Journal of Muscle Research & Cell Motility

, Volume 9, Issue 6, pp 533–540 | Cite as

Phosphorylatable serine residues are located in a non-helical tailpiece of a catch muscle myosin

  • Loriana Castellani
  • Bruce W. ElliottJr
  • Carolyn Cohen
Papers

Summary

Myosin from a molluscan catch muscle displays unusual properties: when phosphorylated in the rod by an endogenous heavy-chain kinase, myosin solubility is enhanced and the molecule folds (Castellani & Cohen,Proc. natn. Acad. Sci. U.S.A.84, (1987) 4058–62). We have now localized the sites of phosphorylation to the carboxy-terminal end of the rod by selective proteolytic cleavage. Two major stretches of sequence, 18 and 21 residues long, have been identified, each containing a single residue of phosphoserine. Analysis of the amino-acid sequence of these two peptides indicates that they form a non-helical tailpiece. We discuss how phosphorylation of this tailpiece might influence enzymatic activity in catch muscle thick filaments.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Achazi, R. K. (1979) Phosphorylation of molluscan paramyosin.Pflügers Arch. ges. Physiol. 379, 197–201.Google Scholar
  2. Atkinson, M. A. L. &Korn, E.D. (1987) A model for the polymerization ofAcanthamoeba myosin II and the regulation of its actin-activated Mg2+ ATPase activity.J. biol. Chem. 262, 15809–11.PubMedGoogle Scholar
  3. Castellani, L. &Cohen, C. (1987a) Myosin rod phosphorylation and the catch state of molluscan muscles.Science 235, 334–7.PubMedGoogle Scholar
  4. Castellani, L. &Cohen, C. (1987b) Rod phosphorylation favors folding in a catch muscle myosin.Proc. natn. Acad. Sci. U.S.A. 84, 4058–62.Google Scholar
  5. Castellani, L. &Cohen, C. (1988) Myosin/paramyosin phosphorylation in molluscan muscles.Biophys. J. 53, 178a.Google Scholar
  6. Chou, P. Y. &Fasman, G. (1978) Prediction of the secondary structure of proteins from their amino acid sequence.Adv. Enzym. 47, 45–148.Google Scholar
  7. Cohen, C. (1982) Matching molecules in the catch mechanism.Proc. natn. Acad. Sci. U.S.A. 79, 3176–8.Google Scholar
  8. Cohen, C., Lanar, D. E. &Parry, D. A. D. (1987) Amino acid sequence and structural repeats in Schistosome paramyosin match those of myosin.Biosci. Rep. 7, 11–6.PubMedGoogle Scholar
  9. Collins, J. H., Kuznicki, J., Bowers, B. &Korn, E. D. (1982) Comparison of the actin binding and filament formation properties of phosphorylated and dephosphorylatedAcanthamoeba myosin II.Biochemistry 21, 6910–5.PubMedGoogle Scholar
  10. Cooley, L. B., Johnson, W. H. &Krause, S. (1979) Phosphorylation of paramyosin and its possible role in the catch mechanism.J. biol. Chem. 254, 2195–8.PubMedGoogle Scholar
  11. CÔté, G. P., Collins, J. H. &Korn, E. D. (1981) Identification of three phosphorylation sites of each heavy chain ofAcanthamoeba myosin II.J. biol. Chem. 256, 12811–6.PubMedGoogle Scholar
  12. CÔté, G. P., Robinson, E. A., Appella, E. &Korn, E. D. (1984) Amino acid sequence of a segment of theAcanthamoeba myosin II heavy chain containing all three regulatory phosphorylation sites.J. biol. Chem. 259, 12781–7.PubMedGoogle Scholar
  13. Craig, R., Smith, R. &Kendrick-Jones, J. (1983) Light-chain phosphorylation controls the conformation of vertebrate non-muscle and smooth muscle myosin molecules.Nature 302, 436–9.PubMedGoogle Scholar
  14. Elliott, B. W., Jr &Cohen, C. (1986) Isolation and characterization of a lysine-specific protease fromPseudomonas aeruginosa.J. biol. Chem. 261, 11259–65.PubMedGoogle Scholar
  15. Hammer, J. A., III, Bowers, B., Paterson, B. M. &Korn, E. D. (1987) Complete nucleotide sequence and deduced polypeptide sequence of a nonmuscle myosin heavy chain gene fromAcanthamoeba: evidence of a hinge in the rodlike tail.J. Cell. Biol. 105, 913–25.PubMedGoogle Scholar
