Gene-environment interactions: The potential role of contaminants in somatic growth and the development of the reproductive system of the American alligator

Molecular and Cellular Endocrinology

Volumn 354, Issue 1-2, 2012, Pages 111-120

  Moore, Brandon C ^a,d   Roark, Alison M ^a,b   Kohno, Satomi ^a,c   Hamlin, Heather J ^a,c   Guillette, Louis J ^a,c  

^a UNIVERSITY OF FLORIDA   (United States)

^b HOOD COLLEGE   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d LOUISIANA TECH UNIVERSITY   (United States)

Author keywords

Activin; Alligator; Aromatase; Follistatin; Growth; Ovary

Indexed keywords

ACTIVIN; AROMATASE; FOLLISTATIN; FOLLITROPIN; HORMONE RECEPTOR; INHIBIN A; MESSENGER RNA; SEX HORMONE;

ALLIGATOR; AMERICAN ALLIGATOR; ANIMAL EXPERIMENT; ARTICLE; BODY GROWTH; BODY MASS; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; ENVIRONMENTAL EXPOSURE; FEMALE; GENE EXPRESSION; GENOTYPE ENVIRONMENT INTERACTION; GROWTH RATE; HATCHING; LAKE; MALE; MOLECULAR DYNAMICS; NONHUMAN; ORGANOGENESIS; OVARY FUNCTION; PRIORITY JOURNAL; REPRODUCTIVE SYSTEM DEVELOPMENT; UNITED STATES; WATER POLLUTION;

ACTIVINS; ALLIGATORS AND CROCODILES; ANIMALS; BIOSYNTHETIC PATHWAYS; BODY WEIGHT; CYTOCHROME P-450 ENZYME SYSTEM; ENVIRONMENTAL EXPOSURE; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION; GENITALIA, FEMALE; OVARY; RECEPTORS, STEROID; TESTOSTERONE; TRANSCRIPTION, GENETIC;

EID: 84858298436     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.10.020     Document Type: Article

References (50)

