Epigenetics and the origins of paternal effects

Hormones and Behavior

Volumn 59, Issue 3, 2011, Pages 306-314

  Curley, James P ^a   Mashoodh, Rahia ^a   Champagne, Frances A ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Epigenetic; Germline; Maternal investment; Paternal effect; Transgerational

Indexed keywords

ENDOCRINE DISRUPTOR; TOXIN;

DRUG EXPOSURE; ENVIRONMENTAL EXPOSURE; EPIGENETICS; EXPERIENCE; FATHER; HUMAN; INHERITANCE; NONHUMAN; NUTRITION; PATERNAL AGE; PATERNAL NUTRITION; PHENOTYPE; PRIORITY JOURNAL; PROGENY; REVIEW;

ANIMALS; EPIGENESIS, GENETIC; EPIGENOMICS; FATHERS; HUMANS; MALE; NUTRITIONAL STATUS; PATERNAL EXPOSURE;

EID: 79952697165     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2010.06.018     Document Type: Review

References (102)

1. Abel E. Paternal contribution to fetal alcohol syndrome. Addict. Biol. 2004, 9:127-133. discussion 135-6.
2. Abel E.L., Tan S.E. Effects of paternal alcohol consumption on pregnancy outcome in rats. Neurotoxicol. Teratol. 1988, 10:187-192.
3. Abel E.L., Bilitzke P. Paternal alcohol exposure: paradoxical effect in mice and rats. Psychopharmacology (Berl) 1990, 100:159-164.
4. Abel E.L., Moore C., Waselewsky D., Zajac C., Russell L.D. Effects of cocaine hydrochloride on reproductive function and sexual behavior of male rats and on the behavior of their offspring. J. Androl. 1989, 10:17-27.
5. Allegrucci C., Thurston A., Lucas E., Young L. Epigenetics and the germline. Reproduction 2005, 129:137-149.
6. Alter M.D., Gilani A.I., Champagne F.A., Curley J.P., Turner J.B., Hen R. Paternal transmission of complex phenotypes in inbred mice. Biol. Psychiatry 2009, 66:1061-1066.
7. Anderson L.M., Riffle L., Wilson R., Travlos G.S., Lubomirski M.S., Alvord W.G. Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 2006, 22:327-331.
8. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
9. Anway M.D., Skinner M.K. Epigenetic programming of the germ line: effects of endocrine disruptors on the development of transgenerational disease. Reprod. Biomed. Online 2008, 16:23-25.
10. Anway M.D., Rekow S.S., Skinner M.K. Comparative anti-androgenic actions of vinclozolin and flutamide on transgenerational adult onset disease and spermatogenesis. Reprod. Toxicol. 2008, 26:100-106.
11. Arnheim N., Calabrese P. Understanding what determines the frequency and pattern of human germline mutations. Nat. Rev. Genet. 2009, 10:478-488.
12. Auroux M. Decrease of learning capacity in offspring with increasing paternal age in the rat. Teratology 1983, 27:141-148.
13. Auroux M.R., Mayaux M.J., Guihard-Moscato M.L., Fromantin M., Barthe J., Schwartz D. Paternal age and mental functions of progeny in man. Hum. Reprod. 1989, 4:794-797.
14. Auroux M., Nawar N.N., Naguib M., Baud M., Lapaquellerie N. Post-pubescent to mature fathers: increase in progeny quality?. Hum. Reprod. 1998, 13:55-59.
15. Auroux M., Volteau M., Ducot B., Wack T., Letierce A., Meyer L., Mayaux M.J. Progeny's mental aptitudes in man: relationship with parental age at conception and with some environmental factors. C R Biol. 2009, 332:603-612.
16. Beaujean N., Taylor J.E., McGarry M., Gardner J.O., Wilmut I., Loi P., Ptak G., Galli C., Lazzari G., Bird A., Young L.E., Meehan R.R. The effect of interspecific oocytes on demethylation of sperm DNA. Proc. Natl Acad. Sci. USA 2004, 101:7636-7640.
17. Bielawski D.M., Zaher F.M., Svinarich D.M., Abel E.L. Paternal alcohol exposure affects sperm cytosine methyltransferase messenger RNA levels. Alcohol. Clin. Exp. Res. 2002, 26:347-351.
