Integrative rodent models for assessing male reproductive toxicity of environmental endocrine active substances

Asian Journal of Andrology

Volumn 16, Issue 1, 2014, Pages 60-70

  Auger, Jacques ^a   Eustache, Florence ^b,c   Rouiller Fabre, Virginie ^d   Canivenc Lavier, Marie Chantal ^e   Livera, Gabriel ^d  

^a HÔTEL DIEU   (France)

^b INSTITUT COCHIN   (France)

^c HÔPITAL JEAN VERDIER   (France)

^d Universite Paris Sud   (France)

^e CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

Author keywords

endocrine active substance; endocrine disruptor; exposure; gonad in culture; low dose; mixture; mouse; rat; rodent; strain

Indexed keywords

ENDOCRINE ACTIVE SUBSTANCE; ENDOCRINE DISRUPTOR; ENVIRONMENTAL CHEMICAL; UNCLASSIFIED DRUG;

ANIMAL CELL CULTURE; ENVIRONMENTAL EXPOSURE; MALE REPRODUCTIVE TOXICITY; NONHUMAN; REPRODUCTION; REPRODUCTIVE TOXICITY; REVIEW; RODENT MODEL; SPECIES DIFFERENCE; STRAIN DIFFERENCE; TESTIS;

ANIMALS; ENDOCRINE DISRUPTORS; ENVIRONMENTAL EXPOSURE; FETUS; HUMANS; MALE; MODELS, ANIMAL; ORGAN CULTURE TECHNIQUES; OXAZOLES; REPRODUCTION; SPERMATOZOA; TESTIS;

EID: 84891941522     PISSN: 1008682X     EISSN: 17457262     Source Type: Journal    
DOI: 10.4103/1008-682X.122366     Document Type: Review

References (56)

