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Fish Physiology and Biochemistry

, Volume 40, Issue 1, pp 279–294 | Cite as

Purification and partial characterization of vitellogenin from spotted wolffish (Anarhichas minor) and development of an enzyme-linked immunosorbent assay for the determination of gender and sexual maturity

  • Domynick Maltais
  • Bernard-Antonin Dupont-Cyr
  • Robert L. Roy
  • Nathalie R. Le François
Article

Abstract

Keywords

Vitellogenin Spotted wolffish Purification Stability Storage ELISA 

Notes

Acknowledgments

This work was financially supported by the Aquaculture Collaborative Research and Development Program, the AquaNet Centre of Excellence, of Fisheries and Oceans Canada, and the Ministère de l’Agriculture, des Pêcheries et de l’Alimentation du Québec. We thank Andréane Bernier, Arianne Savoie, and Tony Grenier as well as the CAMGR staff for their technical assistance. We thank two anonymous reviewers whose comments improved the manuscript.

References

  1. Babin PJ (1987) Apolipoproteins and the association of egg-yolk proteins with plasma high-density-lipoproteins after ovulation and follicular atresia in the rainbow trout (Salmo gairdneri). J Biol Chem 262:4290–4296PubMedGoogle Scholar
  2. Barrero M, Small BC, D’Abramo LR, Hanson LA, Kelly AM (2007) Comparison of estradiol, testosterone, vitellogenin and cathepsin profiles among young adult channel catfish (Ictalurus punctatus) females from four selectively bred strains. Aquaculture 264:390–397CrossRefGoogle Scholar
  3. Benfey TJ, Donaldson EM, Owen TG (1989) An homologous radioimmunoassay for coho salmon (Oncorhynchus kisutch) vitellogenin, with general applicability to other pacific salmonids. Gen Comp Endocr 75:78–82PubMedCrossRefGoogle Scholar
  4. Bon E, Barbe U, Rodriguez JN, Cuisset B, Pelissero C, Sumpter JP, Lemenn F (1997) Plasma vitellogenin levels during the annual reproductive cycle of the female rainbow trout (Oncorhynchus mykiss): Establishment and validation of an ELISA. Comp Biochem Physiol 117B:75–84CrossRefGoogle Scholar
  5. Brasfield SM, Weber LP, Talent LG, Janz DM (2002) Dose-response and time course relationships for vitellogenin induction in male western fence lizards (Sceloporus occidentalis) exposed to ethinylestradiol. Environ Toxicol Chem 21:1410–1416PubMedCrossRefGoogle Scholar
  6. Brion F, Rogerieux F, Noury P, Migeon B, Flammarion P, Thybaud E, Porcher JM (2000) Two-step purification method of vitellogenin from three teleost fish species: rainbow trout (Oncorhynchus mykiss), gudgeon (Gobio gobio) and chub (Leuciscus cephalus). J Chromatogr B 737:3–12CrossRefGoogle Scholar
  7. Brodeur JC, Woodburn KB, Zhang F, Bartels MJ, Klecka GM (2006) Plasma sampling and freezing procedures influence vitellogenin measurements by enzyme-linked immunoassay in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 25:337–348PubMedCrossRefGoogle Scholar
  8. Brown MA, Carne A, Chambers GK (1997) Purification, partial characterization and peptide sequences of vitellogenin from a reptile, the tuatara (Sphenodon punctatus). Comp Biochem Physiol 117B:159–168CrossRefGoogle Scholar
  9. Cheek AO, King VW, Burse JR, Borton DL, Sullivan CV (2004) Bluegill (Lepomis macrochirus) vitellogenin: purification and enzyme-linked immunosorbent assay for detection of endocrine disruption by papermill effluent. Comp Biochem Physiol 137C:249–260Google Scholar
  10. Covens M, Covens L, Ollevier F, Deloof A (1987) A comparative study of some properties of vitellogenin (Vg) and yolk proteins in a number of fresh-water and marine teleost fishes. Comp Biochem Physiol 88B:75–80Google Scholar
