Biochemistry (Moscow)

, Volume 78, Issue 3, pp 260–266

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

  • G. V. Kopylova
  • D. V. Shchepkin
  • L. V. Nikitina
Article

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.

Key words

skeletal myosin isoforms tropomyosin isoforms in vitro motility assay 

Abbreviations

actin-TM

actin-tropomyosin filament

F-actin

filamentary actin

RhPh-F-actin

filamentary actin stained with phalloidin-tetramethylrhodamine

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Barany, M. (1967) J. Gen. Physiol., 50, 197–218.PubMedCrossRefGoogle Scholar
  2. 2.
    Marston, S. B., and Taylor, E. W. (1980) J. Mol. Biol., 139, 573–600.PubMedCrossRefGoogle Scholar
  3. 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.PubMedCrossRefGoogle Scholar
  4. 4.
    Perry, S. V. (2001) J. Muscle Res. Cell. Motil., 22, 5–49.PubMedCrossRefGoogle Scholar
  5. 5.
    Boussouf, S. E., Maytum, R., Jaquet, K., and Geeves, M. A. (2007) J. Muscle Res. Cell. Moti., 28, 49–58.CrossRefGoogle Scholar
  6. 6.
    Gordon, A. M., Homsher, E., and Regnier, M. (2000) Physiol. Rev., 80, 853–924.PubMedGoogle Scholar
  7. 7.
    McKillop, D. F., and Geeves, M. A. (1993) Biophys. J., 65, 693–701.PubMedCrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. 10.
    Chandy, I. K., Lo, J. C., and Ludescher, R. D. (1999) Biochemistry, 38, 9286–9294.PubMedCrossRefGoogle Scholar
  11. 11.
    Landis, C. A., Bobkova, A., Homsher, E., and Tobacman, L. S. (1997) J. Biol. Chem., 272, 14051–14056.PubMedCrossRefGoogle Scholar
  12. 12.
    Landis, C., Back, N., Homsher, E., and Tobacman, L. S. (1999) J. Biol. Chem., 274, 31279–31285.PubMedCrossRefGoogle Scholar
  13. 13.
    Lehrer, S. S., and Morris, E. P. (1982) J. Biol. Chem., 257, 8073–8080.PubMedGoogle Scholar
  14. 14.
    VanBuren, P., Palmiter, K. A., and Warshaw, D. M. (1999) Proc. Natl. Acad. Sci. USA, 96, 12488–12493.PubMedCrossRefGoogle Scholar
  15. 15.
    Honda, H., Kitano, Y., Hatori, K., and Matsuno, K. (1996) FEBS Lett., 383, 55–58.PubMedCrossRefGoogle Scholar
  16. 16.
    Purcell, I. F., Bing, W., and Marston, S. B. (1999) Cardiovasc. Res., 43, 884–891.PubMedCrossRefGoogle Scholar
  17. 17.
    Fraser, I. D., and Marston, S. B. (1995) J. Biol. Chem., 270, 7836–7841.PubMedCrossRefGoogle Scholar
  18. 18.
    Muthuchamy, M., Boivin, G. P., Grupp, I. L., and Wieczorek, D. F. (1998) J. Mol. Cell. Cardiol., 30, 1545–1557.PubMedCrossRefGoogle Scholar
  19. 19.
    Yu, Z. B., Gao, F., Feng, H. Z., and Jin, J. P. (2007) Am. J. Physiol. Cell. Physiol., 292, 1192–1203.CrossRefGoogle Scholar
  20. 20.
    Izumo, S., Nadal-Ginard, B., and Mahdavi, V. (1988) Proc. Natl. Acad. Sci. USA, 85, 339–343.PubMedCrossRefGoogle Scholar
  21. 21.
    Clarke, N. F. (2008) Adv. Exp. Med. Biol., 642, 40–54.PubMedCrossRefGoogle Scholar
  22. 22.
    Tonge, D. P., Jones, S. W., Bardsley, R. G., and Parr, T. (2010) BMC Mol. Biol., 11, 52–59.PubMedCrossRefGoogle Scholar
  23. 23.
    Schiaffino, S., and Reggiani, C. (2011) Physiol. Rev., 91, 1447–1531.PubMedCrossRefGoogle Scholar
  24. 24.
