Prenatal exposure to pesticides disrupts testicular histoarchitecture and alters testosterone levels in male Caiman latirostris

General and Comparative Endocrinology

Volumn 162, Issue 3, 2009, Pages 286-292

  Rey, Florencia ^a   González, Marianela ^a   Zayas, Marcelo A ^a   Stoker, Cora ^a   Durando, Milena ^a   Luque, Enrique H ^a   Muñoz de Toro, Mónica ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Atrazine; Caiman latirostris; Endocrine disruptors; Endosulfan; Testes

Indexed keywords

ATRAZINE; DESMIN; ENDOSULFAN; PESTICIDE; TESTOSTERONE;

AMPHIBIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HATCHLING; HISTOLOGY; INCUBATION TIME; MALE; MORPHOMETRICS; NONHUMAN; OOCYTE; PRENATAL EXPOSURE; PRIORITY JOURNAL; REPRODUCTION; SEMINIFEROUS TUBULE; SEXUAL MATURATION; SIGNAL TRANSDUCTION; TESTIS;

EID: 67349159371     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2009.03.032     Document Type: Article

References (49)

1. American Society of Icthyologists and Herpetologists (ASIH), 2004. Revised by the Herpetological Animal Care an Use Committee, second ed.
2. Anthony C.T., and Skinner M.K. Cytochemical and biochemical characterization of testicular peritubular myoid cells. Biol. Reprod. 40 (1989) 811-823
3. Aravindakshan J., Paquet V., Gregory M., Dufresne J., Fournier M., Marcogliese D.J., and Cyr D.G. Consequences of xenoestrogen exposure on male reproductive function in spottail shiners (Notropis hudsonius). Toxicol. Sci. 78 (2004) 156-165
4. Beldomenico P.M., Rey F., Prado W.S., Villarreal J.C., Muñoz-de-Toro M., and Luque E.H. In ovum exposure to pesticides increases the egg weight loss and decreases hatchlings weight of Caiman latirostris (Crocodylia: Alligatoridae). Ecotoxicol. Environ. Saf. 68 (2007) 246-251
5. Benbrahim-Tallaa L., Siddeek B., Bozec A., Tronchon V., Florin A., Friry C., Tabone E., Mauduit C., and Benahmed M. Alterations of Sertoli cell activity in the long-term testicular germ cell death process induced by fetal androgen disruption. J. Endocrinol. 196 (2008) 21-31
6. Bisson M., and Hontela A. Cytotoxic and endocrine-disrupting potential of atrazine, diazinon, endosulfan, and mancozeb in adrenocortical steroidogenic cells of rainbow trout exposed in vitro. Toxicol. Appl. Pharmacol. 180 (2002) 110-117
7. Boekelheide K., Fleming S.L., Johnson K.J., Patel S.R., and Schoenfeld H.A. Role of Sertoli cells in injury-associated testicular germ cell apoptosis. Proc. Soc. Exp. Biol. Med. 225 (2000) 105-115
8. Crain D.A., Spiteri I.D., and Guillette Jr. L.J. The functional and structural observations of the neonatal reproductive system of alligators exposed in ovo to atrazine, 2, 4-d, or estradiol. Toxicol. Ind. Health 15 (1999) 180-185
9. Crain A., Eriksen M., Iguchi T., Jobling S., Laufer H., LeBlanc G.A., and Guillette L.J. An ecological assessment of bisphenol-A: evidence from comparative biology. Reprod. Toxicol. 24 (2007) 225-239
10. de Montgolfier B., Dufresne J., Letourneau M., Nagler J., Fournier A., Audet C., and Cyr D.G. The expression of multiple connexins throughout spermatogenesis in the rainbow trout testis suggests a role for complex intercellular communication. Biol. Reprod. 76 (2007) 2-8
11. de Montgolfier B., Fournier M., Audet C., Marcogliese D.J., and Cyr D.G. Influence of municipal effluents on the expression of connexins in the brook trout (Salvelinus fontinalis) testis. Aquat. Toxicol. 86 (2008) 38-48
12. Dutta H.M., Misquitta D., and Khan S. The effects of endosulfan on the testes of bluegill fish, Lepomis macrochirus: a histopathological study. Arch. Environ. Contam. Toxicol. 51 (2006) 149-156
13. Fan W., Yanase T., Morinaga H., Gondo S., Okabe T., Nomura M., Komatsu T., Morohashi K., Hayes T.B., Takayanagi R., and Nawata H. Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans. Environ. Health Perspect. 115 (2007) 720-727
14. Fiorini C., Tilloy-Ellul A., Chevalier S., Charuel C., and Pointis G. Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod. Toxicol. 18 (2004) 413-421
