Steroidogenic acute regulatory (StAR) protein and cholesterol side-chain cleavage (P450scc) as molecular and cellular targets for 17α- ethynylestradiol in salmon previtellogenic oocytes

Chemical Research in Toxicology

Volumn 20, Issue 12, 2007, Pages 1811-1819

  Vang, Siv Hege ^a   Kortner, Trond M ^a   Arukwe, Augustine ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

11 OXOTESTOSTERONE; CHOLESTEROL; ENDOCRINE DISRUPTOR; ETHINYLESTRADIOL; MESSENGER RNA; SOMATOMEDIN B; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TESTOSTERONE;

ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CHEMICAL MUTAGENESIS; CHOLESTEROL SIDE CHAIN CLEAVAGE; CONTROLLED STUDY; ENZYME IMMUNOASSAY; GENOTOXICITY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN VARIANT; REAL TIME POLYMERASE CHAIN REACTION; SALMON; STEROIDOGENESIS; TISSUE CULTURE; VITELLOGENESIS; XENOBIOTIC METABOLISM;

ANIMALS; BASE SEQUENCE; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; ENDOCRINE DISRUPTORS; ETHINYL ESTRADIOL; FEMALE; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MOLECULAR SEQUENCE DATA; OOCYTES; PHOSPHOPROTEINS; SALMON; VITELLOGENESIS;

TELEOSTEI;

EID: 38149020828     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx700228g     Document Type: Article

References (59)