  11. De Vlaming V, Wiley HS, Delahunty G, Wallace RA (1980) Goldfish (Carassius auratus) vitellogenin: induction, isolation, properties and relationship to yolk proteins. Comp Biochem Physiol 67B:613–623Google Scholar
  12. Dupont-Cyr B-A (2012) Compression du cycle reproducteur du loup de mer (Anarchichas lupus et A. minor). M.Sc thesis, Université Laval. http://www.theses.ulaval.ca/2012/28684/28684.pdf
  13. Falk-Petersen IB, Hansen TK, Fieler R, Sunde LM (1999) Cultivation of the spotted wolf fish Anarhichas minor (Olafsen)—a new candidate for cold-water fish farming. Aquac Res 30:711–718CrossRefGoogle Scholar
  14. Foss A, Imsland AK, Falk-Petersen IB, Oiestad V (2004) A review of the culture potential of spotted wolffish Anarhichas minor Olafsen. Rev Fish Biol Fisher 14:277–294CrossRefGoogle Scholar
  15. Fukada H, Fujiwara Y, Takahashi T, Hiramatsu N, Sullivan CV, Hara A (2003) Carp (Cyprinus carpio) vitellogenin: purification and development of a simultaneous chemiluminescent immunoassay. Comp Biochem Physiol 134A:615–623CrossRefGoogle Scholar
  16. Guzmán JM, Norberg B, Ramos J, Mylonas CC, Mañanós EL (2008) Vitellogenin, steroid plasma levels and spawning performance of cultured female Senegalese sole (Solea senegalensis). Gen Comp Endocr 156:285–297PubMedCrossRefGoogle Scholar
  17. Heppell SA, Sullivan CV (1999) Gag (Mycteroperca microlepis) vitellogenin: purification, characterization and use for enzyme-linked immunosorbent assay (ELISA) of female maturity in three species of grouper. Fish Physiol Biochem 20:361–374CrossRefGoogle Scholar
  18. Heppell SA, Denslow ND, Folmar LC, Sullivan CV (1995) Universal assay of vitellogenin as a biomarker for environmental estrogens. Environ Health Perspect 103:9–15PubMedCentralPubMedGoogle Scholar
  19. Hiramatsu N, Matsubara T, Weber GM, Sullivan CV, Hara A (2002) Vitellogenesis in aquatic animals. Fish Sci 68(Suppl I):694–699Google Scholar
  20. Inaba K, Buerano CC, Natividad FF, Morisawa M (1997) Degradation of vitellogenins by 170 kDa trypsin-like protease in the plasma of the tilapia, Oreochromis niloticus. Comp Biochem Physiol 118B:85–90CrossRefGoogle Scholar
  21. Jena B, Mohanty J, Das RC, Garnayak SK, Nandi S (2012) Induction, purification and partial characterization of vitellogenin in an Indian major carp Catla catla (Ham.). Aquac Res 1–11 http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2109.2012.03195.x/pdf. Acessed 25 Jan 2013
  22. Kime DE, Tveiten H (2002) Unusual motility characteristics of sperm of the spotted wolffish. J Fish Biol 61:1549–1559CrossRefGoogle Scholar
  23. King JL, Jukes TH (1969) Non-darwinian evolution. Science 164:788–798PubMedCrossRefGoogle Scholar
  24. Kirby MF, Allen YT, Dyer RA, Feist SW, Katsiadaki I, Matthiessen P, Scott AP, Smith A, Stentiford GD, Thain JE, Thomas KV, Tolhurst L, Waldock MJ (2004) Surveys of plasma vitellogenin and intersex in male flounder (Platichthys flesus) as measures of endocrine disruption by estrogenic contamination in United Kingdom estuaries: temporal trends, 1996 to 2001. Environ Toxicol Chem 23:748–758PubMedCrossRefGoogle Scholar
  25. Kishida M, Specker JL (1993) Vitellogenin in tilapia (Oreochromis mossambicus)—induction of 2 forms by estradiol, quantification in plasma and characterization in oocyte extract. Fish Physiol Biochem 12:171–182PubMedCrossRefGoogle Scholar
