Velocity, processivity, and individual steps of single myosin V molecules in live cells

Biophysical Journal

Volumn 96, Issue 10, 2009, Pages 4268-4275

  Pierobon, Paolo ^a   Achouri, Sarra ^a   Courty, Sébastien ^b,c   Dunn, Alexander R ^d   Spudich, James A ^d   Dahan, Maxime ^b,c   Cappello, Giovanni ^a  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN V; QUANTUM DOT; CALMODULIN; FLUORESCENT DYE; STREPTAVIDIN;

ARTICLE; CELL MOTILITY; CELL MOTION; CELL ORGANELLE; CONTROLLED STUDY; CYTOPLASM; FEMALE; HELA CELL; HUMAN; HUMAN CELL; ANIMAL; BIOTINYLATION; CELL SURVIVAL; INTRACELLULAR SPACE; METABOLISM; MOVEMENT (PHYSIOLOGY); PROTEIN TRANSPORT; RABBIT; SEMICONDUCTOR; STAINING; TIME;

ANIMALS; BIOTINYLATION; CALMODULIN; CELL SURVIVAL; CYTOPLASM; FLUORESCENT DYES; HELA CELLS; HUMANS; INTRACELLULAR SPACE; MOVEMENT; MYOSIN TYPE V; PROTEIN TRANSPORT; QUANTUM DOTS; RABBITS; SEMICONDUCTORS; STAINING AND LABELING; STREPTAVIDIN; TIME FACTORS;

EID: 68049143191     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.045     Document Type: Article

References (44)