1. Stocco, D. M. (2000) The role of the StAR protein in steroidogenesis: Challenges for the future. J. Endocrinol. 164, 247-253.
2. Sierra, A. (2004) Neurosteroids: The StAR protein in the brain. J. Neuroendocrinol. 16, 787-793.
3. Geslin, M., and Auperin, B. (2004) Relationship between changes in mRNAs of the genes encoding steroidogenic acute regulatory protein and P450 cholesterol side chain cleavage in head kidney and plasma levels of cortisol in response to different kinds of acute stress in the rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endrocrinol. 135, 70-80.
4. Artemenko, I. P., Zhao, D., Hales, D. B., Hales, K. H., and Jefcoate, C. R. (2001) Mitochondrial processing of newly synthesized steroidogenic acute regulatory protein (StAR), but not total StAR, mediates cholesterol transfer to cytochrome P450 side chain cleavage enzyme in adrenal cells. J. Biol. Chem. 276, 46583-46596.
5. Jefcoate, C. R., Artemenko, I. P., and Zhao, D. (2000) Relationship of StAR expression to mitochondrial cholesterol transfer and metabolism. Endocr. Res. 26, 663-680.
6. Kusakabe, M., Todo, T., McQuillan, H. J., Goetz, F. W., and Young, G. (2002) Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. Endocrinology 143, 2062-2070.
7. Miller, W. L. (1988) Molecular biology of steroid hormone synthesis. Endocr. Rev. 9, 295-318.
8. Callard, G. V., Tchoudakova, A. V., Kishida, M., and Wood, E. (2001) Differential tissue distribution, developmental programming, estrogen regulation and promoter characteristics of cyp19 genes in teleost fish. J. Steroid Biochem. Mol. Biol. 79, 305-314.
9. Kishida, M., and Callard, G. V. (2001) Distinct cytochrome P450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinology 142, 740-750.
10. Arukwe, A., and Goksoyr, A. (2003) Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: Oogenetic, population, and evolutionary implications of endocrine disruption. Comp. Hepatol. 2, 4.
11. Arukwe, A., and Goksøyr, A. (1998) Xenobiotics, xenoestrogens and reproduction disturbancecs in fish. Sarsia 83, 225-241.
12. Nash, J. P., Kime, D. E., Van der Ven, L. T., Wester, P. W., Brion, F., Maack, G., Stahlschmidt-Allner, P., and Tyler, C. R. (2004) Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Perspect. 112, 1725-1733.
13. Meucci, V., and Arukwe, A. (2005) Detection of vitellogenin and zona radiata protein expressions in surface mucus of immature juvenile Atlantic salmon (Salmo salar) exposed to waterborne nonylphenol. Aquat. Toxicol. 73 (1), 1-10.
14. Kwak, H. I., Bae, M. O., Lee, M. H., Lee, Y. S., Lee, B. J., Kang, K. S., Chae, C. H., Sung, H. J., Shin, J. S., Kim, J. H., Mar, W. C., Sheen, Y. Y., and Cho, M. H. (2001) Effects of nonylphenol, bisphenol A, and their mixture on the viviparous swordtail fish (Xiphophorus helleri). Environ. Toxicol. Chem. 20, 787-795.
15. Jobling, S., Beresford, N., Nolan, M., Rodgers-Gray, T., Brighty, G. C., Sumpter, J. P., and Tyler, C. R. (2002) Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol. Reprod. 66, 272-281.
16. Desbrow, C., Routledge, E. J., Brighty, G., Sumpter, J. P., and Waldock, M. J. (1998) Indentification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitrobiological screening. Environ. Sci. Technol. 32, 1559-1565.
17. Larsson, D. G. J., Adolfsson-Erici, M., Parkkonen, J., Pettersson, M., Berg, A. H., Olsson, P. E., and Förlin, L. (1999) Ethinyloestradiol - an undesired fish contraceptive. Aquat. Toxicol. 45, 91-97.
18. Aherne, G. W., and Briggs, R. (1989) The relevance of the presence of certain synthetic steroids in the aquatic environment. J. Pharm. Pharmacol. 41, 735-736.
19. Kolpin, D. W., Furlong, E. T., Meyer, M. T., Thurman, E. M., Zaugg, S. D., Barber, L. B., and Buxton, H. T. (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: A national reconnaissance. Environ. Sci. Technol. 36, 1202-1211.
20. Arukwe, A. (2005) Modulation of brain steroidogenesis by affecting transcriptional changes of steroidogenic acute regulatory (StAR) protein and cholesterol side chain cleavage (P450scc) in juvenile Atlantic salmon (Salmo salar) is a novel aspect of nonylphenol toxicity. Environ. Sci. Technol. 39, 9791-9798.
