Prochloraz-induced oocyte maturation in rainbow trout (Oncorhynchus mykiss), a molecular and functional analysis

Toxicological Sciences

Volumn 118, Issue 1, 2010, Pages 61-70

  Rime, Hélène ^a   Nguyen, Thaovi ^a   Bobe, Julien ^a   Fostier, Alexis ^a   Monod, Gilles ^a  

^a Campus de Beaulieu   (France)

Author keywords

Fish; Fungicide; Imidazole; Meiosis; Oocyte; Reproduction

Indexed keywords

17,20BETA DIHYDROXYPREGN 4 EN 3 ONE; CONNEXIN 43; CYCLOHEXIMIDE; DACTINOMYCIN; FRESH WATER; LUTEINIZING HORMONE; PROCHLORAZ; SOMATOMEDIN; SOMATOMEDIN B; TRILOSTANE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE INDUCTION; GERMINAL VESICLE; IN VITRO STUDY; MEIOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE; PARACRINE SIGNALING; RAINBOW TROUT; REPRODUCTIVE TOXICITY; VITELLOGENESIS;

ANIMALS; CYCLOHEXIMIDE; DACTINOMYCIN; DIHYDROTESTOSTERONE; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; FEMALE; FUNGICIDES, INDUSTRIAL; HYDROXYPROGESTERONES; IMIDAZOLES; LUTEINIZING HORMONE; ONCORHYNCHUS MYKISS; OOCYTES; OVARY; OVULATION; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; WATER POLLUTANTS, CHEMICAL;

ONCORHYNCHUS MYKISS; TELEOSTEI;

EID: 77958495191     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq255     Document Type: Article

References (61)

