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Environmental Epigenetics and Effects on Male Fertility

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 791))

Abstract

Environmental exposures to factors such as toxicants or nutrition can have impacts on testis biology and male fertility. The ability of these factors to influence epigenetic mechanisms in early life exposures or from ancestral exposures will be reviewed. A growing number of examples suggest environmental epigenetics will be a critical factor to consider in male reproduction.

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References

  • Adams NR (1981) A changed responsiveness to oestrogen in ewes with clover disease. J Reprod Fertil Suppl 30:223–230

    PubMed  CAS  Google Scholar 

  • Adams NR (1990) Permanent infertility in ewes exposed to plant oestrogens. Aust Vet J 67: 197–201

    PubMed  CAS  Google Scholar 

  • Adams NR (1995) Detection of the effects of phytoestrogens on sheep and cattle. J Anim Sci 73:1509–1515

    PubMed  CAS  Google Scholar 

  • Allegrucci C, Thurston A, Lucas E et al (2005) Epigenetics and the germline. Reproduction 129:137–149

    PubMed  CAS  Google Scholar 

  • Anetor JI, Wanibuchi H, Fukushima S (2007) Arsenic exposure and its health effects and risk of cancer in developing countries: micronutrients as host defence. Asian Pac J Cancer Prev 8(1):13–23

    PubMed  Google Scholar 

  • Anway MD, Cupp AS, Uzumcu M et al (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466–1469

    Google Scholar 

  • Anway MD, Leathers C, Skinner MK (2006) Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147:5515–5523

    PubMed  CAS  Google Scholar 

  • Arico JK, Katz DJ, van der Vlag J et al (2011) Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells. PLoS Genet 7:e1001391

    PubMed  CAS  Google Scholar 

  • Balabanic D, Rupnik M, Klemencic AK (2011) Negative impact of endocrine-disrupting compounds on human reproductive health. Reprod Fertil Dev 23:403–416

    PubMed  CAS  Google Scholar 

  • Barrionuevo F, Bagheri-Fam S, Klattig J et al (2006) Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol Reprod 74:195–201

    PubMed  CAS  Google Scholar 

  • Bhandari R, Sadler-Riggleman I, Clement TM et al (2011) Basic helix-loop-helix transcription factor TCF21 is a downstream target of the male sex determining gene SRY. PLoS One 6:e19935

    PubMed  CAS  Google Scholar 

  • Bhandari R, Haque Md M, Skinner M (2012a) Global genome analysis of the downstream binding targets of testis determining factor SRY AND SOX9. PLoS One 7:e43380

    PubMed  CAS  Google Scholar 

  • Bhandari RK, Schinke EN, Haque MM et al (2012b) SRY induced TCF21 genome-wide targets and cascade of bHLH factors during sertoli cell differentiation and male sex determination in rats. Biol Reprod 87:131

    PubMed  Google Scholar 

  • Boissonnas CC, Abdalaoui HE, Haelewyn V et al (2010) Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet 18:73–80

    PubMed  Google Scholar 

  • Bott RC, Clopton DT, Cupp AS (2008) A proposed role for VEGF isoforms in sex-specific vasculature development in the gonad. Reprod Domest Anim 43(Suppl 2):310–316

    PubMed  Google Scholar 

  • Bouma GJ, Albrecht KH, Washburn LL et al (2005) Gonadal sex reversal in mutant Dax1 XY mice: a failure to upregulate Sox9 in pre-Sertoli cells. Development 132:3045–3054

    PubMed  CAS  Google Scholar 

  • Bradford ST, Hiramatsu R, Maddugoda MP et al (2009) The cerebellin 4 precursor gene is a direct target of SRY and SOX9 in mice. Biol Reprod 80:1178–1188

    PubMed  CAS  Google Scholar 

  • Bruner-Tran KL, Osteen KG (2011) Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol 31:344–350

    PubMed  CAS  Google Scholar 

  • Buehr M, Gu S, McLaren A (1993) Mesonephric contribution to testis differentiation in the fetal mouse. Development 117:273–281

