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Differential expression of heat-shock proteins in F2 offspring from F1 hybrids produced between thermally selected and normal rainbow trout strains

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  • Aquaculture
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Abstract

Rainbow trout Oncorhynchus mykiss is a cold-water aquaculture species, and a thermally selected strain has been developed by multigenerational high-temperature breeding in Japan. We examined the expression of heat-shock proteins as candidates responsible for thermotolerance in rainbow trout using F2 offspring from F1 hybrids produced between thermally selected and normal strains. From F2 offspring, two groups were selected for western blot analysis, namely, low- and high-thermotolerance groups (times to loss of equilibrium were <30 and ≥60 min, respectively). We demonstrated that the expression levels of Hsp70, Hsp60, and Hsp40 in tail fin tissues were significantly higher in the individuals with high thermotolerance than in those with low thermotolerance under non-heat-shock conditions. In particular, Hsp70 was expressed only in the individuals with high thermotolerance. These results suggest that Hsp70 is a major protein responsible for conferring thermotolerance in rainbow trout.

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References

  1. Kaya CM (1978) Thermal resistance of rainbow trout from a permanently heated stream and two hatchery strains. Prog Fish Cult 40:138–142

    Article  Google Scholar 

  2. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677

    Article  PubMed  CAS  Google Scholar 

  3. Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183

    Article  PubMed  CAS  Google Scholar 

  4. Roberts RJ, Agius C, Saliba C, Bossier P, Sung YY (2010) Heat shock proteins (chaperones) in fish and shellfish and their potential role in relation to fish health: a review. J Fish Dis 33:789–801

    Article  PubMed  CAS  Google Scholar 

  5. Sonna LA, Fujita J, Gaffin SL, Lilly CM (2002) Invited review: effects of heat and cold stress on mammalian gene expression. J Appl Physiol 92:1725–1742

    PubMed  CAS  Google Scholar 

  6. Norris CE, Brown MA, Hickey E, Weber LA, Hightower LE (1997) Low-molecular-weight heat shock proteins in a desert fish (Poeciliopsis lucida): homologs of human Hsp27 and Xenopus Hsp30. Mol Biol Evol 14:1050–1061

    Article  PubMed  CAS  Google Scholar 

  7. Kondo H, Harano R, Nakaya M, Watabe S (2004) Characterization of goldfish heat shock protein-30 induced upon severe heat shock in cultured cells. Cell Stress Chaperones 9:350–358

    Article  PubMed  CAS  Google Scholar 

  8. Mosser DD, Van Oostrom J, Bols NC (1987) Induction and decay of thermotolerance in rainbow trout fibroblasts. J Cell Physiol 132:155–160

    Article  PubMed  CAS  Google Scholar 

  9. Mosser DD, Bols NC (1988) Relationship between heat-shock protein synthesis and thermotolerance in rainbow trout fibroblasts. J Comp Physiol B 158:457–467

    Article  PubMed  CAS  Google Scholar 

  10. Iwama GK, Vijayan MM, Forsyth RB, Ackerman PA (1999) Heat shock proteins and physiological stress in fish. Am Zool 39:901–909

    CAS  Google Scholar 

  11. Ineno T, Tsuchida S, Kanda M, Watabe S (2005) Thermal tolerance of a rainbow trout Oncorhynchus mykiss strain selected by high-temperature breeding. Fish Sci 71:767–775

    Article  CAS  Google Scholar 

  12. Ineno T, Endo M, Watabe S (2008) Differences in self-feeding activity between thermally selected and normal strains of rainbow trout Oncorhynchus mykiss at high temperatures. Fish Sci 74:372–379

    Article  CAS  Google Scholar 

  13. Ikeguchi K, Ineno T, Itoi S, Kondo H, Kinoshita S, Watabe S (2006) Increased levels of mitochondrial gene transcripts in the thermally selected rainbow trout (Oncorhynchus mykiss) strain during embryonic development. Mar Biotechnol 8:178–188

    Article  PubMed  CAS  Google Scholar 

  14. Cox DK (1974) Effects of three heating rates on the critical thermal maximum of bluegill. In: Gibbons JW, Sharitz RR (eds) Thermal ecology. National Technical Information Service, Springfield, pp 158–163

    Google Scholar 

  15. Becker CD, Genoway RG (1979) Evaluation of the critical thermal maximum for determining thermal tolerance of freshwater-fish. Environ Biol Fishes 4:245–256

