Multiple piscine vitellogenins: Biomarkers of fish exposure to estrogenic endocrine disruptors in aquatic environments

Marine Biology

Volumn 149, Issue 1, 2006, Pages 35-47

  Hiramatsu, Naoshi ^a   Matsubara, Takahiro ^b   Fujita, Toshiaki ^c   Sullivan, Craig V ^a   Hara, Akihiko ^c  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b FISHERIES RESEARCH AGENCY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AQUATIC ENVIRONMENT; BIOMARKER; FISH; POLLUTION EXPOSURE;

ANIMALIA; PISCES; VERTEBRATA;

EID: 33645557459     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-005-0214-z     Document Type: Article

References (88)

1. Aida K, Ngan PV, Hibiya T (1973) Physiological studies of gonadal maturation of fishes. I. Sexual differences in composition of plasma protein of ayu in relation to gonadal maturation. Bull Jpn Soc Sci Fish 39:1107-1115
2. Arcand-Hoy LD, Benson WH (1998) Fish reproduction: an ecologically relevant indicator of endocrine disruption. Environ Toxicol Chem 17:49-57
3. Arukwe A, Goksøyr 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 2:1-21
4. Bergink EW, Wallace RA (1974) Precursor-product relationship between amphibian vitellogenin and yolk proteins, lipovitellin and phosvitin. J Biol Chem 249:2897-2903
5. van-Bohemen CG, Lambert JGD, van Oordt PGWJ (1982) Vitellogenin induction by estradiol in estrone-primed rainbow trout, Salmo gairdneri. Gen Comp Endocrinol 46:136-139
6. Campbell CM, Idler DR (1980) Characterization of an estradiol-induced protein from rainbow trout as vitellogenin by the cross reactivity to ovarian yolk fractions. Biol Reprod 22:605-617
7. Carnevali O, Carletta R, Cambi A, Vita A, Bromage N (1999) Yolk formation and degradation during oocyte maturation in seabream, Sparus aurata: involvement of two lysosomal proteinases. Biol Reprod 60:140-146
8. Carnevali O, Mosconi G, Cambi A, Ridlfi S, Zanui S, Polzonetti-Magni AM (2001) Changes of lysosomal enzyme activities in sea bass Dicentrachus labrax egg and developing embryo. Aquaculture 202:249-256
9. Christmann JL, Grayson MJ, Huang RCC (1977) Comparative study of hen yolk phosvitin and plasma vitellogenin. Biochemistry 16:3250-3256
10. Daston GP, Cook JC, Kavlock RJ (2003) Uncertainties for endocrine disruptors: our view on progress. Toxicol Sci 74:245-252
11. Eckelbarger KJ, Davis CV (1996) Ultrastructure of the gonad and gametogenesis in the eastern oyster, Crassostrea virginica. (I) Ovary and oogenesis. Mar Biol 127:79-87
12. Emmersen BK, Petersen IM (1976) Natural occurrence and experimental induction by estradiol-17β, of a lipophosphoprotein (vitellogenin) in flounder (Platichthys flesus, L.). Comp Biochem Physiol 546:443-446
13. EPA (1998) Endocrine Disruptor Screening and Testing Advisory Committee (EDSTAC) Final Report. EPA/743/R-98/003, US Environmental Protection Agency, Washington, DC, August
14. EPA (2002) Draft study plan for the comparative evaluation of fathead minnow assays for detecting endocrine-disrupting chemicals, Washington, DC, February
15. Fagotto F (1995) Regulation of yolk degradation, or how to make sleepy lysosomes. J Cell Sci 108:3645-3647
16. Finn RN, Ostoby G, Norberg B, Fyhn HJ (2002) In vivo oocyte hydration in Atlantic halibut (Hippoglossus hippoglossus). Proteolytic liberation of free amino acids, and ion transport are driving forces of osmotic water influx. J Exp Biol 205:211-224
17. Folmer LC, Denslow ND, Rao V, Chow M, Crain DA, Enblom J, Marcino J, Guillette Jr LJ (1996) Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ Health Perspect 104:1096-1101