1. Andersen, H. R., Vinggaard, A. M., Rasmussen, T. H., Gjermandsen, I. M., and Bonefeld-Jorgensen, E. C. (2002). Effects of currently used pesticides in assays for estrogenicity, androgenicity, and aromatase activity in vitro. Toxicol. Appl. Pharmacol. 179, 1-12.
2. Ankley, G. T., Bencic, D. C., Cavallin, J. E., Jensen, K. M., Kahl, M. D., Makynen, E. A., Martinovic, D., Mueller, N. D., Wehmas, L. C., and Villeneuve, D. L. (2009). Dynamic nature of alterations in the endocrine system of fathead minnows exposed to the fungicide prochloraz. Toxicol. Sci. 112, 344-353.
3. Ankley, G. T., Jensen, K. M., Durhan, E. J., Makynen, E. A., Butterworth, B. C., Kahl, M. D., Villeneuve, D. L., Linnum, A., Gray, L. E., Cardon, M., et al. (2005). Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fathead minnow (Pimephales promelas). Toxicol. Sci. 86, 300-308.
4. Babin, M., Casado, S., Chana, A., Herradon, B., Segner, H., Tarazona, J. V., and Navas, J. M. (2005). Cytochrome P4501A induction caused by the imidazole derivative Prochloraz in a rainbow trout cell line. Toxicol. In Vitro 19, 899-902.
5. Berndtson, A. K., and Chen, T. T. (1994). Two unique CYP1 genes are expressed in response to 3-methylcholanthrene treatment in rainbow trout. Arch. Biochem. Biophys. 310, 187-195.
6. Bobe, J., Maugars, G., Nguyen, T., Rime, H., and Jalabert, B. (2003). Rainbow trout follicular maturational competence acquisition is associated with an increased expression of follicle stimulating hormone receptor and insulin-like growth factor 2 messenger RNAs. Mol. Reprod. Dev. 66, 46-53.
7. Bobe, J., Montfort, J., Nguyen, T., and Fostier, A. (2006). Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays. Reprod. Biol. Endocrinol. 4, 39.
8. Bobe, J., Nguyen, T., and Fostier, A. (2009). Ovarian function of the trout preovulatory ovary: new insights from recent gene expression studies. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 153, 63-68.
9. Bobe, J., Nguyen, T., and Jalabert, B. (2004). Targeted gene expression profiling in the rainbow trout (Oncorhynchus mykiss) ovary during maturational competence acquisition and oocyte maturation. Biol. Reprod. 71, 73-82.
10. Bruzzone, R., White, T. W., Yoshizaki, G., Patino, R., and Paul, D. L. (1995). Intercellular channels in teleosts: functional characterization of two connexins from Atlantic croaker. FEBS Lett. 358, 301-304.
11. Cao, Z., Hong, J., Peterson, R. E., and Aiken, J. M. (2000). Characterization of CYP1A1 and CYP1A3 gene expression in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 49, 101-109.
12. Carnevali, O., Tosti, L., Speciale, C., Peng, C., Zhu, Y., and Maradonna, F. (2010). DEHP impairs zebrafish reproduction by affecting critical factors in oogenesis. PLoS One 5, e10201.
13. Cravedi, J. P., Boudry, G., Baradat, M., Rao, D., and Debrauwer, L. (2001). Metabolic fate of 2,4-dichloroaniline, prochloraz and nonylphenol diethox-ylate in rainbow trout: a comparative in vivo/in vitro approach. Aquat. Toxicol. 53, 159-172.
14. Finn, R. N. (2007). The physiology and toxicology of salmonid eggs and larvae in relation to water quality criteria. Aquat. Toxicol. 81, 337-354.
15. Fostier, A., Breton, B., Jalabert, B., and Marcuzzi, O. (1981a). Evolution des niveaux plasmatiques de la gonadotropine glycoprotéique et de la 17-alpha-hydroxy-20 beta-dihydroprogesterone au cours de la maturation et de l'ovulation chez la truite arc-en-ciel, Salmo gairdnerii. C. R. Acad. Sci. III Sci. Vie 293, 817-820.
16. Fostier, A., and Jalabert, B. (1986). Steroidogenesis in rainbow trout (Salmo gairdneri) at various preovulatory stages: changes in plasma hormone levels and in vivo and in vitro responses of the ovary to salmon gonadotropin. Fish Physiol. Biochem. 2, 87-99.
17. Fostier, A., Jalabert, B., Campbell, C., Terqui, M., and Breton, B. (1981b). Cinétique de libération in vitro de 17 alpha hydroxy-20Beta dihydroproges-térone par des follicules de Truite arc-en-ciel, Salmo gairdnerii. C. R. Acad. Sci. Paris. III Sci. Vie 292, 777-780.
18. Fostier, A., Jalabert, B., and Terqui, M. (1973). Predominant action of a hydroxylated derivative of progesterone on the in vitro maturation of ovocytes of the rainbow trout (Salmo gairdneri). C. R. Acad. Sci. Paris 277, 421-424.
19. Gohin, M., Bobe, J., and Chesnel, F. (2010). Comparative transcriptomic analysis of follicle-enclosed oocyte maturational and developmental competence acquisition in two non-mammalian vertebrates. BMC Genomics 11, 18.
20. Govoroun, M. S., Huet, J. C., Pernollet, J. C., and Breton, B. (1997). Use of immobilized metal ion affinity chromatography and dye-ligand chromatography for the separation and purification of rainbow trout pituitary gonadotropins, GTH I and GTH II. J. Chromatogr. B Biomed. Sci. Appl. 698, 35-46.
