Advertisement

Fish Physiology and Biochemistry

, Volume 35, Issue 3, pp 377–384 | Cite as

Effects of the estrogen mimic genistein as a dietary component on sex differentiation and ethoxyresorufin-O-deethylase (EROD) activity in channel catfish (Ictalurus punctatus)

  • C. C. Green
  • A. M. Kelly
Article

Abstract

A number of aquaculture species, including channel catfish Ictalurus punctatus, are fed high proportions of soybean meal in their diet. We have investigated the potential for the most common phytoestrogen in soybean meal to alter phenotypic sex during sexual differentiation in channel catfish. Channel catfish were fed four dietary concentrations of the phytoestrogen genistein (0, 2, 4, and 8 mg g−1) to determine its effect on gonadal sex differentiation. The four treatment diets were fed to sexually undifferentiated channel catfish between 5 and 140 days post hatch (dph) and between 60 and 150 dph. Phenotypic sex was determined by histological examination of the gonads. Ethoxyresorufin-O-deethylase activity was not significantly different among the treatment and control groups. Phenotypic sex was significantly dependant on dietary phytoestrogen concentration (P = 0.01). Additionally, logistic regression showed a significant relation between genistein concentration in the diet and gonadal sex (P = 0.02). Intersex individuals were present at all treatment concentrations, with increasing proportions of intersex fish as the genistein concentration increased for individuals fed treated diets between 5 and 140 dph. Increased proportions of phenotypically male individuals resulted from chronic dietary exposure to the estrogen mimic genistein. There were no significant differences in the proportions of males and females between feed treatment durations. These findings establish that dietary concentrations of genistein can alter sex ratios in cultured channel catfish populations and demonstrates the need to further understand the actions of this and other prominent phytoestrogens in aquaculture species.

Keywords

Aromatase Endocrine disruption Intersex Phytoestrogens Soybean meal 

Notes

Acknowledgements

This article is based, in part, upon research conducted by the senior author for the Doctor of Philosophy degree in the Department of Zoology, Fisheries and Illinois Aquaculture Center, Southern Illinois University Carbondale, Carbondale, Illinois. Funding was provided by grant #2-02149 from The Office of Research and Development Administration at Southern Illinois University Carbondale with additional funding provided by the Department of Zoology and the Fisheries and Illinois Aquaculture Center, Southern Illinois University Carbondale.

