Environmentally induced epigenetic transgenerational inheritance of male infertility

Current Opinion in Genetics and Development

Volumn 26, Issue , 2014, Pages 79-88

  Guerrero Bosagna, Carlos ^a   Skinner, Michael K ^b  

^a LINKÖPING UNIVERSITY   (Sweden)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA MODIFICATION; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPIGENETIC TRANSGENERATIONAL INHERITANCE; EPIGENETICS; GENETIC ASSOCIATION; HUMAN; INHERITANCE; LIFESTYLE; MALE INFERTILITY; MOLECULAR PATHOLOGY; NONHUMAN; NUTRITIONAL HEALTH; OCCUPATIONAL EXPOSURE; PRIORITY JOURNAL; REVIEW; SEX DETERMINATION; ANIMAL; BIOLOGICAL MODEL; CHEMICALLY INDUCED; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; INTOXICATION; MALE; POLLUTANT;

AGRICULTURAL CHEMICAL; ENDOCRINE DISRUPTOR; POLLUTANT;

AGROCHEMICALS; ANIMALS; ENDOCRINE DISRUPTORS; ENVIRONMENTAL POLLUTANTS; EPIGENESIS, GENETIC; HUMANS; INFERTILITY, MALE; INHERITANCE PATTERNS; MALE; MODELS, GENETIC;

EID: 84905392764     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2014.06.005     Document Type: Review

References (118)

1. Main K.M., Skakkebaek N.E., Virtanen H.E., Toppari J. Genital anomalies in boys and the environment. Best Pract Res Clin Endocrinol Metab 2010, 24:279-289.
2. Sharpe R.M. Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010, 365:1697-1712.
3. Skakkebaek N.E., Rajpert-De Meyts E., Jorgensen N., Main K.M., Leffers H., Andersson A.M., Juul A., Jensen T.K., Toppari J. Testicular cancer trends as 'whistle blowers' of testicular developmental problems in populations. Int J Androl 2007, 30:198-204. discussion 204-195.
4. Andersson A.M., Jorgensen N., Main K.M., Toppari J., Rajpert-De Meyts E., Leffers H., Juul A., Jensen T.K., Skakkebaek N.E. Adverse trends in male reproductive health: we may have reached a crucial 'tipping point'. Int J Androl 2008, 31:74-80.
5. Carlsen E., Giwercman A., Keiding N., Skakkebaek N.E. Evidence for decreasing quality of semen during past 50 years. BMJ 1992, 305:609-613.
6. Merzenich H., Zeeb H., Blettner M. Decreasing sperm quality: a global problem?. BMC Public Health 2010, 10:24.
7. Swan S.H., Elkin E.P., Fenster L. Have sperm densities declined? A reanalysis of global trend data. Environ Health Perspect 1997, 105:1228-1232.
8. Swan S.H., Elkin E.P., Fenster L. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ Health Perspect 2000, 108:961-966.
9. Brenseke B., Prater M.R., Bahamonde J., Gutierrez J.C. Current thoughts on maternal nutrition and fetal programming of the metabolic syndrome. J Pregnancy 2013, 2013:368461.
10. Skakkebaek N.E., Rajpert-De Meyts E., Main K.M. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 2001, 16:972-978.
11. Giwercman A., Giwercman Y.L. Environmental factors and testicular function. Best Pract Res Clin Endocrinol Metab 2011, 25:391-402.
12. Wohlfahrt-Veje C., Main K.M., Skakkebaek N.E. Testicular dysgenesis syndrome: foetal origin of adult reproductive problems. Clin Endocrinol 2009, 71:459-465.
13. Nordkap L., Joensen U.N., Blomberg Jensen M., Jorgensen N. Regional differences and temporal trends in male reproductive health disorders: semen quality may be a sensitive marker of environmental exposures. Mol Cell Endocrinol 2012, 355:221-230.
14. Skinner M.K. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 2011, 6:838-842.
15. Guerrero-Bosagna C., Savenkova M., Haque M.M., Sadler-Riggleman I., Skinner M.K. Environmentally induced epigenetic transgenerational inheritance of altered sertoli cell transcriptome and epigenome: molecular etiology of male infertility. PLoS ONE 2013, 8:e59922.