    PubMed  CAS  Google Scholar 

  • Bullejos M, Koopman P (2005) Delayed Sry and Sox9 expression in developing mouse gonads underlies B6-Y(DOM) sex reversal. Dev Biol 278:473–481

    PubMed  CAS  Google Scholar 

  • Burdge GC, Hoile SP, Uller T et al (2011) Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition. PLoS One 6:e28282

    PubMed  CAS  Google Scholar 

  • Carone BR, Fauquier L, Habib N et al (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084–1096

    PubMed  CAS  Google Scholar 

  • Carrell DT (2012) Epigenetics of the male gamete. Fertil Steril 97:267–274

    PubMed  CAS  Google Scholar 

  • Caserta D, Mantovani A, Marci R et al (2011) Environment and women’s reproductive health. Hum Reprod Update 17:418–433

    PubMed  CAS  Google Scholar 

  • Champagne FA (2008) Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 29:386–397

    PubMed  CAS  Google Scholar 

  • Chan D, Cushnie DW, Neaga OR et al (2010) Strain-specific defects in testicular development and sperm epigenetic patterns in 5,10-methylenetetrahydrofolate reductase-deficient mice. Endocrinology 151:3363–3373

    PubMed  CAS  Google Scholar 

  • Cheng TF, Choudhuri S, Muldoon-Jacobs K (2012) Epigenetic targets of some toxicologically relevant metals: a review of the literature. J Appl Toxicol 32:643–653

    PubMed  CAS  Google Scholar 

  • Clement TM, Bhandari RK, Sadler-Riggleman I et al (2011) Sry directly regulates the neurotrophin-3 promoter during male sex determination and testis development in rats. Biol Reprod 85:227–284

    Google Scholar 

  • Clinton M, Haines LC (2001) An overview of factors influencing sex determination and gonadal development in birds. EXS 97–115

    Google Scholar 

  • Cool J, Capel B (2009) Mixed signals: development of the testis. Semin Reprod Med 27:5–13

    PubMed  CAS  Google Scholar 

  • Cool J, Carmona FD, Szucsik J et al (2008) Peritubular myoid cells are not the migrating population required for testis cord formation in the XY gonad. Sex Dev 2:128–133

    PubMed  CAS  Google Scholar 

  • Crews D, Gillette R, Scarpino SV et al (2012) Epigenetic transgenerational inheritance of altered stress responses. Proc Natl Acad Sci U S A 109:9143–9148

    PubMed  CAS  Google Scholar 

  • Cupp AS, Uzumcu M, Skinner MK (2003) Chemotactic role of neurotropin 3 in the embryonic testis that facilitates male sex determination. Biol Reprod 68:2033–2037

    PubMed  CAS  Google Scholar 

  • Daneau I, Pilon N, Boyer A et al (2002) The porcine SRY promoter is transactivated within a male genital ridge environment. Genesis 33:170–180

    PubMed  CAS  Google Scholar 

  • de Assis S, Warri A, Cruz MI et al (2012) High-fat or ethinyl-oestradiol intake during pregnancy increases mammary cancer risk in several generations of offspring. Nat Commun 3:1053

    PubMed  Google Scholar 

  • DiNapoli L, Capel B (2008) SRY and the standoff in sex determination. Mol Endocrinol 22:1–9

    PubMed  CAS  Google Scholar 

  • Drews U (2000) Local mechanisms in sex specific morphogenesis. Cytogenet Cell Genet 91:72–80

    PubMed  CAS  Google Scholar 

  • Du J, Zhon X, Bernatavichute Y et al (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151:167–180

    PubMed  CAS  Google Scholar 

  • Dunn GA, Bale TL (2011) Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152:2228–2236

    PubMed  CAS  Google Scholar 

  • Durcova-Hills G, Hajkova P, Sullivan S et al (2006) Influence of sex chromosome constitution on the genomic imprinting of germ cells. Proc Natl Acad Sci U S A 103:11184–11188

