Skip to main content
Log in

Study of regulatory effect of tropomyosin on actin-myosin interaction in skeletal muscle by in vitro motility assay

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

The interaction between myosin and actin in striated muscle tissue is regulated by Ca2+ via thin filament regulatory proteins. Skeletal muscle possesses a whole pattern of myosin and tropomyosin isoforms. The regulatory effect of tropomyosin on actin-myosin interaction was investigated by measuring the sliding velocity of both actin and actin-tropomyosin filaments over fast and slow skeletal myosins using the in vitro motility assay. The actin-tropomyosin filaments were reconstructed with tropomyosin isoforms from striated muscle tissue. It was found that tropomyosins with different content of α-, β-, and γ-chains added to actin filaments affect the sliding velocity of filaments in different ways. On the other hand, the sliding velocity of filaments with the same content of α-, β-, and Γ-chains depends on myosin isoforms of striated muscle. The reciprocal effects of myosin and tropomyosin on actin-myosin interaction in striated muscle may play a significant role in maintenance of effective work of striated muscle both during ontogenesis and under pathological conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

actin-TM:

actin-tropomyosin filament

F-actin:

filamentary actin

RhPh-F-actin:

filamentary actin stained with phalloidin-tetramethylrhodamine

References

  1. Barany, M. (1967) J. Gen. Physiol., 50, 197–218.

    Article  PubMed  Google Scholar 

  2. Marston, S. B., and Taylor, E. W. (1980) J. Mol. Biol., 139, 573–600.

    Article  PubMed  CAS  Google Scholar 

  3. Brown, J. H., Zhou, Z., Reshetnikova, L., Robinson, H., Yammani, R. D., Tobacman, L. S., and Cohen, C. (2005) Proc. Natl. Acad. Sci. USA, 102, 18878–18883.

    Article  PubMed  CAS  Google Scholar 

  4. Perry, S. V. (2001) J. Muscle Res. Cell. Motil., 22, 5–49.

    Article  PubMed  CAS  Google Scholar 

  5. Boussouf, S. E., Maytum, R., Jaquet, K., and Geeves, M. A. (2007) J. Muscle Res. Cell. Moti., 28, 49–58.

    Article  CAS  Google Scholar 

  6. Gordon, A. M., Homsher, E., and Regnier, M. (2000) Physiol. Rev., 80, 853–924.

    PubMed  CAS  Google Scholar 

  7. McKillop, D. F., and Geeves, M. A. (1993) Biophys. J., 65, 693–701.

    Article  PubMed  CAS  Google Scholar 

  8. Pirani, A., Vinogradova, M. V., Curmi, P. M., King, W. A., Fletterick, R. J., Craig, R., Tobacman, L. S., Xu, C., Hatch, V., and Lehman, W. (2006) J. Mol. Biol., 357, 707–717.

    Article  PubMed  CAS  Google Scholar 

  9. Lehman, W., Hatch, V., Korman, V., Rosol, M., Thomas, L., Maytum, R., Geeves, M. A., Van Eyk, J. E., Tobacman, L. S., and Craig, R. (2000) J. Mol. Biol., 302, 593–606.

