.C. Lin, D.R. Laybutt, R. Barres, J.A. Owens, M.J. Morris, Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467, 963–966 (2010)

    Article  CAS  PubMed  Google Scholar 

  98. T. Pentinat, M. Ramon-Krauel, J. Cebria, R. Diaz, J.C. Jimenez-Chillaron, Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology 151, 5617–5623 (2010)

    Article  CAS  PubMed  Google Scholar 

  99. R. Mashoodh, B. Franks, J.P. Curley, F.A. Champagne, Paternal social enrichment effects on maternal behavior and offspring growth. Proc. Natl. Acad. Sci. USA 109(Suppl 2), 17232–17238 (2012)

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biomedical Sciences, HCOM, Ohio University, Athens, OH, 45701, USA

    Yuriy Slyvka, Yizhu Zhang & Felicia V. Nowak

  2. Program in Molecular and Cell Biology, Ohio University, Athens, OH, 45701, USA

    Felicia V. Nowak

  3. The Diabetes Institute, Ohio University, Athens, OH, 45701, USA

    Yuriy Slyvka & Felicia V. Nowak

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  1. Yuriy Slyvka
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  2. Yizhu Zhang
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  3. Felicia V. Nowak
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Correspondence to Felicia V. Nowak.

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Slyvka, Y., Zhang, Y. & Nowak, F.V. Epigenetic effects of paternal diet on offspring: emphasis on obesity. Endocrine 48, 36–46 (2015). https://doi.org/10.1007/s12020-014-0328-5

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