Advertisement

Thermostability of tropomyosins from the fast skeletal muscles of tropical fish species

  • Ming-Chih HuangEmail author
  • Cheng-Linn Lee
  • Yoshihiro Ochiai
  • Shugo Watabe
Article

Abstract

In order to investigate the species-specific heat tolerance of tropical fishes, the thermodynamic properties of muscle tropomyosin, a member of myofibrillar proteins, were compared among milkfish, tilapia, grouper, and mudskipper. The purified tropomyosins were subjected to differential scanning calorimetry and circular dichroism spectrometry. To unveil the relationship between the stability and the amino acid sequences, the muscle tropomyosin genes of the four species were also cloned, and their deduced amino acid sequences were compared. Thermodynamic analysis revealed that the milkfish tropomyosin showed lower refolding ability after thermal denaturation, compared with those of the other species. The amino acid sequences of these tropomyosins were similar to each other, with the identity being in the range of 95–96%.

Keywords

Tropical fish Muscle tropomyosin Thermostability Amino acid sequence 

Notes

Acknowledgments

The authors would like to thank Ms. Yui-Han Liu for her help in the experimental work. This study was supported in part by National University of Tainan.

References

  1. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201CrossRefGoogle Scholar
  2. Bailey K (1948) Tropomyosin; a new asymmetric protein component of the muscle fibril. Biochem J 43:271–275CrossRefGoogle Scholar
  3. Crick FH (1953) The packing of α-helices: simple coiled-coils. Acta Cryst 6:689–697CrossRefGoogle Scholar
  4. Crockford T, Johnston IA (1990) Temperature acclimation and the expression of contractile protein isoforms in the skeletal muscles of the common carp (Cyprinus carpio L.). J Comp Physiol B 160:23–30CrossRefGoogle Scholar
  5. Cummins P, Perry SV (1974) Chemical and immunochemical characteristics of tropomyosins from striated and smooth muscle. Biochem J 141:43–49CrossRefGoogle Scholar
  6. Fraser RDB, Harrap BS, MacRae TP, Stewart FHC, Suzuki E (1965) Sequential polypeptides containing S-benzyl-l-cysteinyl and γ-ethyl-l-glutamyl residues. J Mol Biol 14:423–431CrossRefGoogle Scholar
  7. Garnier J, Gibrat JF, Robson B (1996) GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol 266:540–553CrossRefGoogle Scholar
  8. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, pp 571–607Google Scholar
  9. Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–765Google Scholar
  10. Heeley DH, Hong C (1994) Isolation and characterization of tropomyosin from fish muscle. Comp Biochem Physiol B Biochem Mol Biol 108:95–106CrossRefGoogle Scholar
  11. Heeley DH, Bieger T, Waddleton DM, Hong C, Jackman DM, McGowan C, Davidson WS, Beavis RC (1995) Characterization of fast, slow and cardiac muscle tropomyosins from salmonid fish. Eur J Biochem 232:226–234CrossRefGoogle Scholar
  12. Hitchcock-DeGregori SE, Varnell TA (1990) Tropomyosin has discrete actin-binding sites with sevenfold and fourteenfold periodicities. J Mol Biol 214:885–896CrossRefGoogle Scholar
  13. Huang MC, Ochiai Y (2005) Fish fast skeletal muscle tropomyosins show species-specific thermal stability. Comp Biochem Physiol B Biochem Mol Biol 141:461–471CrossRefGoogle Scholar
  14. Huang MC, Ochiai Y, Watabe S (2004) Characterization of tropomyosin from fast skeletal muscle of bluefin tuna Thunnus thynnus. Fish Sci 70:667–674CrossRefGoogle Scholar
  15. Hwang GC, Watabe S, Hashimoto K (1990) Changes in carp myosin ATPase induced by temperature acclimation. J Comp Physiol B 160:233–239CrossRefGoogle Scholar
  16. Hwang GC, Ochiai Y, Watabe S, Hashimoto K (1991) Change of carp myosin subfragment-1 induced by temperature acclimation. J Comp Physiol B 161:141–146CrossRefGoogle Scholar
  17. Imai J, Hirayama Y, Kikuchi K, Kakinuma M, Watabe S (1997) cDNA cloning of myosin heavy chain isoform from carp fast skeletal muscle and their gene expression associated with temperature acclimation. J Exp Biol 200:27–34Google Scholar
  18. Jackman D, Waddleton DM, Younghusband B, Heeley DH (1996) Further characterization of fast, slow and cardiac muscle tropomyosins from salmonid fish. Eur J Biochem 242:363–371CrossRefGoogle Scholar
  19. Johnson P, Smillie LB (1977) Polymerizability of rabbit skeletal tropomyosin: effects of enzymic and chemical modification. Biochemistry 16:2264–2269CrossRefGoogle Scholar