16. Guillette L.J., Iguchi T. Ecology. Life in a contaminated world. Science 2012, 337:1614-1615.
17. Guerrero-Bosagna C., Skinner M.K. Environmentally induced epigenetic transgenerational inheritance of phenotype and disease. Mol Cell Endocrinol 2012, 354:3-8.
18. Skinner M.K., Manikkam M., Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 2010, 21:214-222.
19. Bay K., Asklund C., Skakkebaek N.E., Andersson A.M. Testicular dysgenesis syndrome: possible role of endocrine disrupters. Best Pract Res Clin Endocrinol Metab 2006, 20:77-90.
20. Damgaard I.N., Skakkebaek N.E., Toppari J., Virtanen H.E., Shen H., Schramm K.W., Petersen J.H., Jensen T.K., Main K.M. Persistent pesticides in human breast milk and cryptorchidism. Environ Health Perspect 2006, 114:1133-1138.
21. Andersen H.R., Schmidt I.M., Grandjean P., Jensen T.K., Budtz-Jorgensen E., Kjaerstad M.B., Baelum J., Nielsen J.B., Skakkebaek N.E., Main K.M. Impaired reproductive development in sons of women occupationally exposed to pesticides during pregnancy. Environ Health Perspect 2008, 116:566-572.
22. Main K.M., Mortensen G.K., Kaleva M.M., Boisen K.A., Damgaard I.N., Chellakooty M., Schmidt I.M., Suomi A.M., Virtanen H.E., Petersen D.V., Andersson A.M., Toppari J., Skakkebaek N.E. Human breast milk contamination with phthalates and alterations of endogenous reproductive hormones in infants three months of age. Environ Health Perspect 2006, 114:270-276.
23. Swan S.H., Main K.M., Liu F., Stewart S.L., Kruse R.L., Calafat A.M., Mao C.S., Redmon J.B., Ternand C.L., Sullivan S., Teague J.L. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 2005, 113:1056-1061.
24. Kristensen D.M., Hass U., Lesne L., Lottrup G., Jacobsen P.R., Desdoits-Lethimonier C., Boberg J., Petersen J.H., Toppari J., Jensen T.K., Brunak S., Skakkebaek N.E., Nellemann C., Main K.M., Jegou B., Leffers H. Intrauterine exposure to mild analgesics is a risk factor for development of male reproductive disorders in human and rat. Hum Reprod 2011, 26:235-244.
25. Ramlau-Hansen C.H., Thulstrup A.M., Storgaard L., Toft G., Olsen J., Bonde J.P. Is prenatal exposure to tobacco smoking a cause of poor semen quality? A follow-up study. Am J Epidemiol 2007, 165:1372-1379.
26. Ravnborg T.L., Jensen T.K., Andersson A.M., Toppari J., Skakkebaek N.E., Jorgensen N. Prenatal and adult exposures to smoking are associated with adverse effects on reproductive hormones, semen quality, final height and body mass index. Hum Reprod 2011, 26:1000-1011.
27. Damgaard I.N., Jensen T.K., Petersen J.H., Skakkebaek N.E., Toppari J., Main K.M. Cryptorchidism and maternal alcohol consumption during pregnancy. Environ Health Perspect 2007, 115:272-277.
28. Guo Y.L., Hsu P.C., Hsu C.C., Lambert G.H. Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet 2000, 356:1240-1241.
29. Guo Y.L., Lambert G.H., Hsu C.C., Hsu M.M. Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. Int Arch Occup Environ Health 2004, 77:153-158.
30. Whorton D., Milby T.H., Krauss R.M., Stubbs H.A. Testicular function in DBCP exposed pesticide workers. J Occup Med 1979, 21:161-166.
31. Thrupp L.A. Sterilization of workers from pesticide exposure: the causes and consequences of DBCP-induced damage in Costa Rica and beyond. Int J Health Serv 1991, 21:731-757.
32. Skakkebaek N.E., Jorgensen N., Main K.M., Rajpert-De Meyts E., Leffers H., Andersson A.M., Juul A., Carlsen E., Mortensen G.K., Jensen T.K., Toppari J. Is human fecundity declining?. Int J Androl 2006, 29:2-11.