    PubMed  CAS  Google Scholar 

  • Fawcett D (1975) The ultrastructure and functions of the Sertoli cell. In: Hamilton RGE (ed) Handbook of physiology. American Physiological Society, Washington, DC, pp 22–55

    Google Scholar 

  • Forouzanfar MH, Foreman KJ, Delossantos AM et al (2011) Breast and cervical cancer in 187 countries between 1980 and 2010: a systematic analysis. Lancet 378:1461–1484

    PubMed  Google Scholar 

  • Fowler PA, Bellingham M, Sinclair KD et al (2012) Impact of endocrine-disrupting compounds (EDCs) on female reproductive health. Mol Cell Endocrinol 355:231–239

    PubMed  CAS  Google Scholar 

  • Gao F, Maiti S, Alam N et al (2006) The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis. Proc Natl Acad Sci U S A 103:11987–11992

    PubMed  CAS  Google Scholar 

  • Giwercman A, Giwercman YL (2011) Environmental factors and testicular function. Best Pract Res Clin Endocrinol Metab 25:391–402

    PubMed  CAS  Google Scholar 

  • Gonzalez-Pardo H, Perez Alvarez M (2013) Epigenetics and its implications for psychology. Psicothema 25:3–12

    PubMed  Google Scholar 

  • Govin J, Escoffier E, Rousseaux S et al (2007) Pericentric heterochromatin reprogramming by new histone variants during mouse spermiogenesis. J Cell Biol 176:283–294

    PubMed  CAS  Google Scholar 

  • Grimaldi P, Pucci M, Di Siena S et al (2012) The faah gene is the first direct target of estrogen in the testis: role of histone demethylase LSD1. Cell Mol Life Sci 69:4177–4190

    PubMed  CAS  Google Scholar 

  • Guerrero-Bosagna and Skinner (2012) Environmental epigenetics and phytoestrogen/phytochemical exposures. [epub ahead of print]. doi:10.1016/j.jsbmb.2012.12.011

    Google Scholar 

  • Guerrero-Bosagna C, Settles M, Lucker B et al (2010) Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5:e13100

    PubMed  Google Scholar 

  • Guillette LJ Jr, Iguchi T (2012) Ecology. Life in a contaminated world. Science 337:1614–1615

    PubMed  Google Scholar 

  • Guo YL, Hsu PC, Hsu CC et al (2000) Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet 356:1240–1241

    PubMed  CAS  Google Scholar 

  • Guo YL, Lambert GH, Hsu CC et al (2004) Yucheng: health effects of prenatal exposure to polychlorinated biphenyls and dibenzofurans. Int Arch Occup Environ Health 77:153–158

    PubMed  CAS  Google Scholar 

  • Hammoud SS, Purwar J, Pflueger C et al (2010) Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil Steril 94:1728–1733

    PubMed  CAS  Google Scholar 

  • Hammoud SS, Nix DA, Hammoud AO et al (2011) 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

    PubMed  CAS  Google Scholar 

  • Heyn H, Ferreira HJ, Bassas L et al (2012) Epigenetic disruption of the PIWI pathway in human spermatogenic disorders. PLoS One 7:e47892

    PubMed  CAS  Google Scholar 

  • Hiramatsu R, Matoba S, Kanai-Azuma M et al (2009) A critical time window of SRY action in gonadal sex determination in mice. Development 136:129–138

    PubMed  CAS  Google Scholar 

  • Houshdaran S, Cortessis VK, Siegmund K et al (2007) Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS One 2:e1289

    PubMed  Google Scholar 

  • Ichiyanagi K, Li Y, Watanabe T et al (2011) Locus- and domain-dependent control of DNA methylation at mouse B1 retrotransposons during male germ cell development. Genome Res 21:2058–2066

    PubMed  CAS  Google Scholar 

  • Ikeda Y, Takeda Y, Shikayama T et al (2001) Comparative localization of Dax-1 and Ad4BP/SF-1 during development of the hypothalamic-pituitary-gonadal axis suggests their closely related and distinct functions. Dev Dyn 220:363–376