1. Arukwe A. Organ-specific patterns of P450arom gene isoforms are modulated by p,p'-DDE in adult male European common frog, Rana temporaria. Mar. Environ. Res. 2006, 62:S215-S218.
2. Bristol-Gould S.K., Kreeger P.K., Selkirk C.G., Kilen S.M., Cook R.W., Kipp J.L., Shea L.D., Mayo K.E., Woodruff T.K. Postnatal regulation of germ cells by activin: The establishment of the initial follicle pool. Dev. Biol. 2006, 298:132-148.
3. Clark E.J., Norris D.O., Jones R.E. Interactions of gonadal steroids and pesticides (DDT, DDE) on 458 gonaduct growth in larval tiger salamanders, Ambystoma tigrinum. Gen. Comp. Endocrinol. 1998, 109:94-105.
4. Contractor R.G., Foran C.M., Li S.F., Willett K.L. Evidence of gender- and tissue-specific promoter methylation and the potential for ethinylestradiol-induced changes in Japanese medaka (Oryzias latipes) estrogen receptor and aromatase genes. J. Toxicol. Env. Health-Part A 2004, 67:1-22.
5. Cooke P.S., Naaz A. Role of estrogens in adipocyte development and function. Exp. Biol. Med. 2004, 229:1127-1135.
6. Crain D.A., Janssen S.J., Edwards T.M., Heindel J., Ho S.M., Hunt P., Iguchi T., Juul A., McLachlan J.A., Schwartz J., Skakkebaek N., Soto A.M., Swan S., Walker C., Woodruff T.K., Woodruff T.J., Giudice L.C., Guillette L.J. Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil. Steril. 2008, 90:911-940.
7. Davis L.M., Glenn T.C., Strickland D.C., Guillette L.J., Elsey R.M., Rhodes W.E., Dessauer H.C., Sawyer R.H. Microsatellite DNA analyses support an east-west phylogeographic split of American alligator populations. J. Exp. Zool. 2002, 294:352-372.
8. Edwards T.M., Gunderson M.P., Milnes M.R., Guillette L.J. Gonadotropin-induced testosterone response in peripubertal male alligators. Gen. Comp. Endocrinol. 2004, 135:372-380.
9. Ferguson M.W.J., Joanen T. Temperture-dependent sex detemination in Alligator-mississippensis. J. Zool. 1983, 200:143-177.
10. Garrison A.W., Guillette L.J., Wiese T.E., Avants J.K. Persistent organochlorine pesticides and their metabolites in alligator livers from Lakes Apopka and Woodruff, Florida, USA. Int. J. Environ. Anal. Chem. 2010, 90:159-170.
11. Govoroun M.S., Pannetier M., Pailhoux E., Cocquet J., Brillard J.P., Couty I., Batellier F., Cotinot C. Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Dev. Dyn. 2004, 231:859-870.
12. Gray L.E., Ostby J., Furr J., Wolf C.J., Lambright C., Parks L., Veeramachaneni D.N., Wilson V., Price M., Hotchkiss A., Orlando E., Guillette L. Effects of environmental antiandrogens on reproductive development in experimental animals. Hum. Reprod. Update 2001, 7:248-264.
13. Gray L.E., Wolf C., Lambright C., Mann P., Price M., Cooper R.L., Ostby J. Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p,p'-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate) during sexual differentiation produces diverse profiles of reproductive malformations in the male rat. Toxicol. Industrial Health 1999, 15:94-118.
14. Guillette L.J., Crain D.A., Gunderson M.P., Kools S.A.E., Milnes M.R., Orlando E.F., Rooney A.A., Woodward A.R. Alligators and endocrine disrupting contaminants: A current perspective. Am. Zool. 2000, 40:438-452.
15. Guillette L.J., Woodward A.R., Crain D.A., Masson G.R., Palmer B.D., Cox M.C., Qui Y.X., Orlando E.F. The reproductive cycle of the female American alligator (Alligator mississippiensis). Gen. Comp. Endocrinol. 1997, 108:87-101.
16. Gunderson M.P., Kohno S., Blumberg B., Iguchi T., Guillette L.J. Up-regulation of the alligator CYP3A77 gene by toxaphene and dexamethasone and its short term effect on plasma testosterone concentrations. Aquatic Toxicol. 2006, 78:272-283.
17. Hamlin H.J., Lowers R.H., Albergotti L.C., McCoy M.W., Mutz J., Guillette L.J. Environmental Influence on Yolk Steroids in American Alligators (Alligator mississippiensis). Biol. Reproduction 2010, 83:736-741.
18. Heindel J.J., vom Saal F.S. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Mol. Cell. Endocrinol. 2009, 304:90-96.
19. Hochberg Z., Feil R., Constancia M., Fraga M., Junien C., Carel J.C., Boileau P., Le Bouc Y., Deal C.L., Lillycrop K., Scharfmann R., Sheppard A., Skinner M., Szyf M., Waterland R.A., Waxman D.J., Whitelaw E., Ong K., Albertsson-Wikland K. Child Health, Developmental Plasticity, and Epigenetic Programming. Endocr. Rev. 2011, 32:159-224.
20. Howdeshell K.L., Hotchkiss A.K., Thayer K.A., Vandenbergh J.G., vom Saal F.S. Environmental toxins - Exposure to bisphenol A advances puberty. Nature 1999, 401:763-764.
21. Karmaus W., Osuch J.R., Landgraf J., Taffe B., Mikucki D., Haan P. Prenatal and concurrent exposure to halogenated organic compounds and gene expression of CYP17A1, CYP19A1, and oestrogen receptor alpha and beta genes. Occup. Environ. Med. 2011, 68:430-437.
22. Kimura F., Bonomi L.M., Schneyer A.L. Follistatin regulates germ cell nest breakdown and primordial follicle formation. Endocrinology 2011, 152:697-706.
23. Kipp J.J.L., Kilen S.M., Woodruff T.K., Mayo K.E. Activin regulates estrogen receptor gene expression in the mouse ovary. J. Biol. Chem. 2007, 282:36755-36765.
24. 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.
