Journal of Muscle Research & Cell Motility

, Volume 26, Issue 6–8, pp 461–465 | Cite as

Twitchin purified from molluscan catch muscles regulates interactions between actin and myosin filaments at rest in a phosphorylation-dependent manner

  • Yasutaka Tsutsui
  • Maki Yoshio
  • Kazuhiro Oiwa
  • Akira Yamada


Twitchin, also called mini-titin, is structurally related to the giant elastic protein connectin/titin, and has been found in not only striated but also smooth muscles of bivalves. Many bivalve smooth muscles such as byssus retractor muscles and the opaque part of adductor muscles are known as catch muscles that can maintain high passive tension with little expenditure of energy after they have actively contracted. Twitchin is phosphorylated when this high-tension state (catch state) ceases. Our recent studies revealed that the catch tension is due to interactions between thick and thin filaments in the presence of MgATP at low free Ca2+ concentrations, which can be visualized in vitro under a light microscope (Yamada et al., 2001 Proc Natl Acad Sci USA 98: 6635–6640). We also found that twitchin is essential for the interactions of the catch state in mussel (Mytilus galloprovincialis) catch muscles. In the presence of twitchin, actin filaments bound to purified myosin filaments when twitchin was dephosphorylated by Ser/Thr protein phosphatase 2B, while they did not when it was phosphorylated by cAMP-dependent protein kinase. In the current study we demonstrate the same essential components of the catch state for another bivalve that exhibits catch, i.e., Japanese oyster (Crassostrea gigas).