  26. Kohn YY, Lokman PM, Lilimnik A, Symonds JE (2013) Sex identification in captive hapuku (Polyprion oxygeneios) using ultrasound imagery and plasma levels of vitellogenin and se steroids. Aquaculture 384–387:87–93CrossRefGoogle Scholar
  27. Kokokiris L, Le Menn F, Kentouri M, Kagara M, Fostier A (2001) Seasonal cycle of gonadal development and serum levels of vitellogenin of the red porgy, Pagrus pagrus (Teleostei: Sparidae). Mar Biol 139:549–559CrossRefGoogle Scholar
  28. Le Francois NR, Lemieux H, Blier PU (2002) Biological and technical evaluation of the potential of marine and anadromous fish species for cold-water mariculture. Aquac Res 33:95–108CrossRefGoogle Scholar
  29. Le Francois NR, Tveiten H, Halfyard LC, Foss A (2010) The wolffishes (Family: Anarhichadidae). In: Le Francois NR, Jobling M, Carter C, Blier PU (eds) Finfish aquaculture diversification. CAB International, Wallingford, pp 417–431CrossRefGoogle Scholar
  30. Lomax DP, Roubal WT, Moore JD, Johnson LL (1998) An enzyme-linked immunosorbent assay (ELISA) for measuring vitellogenin in English sole (Pleuronectes vetulus): development, validation and cross-reactivity with other pleuronectids. Comp Biochem Physiol 121B:425–436CrossRefGoogle Scholar
  31. Maltais D, Roy RL (2007) A lateral flow immunoassay for rapid evaluation of vitellogenin levels in plasma and surface mucus of the copper redhorse (Moxostoma hubbsi). Environ Toxicol Chem 26:1672–1676PubMedCrossRefGoogle Scholar
  32. Maltais D, Roy RL (2009) Purification and partial characterization of vitellogenin from shorthead redhorse (Moxostoma macrolepidotum) and copper redhorse (Moxostoma hubbsi) and detection in plasma and mucus with a heterologous antibody. Fish Physiol Biochem 35:241–254PubMedCrossRefGoogle Scholar
  33. Maltais D, Roy RL, Couillard CM (2010) Hybrid ELISAs for vitellogenins of the endangered copper redhorse Moxostoma hubbsi and the shorthead redhorse Moxostoma macrolepidotum (Cypriniformes, catostomidae). Ecotoxicol Environ Saf 73:883–892PubMedCrossRefGoogle Scholar
  34. Mañanós E, Zanuy S, Le MF, Carrillo M, Núñez J (1994) Sea bass (Dicentrarchus labrax L.) vitellogenin. 1. Induction, purification and partial characterization. Comp Biochem Physiol 107B:205–216Google Scholar
  35. 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 28:295–299CrossRefGoogle Scholar
  36. Methven DA, Crim LW, Norberg B, Brown JA, Goff GP, Huse I (1992) Seasonal reproduction and plasma levels of sex steroids and vitellogenin in Atlantic halibut (Hippoglossus hippoglossus). Can J Fish Aquat Sci 49:754–759CrossRefGoogle Scholar
  37. Mommsen TP, Walsh PJ (1988) Vitellogenesis and oocyte assembly. In: Hoar WS, Randall DJ, Donaldson EM (eds) Reproduction. Endocrine tissues and hormones. Fish physiology, vol 9A. Academic Press, New York, pp 347–406Google Scholar
  38. Mosconi G, Carnevali O, Carletta R, Nabissi M, Polzonetti-Magni AM (1998) Gilthead seabream (Sparus aurata) vitellogenin: purification, partial characterization, and validation of an enzyme-linked immunosorbent assay (ELISA). Gen Comp Endocr 110:252–261PubMedCrossRefGoogle Scholar
  39. Ndiaye P, Forgue J, Lamothe V, Cauty C, Tacon P, Lafon P, Davail B, Fostier A, Le Menn F, Núñez J (2006) Tilapia (Oreochromis niloticus) vitellogenins: development of homologous and heterologous ELISAs and analysis of vitellogenin pathway through the ovarian follicle. J Exp Zool Part A 305:576–593CrossRefGoogle Scholar
  40. Ng BT, Idler DR (1983) Yolk formation and differentiation in teleost fishes. In: Hoar WS, Randall DJ, Donaldson EM (eds) Reproduction. Endocrine tissues and hormones. Fish physiology, vol 9A. Academic Press, New York, pp 373–404CrossRefGoogle Scholar