33. Pimentel D., Cooperstein S., Randell H., Filiberto D., Sorrentino S., Kaye B., Nicklin C., Yagi J., Brian J., O'Hern J., Habas A., Weinstein1 C. Ecology of increasing diseases: population growth and environmental degradation. Human Ecology 2007, 35:653-668.
34. Dohle G.R., Halley D.J., Van Hemel J.O., van den Ouwel A.M., Pieters M.H., Weber R.F., Govaerts L.C. Genetic risk factors in infertile men with severe oligozoospermia and azoospermia. Hum Reprod 2002, 17:13-16.
35. Huynh T., Mollard R., Trounson A. Selected genetic factors associated with male infertility. Hum Reprod Update 2002, 8:183-198.
36. Grigorova M., Punab M., Ausmees K., Laan M. FSHB promoter polymorphism within evolutionary conserved element is associated with serum FSH level in men. Hum Reprod 2008, 23:2160-2166.
37. Crackower M.A., Kolas N.K., Noguchi J., Sarao R., Kikuchi K., Kaneko H., Kobayashi E., Kawai Y., Kozieradzki I., Landers R., Mo R., Hui C.C., Nieves E., Cohen P.E., Osborne L.R., Wada T., Kunieda T., Moens P.B., Penninger J.M. Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 2003, 300:1291-1295.
38. Sinha N., Puri P., Nairn A.C., Vijayaraghavan S. Selective ablation of Ppp1cc gene in testicular germ cells causes oligo-teratozoospermia and infertility in mice. Biol Reprod 2013, (Epub ahead of print).
39. Bashamboo A., Ferraz-de-Souza B., Lourenco D., Lin L., Sebire N.J., Montjean D., Bignon-Topalovic J., Mandelbaum J., Siffroi J.P., Christin-Maitre S., Radhakrishna U., Rouba H., Ravel C., Seeler J., Achermann J.C., McElreavey K. Human male infertility associated with mutations in NR5A1 encoding steroidogenic factor 1. Am J Hum Genet 2010, 87:505-512.
40. Okada H., Tajima A., Shichiri K., Tanaka A., Tanaka K., Inoue I. Genome-wide expression of azoospermia testes demonstrates a specific profile and implicates ART3 in genetic susceptibility. PLoS Genet 2008, 4:e26.
41. Kosova G., Scott N.M., Niederberger C., Prins G.S., Ober C. Genome-wide association study identifies candidate genes for male fertility traits in humans. Am J Hum Genet 2012, 90:950-961.
42. Hu Z., Xia Y., Guo X., Dai J., Li H., Hu H., Jiang Y., Lu F., Wu Y., Yang X., Yao B., Lu C., Xiong C., Li Z., Gui Y., Liu J., Zhou Z., Shen H., Wang X., Sha J. A genome-wide association study in Chinese men identifies three risk loci for non-obstructive azoospermia. Nat Genet 2012, 44:183-186.
43. Aston K.I., Carrell D.T. Genome-wide study of single-nucleotide polymorphisms associated with azoospermia and severe oligozoospermia. J Androl 2009, 30:711-725.
44. Aston K.I., Krausz C., Laface I., Ruiz-Castane E., Carrell D.T. Evaluation of 172 candidate polymorphisms for association with oligozoospermia or azoospermia in a large cohort of men of European descent. Hum Reprod 2010, 25:1383-1397.
45. Hughes I.A., Martin H., Jaaskelainen J. Genetic mechanisms of fetal male undermasculinization: a background to the role of endocrine disruptors. Environ Res 2006, 100:44-49.
46. 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.
47. Guerrero-Bosagna C., Skinner M. Environmental epigenetics and effects on male fertility. Advances in experimental medicine and biology 2014, 67-81.
48. Oosterhuis J.W., Looijenga L.H. Testicular germ-cell tumours in a broader perspective. Nat Rev Cancer 2005, 5:210-222.
49. Rajender S., Avery K., Agarwal A. Epigenetics, spermatogenesis and male infertility. Mutat Res 2011, 727:62-71.
50. Hammoud S.S., Nix D.A., Hammoud A.O., Gibson M., Cairns B.R., Carrell D.T. 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 2011, 26:2558-2569.
51. Hammoud S.S., Purwar J., Pflueger C., Cairns B.R., Carrell D.T. Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil Steril 2010, 94:1728-1733.
