A computational model for asynchronous oocyte growth dynamics in a batch-spawning fish

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 68, Issue 9, 2011, Pages 1528-1538

  Li, Zhenhong ^a   Villeneuve, Daniel L ^b   Jensen, Kathleen M ^b   Ankley, Gerald T ^b   Watanabe, Karen H ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSORPTION; ANDROGEN; BIOCHEMISTRY; BIOINDICATOR; BIOLOGICAL DEVELOPMENT; CLUTCH SIZE; CYPRINID; ECOTOXICOLOGY; ENDOCRINE DISRUPTOR; GERM CELL; GROWTH MODELING; METABOLITE; POLLUTION EFFECT; POLLUTION EXPOSURE; PROTEIN; SPAWNING;

PIMEPHALES PROMELAS;

EID: 80052545188     PISSN: 0706652X     EISSN: 12057533     Source Type: Journal    
DOI: 10.1139/f2011-066     Document Type: Article

References (41)

1. Ankley, G.T., and Villeneuve, D.L. 2006. The fathead minnow in aquatic toxicology: past, present and future. Aquat. Toxicol. 78(1): 91-102. doi:10.1016/j.aquatox.2006.01.018. PMID:16494955.
2. 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(6): 1276-1290. PMID:11392137.
3. Ankley, G.T., Kahl, M.D., Jensen, K.M., Hornung, M.W., Korte, J.J., Makynen, E.A., and Leino, R.L. 2002. Evaluation of the aromatase inhibitor fadrozole in a short-term reproduction assay with the fathead minnow (Pimephales promelas). Toxicol. Sci. 67(1): 121-130. doi:10.1093/toxsci/67.1.121. PMID:11961225.
4. Ankley, G.T., Jensen, K.M., Makynen, E.A., Kahl, M.D., Korte, J.J., Hornung, M.W., Henry, T.R., Denny, J.S., Leino, R.L., Wilson, V. S., Cardon, M.C., Hartig, P.C., and Gray, L.E. 2003. Effects of the androgenic growth promoter 17-beta-trenbolone on fecundity and reproductive endocrinology of the fathead minnow. Environ. Toxicol. Chem. 22(6): 1350-1360. doi:10.1002/etc.5620220623. PMID:12785594.
5. Ankley, G.T., Jensen, K.M., Durhan, E.J., Makynen, E.A., Butter-worth, B.C., Kahl, M.D., Villeneuve, D.L., Linnum, A., Gray, L.E., Cardon, M., and Wilson, V.S. 2005a. Effects of two fungicides with multiple modes of action on reproductive endocrine function in the fathead minnow (Pimephales promelas). Toxicol. Sci. 86(2): 300-308. doi:10.1093/toxsci/kfi202. PMID:15901916.
6. Ankley, G.T., Kuehl, D.W., Kahl, M.D., Jensen, K.M., Linnum, A., Leino, R.L., and Villeneuve, D.A. 2005b. Reproductive and developmental toxicity and bioconcentration of perfluorooctane-sulfonate in a partial life-cycle test with the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 24(9): 2316-2324. doi:10.1897/04-634R.1. PMID:16193761.
7. Ankley, G.T., Jensen, K.M., Kahl, M.D., Makynen, E.A., Blake, L.S., Greene, K.J., Johnson, R.D., and Villeneuve, D.L. 2007. Ketoconazole in the fathead minnow (Pimephales promelas): reproductive toxicity and biological compensation. Environ. Toxicol. Chem. 26(6): 1214-1223. doi:10.1897/06-428R.1. PMID:17571688.
8. Ankley, G.T., Bencic, D.C., Breen, M.S., Collette, T.W., Conolly, R.B., Denslow, N.D., Edwards, S.W., Ekman, D.R., Garcia-Reyero, N., Jensen, K.M., Lazorchak, J.M., Martinovic, D., Miller, D.H., Perkins, E.J., Orlando, E.F., Villeneuve, D.L., Wang, R.-L., and Watanabe, K.H. 2009a. Endocrine disrupting chemicals in fish: developing exposure indicators and predictive models of effects based on mechanism of action. Aquat. Toxicol. 92(3): 168-178. doi:10.1016/j.aquatox.2009.01.013. PMID:19261338.
9. 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. 2009b. Dynamic nature of alterations in the endocrine system of fathead minnows exposed to the fungicide prochloraz. Toxicol. Sci. 112(2): 344-353. doi:10.1093/toxsci/ kfp227. PMID:19767443.
10. Bois, F.Y., and Maszle, D.R. 1997. MCSim: a Monte Carlo simulation program. J. Stat. Softw. 2(9): 1-56.
11. Coward, K., and Bromage, N.R. 1998. Histological classification of oocyte growth and the dynamics of ovarian recrudescence in Tilapia zillii. J. Fish Biol. 53(2): 285-302. doi:10.1111/j.1095-8649.1998.tb00981.x.
12. Durhan, E.J., Lambright, C.S., Makynen, E.A., Lazorchak, J., Hartig, P.C., Wilson, V.S., Gray, L.E., and Ankley, G.T. 2006. Identification of metabolites of trenbolone acetate in androgenic runoff from a beef feedlot. Environ. Health Perspect. 114(S-1): 65-68. doi:10. 1289/ehp.8055. PMID:16818248.
