Obesity-related DNA methylation at imprinted genes in human sperm: Results from the TIEGER study

Clinical Epigenetics

Volumn 8, Issue 1, 2016, Pages

  Soubry, Adelheid ^a   Guo, Lisa ^b   Huang, Zhiqing ^b   Hoyo, Cathrine ^c   Romanus, Stephanie ^a   Price, Thomas ^b   Murphy, Susan K ^b,d  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d DUKE CANCER INSTITUTE   (United States)

Author keywords

Epigenetics; Imprinted gene; Methylation; Obesity; Sperm; TIEGER study

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; GENE; GENOME IMPRINTING; HUMAN; LIFESTYLE MODIFICATION; LIMIT OF QUANTITATION; MALE; MALE FERTILITY; MEG3 GENE; MEG3IG GENE; OBESITY; PEG10 GENE; PRIORITY JOURNAL; PYROSEQUENCING; SGCE GENE; SNRPN GENE; SPERM; UNITED STATES; GENETICS; METABOLISM; SPERMATOZOON; STATISTICAL MODEL; YOUNG ADULT;

H19 LONG NON-CODING RNA; LONG UNTRANSLATED RNA; MEG3 NON-CODING RNA, HUMAN;

ADULT; DNA METHYLATION; GENOMIC IMPRINTING; HUMANS; LINEAR MODELS; MALE; OBESITY; OVERWEIGHT; RNA, LONG NONCODING; SPERMATOZOA; YOUNG ADULT;

EID: 84966349300     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-016-0217-2     Document Type: Article

References (53)