    PubMed  CAS  Google Scholar 

  • Inbar-Feigenberg M, Choufani S, Butcher DT, Roifman M, Weksberg R. (2013) Basic concepts of epigenetics. Fertil Steril 1;99(3):607–615

    Google Scholar 

  • Johnson LM, Bostick M, Zhang X et al (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17:379–384

    PubMed  CAS  Google Scholar 

  • Jost A, Magre S, Agelopoulou R (1981) Early stages of testicular differentiation in the rat. Hum Genet 58:59–63

    PubMed  CAS  Google Scholar 

  • Kanai Y, Hiramatsu R, Matoba S et al (2005) From SRY to SOX9: mammalian testis differentiation. J Biochem 138:13–19

    PubMed  CAS  Google Scholar 

  • Karl J, Capel B (1998) Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev Biol 203:323–333

    PubMed  CAS  Google Scholar 

  • Karmaus W, Ziyab AH, Everson T et al (2013) Epigenetic mechanisms and models in the origins of asthma. Curr Opin Allergy Clin Immunol 13:63–69

    PubMed  Google Scholar 

  • Khazamipour N, Noruzinia M, Fatehmanesh P et al (2009) MTHFR promoter hypermethylation in testicular biopsies of patients with non-obstructive azoospermia: the role of epigenetics in male infertility. Hum Reprod 24:2361–2364

    PubMed  CAS  Google Scholar 

  • Kidokoro T, Matoba S, Hiramatsu R et al (2005) Influence on spatiotemporal patterns of a male-specific Sox9 activation by ectopic Sry expression during early phases of testis differentiation in mice. Dev Biol 278:511–525

    PubMed  CAS  Google Scholar 

  • Kim Y, Capel B (2006) Balancing the bipotential gonad between alternative organ fates: a new perspective on an old problem. Dev Dyn 235:2292–2300

    PubMed  CAS  Google Scholar 

  • Kobayashi H, Sato A, Otsu E et al (2007) Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 16:2542–2551

    PubMed  CAS  Google Scholar 

  • Lees-Murdock DJ, Walsh CP (2008) DNA methylation reprogramming in the germ line. Epigenetics 3:5–13

    PubMed  Google Scholar 

  • Magre S, Jost A (1980) The initial phases of testicular organogenesis in the rat. An electron microscopy study. Arch Anat Microsc Morphol Exp 69:297–318

    PubMed  CAS  Google Scholar 

  • Main KM, Skakkebaek NE, Virtanen HE et al (2010) Genital anomalies in boys and the environment. Best Pract Res Clin Endocrinol Metab 24:279–289

    PubMed  Google Scholar 

  • Malki S, Nef S, Notarnicola C et al (2005) Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO J 24:1798–1809

    PubMed  CAS  Google Scholar 

  • Manikkam M, Guerrero-Bosagna C, Tracey R et al (2012a) Transgenerational actions of environmental compounds on reproductive disease and epigenetic biomarkers of ancestral exposures. PLoS One 7:e31901

    PubMed  CAS  Google Scholar 

  • Manikkam M, Tracey R, Guerrero-Bosagna C et al (2012b) Pesticide and insect repellent mixture (Permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations. Reprod Toxicol 34:708–719

    PubMed  CAS  Google Scholar 

  • Manikkam M, Tracey R, Guerrero-Bosagna C et al (2012c) Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS One 7:e46249

    PubMed  CAS  Google Scholar 

  • Manikkam M, Tracey R, Guerrero-Bosagna C et al (2013) Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations. PLoS One 8:e55387

    PubMed  CAS  Google Scholar 

  • Marques CJ, Carvalho F, Sousa M et al (2004) Genomic imprinting in disruptive spermatogenesis. Lancet 363:1700–1702

    PubMed  CAS  Google Scholar 

  • Marques CJ, Costa P, Vaz B et al (2008) Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 14:67–74

    PubMed  CAS  Google Scholar 

  • Marques CJ, Francisco T, Sousa S et al (2010) Methylation defects of imprinted genes in human testicular spermatozoa. Fertil Steril 94:585–594

