Table of Contents
Journal of Biophysics
Volume 2015 (2015), Article ID 465693, 9 pages
http://dx.doi.org/10.1155/2015/465693
Research Article

Flexural Stiffness of Myosin Va Subdomains as Measured from Tethered Particle Motion

1Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, VT 05405, USA
2Department of Mechanical & Aeronautical Engineering, Clarkson University, Potsdam, NY 13699, USA

Received 25 August 2015; Revised 29 October 2015; Accepted 8 November 2015

Academic Editor: Andrei B. Rubin

Copyright © 2015 Arthur J. Michalek et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. D. Mehta, R. S. Rock, M. Rief, J. A. Spudich, M. S. Mooseker, and R. E. Cheney, “Myosin-V is a processive actin-based motor,” Nature, vol. 400, no. 6744, pp. 590–593, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. J. P. Holt, K. Bottomly, and M. S. Mooseker, “Assessment of myosin II, Va, VI and VIIa loss of function on endocytosis and endocytic vesicle motility in bone marrow-derived dendritic cells,” Cell Motility and the Cytoskeleton, vol. 64, no. 10, pp. 756–766, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. J. R. Sellers and L. S. Weisman, Myosin V., vol. 7 of Proteins and Cell Regulation, 2008.
  4. R. E. Cheney, M. K. O'Shea, J. E. Heuser et al., “Brain myosin-V is a two-headed unconventional myosin with motor activity,” Cell, vol. 75, no. 1, pp. 13–23, 1993. View at Publisher · View at Google Scholar · View at Scopus
  5. P.-D. Coureux, H. L. Sweeney, and A. Houdusse, “Three myosin V structures delineate essential features of chemo-mechanical transduction,” The EMBO Journal, vol. 23, no. 23, pp. 4527–4537, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Sakamoto, M. R. Webb, E. Forgacs, H. D. White, and J. R. Sellers, “Direct observation of the mechanochemical coupling in myosin Va during processive movement,” Nature, vol. 455, no. 7209, pp. 128–132, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Kodera, D. Yamamoto, R. Ishikawa, and T. Ando, “Video imaging of walking myosin V by high-speed atomic force microscopy,” Nature, vol. 468, no. 7320, pp. 72–76, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. D. M. Warshaw, G. G. Kennedy, S. S. Work, E. B. Krementsova, S. Beck, and K. M. Trybus, “Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity,” Biophysical Journal, vol. 88, no. 5, pp. L30–L32, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Yildiz, J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldman, and P. R. Selvin, “Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization,” Science, vol. 300, no. 5628, pp. 2061–2065, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. J. R. Sellers and C. Veigel, “Walking with myosin V,” Current Opinion in Cell Biology, vol. 18, no. 1, pp. 68–73, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. D. N. Krementsov, E. B. Krementsova, and K. M. Trybus, “Myosin V: regulation by calcium, calmodulin, and the tail domain,” Journal of Cell Biology, vol. 164, no. 6, pp. 877–886, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Lu, E. B. Krementsova, and K. M. Trybus, “Regulation of myosin V processivity by calcium at the single molecule level,” The Journal of Biological Chemistry, vol. 281, no. 42, pp. 31987–31994, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Sakamoto, I. Amitani, E. Yokota, and T. Ando, “Direct observation of processive movement by individual myosin V molecules,” Biochemical and Biophysical Research Communications, vol. 272, no. 2, pp. 586–590, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Y. Ali, E. B. Krementsova, G. G. Kennedy et al., “Myosin Va maneuvers through actin intersections and diffuses along microtubules,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 11, pp. 4332–4336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Y. Ali, S. B. Previs, K. M. Trybus, H. L. Sweeney, and D. M. Warshaw, “Myosin VI has a one track mind versus myosin va when moving on actin bundles or at an intersection,” Traffic, vol. 14, no. 1, pp. 70–81, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. S. R. Nelson, M. Y. Ali, K. M. Trybus, and D. M. Warshaw, “Random walk of processive, quantum dot-labeled myosin Va molecules within the actin cortex of COS-7 cells,” Biophysical Journal, vol. 97, no. 2, pp. 509–518, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. C. M. Brawley and R. S. Rock, “Unconventional myosin traffic in cells reveals a selective actin cytoskeleton,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 24, pp. 9685–9690, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. B. D. Dunn, T. Sakamoto, M.