References

  1. Bennetau-Pelissero C, Brenton BB, Bennetau B et al (2001) Effect of genistein-enriched diets on the endocrine process of gametogenesis and on reproduction efficiency of the rainbow trout Oncorhynchus mykiss. Gen Comp Endocrinol 121:173–187. doi: 10.1006/gcen.2000.7585 PubMedCrossRefGoogle Scholar
  2. Boonyaratpalin A, Suraneiranat P, Tunpibal T (1998) Replacement of fish meal with various types of soybean products in diets for the Asian seabass, Lates calcarifer. Aquaculture 161:67–78. doi: 10.1016/S0044-8486(97)00257-3 CrossRefGoogle Scholar
  3. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi: 10.1016/0003-2697(76)90527-3 PubMedCrossRefGoogle Scholar
  4. Brooks JD, Thompson LU (2005) Mammalian lignans and genistein decrease the activities of aromatase and 17β-hydroxysteroid dehydrogenase in MCF-7 cells. J Steroid Biochem 94:461–467. doi: 10.1016/j.jsbmb.2005.02.002 CrossRefGoogle Scholar
  5. Burison BK, Hartmann A, Lister A et al (2003) A toxicity identification evaluation approach to studying estrogenic substances in hog manure and agriculture runoff. Environ Toxicol Chem 22:2243–2250. doi: 10.1897/02-437 CrossRefGoogle Scholar
  6. Chan HY, Wang H, Leung LK (2003) The red clover (Trifolium pretense) isoflavones biochanin A modulates the biotransformation pathways of 7, 12-imethylbenz[a]anthracene. Br J Nutr 90:87–92. doi: 10.1079/BJN2003868 PubMedCrossRefGoogle Scholar
  7. Chun HS, Chang HJ, Choi EH et al (2005) Molecular and absorbtion properties of 12 soy isoflavones and their structure-activity relationship with selected biological activities. Biotechnol Lett 27:1105–1111. doi: 10.1007/s10529-005-8457-9 PubMedCrossRefGoogle Scholar
  8. Davis KB, Simco BA, Goudie CA et al (1990) Hormonal sex manipulation and evidence for female homogamety in channel catfish. Gen Comp Endocrinol 78:218–223. doi: 10.1016/0016-6480(90)90008-A PubMedCrossRefGoogle Scholar
  9. Davis KB, Goudie CA, Simco BA et al (1992) Influence of dihydrotestosterone on sex determination in channel catfish and blue catfish: period of developmental sensitivity. Gen Comp Endocrinol 86:147–151. doi: 10.1016/0016-6480(92)90136-8 PubMedCrossRefGoogle Scholar
  10. Eldridge AC, Kwolek WF (1983) Soybean isoflavones: effect of environmental and variety on composition. J Agric Food Chem 31:394–396. doi: 10.1021/jf00116a052 PubMedCrossRefGoogle Scholar
  11. Forlano PM, Bass AH (2005) Steroid regulation of brain aromatase expression in gila: female preoptic and vocal motor nuclei. J Neurobiol 65:50–58. doi: 10.1002/neu.20178 PubMedCrossRefGoogle Scholar
  12. Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227. doi: 10.1016/S0044-8486(01)00526-9 CrossRefGoogle Scholar
  13. Galvez JI, Mazik PM, Phelps RP et al (1995) Masculinization of channel catfish Ictalurus punctatus by oral administration of trenbolone acetate. J World Aquacult Soc 26:378–383. doi: 10.1111/j.1749-7345.1995.tb00832.x CrossRefGoogle Scholar
  14. Goudie CA, Redner BD, Simco BA et al (1983) Feminization of channel catfish by oral administration of steroid sex hormones. Trans Am Fish Soc 112:670–672. doi :10.1577/1548-8659(1983)112<670:FOCCBO>2.0.CO;2CrossRefGoogle Scholar
  15. Ibarreta D, Daxenberger A, Meyer HHD (2001) Possible health impact of phytoestrogens and xenoestrogens in food. Acta Pathol Microbiol Immunol Scand 109:161–184Google Scholar
  16. Ishibashi H, Kobayashi M, Koshiishi T et al (2002) Induction of plasma vitellogenin synthesis by the commercial fish diets in male goldfish (Carassius auratus) and dietary phytoestrogens. J Health Sci 48:427–434. doi: 10.1248/jhs.48.427 CrossRefGoogle Scholar
  17. Kikuchi K (1999) Use of defatted soybean meal as a substitute for fish meal in diets of Japanese flounder (Paralichthys olivaceus). Aquaculture 179:3–11. doi: 10.1016/S0044-8486(99)00147-7 CrossRefGoogle Scholar
  18. Kiparissis Y, Hughes R, Metcalfe C et al (2001) Identification of the isoflavonoid genistein in bleached kraft mill effluent. Environ Sci Technol 35:2423–2427. doi: 10.1021/es001679+ PubMedCrossRefGoogle Scholar
  19. Kiparissis Y, Balch GC, Metcalfe TL et al (2003) Effects of the isoflavones genistein and equol on the gonadal development of Japanese medaka (Oryzias latipes). Environ Health Perspect 111:1158–1163PubMedGoogle Scholar
  20. Larsson DG, Hällman H, Förlin L (2000) More male fish embryos near a pulp mill. Environ Toxicol Chem 19:2911–2917. doi :10.1897/1551-5028(2000)019<2911:MMFENA>2.0.CO;2CrossRefGoogle Scholar
