Switch between Large Hand-Over-Hand and Small Inchworm-like Steps in Myosin VI

Cell

Volumn 142, Issue 6, 2010, Pages 879-888

  Nishikawa, So ^a   Arimoto, Ikuo ^a   Ikezaki, Keigo ^a   Sugawa, Mitsuhiro ^a   Ueno, Hiroshi ^a   Komori, Tomotaka ^a   Iwane, Atsuko H ^a   Yanagida, Toshio ^a,b,c  

^a OSAKA UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

Author keywords

Proteins

Indexed keywords

ADENOSINE DIPHOSPHATE; GOLD NANOPARTICLE; MYOSIN VI; QUANTUM DOT; ACTIN; GOLD; METAL NANOPARTICLE; MYOSIN HEAVY CHAIN;

ARTICLE; CELL VACUOLE; MEMBRANE; NANOIMAGING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; TASK PERFORMANCE; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; DIMERIZATION; FLUORESCENCE MICROSCOPY; HUMAN; METABOLISM; MICROSCOPY; PROTEIN TERTIARY STRUCTURE;

ACTINS; ANIMALS; CHICKENS; DIMERIZATION; GOLD; HUMANS; METAL NANOPARTICLES; MICROSCOPY; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MYOSIN HEAVY CHAINS; PROTEIN STRUCTURE, TERTIARY; QUANTUM DOTS;

EID: 77956634165     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.08.033     Document Type: Article

References (42)

