Who's your daddy?: Paternal inheritance of metabolic disease risk

Current Opinion in Endocrinology, Diabetes and Obesity

Volumn 24, Issue 1, 2017, Pages 47-55

  Isganaitis, Elvira ^a   Suehiro, Harumi ^a   Cardona, Connie ^a  

^a JOSLIN DIABETES CENTER   (United States)

Author keywords

Epigenetics; Germ cells; Intergenerational; Obesity; Paternal

Indexed keywords

DNA; HISTONE; PROBIOTIC AGENT; SMALL UNTRANSLATED RNA; TRANSFER RNA; UNTRANSLATED RNA; VITAMIN;

DIABETES MELLITUS; DISEASE PREDISPOSITION; DNA METHYLATION; EPIGENETICS; EXERCISE; GENE EXPRESSION; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOME IMPRINTING; GERM CELL; HUMAN; MALNUTRITION; METABOLIC DISORDER; METABOLITE; MICROBIOME; OBESITY; OVERNUTRITION; PATERNAL EXPOSURE; PATERNAL INHERITANCE; PLACENTA; PROGENY; REVIEW; SEMINAL PLASMA; SPERM QUALITY; TRANSPORT VESICLE; WEIGHT REDUCTION; COMPLICATION; FATHER; FEMALE; GENETIC EPIGENESIS; GENETICS; HEALTH STATUS; MALE; METABOLISM; NUCLEAR REPROGRAMMING; NUTRITIONAL STATUS; PHYSIOLOGY; PREGNANCY; RISK; SPERMATOZOON;

CELLULAR REPROGRAMMING; DISEASE SUSCEPTIBILITY; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; FATHERS; FEMALE; HEALTH STATUS; HISTONES; HUMANS; MALE; METABOLIC DISEASES; NUTRITIONAL STATUS; OBESITY; PATERNAL INHERITANCE; PREGNANCY; RISK; SPERMATOZOA;

EID: 85001104652     PISSN: 1752296X     EISSN: 17522978     Source Type: Journal    
DOI: 10.1097/MED.0000000000000307     Document Type: Review

References (92)

1. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008; 359:61-73.
2. Gluckman PD, Hanson MA, Bateson P, et al. Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet 2009; 373:1654-1657.
3. Hanson M, Gluckman P. Developmental origins of noncommunicable disease: population and public health implications. Am J Clin Nutr 2011; 94 (6 Suppl):1754S-1758S.
4. World Health Organization CoECO. Report of the Commission on Ending Childhood Obesity, 2016. Available at: http://www.who.int/end-childhoodobesity/en/. [Accessed 11 November 2016]
5. Taveras EM, Perkins M, Woo Baidal JA, et al. The impact of the first 1000 days on childhood obesity. Durham, NC: Robert Wood Johnson Foundation, Healthy Eating Research; 2016.
6. Lumey LH. Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944-1945. Paediatr Perinat Epidemiol 1992; 6:240-253.
7. Painter RC, Osmond C, Gluckman P, et al. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008; 115:1243-1249.
8. Bygren LO, Kaati G, Edvinsson S. Longevity determined by paternal ancestors' nutrition during their slow growth period. Acta Biotheor 2001; 49:53-59.
9. Bygren LO, Tinghog P, Carstensen J, et al. Change in paternal grandmothers' early food supply influenced cardiovascular mortality of the female grandchildren. BMC Genet 2014; 15:12.
10. Kaati G, Bygren LO, Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet 2002; 10:682-688.
11. Isganaitis E, Woo M, Ma H, et al. Developmental programming by maternal insulin resistance: hyperinsulinemia, glucose intolerance, and dysregulated lipid metabolism in male offspring of insulin-resistant mice. Diabetes 2014; 63:688-700.
12. Fasting MH, Oken E, Mantzoros CS, et al. Maternal levels of corticotropin releasing hormone during pregnancy in relation to adiponectin and leptin in early childhood. J Clin Endocrinol Metab 2009; 94:1409-1415.
13. Oken E, Taveras EM, Kleinman KP, et al. Gestational weight gain and child adiposity at age 3 years. Am J Obstet Gynecol 2007; 196:322.e1-322.e8.
14. Pettitt DJ, Lawrence JM, Beyer J, et al. Association between maternal diabetes in utero and age at offspring's diagnosis of type 2 diabetes. Diabetes Care 2008; 31:2126-2130.
15. Pigeyre M, Yazdi FT, Kaur Y, Meyre D. Recent progress in genetics, epigenetics and metagenomics unveils the pathophysiology of human obesity. Clin Sci (Lond) 2016; 130:943-986.
16. Trerotola M, Relli V, Simeone P, Alberti S. Epigenetic inheritance and the missing heritability. Hum Genomics 2015; 9:17.
17. Dick KJ, Nelson CP, Tsaprouni L, et al. DNA methylation and body-mass index: a genome-wide analysis. Lancet 2014; 383:1990-1998.
18. Schloss PD, Iverson KD, Petrosino JF, Schloss SJ. The dynamics of a family's gut microbiota reveal variations on a theme. Microbiome 2014; 2:25.
19. Soderborg TK, Borengasser SJ, Barbour LA, Friedman JE. Microbial transmission from mothers with obesity or diabetes to infants: an innovative opportunity to interrupt a vicious cycle. Diabetologia 2016; 59:895-906. An excellent review of the role of the microbiome in mother-child transmission of obesity risk.
20. Fisher SJ. Why is placentation abnormal in preeclampsia? Am J Obstet Gynecol 2015; 213 (4 Suppl):S115-S122.
21. Katsi V, Felekos I, Siristatidis C, et al. Preeclampsia: what does the father have to do with it? Curr Hypertens Rep 2015; 17:60.
22. McPherson NO, Bell VG, Zander-Fox DL, et al. When two obese parents are worse than one! Impacts on embryo and fetal development. Am J Physiol Endocrinol Metab 2015; 309:E568-E581.
23. Binder NK, Beard SA, Kaitu'u-Lino TJ, et al. Paternal obesity in a rodent model affects placental gene expression in a sex-specific manner. Reproduction 2015; 149:435-444.
24. L'Abee C, Vrieze I, Kluck T, et al. Parental factors affecting the weights of the placenta and the offspring. J Perinat Med 2011; 39:27-34.
25. Wills AK, Chinchwadkar MC, Joglekar CV, et al. Maternal and paternal height and BMI and patterns of fetal growth: the Pune Maternal Nutrition Study. Early Hum Dev 2010; 86:535-540.
26. Strom-Roum EM, Haavaldsen C, Tanbo TG, Eskild A. Paternal age, placental weight and placental to birthweight ratio: a population-based study of 590,835 pregnancies. Hum Reprod 2013; 28:3126-3133.
27. Waddington CH. The epigenotype. 1942. Int J Epidemiol 2012; 41:10-13.
28. Wu C, Morris JR. Genes, genetics, and epigenetics: a correspondence. Science 2001; 293:1103-1105.
29. Zhang D, Cheng L, Badner JA, et al. Genetic control of individual differences in gene-specific methylation in human brain. Am J Hum Genet 2010; 86:411-419.
30. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998; 19:219-220.
31. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293:1089-1093.
32. Ziller MJ, Gu H, Muller F, et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 2013; 500:477-481.