18. Bluhm C.K., Gowaty P.A. Reproductive compensation for offspring viability deficits by female mallards, Anas platyrhynchos. Anim. Behav. 2004, 68:985-992.
19. Bolund E., Schielzeth H., Forstmeier W. Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males. Proc. Biol. Sci. 2009, 276:707-715.
20. Boucher B.J., Ewen S.W., Stowers J.M. Betel nut (Areca catechu) consumption and the induction of glucose intolerance in adult CD1 mice and in their F1 and F2 offspring. Diabetologia 1994, 37:49-55.
21. Brunton P.J., Russell J.A. The expectant brain: adapting for motherhood. Nat. Rev. Neurosci. 2008, 9:11-25.
22. Burley N. The differential-allocation hypothesis: an experimental test. Am. Nat. 1988, 132:611-628.
23. Chen T.H., Chiu Y.H., Boucher B.J. Transgenerational effects of betel-quid chewing on the development of the metabolic syndrome in the Keelung Community-based Integrated Screening Program. Am. J. Clin. Nutr. 2006, 83:688-692.
24. Cheng R.Y., Hockman T., Crawford E., Anderson L.M., Shiao Y.H. Epigenetic and gene expression changes related to transgenerational carcinogenesis. Mol. Carcinog. 2004, 40:1-11.
25. Clutton-Brock T.H. The evolution of parental care 1991, Vol. 1. Princeton University Press, Princeton, New Jersey.
26. Constancia M., Kelsey G., Reik W. Resourceful imprinting. Nature 2004, 432:53-57.
27. Crews D., Gore A.C., Hsu T.S., Dangleben N.L., Spinetta M., Schallert T., Anway M.D., Skinner M.K. Transgenerational epigenetic imprints on mate preference. Proc. Natl Acad. Sci. USA 2007, 104:5942-5946.
28. Cropley J.E., Suter C.M., Beckman K.B., Martin D.I. Germ-line epigenetic modification of the murine A vy allele by nutritional supplementation. Proc. Natl Acad. Sci. USA 2006, 103:17308-17312.
29. Cunningham E.J., Russell A.F. Egg investment is influenced by male attractiveness in the mallard. Nature 2000, 404:74-77.
30. Curley J.P., Barton S., Surani A., Keverne E.B. Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proc Biol Sci. 2004, 271:1303-1309.
31. Curley J.P., Rock V., Moynihan A.M., Bateson P., Keverne E.B., Champagne F.A. Developmental shifts in the behavioral phenotypes of inbred mice: the role of postnatal and juvenile social experiences. Behav. Genet. 2010, 40:220-232.
32. Delbes G., Hales B.F., Robaire B. Toxicants and human sperm chromatin integrity. Mol. Hum. Reprod. 2010, 16:14-22.
33. Dolinoy D.C., Jirtle R.L. Environmental epigenomics in human health and disease. Environ. Mol. Mutagen. 2008, 49:4-8.
34. Dolinoy D.C., Huang D., Jirtle R.L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl Acad. Sci. USA 2007, 104:13056-13061.
35. Drake A.J., Liu L. Intergenerational transmission of programmed effects: public health consequences. Trends Endocrinol. Metab. 2010, 21:206-213.
36. Drake A.J., Walker B.R., Seckl J.R. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R34-R38.
37. Drickamer L.C., Gowaty P.A., Holmes C.M. Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim. Behav. 2000, 59:371-378.
38. Drickamer L.C., Gowaty P.A., Wagner D.M. Free mutual mate preferences in house mice affect reproductive success and offspring performance. Anim. Behav. 2003, 65:105-114.
39. Dunn G.A., Bale T.L. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 2009, 150:4999-5009.
40. Egan C.M., Sridhar S., Wigler M., Hall I.M. Recurrent DNA copy number variation in the laboratory mouse. Nat. Genet. 2007, 39:1384-1389.
41. Flanagan J.M., Popendikyte V., Pozdniakovaite N., Sobolev M., Assadzadeh A., Schumacher A., Zangeneh M., Lau L., Virtanen C., Wang S.C., Petronis A. Intra- and interindividual epigenetic variation in human germ cells. Am. J. Hum. Genet. 2006, 79:67-84.
