Neonatal expression of amh, sox9 and sf-1 mRNA in Caiman latirostris and effects of in ovo exposure to endocrine disrupting chemicals

General and Comparative Endocrinology

Volumn 191, Issue , 2013, Pages 31-38

  Durando, Milena ^a   Cocito, Laura ^a   Rodríguez, Horacio A ^a   Varayoud, Jorgelina ^a   Ramos, Jorge G ^a   Luque, Enrique H ^a   Muñoz de Toro, Mónica ^a  

^a UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

Bisphenol A; Crocodilian; Endosulfan; Sex determining genes; Sexual dimorphism; Temperature dependent sex determination

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ENDOCRINE DISRUPTOR; ENDOSULFAN; ESTRADIOL; MESSENGER RNA; MUELLERIAN INHIBITING FACTOR; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR SOX9;

ADRENAL GLAND; AMH GENE; ANIMAL TISSUE; ARTICLE; CAIMAN; CAIMAN LATIROSTRIS; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION; GONAD; HORMONE DEPENDENT SEX DETERMINATION; MALE; MESONEPHROS; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEX DETERMINATION; SEX DIFFERENCE; SF 1 GENE; SOX9 GENE; TEMPERATURE DEPENDENT SEX DETERMINATION;

EID: 84879701005     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.05.013     Document Type: Article

References (61)