  41. Nilsen BM, Berg K, Arukwe A, Goksoyr A (1998) Monoclonal and polyclonal antibodies against fish vitellogenin for use in pollution monitoring. Mar Environ Res 46:153–157CrossRefGoogle Scholar
  42. Norberg B (1995) Atlantic halibut (Hippoglossus hippoglossus) vitellogenin: induction, isolation and partial characterization. Fish Physiol Biochem 14:1–13PubMedCrossRefGoogle Scholar
  43. Norberg B, Haux C (1985) Induction, isolation and a characterization of the lipid content of plasma vitellogenin from two Salmo species: rainbow trout (Salmo gairdneri) and sea trout (Salmo trutta). Comp Biochem Physiol 81B:869–876Google Scholar
  44. Norberg B, Haux C (1988) An homologous radioimmunoassay for brown trout (Salmo trutta) vitellogenin. Fish Physiol Biochem 5:59–68PubMedCrossRefGoogle Scholar
  45. Nuñez Rodriguez J, Kah O, Geffard M, Lemenn F (1989) Enzyme-linked immunosorbent-assay (Elisa) for sole (Solea vulgaris) vitellogenin. Comp Biochem Physiol 92B:741–746Google Scholar
  46. Nuñez Rodriguez J, Dugue R, Oteme ZJ, Hem S, Lemenn F (1997) Vitellogenin plasma levels in two cultured African catfish species, Chrysichthys nigrodigitatus (Claroteidae) and Heterobranchus longifilis (Clariidae). Aquat Living Resour 10:231–238CrossRefGoogle Scholar
  47. Palumbo AJ, Linares-Casenave J, Jewell W, Doroshov SI, Tjeerdema RS (2007) Induction and partial characterization of California halibut (Paralichthys californicus) vitellogenin. Comp Biochem Physiol 146A:200–207CrossRefGoogle Scholar
  48. Palumbo AJ, Koivunen M, Tjeerdema RS (2009) Optimization and validation of a California halibut environmental estrogen bioassay using a heterologous ELISA. Sci Total Environ 407:953–961PubMedCrossRefGoogle Scholar
  49. 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:113–125Google Scholar
  50. Peck KA, Lomax DP, Olson OP, Sol SY, Swanson P, Johnson LL (2011) Development of an enzyme-linked immunosorbent assay for quantifying vitellogenin in pacific salmon and assessment of field exposure to environmental estrogens. Environ Toxicol Chem 30:477–486PubMedCrossRefGoogle Scholar
  51. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org
  52. Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22Google Scholar
  53. Roubal WT, Lomax DP, Willis ML, Johnson LL (1997) Purification and partial characterization of English sole (Pleuronectes vetulus) vitellogenin. Comp Biochem Physiol 118B:613–622CrossRefGoogle Scholar
  54. Roy RL, Morin Y, Courtenay SC, Robichaud P (2004) Purification of vitellogenin from smooth flounder (Pleuronectes putnami) and measurement in plasma by homologous ELISA. Comp Biochem Physiol 139B:235–244CrossRefGoogle Scholar
  55. Schafhauser-Smith D, Benfey TJ (2001) The purification and development of a quantitative enzyme linked immunosorbent assay (ELISA) for the measurement of vitellogenin in diploid and triploid brook trout (Salvelinus fontinalis). Fish Physiol Biochem 24:287–298CrossRefGoogle Scholar
  56. Selman K, Wallace RA (1983) Oogenesis in Fundulus heteroclitus. III. Vitellogeniesis. J Exp Zool 226:441–457PubMedCrossRefGoogle Scholar
  57. Silversand C, Haux C (1989) Isolation of turbot (Scophthalmus maximus) vitellogenin by high-performance anion-exchange chromatography. J Chromatogr 478:387–397PubMedGoogle Scholar
  58. Silversand C, Hyllner SJ, Haux C (1993) Isolation, immunochemical detection, and observations of the instability of vitellogenin from four teleosts. J Exp Zool 267:587–597CrossRefGoogle Scholar