  16. Kawamoto, S. &Adelstein, R. S. (1988) The heavy chain of smooth muscle myosin is phosphorylated in aorta cells.J. biol. Chem. 263, 1099–102.PubMedGoogle Scholar
  17. Kemp, B. E., Graves, D. J., Benjamini, E. &Krebs, E. G. (1977) Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinaseJ. biol. Chem. 252, 4888–94.PubMedGoogle Scholar
  18. Kuczmarski, E. R. &Spudich, J. A. (1980) Regulation of myosin self-assembly: phosphorylation ofDictyostelium heavy chain inhibits formation of thick filaments.Proc. natn. Acad. Sci. U.S.A. 77, 7292–6.Google Scholar
  19. Kuznicki, J. (1986) Phosphorylation of myosin in nonmuscle and smooth muscle cells.FEBS Lett. 204, 169–76.PubMedGoogle Scholar
  20. Kuznicki, J., Albanesi, J. P., CÔté, G. P. &Korn, E. D. (1983) Supramolecular regulation of the actin-activated ATPase activity of filaments ofAcanthamoeba myosin II.J. biol. Chem. 258, 6011–4.PubMedGoogle Scholar
  21. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 227, 680–5.PubMedGoogle Scholar
  22. Lipman, D. J. &Pearson, W. R. (1985) Rapid and sensitive protein similarity searches.Science 227, 1435–41.PubMedGoogle Scholar
  23. Matsudaira, P. (1987) Sequence from picomole quantities of proteins electroblotted onto poly vinylidene difluoride membranes.J. biol. Chem. 262, 10035–8.PubMedGoogle Scholar
  24. Mclachlan, A. D. (1984) Structural implications of the myosin amino acid sequence.A. Rev. Biophys. Bioengng. 13, 167–89.Google Scholar
  25. Mikoryak, C. A., Elliott, B. W., Jr., Kimball, M. E. &Steiner, L. A. (1986) An extra disulfide bridge in the constant domain ofRana catesbiana immunoglobulin light chains.J. Immunol. 136, 217–23.PubMedGoogle Scholar
  26. Nagai, R., Larson, D. M. &Periasamy, M. (1988) Characterization of a mammalian smooth muscle myosin heavy chain cDNA clone and its expression in various smooth muscle types.Proc. natn. Acad. Sci. U.S.A. 85, 1047–51.Google Scholar
  27. Nonomura, Y. (1974) Fine structure of the thick filament in molluscan catch muscle.J. molec. Biol. 88, 445–55.PubMedGoogle Scholar
  28. Parry, D. A. D. (1975) Analysis of the primary sequence of α-tropomyosin from rabbit skeletal muscle.J. molec. Biol. 98, 519–35.PubMedGoogle Scholar
  29. Rozek, C. E. &Davidson, N. (1986) Differential processing of RNA transcribed from the single-copyDrosophila myosin heavy chain gene produces four mRNAs that encode two polypeptides.Proc. natn. Acad. Sci. U.S.A. 83, 2128–32.Google Scholar
  30. Stull, J. T. &Buss, J. E. (1977) Phosphorylation of cardiac troponin by cyclic adenosine 3′∶5′-monophosphatedependent protein kinase.J. biol. Chem. 252, 851–7.PubMedGoogle Scholar
  31. Szent-Györgyi, A. G., Cohen, C. &Kendrick-Jones, J. (1971) Paramyosin and filaments of molluscan “catch” muscles. II. Native filaments: isolation and characterization.J. molec. Biol. 56, 239–58.PubMedGoogle Scholar
  32. Trybus, K. M., Huiatt, T. W. &Lowey, S. (1982) A bent monomeric conformation of myosin from smooth muscle.Proc. natn. Acad. Sci. U.S.A. 79, 6151–5.Google Scholar
  33. Trybus, K. &Lowey, S. (1984) Conformational states of smooth muscle myosin. Effects of light chain phosphorylation and ionic strength.J. biol. Chem. 259, 8564–71.PubMedGoogle Scholar
  34. Wilbur, W. J. &Lipman, D. J. (1983) Rapid similarity searches of nucleic acid and protein data banks.Proc. natn. Acad. Sci. U.S.A. 80, 726–30.Google Scholar
  35. Yanagisawa, M., Hamada, Y., Katsuragawa, Y., Imamura, M., Mikawa, T. &Masaki, T. (1987) Complete primary sequence of vertebrate smooth muscle myosin heavy chain deduced from its complementary DNA sequence.J. molec. Biol. 198, 143–57.PubMedGoogle Scholar

Copyright information

© Chapman and Hall Ltd 1988

Authors and Affiliations

  • Loriana Castellani
    • 1
  • Bruce W. ElliottJr
    • 1
  • Carolyn Cohen
    • 1
  1. 1.Rosenstiel Basic Medical Sciences Research CenterBrandeis UniversityWalthamUSA

Personalised recommendations