18. Fukada H, Haga A, Fujita T, Hiramatsu N, Sullivan CV, Hara A (2001) Development and validation of chemi-luminescent immunoassay for vitellogenin in five salmonid species. Comp Biochem Physiol 130A: 163-170
19. Giesy JP, Synder EM (1998) Xenobiotic modulation of endocrine function in fishes. In: Kendall RJ, Dickerson RL, Giesy JP, Suk WA (eds) Principles and processes for evaluating endocrine disruption in wildlife. SETAC Press, Florida, pp 155-237
20. Haga A, Fukada H, Fujita T, Hiramatsu N, Hara A (2001) Estimation of baseline vitellogenin level in male salmonid serum. In: Suzuki T, Masunaga S, Watanabe C (eds) Environmental science, vol 8. MYU, Tokyo, pp 197
21. Hara A, Hirai H (1976) Iron-binding activity of female-specific serum proteins of rainbow trout (Salmo gairdneri) and chum salmon (Oncorhynchus keta). Biochim Biophys Acta 437:549-557
22. Hara A, Hirai H (1978) Comparative studies on immunochemical properties of female-specific serum protein and egg yolk proteins in rainbow trout (Salmo gairdneri). Comp Biochem Physiol 59B:339-343
23. Hara A, Takano K, Hirai H (1983) Immunochemical identification of female-specific serum protein, vitellogenin, in the medaka, Oryzias latipes (Teleosts). Comp Biochem Physiol 76A:135-141
24. Kara A, Takemura A, Matsubara T, Takano K (1986) Immunochemical identification of female-specific serum proteins in a viviparous fish, the white-edged rockfish (Sebastes taczanowskii), during vitellogenesis and pregnancy, and after estrogen treatment. Bull Fac Fish Hokkaido Univ 37:101-110
25. Hartling RC, Kunkel JG (1999) Developmental fate of the yolk protein lipovitellin in embryos and larvae of winter flounder, Pleuronectes americanus. J Exp Zool 284:686-696
26. Hashimoto S, Bessho H, Hara A, Nakamura M, Iguchi T, Fujita K (2000) Elevated serum vitellogenin levels and gonadal abnormalities in wild male flounder (Pleuronectes yokohamae) from Tokyo Bay, Japan. Mar Environ Res 49:37-53
27. Hiramatsu N, Cheek AO, Sullivan CV, Matsubara T, Hara A (2005) Vitellogenesis and endocrine disruption. In: Mommsen TP, Moon TW (eds) Biochemistry and molecular biology of fishes, vol 6. Elsevier, Amsterdam, 562 pp
28. Hiramatsu N, Matsubara T, Weber GM, Sullivan CV, Hara A (2002a) Vitellogenesis in aquatic animals. Fish Sci 68 (Suppl I):694-699
29. Hiramatsu N, Hara A, Hiramatsu K, Fukada H, Weber GM, Denslow ND, Sullivan CV (2002b) Vitellogenin-derived yolk proteins of white perch, Morone americana: Purification, characterization and vitellogenin-receptor binding. Biol Reprod 67:655-667
30. Hiramatsu N, Ichikawa N, Fukada H, Fujita T, Sullivan CV, Hara A (2002c) Identification and characterization of proteases involved in specific proteolysis of vitellogenin and yolk proteins in salmonids. J Exp Zool 292:11-25
31. Hiramatsu N, Matsubara T, Hara A, Donato DM, Hiramatsu K, Denslow ND, Sullivan CV (2002d) Identification, purification and classification of multiple forms of vitellogenin from white perch (Morone americana). Fish Physiol Biochem 26:355-370
32. Hiramatsu N, Hiramatsu K, Hirano K, Hara A (2002e) Vitellogenin-derived yolk proteins in a hybrid sturgeon, bester (Huso huso x Acipencer luthenus): Identification, characterization and course of proteolysis during embryogenesis. Comp Biochem Physiol 131A:429-441
33. Heppell SA, Jackson LF, Weber GM, Sullivan CV (1999) Enzyme-linked immunosorbent assay (ELISA) of vitellogenin in temperate basses (Genus Morone): plasma and in vitro analysis. Trans Am Fish Soc 128:532-541