    PubMed  CAS  Google Scholar 

  • Martinez-Arguelles DB, Culty M, Zirkin BR et al (2009) In utero exposure to di-(2-ethylhexyl) phthalate decreases mineralocorticoid receptor expression in the adult testis. Endocrinology 150:5575–5585

    PubMed  CAS  Google Scholar 

  • McClelland K, Bowles J, Koopman P (2012) Male sex determination: insights into molecular mechanisms. Asian J Androl 14:164–171

    PubMed  CAS  Google Scholar 

  • McLaren A (1991) Development of the mammalian gonad: the fate of the supporting cell lineage. Bioessays 13:151–156

    PubMed  CAS  Google Scholar 

  • McLaren A (2000) Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol 163:3–9

    PubMed  CAS  Google Scholar 

  • Merchant-Larios H, Moreno-Mendoza N, Buehr M (1993) The role of the mesonephros in cell differentiation and morphogenesis of the mouse fetal testis. Int J Dev Biol 37:407–415

    PubMed  CAS  Google Scholar 

  • Miyamoto Y, Taniguchi H, Hamel F et al (2008) A GATA4/WT1 cooperation regulates transcription of genes required for mammalian sex determination and differentiation. BMC Mol Biol 9:44

    PubMed  Google Scholar 

  • Moreno-Mendoza N, Harley V, Merchant-Larios H (2003) Cell aggregation precedes the onset of Sox9-expressing preSertoli cells in the genital ridge of mouse. Cytogenet Genome Res 101:219–223

    PubMed  CAS  Google Scholar 

  • Morgan CP, Bale TL (2011) Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 31:11748–11755

    PubMed  CAS  Google Scholar 

  • Nikolova G, Vilain E (2006) Mechanisms of disease: transcription factors in sex determination–relevance to human disorders of sex development. Nat Clin Pract Endocrinol Metab 2:231–238

    PubMed  CAS  Google Scholar 

  • North ML, Ellis AK (2011) The role of epigenetics in the developmental origins of allergic disease. Ann Allergy Asthma Immunol 10:355–361, quiz 362

    Google Scholar 

  • Ogino S, Lochhead P, Chan AT et al (2013) Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease. Mod Pathol 26:465–484

    PubMed  CAS  Google Scholar 

  • Ooi SK, Qiu C, Bernstein E et al (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448:714–717

    PubMed  CAS  Google Scholar 

  • Ostrer H (2000) Sexual differentiation. Semin Reprod Med 18:41–49

    PubMed  CAS  Google Scholar 

  • Ottolenghi C, Uda M, Crisponi L et al (2007) Determination and stability of sex. Bioessays 29:15–25

    PubMed  CAS  Google Scholar 

  • Paradowska AS, Miller D, Spiess AN et al (2012) Genome wide identification of promoter binding sites for H4K12ac in human sperm and its relevance for early embryonic development. Epigenetics 7:1057–1070

    PubMed  CAS  Google Scholar 

  • Park CJ, Nah WH, Lee JE et al (2012) Butyl paraben-induced changes in DNA methylation in rat epididymal spermatozoa. Andrologia 44(Suppl 1):187–193

    PubMed  CAS  Google Scholar 

  • Parker KL, Schimmer BP, Schedl A (2001) Genes essential for early events in gonadal development. EXS 91:11–24

    PubMed  CAS  Google Scholar 

  • Parkin DM (2004) International variation. Oncogene 23:6329–6340

    PubMed  CAS  Google Scholar 

  • Parma P, Radi O (2012) Molecular mechanisms of sexual development. Sex Dev 6:7–17

    PubMed  CAS  Google Scholar 

  • Pimentel D, Cooperstein S, Randell H et al (2007) Ecology of increasing diseases: population growth and environmental degradation. Hum Ecol 35:653–668

    Google Scholar 

  • Poplinski A, Tuttelmann F, Kanber D et al (2010) Idiopathic male infertility is strongly associated with aberrant methylation of MEST and IGF2/H19 ICR1. Int J Androl 33:642–649