21. Lyssimachou, A., and Arukwe, A. (2007) Alteration of brain and interrenal StAR protein, P450scc, and Cyp11beta mRNA levels in atlantic salmon after nominal waterborne exposure to the synthetic pharmaceutical estrogen ethynylestradiol. J. Toxicol. Environ. Health A 70, 606-613.
22. Kortner, T. M., and Arukwe, A. (2007) The xenoestrogen, 4-nonylphenol, impaired steroidogenesis in previtellogenic oocyte culture of Atlantic cod (Gadus morhua) by targeting the StAR protein and P450scc expressions. Gen. Comp. Endrocrinol. 150, 419-429.
23. Nader, M. R., Miura, T., Ando, N., Miura, C., and Yamauchi, K. (1999) Recombinant human insulin-like growth factor I stimulates all stages of 11-ketotestosterone-induced spermatogenesis in the Japanese eel, Anguilla japonica, in vitro. Biol. Reprod. 61, 944-947.
24. Chirgwin, J. M., Przybyla, A. E., MacDonald, R. J., and Rutter, W. J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294-5299.
25. Chomczynski, P., and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
26. Arukwe, A. (2006) Toxicological housekeeping genes: Do they really keep the house? Environ. Sci. Technol. 40, 7944-7949.
27. Steele, B. K., Meyers, C., and Ozbun, M. A. (2002) Variable expression of some "housekeeping" genes during human keratinocyte differentiation. Anal. Biochem. 307, 341-347.
28. Lyssimachou, A., Jenssen, B. M., and Arukwe, A. (2006) Brain cytochrome P450 aromatase gene isoforms and activity levels in atlantic salmon after waterborne exposure to nominal environmental concentrations of the pharmaceutical ethynylestradiol and antifoulant tributyltin. Toxicol. Sci. 91, 82-92.
29. Barannikova, I. A., Dyubin, V. P., Bayunova, L. V., and Semenkova, T. B. (2002) Steroids in the control of reproductive function in fish. Neurosci. Behav. Physiol. 32, 141-148.
30. Jiang, J. Q., Young, G., Kobayashi, T., and Nagahama, Y. (1998) Eel (Anguilla japonica) testis 11beta-hydroxylase gene is expressed in interrenal tissue and its product lacks aldosterone synthesizing activity. Mol. Cell. Endocrinol. 146, 207-211.
31. Bieniarz, K., and Epler, P. (1992) Advances in reproductive endocrinology of fish. J. Physiol. Pharmacol. 43, 215-222.
32. Yadetie, F., and Male, R. (2002) Effects of 4-nonylphenol on gene expression of pituitary hormones in juvenile Atlantic salmon (Salmo salar). Aquat. Toxicol. 58, 113-129.
33. Hutchinson, T. H., and Pickford, D. B. (2002) Ecological risk assessment and testing for endocrine disruption in the aquatic environment. Toxicology 181-182, 383-387.
34. Halm, S., Pounds, N., Maddix, S., Rand-Weaver, M., Sumpter, J. P., Hutchinson, T. H., and Tyler, C. R. (2002) Exposure to exogenous 17beta-oestradiol disrupts p450aromB mRNA expression in the brain and gonad of adult fathead minnows (Pimephales promelas). Aquat. Toxicol. 60, 285-299.
35. Kazeto, Y., Place, A. R., and Trant, J. M. (2004) Effects of endocrine disrupting chemicals on the expression of CYP19 genes in zebrafish (Danio rerio) juveniles. Aquat. Toxicol. 69, 25-34.
36. Trant, J. M., Gavasso, S., Ackers, J., Chung, B. C., and Place, A. R. (2001) Developmental expression of cytochrome P450 aromatase genes (CYP19a and CYP19b) in zebrafish fry (Danio rerio). J. Exp. Zool. 290, 475-483.
37. Hilscherova, K., Jones, P. D., Gracia, T., Newsted, J. L., Zhang, X., Sanderson, J. T., Yu, R. M., Wu, R. S., and Giesy, J. P. (2004) Assessment of the effects of chemicals on the expression of ten steroidogenic genes in the H295R cell line using real-time PCR. Toxicol. Sci. 81, 78-89.
38. Walsh, L. P., Webster, D. R., and Stocco, D. M. (2000) Dimethoate inhibits steroidogenesis by disrupting transcription of the steroidogenic acute regulatory (StAR) gene. J. Endocrinol. 167, 253-263.
39. Comeau, L. A., Campana, S. E., Chouinard, G. A., and Hanson, J. M. (2001) Timing of Atlantic cod Gadus morhua seasonal migrations in relation to serum levels of gonadal and thyroidal hormones. Marine Ecol. Prog. Ser. 221, 245-253.
