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Qualitative and quantitative changes of FoF1-ATPase in Japanese flounder and red sea bream associated with rearing temperatures

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Abstract

Fast skeletal muscles of Japanese flounder Paralichthys olivaceus and red sea bream Pagrus major were examined for quantitative and qualitative changes of mitochondrial ATP synthase (F0F1-ATPase) in association with rearing temperatures. The specific activities of F0F1-ATPase from Japanese flounder reared at 10°C, 15°C and 25°C for 4 weeks were determined to be 81±11, 74±13 and 83±11 nmol/min·mg mitochondrial protein, respectively. The corresponding activity from red sea bream reared at 8°C for 5 weeks was determined to be 65±9 nmol/min·mg mitochondrial protein, which was higher than 33±9 nmol/min·mg mitochondrial protein in fish reared at 23°C. The contents of α- and β-F1-ATPase in total mitochondrial proteins were not significantly different between fish reared at different temperatures for the two fish species. However, the contents of β-F1-ATPase in the total fast skeletal muscle extracts, prepared from Japanese flounder reared at 10°C, were 2.1- and 2.9-fold higher than those for fish reared at 15°C and 25°C, respectively. The corresponding content from red seabream reared at 8°C was 2.2-fold higher than that for fish reared at 23°C. Therefore, the changes in F0F1-ATPase depending on rearing temperatures were species-specific.

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References

  1. Fry FE, Hart JS. Cruising speed of goldfish in relation to water temperature. J. Fish. Res. Board Can. 1948; 7; 169–175.

    Google Scholar 

  2. Johnson TP, Bennett AF. The thermal acclimation of burst escape performance in fish: an integrated study of molecular and cellular physiology and organismal performance. J. Exp. Biol. 1995; 198: 2165–2175.

    PubMed  Google Scholar 

  3. Johnston IA, Temple GK. Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour. J. Exp. Biol. 2002; 205: 2305–2322.

    PubMed  Google Scholar 

  4. Watabe S, Imai J, Nakaya M, Hirayama Y, Okamoto Y, Masaki H, Uozumi T, Hirono I, Aoki T. Temperature acclimation induces light meromyosin isoforms with different primary structures in carp fast skeletal muscle. Biochem. Biophys. Res. Commun. 1995; 208: 118–125.

    Article  PubMed  CAS  Google Scholar 

  5. Imai J, Hirayama Y, Kikuchi K, Kakinuma M, Watabe S. cDNA cloning of myosin heavy chain isoforms from carp fast skeletal muscle and their gene expression associated with temperature acclimation. J. Exp. Biol. 1997; 200: 27–34.

    PubMed  CAS  Google Scholar 

  6. Hirayama Y, Kobiyama A, Ochiai Y, Watabe S. Two types of mRNA encoding myosin regulatory light chain in carp last skeletal muscle differ in their 3′ non-coding regions and expression patterns following temperature acclimation. J. Exp. Biol. 1998; 201: 2815–2820.

    CAS  Google Scholar 

  7. Watabe S, Hirayama Y, Nakaya M, Kakinuma M, Kikuchi K, Guo X-F, Kanoh S, Chaen S, Ooi T. Carp expresses fast skeletal myosin isoforms with altered motor functions and structural stabilities to compensate for changes in environmental temperature. J. Therm. Biol. 1998; 22: 375–390.

    Article  Google Scholar 

  8. Watabe S. Temperature plasticity of contractile proteins in fish muscle. J. Exp. Biol. 2002; 205: 2231–2236.

    PubMed  CAS  Google Scholar 

  9. Kobiyama A, Hirayama M, Muramatsu-Uno M, Watabe S. Functional analysis on the 5′-flanking region of carp fast skeletal myosin heavy chain genes for their expression at different temperatures. Gene 2006; 372: 82–91.

    Article  PubMed  CAS  Google Scholar 

  10. Crockford T, Johnston IA. Temperature acclimation and the expression of contractile protein isoforms in the skeletal muscles of the common carp. J. Comp. Physiol. B 1990; 160: 23–30.

    Article  CAS  Google Scholar 

  11. Senior AE. ATP synthesis by oxidative phosphorylation. Physiol. Rev. 1988; 68: 177–231.

    PubMed  CAS  Google Scholar 

  12. Sangawa H, Himeda T, Shibata H, Higuti T. Gene expression of subunit c (P1), subunit c (P2), and oligomycin sensitivity-conferring protein may play a key role in biogenesis of H+-ATP synthase in various rat tissues. J. Biol. Chem. 1997; 272: 6034–6037.

    Article  PubMed  CAS  Google Scholar 

  13. Anderson S, Bankier AT, Barrell BG, de Bruijn MHL, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG. Sequence and organization of the human mitochondrial genome. Nature 1981; 290: 457–465.

    Article  PubMed  CAS  Google Scholar 

  14. Itoi S, Kinoshita S, Kikuchi K, Watabe S. Changes of carp F0F1-ATPase in association with temperature acclimation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003; 284: R153-R163.

    PubMed  CAS  Google Scholar 

  15. Johnston IA, Maitland B. Temperature acclimation in crucian carp, Carassius carassius L., morphometric analyses of muscle fibre ultrastructure. J. Fish Biol. 1980; 17: 113–125.

    Article  Google Scholar 

  16. Tyler S, Sidell BD. Changes in mitochondrial distribution and diffusion distances in muscle of goldfish upon acclimation to warm and cold temperatures. J. Exp. Zool. 1984; 232: 1–9.

    Article  Google Scholar 

  17. Johnston IA, Dunn JF. Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish. Soc. Exp. Biol. Symp. 1987; 41: 67–93.