34. Heppell SA, Sullivan CV (1999) Gag (Mycteroperca microlepis) vitellogenin: purification, characterization and use for enzyme-linked immunosorbent assay (ELlSA) of female maturity in three species of grouper. Fish Physiol Biochem 20:361-374
35. Idler DR, Hwang SJ, Crim LW (1979) Quantification of vitellogenin in Atlantic salmon (Salmo salar) plasma by radioimmunoassay. J Fish Res Bd Can 36:574-578
36. Kime DE, Nash JP, Scott AP (1999) Vitellogenesis as a biomarker of reproductive disruption by xenobiotics. Aquaculture 177:345-352
37. Korte JJ, Mylchreest E, Ankley GT (2004) Comparative evaluation of ELISAs for detecting vitellogenin in the fathead minnow (Pimephales promelas) - a response to Tyler et al. Comp Biochem Physiol 138C:533-536
38. Kwon HC, Mugiya Y, Yamada J, Hara A (1990) Enzyme linked-immunosorbent assay (ELISA) of vitellogenin in white-spotted charr, Salvelinus leucomaenis. Bull Fac Fish Hokkaido Univ 41:241-259
39. +-ATPase in the hydration of Atlantic croaker and spotted seatrout oocytes during final maturation. J Exp Zool 258:126-136
40. LaFleur Jr GJ, Byrne BM, Kanungo J, Nelson LD, Greenberg RM, Wallace RA (1995a) Fundulus heteroclitus vitellogenin: the deduced primary structure of a piscine precursor to noncrystalline, liquid-phase yolk protein. J Mol Evol 41:505-521
41. LaFleur Jr GJ, Byrne BM, Haux C, Greenberg RM, Wallace RA (1995b) Liver-derived cDNAs: vitellogenin and vitelline envelope protein precursors (choriogenins). In: Goetz FW, Thomas P (eds) Proceedings of the fifth international symposium on the reproductive physiology of fish. University of Texas, Austin, pp 336-338
42. Larkin P, Knoebl I, Denslow ND (2003) Differential gene expression analysis in fish exposed to endocrine disrupting compounds. Comp Biochem Physiol 136B:149-161
43. Le Menn F (1979) Some aspects of vitellogenesis in a teleostean fish: Gobius niger L. Comp Biochem Physiol 62A:495-500
44. Maitre JL, Le Guellec C, Derrien S, Tenniswood M, Valotaire Y (1985) Measurement of vitellogenin from rainbow trout by rocket immunoelectrophoresis: application to the kinetic analysis of estrogen stimulation in the male. Can J Biochem Cell Biol 63:982-987
45. Marin GM, Matozzo V (2004) Vitellogenin induction as a biomarker of exposure to estorogenic compounds in aquatic environment. Mar Pollut Bull 48:835-839
46. Matsubara T, Koya Y (1997) Course of proteolytic cleavage in three classes of yolk proteins during oocyte maturation in barfin flounder (Verasper moseri). J Exp Zool 272:34-45
47. Matsubara T, Ohkubo N, Andoh T, Sullivan CV, Hara A (1999) Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost that spawns pelagic eggs. Dev Biol 213:18-32
48. Matsubara T, Nagae M, Ohkubo N, Andoh T, Sawaguchi S, Hiramatsu N, Sullivan CV, Hara A (2003) Multiple vitellogenins and their unique roles in marine teleosts. Fish Physiol Biochem 28:295-299
49. Mommsen TP, Walsh PJ (1988) Vitellogenesis and oocyte assembly. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XI A. Academic, New York, pp 347-406
50. Mylchreest E, Snajdr S, Korte JJ, Ankley GT (2003) Comparison of ELISAs for detecting vitellogenin in the fathead minnow (Pimephales promelas). Comp Biochem Physiol 134C:251-257
51. Nakada N, Nyunoya H, Nakamura M, Hara A, Iguchi T, Takada H (2004) Identification of estrogenic compounds in wastewater effluent. Environ Toxicol Chem 23:2807-2815