1. WHO/UNEP (World Health Organization/United Nations Environment Programme), 2013. State of the Science of Endocrine Disrupting Chemicals-2012. p. 296 Available from: http://www.who.int/mediacentre/news/releases/2013/ hormone- disrupting-20130219/en/index.html.
2. Federal Reserve Board, G.17-Industrial Production and Capacity Utilization, Industrial Production for Chemicals (NAICS=325), The Federal Reserve Board Data Download Program, 2008. Available from: http://www.federal reserve. gov/datadownload/Download.aspx? rel=G17 and series=4374e4378caec43 76beeaa4874d28776fa28768c287711e and filetype=spreadsheetml and label=include and layout=seriescolumn and from=28701/28701/21919 and to=28712/28731/22009.e and filetype.
3. EFSA Scientific Committee; Scientific Opinion on the hazard assessment of endocrine disruptors: scientific criteria for identification of endocrine disruptors and appropriateness of existing test methods for assessing effects mediated by these substances on human health and the environment. EFSA J 2013; 11: 3132. [84 pp.]. Available from: www.efsa.europa.eu/efsajournal.
4. Kortenkamp A, Martin O, Faust M, Evans R, McKinlay R, et al. 2011 State of the Art Assessment of Endocrine Disrupters. Final Report. [Online]. Available from: http://ec.europa.eu/environment/endocrine/documents/4- SOTA%20EDC%20Final%20 Report%20 V3%206%20Feb%2012.pdf.
5. Calafat AM, Ye X, Wong LY, Bishop AM, Needham LL. Urinary concentrations of four parabens in the U.S. population: NHANES 2005-2006. Environ Health Perspect 2010; 118: 679-85.
6. Calafat AM. The U.S. National Health and Nutrition Examination Survey and human exposure to environmental chemicals. Int J Hyg Environ Health 2012; 215: 99-101.
7. Chevrier C, Petit C, Philippat C, Mortamais M, Slama R, et al. Maternal urinary phthalates and phenols and male genital anomalies. Epidemiology 2012; 23: 353-6.
8. Hauser R, Meeker JD, Singh NP, Silva MJ, Ryan L, et al. DNA damage in human sperm is related to urinary levels of phthalate monoester and oxidative metabolites. Hum Reprod 2007; 22: 688-95.
9. Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, et al. Study for Future Families Research Team. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 2005; 113: 1056-61.
10. Vandenbergh JG. Animal models and studies of in utero endocrine disruptor effects. ILAR J 2004; 45:438-42.
11. Woodruff TJ. Bridging epidemiology and model organisms to increase understanding of endocrine disrupting chemicals and human health effects. J Steroid Biochem Mol Biol 2011; 127: 108-17.
12. Johnson KJ, Heger NE, Boekelheide K. Of mice and men (and rats): phthalate-induced fetal testis endocrine disruption is species-dependent. Toxicol Sci 2012; 129: 235-48
13. WHO (World Health Organization), 2012. Endocrine disrupters and child health: possible developmental early effects of endocrine disrupters on child health. 84 pp. Available from: http://www.who.int/ceh/publications/endocrine- disrupters-child/en/index.html.
14. Saghir SA, Khan SA, McCoy AT. Ontogeny of mammalian metabolizing enzymes in humans and animals used in toxicological studies. Crit Rev Toxicol 2012; 42:323-57.
15. Hauser H, Gandelman R. Contiguity to males in utero affects avoidance responding in adult female mice. Science 1983; 220: 437-8.
16. Morley-Fletcher S, Palanza P, Parolaro D, Viganò D, Laviola G. Intrauterine position has long-term influence on brain mu-opioid receptor density and behaviour in mice. Psychoneuroendocrinology 2003; 28: 386-400.
17. Auger J. Assessing human sperm morphology: top models, underdogs or biometrics? Asian J Androl 2010; 12: 36-46.
18. Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J Urol 2003; 170: 5-11.
19. Howdeshell KL, Rider CV, Wilson VS, Gray LE Jr. Mechanisms of action of phthalate esters, individually and in combination, to induce abnormal reproductive development in male laboratory rats. Environ Res 2008; 108: 168-76.
20. Drake AJ, van den Driesche S, Scott HM, Hutchison GR, Seckl JR, et al. Glucocorticoids amplify dibutyl phthalate-induced disruption of testosterone production and male reproductive development. Endocrinology 2009; 150: 5055-64.
21. Mylchreest E, Sar M, Wallace DG, Foster PM. Fetal testosterone insufficiency and abnormal proliferation of Leydig cells and gonocytes in rats exposed to di (n-butyl) phthalate. Reprod Toxicol 2002; 16: 19-28.
22. Lehraiki A, Racine C, Krust A, Habert R, Levacher C. Phthalates impair germ cell number in the mouse fetal testis by an androgen-and estrogen-independent mechanism. Toxicol Sci 2009; 111: 372-82.
23. Marty MS, Allen B, Chapin RE, Cooper R, Daston GP, et al. Inter-laboratory control data for reproductive endpoints required in the OPPTS 870.3800/OECD 416 reproduction and fertility test. Birth Defects Res B Dev Reprod Toxicol 2009; 86: 470-89.
24. Chapin RE, Filler RS, Gulati D, Heindel JJ, Katz D F, et al. Methods for assessing rat sperm motility. Reprod Toxicol 1992; 6: 267-73.
25. López-Casas P P, Mizrak SC, López-Fernández LA, Paz M, de Rooij DG, et al. The effects of different endocrine disruptors defining compound-specific alterations of gene expression profiles in the developing testis. Reprod Toxicol 2012; 33: 106-15.
26. Anway MD, Skinner MK. Transgenerational effects of the endocrine disruptor vinclozolin on the prostate transcriptome and adult onset disease. Prostate 2008; 68: 517-29.
27. Phillips K P, Foster WG. Key developments in endocrine disrupter research and human health. J Toxicol Environ Health B Crit Rev 2008; 11: 322-44.