13. Forbes, V.E., Palmqvist, A., and Bach, L. 2006. The use and misuse of biomarkers in ecotoxicology. Environ. Toxicol. Chem. 25(1): 272-280. doi:10.1897/05-257R.1. PMID:16494252.
14. Gilbert, S.F. 2000. Developmental biology. Sinauer Associates, Sunderland, Massachusetts.
15. Hirao, Y., and Miyano, T. 2008. In vitro growth of mouse oocytes: oocyte size at the beginning of culture influences the appropriate length of culture period. J. Mammal. Ova Res. 25(1): 56-62. doi:10.1274/jmor.25.56.
16. Jensen, K.M., Korte, J.J., Kahl, M.D., Pasha, M.S., and Ankley, G.T. 2001. Aspects of basic reproductive biology and endocrinology in the fathead minnow (Pimephales promelas). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 128(1): 127-141. doi:10.1016/S1532-0456(00)00185-X. PMID:11166681.
17. Jensen, K.M., Kahl, M.D., Makynen, E.A., Korte, J.J., Leino, R.L., Butterworth, B.C., and Ankley, G.T. 2004. Characterization of responses to the antiandrogen flutamide in a short-term reproduction assay with the fathead minnow. Aquat. Toxicol. 70(2): 99-110. doi:10.1016/j.aquatox.2004.06.012. PMID:15522428.
18. Jensen, K.M., Makynen, E.A., Kahl, M.D., and Ankley, G.T. 2006. Effects of the feedlot contaminant 17alpha-trenbolone on reproductive endocrinology of the fathead minnow. Environ. Sci. Technol. 40(9): 3112-3117. doi:10.1021/es052174s. PMID: 16719119.
19. Kim, J., Hayton, W.L., and Schultz, I.R. 2006. Modeling the brain-pituitary-gonad axis in salmon. Mar. Environ. Res. 62(Suppl. 1): S426-S432. doi:10.1016/j.marenvres.2006.04.022. PMID: 16716390.
20. Leino, R.L., Jensen, K.M., and Ankley, G.T. 2005. Gonadal histology and characteristic histopathology associated with endocrine disruption in the adult fathead minnow (Pimephales promelas). Environ. Toxicol. Pharmacol. 19(1): 85-98. doi:10.1016/j.etap. 2004.05.010.
21. Li, Z., Kroll, K., Jensen, K.M., Villeneuve, D.L., Ankley, G.T., Brian, J.V., Sepulveda, M.S., Orlando, E.F., Lazorchak, J.M., Kostich, M., Armstrong, B., Denslow, N.D., and Watanabe, K.H. 2011. A computational model of the hypothalamic-pituitary-gonadal axis in female fathead minnows (Pimephales promelas) exposed to 17alpha-ethynylestradiol and 17beta-trenbolone. BMC Syst. Biol. 5(1): 63. doi:10.1186/1752-0509-5-63. PMID:21545743.
22. Milla, S., Jalabert, B., Rime, H., Prunet, P., and Bobe, J. 2006. Hydration of rainbow trout oocyte during meiotic maturation and in vitro regulation by 17,20b-dihydroxy-4-pregnen-3-one and cortisol. J. Exp. Biol. 209(6): 1147-1156. doi:10.1242/jeb. 02094. PMID:16513941.
23. Miller, D.H., Jensen, K.M., Villeneuve, D.L., Kahl, M.D., Makynen, E.A., Durhan, E.J., and Ankley, G.T. 2007. Linkage of biochemical responses to population-level effects: a case study with vitellogenin in the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 26(3): 521-527. doi:10.1897/06-318R.1. PMID:17373517.
24. Murphy, C.A., Rose, K.A., Rahman, M.S., and Thomas, P. 2009. Testing and applying a fish vitellogenesis model to evaluate laboratory and field biomarkers of endocrine disruption in Atlantic croaker (Micropogonias undulatus) exposed to hypoxia. Environ. Toxicol. Chem. 28(6): 1288-1303. doi:10.1897/08-304.1. PMID: 19642826.
25. Nagahama, Y., Yoshikuni, M., Yamashita, M., Tokumoto, T., and Katsu, Y. 1995. Regulation of oocyte growth and maturation in fish. Curr. Top. Dev. Biol. 30: 103-145. doi:10.1016/S0070-2153 (08)60565-7. PMID:7555044.
26. Perazzolo, L.M., Coward, K., Davail, B., Normand, E., Tyler, C.R., Pakdel, F., Schneider, W.J., and Le Menn, F. 1999. Expression and localization of messenger ribonucleic acid for the vitellogenin receptor in ovarian follicles throughout oogenesis in the rainbow trout, Oncorhynchus mykiss. Biol. Reprod. 60(5): 1057-1068. doi:10.1095/biolreprod60.5.1057. PMID:10208965.
27. Schulz, R.W., Vischer, H.F., Cavaco, J.E., Santos, E.M., Tyler, C.R., Goos, H.J., and Bogerd, J. 2001. Gonadotropins, their receptors, and the regulation of testicular functions in fish. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129(2-3): 407-417. doi:10.1016/ S1096-4959(01)00339-6. PMID:11399475.