-S. S. Hong, J. R. Sellers, and P. A. Takizawa, “Myo4p is a monomeric myosin with motility uniquely adapted to transport mRNA,” The Journal of Cell Biology, vol. 178, no. 7, pp. 1193–1206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Shiroguchi and K. Kinosita Jr., “Myosin V walks by lever action and Brownian motion,” Science, vol. 316, no. 5828, pp. 1208–1212, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. M. L. Walker, S. A. Burgess, J. R. Sellers et al., “Two-headed binding of a processive myosin to F-actin,” Nature, vol. 405, no. 6788, pp. 804–807, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Vilfan, “Elastic lever-arm model for myosin V,” Biophysical Journal, vol. 88, no. 6, pp. 3792–3805, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. P. C. Nelson, C. Zurla, D. Brogioli, J. F. Beausang, L. Finzi, and D. Dunlap, “Tethered particle motion as a diagnostic of DNA tether length,” Journal of Physical Chemistry B, vol. 110, no. 34, pp. 17260–17267, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. N. Pouget, C. Dennis, C. Turlan, M. Grigoriev, M. Chandler, and L. Salomé, “Single-particle tracking for DNA tether length monitoring,” Nucleic Acids Research, vol. 32, no. 9, article e73, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. D. A. Schafer, J. Gellest, M. P. Sheetz, and R. Landick, “Transcription by single molecules of RNA polymerase observed by light microscopy,” Nature, vol. 352, no. 6334, pp. 444–448, 1991. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Yin, R. Landick, and J. Gelles, “Tethered particle motion method for studying transcript elongation by a single RNA polymerase molecule,” Biophysical Journal, vol. 67, no. 6, pp. 2468–2478, 1994. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Brinkers, H. R. C. Dietrich, F. H. De Groote, I. T. Young, and B. Rieger, “The persistence length of double stranded DNA determined using dark field tethered particle motion,” Journal of Chemical Physics, vol. 130, no. 21, Article ID 215105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. X.-D. Li, S. J. Hyun, K. Mabuchi, R. Craig, and M. Ikebe, “The globular tail domain of myosin Va functions as an inhibitor of the myosin Va motor,” The Journal of Biological Chemistry, vol. 281, no. 31, pp. 21789–21798, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. J. E. Baker, E. B. Krementsova, G. G. Kennedy, A. Armstrong, K. M. Trybus, and D. M. Warshaw, “Myosin V processivity: multiple kinetic pathways for head-to-head coordination,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 15, pp. 5542–5546, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. J. R. Moore, E. B. Krementsova, K. M. Trybus, and D. M. Warshaw, “Does the myosin V neck region act as a lever?” Journal of Muscle Research and Cell Motility, vol. 25, no. 1, pp. 29–35, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. J. E. Cronan Jr., “Biotination of proteins in vivo: a post-translational modification to label, purify, and study proteins,” The Journal of Biological Chemistry, vol. 265, no. 18, pp. 10327–10333, 1990. View at Google Scholar · View at Scopus
  31. D. M. Warshaw, J. M. Desrosiers, S. S. Work, and K. M. Trybus, “Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity in vitro,” The Journal of Cell Biology, vol. 111, no. 2, pp. 453–463, 1990. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Y. Ali, H. Lu, C. S. Bookwalter, D. M. Warshaw, and K. M. Trybus, “Myosin V and Kinesin act as tethers to enhance each others' processivity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 12, pp. 4691–4696, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. V. G. Mavrantzas and A. N. Beris, “A hierarchical model for surface effects on chain conformation and rheology of polymer solutions. II. Application to a neutral surface,” Journal of Chemical Physics, vol. 110, no. 1, pp. 628–638, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Ram, P. Prabhat, J. Chao, E. S. Ward, and R. J. Ober, “High accuracy 3D quantum dot tracking with multifocal plane microscopy for the study of fast intracellular dynamics in live cells,” Biophysical Journal, vol. 95, no. 12, pp. 6025–6043, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Howard and J. A. Spudich, “Is the lever arm of myosin a molecular elastic element?” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 9, pp. 4462–4464, 1996. View at Google Scholar · View at Scopus
  36. C. Veigel, S. Schmitz, F. Wang, and J. R. Sellers, “Load-dependent kinetics of myosin-V can explain its high processivity,” Nature Cell Biology, vol. 7, no. 9, pp. 861–869, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Nguyen and H. Higuchi, “Motility of myosin V regulated by the dissociation of single calmodulin,” Nature Structural and Molecular Biology, vol. 12, no. 2, pp. 127–132, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Zhang, M. Yusuf Ali, D. M. Warshaw, and N. M. Kad, “A branched kinetic scheme describes the mechanochemical coupling of myosin va processivity in response to substrate,” Biophysical Journal, vol. 103, no. 4, pp. 728–737, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. K. M. Trybus, “Myosin V from head to tail,” Cellular and Molecular Life Sciences, vol. 65, no. 9, pp. 1378–1389, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Liu, D. W. Taylor, E. B. Krementsova, K. M. Trybus, and K. A. Taylor, “Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography,” Nature, vol. 442, no. 7099, pp. 208–211, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Thirumurugan, T. Sakamoto, J. A. Hammer III, J. R. Sellers, and P. J. Knight, “The cargo-binding domain regulates structure and activity of myosin 5,” Nature, vol. 442, no. 7099, pp. 212–215, 2006. View at Publisher · View at Google Scholar · View at Scopus