33. Stein R, Razin A, Cedar H. In vitro methylation of the hamster adenine phosphoribosyl transferase gene inhibits its expression in mouse L cells. Proc Natl Acad Sci U S A 1982; 79:3418-3422.
34. Guo F, Yan L, Guo H, et al. The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 2015; 161:1437-1452.
35. Radford EJ, Ito M, Shi H, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 2014; 345:1255903.
36. Wei Y, Yang CR, Wei YP, et al. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc Natl Acad Sci U S A 2014; 111:1873-1878.
37. Martinez D, Pentinat T, Ribo S, et al. In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered Lxra DNA methylation. Cell Metab 2014; 19:941-951.
38. Carone BR, Fauquier L, Habib N, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010; 143:1084-1096.
39. Shea JM, Serra RW, Carone BR, et al. Genetic and epigenetic variation, but not diet, shape the sperm methylome. Dev Cell 2015; 35:750-758.
40. Dominguez-Salas P, Moore SE, Baker MS, et al. Maternal nutrition at conception modulates DNA methylation of human metastable epialleles. Nat Commun 2014; 5:3746.
41. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999; 23:314-318.
42. Kuhnen P, Handke D, Waterland RA, et al. Interindividual variation in DNA methylation at a putative POMC metastable epiallele is associated with obesity. Cell Metab 2016; 24:502-509.
43. Lim AL, Ng S, Leow SC, et al. Epigenetic state and expression of imprinted genes in umbilical cord correlates with growth parameters in human pregnancy. J Med Genet 2012; 49:689-697.
44. Waterland RA, Lin JR, Smith CA, Jirtle RL. Postweaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum Mol Genet 2006; 15:705-716.
45. Soubry A, Guo L, Huang Z, et al. Obesity-related DNA methylation at imprinted genes in human sperm: results from the TIEGER study. Clin Epigenetics 2016; 8:51.
46. Morita S, Nakabayashi K, Kawai T, et al. Gene expression profiling of white adipose tissue reveals paternal transmission of proneness to obesity. Sci Rep 2016; 6:21693.
47. Morita S, Horii T, Kimura M, et al. Paternal allele influences high fat dietinduced obesity. PLoS One 2014; 9:e85477.
48. Lambrot R, Xu C, Saint-Phar S, et al. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun 2013; 4:2889.
49. Radford EJ, Isganaitis E, Jimenez-Chillaron J, et al. An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS Genet 2012; 8:e1002605.
50. Terashima M, Barbour S, Ren J, et al. Effect of high fat diet on paternal sperm histone distribution and male offspring liver gene expression. Epigenetics 2015; 10:861-871.
51. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403:41-45.
52. Oliva R. Protamines and male infertility. Hum Reprod Update 2006; 12:417-435.
53. Hammoud SS, Nix DA, Zhang H, et al. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009; 460:473-478.
54. Siklenka K, Erkek S, Godmann M, et al. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 2015; 350:aab2006.
55. Grishok A, Pasquinelli AE, Conte D, et al. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 2001; 106:23-34.
56. Luo LF, Hou CC, Yang WX. Small noncoding RNAs and their associated proteins in spermatogenesis. Gene 2016; 578:141-157.
57. de Castro Barbosa T, Ingerslev LR, Alm PS, et al. High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Mol Metab 2016; 5:184-197.
58. Fullston T, McPherson NO, Owens JA, et al. Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an 'obesogenic' diet. Physiol Rep 2015; 3:. doi: 10.14814/phy2.12336. PubMed PMID: 25804263; PMCID: PMC4393169.
59. Fullston T, Ohlsson Teague EM, Palmer NO, et al. 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 2013; 27:4226-4243.
60. McPherson NO, Owens JA, Fullston T, Lane M. Preconception diet or exercise intervention in obese fathers normalizes sperm microRNA profile and metabolic syndrome in female offspring. Am J Physiol Endocrinol Metab 2015; 308:E805-E821.
61. Sharma U, Conine CC, Shea JM, et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 2016; 351:391-396.
62. Chen Q, Yan M, Cao Z, et al. SpermtsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 2016; 351:397-400.
63. Bieniek JM, Kashanian JA, Deibert CM, et al. Influence of increasing body mass index on semen and reproductive hormonal parameters in a multiinstitutional cohort of subfertile men. Fertil Steril 2016; 106:1070-1075.
64. McPherson NO, Fullston T, Kang WX, et al. Paternal under-nutrition programs metabolic syndrome in offspring which can be reversed by antioxidant/vitamin food fortification in fathers. Sci Rep 2016; 6:27010.
65. Binder NK, Sheedy JR, Hannan NJ, Gardner DK. Male obesity is associated with changed spermatozoa Cox4i1 mRNA level and altered seminal vesicle fluid composition in a mouse model. Mol Hum Reprod 2015; 21:424-434.