15. Gormley K.L., and Teather K.L. Developmental, behavioral, and reproductive effects experienced by Japanese medaka (Oryzias latipes) in response to short-term exposure to endosulfan. Ecotoxicol. Environ. Saf. 54 (2003) 330-338
16. Guillette L.J., and Edwards T.M. Environmental influences on fertility: can we learn lessons from studies of wildlife?. Fertil. Steril. 89 (2008) 21-24
17. Hayes T., Collins A., Lee M., Mendoza M., Noriega N., Stuart A.A., and Vonk A. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc. Natl. Acad. Sci. USA 99 (2002) 5476-5480
18. Hayes T.B., Stuart A.A., Mendoza M., Collins A., Noriega N., Vonk A., Johnston G., Liu R., and Kpodzo D. Characterization of atrazine-induced gonadal malformations in African clawed frogs (Xenopus laevis) and comparisons with effects of an androgen antagonist (cyproterone acetate) and exogenous estrogen (17beta-estradiol): support for the demasculinization/feminization hypothesis. Environ. Health Perspect. 114 (2006) 134-141
19. Hodges L.C., Bergerson J.S., Hunter D.S., and Walker C.L. Estrogenic effects of organochlorine pesticides on uterine leiomyoma cells in vitro. Toxicol. Sci. 54 (2000) 355-364
20. IPCS Global Assessment of the State-of-the-Science of Endocrine Disruptors. International Program of Chemical Safety, World Health Organization, Geneva, Switzerland, 2002.
21. Jobling S., Beresford N., Nolan M., Rodgers-Gray T., Brighty G.C., Sumpter J.P., and Tyler C.R. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol. Reprod. 66 (2002) 272-281
22. Jobling S., Williams R., Johnson A., Taylor A., Gross-Sorokin M., Nolan M., Tyler C.R., van Aerle R., Santos E., and Brighty G. Predicted exposures to steroid estrogens in U.K. Rivers correlate with widespread sexual disruption in wild fish populations. Environ. Health Perspect. 114 (2006) 32-39
23. Kang K., Wilson M.R., Hayashi T., Chang C.C., and Trosko J.E. Inhibition of gap junctional intercellular communication in normal human breast epithelial cells after treatment with pesticides, PCBs, and PBBs, alone or in mixtures. Environ. Health Perspect. 104 (1996) 192-200
24. Kang K.S., Lee Y.S., Kim H.S., and Kim S.H. DI-(2-ethylhexyl) phthalate-induced cell proliferation is involved in the inhibition of gap junctional intercellular communication and blockage of apoptosis in mouse Sertoli cells. J. Toxicol. Environ. Health A 65 (2002) 447-459
25. Kass L., Varayoud J., Ortega H., Muñoz-de-Toro M., and Luque E.H. Detection of bromodeoxyuridine in formalin-fixed tissue. DNA denaturation following microwave or enzymatic digestion pretreatment is required. Eur. J. Histochem. 44 (2000) 185-191
26. Kloas W., Lutz I., Springer T., Krueger H., Wolf J., Holden L., and Hosmer A. Does atrazine influence larval development and sexual differentiation in Xenopus laevis?. Toxicol. Sci. 107 (2009) 376-384
27. Laabs V., Amelung W., Pinto A.A., Wantzen M., da Silva C.J., and Zech W. Pesticides in surface water, sediment, and rainfall of the northeastern pantanal basin. Brazil. J. Environ. Qual. 31 (2002) 1636-1648
28. Legler J., Dennekamp M., Vethaak A.D., Brouwer A., Koeman J.H., van der Burg B., and Murk A.J. Detection of estrogenic activity in sediment-associated compounds using in vitro reporter gene assays. Sci. Total Environ. 293 (2002) 69-83
29. Maekawa M., Kamimura K., and Nagano T. Peritubular myoid cells in the testis: their structure and function. Arch. Histol. Cytol. 59 (1996) 1-13
30. Matter J.M., Crain D.A., Sills-McMurry C., Pickford D.B., Rainwater T.R., Reynolds K.D., Rooney A.A., Dickerson R.L., and Guillette L.J. Effects of endocrine-disrupting contaminants in reptiles: Alligators. In: Kendall R.J., Dickerson R., Giesy J.P., and Suk W.A. (Eds). Principles and Processes for Evaluating Endocrine Disruption in Wildlife (1998), SETAC Press, Pensacola, FL 267-289