  59. Specker JL, Sullivan CV (1994) Vitellogenesis in fishes: status and perspectives. Perspectives in comparative endocrinology. National Research Council Canada, Ottawa, pp 304–315Google Scholar
  60. Sumpter JP, Scott AP, Baynes SM, Witthames PR (1984) Early stages of the reproductive-cycle in virgin female rainbow-trout (Salmo-Gairdneri Richardson). Aquaculture 43:235–242CrossRefGoogle Scholar
  61. Susca V, Corriero A, Bridges CR, De Metrio G (2001) Study of the sexual maturity of female bluefin tuna: purification and partial characterization of vitellogenin and its use in an enzyme-linked immunosorbent assay. J Fish Biol 58:815–831CrossRefGoogle Scholar
  62. Tao Y, Hara A, Hodson RG, Woods L III, Sullivan CV (1993) Purification, characterization and immunoassay of striped bass (Morone saxatilis) vitellogenin. Fish Physiol Biochem 12:31–46PubMedCrossRefGoogle Scholar
  63. Templeman W (1986) Contribution to biology of the spotted wolffish (Anarhichas minor) in the Northwest Atlantic. J North Atl Fish Sci 7:47–55CrossRefGoogle Scholar
  64. Tyler CR, Sumpter JP (1990) The purification and partial characterization of carp, Cyprinus carpio, vitellogenin. Fish Physiol Biochem 8:111–120PubMedCrossRefGoogle Scholar
  65. Tyler CR, Sumpter JP (1996) Oocyte growth and development in teleosts. Rev Fish Biol Fisher 6:287–318CrossRefGoogle Scholar
  66. Tyler CR, van der Eerden B, Jobling S, Panter G, Sumpter JP (1996) Measurement of vitellogenin, a biomarker for exposure to oestrogenic chemicals, in a wide variety of cyprinid fish. J Comp Physiol 166:418–426CrossRefGoogle Scholar
  67. Tyler CR, van Aerle R, Hutchinson TH, Maddix S, Trip H (1999) An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin. Environ Toxicol Chem 18:337–347CrossRefGoogle Scholar
  68. Tyler CR, van Aerle R, Nilsen MV, Blackwell R, Maddix S, Nilsen BM, Berg K, Hutchinson TH, Goksøyr A (2002) Monoclonal antibody enzyme-linked immunosorbent assay to quantify vitellogenin for studies on environmental estrogens in the rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 21:47–54PubMedCrossRefGoogle Scholar
  69. Vega-Lopez AN, Martinez-Tabche L, Dominguez-Lopez ML, Garcia-Latorre E, Ramon-Gallegos E, Garcia-Gasca A (2006) Vitellogenin induction in the endangered goodeid fish Girardinichthys viviparus: vitellogenin characterization and estrogenic effects of polychlorinated biphenyls. Comp Biochem Physiol 142C:356–364Google Scholar
  70. Watts M, Pankhurst NW, Pryce A, Sun B (2003) Vitellogenin isolation, purification and antigenic cross-reactivity in three teleost species. Comp Biochem Physiol 134B:467–476CrossRefGoogle Scholar
  71. Yao Z, Crim LW (1996) A biochemical characterization of vitellogenins isolated from the marine fish ocean pout (Macrozoarces americanus L.), lumpfish (Cyclopterus lumpus) and Atlantic cod (Gadus morhua). Comp Biochem Physiol 113B:247–253CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Domynick Maltais
    • 1
  • Bernard-Antonin Dupont-Cyr
    • 2
  • Robert L. Roy
    • 1
  • Nathalie R. Le François
    • 2
    • 3
    • 4
  1. 1.Pêches et Océans CanadaInstitut Maurice-LamontageMont-JoliCanada
  2. 2.Département des Sciences Animales, Faculté des Sciences de l’Agriculture et de l’AlimentationUniversité LavalQuebecCanada
  3. 3.Département de Biologie, Chimie et GéographieUniversité du Québec à RimouskiRimouskiCanada
  4. 4.Biodôme de Montréal, Division des collections vivantes et de la rechercheMontrealCanada

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