1. Wadhwa PD, Buss C, Entringer S, Swanson JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009;27(5):358–68.
2. Mitchell NS, Catenacci VA, Wyatt HR, Hill JO. Obesity: overview of an epidemic. Psychiatr Clin North Am. 2011;34(4):717–32.
3. Soubry A, Hoyo C, Jirtle RL, Murphy SK. A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. Bioessays. 2014;36(4):359–71.
4. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005;135(6):1382–6.
5. Furrow RE, Feldman MW. Genetic variation and the evolution of epigenetic regulation. Evolution. 2014;68(3):673–83.
6. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127(19):4195–202.
7. Jenkins TG, Carrell DT. The sperm epigenome and potential implications for the developing embryo. Reproduction. 2012;143(6):727–34.
8. Wu Q, Suzuki M. Parental obesity and overweight affect the body-fat accumulation in the offspring: the possible effect of a high-fat diet through epigenetic inheritance. Obes Rev. 2006;7(2):201–8.
9. McPherson NO, Fullston T, Bakos HW, Setchell BP, Lane M. Obese father’s metabolic state, adiposity, and reproductive capacity indicate son’s reproductive health. Fertil Steril. 2014;101(3):865–73.
10. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, Gu H, Zamore PD, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell. 2010;143(7):1084–96.
11. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod. 2012;27(5):1391–400.
12. Soubry A. Epigenetic inheritance and evolution: a paternal perspective on dietary influences. Prog Biophys Mol Biol. 2015;118(1-2):79–85.
13. Surén P, Gunnes N, Roth C, Bresnahan M, Hornig M, Hirtz D, Lie KK, Lipkin WI, Magnus P, Reichborn-Kjennerud T, et al. Parental obesity and risk of autism spectrum disorder. Pediatrics. 2014;133(5):e1128–38.
14. Figueroa-Colon R, Arani RB, Goran MI, Weinsier RL. Paternal body fat is a longitudinal predictor of changes in body fat in premenarcheal girls. Am J Clin Nutr. 2000;71(3):829–34.
15. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J. Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet. 2006;14(2):159–66.
16. Gluckman PD, Hanson MA, Beedle AS. Non-genomic transgenerational inheritance of disease risk. Bioessays. 2007;29(2):145–54.
17. Carrell DT. Epigenetics of the male gamete. Fertil Steril. 2012;97(2):267–74.
18. Russo VEA, Martienssen RA, Riggs AD. Epigenetic mechanisms of gene regulation. Cold Spring Harbor: Cold Spring Harbor Laboratry Press; 1996.
19. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6–21.
20. Wei Y, Yang CR, Wei YP, Zhao ZA, Hou Y, Schatten H, Sun QY. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc Natl Acad Sci U S A. 2014;111(5):1873–8.
21. Binder NK, Beard SA, Kaitu’u-Lino TJ, Tong S, Hannan NJ, Gardner DK. Paternal obesity in a rodent model affects placental gene expression in a sex-specific manner. Reproduction. 2015;149(5):435–44.
22. Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, Suderman M, Hallett M, Kimmins S. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun. 2013;4:2889.
23. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010;467(7318):963–6.
24. Soubry A, Schildkraut JM, Murtha A, Wang F, Huang Z, Bernal A, Kurtzberg J, Jirtle RL, Murphy SK, Hoyo C. Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort. BMC Med. 2013;11:29.
25. Soubry A, Murphy SK, Wang F, Huang Z, Vidal AC, Fuemmeler BF, Kurtzberg J, Murtha A, Jirtle RL, Schildkraut JM, et al. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes (Lond). 2013;37(7):907–13.
26. Skaar DA, Li Y, Bernal AJ, Hoyo C, Murphy SK, Jirtle RL. The human imprintome: regulatory mechanisms, methods of ascertainment, and roles in disease susceptibility. Ilar J. 2012;53(3–4):341–58.
27. Kalish JM, Jiang C, Bartolomei MS. Epigenetics and imprinting in human disease. Int J Dev Biol. 2014;58(2–4):291–8.
28. WHO. World Health Organization laboratory manual for the examination and processing of human semen. 5th ed. Geneva: WHO Press; 2010. p. 287.
29. Nye MD, Hoyo C, Huang Z, Vidal AC, Wang F, Overcash F, Smith JS, Vasquez B, Hernandez B, Swai B, et al. Associations between methylation of paternally expressed gene 3 (PEG3), cervical intraepithelial neoplasia and invasive cervical cancer. PLoS One. 2013;8(2):e56325.
30. Murphy SK, Huang Z, Hoyo C. Differentially methylated regions of imprinted genes in prenatal, perinatal and postnatal human tissues. PLoS One. 2012;7(7):e40924.
31. Nowak K, Stein G, Powell E, He LM, Naik S, Morris J, Marlow S, Davis TL. Establishment of paternal allele-specific DNA methylation at the imprinted mouse Gtl2 locus. Epigenetics. 2011;6(8):1012–20.