31. Menone M.L., Aizpún de Moreno J.E., Moreno V.J., Lanfranchi A.L., Metcalfe T.L., and Metcalfe C.D. PCBs and organochlorines in tissues of silverside (Odontesthes bonariensis) from a coastal lagoon in Argentina. Arch. Environ. Contam. Toxicol. 38 (2000) 202-208
32. Milnes M.R., Bryan T.A., Medina J.G., Gunderson M.P., and Guillette Jr. L.J. Developmental alterations as a result of in ovo exposure to the pesticide metabolite p,p′-DDE in Alligator mississippiensis. Gen. Comp. Endocrinol. 144 (2005) 257-263
33. Milnes M.R., Bermudez D.S., Bryan T.A., Edwards T.M., Gunderson M.P., Larkin I.L., Moore B.C., and Guillette Jr. L.J. Contaminant-induced feminization and demasculinization of nonmammalian vertebrate males in aquatic environments. Environ. Res. 100 (2006) 3-17
34. Muñoz-de-Toro M., Maffini M., Giardina R., and Luque E.H. Processing fine needle aspirates of prostate carcinomas for standard immunocytochemical studies and in situ apoptosis detection. Path. Res. Practice 194 (1998) 631-636
35. Oberdörster E., and Cheek A.O. Gender benders at the beach: endocrine disruption in marine and estuarine organisms. Environ. Toxicol. Chem. 20 (2001) 23-36
36. Oka T., Tooi O., Mitsui N., Miyahara M., Ohnishi Y., Takase M., Kashiwagi A., Shinkai T., Santo N., and Iguchi T. Effect of atrazine on metamorphosis and sexual differentiation in Xenopus laevis. Aquat. Toxicol. 87 (2008) 215-226
37. Orlando E.F., and Guillette Jr. L.J. Sexual dimorphic responses in wildlife exposed to endocrine disrupting chemicals. Environ. Res. 104 (2007) 163-173
38. Sanderson J.T., Letcher R.J., Heneweer M., Giesy J.P., and van den Berg M. Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environ. Health Perspect. 109 (2001) 1027-1031
39. Sridharan S., Brehm R., Bergmann M., and Cooke P.S. Role of connexin 43 in Sertoli cells of testis. Ann. N.Y. Acad. Sci. 1120 (2007) 131-143
40. Siegel S. Nonparametric Statistics for the Behavioral Sciences (1956), McGraw-Hill, New York
41. Soto A.M., Chung K.L., and Sonnenschein C. The pesticides endosulfan, toxaphene, and dieldrin have estrogenic effects on human estrogen sensitive cells. Environ. Health Perspect. 102 (1994) 380-383
42. Stoker C., Rey F., Rodriguez H.A., Ramos J.G., Sirosky P., Larriera A., Luque E.H., and Muñoz-de-Toro M. Sex reversal effects on Caiman latirostris exposed to environmentally relevant doses of the xenoestrogen bisphenol A. Gen. Comp. Endocrinol. 133 (2003) 287-296
43. Stoker C., Beldoménico P.M., Bosquiazzo V.L., Zayas M.A., Rey F., Rodríguez H., Muñoz-de-Toro M., and Luque E.H. Developmental exposure to endocrine disruptor chemicals alters follicular dynamics and steroid levels in Caiman latirostris. Gen. Comp. Endocrinol. 156 (2008) 603-612
44. Storrs S.I., and Semlitsch R.D. Variation in somatic and ovarian development: predicting susceptibility of amphibians to estrogenic contaminants. Gen. Comp. Endocrinol. 156 (2008) 524-530
45. Varayoud J., Monje L., Bernhardt T., Muñoz-de-Toro M., Luque E.H., and Ramos J.G. Endosulfan modulates estrogen-dependent genes like a non-uterotrophic dose of 17-β estradiol. Reprod. Toxicol. 26 (2008) 138-145
46. Vonier P.M., Crain D.A., McLachlan J.A., Guillette Jr. L.J., and Arnold S.F. Interaction of environmental chemicals with the estrogen and progesterone receptors from the oviduct of the American alligator. Environ. Health Perspect. 104 (1996) 1318-1322
47. Wilhelms K.W., Cutler S.A., Proudman J.A., Carsia R.V., Anderson L.L., and Scanes C.G. Lack of effects of atrazine on estrogen responsive organs and circulating hormone concentrations in sexually immature female Japanese quail (Coturnix coturnix japonica). Chemosphere 65 (2006) 674-681
48. Williams G.T., and Smith C.A. Molecular regulation of apoptosis: genetic controls on cell death. Cell 74 (1993) 777-779
49. Wu T.H., Rainwater T.R., Platt S.G., McMurry S.T., and Anderson T.A. Organochlorine contaminants in Morelet's crocodile (Crocodylus moreletii) eggs from Belize. Chemosphere 40 (2000) 671-678