28. Seki, M., Fujishima, S., Nozaka, T., Maeda, M., and Kobayashi, K. 2006. Comparison of response to 17b-estradiol and 17b-trenbolone among three small fish species. Environ. Toxicol. Chem. 25(10): 2742-2752. doi:10.1897/05-647R.1. PMID: 17022416.
29. Specker, J.L., and Sullivan, C.V. 1994. Vitellogenesis in fishes: status and perspectives. In Perspectives in comparative endocrinology. Edited by K.G. Davey, R.E. Peter, and S.S. Tobe. National Research Council of Canada, Ottawa, Canada. pp. 304-315.
30. Tyler, C.R., and Sumpter, J.P. 1996. Oocyte growth and development in teleosts. Rev. Fish Biol. Fish. 6(3): 287-318. doi:10.1007/ BF00122584.
31. Tyler, C.R., Sumpter, J.P., and Bromage, N.R. 1988. In vivo ovarian uptake and processing of vitellogenin in the rainbow trout, Salmo gairdneri. J. Exp. Zool. 246(2): 171-179. doi:10.1002/jez. 1402460209.
32. Tyler, C.R., Sumpter, J.P., and Witthames, P.R. 1990. The dynamics of oocyte growth during vitellogenesis in the rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 43(2): 202-209. doi:10. 1095/biolreprod43.2.202. PMID:2378932.
33. Tyler, C.R., Pottinger, T.G., Santos, E., Sumpter, J.P., Price, S.A., Brooks, S., and Nagler, J.J. 1996. Mechanisms controlling egg size and number in the rainbow trout, Oncorhynchus mykiss. Biol. Reprod. 54(1): 8-15. doi:10.1095/biolreprod54.1.8. PMID: 8837994.
34. Villeneuve, D.L., Murphy, M.B., Kahl, M.D., Jensen, K.M., Butterworth, B.C., Makynen, E.A., Durhan, E.J., Linnum, A., Leino, R.L., Curtis, L.R., Giesy, J.P., and Ankley, G.T. 2006. Evaluation of the methoxytriazine herbicide prometon using a short-term fathead minnow reproduction test and a suite of in vitro bioassays. Environ. Toxicol. Chem. 25(8): 2143-2153. doi:10.1897/05-604R.1. PMID:16916034.
35. Villeneuve, D.L., Miracle, A.L., Jensen, K.M., Degitz, S.J., Kahl, M.D., Korte, J.J., Greene, K.J., Blake, L.S., Linnum, A.L., and Ankley, G.T. 2007. Development of quantitative real-time PCR assays for fathead minnow (Pimephales promelas) gonadotropin b subunit mRNAs to support endocrine disruptor research. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 145(2): 171-183. doi:10.1016/j.cbpc.2006.11.003. PMID:17236816.
36. Villeneuve, D.L., Mueller, N.D., Martinovic, D., Makynen, E.A., Kahl, M.D., Jensen, K.M., Durhan, E.J., Cavallin, J.E., Bencic, D., and Ankley, G.T. 2009. Direct effects, compensation, and recovery in female fathead minnows exposed to a model aromatase inhibitor. Environ. Health Perspect. 117(4): 624-631. PMID: 19440503.
37. Villeneuve, D.L., Garcia-Reyero, N., Martinovic, D., Mueller, N.D., Cavallin, J.E., Durhan, E.J., Makynen, E.A., Jensen, K.M., Kahl, M.D., Blake, L.S., Perkins, E.J., and Ankley, G.T. 2010. I. Effects of a dopamine receptor antagonist on fathead minnow, Pimephales promelas, reproduction. Ecotoxicol. Environ. Saf. 73(4): 472-477. doi:10.1016/j.ecoenv.2009.09.007. PMID:19783049.
38. Wallace, R.A., and Selman, K. 1981. Cellular and dynamic aspects of oocyte growth in teleosts. Am. Zool. 21(2): 325-343. doi:10.1093/ icb/21.2.325.
39. Watanabe, K.H., Jensen, K.M., Orlando, E.F., and Ankley, G.T. 2007. What is normal? A characterization of the values and variability in reproductive endpoints of the fathead minnow, Pimephales promelas. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 146: 348-356. doi:10.1016/j.cbpc.2007.04.015. PMID:17600770.
40. Wolf, J.C., Dietrich, D.R., Friederich, U., Caunter, J., and Brown, A.R. 2004. Qualitative and quantitative histomorphologic assessment of fathead minnow Pimephales promelas gonads as an endpoint for evaluating endocrine-active compounds: a pilot methodology study. Toxicol. Pathol. 32(5): 600-612. doi:10. 1080/01926230490515201. PMID:15603544.
41. Yaron, Z., Gur, G., Melamed, P., Rosenfeld, H., Elizur, A., and Levavi-Sivan, B. 2003. Regulation of fish gonadotropins. Int. Rev. Cytol. 225: 131-185. doi:10.1016/S0074-7696(05)25004-0. PMID:12696592.