  20. Johnston IA (1979) Calcium regulatory proteins and temperature acclimation of actomyosin ATPase from a eurythermal teleost (Carassius auratus L.). J Comp Physiol B 129:163–167CrossRefGoogle Scholar
  21. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282Google Scholar
  22. Kiefer F, Arnold K, Künzli M, Bordoli L, Schwede T (2009) The SWISS-MODEL repository and associated resources. Nucleic Acids Res 37:D387–D392CrossRefGoogle Scholar
  23. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  24. Laemmli UK (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  25. Lees-Miller JP, Helfman DM (1991) The molecular basis for tropomyosin isoform diversity. BioEssays 13:429–437CrossRefGoogle Scholar
  26. Lehrer SS, Morris EP (1982) Dual effects of tropomyosin and troponin-tropomyosin on actomyosin subfragment 1 ATPase. J Biol Chem 257:8073–8080Google Scholar
  27. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164CrossRefGoogle Scholar
  28. Mak AS, Smillie LB, Stewart GB (1980) A comparison of the amino acid sequences of rabbit skeletal muscle α- and β- tropomyosin. J Biol Chem 255:3647–3655Google Scholar
  29. Matsudaira P (1987) Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem 262:10035–10038Google Scholar
  30. McLachlan AD, Stewart M (1976) The 14-fold periodicity in α-tropomyosin and the interaction with action. J Mol Biol 103:271–298CrossRefGoogle Scholar
  31. Nakaya M, Watabe S, Ooi T (1995) Differences in the thermal stability of acclimation temperature-associated types of carp myosin and its rod on differential scanning calorimetry. Biochemistry 34:3114–3120CrossRefGoogle Scholar
  32. Nakaya M, Kakinuma M, Watabe S, Ooi T (1997) Differential scanning calorimetry and CD spectrometry of acclimation temperature-associated type of carp light meromyosin. Biochemistry 36:9179–9184CrossRefGoogle Scholar
  33. Ochiai Y, Ahmed K, Ahsan MN, Funabara D, Nakaya M, Watabe S (2001) cDNA cloning and deduced amino acid sequence of tropomyosin from fast skeletal muscle of white croaker Pennahia argentata. Fish Sci 67:556–558CrossRefGoogle Scholar
  34. Ochiai Y, Huang MC, Fukushima H, Watabe S (2003) cDNA cloning and thermodynamic properties of tropomyosin from walleye pollock Theragra chalcogramma fast skeletal muscle. Fish Sci 69:1031–1036Google Scholar
  35. Ochiai Y, Ozawa H, Huang MC, Watabe S (2010) Characterization of two tropomyosin isoforms from the fast skeletal muscle of bluefin tuna Thunnus thynnus orientalis. Arch Biochem Biophys 502:96–103CrossRefGoogle Scholar
  36. Penney RK, Goldspink G (1981) Regulatory proteins and thermostability of myofibrillar ATPase in acclimated goldfish. Comp Biochem Physiol 69B:577–583Google Scholar
  37. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic tree. Mol Biol Evol 4:406–425Google Scholar
  38. Sambrook J, Russell DW (2001) Plasmids and their usefulness in molecular cloning. Molecular cloning: a laboratory manual, vol 1, 3nd edn. Cold Spring Harbor Laboratory Press, New York, pp 31–138Google Scholar
  39. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385CrossRefGoogle Scholar
  40. Seki N, Iwabuchi S (1978) On the subunit composition of fish tropomyosins. Bull Jpn Soc Sci Fish 44:1333–1340CrossRefGoogle Scholar
  41. Smillie LB (1979) Structure and functions of tropomyosin from muscle and non-muscle sources. Trends Biochem Sci 4:151–155CrossRefGoogle Scholar
  42. Tamura K, Stecher G, Daniel Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  43. Watabe S, Imai J, Nakaya M, Hirayama Y, Okamoto Y, Masaki H, Uozumi T, Hirono I, Aoki T (1995) Temperature acclimation induces light meromyosin isoforms with different primary structures in carp fast skeletal muscle. Biochem Biophys Res Commun 208:118–125CrossRefGoogle Scholar
  44. Yang JT, Wu CC, Martinez HM (1986) Calculation of protein conformation from circular dichroism. Methods Enzymol 130:208–268CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Biological Sciences and TechnologyNational University of TainanTainanRepublic of China
  2. 2.Department of Aquatic Bioscience, Graduate School of Agricultural and Life SciencesUniversity of TokyoTokyoJapan
  3. 3.Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan
  4. 4.Kitasato University School of Marine BiosciencesSagamiharaJapan

Personalised recommendations