1. American Society of Icthyologists and Herpetologists (ASIH), 2004. Guidelines for Use of Live Amphibians and Reptiles in Field and Laboratory Research. Revised by the Herpetological Animal Care and Use Committee, second ed. Available from: http://www.asih.org/publications.
2. Barske L.A., Capel B. Estrogen represses SOX9 during sex determination in the red-eared slider turtle Trachemys scripta. Dev. Biol. 2010, 341:305-314.
3. Beldomenico P.M., Rey F., Prado W.S., Villarreal J.C., Muñoz-de-Toro M., 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. 2007, 68:246-251.
4. Bisson M., 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. Pharm. Acol. 2002, 180:110-117.
5. Boggs A.S., Hamlin H.J., Lowers R.H., Guillette L.J. Seasonal variation in plasma thyroid hormone concentrations in coastal versus inland populations of juvenile American alligators (Alligator mississippiensis): influence of plasma iodide concentrations. Gen. Comp. Endocrinol. 2011, 174:362-369.
6. Cooke P.S., Simon L., Cimafranca M.A., Gore A.C., Crews D. Environmental endocrine disruptors and male reproductive toxicology. Comprehensive Toxicology 2010, 232-246. Elsevier Inc., Amsterdam. C.A. McQueen, J. Bond, K. Ramos, J. Lamb, F.P. Guengerich, D. Lawrence, M. Walker, M. Campen, R. Schnellmann, G.S. Yost, R.A. Roth, P. Ganey, S. Hooser, J. Richburg, P. Hoyer, T. Knudsen, G. Daston, M. Philbert, R. Roberts (Eds.).
7. Couse J.F., Hewitt S.C., Bunch D.O., Sar M., Walker V.R., Davis B.J., Korach K.S. Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science 1999, 286:2328-2331.
8. Crain D.A., Guillette L.J., Rooney A.A., Pickford D.B. Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminants. Environ. Health Perspect. 1997, 105:528-533.
9. Crews D., Cantú A.R., Rhen T., Vohra R. The relative effectiveness of estrone, estradiol-17 beta, and estriol in sex reversal in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination. Gen. Comp. Endocrinol. 1996, 102:317-326.
10. de Montgolfier B., Dufresne J., Letourneau M., Nagler J., Fournier A., Audet C., Cyr D.G. The expression of multiple connexins throughout spermatogenesis in the rainbow trout testis suggests a role for complex intercellular communication. Biol. Reprod. 2007, 76:2-8.
11. Dupont S., Dennefeld C., Krust A., Chambon P., Mark M. Expression of Sox9 in granulosa cells lacking the estrogen receptors, ERalpha and ERbeta. Dev. Dyn. 2003, 226:103-106.
12. Durando M., Kass L., Perdomo V., Bosquiazzo V.L., Luque E.H., Muñoz-de-Toro M. Prenatal exposure to bisphenol A promotes angiogenesis and alters steroid-mediated responses in the mammary glands of cycling rats. J. Steroid Biochem. Mol. Biol. 2011, 127:35-43.
13. Fan W., Yanase T., Morinaga H., Gondo S., Okabe T., Nomura M., Hayes T.B., Takayanagi R., Nawata H. Herbicide atrazine activates SF-1 by direct affinity and concomitant co-activators recruitments to induce aromatase expression via promoter II. Biochem. Biophys. Res. Commun. 2007, 355:1012-1018.
14. Ferguson M.W.J. Reproductive biology and embryology of the crocodilians. Biology of the Reptilia 1985, 329-491. Wiley, New York. C. Gans, F. Billet, P.F.A. Maderson (Eds.).
15. Fernandino J.I., Hattori R.S., Kimura H., Strüssmann C.A., Somoza G.M. Expression profile and estrogenic regulation of anti-Müllerian hormone during gonadal development in pejerrey Odontesthes bonariensis, a teleost fish with strong temperature-dependent sex determination. Dev. Dyn. 2008, 237:3192-3199.
16. Fleming A., Crews D. Estradiol and incubation temperature modulate regulation of steroidogenic factor 1 in the developing gonad of the red-eared slider turtle. Endocrinology 2001, 142:1403-1411.
17. Flint S., Markle T., Thompson S., Wallace E. Bisphenol A exposure, effects, and policy: a wildlife perspective. J. Environ. Manage. 2012, 104:19-34.
18. Fromme H., Küchler T., Otto T., Pilz K., Müller J., Wenzel A. Occurrence of phthalates and bisphenol A and F in the environment. Water Res. 2002, 36:1429-1438.
19. Gilbert S.F. Environmental sex determination. Developmental Biology 2000, Sinauer Associates, Sunderland, MA, Available from: http://www.ncbi.nlm.nih.gov/books/NBK9989/. Sixth ed.