52. Kobayashi H., Sato A., Otsu E., Hiura H., Tomatsu C., Utsunomiya T., Sasaki H., Yaegashi N., Arima T. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 2007, 16:2542-2551.
53. Marques C.J., Carvalho F., Sousa M., Barros A. Genomic imprinting in disruptive spermatogenesis. Lancet 2004, 363:1700-1702.
54. Marques C.J., Costa P., Vaz B., Carvalho F., Fernandes S., Barros A., Sousa M. Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 2008, 14:67-74.
55. Marques C.J., Francisco T., Sousa S., Carvalho F., Barros A., Sousa M. Methylation defects of imprinted genes in human testicular spermatozoa. Fertil Steril 2010, 94:585-594.
56. Paradowska A.S., Miller D., Spiess A.N., Vieweg M., Cerna M., Dvorakova-Hortova K., Bartkuhn M., Schuppe H.C., Weidner W., Steger K. Genome wide identification of promoter binding sites for H4K12ac in human sperm and its relevance for early embryonic development. Epigenetics 2012, 7:1057-1070.
57. Houshdaran S., Cortessis V.K., Siegmund K., Yang A., Laird P.W., Sokol R.Z. Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS ONE 2007, 2:e1289.
58. Wu W., Shen O., Qin Y., Niu X., Lu C., Xia Y., Song L., Wang S., Wang X. Idiopathic male infertility is strongly associated with aberrant promoter methylation of methylenetetrahydrofolate reductase (MTHFR). PLoS ONE 2010, 5:e13884.
59. Boissonnas C.C., Abdalaoui H.E., Haelewyn V., Fauque P., Dupont J.M., Gut I., Vaiman D., Jouannet P., Tost J., Jammes H. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet 2010, 18:73-80.
60. Steilmann C., Cavalcanti M.C., Bartkuhn M., Pons-Kuhnemann J., Schuppe H.C., Weidner W., Steger K., Paradowska A. The interaction of modified histones with the bromodomain testis-specific (BRDT) gene and its mRNA level in sperm of fertile donors and subfertile men. Reproduction 2010, 140:435-443.
61. Sonnack V., Failing K., Bergmann M., Steger K. Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 2002, 34:384-390.
62. Okada Y., Scott G., Ray M.K., Mishina Y., Zhang Y. Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature 2007, 450:119-123.
63. Ichiyanagi K., Li Y., Watanabe T., Ichiyanagi T., Fukuda K., Kitayama J., Yamamoto Y., Kuramochi-Miyagawa S., Nakano T., Yabuta Y., Seki Y., Saitou M., Sasaki H. Locus- and domain-dependent control of DNA methylation at mouse B1 retrotransposons during male germ cell development. Genome Res 2011, 21:2058-2066.
64. Heyn H., Ferreira H.J., Bassas L., Bonache S., Sayols S., Sandoval J., Esteller M., Larriba S. Epigenetic disruption of the PIWI pathway in human spermatogenic disorders. PLoS ONE 2012, 7:e47892.
65. Shanker S., Hu Z., Wilkinson M.F. Epigenetic regulation and downstream targets of the Rhox5 homeobox gene. Int J Androl 2008, 31:462-470.
66. Nicholls P.K., Harrison C.A., Walton K.L., McLachlan R.I., O'Donnell L., Stanton P.G. Hormonal regulation of sertoli cell micro-RNAs at spermiation. Endocrinology 2011, 152:1670-1683.
67. Papaioannou M.D., Pitetti J.L., Ro S., Park C., Aubry F., Schaad O., Vejnar C.E., Kuhne F., Descombes P., Zdobnov E.M., McManus M.T., Guillou F., Harfe B.D., Yan W., Jegou B., Nef S. Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 2009, 326:250-259.
68. Korhonen H.M., Meikar O., Yadav R.P., Papaioannou M.D., Romero Y., Da Ros M., Herrera P.L., Toppari J., Nef S., Kotaja N. Dicer is required for haploid male germ cell differentiation in mice. PLoS ONE 2011, 6:e24821.
69. Martinez-Arguelles D.B., Campioli E., Culty M., Zirkin B.R., Papadopoulos V. Fetal origin of endocrine dysfunction in the adult: the phthalate model. J Steroid Biochem Mol Biol 2013, 137:5-17.