1. Ali M.Y., Homma K., Iwane A.H., Adachi K., Itoh H., Kinosita K., Yanagida T., Ikebe M. Unconstrained steps of myosin VI appear longest among known molecular motors. Biophys. J. 2004, 86:3804-3810.
2. Altman D., Goswami D., Hasson T., Spudich J.A., Mayor S. Precise positioning of myosin VI on endocytic vesicles in vivo. PLoS Biol. 2007, 5:e210.
3. Altman D., Sweeney H.L., Spudich J.A. The mechanism of myosin VI translocation and its load-induced anchoring. Cell 2004, 116:737-749.
4. Bahloul A., Chevreux G., Wells A.L., Martin D., Nolt J., Yang Z., Chen L.Q., Potier N., Van Dorsselaer A., Rosenfeld S., et al. The unique insert in myosin VI is a structural calcium-calmodulin binding site. Proc. Natl. Acad. Sci. USA 2004, 101:4787-4792.
5. Balci H., Ha T., Sweeney H.L., Selvin P.R. Interhead distance measurements in myosin VI via SHRImP support a simplified hand-over-hand model. Biophys. J. 2005, 89:413-417.
6. Bryant Z., Altman D., Spudich J.A. The power stroke of myosin VI and the basis of reverse directionality. Proc. Natl. Acad. Sci. USA 2007, 104:772-777.
7. Churchman L.S., Okten Z., Rock R.S., Dawson J.F., Spudich J.A. Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time. Proc. Natl. Acad. Sci. USA 2005, 102:1419-1423.
8. Churchman L.S., Spudich J.A. Colocalization of Fluorescent Probes: Accurate and Precise Registration with Nanometer Resolution. Single-molecule techniques: a Laboratory Manual 2007, 73-84. P.R. Selvin, T.J. Ha (Eds.).
9. De La Cruz E.M., Ostap E.M., Sweeney H.L. Kinetic mechanism and regulation of myosin VI. J. Biol. Chem. 2001, 276:32373-32381.
10. Dunn A.R., Spudich J.A. Dynamics of the unbound head during myosin V processive translocation. Nat. Struct. Mol. Biol. 2007, 14:246-248.
11. Funatsu T., Harada Y., Tokunaga M., Saito K., Yanagida T. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature 1995, 374:555-559.
12. Goldman Y.E. Kinetics of the Actomyosin ATPase in Muscle Fibers. A Rev Physiol. 1987, 49:637-654.
13. Harada Y., Sakurada K., Aoki T., Thomas D.D., Yanagida T. Mechanochemical coupling in actomyosin energy transduction studied by in vitro movement assay. J. Mol. Biol. 1990, 216:49-68.
14. Iwaki M., Iwane A.H., Shimokawa T., Cooke R., Yanagida T. Brownian search-and-catch mechanism for myosin-VI steps. Nat. Chem. Biol. 2009, 5:403-405.
15. Kinosita K., Itoh H., Ishiwata S., Hirano K., Nishizaka T., Hayakawa T. Dual-view microscopy with a single camera: real-time imaging of molecular orientations and calcium. J. Cell Biol. 1991, 115:67-73.
16. Lan G., Sun S.X. Flexible light-chain and helical structure of F-actin explain the movement and step size of myosin-VI. Biophys. J. 2006, 91:4002-4013.
17. Menetrey J., Bahloul A., Wells A.L., Yengo C.M., Morris C.A., Sweeney H.L., Houdusse A. The structure of the myosin VI motor reveals the mechanism of directionality reversal. Nature 2005, 435:779-785.
18. Menetrey J., Llinas P., Cicolari J., Squires G., Liu X., Li A., Sweeney H.L., Houdusse A. The post-rigor structure of myosin VI and implications for the recovery stroke. EMBO J. 2008, 27:244-252.
19. Mukherjea M., Llinas P., Kim H., Travaglia M., Safer D., Menetrey J., Franzini-Armstrong C., Selvin P.R., Houdusse A., Sweeney H.L. Myosin VI dimerization triggers an unfolding of a three-helix bundle in order to extend its reach. Mol. Cell 2009, 35:305-315.
20. Nishikawa S., Homma K., Komori Y., Iwaki M., Wazawa T., Hikikoshi Iwane A., Saito J., Ikebe R., Katayama E., Yanagida T., et al. Class VI myosin moves processively along actin filaments backward with large steps. Biochem. Biophys. Res. Commun. 2002, 290:311-317.
21. Okten Z., Churchman L.S., Rock R.S., Spudich J.A. Myosin VI walks hand-over-hand along actin. Nat. Struct. Mol. Biol. 2004, 11:884-887.
22. Park H., Li A., Chen L.Q., Houdusse A., Selvin P.R., Sweeney H.L. The unique insert at the end of the myosin VI motor is the sole determinant of directionality. Proc. Natl. Acad. Sci. USA 2007, 104:778-783.
23. Park H., Ramamurthy B., Travaglia M., Safer D., Chen L.Q., Franzini-Armstrong C., Selvin P.R., Sweeney H.L. Full-length myosin VI dimerizes and moves processively along actin filaments upon monomer clustering. Mol. Cell 2006, 21:331-336.
24. Phichith D., Travaglia M., Yang Z., Liu X., Zong A.B., Safer D., Sweeney H.L. Cargo binding induces dimerization of myosin VI. Proc. Natl. Acad. Sci. USA 2009, 106:17320-17324.
25. Reifenberger J.G., Toprak E., Kim H., Safer D., Sweeney H.L., Selvin P.R. Myosin VI undergoes a 180 degrees power stroke implying an uncoupling of the front lever arm. Proc. Natl. Acad. Sci. USA 2009, 106:18255-18260.
26. Rock R.S., Ramamurthy B., Dunn A.R., Beccafico S., Rami B.R., Morris C., Spink B.J., Franzini-Armstrong C., Spudich J.A., Sweeney H.L. A flexible domain is essential for the large step size and processivity of myosin VI. Mol. Cell 2005, 17:603-609.
27. Rock R.S., Rice S.E., Wells A.L., Purcell T.J., Spudich J.A., Sweeney H.L. Myosin VI is a processive motor with a large step size. Proc. Natl. Acad. Sci. USA 2001, 98:13655-13659.
28. Shiroguchi K., Kinosita K. Myosin V walks by lever action and Brownian motion. Science 2007, 316:1208-1212.
29. Sivaramakrishnan S., Spudich J.A. Coupled myosin VI motors facilitate unidirectional movement on an F-actin network. J. Cell Biol. 2009, 187:53-60.
30. Spink B.J., Sivaramakrishnan S., Lipfert J., Doniach S., Spudich J.A. Long single α-helical tail domains bridge the gap between structure and function of myosin VI. Nat. Struct. Mol. Biol. 2008, 15:591-597.
31. Spudich J.A., Sivaramakrishnan S. Myosin VI: an innovative motor that challenged the swinging lever arm hypothesis. Nat. Rev. Mol. Cell Biol. 2010, 11:128-137.
32. Sun Y., Schroeder H.W., Beausang J.F., Homma K., Ikebe M., Goldman Y.E. Myosin VI walks " wiggly" on actin with large and variable tilting. Mol. Cell 2007, 28:954-964.
33. Sweeney H.L., Houdusse A. What can myosin VI do in cells?. Curr. Opin. Cell Biol. 2007, 19:57-66.
34. Taniguchi Y., Nishiyama M., Ishii Y., Yanagida T. Entropy rectifies the Brownian steps of kinesin. Nat. Chem. Biol. 2005, 1:342-347.
35. Thompson R.E., Larson D.R., Webb W.W. Precise nanometer localization analysis for individual fluorescent probes. Biophys. J. 2002, 82:2775-2783.
36. Tokunaga M., Kitamura K., Saito K., Iwane A.H., Yanagida T. Single molecule imaging of fluorophores and enzymatic reactions achieved by objective-type total internal reflection fluorescence microscopy. Biochem. Biophys. Res. Commun. 1997, 235:47-53.
37. Ueno H., Nishikawa S., Iino R., Tabata K.V., Sakakibara S., Yanagida T., Noji H. Simple Dark-Field Microscopy with Nanometer Spatial Precision and Microsecond Temporal Resolution. Biophys. J. 2010, 98:2014-2023.
38. Vale R.D., Funatsu T., Pierce D.W., Romberg L., Harada Y., Yanagida T. Direct observation of single kinesin molecules moving along microtubules. Nature 1996, 380:451-453.
39. Warshaw D.M., Kennedy G.G., Work S.S., Krementsova E.B., Beck S., Trybus K.M. Differential Labeling of Myosin V Heads with Quantum Dots Allows Direct Visualization of Hand-Over-Hand Processivity. Biophys. J. 2005, 88:L30-L32.
40. Wells A.L., Lin A.W., Chen L.Q., Safer D., Cain S.M., Hasson T., Carragher B.O., Milligan R.A., Sweeney H.L. Myosin VI is an actin-based motor that moves backwards. Nature 1999, 401:505-508.
41. Yildiz A., Forkey J.N., McKinney S.A., Ha T., Goldman Y.E., Selvin P.R. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 2003, 300:2061-2065.
42. Yildiz A., Park H., Safer D., Yang Z., Chen L.Q., Selvin P.R., Sweeney H.L. Myosin VI steps via a hand-over-hand mechanism with its lever arm undergoing fluctuations when attached to actin. J. Biol. Chem. 2004, 279:37223-37226.