  21. Latonnelle K, Fostier A, Le Menn F et al (2002) Binding affinities of hepatic nuclear estrogen receptors for phytoestrogens in rainbow trout (Oncorhynchus mykiss) and Siberian sturgeon (Acipenser baeri). Gen Comp Endocrinol 129:69–79. doi: 10.1016/S0016-6480(02)00512-9 PubMedCrossRefGoogle Scholar
  22. Levine SL, Oris JT (1999) Enhancement of acute parathion toxicity to fathead minnows following pre-exposure to propiconazole. Pestic Biochem Physiol 65:102–109. doi: 10.1006/pest.1999.2434 CrossRefGoogle Scholar
  23. MacLatchy DL, Van Der Kraak GJ (1995) The phytoestrogen b-sitosterol alters the reproductive endocrine status of goldfish. Toxicol Appl Pharmacol 134:305–312. doi: 10.1006/taap.1995.1196 PubMedCrossRefGoogle Scholar
  24. Mambrini M, Roem AJ, Cravèdi JP et al (1999) Effects of replacing fish meal with soy protein concentrate and of DL-methionine supplementation in high energy, extruded diets on the growth and nutrient utilization of rainbow trout, Oncorhynchus mykiss. J Anim Sci 77:2990–2999PubMedGoogle Scholar
  25. Pasmanik M, Schlincer BA, Callard GV (1988) In vivo steroid regulation of aromatase and 5-alpha-reductase in goldfish brain and pituitary. Gen Comp Endocrinol 71:175–182. doi: 10.1016/0016-6480(88)90308-5 PubMedCrossRefGoogle Scholar
  26. Patiňo R, Davis KB, Shoore JE et al (1996) Sex differentiation of channel catfish gonads: normal development and effects of temperature. J Exp Zool 276:209–218. doi :10.1002/(SICI)1097-010X(19961015)276:3<209::AID-JEZ5>3.0.CO;2-RCrossRefGoogle Scholar
  27. Pelissero C, Bennetau B, Babin P et al (1991) The estrogenic activity of certain phytoestrogens in the Siberian sturgeon Acipenser baeri. J Steroid Biochem Mol Biol 38:293–299. doi: 10.1016/0960-0760(91)90100-J PubMedCrossRefGoogle Scholar
  28. Rondán M, Hernández MD, Egea MA et al (2004) Effects of fishmeal replacement with soybean meal as protein source, and protein replacement with carbohydrates as an alternative energy source on sharpsnout sea bream, Diplodus puntazzo, fatty acid profile. Aquacult Res 35:1220–1228. doi: 10.1111/j.1365-2109.2004.01130.x CrossRefGoogle Scholar
  29. Ronis MJ, Ingelman-Sundberg J, Badger T (1994) Induction, suppression and inhibition of multiple hepatic cytochrome P450 isozymes in male rat and bobwhite quail (Colinus virginianus) by ergosterol biosynthesis inhibiting compounds. Toxicol Appl Pharmacol 44:1953–1965Google Scholar
  30. Setchell KD, Cassidy A (1999) Dietary isoflavones: biological effects and relevance to human health. J Nutr 129:758S–767SPubMedGoogle Scholar
  31. Shon YH, Park SD, Nam KS (2006) Effective chemopreventive activity of genistein against human breast cancer cells. Biochem Mol Biol 39:448–451Google Scholar
  32. Spengler P, Wolfgang K, Metzger JW (2001) Substances with estrogenic activity in effluents of sewage treatment plants in southwestern Germany. 1. Chemical analysis. Environ Toxicol Chem 20:2133–2141. doi :10.1897/1551-5028(2001)020<2133:SWEAIE>2.0.CO;2PubMedCrossRefGoogle Scholar
  33. Tidwell JH, Allan GL (2001) Fish as food: aquaculture’s contribution. EMBO Rep 2:958–963. doi: 10.1093/embo-reports/kve236 PubMedCrossRefGoogle Scholar
  34. Tzchori I, Degani G, Elisha R et al (2004) The influence of phytoestrogens and oestradiol-17β on growth and sex determination in the European eel (Anguilla anguilla). Aquacult Res 35:1213–1219. doi: 10.1111/j.1365-2109.2004.01129.x CrossRefGoogle Scholar
  35. Wang HJ, Murphy PA (1994) Isoflavone composition of American and Japanese soybeans in Iowa: effects of variety, crop year, and location. J Agric Food Chem 1994:1674–1677. doi: 10.1021/jf00044a017 CrossRefGoogle Scholar
  36. Whyte JJ, Jung RE, Schmitt CJ et al (2000) Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev Toxicol 30:347–570. doi: 10.1080/10408440091159239 PubMedCrossRefGoogle Scholar
  37. Willett KL, McDonald SJ, Steinberg MA et al (1997) Biomarker sensitivity for PAH contamination in two marine fish species collected in Galveston Bay, Texas. Environ Toxicol Chem 16:1472–1479. doi :10.1897/1551-5028(1997)016<1472:BSFPAH>2.3.CO;2CrossRefGoogle Scholar
  38. Willett KL, Gardinali PR, Lienesch LA et al (2000) Comparative metabolism and excretion of benzo(a)pyrene in 2 species of ictalurid catfish. Toxicol Sci 58:68–76. doi: 10.1093/toxsci/58.1.68 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of Zoology, Fisheries and Illinois Aquaculture CenterSouthern Illinois UniversityCarbondaleUSA
  2. 2.Aquaculture Research StationLouisiana State University Agricultural CenterBaton RougeUSA
  3. 3.Cooperative Extension Program, Aquaculture and Fisheries CenterUniversity of Arkansas at Pine BluffLonokeUSA

Personalised recommendations