42. Fraga M.F., Ballestar E., Paz M.F., Ropero S., Setien F., Ballestar M.L., Heine-Suner D., Cigudosa J.C., Urioste M., Benitez J., Boix-Chornet M., Sanchez-Aguilera A., Ling C., Carlsson E., Poulsen P., Vaag A., Stephan Z., Spector T.D., Wu Y.Z., Plass C., Esteller M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. USA 2005, 102:10604-10609.
43. Frans E.M., Sandin S., Reichenberg A., Lichtenstein P., Langstrom N., Hultman C.M. Advancing paternal age and bipolar disorder. Arch. Gen. Psychiatry 2008, 65:1034-1040.
44. Garcia-Palomares S., Navarro S., Pertusa J.F., Hermenegildo C., Garcia-Perez M.A., Rausell F., Cano A., Tarin J.J. Delayed fatherhood in mice decreases reproductive fitness and longevity of offspring. Biol. Reprod. 2009, 80:343-349.
45. Garcia-Palomares S., Pertusa J.F., Minarro J., Garcia-Perez M.A., Hermenegildo C., Rausell F., Cano A., Tarin J.J. Long-term effects of delayed fatherhood in mice on postnatal development and behavioral traits of offspring. Biol. Reprod. 2009, 80:337-342.
46. Gilbert L., Williamson K.A., Hazon N., Graves J.A. Maternal effects due to male attractiveness affect offspring development in the zebra finch. Proc Biol Sci. 2006, 273:1765-1771.
47. Gowaty P.A. Reproductive compensation. J. Evol. Biol. 2008, 21:1189-1200.
48. Gowaty P.A., Anderson W.W., Bluhm C.K., Drickamer L.C., Kim Y.K., Moore A.J. The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc. Natl Acad. Sci. USA 2007, 104:15023-15027.
49. Grandjean V., Gounon P., Wagner N., Martin L., Wagner K.D., Bernex F., Cuzin F., Rassoulzadegan M. The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 2009, 136:3647-3655.
50. Hales B.F., Robaire B. Paternal exposure to drugs and environmental chemicals: effects on progeny outcome. J. Androl. 2001, 22:927-936.
51. Hamatani T., Falco G., Carter M.G., Akutsu H., Stagg C.A., Sharov A.A., Dudekula D.B., VanBuren V., Ko M.S. Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 2004, 13:2263-2278.
52. Harris W.E., Uller T. Reproductive investment when mate quality varies: differential allocation versus reproductive compensation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:1039-1048.
53. Harrison M., Langley-Evans S.C. Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br. J. Nutr. 2009, 101:1020-1030.
54. He F., Lidow I.A., Lidow M.S. Consequences of paternal cocaine exposure in mice. Neurotoxicol. Teratol. 2006, 28:198-209.
55. Hegedus A.M., Alterman A.I., Tarter R.E. Learning achievement in sons of alcoholics. Alcohol. Clin. Exp. Res. 1984, 8:330-333.
56. Jablonka E., Lamb M.J. Epigenetic Inheritance and Evolution: the Lamarckian Dimension 1995, Oxford University Press, Vol.
57. Jablonka E., Raz G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 2009, 84:131-176.
58. Jimenez-Chillaron J.C., Isganaitis E., Charalambous M., Gesta S., Pentinat-Pelegrin T., Faucette R.R., Otis J.P., Chow A., Diaz R., Ferguson-Smith A., Patti M.E. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009, 58:460-468.
59. Kaati G., Bygren L.O., Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur. J. Hum. Genet. 2002, 10:682-688.
60. Kaati G., Bygren L.O., Pembrey M., Sjostrom M. Transgenerational response to nutrition, early life circumstances and longevity. Eur. J. Hum. Genet. 2007, 15:784-790.
61. Keverne E.B., Curley J.P. Epigenetics, brain evolution and behaviour. Front. Neuroendocrinol. 2008, 29:398-412.
62. Lane N., Dean W., Erhardt S., Hajkova P., Surani A., Walter J., Reik W. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003, 35:88-93.
