Direct observation of the myosin-Va power stroke and its reversal

Nature Structural and Molecular Biology

Volumn 17, Issue 5, 2010, Pages 590-595

  Sellers, James R ^a   Veigel, Claudia ^b,c  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN VA;

ARTICLE; ASSAY; CELL FUNCTION; CONFORMATION; CONFORMATIONAL TRANSITION; OSCILLATION; PRIORITY JOURNAL; PROTEIN BINDING; STROKE;

ACTINS; ANIMALS; BIOMECHANICS; MICE; MYOSIN TYPE V; PROTEIN BINDING;

EID: 77951978236     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1820     Document Type: Article

References (47)

1. Sellers, J.R. & Veigel, C. Walking with myosin V. Curr. Opin. Cell Biol. 18, 68-73 (2006).
2. Mehta, A.D. et al. Myosin-V is a processive actin-based motor. Nature 400, 590-593 (1999).
3. Sakamoto, T., Webb, M.R., Forgacs, E., White, H.D. & Sellers, J.R. Direct observation of the mechanochemical coupling in myosin Va during processive movement. Nature 455, 128-132 (2008).
4. Veigel, C., Wang, F., Bartoo, M.L., Sellers, J.R. & Molloy, J.E. The gated gait of the processive molecular motor, myosin V. Nat. Cell Biol. 4, 59-65 (2002).
5. Yildiz, A. et al. Myosin V walks hand-over-hand: Single fuorophore imaging with 1.5-nm localization. Science 300, 2061-2065 (2003).
6. De La Cruz, E.M., Wells, A.L., Rosenfeld, S.S., Ostap, E.M. & Sweeney, H.L. The kinetic mechanism of myosin V. Proc. Natl. Acad. Sci. USA 96, 13726-13731 (1999).
7. Rosenfeld, S.S. & Sweeney, H.L. A model of myosin V processivity. J. Biol. Chem. 279, 40100-40111 (2004).
8. Volkmann, N. et al. The structural basis of myosin V processive movement as revealed by electron cryomicroscopy. Mol. Cell 19, 595-605 (2005).
9. Coureux, P.D., Sweeney, H.L. & Houdusse, A. Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J. 23, 4527-4537 (2004).
10. Walker, M.L. et al. Two-headed binding of a processive myosin to F-actin. Nature 405, 804 (2000).
11. Burgess, S. et al. The prepower stroke conformation of myosin V. J. Cell Biol. 159, 983-991 (2002).
12. Forkey, J.N., Quinlan, M.E., Shaw, M.A., Corrie, J.E.T. & Goldman, Y.E. Three-dimensional structural dynamics of myosin V by single-molecule fuorescence polarization. Nature 422, 399-404 (2003).
13. Toprak, E. et al. Defocused orientation and position imaging (DOPI) of myosin V. Proc. Natl. Acad. Sci. USA 103, 6495-6499 (2006).
14. Dunn, A.R. & Spudich, J.A. Dynamics of the unbound head during myosin V processive translocation. Nat. Struct. Mol. Biol. 14, 246-248 (2007).
15. Cappello, G. et al. Myosin V stepping mechanism. Proc. Natl. Acad. Sci. USA 104, 15328-15333 (2007).
16. Uemura, S., Higuchi, H., Olivares, A.O., De La Cruz, E.M. & Ishiwata, S. Mechanochemical coupling of two substeps in a single myosin V motor. Nat. Struct. Mol. Biol. 11, 877-883 (2004).
17. Shiroguchi, K. & Kinosita, K. Myosin V walks by lever action and Brownian motion. Science 316, 1208-1212 (2007).
18. Rief, M. et al. Myosin-V stepping kinetics: a molecular model for processivity. Proc. Natl. Acad. Sci. USA 97, 9482-9486 (2000).
19. Gebhardt, J.C.M., Clemen, A.E.M., Jaud, J. & Rief, M. Myosin-V is a mechanical ratchet. Proc. Natl. Acad. Sci. USA 103, 8680-8685 (2006).
20. Carter, N.J. & Cross, R.A. Mechanics of the kinesin step. Nature 435, 308-312 (2005).
21. Veigel, C., Schmitz, S., Wang, F. & Sellers, J.R. Load-dependent kinetics of myosin-V can explain its high processivity. Nat. Cell Biol. 7, 861-869 (2005).
22. Finer, J.T., Simmons, R.M. & Spudich, J.A. Single myosin molecle mechanics-piconewton forces and nanometre steps. Nature 368, 113-119 (1994).
23. Veigel, C., Bartoo, M.L., White, D.C.S., Sparrow, J.C. & Molloy, J.E. The stiffness of rabbit skeletal actomyosin cross-bridges determined with an optical tweezers transducer. Biophys. J. 75, 1424-1438 (1998).