20. Gormley K.L., 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. 2003, 54:330-338.
21. Guillette L.J., Edwards T.M. Environmental influences on fertility: can we learn lessons from studies of wildlife?. Fertil. Steril. 2008, 89:21-24.
22. Hamlin H.J., Guillette L.J. Embryos as targets of endocrine disrupting contaminants in wildlife. Birth Defects Res. C Embryo Today 2011, 93:19-33.
23. Hayes T.B., Collins A., Lee M., Mendoza M., Noriega N., Stuart A.A., Vonk A. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:5476-5480.
24. Hayes T.B., Anderson L.L., Beasley V.R., de Solla S.R., Iguchi T., Ingraham H., Kestemont P., Kniewald J., Kniewald Z., Langlois V.S., Luque E.H., McCoy K.A., Muñoz-de-Toro M., Oka T., Oliveira C.A., Orton F., Ruby S., Suzawa M., Tavera-Mendoza L.E., Trudeau V.L., Victor-Costa A.B., Willingham E. Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes. J. Steroid Biochem. Mol. Biol. 2011, 127:64-73.
25. Johns S.M., Denslow N.D., Kane M.D., Watanabe K.H., Orlando E.F., Sepúlveda M.S. Effects of estrogens and antiestrogens on gene expression of fathead minnow (Pimephales promelas) early life stages. Environ. Toxicol. 2011, 26:195-206.
26. Kass L., Altamirano G.A., Bosquiazzo V.L., Luque E.H., Muñoz-de-Toro M. Perinatal exposure to xenoestrogens impairs mammary gland differentiation and modifies milk composition in Wistar rats. Reprod. Toxicol. 2012, 33:390-400.
27. Kent J., Wheatley S.C., Andrews J.E., Sinclair A.H., Koopman P. A male-specific role for SOX9 in vertebrate sex determination. Development 1996, 122:2813-2822.
28. Kobayashi A., Chang H., Chaboissier M.C., Schedl A., Behringer R.R. Sox9 in testis determination. Ann. N.Y. Acad. Sci. 2005, 1061:9-17.
29. Kohno S., Bermudez D.S., Katsu Y., Iguchi T., Guillette L.J. Gene expression patterns in juvenile American alligators (Alligator mississippiensis) exposed to environmental contaminants. Aquat. Toxicol. 2008, 88:95-101.
30. Kohno S., Katsu Y., Urushitani H., Ohta Y., Iguchi T., Guillette L.J. Potential contributions of heat shock proteins to temperature-dependent sex determination in the American alligator. Sex. Dev. 2010, 4:73-87.
31. Koopman P., Gubbay J., Vivian N., Goodfellow P., Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 1991, 351:117-121.
32. Lang J.W., Andrews H.V. Temperature-dependent sex determination in crocodilians. J. Exp. Zool. 1994, 270:28-44.
33. Milnes M.R., Roberts R.N., Guillette L.J. Effects of incubation temperature and estrogen exposure on aromatase activity in the brain and gonads of embryonic alligators. Environ. Health Perspect. 2002, 110:393-396.
34. Moore B.C., Hamlin H.J., Botteri N.L., Lawler A.N., Mathavan K.K., Guillette L.J. Posthatching development of Alligator mississippiensis ovary and testis. J. Morphol. 2010, 271:580-595.
35. Morais da Silva S., Hacker A., Harley V., Goodfellow P., Swain A., Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 1996, 14:62-68.
36. Mork L., Capel B. Oestrogen shuts the door on SOX9. BMC Biol. 2010, 8:110.
37. Morrish B.C., Sinclair A.H. Vertebrate sex determination: many means to an end. Reproduction 2002, 124:447-457.
38. Münsterberg A., Lovell-Badge R. Expression of the mouse anti-Müllerian hormone gene suggests a role in both male and female sexual differentiation. Development 1991, 113:613-624.
39. Nakamura M. The mechanism of sex determination in vertebrates - are sex steroids the key-factor?. J. Exp. Zool. A Ecol. Genet. Physiol. 2010, 313:381-398.
40. National Research Council Hormonally Active Agents in the Environment 1999, National Academy Press, Washington, DC.
41. Oréal E., Pieau C., Mattei M.G., Josso N., Picard J.Y., Carré-Eusèbe D., Magre S. Early expression of AMH in chicken embryonic gonads precedes testicular SOX9 expression. Dev. Dyn. 1998, 212:522-532.
42. Ramos J.G., Varayoud J., Kass L., Rodríguez H., Costabel L., Muñoz-de-Toro M., Luque E.H. Bisphenol a induces both transient and permanent histofunctional alterations of the hypothalamic-pituitary-gonadal axis in prenatally exposed male rats. Endocrinology 2003, 144:3206-3215.