    PubMed  CAS  Google Scholar 

  • Rajender S, Avery K, Agarwal A (2011) Epigenetics, spermatogenesis and male infertility. Mutat Res 727:62–71

    PubMed  CAS  Google Scholar 

  • Raymond CS, Murphy MW, O’Sullivan MG et al (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14:2587–2595

    PubMed  CAS  Google Scholar 

  • Reddy PM, Reddy PR (1990) Differential regulation of DNA methylation in rat testis and its regulation by gonadotropic hormones. J Steroid Biochem 35:173–178

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ricci G, Catizone A, Innocenzi A et al (1999) Hepatocyte growth factor (HGF) receptor expression and role of HGF during embryonic mouse testis development. Dev Biol 216:340–347

    PubMed  CAS  Google Scholar 

  • Salian S, Doshi T, Vanage G (2009) Perinatal exposure of rats to Bisphenol A affects the fertility of male offspring. Life Sci 85:742–752

    PubMed  CAS  Google Scholar 

  • Schug TT, Janesick A, Blumberg B et al (2011) Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol 127:204–215

    PubMed  CAS  Google Scholar 

  • Sekido R, Lovell-Badge R (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930–934

    PubMed  CAS  Google Scholar 

  • Sekido R, Bar I, Narvaez V, Penny G et al (2004) SOX9 is up-regulated by the transient expression of SRY specifically in Sertoli cell precursors. Dev Biol 274:271–279

    PubMed  CAS  Google Scholar 

  • Sertoli E (1865) On the existence of special branched cells in hte seminiferous tubule of the human testes. Morgangni 7:31–39

    Google Scholar 

  • Setchell BP, Waites GMH (1975) In: Hamilton D, Greep RO (eds) Handbook of physiology. American Physiological Society, Washington, DC, pp 143–172

    Google Scholar 

  • Shanker S, Hu Z, Wilkinson MF (2008) Epigenetic regulation and downstream targets of the Rhox5 homeobox gene. Int J Androl 31:462–470

    PubMed  CAS  Google Scholar 

  • Sharpe RM (2010) Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365:1697–1712

    PubMed  CAS  Google Scholar 

  • Shukla KK, Mahdi AA, Rajender S (2012) Apoptosis, spermatogenesis and male infertility. Front Biosci Elite Ed 4:746–754

    PubMed  Google Scholar 

  • Singh KP, DuMond JW Jr (2007) Genetic and epigenetic changes induced by chronic low dose exposure to arsenic of mouse testicular Leydig cells. Int J Oncol 30:253–260

    PubMed  CAS  Google Scholar 

  • Singh KP, Kumari R, Pevey C et al (2009) Long duration exposure to cadmium leads to increased cell survival, decreased DNA repair capacity, and genomic instability in mouse testicular Leydig cells. Cancer Lett 279:84–92

    PubMed  CAS  Google Scholar 

  • Skakkebaek NE, Rajpert-De Meyts E, Main KM (2001) Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972–978

    PubMed  CAS  Google Scholar 

  • Skakkebaek NE, Rajpert-De Meyts E et al (2007) Testicular cancer trends as ‘whistle blowers’ of testicular developmental problems in populations. Int J Androl 30:198–204, discussion 204–195

    PubMed  CAS  Google Scholar 

  • Skinner MK (1991) Cell-cell interactions in the testis. Endocr Rev 12:45–77

    PubMed  CAS  Google Scholar 

  • Skinner MK (2011) Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 6:838–842

    PubMed  CAS  Google Scholar 

  • Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21:214–222

    PubMed  CAS  Google Scholar 

  • Sonnack V, Failing K, Bergmann M et al (2002) Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 34:384–390

    PubMed  CAS  Google Scholar 

  • Steilmann C, Cavalcanti MC, Bartkuhn M et al (2010) 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 140:435–443

    PubMed  CAS  Google Scholar 

  • Stoccoro A, Karlsson HL, Coppede F et al (2012) Epigenetic effects of nano-sized materials. Toxicology. Dec 10. [Epub ahead of print]. doi:10.1016/j.tox.2012.12.002