25. Lance V.A., Vliet K.A. EFFECT of mammalian gonadotropins on testosterone secretion in male alligators. J. Exp. Zool. 1987, 241:91-94.
26. Mendez M.A., Garcia-Esteban R., Guxens M., Vrijheid M., Kogevinas M., Goni F., Fochs S., Sunyer J. Prenatal organochlorine compound exposure, rapid weight gain, and overweight in infancy. Environ. Health Perspect. 2011, 119:272-278.
27. Milnes M.R., Bryan T.A., Katsu Y., Kohno S., Moore B.C., Iguchi T., Guillette L.J. Increased posthatching mortality and loss of sexually dimorphic gene expression in alligators (Alligator mississippiensis) from a contaminated environment. Biol. Reprod. 2008, 78:932-938.
28. Milnes M.R., Bryan T.A., Medina J.G., Gunderson M.P., Guillette L.J. Developmental alterations as a result of in ovo exposure to the pesticide metabolite p,p'-DDE in Alligator mississippiensis. Gen. Comp. Endocrinol. 2005, 144:257-263.
29. Milnes M.R., Guillette L.J. Alligator tales: new lessons about environmental contaminants from a sentinel species. Bioscience 2008, 58:1027-1036.
30. Moore B.C., Hamlin H.J., Botteri N.L., Guillette L.J. Gonadal mRNA expression levels of TGFβ signaling factors correspond with post hatching morphological development in American alligators. Sexual Development 2010, 4.
31. 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.
32. Moore B.C., Kohno S., Cook R.W., Alvers A.L., Hamlin H.J., Woodruff T.K., Guillette L.J. Altered Sex Hormone Concentrations and Gonadal mRNA Expression Levels of Activin Signaling Factors in Hatchling Alligators From a Contaminated Florida Lake. J. Exp. Zool. Part a-Ecol. Genet. Physiol. 2010, 313A:218-230.
33. Moore B.C., Milnes M.R., Kohno S., Katsu Y., Iguchi T., Guillette L.J. Influences of sex, incubation temperature, and environmental quality on gonadal estrogen and androgen receptor messenger rna expression in juvenile american alligators (Alligator mississippiensis). Biol. Reprod. 2010, 82:194-201.
34. Narbaitz R., DeRobertis E.M. Postnatal evolution of steroidogenic cells in chick ovary. Histochemie 1968, 15:187.
35. Newbold R.R. Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol. Appl. Pharmacol. 2004, 199:142-150.
36. Newbold R.R., Padilla-Banks E., Snyder R., Jefferson W.N. Developmental exposure to environmental estrogens is associated with obesity later in life. Pediatr. Res. 2005, 58:1126-1126.
37. Onagbesan O., Bruggeman V., Decuypere E. Intra-ovarian growth factors regulating ovarian function in avian species: A review. Anim. Reprod. Sci. 2009, 111:121-140.
38. Oreal E., Mazaud S., Picard J.Y., Magre S., Carre-Eusebe D. Different patterns of anti-Mullerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4, and Lhx9 expression, in the chick differentiating gonads. Dev. Dyn. 2002, 225:221-232.
39. Pangas S.A., Jorgez C.J., Tran M., Agno J., Li X.H., Brown C.W., Kumar T.R., Matzuk M.M. Intraovarian activins are required for female fertility. Mol. Endocrinol. 2007, 21:2458-2471.
40. Raivio T., Dunkel L. Inhibins in childhood and puberty. Best Pract. Res. Clin. Endoc. Metab. 2002, 16:43-52.
41. Rauschenberger R.H., Wiebe J.J., Sepulveda M.S., Scarborough J.E., Gross T.S. Parental exposure to pesticides and poor clutch viability in American alligators. Environ. Sci. Technol. 2007, 41:5559-5563.
42. Rusiecki J.A., Baccarelli A., Bollati V., Tarantini L., Moore L.E., Bonefeld-Jorgensen E.C. Global DNA Hypomethylation Is Associated with High Serum-Persistent Organic Pollutants in Greenlandic Inuit. Environ. Health Perspect. 2008, 116:1547-1552.
43. Seder C.W., Hartojo W., Lin L., Silvers A.L., Wang Z., Thomas D.G., Giordano T.J., Chen G., Chang A.C., Orringer M.B., Beer D.G. INHBA overexpression promotes cell proliferation and may be epigenetically regulated in esophageal adenocarcinoma. J. Thoracic Oncol. 2009, 4:455-462.
44. Shutoh Y., Takeda M., Ohtsuka R., Haishima A., Yamaguchi S., Fujie H., Komatsu Y., Maita K., Harada T. Low dose effects of dichlorodiphenyltrichloroethane (DDT) on gene transcription and DNA methylation in the hypothalamus of young male rats: implication of hormesis-like effects. J. Toxicol. Sci. 2009, 34:469-482.
45. Utriainen P., Li J.Q., Kuulasmaa T., Voutilainen R. Inhibition of DNA methylation increases follistatin expression and secretion in the human adrenocortical cell line NCI-H295R. J. Endocrinol. 2006, 188:305-310.
46. Welshons W.V., Nagel S.C., vom Saal F.S.V. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol a at levels of human exposure. Endocrinology 2006, 147:S56-S69.
47. Welshons W.V., Thayer K.A., Judy B.M., Taylor J.A., Curran E.M., vom Saal F.S. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ. Health Perspect. 2003, 111:994-1006.
48. P.M. Wilkinson, Nesting ecology of the American alligator in coastal South Carolina. Study Completion Report August 1978-September 1983. SC Wildlife and Marine Resources Department, Columbia, SC, 1983.
49. Yao H.H.C. The pathway to femaleness: current knowledge on embryonic development of the ovary. Mol. Cell. Endocrinol. 2005, 230:87-93.
50. Zama A.M., Uzumcu M. Epigenetic effects of endocrine-disrupting chemicals on female reproduction: an ovarian perspective. Front. Neuroendocrinol. 2010, 31:420-439.