32. Kagami M, O’Sullivan MJ, Green AJ, Watabe Y, Arisaka O, Masawa N, Matsuoka K, Fukami M, Matsubara K, Kato F, et al. The IG-DMR and the MEG3-DMR at human chromosome 14q32.2: hierarchical interaction and distinct functional properties as imprinting control centers. PLoS Genet. 2010;6(6):e1000992.
33. Donkin I, Versteyhe S, Ingerslev LR, Qian K, Mechta M, Nordkap L, Mortensen B, Appel EV, Jorgensen N, Kristiansen VB, et al. Obesity and bariatric surgery drive epigenetic variation of spermatozoa in humans. Cell Metab. 2016;23(2):369–78.
34. Feinberg JI, Bakulski KM, Jaffe AE, Tryggvadottir R, Brown SC, Goldman LR, Croen LA, Hertz-Picciotto I, Newschaffer CJ, Daniele Fallin M, et al. Paternal sperm DNA methylation associated with early signs of autism risk in an autism-enriched cohort. Int J Epidemiol. 2015;44(4):1199–210.
35. Aston KI, Uren PJ, Jenkins TG, Horsager A, Cairns BR, Smith AD, Carrell DT. Aberrant sperm DNA methylation predicts male fertility status and embryo quality. Fertil Steril. 2015;104(6):1388–97. e1385.
36. Mitchell M, Bakos HW, Lane M. Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil Steril. 2011;95(4):1349–53.
37. Binder NK, Hannan NJ, Gardner DK. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One. 2012;7(12):e52304.
38. Du Plessis SS, Cabler S, McAlister DA, Sabanegh E, Agarwal A. The effect of obesity on sperm disorders and male infertility. Nat Rev Urol. 2010;7(3):153–61.
39. Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M. 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. 2012;302(7):E768–780.
40. Ge ZJ, Liang QX, Hou Y, Han ZM, Schatten H, Sun QY, Zhang CL. Maternal obesity and diabetes may cause DNA methylation alteration in the spermatozoa of offspring in mice. Reprod Biol Endocrinol. 2014;12:29.
41. Shea JM, Serra RW, Carone BR, Shulha HP, Kucukural A, Ziller MJ, Vallaster MP, Gu H, Tapper AR, Gardner PD, et al. Genetic and epigenetic variation, but not diet, shape the sperm methylome. Dev Cell. 2015;35(6):750–8.
42. Pathak S, D’Souza R, Ankolkar M, Gaonkar R, Balasinor NH. Potential role of estrogen in regulation of the insulin-like growth factor2-H19 locus in the rat testis. Mol Cell Endocrinol. 2010;314(1):110–7.
43. Rahman MB, Kamal MM, Rijsselaere T, Vandaele L, Shamsuddin M, Van Soom A. Altered chromatin condensation of heat-stressed spermatozoa perturbs the dynamics of DNA methylation reprogramming in the paternal genome after in vitro fertilisation in cattle. Reprod Fertil Dev. 2014;26(8):1107–16.
44. Tavalaee M, Bahreinian M, Barekat F, Abbasi H, Nasr-Esfahani MH. Effect of varicocelectomy on sperm functional characteristics and DNA methylation. Andrologia. 2015;47(8):904–9.
45. Boucher JG, Boudreau A, Ahmed S, Atlas E. In vitro effects of bisphenol A beta-D-glucuronide (BPA-G) on adipogenesis in human and murine preadipocytes. Environ Health Perspect. 2015;123(12):1287–93.
46. Murphy SK, Adigun A, Huang Z, Overcash F, Wang F, Jirtle RL, Schildkraut JM, Murtha AP, Iversen ES, Hoyo C. Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke. Gene. 2012;494(1):36–43.
47. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105(44):17046–9.
48. Khulan B, Cooper WN, Skinner BM, Bauer J, Owens S, Prentice AM, Belteki G, Constancia M, Dunger D, Affara NA. Periconceptional maternal micronutrient supplementation is associated with widespread gender related changes in the epigenome: a study of a unique resource in the Gambia. Hum Mol Genet. 2012;21(9):2086–101.
49. Soubry A, Murphy SK, Huang Z, Murtha A, Schildkraut JM, Jirtle RL, Wang F, Kurtzberg J, Demark-Wahnefried W, Forman MR, et al. The effects of depression and use of antidepressive medicines during pregnancy on the methylation status of the IGF2 imprinted control regions in the offspring. Clin Epigenetics. 2011;3:2.
50. Vidal AC, Murphy SK, Murtha AP, Schildkraut JM, Soubry A, Huang Z, Neelon SE, Fuemmeler B, Iversen E, Wang F, et al. Associations between antibiotic exposure during pregnancy, birth weight and aberrant methylation at imprinted genes among offspring. Int J Obes (Lond). 2013;37(7):907–13.
51. Vidal AC, Semenova V, Darrah T, Vengosh A, Huang Z, King K, Nye MD, Fry R, Skaar D, Maguire R, et al. Maternal cadmium, iron and zinc levels, DNA methylation and birth weight. BMC Pharmacol Toxicol. 2015;16:20.
52. National Center for Chronic Disease Prevention and Health Promotion DoPH. BRFSS prevalence and trends data. In: Center for disease control and prevention. 2015.
53. McPherson NO, Bakos HW, Owens JA, Setchell BP, Lane M. Improving metabolic health in obese male mice via diet and exercise restores embryo development and fetal growth. PLoS One. 2013;8(8):e71459.