21. Hajnik, C. A., Goetz, F. W., Hsu, S. Y., and Sokal, N. (1998). Characterization of a ribonucleic acid transcript from the brook trout (Salvelinus fontinalis) ovary with structural similarities to mammalian adipsin/complement factor D and tissue kallikrein, and the effects of kallikrein-like serine proteases on follicle contraction. Biol. Reprod. 58, 887-897.
22. Hansson, M. C., Wittzell, H., Persson, K., and von Schantz, T. (2004). Unprecedented genomic diversity of AhR1 and AhR2 genes in Atlantic salmon (Salmo salar L.). Aquat. Toxicol. 68, 219-232.
23. Hegelund, T., and Celander, M. C. (2003). Hepatic versus extrahepatic expression of CYP3A30 and CYP3A56 in adult killifish (Fundulus heteroclitus). Aquat. Toxicol. 64, 277-291.
24. Hinfray, N., Porcher, J. M., and Brion, F. (2006). Inhibition of rainbow trout (Oncorhynchus mykiss) P450 aromatase activities in brain and ovarian microsomes by various environmental substances. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 144, 252-262.
25. Jalabert, B. (1975). Modulation of 17-alpha-hydroxy-20 beta-dihydroprogesterone or gonadotropic extract activity on the in vitro intrafollicular maturation of rainbow trout (Salmo gairdnerii) oocytes by various steroids lacking maturing activity. C R Acad. Sci. Hebd. Seances Acad. Sci. D 281, 811-814.
26. Jalabert, B. (1976). In vitro oocyte maturation and ovulation in rainbow trout (Salmo gairdneri), northern pike (Esox lucius), and goldfish (Carassius auratus). J. Fish. Res. Board Can. 33, 974-988.
27. Jalabert, B., and Fostier, A. (1984a). The follicular sensitivity in vitro to maturation-inducing hormones in rainbow trout, Salmo gairdneri: role of oestradiol-17β. Aqua 43, 1-11.
28. Jalabert, B., and Fostier, A. (1984b). The modulatory effect in vitro of oestradiol-17b, testosterone or cortisol on the output of 17a-hydroxy-20b-dihydroprogesterone by rainbow trout (Salmo gairdneri) ovarian follicles stimulated by the maturational gonadotropin s-GtH. Reprod. Nutr. Dev. 24, 127-136.
29. Kagawa, H., Kobayashi, M., Hasegawa, Y., and Aida, K. (1994a). Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. Gen. Comp. Endocrinol. 95, 293-300.
30. Kagawa, H., Tanaka, H., Okuzawa, K., and Hirose, K. (1994b). Development of maturational competence of oocytes of red seabream, Pagrus major, after human chorionic gonadotropin treatment in vitro requires RNA and protein synthesis. Gen. Comp. Endocrinol. 94, 199-206.
31. Kahle, M., Buerge, I. J., Hauser, A., Muller, M. D., and Poiger, T. (2008). Azole fungicides: occurrence and fate in wastewater and surface waters. Environ. Sci. Technol. 42, 7193-7200.
32. Kamangar, B. B., Gabillard, J. C., and Bobe, J. (2006). Insulin-like growth factor-binding protein (IGFBP)-1, -2, -3, -4, -5, and -6 and IGFBP-related protein 1 during rainbow trout postvitellogenesis and oocyte maturation: molecular characterization, expression profiles, and hormonal regulation. Endocrinology 147, 2399-2410.
33. Karchner, S. I., Powell, W. H., and Hahn, M. E. (1999). Identification and functional characterization of two highly divergent aryl hydrocarbon receptors (AHR1 and AHR2) in the teleost Fundulus heteroclitus. Evidence for a novel subfamily of ligand-binding basic helix loop helix-Per-ARNT-Sim (bHLH-PAS) factors. J. Biol. Chem. 274, 33814-33824.
34. Kreuger, J. (1998). Pesticides in stream water within an agricultural catchment in southern Sweden, 1990-1996. Sci. Total Environ. 216, 227-251.
35. Kronvang, B., Laubel, A., Larsen, S. E., and Friberg, N. (2003). Pesticides and heavy metal in Danish streambed sediment. Hydrobiologia 494, 93-101.
36. Le Gac, F., Thomas, J. L., Mourot, B., and Loir, M. (2001). In vivo and in vitro effects of prochloraz and nonylphenol ethoxylates on trout spermatogenesis. Aquat. Toxicol. 53, 187-200.
37. Lee, S. J., Wang-Buhler, J. L., Cok, I., Yu, T. S., Yang, Y. H., Miranda, C. L., Lech, J., and Buhler, D. R. (1998). Cloning, sequencing, and tissue expression of CYP3A27, a new member of the CYP3A subfamily from embryonic and adult rainbow trout livers. Arch. Biochem. Biophys. 360, 53-61.
38. Mason, J. I., Carr, B. R., and Murry, B. A. (1987). Imidazole antimycotics: selective inhibitors of steroid aromatization and progesterone hydroxylation. Steroids 50, 179-189.
39. Monod, G., de Mones, A., and Fostier, A. (1993). Inhibition of ovarian microsomal aromatase and follicular oestradiol secretion by imidazole fungicides in rainbow trout. Mar. Environ. Res. 35, 135-157.
40. Monod, G., Rime, H., Bobe, J., and Jalabert, B. (2004). Agonistic effect of imidazole and triazole fungicides on in vitro oocyte maturation in rainbow trout (Oncorhynchus mykiss). Mar. Environ. Res. 58, 143-146.
41. Mourot, B., Nguyen, T., Fostier, A., and Bobe, J. (2006). Two unrelated putative membrane-bound progestin receptors, progesterone membrane receptor component 1 (PGMRC1) and membrane progestin receptor (mPR) beta, are expressed in the rainbow trout oocyte and exhibit similar ovarian expression patterns. Reprod. Biol. Endocrinol. 4, 6.
