Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

The core of the motor domain determines the direction of myosin movement

Nature volume 412, pages 831–834 (2001)Cite this article

Abstract

Myosins constitute a superfamily of at least 18 known classes of molecular motors that move along actin filaments1,2,3. Myosins move towards the plus end of F-actin filaments; however, it was shown recently that a certain class of myosin, class VI myosin, moves towards the opposite end of F-actin, that is, in the minus direction4. As there is a large, unique insertion in the myosin VI head domain between the motor domain and the light-chain-binding domain (the lever arm), it was thought that this insertion alters the angle of the lever-arm switch movement, thereby changing the direction of motility4. Here we determine the direction of motility of chimaeric myosins that comprise the motor domain and the lever-arm domain (containing an insert) from myosins that have movement in the opposite direction. The results show that the motor core domain, but neither the large insert nor the converter domain, determines the direction of myosin motility.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structure of myosin constructs.
Figure 2: Direction of the movement of myosin constructs.

Similar content being viewed by others

References

  1. Mooseker, M. S. & Cheney, R. E. Unconventional myosins. Annu. Rev. Cell Dev. Biol. 11, 633–675 (1995).

    Article  CAS  PubMed  Google Scholar 

  2. Titus, M. A. Unconventional myosins: new frontiers in actin-based motors. Trends Cell Biol. 7, 119–123 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Hodge, T. & Cope, M. J. A myosin family tree. J. Cell Sci. 113, 3353–3354 (2000).

    CAS  PubMed  Google Scholar 

  4. Wells, A. L. et al. Myosin VI is an actin-based motor that moves backwards. Nature 401, 505–508 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Kellerman, K. A. & Miller, K. G. An unconventional myosin heavy chain gene from Drosophila melanogaster. J. Cell Biol. 119, 823–834 (1992).

    Article  CAS  PubMed  Google Scholar 

  6. Hasson, T. & Mooseker, M. S. Porcine myosin VI: characterization of a new mammalian unconventional myosin. J. Cell Biol. 127, 425–440 (1994).

    Article  CAS  PubMed  Google Scholar 

  7. Hasson, T. et al. Unconventional myosin in inner ear sensory epithelia. J. Cell Biol. 137, 1287–1307 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Baker, J. P. & Titus, M. A. A family of unconventional myosins from the nematode Caenorhabditis elegans. J. Mol. Biol. 272, 523–535 (1997).

    Article  CAS  PubMed  Google Scholar 

  9. Mermall,V., McNally, J. G. & Miller, K. G. Transport of cytoplasmic particle catalyzed by an unconventional myosin in living Drosophila embryo. Nature 369, 560–562 (1994).

    Article  ADS  Google Scholar 

  10. Avraham, K. B. et al. The mouse Snell's walzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nature Genet. 11, 369–375 (1995).

    Article  CAS  PubMed  Google Scholar 

  11. Kelleher, J. F. et al. Myosin VI is required for asymmetric segregation of cellular components during C. elegans spermatogenesis. Curr. Biol. 10, 1489–1496 (2000).

    Article  CAS  PubMed  Google Scholar 

  12. Mehta, A. D. et al. Myosin-V is a processive actin-based motor. Nature 400, 590–593 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Walker, M. L. et al. Two-headed binding of a processive myosin to F-actin. Nature 405, 804–807 (2000).

    Article  ADS  CAS  PubMed  Google Scholar 

  14. Sakamoto, T., Amitani, I., Yokota, E. & Ando, T. Direct observation of processive movement by individual myosin V molecules. Biochem. Biophys. Res. Commun. 272, 586–590 (2000).

    Article  CAS  PubMed  Google Scholar 

  15. Endow, S. A. & Waligora, K. W. Determination of kinesin motor polarity. Science 281, 1200–1202 (1998).

    Article  ADS  CAS  PubMed  Google Scholar 

  16. Sablin, E. P. et al. Direction determination in the minus-end-directed kinesin motor ncd. Nature 395, 813–816 (1998).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Endow, S. A. & Higuchi, H. A mutant of the motor protein kinesin that moves in both directions on microtubules. Nature 406, 913–916 (2000).

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Houdusse, A., Kalabokis,V. N., Himmel, D., Szent-Gyorgyi, A. G. & Cohen, C. Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97, 459–470 (1999).

    Article  CAS  PubMed  Google Scholar 

  19. Dominguez, R., Freyzon, Y., Trybus, K. M. & Cohen, C. Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state. Cell 94, 559–571 (1998).

    Article  CAS  PubMed  Google Scholar 

  20. Smith, C. A. & Rayment, I. X-ray structure of the magnesium(II).ADP.vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 Å resolution. Biochemistry 35, 5404–5417 (1996).

    Article  CAS  PubMed  Google Scholar 

  21. Spudich, J. A. & Watt, J. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866–4871 (1971).

    CAS  PubMed  Google Scholar 

  22. Chien, Y. H. & Dawid, I. B. Isolation and characterization of calmodulin genes from Xenopus laevis. Mol. Cell. Biol. 4, 507–513 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhu, T., Sata, M. & Ikebe, M. Functional expression of mammalian myosin Iβ: analysis of its motor activity. Biochemistry 35, 513–522 (1996).

    Article  CAS  PubMed  Google Scholar 

  24. Homma, K., Saito, J., Ikebe, R. & Ikebe, M. Ca2+ dependent regulation of the motor activity of myosin V. J. Biol. Chem. 275, 34766–34771 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. Ikebe, M. & Hartshorne, D. J. Effects of Ca2+ on the conformation and enzymatic activity of smooth muscle myosin. J. Biol. Chem. 260, 13146–13153 (1985).

    CAS  PubMed  Google Scholar 

  26. Sata, M., Matsuura, M. & Ikebe, M. Characterization of the motor and enzymatic properties of smooth muscle long S1 and short HMM: role of the two-headed structure on the activity and regulation of the myosin motor. Biochemistry 35, 11113–11118 (1996).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank N. Jenkins and K. Avraham for sending us the cDNA fragments of mouse myosin V and mouse myosin VI. We also thank D. J. Schmidt for reading the manuscript.

Author information

Authors and Affiliations

  1. Department of Physiology, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, 01655-0127, Massachusetts, USA

    Kazuaki Homma, Misako Yoshimura, Junya Saito, Reiko Ikebe & Mitsuo Ikebe

Authors
  1. Kazuaki Homma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Misako Yoshimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junya Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Reiko Ikebe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mitsuo Ikebe
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Homma, K., Yoshimura, M., Saito, J. et al. The core of the motor domain determines the direction of myosin movement. Nature 412, 831–834 (2001). https://doi.org/10.1038/35090597

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35090597

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing