Load-dependent kinetics of myosin-V can explain its high processivity

Nature Cell Biology

Volumn 7, Issue 9, 2005, Pages 861-869

  Veigel, Claudia ^a   Schmitz, Stephan ^a   Wang, Fei ^b   Sellers, James R ^b  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

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

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; MYOSIN V; ACTIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; MOLECULAR MOTOR;

ACTIN MYOSIN INTERACTION; ARTICLE; BINDING KINETICS; CONTROLLED STUDY; DIFFUSION; FORCE TRANSDUCER; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN PROCESSING; RABBIT; ANIMAL; BINDING SITE; BIOMECHANICS; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; MECHANICAL STRESS; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; WEIGHT BEARING;

ORYCTOLAGUS CUNICULUS;

ACTINS; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; BIOMECHANICS; CHICKENS; MICE; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; MYOSIN TYPE V; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; RABBITS; STRESS, MECHANICAL; WEIGHT-BEARING;

EID: 26944449015     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1287     Document Type: Article

References (41)

1. Reck-Peterson, S., Provance, D. W., Mooseker, M. S. & Mercer, J. A. Review: Class V myosins. Biochim. Biophys. Acta 1496, 36-51 (2000).
2. Sellers, J. R. Myosins (Oxford University Press, Oxford, 1999).
3. Cheney, R. E. et al. Brain Myosin-V is a two-headed unconventional myosin with motor activity. Cell 75, 13-23 (1993).
4. Miller, E. & Sheetz, M. P. Characterization of myosin-V binding to brain vesicles. J. Biol. Chem. 275, 2598-2606 (2000).
5. Vale, R. D. Myosin V motor proteins: Marching stepwise towards a mechanism. J. Cell Biol. 163, 445-450 (2003).
6. Mehta, A. D. et al. Myosin-V is a processive actin-based motor. Nature 400, 590-593 (1999).
7. Rief, M. et al. Myosin-V stepping kinetics: A molecular model for processivity. Proc. Natl Acad. Sci. 97, 9482-9486 (2000).
8. Sakamoto, T., Amitani, I., Yokota, E. & Ando, T. Direct observation of processive movement by individual myosin-V molecules. Biochem. Biophys. Res. Comm. 272, 586-590 (2000).
9. Sakamoto, T. et al. Neck length and processivity of myosin-V. J. Biol. Chem. 278, 29201-29207 (2003).
10. Yildiz, A. et al. Myosin-V walks hand over hand: Single fluorophore imaging with 1.5nm localisation. Science 300, 2061-2065 (2003).
11. Forkey, J. N., Quinlan, M. E., Shaw, M. A., Corrie, J. E. & Goldman, Y. E. Three dimensional structural dynamics of myosin-V by single-molecule fluorescence polarisation. Nature 422, 399-404 (2003).
12. Walker, M. et al. Two-headed binding of a processive myosin to F-actin. Nature 405, 804-807 (2000).
13. Veigel, C., Wang, F., Bartoo, M. L., Sellers, J. R. & Molloy, J. E. The gated gait of the processive molecular motor myosin-V. Nature Cell Biol. 4, 59-65 (2002).
14. Ali, M. Y. et al. Myosin-V is a left-handed spiral motor on the right-handed actin helix. Nature Struct. Biol. 9, 464-467 (2002).
15. Tanaka, H. et al. The motor domain determines the large step of myosin V. Nature 415, 192-195 (2002).
16. Schnitzer, M. J. & Block, S. M. Statistical kinetics of processive enzymes. Cold Spring Harb. Symp. Quant. Biol. 60, 793-802 (1995).
17. Kolomeisky, A. B. & Fisher, M. E. A simple kinetic model describes the processivity of myosin-V. Biophys. J. 84, 1642-1650 (2003).
18. Lan, G. & Sun, S. X. Dynamics of myosin processivity. Biophys. J. 88, 4107-4117 (2005).
19. 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).
20. Purcell, T. J., Morris, C., Spudich, J. A. & Sweeney, H. L. Role of the lever arm in the processive stepping of myosin-V. Proc. Natl Acad. Sci. USA 92, 14159-14164 (2002).
21. Huxley, A. F. Muscle structure and theories of contraction. Progr. Biophys. Biophys. Chem. 7, 255-318 (1957).
22. 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. 96, 13726-13731 (1999).
23. Baker, J. E. et al. Myosin-V processivity: Multiple kinetic pathways for head-to-head coordination. Proc. Natl Acad. Sci. USA 101, 5542-5546 (2004).
24. Clemen, A. E. et al. Force dependent stepping kinetics of myosin-V. Biophys. J. 88, 4402-4410 (2005).
25. 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).
26. Uemura, S., Higuchi, H., Olivares, A. O., DeLaCruz, E. M. & Ishiwata, S. Mechanochemical coupling of two substeps in a single myosin-V motor. Nature Struct. Biol. 11, 877-883 (2004).
27. Rosenfeld, S. S. & Sweeney, H. L. A model for myosin-V processivity. J. Biol. Chem. 279, 40100-40111 (2004).
28. 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).
29. Veigel, C., Bartoo, M. L., White, D. C. S, Sparrow, J. C. & Molloy, J. E. The stiffness of rabbit skeletal, acto-myosin crossbridges determined with an optical tweezers transducer. Biophys. J. 75, 1424-1438 (1998).
30. Wang, F. et al. Effect of ADP and ionic strength on the kinetic and motile properties of recombinant mouse myosin-V. J. Biol. Chem. 275, 4329-4335 (2000).
31. Veigel, C. et al. The motor protein myosin-I produces its working stroke in two steps. Nature 398, 530-533 (1999).
32. Veigel, C., Molloy, J. E., Schmitz, S. & Kendrick-Jones, J. Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nature Cell Biol. 5, 980-986 (2003).
33. Howard, J. Mechanics of Motor Proteins and the Cytoskeleton (Sinauer Associates, Inc., Sunderland, 2001).
34. Lymn, R. W. & Taylor, E. W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624 (1971).
35. Burgess, S. et al. The prepower stroke conformation of myosin-V. J. Cell Biol. 159, 983-991 (2002).
36. Whittaker, M. et al. A 35-Å movement of smooth muscle myosin on ADP release. Nature 378, 748-751 (1995).
37. Berger, C. E. M, Fagnant, P. M., Heizmann, S., Trybus, K. M. & Geeves, M. A. ADP binding induces and asymmetry between the heads of unphosphorylated myosin J. Biol. Chem. 276, 23240-23245 (2001).
38. Lombardi, V. et al. Elastic distortion of the myosin head and repriming of the working stroke in muscle. Nature 374, 553-555 (1995).
39. Cheney, R. E. Purification and assay of myosin-V. Methods Enzymol. 298, 3-18 (1998).
40. Mehta, A. D., Finer, J. T. & Spudich, J. A. Stiffness of muscle myosin. Detection of single-molecule interactions using correlated thermal diffusion. Proc. Natl Acad. Sci. USA 94, 7927-7931 (1997).
41. Tyska, M. J. et al. Two heads of myosin are better than one for generating force and motion. Proc. Natl. Acad. Sci. USA 96, 4402-4407 (1999).