63. Ledig M., Misslin R., Vogel E., Holownia A., Copin J.C., Tholey G. Paternal alcohol exposure: developmental and behavioral effects on the offspring of rats. Neuropharmacology 1998, 37:57-66.
64. Lin W.Y., Chiu T.Y., Lee L.T., Lin C.C., Huang C.Y., Huang K.C. Betel nut chewing is associated with increased risk of cardiovascular disease and all-cause mortality in Taiwanese men. Am. J. Clin. Nutr. 2008, 87:1204-1211.
65. Linschooten J.O., Van Schooten F.J., Baumgartner A., Cemeli E., Van Delft J., Anderson D., Godschalk R.W. Use of spermatozoal mRNA profiles to study gene-environment interactions in human germ cells. Mutat. Res. 2009, 667:70-76.
66. Little R.E. Mother's and father's birthweight as predictors of infant birthweight. Paediatr. Perinat. Epidemiol. 1987, 1:19-31.
67. Lundstrom S., Haworth C.M., Carlstrom E., Gillberg C., Mill J., Rastam M., Hultman C.M., Ronald A., Anckarsater H., Plomin R., Lichtenstein P., Reichenberg A. Trajectories leading to autism spectrum disorders are affected by paternal age: findings from two nationally representative twin studies. J. Child Psychol. Psychiatry 2010, 51:850-856.
68. Lupo di Prisco C., Lucarini N., Dessi-Fulgheri F. Testosterone aromatization in rat brain is modulated by social environment. Physiol. Behav. 1978, 20:345-348.
69. Malaspina D., Harlap S., Fennig S., Heiman D., Nahon D., Feldman D., Susser E.S. Advancing paternal age and the risk of schizophrenia. Arch. Gen. Psychiatry 2001, 58:361-367.
70. Malaspina D., Reichenberg A., Weiser M., Fennig S., Davidson M., Harlap S., Wolitzky R., Rabinowitz J., Susser E., Knobler H.Y. Paternal age and intelligence: implications for age-related genomic changes in male germ cells. Psychiatr. Genet. 2005, 15:117-125.
71. McIntosh G.C., Olshan A.F., Baird P.A. Paternal age and the risk of birth defects in offspring. Epidemiology 1995, 6:282-288.
72. Meek L.R., Myren K., Sturm J., Burau D. Acute paternal alcohol use affects offspring development and adult behavior. Physiol. Behav. 2007, 91:154-160.
73. Mohn F., Schubeler D. Genetics and epigenetics: stability and plasticity during cellular differentiation. Trends Genet. 2009, 25:129-136.
74. Morgan H.D., Sutherland H.G., Martin D.I., Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 1999, 23:314-318.
75. Nachman M.W., Crowell S.L. Estimate of the mutation rate per nucleotide in humans. Genetics 2000, 156:297-304.
76. Oakes C.C., Smiraglia D.J., Plass C., Trasler J.M., Robaire B. Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats. Proc. Natl Acad. Sci. USA 2003, 100:1775-1780.
77. Ouko L.A., Shantikumar K., Knezovich J., Haycock P., Schnugh D.J., Ramsay M. Effect of alcohol consumption on CpG methylation in the differentially methylated regions of H19 and IG-DMR in male gametes: implications for fetal alcohol spectrum disorders. Alcohol. Clin. Exp. Res. 2009, 33:1615-1627.
78. Pandey S.C., Ugale R., Zhang H., Tang L., Prakash A. Brain chromatin remodeling: a novel mechanism of alcoholism. J. Neurosci. 2008, 28:3729-3737.
79. Pembrey M.E., Bygren L.O., Kaati G., Edvinsson S., Northstone K., Sjostrom M., Golding J. Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 2006, 14:159-166.
80. Plagge A., Gordon E., Dean W., Boiani R., Cinti S., Peters J., Kelsey G. The imprinted signaling protein XL alpha s is required for postnatal adaptation to feeding. Nat. Genet. 2004, 36:818-826.
81. Probst A.V., Dunleavy E., Almouzni G. Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell Biol. 2009, 10:192-206.
82. Rakyan V.K., Chong S., Champ M.E., Cuthbert P.C., Morgan H.D., Luu K.V., Whitelaw E. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc. Natl Acad. Sci. USA 2003, 100:2538-2543.
83. Rassoulzadegan M., Grandjean V., Gounon P., Vincent S., Gillot I., Cuzin F. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 2006, 441:469-474.
84. Ratikainen I.I., Kokko H. Differential allocation and compensation: who deserves the silver spoon?. Behav. Ecol. 2009, 21:195-200.
85. Reichenberg A., Gross R., Weiser M., Bresnahan M., Silverman J., Harlap S., Rabinowitz J., Shulman C., Malaspina D., Lubin G., Knobler H.Y., Davidson M., Susser E. Advancing paternal age and autism. Arch. Gen. Psychiatry 2006, 63:1026-1032.
86. Risch N., Reich E.W., Wishnick M.M., McCarthy J.G. Spontaneous mutation and parental age in humans. Am. J. Hum. Genet. 1987, 41:218-248.
87. Schalkwyk L.C., Meaburn E.L., Smith R., Dempster E.L., Jeffries A.R., Davies M.N., Plomin R., Mill J. Allelic skewing of DNA methylation is widespread across the genome. Am. J. Hum. Genet. 2010, 86:196-212.
88. Sheldon B.C. Differential allocation: tests, mechanisms and implications. Trends Ecol. Evol. 2000, 15:397-402.
89. Shi L., Wu J. Epigenetic regulation in mammalian preimplantation embryo development. Reprod. Biol. Endocrinol. 2009, 7:59.
90. Skinner M.K. What is an epigenetic transgenerational phenotype? F3 or F2. Reprod. Toxicol. 2008, 25:2-6.
91. Skinner M.K., Anway M.D., Savenkova M.I., Gore A.C., Crews D. Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS ONE 2008, 3:e3745.
92. Smith R.G., Kember R.L., Mill J., Fernandes C., Schalkwyk L.C., Buxbaum J.D., Reichenberg A. Advancing paternal age is associated with deficits in social and exploratory behaviors in the offspring: a mouse model. PLoS ONE 2009, 4:e8456.
93. Stouder C., Paoloni-Giacobino A. Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction 2010, 139:373-379.
94. Stouder C., Deutsch S., Paoloni-Giacobino A. Superovulation in mice alters the methylation pattern of imprinted genes in the sperm of the offspring. Reprod. Toxicol. 2009, 28:536-541.
95. Tarter R.E., Hegedus A.M., Goldstein G., Shelly C., Alterman A.I. Adolescent sons of alcoholics: neuropsychological and personality characteristics. Alcohol. Clin. Exp. Res. 1984, 8:216-222.
96. Wagner K.D., Wagner N., Ghanbarian H., Grandjean V., Gounon P., Cuzin F., Rassoulzadegan M. RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev. Cell 2008, 14:962-969.
97. Walter C.A., Intano G.W., McCarrey J.R., McMahan C.A., Walter R.B. Mutation frequency declines during spermatogenesis in young mice but increases in old mice. Proc. Natl Acad. Sci. USA 1998, 95:10015-10019.
98. Weiser M., Reichenberg A., Werbeloff N., Kleinhaus K., Lubin G., Shmushkevitch M., Caspi A., Malaspina D., Davidson M. Advanced parental age at birth is associated with poorer social functioning in adolescent males: shedding light on a core symptom of schizophrenia and autism. Schizophr. Bull. 2008, 34:1042-1046.
99. Wohr M., Oddi D., D'Amato F.R. Effect of altricial pup ultrasonic vocalization on maternal behavior Handbook of Behavioral Neuroscience. 2009, 19:159-166.
100. Wozniak D.F., Cicero T.J., Kettinger L., Meyer E.R. Paternal alcohol consumption in the rat impairs spatial learning performance in male offspring. Psychopharmacology (Berl) 1991, 105:289-302.
101. Yauk C., Polyzos A., Rowan-Carroll A., Somers C.M., Godschalk R.W., Van Schooten F.J., Berndt M.L., Pogribny I.P., Koturbash I., Williams A., Douglas G.R., Kovalchuk O. Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc. Natl Acad. Sci. USA 2008, 105:605-610.
102. Youngson N.A., Whitelaw E. Transgenerational epigenetic effects. Annu. Rev. Genomics Hum. Genet. 2008, 9:233-257.