42. Nagahama, Y., and Adachi, S. (1985). Identification of maturation-inducing steroid in a teleost, the amago salmon (Oncorhynchus rhodurus). Dev. Biol. 109, 428-435.
43. Pocar, P., Perazzoli, F., Luciano, A. M., and Gandolfi, F. (2001). In vitro reproductive toxicity of polychlorinated biphenyls: effects on oocyte maturation and developmental competence in cattle. Mol. Reprod. Dev. 58, 411-416.
44. Tanaka, M., Telecky, T. M., Fukada, S., Adachi, S., Chen, S., and Nagahama, Y. (1992). Cloning and sequence analysis of the cDNA encoding P-450 aromatase (P450arom) from a rainbow trout (Oncorhynchus mykiss) ovary; relationship between the amount of P450arom mRNA and the production of oestradiol-17 beta in the ovary. J. Mol. Endocrinol. 8, 53-61.
45. Tchoudakova, A., Kishida, M., Wood, E., and Callard, G. V. (2001). Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J. Steroid Biochem. Mol. Biol. 78, 427-439.
46. Thomas, P. (2008). Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front. Neuroendocrinol. 29, 292-312.
47. Tokumoto, T., Tokumoto, M., Horiguchi, R., Ishikawa, K., and Nagahama, Y. (2004). Diethylstilbestrol induces fish oocyte maturation. Proc. Natl. Acad. Sci. U.S.A 101, 3686-3690.
48. Villeneuve, D. L., Ankley, G. T., Makynen, E. A., Blake, L. S., Greene, K. J., Higley, E. B., Newsted, J. L., Giesy, J. P., and Hecker, M. (2007). Comparison of fathead minnow ovary explant and H295R cell-based steroidogenesis assays for identifying endocrine-active chemicals. Ecotoxicol. Environ. Saf. 68, 20-32.
49. Villeneuve, D. L., Blake, L. S., Brodin, J. D., Cavallin, J. E., Durhan, E. J., Jensen, K. M., Kahl, M. D., Makynen, E. A., Martinovic, D., Mueller, N. D., et al. (2008). Effects of a 3beta-hydroxysteroid dehydrogenase inhibitor, trilostane, on the fathead minnow reproductive axis. Toxicol. Sci. 104, 113-123.
50. Vinggaard, A. M., Breinholt, V., and Larsen, J. C. (1999). Screening of selected pesticides for oestrogen receptor activation in vitro. Food Addit. Contam. 16, 533-542.
51. Vinggaard, A. M., Hass, U., Dalgaard, M., Andersen, H. R., Bonefeld-Jorgensen, E., Christiansen, S., Laier, P., and Poulsen, M. E. (2006). Prochloraz: an imidazole fungicide with multiple mechanisms of action. Int. J. Androl. 29, 186-192.
52. Vinggaard, A. M., Hnida, C., Breinholt, V., and Larsen, J. C. (2000). Screening of selected pesticides for inhibition of CYP19 aromatase activity in vitro. Toxicol. In Vitro 14, 227-234.
53. Vinggaard, A. M., Nellemann, C., Dalgaard, M., Jorgensen, E. B., and Andersen, H. R. (2002). Antiandrogenic effects in vitro and in vivo of the fungicide prochloraz. Toxicol. Sci. 69, 344-353.
54. Weber, G. M., and Sullivan, C. V. (2000). Effects of insulin-like growth factor-I on In vitro final oocyte maturation and ovarian steroidogenesis in striped bass, Morone saxatilis. Biol. Reprod. 63, 1049-1057.
55. Weber, G. M., and Sullivan, C. V. (2005). Insulin-like growth factor-I induces oocyte maturational competence but not meiotic resumption in white bass (Morone chrysops) follicles in vitro: evidence for rapid evolution of insulin-like growth factor action. Biol. Reprod. 72, 1177-1186.
56. Weber, L. P., Diamond, S. L., Bandiera, S. M., and Janz, D. M. (2002). Expression of HSP70 and CYP1A protein in ovary and liver of juvenile rainbow trout exposed to beta-naphthoflavone. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 131, 387-394.
57. Weber, L. P., and Janz, D. M. (2001). Effect of beta-naphthoflavone and dimethylbenz[a]anthracene on apoptosis and HSP70 expression in juvenile channel catfish (Ictalurus punctatus) ovary. Aquat. Toxicol. 54, 39-50.
58. Yamauchi, M., Kim, E. Y., Iwata, H., and Tanabe, S. (2005). Molecular characterization of the aryl hydrocarbon receptors (AHR1 and AHR2) from red seabream (Pagrus major). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 141, 177-187.
59. Yoshizaki, G., Patino, R., and Thomas, P. (1994). Connexin messenger ribonucleic acids in the ovary of Atlantic croaker: molecular cloning and characterization, hormonal control, and correlation with appearance of oocyte maturational competence. Biol. Reprod. 51, 493-503.
60. Zhang, X., Hecker, M., Tompsett, A. R., Park, J. W., Jones, P. D., Newsted, J., Au, D., Kong, R., Wu, R. S., and Giesy, J. P. (2008). Responses of the medaka HPG axis PCR array and reproduction to prochloraz and ketoconazole. Environ. Sci. Technol. 42, 6762-6769.
61. Zhou, H., Qu, Y., Wu, H., Liao, C., Zheng, J., Diao, X., and Xue, Q. (2010). Molecular phylogenies and evolutionary behavior of AhR (aryl hydrocarbon receptor) pathway genes in aquatic animals: implications for the toxicology mechanism of some persistent organic pollutants (POPs). Chemosphere 78, 193-205.