Vinclozolin-No transgenerational inheritance of anti-androgenic effects after maternal exposure during organogenesis via the intraperitoneal route

Reproductive Toxicology

Volumn 37, Issue , 2013, Pages 6-14

  Schneider, Steffen ^a   Marxfeld, Heike ^a   Gröters, Sibylle ^a   Buesen, Roland ^a   van Ravenzwaay, Bennard ^a  

^a BASF SE   (Germany)

Author keywords

Anti androgen; Fertility; Rat; Reproduction; Spermatogenesis; Transgenerational inheritance; Vinclozolin

Indexed keywords

VINCLOZOLIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; GERM CELL; GESTATION PERIOD; HYPOSPADIAS; INHERITANCE; MALE; NONHUMAN; ORGANOGENESIS; PROGENY; RAT; REPRODUCTIVE TOXICITY; SEMEN ANALYSIS; SEXUAL DYSFUNCTION; SEXUAL MATURITY; SPERMATOGENESIS; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TOXICITY TESTING; TRANSGENERATIONAL INHERITANCE;

ANDROGEN ANTAGONISTS; ANIMALS; FEMALE; GENITALIA, MALE; HYPOSPADIAS; MALE; MATERNAL-FETAL EXCHANGE; ORGANOGENESIS; OXAZOLES; PREGNANCY; RATS; RATS, WISTAR; REPRODUCTION; SEXUAL MATURATION; SPERM COUNT; SPERM MOTILITY;

EID: 84873528277     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.12.003     Document Type: Article

References (56)

1. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308(June (5727)):1466-1469. (+ Science Supporting Online Material, http://www.sciencemag.org/cgi/data/308/5727/1466/DC1/1, dated 31.05.05).
2. WHO-JMPR (1995). Vinclozolin: 375-404.
3. Kelce W.R., Monosson E., Gamcsik M.P., Laws S.C., Gray L.E. Environmental hormone disruptors: evidence that Vinclozolin developmental toxicity is mediated by anti-androgenic metabolites. Toxicology and Applied Pharmacology 1994, 126:276-285.
4. Wong C., Kelce W.R., Sar M., Wilson E.M. Androgen receptor antagonist versus agonist activities of the fungicide Vinclozolin relative to hydroxyflutamide. Journal of Biological Chemistry 1995, 270:1998-2003.
5. Molina-Molina J.M., Hillenweck A., Jouanin I., Zalko D., Cravedi J.P., Fernández M.F., et al. Steroid receptor profiling of Vinclozolin and its primary metabolites. Toxicology and Applied Pharmacology 2006, 216:44-54.
6. Kelce W.R., Lambright C., Gray L.E., Roberts K. Vinclozolin and pp'-DDE alter androgen-dependent gene expression: in vivo confirmation of an androgen receptor mediated mechanism. Toxicology and Applied Pharmacology 1997, 142:192-200.
7. van Ravenzwaay B. Discussion of prenatal and reproductive toxicity of Reg. No. 83-258 (Vinclozolin). Data submission to U.S. EPA from BASF Corporation, MRID 425813-02; 1992.
8. Matsuura I., Saitoh T., Ashina M., Wako Y., Iwata H., Toyota N., et al. Evaluation of a two-generation reproduction toxicity study adding endpoints to detect endocrine disrupting activity using Vinclozolin. Journal of Toxicological Sciences 2005, 30(Spec. issue):163-188.
9. Ostby J.S., Gray L.E., Kelce W.R., Wolf C.J., Huey O.P. Sexual differentiation in male rats exposed to low doses of the antiandrogen Vinclozolin. Biology of Reproduction 1997, 56(Suppl. 1):99.
10. Hellwig J., van Ravenzwaay B., Mayer M., Gembardt C. Pre- and postnatal oral toxicity of Vinclozolin in Wistar and Long-Evans rats. Regulatory Toxicology and Pharmacology 2000, 32(1):42-50.
11. Gray L.E., Ostby J.S., Kelce W.R. Developmental effects of an environmental antiandrogen: the fungicide Vinclozolin alters sex differentiation of the male rats. Toxicology and Applied Pharmacology 1994, 129:46-52.
12. Wolf C.J., LeBlanc G., Ostby J.S., Gray L.E. Characterization of the period of sensitivity of fetal male sexual development to Vinclozolin. Toxicological Sciences 2000, 55:152-161.
13. Schneider S., Kaufmann W., Buesen R.V., Ravenzwaay B. Vinclozolin-the lack of a transgenerational effect after oral maternal exposure during organogenesis. Reproductive Toxicology 2008, 25:352-360.
14. Buckley J., Willingham E., Agras K., Baskin L.S. Embryonic exposure to the fungicide vinclozolin causes virilization of females and alteration of progesterone receptor expression in vivo: an experimental study in mice. Environmental Health 2006, 5:4.
15. Elzeinova F., Novakova V., Buckiova D., Kubatova A., Peknicova J. Effect of low dose of vinclozolin on reproductive tract development and sperm parameters in CD1 outbred mice. Reproductive Toxicology 2008, 26(3-4):231-238.
16. 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. Reproductive Toxicology 2004, 18:765-774.
17. Anway M.D., Memon M.A., Uzumcu M., Skinner M.K. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. Journal of Andrology 2006, 27:868-879.
18. Anway M.D., Rekow S.S., Skinner M.K. Comparative anti-androgenic actions of vinclozolin and flutamide on transgenerational adult onset disease and spermatogenesis. Reproductive Toxicology 2008, 26(2):100-106.
19. Anway M.D., Leathers C., Skinner M.K. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 2006, 147:5515-5523.
20. 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(5):713-721.
21. Anway M.D., Rekow S.S., Skinner M.K. Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics 2008, 91:30-40.
22. Anway M.D., Skinner M.K. Transgenerational effects of the endocrine disruptor vinclozolin on the prostate transcriptome and adult onset disease. Prostate 2008, 68:517-529.
23. Cowin P.A., Foster P., Pedersen J., Hedwards S., McPherson S.J., Risbridger G.A. Early-onset endocrine disruptor-induced prostatitis in the rat. Environmental Health Perspectives 2008, 116(7):923-929.
24. Cowin P.A., Gold E., Aleksova J., O'Bryan M.K., Foster P., Scott H.S., et al. Vinclozolin exposure in utero induces postpubertal prostatitis and reduces sperm production via a reversible hormone-regulated mechanism. Endocrinology 2010, 151(2):783-792.
25. Guerrero-Bosagna C., Settles M., Lucker B., Skinner M.K. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 2010, 5(9). [Art. No. e13100].
26. Clement T.M., Savenkova M., Settles M., Anway M.D., Skinner M.K. Alterations in the developing testis transcriptome following embryonic vinclozolin exposure. Reproductive Toxicology 2010, 30(3):353-364.
27. Inawaka K., Kawabe M., Takahashi S., Doi Y., Tomigahara Y., Tarui H., et al. Maternal exposure to antiandrogenic compounds, vinclozolin, flutamide and procimidone, has no effects on spermatogenesis and DNA methylation in male rats of subsequent generations. Toxicology and Applied Pharmacology 2009, 237:178-187.