    Google Scholar 

  • Stouder C, Somm E, Paoloni-Giacobino A (2011) Prenatal exposure to ethanol: a specific effect on the H19 gene in sperm. Reprod Toxicol 31:507–512

    PubMed  CAS  Google Scholar 

  • Sun C, Burgner DP, Ponsonby AL et al (2013) Effects of early-life environment and epigenetics on cardiovascular disease risk in children: highlighting the role of twin studies. Pediatr Res 73(4 Pt 2):523–530

    Google Scholar 

  • Takasaki N, Rankin T, Dean J (2001) Normal gonadal development in mice lacking GPBOX, a homeobox protein expressed in germ cells at the onset of sexual dimorphism. Mol Cell Biol 21:8197–8202

    PubMed  CAS  Google Scholar 

  • Thrupp LA (1991) Sterilization of workers from pesticide exposure: the causes and consequences of DBCP-induced damage in Costa Rica and beyond. Int J Health Serv 21:731–757

    PubMed  CAS  Google Scholar 

  • Tracey R, Manikkam M, Guerrero-Bosagna C, Skinner MK (2013) Hydrocarbons (jet fuel JP-8) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. Reprod Toxicol 36:104–116

    Google Scholar 

  • Tsugane S, Sasazuki S (2007) Diet and the risk of gastric cancer: review of epidemiological evidence. Gastric Cancer 10:75–83

    PubMed  Google Scholar 

  • Vaillant S, Magre S, Dorizzi M et al (2001) Expression of AMH, SF1, and SOX9 in gonads of genetic female chickens during sex reversal induced by an aromatase inhibitor. Dev Dyn 222: 228–237

    PubMed  CAS  Google Scholar 

  • Vavouri T, Lehner B (2011) Chromatin organization in sperm may be the major functional consequence of base composition variation in the human genome. PLoS Genet 7:e1002036

    PubMed  CAS  Google Scholar 

  • Waites GM, Gladwell RT (1982) Physiological significance of fluid secretion in the testis and blood-testis barrier. Physiol Rev 62:624–671

    PubMed  CAS  Google Scholar 

  • Wallace DC (2010) Bioenergetics and the epigenome: interface between the environment and genes in common diseases. Dev Disabil Res Rev 16:114–119

    PubMed  Google Scholar 

  • Wallis MC, Waters PD, Graves JA (2008) Sex determination in mammals–before and after the evolution of SRY. Cell Mol Life Sci 65:3182–3195

    PubMed  CAS  Google Scholar 

  • Whorton D, Milby TH, Krauss RM et al (1979) Testicular function in DBCP exposed pesticide workers. J Occup Med 21:161–166

    PubMed  CAS  Google Scholar 

  • Wilhelm D, Martinson F, Bradford S et al (2005) Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev Biol 287:111–124

    PubMed  CAS  Google Scholar 

  • Wilhelm D, Hiramatsu R, Mizusaki H et al (2007) SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J Biol Chem 282:10553–10560

    PubMed  CAS  Google Scholar 

  • Wu W, Shen O, Qin Y et al (2010) Idiopathic male infertility is strongly associated with aberrant promoter methylation of methylenetetrahydrofolate reductase (MTHFR). PLoS One 5:e13884

    PubMed  Google Scholar 

  • Xu Z, Gao X, He Y et al (2012) Synergistic effect of SRY and its direct target, WDR5, on Sox9 expression. PLoS One 7:e34327

    PubMed  CAS  Google Scholar 

  • Yuen RK, Chen B, Blair JD et al (2013) Hypoxia alters the epigenetic profile in cultured human placental trophoblasts. Epigenetics 8

    Google Scholar 

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Correspondence to Michael K. Skinner .

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Guerrero-Bosagna, C., Skinner, M.K. (2014). Environmental Epigenetics and Effects on Male Fertility. In: Baldi, E., Muratori, M. (eds) Genetic Damage in Human Spermatozoa. Advances in Experimental Medicine and Biology, vol 791. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7783-9_5

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