66. Javurek AB, Spollen WG, Johnson SA, et al. Consumption of a high-fat diet alters the seminal fluid and gut microbiomes in male mice. Reprod Fertil Dev 2016. doi: 10.1071/RD16119. PubMed PMID: 27569192.
67. Javurek AB, Spollen WG, Ali AM, et al. Discovery of a novel seminal fluid microbiome and influence of estrogen receptor alpha genetic status. Sci Rep 2016; 6:23027.
68. Pryke SR, Griffith SC. Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch. Science 2009; 323:1605-1607.
69. Mashoodh R, Franks B, Curley JP, Champagne FA. Paternal social enrichment effects on maternal behavior and offspring growth. Proc Natl Acad Sci U S A 2012; 109 (Suppl 2):17232-17238.
70. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, et al. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009; 58:460-468.
71. Seisenberger S, Andrews S, Krueger F, et al. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 2012; 48:849-862.
72. Watkins AJ, Sinclair KD. Paternal low protein diet affects adult offspring cardiovascular and metabolic function inmice. Am J Physiol Heart Circ Physiol 2014; 306:H1444-H1452.
73. Anderson LM, Riffle L, Wilson R, et al. Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 2006; 22:327-331.
74. Han TS, Hart CL, Haig C, et al. Contributions of maternal and paternal adiposity and smoking to adult offspring adiposity and cardiovascular risk: the Midspan Family Study. BMJ Open 2015; 5:e007682.
75. Cooper R, Hypponen E, Berry D, Power C. 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 2010; 92:946-953.
76. Li L, Law C, Lo Conte R, Power C. Intergenerational influences on childhood body mass index: the effect of parental body mass index trajectories. Am J Clin Nutr 2009; 89:551-557.
77. Sorensen T, Ajslev TA, Angquist L, et al. Comparison of associations of maternal peri-pregnancy and paternal anthropometrics with child anthropometrics from birth through age 7 y assessed in the Danish National Birth Cohort. Am J Clin Nutr 2016; 104:389-396.
78. Corsi DJ, Subramanian SV, Ackerson LK, Davey Smith G. Is there a greater maternal than paternal influence on offspring adiposity in India? Arch Dis Child 2015; 100:973-979.
79. McCarthy FP, Khashan AS, Murray D, et al., SCOPE Ireland Cohort study and the Cork BASELINE Birth Cohort Study. Parental physical and lifestyle factors and their association with newborn body composition. BJOG 2016; 123:1824-1829.
80. Ornellas F, Souza-Mello V, Mandarim-de-Lacerda CA, Aguila MB. Programming of obesity and comorbidities in the progeny: lessons from a model of diet-induced obese parents. PLoS One 2015; 10:e0124737.
81. Masuyama H, Mitsui T, Eguchi T, et al. The effects of paternal high-fat diet exposure on offspring metabolism with epigenetic changes in the mouse adiponectin and leptin gene promoters. Am J Physiol Endocrinol Metab 2016; 311:E236-E245.
82. Ng SF, Lin RC, Laybutt DR, et al. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010; 467: 963-966.
83. Binder NK, Hannan NJ, Gardner DK. Paternal diet-induced obesity retards early mouse embryo development, mitochondrial activity and pregnancy health. PLoS One 2012; 7:e52304.
84. Lindsay RS, Dabelea D, Roumain J, et al. Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes 2000; 49:445-449.
85. Wang C, Yatsuya H, Tamakoshi K, et al. Association between parental history of diabetes and the incidence of type 2 diabetes mellitus differs according to the sex of the parent and offspring's body weight: a finding from a Japanese worksite-based cohort study. Prev Med 2015; 81:49-53.
86. Yehuda R, Daskalakis NP, Lehrner A, et al. Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in Holocaust survivor offspring. Am J Psychiatry 2014; 171: 872-880.
87. Wu L, Lu Y, Jiao Y, et al. Paternal psychological stress reprograms hepatic gluconeogenesis in offspring. Cell Metab 2016; 23:735-743.
88. Donkin I, Versteyhe S, Ingerslev LR, et al. Obesity and bariatric surgery drive epigenetic variation of spermatozoa in humans. Cell Metab 2016; 23:369-378.
89. Murashov AK, Pak ES, Koury M, et al. Paternal long-term exercise programs offspring for low energy expenditure and increased risk for obesity in mice. FASEB J 2016; 30:775-784.
90. Waterland RA, Travisano M, Tahiliani KG, et al. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 2008; 32:1373-1379.
91. Sabet JA, Park LK, Iyer LK, et al. Paternal B vitamin intake is a determinant of growth, hepatic lipid metabolism and intestinal tumor volume in female Apc1638N mouse offspring. PLoS One 2016; 11:e0151579.
92. Callaghan BL, Cowan CS, Richardson R. Treating generational stress: effect of paternal stress on development of memory and extinction in offspring is reversed by probiotic treatment. Psychol Sci 2016; 27:1171-1180.