28. Gray L., Furr J. Vinclozolin treatment induces reproductive malformations and infertility in male rats when administered during sexual but not gonadal differentiation; however, the effects are not transmitted to the subsequent generations. Biology of Reproduction 2008, 227-228((735) Sp. iss.).
29. Stouder C., Paolo-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.
30. Wadas B.C., Hartshorn C.A., Aurand E.R., Palmer J.S., Roselli C.E., Noel M.L., et al. Prenatal exposure to vinclozolin disrupts selective aspects of the gonadotrophin-releasing hormone neuronal system of the rabbit. Journal of Neuroendocrinology 2010, 22(6):518-526.
31. Vandegehuchte M.B., Lemiere F., Vanhaecke Lynn, Vanden Berghe W., Janssen C.R. Direct and transgenerational impact on Daphnia magna of chemicals with a known effect on DNA methylation. Biochemistry and Physiology Part C Toxicology & Pharmacology 2010, 151(3):278-285.
32. Martinovic-Weigelt D., Wang R.L., Villeneuve D.L., Bencic D.C., Lazorchak J., Ankley G.T. Gene expression profiling of the androgen receptor antagonists flutamide and vinclozolin in zebrafish (Danio rerio) gonads. Aquatic Toxicology (Amsterdam) 2011, 101(2):447-458.
33. OECD. Guideline for Testing of Chemicals, No. 416, Two-Generation Reproduction Toxicity Study, adopted 22 January 2001. Paris: Organisation for Economic Cooperation and Development; 2001.
34. OECD. Principles of Good Laboratory Practice. Paris: Organisation for Economic Cooperation and Development; 1981.
35. German Chemicals Act. Chemikaliengesetz; Bundesgesetzblatt Teil I, 22 March 1990 and 29 July 1994, Germany; 1994.
36. Hartl DL. Genetic management of outbred laboratory rodent populations. Charles River reference paper; 2001.
37. White WJ, Charn SL. The development and maintenance of the Crl:CD®(SD)IGS Rat Breeding System. Charles River reference paper; 1998.
38. Slott V.L., Suarez J.D., Perreault S.D. Rat sperm motility analysis: methodologic considerations. Reproductive Toxicology 1991, 5:449-458.
39. Feuston M.H., Bodnar K.R., Kerstetter S.L., Grink C.P., Belcak M.J., Singer E.J. Reproductive toxicity of 2-methoxyethanol applied dermally to occluded and nonoccluded sites in male rats. Toxicology and Applied Pharmacology 1989, 100(1):145-161.
40. Salewski E. Färbemethode zum makroskopischen Nachweis von Implantationsstellen am Uterus der Ratte. Naunyn-Schmiedebergs Archiv für Pharmakologie und experimentelle Pathologie 1964, 247:367.
41. Dunnett C.W. A multiple comparison procedure for comparing several treatments with a control. Journal of the American Statistical Association 1955, 50:1096-1121.
42. Dunnett C.W. New tables for multiple comparisons with a control. Biometrics 1964, 20:482-491.
43. Hettmansperger T.P. Statistical inference based on ranks 1984, John Wiley & Sons, New York, p. 132-142.
44. Nijenhuis A., Wilf H.S. Combinatorial algorithms 1978, Academic Press, New York, pp. 26-38.
45. Siegel S. Non-parametric statistics for the behavioral sciences 1956, McGraw-Hill, New York.
46. Holm S. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 1979, 6:65-70.
47. Majdic G., Millar M.R., Saunders P.T. Immunolocalisation of androgen receptor to interstitial cells in fetal rat testes and to mesenchymal and epithelial cells of associated ducts. Journal of Endocrinology 1995, 147:285-293.
48. You L., Casanova M., Archibeque-Engle S., Sar M., Fan L., Heck H. Androgen receptor expression in the testes and epididymides of prenatal and postnatal Sprague-Dawley rats. Endocrine 1998, 9:253-261.
49. Sierra-Santoyo A., Castaneda-Hernandez G., Harrison R.A., Barton H.A., Hughes M.F. Pharmacokinetics and dosimetry of the antiandrogen vinclozolin after oral administration in the rat. Toxicological Sciences 2008, 106(1):55-63.
50. Sinha Hikim A.P., Swedloff R.S. Hormonal and genetic control of germ cell apoptosis in the testis. Reviews of Reproduction 1999, 4:38-47.
51. LeBaron M.J., Rasoulpour R.J., Klapacz J., Ellis-Hutchings R.G., Hollnagel H.M., Gollapudi B.B. Epigenetics and chemical safety assessment. Mutation Research-Reviews in Mutation Research 2010, 705(2):83-95.
52. Skinner M.K., Manikkam M., Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends in Endocrinology and Metabolism 2010, 21((4) Sp. iss.):214-222.
53. Skinner M.K. Role of epigenetics in developmental biology and transgenerational inheritance. Birth Defects Research Part C: Embryo Today-Reviews 2011, 93(1):51-55.
54. 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, 3:11. [Article No. e3745].
55. Rasoulpour R.J., LeBaron M.J., Ellis-Hutchings R.G., Klapacz J., Gollapudi B.B. Epigenetic screening in product safety assessment: are we there yet?. Toxicology Mechanisms and Methods 2011, 21((4) sp. iss.):298-311.
56. Goodman J.I., Augustine K.A., Cunningham M.L., Dixon D., Dragan Y.P., Falls J.G., et al. What do we need to know prior to thinking about incorporating an epigenetic evaluation into safety assessments. Toxicological Sciences 2010, 116(2):375-381.