    Article  Google Scholar 

  16. Bols NC, Barlian A, Chirinotrejo M, Caldwell SJ, Goegan P, Lee LEJ (1994) Development of a cell-line from primary cultures of rainbow-trout, Oncorhynchus mykiss (Walbaum), gills. J Fish Dis 17:601–611

    Article  Google Scholar 

  17. Tan E, Wongwarangkana C, Kinoshita S, Suzuki Y, Oshima K, Hattori M, Ineno T, Tamaki K, Kera A, Muto K, Yada T, Kitamura S, Asakawa S, Watabe S (2012) Global gene expression analysis of gill tissues from normal and thermally selected strains of rainbow trout. Fish Sci. doi:10.1007/s12562-012-0522-4

  18. Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449

    PubMed  CAS  Google Scholar 

  19. Li J, Qian X, Sha B (2009) Heat shock protein 40: structural studies and their functional implications. Protein Pept Lett 16:606–612

    Article  PubMed  CAS  Google Scholar 

  20. Summers DW, Douglas PM, Ramos CH, Cyr DM (2009) Polypeptide transfer from Hsp40 to Hsp70 molecular chaperones. Trends Biochem Sci 34:230–233

    Article  PubMed  CAS  Google Scholar 

  21. Levy-Rimler G, Bell RE, Ben-Tal N, Azem A (2002) Type I chaperonins: not all are created equal. FEBS Lett 529:1–5

    Article  PubMed  CAS  Google Scholar 

  22. Singh B, Gupta RS (1992) Expression of human 60-kD heat shock protein (HSP60 or P1) in Escherichia coli and the development and characterization of corresponding monoclonal antibodies. DNA Cell Biol 11:489–496

    Article  PubMed  CAS  Google Scholar 

  23. Sherman M, Goldberg AL (1992) Heat shock in Escherichia coli alters the protein-binding properties of the chaperonin groEL by inducing its phosphorylation. Nature 357:167–169

    Article  PubMed  CAS  Google Scholar 

  24. Sherman M, Goldberg AL (1994) Heat shock-induced phosphorylation of GroEL alters its binding and dissociation from unfolded proteins. J Biol Chem 269:31479–31483

    PubMed  CAS  Google Scholar 

  25. Zatsepina OG, Ulmasov KA, Beresten SF, Molodtsov VB, Rybtsov SA, Evgen’ev MB (2000) Thermotolerant desert lizards characteristically differ in terms of heat-shock system regulation. J Exp Biol 203:1017–1025

    PubMed  CAS  Google Scholar 

  26. Calabria G, Dolgova O, Rego C, Castañeda LE, Rezende EL, Balanyà J, Pascual M, Sørensen JG, Loeschcke V, Santos M (2012) Hsp70 protein levels and thermotolerance in Drosophila subobscura: a reassessment of the thermal co-adaptation hypothesis. J Evol Biol 25:691–700

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported in part by a grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan.

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Authors and Affiliations

  1. Research Center for Aquatic Genomics, National Research Institute of Fisheries Science, Fisheries Research Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa, 236-8648, Japan

    Nobuhiko Ojima & Miyuki Mekuchi

  2. Kobayashi Branch, Miyazaki Prefectural Fisheries Research Institute, Kobayashi, Miyazaki, 886-0005, Japan

    Toshinao Ineno, Koichi Tamaki & Akio Kera

  3. Laboratory of Aquatic Molecular Biology and Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo, 113-8657, Japan

    Shigeharu Kinoshita & Shuichi Asakawa

  4. Laboratory of Marine Biochemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo, 113-8657, Japan

    Shugo Watabe

  5. Kitasato University School of Marine Biosciences, 1-15-1 Kitasato, Minami, Sagamihara, Kanagawa, 252-0373, Japan

    Shugo Watabe

Authors
  1. Nobuhiko Ojima
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  2. Miyuki Mekuchi
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  3. Toshinao Ineno
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  4. Koichi Tamaki
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  5. Akio Kera
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  6. Shigeharu Kinoshita
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  7. Shuichi Asakawa
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  8. Shugo Watabe
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Correspondence to Nobuhiko Ojima.

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Ojima, N., Mekuchi, M., Ineno, T. et al. Differential expression of heat-shock proteins in F2 offspring from F1 hybrids produced between thermally selected and normal rainbow trout strains. Fish Sci 78, 1051–1057 (2012). https://doi.org/10.1007/s12562-012-0523-3

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  • DOI: https://doi.org/10.1007/s12562-012-0523-3

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