52. Nath P, Sundararaj BI (1981) Isolation and identification of female-specific serum lipophosphoprotein (vitellogenin) in the catfish, Heteropneustes fossilis. Gen Comp Endocrinol 43:184-190
53. Nunez Rodriguez J, Kah O, Geffard M, Le Menn F (1989) Enzyme-linked immunosorbent assay (ELISA) for sole (Soles vulgaris) vitellogenin. Comp Biochem Physiol 92B:741-746
54. OECD (2001) Guidelines for the testing of chemicals. Draft proposal for a new guideline: short-term reproductive test with the fathead minnow for identification of endocrine disrupting chemicals. OECD Environmental Health and Safety Publications
55. Ohkubo N, Mochida K, Adachi S, Hara A, Hotta K, Nakamura Y, Matsubara T (2003) Development of enzyme-linked immunosorbent assays (ELISAs) for two forms of vitellogenin in Japanese common goby (Acanthogobius flavimanus). Gen Comp Endocrinol 131:353-364
56. Okuzawa K (2002) Puberty in teleosts. Fish Physiol Biochem 26:31-41
57. Opresko LK, Wiley HS (1987) Receptor-mediated endocytosis in Xenopus oocytes. I. Characterization of the vitellogenin receptor system. J Biol Chem 262:4109-4115
58. Pait AS, Nelson JO (2002) Endocrine disruption in fish: an assessment of recent research and results. NOAA Tech Memo NOS NCCOS CCMA 149. Silver Spring, MD: NOAA, NOS, Center for Coastal Monitoring and Assessment, p 55
59. Palmer BD, Selcer KW (1996) Vitellogenin as a biomarker for xenobiotic estrogens: a review. In: Bengtson DA, Henshel DS(eds) Environmental toxicology and risk assessment: biomarkers and risk assessment, vol 5, ASTM STP 1306. American Society, Philadelphia, pp 3-21
60. Pan MJ, Bell WJ, Telfer WH (1969) Vitellogenic blood protein synthesis by insect fat body. Science 165:393-394
61. Parks LG, Cheek AO, Denslow ND, Heppell SA, McLachlan JA, LeBlanc GA, Sullivan CV (1999) Fathead minnow (Pimephales promelas) vitellogenin: purification, characterization and quantitative immunoassay for the detection of estrogenic compounds. Comp Biochem Physiol 123C: 113-125
62. Patiño R, Sullivan CV (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26:57-70
63. Pipe RK (1987) Oogenesis in the marine mussel Mytilus edulis: an ultrastructural study. Mar Biol 95:405-414
64. Plack PA, Pritchard DJ, Fraser NW (1971) Egg proteins in cod serum: natural occurrence and induction by injections of oestradiol 3-benzoate. Biochem J 121:847-856
65. Polzonetti-Magni AM, Mosconi G, Soverchia L, Kikuyama S, Carnevali O (2004) Multihormonal control of vitellogenesis in lower vertebrates. Int Rev Cytol 239:1-46
66. Purdom CE, Hardiman PA, Bye VJ, Eno NC, Tyler CR, Sumpter JP (1994) Estrogenic effects of effluents from sewage treatment works. Chem Ecol 8:275-285
67. Reith M, Munholland J, Kelly J, Finn RN, Fyhn HJ (2001) Lipovitellins derived from two forms of vitellogenin are differentially processed during oocyte maturation in haddock (Melanogrammus aeglefinus). J Exp Zool 291:58-67
68. Romano M, Rosanova P, Anteo C, Limatola E (2004) Vertebrate yolk proteins: a review. Mol Reprod Dev 69:109-118
69. Sawaguchi S, Koya Y, Yoshizaki N, Ohkubo N, Andoh T, Hiramatsu N, Sullivan CV, Hara A, Matsubara T (2005) Identification, characterization and cDNA cloning of three forms of vitellogenin, two general forms and a phosvitinless form, in a viviparous mosquitofish, Gambusia affinis. Biol Reprod 72:1045-1060
70. Selman K, Wallace RA (1989) Cellular aspects of oocyte growth in teleost. Zool Sci 6:211-231