    Article  PubMed  CAS  Google Scholar 

  10. Chandy, I. K., Lo, J. C., and Ludescher, R. D. (1999) Biochemistry, 38, 9286–9294.

    Article  PubMed  CAS  Google Scholar 

  11. Landis, C. A., Bobkova, A., Homsher, E., and Tobacman, L. S. (1997) J. Biol. Chem., 272, 14051–14056.

    Article  PubMed  CAS  Google Scholar 

  12. Landis, C., Back, N., Homsher, E., and Tobacman, L. S. (1999) J. Biol. Chem., 274, 31279–31285.

    Article  PubMed  CAS  Google Scholar 

  13. Lehrer, S. S., and Morris, E. P. (1982) J. Biol. Chem., 257, 8073–8080.

    PubMed  CAS  Google Scholar 

  14. VanBuren, P., Palmiter, K. A., and Warshaw, D. M. (1999) Proc. Natl. Acad. Sci. USA, 96, 12488–12493.

    Article  PubMed  CAS  Google Scholar 

  15. Honda, H., Kitano, Y., Hatori, K., and Matsuno, K. (1996) FEBS Lett., 383, 55–58.

    Article  PubMed  CAS  Google Scholar 

  16. Purcell, I. F., Bing, W., and Marston, S. B. (1999) Cardiovasc. Res., 43, 884–891.

    Article  PubMed  CAS  Google Scholar 

  17. Fraser, I. D., and Marston, S. B. (1995) J. Biol. Chem., 270, 7836–7841.

    Article  PubMed  CAS  Google Scholar 

  18. Muthuchamy, M., Boivin, G. P., Grupp, I. L., and Wieczorek, D. F. (1998) J. Mol. Cell. Cardiol., 30, 1545–1557.

    Article  PubMed  CAS  Google Scholar 

  19. Yu, Z. B., Gao, F., Feng, H. Z., and Jin, J. P. (2007) Am. J. Physiol. Cell. Physiol., 292, 1192–1203.

    Article  Google Scholar 

  20. Izumo, S., Nadal-Ginard, B., and Mahdavi, V. (1988) Proc. Natl. Acad. Sci. USA, 85, 339–343.

    Article  PubMed  CAS  Google Scholar 

  21. Clarke, N. F. (2008) Adv. Exp. Med. Biol., 642, 40–54.

    Article  PubMed  CAS  Google Scholar 

  22. Tonge, D. P., Jones, S. W., Bardsley, R. G., and Parr, T. (2010) BMC Mol. Biol., 11, 52–59.

    Article  PubMed  Google Scholar 

  23. Schiaffino, S., and Reggiani, C. (2011) Physiol. Rev., 91, 1447–1531.

    Article  PubMed  CAS  Google Scholar 

  24. Margossian, S. S., and Lowey, S. (1982) Methods Enzymol., 85, Pt. B, 55–71.

    Article  PubMed  CAS  Google Scholar 

  25. Hayashi, H., Takiguchi, K., and Higashi-Fujime, S. (1989) J. Biochem. (Tokyo), 105, 875–877.

    CAS  Google Scholar 

  26. Saeki, K., Tokunaga, M., Ting, H. A., and Wakabayashi, T. (1989) J. Biochem. (Tokyo), 106, 606–611.

    CAS  Google Scholar 

  27. Unsworth, B. R., Witzmann, F. A., and Fitts, R. H. (1982) J. Biol. Chem., 257, 15129–15136.

    PubMed  CAS  Google Scholar 

  28. Laemmli, U. K. (1970) Nature, 227, 680–685.

    Article  PubMed  CAS  Google Scholar 

  29. Iorga, B., Adamek, N., and Geeves, M. A. J. (2007) Biol. Chem., 282, 3559–3570.

    CAS  Google Scholar 

  30. Bicer, S., and Reiser, P. J. J. (2004) Muscle Res. Cell Motil., 25, 623–633.

    Article  CAS  Google Scholar 

  31. Pardee, J. D., and Spudich, J. A. (1982) Methods Cell Biol., 24, 271–289.

    Article  PubMed  CAS  Google Scholar 

  32. Smillie, L. B. (1982) Methods Enzymol., 85, Pt. B, 234–241.

    Article  PubMed  CAS  Google Scholar 

  33. Bronson, D. D., and Schachat, F. H. (1982) J. Biol. Chem., 257, 3937–3944.

    PubMed  CAS  Google Scholar 

  34. Mashanov, G. I., and Molloy, J. E. (2007) Biophys. J., 92, 2199–2211.

    Article  PubMed  CAS  Google Scholar 

  35. Gordon, A. M., LaMadrid, M. A., Chen, Y., Luo, Z., and Chase, P. B. (1997) Biophys. J., 72, 1295–1307.

    Article  PubMed  CAS  Google Scholar 

  36. Singh, A., and Hitchcock-DeGregori, S. E. (2007) Biochemistry, 46, 14917–14927.

    Article  PubMed  CAS  Google Scholar 

  37. Oguchi, Y., Ishizuka, J., Hitchcock-DeGregori, S. E., Ishiwata, S., and Kawai, M. (2011) J. Mol. Biol., 414, 667–680.

    Article  PubMed  CAS  Google Scholar 

  38. Ali, L. F., Cohen, J. M., and Tobacman, L. S. (2010) Biochemistry, 49, 10873–10880.

    Article  PubMed  CAS  Google Scholar 

  39. Lu, X., Tobacman, L. S., and Kawai, M. (2006) Biophys. J., 91, 4230–4240.

    Article  PubMed  CAS  Google Scholar 

  40. Kawai, M., Lu, X., Hitchcock-Degregori, S. E., Stanton, K. J., and Wandling, M. W. (2009) J. Biophys., 2009, 380–967.

    Google Scholar 

  41. Chen, W., Wen, K. K., Sens, A. E., and Rubenstein, P. A. (2006) Biophys. J., 90, 1308–1318.

    Article  PubMed  CAS  Google Scholar 

  42. Sliwinska, M., Zukowska, M., Borys, D., and Moraczewska, J. (2011) Cytoskeleton (Hoboken), 68, 300–312.

    Article  CAS  Google Scholar 

  43. Rajan, S., Jagatheesan, G., Karam, C. N., Alves, M. L., Bodi, I., Schwartz, A., Bulcao, C. F., D’Souza, K. M., Akhter, S. A., Boivin, G. P., Dube, D. K., Petrashevskaya, N., Herr, A. B., Hullin, R., Liggett, S. B., Wolska, B. M., Solaro, R. J., and Wieczorek, D. F. (2010) Circulation, 121, 410–418.

    Article  PubMed  CAS  Google Scholar 

  44. Kalyva, A., Schmidtmann, A., and Geeves, M. A. (2012) Biochemistry, 51, 6388–6399.

    Article  PubMed  CAS  Google Scholar 

  45. Ajtai, K., Halstead, M. F., Nyitrai, M., Penheiter, A. R., Zheng, Y., and Burghardt, T. P. (2009) Biochemistry, 48, 5263–5275.

    Article  PubMed  CAS  Google Scholar 

  46. Oztug Durer, Z. A., Kamal, J. K., Benchaar, S., Chance, M. R., and Reisler, E. (2011) J. Mol. Biol., 414, 204–216.

    Article  PubMed  CAS  Google Scholar 

  47. Borovikov, Y. S., Dedova, I. V., dos Remedios, C. G., Vikhoreva, N. N., Vikhorev, P. G., Avrova, S. V., Hazlett, T. L., and Van Der Meer, B. W. (2004) Biophys. J., 86, 3020–3029.

    Article  PubMed  CAS  Google Scholar 

  48. Shchepkin, D. V., Kopylova, G. V., and Nikitina, L. V. (2011) Biochem. Biophys. Res. Commun., 415, 104–108.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. V. Nikitina.

Additional information

Original Russian Text © G. V. Kopylova, D. V. Shchepkin, L. V. Nikitina, 2013, published in Biokhimiya, 2013, Vol. 78, No. 3, pp. 348–356.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kopylova, G.V., Shchepkin, D.V. & Nikitina, L.V. Study of regulatory effect of tropomyosin on actin-myosin interaction in skeletal muscle by in vitro motility assay. Biochemistry Moscow 78, 260–266 (2013). https://doi.org/10.1134/S0006297913030073

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297913030073

Key words

Navigation