Mytilus Edulis Dependent Protein Kinase Soluble Protein Fraction Catch State Myosin Heavy Chain Gene 
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  1. Baguet F, Gillis JM (1968) Energy cost of tonic contraction in a lamellibranch catch muscleJ Physiol 198:127–143Google Scholar
  2. Benian GM, Ayme-Southgate A, Tinley TL (1999) The genetics and molecular biology of the titin/connectin-like proteins of invertebratesRev Physiol Biochem Pharmacol 138:235–268PubMedGoogle Scholar
  3. Cole RA, Twarog BM (1972) Relaxation of catch in a molluscan smooth muscle. I. Effects of drugs which act on the adenyl cyclase systemComp Biochem Physiol A 43:321–330PubMedCrossRefGoogle Scholar
  4. Funabara D, Kinoshita S, Watabe S, Siegman MJ, Butler TM, Hartshorne DJ (2001) Phosphorylation of molluscan twitchin by the cAMP-dependent protein kinaseBiochemistry 40:2087–2095PubMedCrossRefGoogle Scholar
  5. Funabara D, Watabe S, Mooers SU, Narayan S, Dudas C, Hartshorne DJ, Siegman MJ, Butler TM (2003) Twitchin from molluscan catch muscle: primary structure and relationship between site-specific phosphorylation and mechanical functionJ Biol Chem 278:29308–29316PubMedCrossRefGoogle Scholar
  6. Gregorio CC, Granzier H, Sorimachi H, Labeit S (1999) Muscle assembly: a titanic achievement?Curr Opin Cell Biol 11:18–25PubMedCrossRefGoogle Scholar
  7. Ishii N, Simpson AWM, Ashley CC (1989) Free calcium at rest during ‘catch’ in single smooth muscle cellsScience 243:1367–1368PubMedGoogle Scholar
  8. Johnson WH, Kahn JS, Szent-Györgyi AG (1959) Paramyosin and contraction of ‘catch muscles’Science 130:160–161PubMedGoogle Scholar
  9. Kendrick-Jones J, Lehman W, Szent-Györgyi AG (1970) Regulation in molluscan musclesJ Mol Biol 54:313–326PubMedCrossRefGoogle Scholar
  10. Labeit S, Gautel M, Lakey A, Trinick J (1992) Towards a molecular understanding of titinEMBO J 11:1711–1716PubMedGoogle Scholar
  11. Labeit S, Kolmerer B (1995) Titins: giant proteins in charge of muscle ultrastructure and elasticityScience 270:293–296PubMedGoogle Scholar
  12. Lowy J, Millman BM (1963) The contractile mechanism of the anterior byssus retractor muscle of Mytilus edulisPhil Trans B 246:105–148Google Scholar
  13. Maruyama K (1994) Connectin, an elastic protein of striated muscleBiophys Chem 50:73–85PubMedCrossRefGoogle Scholar
  14. Maruyama K, Matsubara S, Natori R, Nonomura Y, Kimura S, Ohashi K, Murakami F, Handa S, Eguchi G (1977) Connectin, an elastic protein of muscle. Characterization and functionJ Biochem 82:317–337PubMedGoogle Scholar
  15. Millman BM (1964) Contraction in the opaque part of the adductor muscle of the oyster(Crassostrea angulata) J Physiol 173:238–262PubMedGoogle Scholar
  16. Pfitzer G, Rüegg JC (1982) Molluscan catch muscle: regulation and mechanics in living and skinned anterior byssus retractor muscle of Mytilus edulisJ Comp Physiol 147:137–142Google Scholar
  17. Probst WC, Cropper EC, Heierhorst J, Hooper SL, Jaffe H, Vilim F, Beushausen S, Kupfermann I, Weiss KR (1994) cAMP-dependent phosphorylation of Aplysia twitchin may mediate modulation of muscle contractions by neuropeptide cotransmittersProc Natl Acad Sci USA 91:8487–8491PubMedCrossRefGoogle Scholar
  18. Rüegg JC (1971) Smooth muscle tone. Physiol Rev 51:201–248PubMedGoogle Scholar
  19. Siegman MJ, Funabara D, Kinoshita S, Watabe S, Hartshorne DJ, Butler TM (1998) Phosphorylation of a twitchin-related protein controls catch and calcium sensitivity of force production in invertebrate smooth muscle. Proc Natl Acad Sci USA 95:5383–5388PubMedCrossRefGoogle Scholar
  20. Siegman MJ, Mooers SU, Li C, Narayan S, Trinkle-Mulcahy L, Watabe S, Hartshorne DJ, Butler TM (1997) Phosphorylation of a high molecular weight (~600 kDa) protein regulates catch in invertebrate smooth muscleJ Muscle Res Cell Motil 18:655–670PubMedCrossRefGoogle Scholar
  21. Sobieszek A (1973) The fine structure of the contractile apparatus of the anterior byssus retractor muscle of Mytilus edulisJ Ultrastruct Res 43:313–343PubMedCrossRefGoogle Scholar
  22. Spudich JA, Watt S (1971) The regulation of rabbit skeletal muscle contractionJ Biol Chem 246:4866–4871PubMedGoogle Scholar
  23. Szent-Györgyi AG, Cohen C, Kendrick-Jones J (1971) Paramyosin and the filaments of molluscan ‘catch’ muscles. II. Native filaments: isolation and characterization. J Mol Biol 56:239–258PubMedCrossRefGoogle Scholar
  24. Twarog BM (1954) Responses of a molluscan smooth muscle to acetylcholine and 5-hydroxytryptamineJ Cell Comp Physiol 44:141–163CrossRefGoogle Scholar
  25. Vibert P, Edelstein SM, Castellani L, Elliott BW Jr (1993) Mini-titins in striated and smooth molluscan muscles: structure, location and immunological crossreactivityJ Muscle Res Cell Motil 14:598–607PubMedCrossRefGoogle Scholar
  26. Vibert P, York ML, Castellani L, Edelstein S, Elliott B, Nyitray L (1996) Structure and distribution of mini-titinsAdv Biophys 33:199–209PubMedCrossRefGoogle Scholar
  27. Wang K, McClure J, Tu A (1979) Titin: major myofibrillar components of striated muscleProc Natl Acad Sci USA 76:3698–3702PubMedCrossRefGoogle Scholar
  28. Watabe S, Hartshorne DJ (1990) Paramyosin and the catch mechanismComp Biochem Physiol B 96:639–646PubMedCrossRefGoogle Scholar
  29. Yamada A, Ishii N, Shimmen T, Takahashi K (1989) Mg-ATPase activity and motility of native thick filaments isolated from the anterior byssus retractor muscle of Mytilus edulisJ Muscle Res Cell Motil 10:124–134PubMedCrossRefGoogle Scholar
  30. Yamada A, Yoshio M, Kojima H, Oiwa K (2001) An in vitro assay reveals essential protein components for the ‘catch’ state of invertebrate smooth muscleProc Natl Acad Sci USA 98:6635–6640PubMedCrossRefGoogle Scholar
  31. Yamada A, Yoshio M, Nakamura A, Kohama K, Oiwa K (2004) Protein phosphatase 2B dephosphorylates twitchin, initiating the catch state of invertebrate smooth muscleJ Biol Chem 279:40762–40768PubMedCrossRefGoogle Scholar
  32. Yamada A, Yoshio M, Oiwa K, Nyitray L (2000) Catchin, a novel protein in molluscan catch muscles, is produced by alternative splicing from the myosin heavy chain geneJ Mol Biol 295:169–178PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Yasutaka Tsutsui
    • 1
  • Maki Yoshio
    • 2
  • Kazuhiro Oiwa
    • 1
    • 2
  • Akira Yamada
    • 2
  1. 1.Graduate School of Life ScienceUniversity of HyogoKamigori, Ako-gun, HyogoJapan
  2. 2.Kansai Advanced Research CenterNational Institute of Information and Communications TechnologyKobe, HyogoJapan

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