43. Ramsey M., Crews D. Adrenal-kidney-gonad complex measurements may not predict gonad-specific changes in gene expression patterns during temperature-dependent sex determination in the red-eared slider turtle (Trachemys scripta elegans). J. Exp. Zool. A Ecol. Genet. Physiol. 2007, 307:463-470.
44. Rey F., González M., Zayas M.A., Stoker C., Durando M., Luque E.H., Muñoz-de-Toro M. Prenatal exposure to pesticides disrupts testicular histoarchitecture and alters testosterone levels in male Caiman latirostris. Gen. Comp. Endocrinol. 2009, 162:286-292.
45. Rey R., Lukas-Croisier C., Lasala C., Bedecarrás P. AMH/MIS: what we know already about the gene, the protein and its regulation. Mol. Cell. Endocrinol. 2003, 211:21-31.
46. Richter C.A., Birnbaum L.S., Farabollini F., Newbold R.R., Rubin B.S., Talsness C.E., Vandenbergh J.G., Walser-Kuntz D.R., Vom Saal F.S. In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 2007, 24:199-224.
47. Schimmer B.P., White P.C. Minireview: steroidogenic factor 1: its roles in differentiation, development, and disease. Mol. Endocrinol. 2010, 24:1322-1337.
48. Sinclair A.H., Berta P., Palmer M.S., Hawkins J.R., Griffiths B.L., Smith M.J., Foster J.W., Frischauf A.M., Lovell-Badge R., Goodfellow P.N. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 1990, 346:240-244.
49. Smith C.A., Joss J.M.P. Gonadal sex differentiation in Alligator mississippiensis, a species with temperature-dependent sex determination. Cell Tissue Res. 1993, 273:149-162.
50. Sridharan S., Brehm R., Bergmann M., Cooke P.S. Role of connexin 43 in Sertoli cells of testis. Ann. N.Y. Acad. Sci. 2007, 1120:131-143.
51. Stoker C., Rey F., Rodríguez H., Ramos J.G., Sirosky P., Larriera A., Luque E.H., Muñoz-de-Toro M. Sex reversal effects on Caiman latirostris exposed to environmentally relevant doses of the xenoestrogen bisphenol A. Gen. Comp. Endocrinol. 2003, 133:287-296.
52. Stoker C., Beldoménico P.M., Bosquiazzo V.L., Zayas M.A., Rey F., Rodríguez H., Muñoz-de-Toro M., Luque E.H. Developmental exposure to endocrine disruptor chemicals alters follicular dynamics and steroid levels in Caiman latirostris. Gen. Comp. Endocrinol. 2008, 156:603-612.
53. Stoker C., Repetti M.R., García S.R., Zayas M.A., Galoppo G.H., Beldoménico H.R., Luque E.H., Muñoz-de-Toro M. Organochlorine compound residues in the eggs off broad-snouted caimans (Caiman latirostris) and correlation with measures of reproductive performance. Chemosphere 2011, 84:311-317.
54. Urushitani H., Katsu Y., Miyagawa S., Kohno S., Ohta Y., Guillette L.J., Iguchi T. Molecular cloning of anti-Müllerian hormone from the American alligator, Alligator mississippiensis. Mol. Cell. Endocrinol. 2011, 333:190-199.
55. Varayoud J., Monje L., Bernhardt T., Muñoz-de-Toro M., Luque E.H., Ramos J.G. Endosulfan modulates estrogen-dependent genes like a non-uterotrophic dose of 17beta-estradiol. Reprod. Toxicol. 2008, 26:138-145.
56. Warner D.A. Sex determination in reptiles. Hormones and Reproduction of Vertebrates 2011, 1-38. Elsevier Inc., San Diego, CA. D.O. Norris, K.H. Lopez (Eds.).
57. Western P.S., Harry J.L., Graves J.A., Sinclair A.H. Temperature-dependent sex determination: upregulation of SOX9 expression after commitment to male development. Dev. Dyn. 1999, 214:171-177.
58. Western P.S., Harry J.L., Graves J.A., Sinclair A.H. Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression. Dev. Dyn. 1999, 216:411-419.
59. Western P.S., Harry J.L., Marshall Graves J.A., Sinclair A.H. Temperature-dependent sex determination in the American alligator: expression of SF1, WT1 and DAX1 during gonadogenesis. Gene 2000, 241:223-232.
60. Wetherill Y.B., Akingbemi B.T., Kanno J., McLachlan J.A., Nadal A., Sonnenschein C., Watson C.S., Zoeller R.T., Belcher S.M. In vitro molecular mechanisms of bisphenol A action. Reprod. Toxicol. 2007, 24:178-198.
61. Zayas M.A., Rodríguez H.A., Galoppo G.H., Durando M., Luque E.H., Muñoz-de-Toro M. Hematology and blood biochemistry of young healthy broad-snouted caimans (Caiman latirostris). J. Herpetol. 2011, 45:516-524.