71. Selman K, Wallace RA, Cerda J (2001) Bafilomysin A1 inhibits proteolytic cleavage of and hydration but not yolk crystal disassembly or meiosis during maturation of sea bass oocytes. J Exp Zool 290:265-278
72. Shen X, Steyrer E, Retzek H, Sanders EJ, Schneider WJ (1993) Chicken oocyte growth: receptor-mediated yolk deposition. Cell Tissue Res 272:459-471
73. Shimizu M, Fujiwara Y, Fukada H, Hara A (2002) Purification and identification of a second form of vitellogenin from ascites of medaka (Oryzias latipes) treated with estrogen. J Exp Zool 293:726-735
74. Specker JL, Anderson TR (1994) Developing an ELISA for a model protein-vitellogenin. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 3. Analytical techniques. Elsevier, Amsterdam, pp 567-578
75. Specker JL, Sullivan CV (1994) Vitellogenesis in fishes: status and perspectives. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. National Research Council, Ottawa, pp 304-315
76. Stifani S, Le Menn F, Rodriguez JN, Schneider WJ (1990) Regulation of oogenesis: the piscine receptor for vitellogenin. Biochem Biophys Acta 1045:271-279
77. Sullivan CV, Hiramatsu N, Kennedy AM, Clark RW, Weber GM, Matsubara T, Kara A (2003) Induced maturation and spawning: opportunities and applications for research on oogenesis. Fish Physiol Biochem 28:481-486
78. Sumpter JP (1997) Environmental control of fish reproduction: a different perspective. Fish Physiol Biochem 17:25-31
79. Takemura A, Kim BH (2001) Effects of estradiol-17β treatment on in vitro and in vivo synthesis of two distinct vitellogenins in tilapia. Comp Biochem Physiol 129A:641-651
80. Trichet V, Buisine N, Mouchel N, Moran P, Pendas AM, Le Pennec JP, Wolff J (2000) Genomic analysis of the vitellogenin locus in rainbow trout (Oncorhynchus mykiss) reveals a complex history of gene amplification and retroposon activity. Mol Gen Genet 263:828-837
81. Tyler CR, van der Eerden B, Jobling S, Panter G, Sumpter JP (1996) Measurement of vitellogenin, a biomarker for exposure to estrogenic chemicals, in a wide variety of cyprinid fish. J Comp Physiol B 166:418-426
82. Tyler CR, Santos EM, Prat F (1999) Unscrambling the egg-cellular, biochemical, molecular and endocrine advances in oogenesis. In: Norberg B, Kjesbu OS, Taranger GL, Anderson E, Stefansson SO (eds) Proceedings of sixth international symposium on the reproductive physiology of fish. Institute of Marine Research and University of Bergen, Bergen, pp 237-280
83. Tyler CR, van Aerle R, Santos EM (2004) ELISAs for detecting vitellogenin in the fathead minnow (Pimephales promelas) - a critical analysis. Response to Mylchreest et al., Comp Biochem Physiol C 134:251-257,
84. Tyler CR, van Aerle R, Santos EM Comp Biochem Physiol C 2003, 138C:531-532
85. Wallace RA (1985) Vitellogenesis and oocyte growth in nonmammalian vertebrates. In: Browder LW (ed) Developmental biology, vol 1. Plenum Press, New York, pp 127-177
86. Wang H, Yan T, Tan JTT, Gong ZA (2000) Zebrafish vitellogenin gene (vg3) encodes a novel vitellogenin without a phosvitin domain and may represent a primitive vertebrate vitellogenin gene. Gene 256:303-310
87. Yoshizaki N, Yonezawa S (1998) Cysteine proteinase play a key role for the initiation of yolk digestion during development of Xenopus laevis. Dev Growth Differ 40:659-667
88. Zhang F, Bartels MJ, Brodeur JC, Woodburn KB (2004) Quantitative measurement of fathead minnow vitellogenin by liquid chromatography combined with tandem mass spectrometry using a signature peptide of vitellogenin. Envion Toxicol Chem 23:1408-1415