    Margossian, S. S., and Lowey, S. (1982) Methods Enzymol., 85, Pt. B, 55–71.PubMedCrossRefGoogle Scholar
  25. 25.
    Hayashi, H., Takiguchi, K., and Higashi-Fujime, S. (1989) J. Biochem. (Tokyo), 105, 875–877.Google Scholar
  26. 26.
    Saeki, K., Tokunaga, M., Ting, H. A., and Wakabayashi, T. (1989) J. Biochem. (Tokyo), 106, 606–611.Google Scholar
  27. 27.
    Unsworth, B. R., Witzmann, F. A., and Fitts, R. H. (1982) J. Biol. Chem., 257, 15129–15136.PubMedGoogle Scholar
  28. 28.
    Laemmli, U. K. (1970) Nature, 227, 680–685.PubMedCrossRefGoogle Scholar
  29. 29.
    Iorga, B., Adamek, N., and Geeves, M. A. J. (2007) Biol. Chem., 282, 3559–3570.Google Scholar
  30. 30.
    Bicer, S., and Reiser, P. J. J. (2004) Muscle Res. Cell Motil., 25, 623–633.CrossRefGoogle Scholar
  31. 31.
    Pardee, J. D., and Spudich, J. A. (1982) Methods Cell Biol., 24, 271–289.PubMedCrossRefGoogle Scholar
  32. 32.
    Smillie, L. B. (1982) Methods Enzymol., 85, Pt. B, 234–241.PubMedCrossRefGoogle Scholar
  33. 33.
    Bronson, D. D., and Schachat, F. H. (1982) J. Biol. Chem., 257, 3937–3944.PubMedGoogle Scholar
  34. 34.
    Mashanov, G. I., and Molloy, J. E. (2007) Biophys. J., 92, 2199–2211.PubMedCrossRefGoogle Scholar
  35. 35.
    Gordon, A. M., LaMadrid, M. A., Chen, Y., Luo, Z., and Chase, P. B. (1997) Biophys. J., 72, 1295–1307.PubMedCrossRefGoogle Scholar
  36. 36.
    Singh, A., and Hitchcock-DeGregori, S. E. (2007) Biochemistry, 46, 14917–14927.PubMedCrossRefGoogle Scholar
  37. 37.
    Oguchi, Y., Ishizuka, J., Hitchcock-DeGregori, S. E., Ishiwata, S., and Kawai, M. (2011) J. Mol. Biol., 414, 667–680.PubMedCrossRefGoogle Scholar
  38. 38.
    Ali, L. F., Cohen, J. M., and Tobacman, L. S. (2010) Biochemistry, 49, 10873–10880.PubMedCrossRefGoogle Scholar
  39. 39.
    Lu, X., Tobacman, L. S., and Kawai, M. (2006) Biophys. J., 91, 4230–4240.PubMedCrossRefGoogle Scholar
  40. 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. 41.
    Chen, W., Wen, K. K., Sens, A. E., and Rubenstein, P. A. (2006) Biophys. J., 90, 1308–1318.PubMedCrossRefGoogle Scholar
  42. 42.
    Sliwinska, M., Zukowska, M., Borys, D., and Moraczewska, J. (2011) Cytoskeleton (Hoboken), 68, 300–312.CrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 44.
    Kalyva, A., Schmidtmann, A., and Geeves, M. A. (2012) Biochemistry, 51, 6388–6399.PubMedCrossRefGoogle Scholar
  45. 45.
    Ajtai, K., Halstead, M. F., Nyitrai, M., Penheiter, A. R., Zheng, Y., and Burghardt, T. P. (2009) Biochemistry, 48, 5263–5275.PubMedCrossRefGoogle Scholar
  46. 46.
    Oztug Durer, Z. A., Kamal, J. K., Benchaar, S., Chance, M. R., and Reisler, E. (2011) J. Mol. Biol., 414, 204–216.PubMedCrossRefGoogle Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. 48.
    Shchepkin, D. V., Kopylova, G. V., and Nikitina, L. V. (2011) Biochem. Biophys. Res. Commun., 415, 104–108.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  • G. V. Kopylova
    • 1
  • D. V. Shchepkin
    • 1
  • L. V. Nikitina
    • 1
  1. 1.Institute of Immunology and PhysiologyUral Division of the Russian Academy of SciencesEkaterinburgRussia

Personalised recommendations