28. Anway MD, Memon MA, Uzumcu M, Skinner MK. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J Androl 2006; 27: 868-79.
29. 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: 373-9.
30. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 2012; 33: 378-455.
31. OECD. 2012 Guidance document on standardised test guidelines for evaluating chemicals for endocrine disruption. Available from: http://search.oecd.org/officialdocuments/displaydocumentpdf/?cote=env/jm/mono (2012) 22 and doclanguage=en.
32. Giwercman A, Rylander L, Hagmar L, Giwercman YL. Ethnic differences in occurrence of TDS-genetics and/or environment? Int J Androl 2006; 29: 291-7.
33. Eustache F, Mondon F, Canivenc-Lavier MC, Lesaffre C, Fulla Y, et al. Chronic dietary exposure to a low-dose mixture of genistein and vinclozolin modifies the reproductive axis, testis transcriptome, and fertility. Environ Health Perspect 2009; 117: 1272-9.
34. Lehraiki A, Messiaen S, Berges R, Canivenc-Lavier MC, Auger J, et al. Antagonistic effects of gestational dietary exposure to low-dose vinclozolin and genistein on rat fetal germ cell development. Reprod Toxicol 2011; 31: 424-30.
35. Kouidhi W, Desmetz C, Nahdi A, Bergès R, Cravedi J P, et al. In utero and lactational exposure to low-dose genistein-vinclozolin mixture affects the development and growth factor mRNA expression of the submandibular salivary gland in immature female rats. Toxicol Pathol 2012; 40: 593-604.
36. Kouidhi W, Bergès R, Tiffon C, Desmetz C, El May M, et al. Perinatal xenohormone exposure impacts sweet preference and submandibular development in male rats. Oral Dis 2013.
37. El Sheikh Saad H, Meduri G, Phrakonkham P, Bergès R, Vacher S, et al. Abnormal peripubertal development of the rat mammary gland following exposure in utero and during lactation to a mixture of genistein and the food contaminant vinclozolin. Reprod Toxicol 2011; 32: 15-25.
38. Jedeon K, De la Dure-Molla M, Brookes SJ, Loiodice S, Marciano C, et al. Enamel defects reflect perinatal exposure to bisphenol A. Am J Pathol 2013; 183: 108-18.
39. Auger J, Le Denmat D, Berges R, Doridot L, Salmon B, et al. Environmental levels of oestrogenic and antiandrogenic compounds feminize digit ratios in male rats and their unexposed male progeny. Proc Biol Sci 2013; 280: 20131532.
40. Habert R, Devif I, Gangnerau MN, Lecerf L. Ontogenesis of the in vitro response of rat testis to gonadotropin-releasing hormone. Mol Cell Endocrinol 1991; 82: 199-206.
41. Livera G, Delbes G, Pairault C, Rouiller-Fabre V, Habert R. Organotypic culture, a powerful model for studying rat and mouse fetal testis development. Cell Tissue Res 2006; 324: 507-21.
42. Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature 2011; 471: 504-7.
43. Lambrot R, Muczynski V, Lécureuil C, Angenard G, Coffigny H, et al. Phthalates impair germ cell development in the human fetal testis in vitro without change in testosterone production. Environ Health Perspect 2009; 117: 32-7.
44. Muczynski V, Cravedi J P, Lehraiki A, Levacher C, Moison D, et al. Effect of mono-(2-ethylhexyl) phthalate on human and mouse fetal testis: in vitro and in vivo approaches. Toxicol Appl Pharmacol 2012; 261: 97-104.
45. Delbès G, Levacher C, Duquenne C, Racine C, Pakarinen P, et al. Endogenous estrogens inhibit mouse fetal Leydig cell development via estrogen receptor alpha. Endocrinology 2005; 146: 2454-61.
46. N'Tumba-Byn T, Moison D, Lacroix M, Lecureuil C, Lesage L, et al. Differential effects of bisphenol A and diethylstilbestrol on human, rat and mouse fetal leydig cell function. PLoS One 2012; 7: e51579.
47. Thigpen JE, Setchell KD, Padilla-Banks E, Haseman JK, Saunders HE, et al. Variations in phytoestrogen content between different mill dates of the same diet produces significant differences in the time of vaginal opening in CD-1 mice and F344 rats but not in CD Sprague-Dawley rats. Environ Health Perspect 2007; 115: 1717-26.
48. Hellwig J, van Ravenzwaay B, Mayer M, Gembardt C. Pre-and postnatal oral toxicity of vinclozolin in Wistar and Long-Evans rats. Regul Toxicol Pharmacol 2000; 32: 42-50.
49. Saghir SA, Khan SA, McCoy AT. Ontogeny of mammalian metabolizing enzymes in humans and animals used in toxicological studies. Crit Rev Toxicol 2012; 42: 323-57.
50. Geis RB, Diel P, Degen GH, Vollmer G. Effects of genistein on the expression of hepatic genes in two rat strains (Sprague-Dawley and Wistar). Toxicol Lett 2005; 157: 21-9.
51. Wilson VS, Howdeshell KL, Lambright CS, Furr J, Earl Gray L Jr. Differential expression of the phthalate syndrome in male Sprague-Dawley and Wistar rats after in utero DEHP exposure. Toxicol Lett 2007; 170: 177-84.
52. vom Saal FS, Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect 2005; 113: 926-33.
53. Mitchell RT, Childs AJ, Anderson RA, van den Driesche S, Saunders PT, et al. Do phthalates affect steroidogenesis by the human fetal testis? Exposure of human fetal testis xenografts to di-n-butyl phthalate. J Clin Endocrinol Metab 2012; 97: E341-8.
54. Heger NE, Hall SJ, Sandrof MA, McDonnell EV, Hensley JB, et al. Human fetal testis xenografts are resistant to phthalate-induced endocrine disruption. Environ Health Perspect 2012; 120: 1137-43.
55. Mitchell RT, Sharpe RM, Anderson RA, McKinnell C, Macpherson S, et al. Diethylstilboestrol exposure does not reduce testosterone production in human fetal testis xenografts. PLoS One 2013; 8: e61726.
56. Klimisch HJ, Andreae M, Tillmann U. A systematic approach for evaluating the quality of experimental toxicological and ecotoxicological data. Regul Toxicol Pharmacol 1997; 25: 1-5.