    CAS  Google Scholar 

  18. Dunn JF. Low-temperature adaptation of oxidative energy production in cold-water fishes. Can. J. Zool. 1988; 66: 1098–1104.

    Article  Google Scholar 

  19. Wodtke E. Temperature adaptation of biological membranes: the effects of acclimation temperature on the unsaturation of the main neutral and charged phospholipids in mitochondrial membranes of the carp (Cyprinus carpio L.). Biochim. Biophys. Acta 1981; 640: 698–709.

    Article  PubMed  CAS  Google Scholar 

  20. Wodtke E. Temperature adaptation of biological membranes: compensation of the molar activity of cytochrome c oxidase in the mitochondrial energy-transducing membrane during thermal acclimation of the carp (Cyprinus carpio L.). Biochim. Biophys. Acta 1981; 640: 710–720.

    Article  PubMed  CAS  Google Scholar 

  21. Watabe S, Itoi S. Extending the pre-rigor state of fish by enhancing mitochondrial ATP synthesis. In: Mori Y, Hayashi T, Highley E (eds). Value-addition to Agricultural Products-Towards Increase of Farmers’ Income and Vitalization of Rural Economy, Symposium Series, No. 11, Japan International Research Center for Agricultural Sciences, Tsukuba, Japan. 2003; 104–111.

    Google Scholar 

  22. Watabe S, Hwang G-C, Ushio H, Hashimoto K. Changes in rigor-mortis progress of carp induced by temperature acclimation. Agric. Biol. Chem. 1990; 54: 219–221.

    CAS  Google Scholar 

  23. Itoi S, Kawahara S, Kondo H, Sakai T, Watabe S. Changes in mitochondrial fatty acid composition following temperature acclimation of carp and their possible effects on F0F1-ATPase activity. Fish Physiol. Biochem. 2003; 29: 237–244.

    Article  CAS  Google Scholar 

  24. Stiggall DL, Galante YM, Hatefi Y. Preparation and properties of anATP-Piexchange complex (complex V) from bovine heart mitochondria. J. Biol. Chem. 1978; 253: 956–964.

    PubMed  CAS  Google Scholar 

  25. Weber K, Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J. Biol. Chem. 1969; 244: 4406–4412.

    PubMed  CAS  Google Scholar 

  26. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680–685.

    Article  PubMed  CAS  Google Scholar 

  27. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 1987; 262: 10035–10038.

    PubMed  CAS  Google Scholar 

  28. Engvall E, Jonsson K, Perlmann P. Enzyme-linked immunosorbent assay. II. Quantitative assay of protein antigen, immunoglobulin G, by means of enzyme-labelled antigen and antibody-coated tubes. Biochim. Biophys. Acta 1971; 251: 427–434.

    PubMed  CAS  Google Scholar 

  29. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Current Protocols in Molecular Biology. Green Publishing Associated and Wiley-Interscience, New York. 1987.

    Google Scholar 

  30. Kikuchi K, Itoi S, Watabe S. Increased levels of mitochondrial ATP synthase β-subunit in fast skeletal muscle of carp acclimated to cold temperature. Fish. Sci. 1999; 65: 629–636.

    CAS  Google Scholar 

  31. Marchuk D, Drumm M, Saulono A, Collins FS. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 1991; 19: 1154.

    Article  PubMed  CAS  Google Scholar 

  32. Church GM, Gilbert W. Genomic sequencing. Proc. Natl Acad. Sci. USA 1984; 81: 1991–1995.

    Article  PubMed  CAS  Google Scholar 

  33. Walker JE, Fearnley IM, Gay NJ, Gibson BW, Northrop FD, Powell SJ, Runswick MJ, Saraste M, Tybulewicz VLJ. Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J. Mol. Biol. 1985; 184: 677–701.

    Article  PubMed  CAS  Google Scholar 

  34. Egginton S, Sidell BD. Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1989; 256: R1-R9.

    CAS  Google Scholar 

  35. St-Pierre J, Charest P-M, Guderley H. Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimatisation of rainbow trout Oncorhynchus mykiss. J. Exp. Biol. 1998; 201: 2961–2970.

    CAS  Google Scholar 

  36. Duthie GG. The respiratory metabolism of temperature-adapted flatfish at rest and during swimming activity and the use of anaerobic metabolism at moderate swimming speeds. J. Exp. Biol. 1982; 97: 359–373.

    PubMed  CAS  Google Scholar 

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Author notes

  1. Shiro Itoi

    Present address: Department of Marine Science and Resources, Nihon University, 252-8510, Fujisawa, Kanagawa, Japan

Authors and Affiliations

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

    Shiro Itoi, Koki Ikeguchi & Shugo Watabe

  2. National Research Institute of Fisheries Science, 236-8648, Yokohama, Japan

    Masaki Kaneniwa, Ryuji Kuwahara, Ichiro Ohara, Noriko Ishida & Michiaki Yamashita

Authors
  1. Shiro Itoi
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  2. Koki Ikeguchi
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  3. Masaki Kaneniwa
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  4. Ryuji Kuwahara
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  5. Ichiro Ohara
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  7. Michiaki Yamashita
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  8. Shugo Watabe
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Correspondence to Shugo Watabe.

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Itoi, S., Ikeguchi, K., Kaneniwa, M. et al. Qualitative and quantitative changes of FoF1-ATPase in Japanese flounder and red sea bream associated with rearing temperatures. Fish Sci 73, 429–439 (2007). https://doi.org/10.1111/j.1444-2906.2007.01351.x

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  • DOI: https://doi.org/10.1111/j.1444-2906.2007.01351.x

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