1. Sellers, J. R., and C. Veigel. 2006. Walking with myosin V. Curr. Opin. Cell Biol. 18:68-73.
2. Walker, M. L., S. A. Burgess, J. R. Sellers, F. Wang, J. A. Hammer, et al. 2000. Two-headed binding of a processive myosin to f-actin. Nature. 405:804-807.
3. Burgess, S., M. Walker, F. Wang, J. R. Sellers, H. D. White, et al. 2002. The prepower stroke conformation of myosin V. J. Cell Biol. 159:983-991.
4. Coureux, P. D., A. L. Wells, J. Ménétrey, C. M. Yengo, C. A. Morris, et al. 2003. A structural state of the myosin V motor without bound nucleotide. Nature. 425:419-423.
5. Yildiz, A., J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldman, et al. 2003. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science. 300:2061-2065.
6. Veigel, C., S. Schmitz, F. Wang, and J. R. Sellers. 2005. Load-dependent kinetics of myosin-V can explain its high processivity. Nat. Cell Biol. 7:861-869.
7. Gebhardt, J. C., A. E. Clemen, J. Jaud, and M. Rief. 2006. Myosin-V is a mechanical ratchet. Proc. Natl. Acad. Sci. USA. 103:8680-8685.
8. Cappello, G., P. Pierobon, C. Symonds, L. Busoni, C. Gebhardt, et al. 2007. Myosin V stepping mechanism. Proc. Natl. Acad. Sci. USA. 104:15328-15333.
9. Rief, M., R. S. Rock, A. D. Mehta, M. S. Mooseker, R. E. Cheney, et al. 2000. Myosin-V stepping kinetics: a molecular model for processivity. Proc. Natl. Acad. Sci. USA. 97:9482.
10. Ali, M. Y., S. Uemura, K. Adachi, H. Itoh, K. Kinosita, et al. 2002. Myosin V is a left-handed spiral motor on the right-handed actin helix. Nat. Struct. Biol. 9:464-467.
11. Mehta, A. D., R. S. Rock, M. Rief, J. A. Spudich, M. S. Mooseker, et al. 1999. Myosin-V is a processive actin-based motor. Nature. 400:590-593.
12. Veigel, C., F. Wang, M. L. Bartoo, J. R. Sellers, and J. E. Molloy. 2002. The gated gait of the processive molecular motor myosin V. Nat. Cell Biol. 4:59-65.
13. Sakamoto, T., A. Yildez, P. R. Selvin, and J. R. Sellers. 2005. Step-size is determined by neck length in myosin V. Biochemistry. 44:16203-16210.
14. Clemen, A. E.-M., M. Vilfan, J. Jaud, J. Zhang, M. Barmann, et al. 2005. Force-dependent stepping kinetics of myosin-V. Biophys. J. 88:4402-4410.
15. Purcell, T. J., H. L. Sweeney, and J. A. Spudich. 2005. A force-dependent state controls the coordination of processive myosin V. Proc. Natl. Acad. Sci. USA. 102:13873-13878.
16. Uemura, S., H. Higuchi, A. O. Olivares, E. M. De La Cruz, and S. Ishiwata. 2004. Mechanochemical coupling of two substeps in a single myosin V motor. Nat. Struct. Mol. Biol. 11:877-883.
17. Moore, J. R., E. B. Krementsova, K. M. Trybus, and D. M. Warshaw. 2001. Myosin V exhibits a high duty cycle and large unitary displacement. J. Cell Biol. 155:625-635.
18. Warshaw, D. M., G. G. Kennedy, S. S. Work, E. B. Krementsova, S. Beck, et al. 2005. Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity. Biophys. J. 88:L30-L32.
19. Churchman, L. S., Z. Okten, R. S. Rock, J. F. Dawson, and J. A. Spudich. 2005. Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time. Proc. Natl. Acad. Sci. USA. 102:1419-1423.
20. Syed, S., G. E. Snyder, C. Franzini-Armstrong, P. R. Selvin, and Y. E. Goldman. 2006. Adaptability of myosin V studied by simultaneous detection of position and orientation. EMBO J. 25:1795-1803.
21. Rosenfeld, S. S., and H. L. Sweeney. 2004. A model of myosin V processivity. J. Biol. Chem. 279:40100-40111.
22. De La Cruz, E. M., A. L. Wells, S. S. Rosenfeld, E. M. Ostap, and H. L. Sweeney. 1999. The kinetic mechanism of myosin V. Proc. Natl. Acad. Sci. USA. 96:13726-13731.
23. De La Cruz, E. M., H. L. Sweeney, and E. M. Ostap. 2000. ADP inhibition of myosin V ATPase activity. Biophys. J. 79:1524-1529.
24. Schott, D. H., R. N. Collins, and A. Bretscher. 2002. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J. Cell Biol. 156:35-39.
25. Xie, X. S., J. Yu, and W. Y. Yang. 2006. Living cells as test tubes. Science. 312:228-230.
26. Kural, C., A. S. Serpinskaya, Y.-H. Chou, R. D. Goldman, V. I. Gelfand, et al. 2007. Tracking melanosomes inside a cell to study molecular motors and their interaction. Proc. Natl. Acad. Sci. USA. 104:5378-5382.
27. Levi, V., and E. Gratton. 2007. Exploring dynamics in living cells by tracking single particles. Cell Biochem. Biophys. 48:1-15.
28. Ross, J. L., H. Shuman, E. L. Holzbaur, and Y. E. Goldman. 2008. Kinesin and dynein-dynactin at intersecting microtubules: motor density affects dynein function. Biophys. J. 94:3115-3125.
29. Levi, V., V. I. Gelfand, A. S. Serpinskaya, and E. Gratton. 2006. Melanosomes transported by myosin-V in Xenopus melanophores perform slow 35-nm steps. Biophys. J. 90:L07-L09.
30. Courty, S., C. Luccardini, Y. Bellaiche, G. Cappello, and M. Dahan. 2006. Single quantum dot tracking of individual kinesins in live cells. Nano Lett. 6:1491-1495.
31. Dahan, M., S. Lévi, C. Luccardini, P. Rostaing, B. Riveau, et al. 2003. Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science. 302:442-445.
32. Nan, X., P. A. Sims, P. Chen, and X. S. Xie. 2005. Observation of individual microtubule motor steps in living cells with endocytosed quantum dots. J. Phys. Chem. B. 109:24220-24224.
33. Michalet, X., F. F. Pinaud, L. A. Bentolila, J. M. Tsay, S. Doose, et al. 2005. Quantum dots for live cells, in vivo imaging, and diagnostics. Science. 307:538-544.
34. Dunn, A. R., and J. A. Spudich. 2007. Dynamics of the unbound head during myosin V processive translocation. Nat. Struct. Mol. Biol. 14:246-248.
35. Gèrard, A., S. E. Polo, D. Roche, and G. Almouzni. 2006. Methods for studying chromatin assembly coupled to DNA repair. Methods Enzymol. 409:358-374.
36. Sweeney, H. L., S. S. Rosenfeld, F. Brown, L. Faust, J. Smith, et al. 1998. Kinetic tuning of myosin via a flexible loop adjacent to the nucleotide binding pocket. J. Biol. Chem. 273:6262-6270.
37. Okada, C. Y., and M. Rechsteiner. 1982. Introduction of macromolecules into cultured mammalian cells by osmotic lysis of pinocytic vesicles. Cell. 29:33-41.
38. Gelles, J., B. J. Schnapp, and M. P. Sheetz. 1988. Tracking kinesin-driven movements with nanometer-scale precision. Nature. 331:450-453.
39. Kerssemakers, J. W. J., E. L. Munteanu, L. Laan, T. L. Noetzel, M. E. Janson, et al. 2006. Assembly dynamics of microtubules at molecular resolution. Nature. 442:709-712.
40. Vale, R. D., and R. A. Milligan. 2000. The way things move: looking under the hood of molecular motor proteins. Science. 288:88-95.
41. Ali, M. Y., E. B. Krementsova, G. G. Kennedy, R. Mahaffy, T. D. Pollard, et al. 2007. Myosin Va maneuvers through actin intersections and diffuses along microtubules. Proc. Natl. Acad. Sci. USA. 104:4332-4336.
42. Luccardini, C., C. Tribet, F. Vial, V. Marchi-Artzner, and M. Dahan. 2006. Size, charge, and interactions with giant lipid vesicles of quantum dots coated with an amphiphilic macromolecule. Langmuir. 22:2304-2310.
43. Nan, X., P. A. Sims, and X. S. Xie. 2008. Organelle tracking in a living cell with microsecond time resolution and nanometer spatial precision. ChemPhysChem. 9:707-712.
44. Seitz, A., and T. Surrey. 2006. Processive movements of single kinesins on crowded microtubules visualized using quantum dots. EMBO J. 25:267-277.