70. Uzumcu M., Suzuki H., Skinner M.K. Effect of the anti-androgenic endocrine disruptor vinclozolin on embryonic testis cord formation and postnatal testis development and function. Reprod Toxicol 2004, 18:765-774.
71. LaRocca J., Boyajian A., Brown C., Smith S.D., Hixon M. Effects of in utero exposure to bisphenol A or diethylstilbestrol on the adult male reproductive system. Birth Defects Res B Dev Reprod Toxicol 2011, 92:526-533.
72. Park C.J., Nah W.H., Lee J.E., Oh Y.S., Gye M.C. Butyl paraben-induced changes in DNA methylation in rat epididymal spermatozoa. Andrologia 2012, 44(Suppl 1):187-193.
73. Stouder C., Paoloni-Giacobino A. Specific transgenerational imprinting effects of the endocrine disruptor methoxychlor on male gametes. Reproduction 2011, 141:207-216.
74. 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.
75. Doshi T., D'Souza C., Vanage G. Aberrant DNA methylation at Igf2-H19 imprinting control region in spermatozoa upon neonatal exposure to bisphenol A and its association with post implantation loss. Mol Biol Rep 2013, 40:4747-4757.
76. Doshi T., Mehta S.S., Dighe V., Balasinor N., Vanage G. Hypermethylation of estrogen receptor promoter region in adult testis of rats exposed neonatally to bisphenol A. Toxicology 2011, 289:74-82.
77. Stouder C., Somm E., Paoloni-Giacobino A. Prenatal exposure to ethanol: a specific effect on the H19 gene in sperm. Reprod Toxicol 2011, 31:507-512.
78. Guerrero-Bosagna C., Covert T., Haque M.M., Settles M., Nilsson E.E., Anway M.D., Skinner M.K. Epigenetic transgenerational inheritance of vinclozolin induced mouse adult onset disease and associated sperm epigenome biomarkers. Reprod Toxicol 2012, 34:694-707.
79. Guerrero-Bosagna C., Settles M., Lucker B., Skinner M. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 2010, 5:e13100.
80. Lee S.-H., Oh T. Genome-wide analysis of epigenetic changes in mouse sperm by maternal exposure to endocrine disruptor vinclozolin. Mol Cell Toxicol 2012, 43-52.
81. 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.
82. Anway M.D., Leathers C., Skinner M.K. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 2006, 147:5515-5523.
83. Anway M.D., Memon M.A., Uzumcu M., Skinner M.K. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J Androl 2006, 27:868-879.
84. Olsen A.K., Andreassen A., Singh R., Wiger R., Duale N., Farmer P.B., Brunborg G. Environmental exposure of the mouse germ line: DNA adducts in spermatozoa and formation of de novo mutations during spermatogenesis. PLoS ONE 2010, 5:e11349.
85. Singh K.P., Kumari R., Pevey C., Jackson D., DuMond J.W. Long duration exposure to cadmium leads to increased cell survival, decreased DNA repair capacity, and genomic instability in mouse testicular Leydig cells. Cancer Lett 2009, 279:84-92.
86. Grimaldi P., Pucci M., Di Siena S., Di Giacomo D., Pirazzi V., Geremia R., Maccarrone M. The faah gene is the first direct target of estrogen in the testis: role of histone demethylase LSD1. Cell Mol Life Sci 2012, 69:4177-4190.
87. Reddy P.M., Reddy P.R. Differential regulation of DNA methylation in rat testis and its regulation by gonadotropic hormones. J Steroid Biochem 1990, 35:173-178.
88. Nilsson E., Larsen G., Manikkam M., Guerrero-Bosagna C., Savenkova M., Skinner M. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS ONE 2012, 7:e36129.
89. Wong C., Kelce W.R., Sar M., Wilson E.M. Androgen receptor antagonist versus agonist activities of the fungicide vinclozolin relative to hydroxyflutamide. J Biol Chem 1995, 270:19998-20003.
90. Doyle T.J., Bowman J.L., Windell V.L., McLean D.J., Kim K.H. Transgenerational effects of di-(2-ethylhexyl) phthalate on testicular germ cell associations and spermatogonial stem cells in mice. Biol Reprod 2013, 88:112.
91. Salian S., Doshi T., Vanage G. Perinatal exposure of rats to bisphenol A affects fertility of male offspring--an overview. Reprod Toxicol 2011, 31:359-362.