40. Dahle, R., Taranger, G. L., Karlsen, O., Kjesbu, O. S., and Norberg, B. (2003) Gonadal development and associated changes in liver size and sexual steroids during the reproductive cycle of captive male and female Atlantic cod (Gadus morhua L.). Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 136, 641-653.
41. Ankley, G. T., Jensen, K. M., Kahl, M. D., Korte, J. J., and Makynen, E. A. (2001) Description and evaluation of a short-term reproduction test with the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 20, 1276-1290.
42. Loomis, A. K., and Thomas, P. (2000) Effects of estrogens and xenoestrogens on androgen production by Atlantic croaker testes in vitro: Evidence for a nongenomic action mediated by an estrogen membrane receptor. Biol. Reprod. 62, 995-1004.
43. Borg, B. (1994) Androgens in teleosts fishes. Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 109, 219-245.
44. Rohr, D. H., Lokman, P. M., Davie, P. S., and Young, G. (2001) 11-Ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla australis. Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 130, 701-714.
45. Vendola, K., Zhou, J., Wang, J., Famuyiwa, O. A., Bievre, M., and Bondy, C. A. (1999) Androgens promote oocyte insulin-like growth factor I expression and initiation of follicle development in the primate ovary. Biol. Reprod. 61, 353-357.
46. Kortner, T. M., Rocha, E., Silva, P., Castro, F., and Arukwe, A. (2007) Genomic approach in evaluating the role of androgens on the growth of Atlantic cod (Gadus morhua) previtellogenic oocytes. BMC Genomics, submitted for publication.
47. Ho, S. M., Taylor, S., and Callard, I. P. (1982) Effect of hypophysectomy and growth hormone on estrogen-induced vitellogenesis in the freshwater turtle, Chrysemys picta. Gen. Comp. Endrocrinol. 48, 254-260.
48. Bieniarz, K., and Kime, D. E. (1986) Autoradiographic localization of gonadotrophin receptors in ovaries of the common carp, Cyprinus carpio L. Gen. Comp. Endrocrinol. 64, 151-156.
49. Tyler, C. R., and Sumpter, J. P. (1996) Oocyte growth and development in teleost. Rev. Fish Biol. Fish. 6, 287-318.
50. Van den Belt, K., Verheyen, R., and Witters, H. (2003) Comparison of vitellogenin responses in zebrafish and rainbow trout following exposure to environmental estrogens. Ecotoxicol. Environ. Saf. 56, 271-281.
51. Schultz, I. R., Skillman, A., Nicolas, J. M., Cyr, D. G., and Nagler, J. J. (2003) Short-term exposure to 17 alpha-ethynylestradiol decreases the fertility of sexually maturing male rainbow trout (Oncorhynchus mykiss). Environ. Toxicol. Chem. 22, 1272-1280.
52. Walsh, L. P., McCormick, C., Martin, C., and Stocco, D. M. (2000) Roundup inhibits steroidogenesis by disrupting steroidogenic acute regulatory (StAR) protein expression. Environ. Health Perspect. 108, 769-776.
53. Fukuzawa, N. H., Ohsako, S., Wu, Q., Sakaue, M., Fujii-Kuriyama, Y., Baba, T., and Tohyama, C. (2004) Testicular cytochrome P450scc and LHR as possible targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the mouse. Mol. Cell. Endocrinol. 221, 87-96.
54. Fukuzawa, N. H., Ohsako, S., Nagano, R., Sakaue, M., Baba, T., Aoki, Y., and Tohyama, C. (2003) Effects of 3,3′,4,4′,5-pentachlorobiphenyl, a coplanar polychlorinated biphenyl congener, on cultured neonatal mouse testis. Toxicol. in Vitro 17, 259-269.
55. Fairbrother, A., Smits, J., and Grasman, K. (2004) Avian immunotoxicology. J. Toxicol. Environ. Health, Part B 7, 105-137.
56. Rotchell, J. M., and Ostrander, G. K. (2003) Molecular markers of endocrine disruption in aquatic organisms. J. Toxicol. Environ. Health, Part B 6, 453-196.
57. Colborn, T., vom Saal, F. S., and Soto, A. M. (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect. 101, 378-384.
58. Guillette, L. J. J., Gross, T. S., Masson, G. R., Matter, J. M., Percival, H. F., and Woodward, A. R. (1994) Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 102, 680-688.
59. Orlando, E. F., Davis, W. P., and Guillette, L. J., Jr. (2002) Aromatase activity in the ovary and brain of the eastern mosquitofish (Gambusia holbrooki) exposed to paper mill effluent. Environ. Health Perspect. 110 (Suppl. 3), 429-433.