24. Molloy, J.E., Burns, J.E., Kendrick-Jones, J., Tregear, R.T. & White, D.C.S. Movement and force produced by a single myosin head. Nature 378, 209-212 (1995).
25. Veigel, C. et al. The motor protein myosin-I produces its working stroke in two steps. Nature 398, 530-533 (1999).
26. Robblee, J.P., Cao, W.X., Henn, A., Hannemann, D.E. & De La Cruz, E.M. Thermodynamics of nucleotide binding to actomyosin V and VI: a positive heat capacity change accompanies strong ADP binding. Biochemistry 44, 10238-10249 (2005).
27. Kad, N.M., Trybus, K.M. & Warshaw, D.M. Load and Pi control fux through the branched kinetic cycle of myosin V. J. Biol. Chem. 283, 17477-17484 (2008).
28. Takagi, Y., Shuman, H. & Goldman, Y.E. Coupling between phosphate release and force generation in muscle actomyosin. Phil. Trans. R. Soc. Lond. B 359, 1913-1920 (2004).
29. Moore, J.R., Krementsova, E.B., Trybus, K.M. & Warshaw, D.M. Myosin V exhibits a high duty cycle and large unitary displacement. J. Cell Biol. 155, 625-635 (2001).
30. Purcell, T.J., Sweeney, H.L. & Spudich, J.A. A force-dependent state controls the coordination of processive myosin V. Proc. Natl. Acad. Sci. USA 102, 13873-13878 (2005).
31. Huxley, A.F. & Simmons, R.M. Proposed mechanism of force generation in striated muscle. Nature 233, 533-538 (1971).
32. Oguchi, Y. et al. Load-dependent ADP binding to myosins V and VI: implications for subunit coordination and function. Proc. Natl. Acad. Sci. USA 105, 7714-7719 (2008).
33. Veigel, C., Molloy, J.E., Schmitz, S. & Kendrick-Jones, J. Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nat. Cell Biol. 5, 980-986 (2003).
34. Howard, J. Mechanics of Motor Proteins and the Cytoskeleton 76-89 (Sinauer, Sunderland, Massachusetts, USA, 2001).
35. Clemen, A.E.M. et al. Force-dependent stepping kinetics of myosin-V. Biophys. J. 88, 4402-4410 (2005).
36. Syed, S., Snyder, G.E., Franzini-Armstrong, C., Selvin, P.R. & Goldman, Y.E. Adaptability of myosin V studied by simultaneous detection of position and orientation. EMBO J. 25, 1795-1803 (2006).
37. Forgacs, E. et al. Kinetics of ADP dissociation from the trail and lead heads of actomyosin V following the power stroke. J. Biol. Chem. 283, 766-773 (2008).
38. Hannemann, D.E., Cao, W.X., Olivares, A.O., Robblee, J.P. & De La Cruz, E.M. Magnesium, ADP, and actin binding linkage of myosin V: evidence for multiple myosin V-ADP and actomyosin V-ADP states. Biochemistry 44, 8826-8840 (2005).
39. Vilfan, A. Elastic lever-arm model for myosin V. Biophys. J. 88, 3792-3805 (2005).
40. Nyitrai, M.G.M.A. Adenosine diphosphate and strain sensitivity in myosin motors. Phil. Trans. R. Soc. Lond. B 359, 1867-1877 (2004).
41. Nishizaka, T., Miyata, H., Yoshikawa, H., Ishiwata, S. & Kinosita, K. Unbinding force of a single motor molecule of muscle measured using optical tweezers. Nature 377, 251-254 (1995).
42. Duke, T.A.J. Molecular model of muscle contraction. Proc. Natl. Acad. Sci. USA 96, 2770-2775 (1999).
43. 2+. Biochem. Biophys. Res. Commun. 366, 233-238 (2008).
44. Hudspeth, A.J. & Gillespie, P.G. Pulling springs to tune transduction\adaptation by hair-cells. Neuron 12, 1-9 (1994).
45. Kruse, K. & Julicher, F. Oscillations in cell biology. Curr. Opin. Cell Biol. 17, 20-26 (2005).
46. van Mameren, J., Vermeulen, K.C., Gittes, F. & Schmidt, C.F. Leveraging single protein polymers to measure fexural rigidity. J. Phys. Chem. B 113, 3837-3844 (2009).
47. Colquhoun, D. & Sigworth, F.J. Practical analysis of records. in. Single Channel Recording (eds. Sakmann, B. & Neher, E.) 558-563 (Plenum Press, New York, USA, 1995).