92. Salian S., Doshi T., Vanage G. Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to bisphenol A. Life Sci 2009, 85:11-18.
93. Mohamed el S.A., Song W.H., Oh S.A., Park Y.J., You Y.A., Lee S., Choi J.Y., Kim Y.J., Jo I., Pang M.G. The transgenerational impact of benzo(a)pyrene on murine male fertility. Hum Reprod 2010, 25:2427-2433.
94. Dunn G.A., Bale T.L. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 2011, 152:2228-2236.
95. Skinner M.K., Manikkam M., Tracey R., Nilsson E., Haque M.M., Guerrero-Bosagna C. Ancestral DDT exposures promote epigenetic transgenerational inheritance of obesity. BMC Med 2013, 11:228.
96. Waterland R.A., Travisano M., Tahiliani K.G., Rached M.T., Mirza S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes (Lond) 2008, 32:1373-1379.
97. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations. PLoS ONE 2013, 8:e55387.
98. Tracey R., Manikkam M., Guerrero-Bosagna C., Skinner M. Hydrocarbon (Jet Fuel JP-8) induces epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations. Reprod Toxicol 2013, 36:104-116.
99. Bruner-Tran K.L., Osteen K.G. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol 2011, 31:344-350.
100. Nilsson E.E., Anway M.D., Stanfield J., Skinner M.K. Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease. Reproduction 2008, 135:713-721.
101. Manikkam M., Guerrero-Bosagna C., Tracey R., Haque M.M., Skinner M.K. Transgenerational actions of environmental compounds on reproductive disease and epigenetic biomarkers of ancestral exposures. PLoS ONE 2012, 7:e31901.
102. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M. Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations. Reprod Toxicol 2012, 34:708-719.
103. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M.K. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS ONE 2012, 7:e46249.
104. Chamorro-Garcia R., Sahu M., Abbey R.J., Laude J., Pham N., Blumberg B. Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice. Environ Health Perspect 2013, 121:359-366.
105. Hauser M.T., Aufsatz W., Jonak C., Luschnig C. Transgenerational epigenetic inheritance in plants. Biochim Biophys Acta 2011, 1809:459-468.
106. Ruden D.M., Lu X. Hsp90 affecting chromatin remodeling might explain transgenerational epigenetic inheritance in Drosophila. Curr Genomics 2008, 9:500-508.
107. Greer E.L., Maures T.J., Ucar D., Hauswirth A.G., Mancini E., Lim J.P., Benayoun B.A., Shi Y., Brunet A. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 2011, 479:365-371.
108. Pembrey M.E. Male-line transgenerational responses in humans. Hum Fertil (Camb) 2010, 13:268-271.
109. Lees-Murdock D.J., Walsh C.P. DNA methylation reprogramming in the germ line. Epigenetics 2008, 3:5-13.
110. Reik W., Dean W., Walter J. Epigenetic reprogramming in mammalian development. Science 2001, 293:1089-1093.
111. Allegrucci C., Thurston A., Lucas E., Young L. Epigenetics and the germline. Reproduction 2005, 129:137-149.
112. Durcova-Hills G., Hajkova P., Sullivan S., Barton S., Surani M.A., McLaren A. Influence of sex chromosome constitution on the genomic imprinting of germ cells. Proc Natl Acad Sci U S A 2006, 103:11184-11188.
113. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007, 8:253-262.
114. Clement T.M., Anway M.D., Uzumcu M., Skinner M.K. Regulation of the gonadal transcriptome during sex determination and testis morphogenesis: comparative candidate genes. Reproduction 2007, 134:455-472.
115. Clement T.M., Savenkova M.I., Settles M., Anway M.D., Skinner M.K. Alterations in the developing testis transcriptome following embryonic vinclozolin exposure. Reprod Toxicol 2010, 30:353-364.
116. Anway M.D., Rekow S.S., Skinner M.K. Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics 2008, 91:30-40.
117. Skinner M., Guerrero-Bosagna C., Haque M.M., Nilsson E., Bhandari R., McCarrey J. Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and subsequent germline. PLoS ONE 2013, 8:e66318.
118. Skinner M.K., Manikkam M., Haque M.M., Zhang B., Savenkova M. Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions. Genome Biol 2012, 13:R91.