Higher plant myosin XI moves processively on actin with 35 nm steps at high velocity

EMBO Journal

Volumn 22, Issue 6, 2003, Pages 1263-1272

  Tominaga, Motoki ^a   Kojima, Hiroaki ^a   Yokota, Etsuo ^b   Orii, Hidefumi ^b   Nakamori, Rinna ^a   Katayama, Eisaku ^c,d   Anson, Michael ^e   Shimmen, Teruo ^b   Oiwa, Kazuhiro ^a  

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

^b UNIVERSITY OF HYOGO   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

In vitro motility; Myosin XI; Optical trap; Processivity; Single molecule

Indexed keywords

MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE;

ACTIN FILAMENT; ANGIOSPERM; ARTICLE; ENZYME KINETICS; ENZYME PURIFICATION; MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; SEQUENCE ANALYSIS; VELOCITY;

ACTINS; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; CALMODULIN-BINDING PROTEINS; CYTOPLASMIC STREAMING; DIMERIZATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; MYOSIN HEAVY CHAINS; MYOSIN LIGHT CHAINS; MYOSINS; NANOTECHNOLOGY; TOBACCO;

ALGAE; EMBRYOPHYTA; MAGNOLIOPHYTA; NICOTIANA TABACUM;

EID: 0037451289     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg130     Document Type: Article

References (47)

1. Ali, M.Y., Uemura, S., Adachi, K., Itoh, H., Kinosita, K., Jr and Ishiwata, S. (2002) Myosin V is a left-handed spiral motor on the right-handed actin helix. Nature Struct. Biol., 9, 464-467.
2. Anson, M. (1992) Temperature dependence and Arrhenius activation energy of F-actin velocity generated in vitro by skeletal myosin. J. Mol. Biol., 224, 1029-1038.
3. Block, S.M., Goldstein, L.S. and Schnapp, B.J. (1990) Bead movement by single kinesin molecules studied with optical tweezers. Nature, 348, 348-352.
4. De La Cruz, E.M., Wells, A.L., Rosenfeld, S.S., Ostap, E.M. and Sweeney, H.L. (1999) The kinetic mechanism of myosin V. Proc. Natl Acad. Sci. USA, 96, 13726-13731.
5. Espreafico, E.M., Cheney, R.E., Matteoli, M., Nascimento, A.A., De Camilli, P.V., Larson, R.E. and Mooseker, M.S. (1992) Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains. J. Cell Biol., 119, 1541-1557.
6. Finer, J.T., Simmons, R.M. and Spudich, J.A. (1994) Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature, 368, 113-119.
7. Guilford, W.H., Dupuis, D.E., Kennedy, G., Wu, J., Patlak, J.B. and Warshaw, D.M. (1997) Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap. Biophys. J., 72, 1006-1021.
8. Hackney, D.D. (1995) Highly processive microtubule-stimulated ATP hydrolysis by dimeric kinesin head domains. Nature, 377, 448-450.
9. Hancock, W.O. and Howard, J. (1998) Processivity of the motor protein kinesin requires two heads. J. Cell Biol., 140, 1395-1405.
10. Higashi-Fujime, S. and Sumiyoshi, H. (2001) Molecular sliding mechanism of the fastest Chara myosin from green algae. Curr. Top. Biochem. Res., 4, 61-70.
11. Higashi-Fujime, S., Ishikawa, R., Iwasawa, H., Kagami, O., Kurimoto, E., Kohama, K. and Hozumi, T. (1995) The fastest actin-based motor protein from the green algae, Chara and its distinct mode of interaction with actin. FEBS Lett., 375, 151-154.
12. Homsher, E., Wang, F. and Sellers, J.R. (1992) Factors affecting movement of F-actin filaments propelled by skeletal muscle heavy meromyosin. Am. J. Physiol., 262, C714-C723.
13. Kamiya, N. (1981) Physical and chemical basis of cytoplasmic streaming. Annu. Rev. Plant Physiol., 32, 205-236.
14. Kashiyama, T., Kimura, N., Mimura, T. and Yamamoto, K. (2000) Cloning and characterization of a myosin from characean alga, the fastest motor protein in the world. J. Biochem., 127, 1065-1070.
15. Katayama, E. and Ikebe, M. (1995) Mode of caldesmon binding to smooth muscle thin filament: possible projection of the amino-terminal of caldesmon from native thin filament. Biophys. J., 68, 2419-2428.
16. Kimura, Y., Toyoshima, N., Hirakawa, N., Okamoto, K., Ishijima, A. and Higashi-Fujime, S. (2002) Mechanical properties of Chara myosin. Biophys. J., 82, 411a.
17. Kinkema, M. and Schiefelbein, J. (1994) A myosin from a higher plant has structural similarities to class V myosins. J. Mol. Biol., 239, 591-597.
18. Kinkema, M., Wang, H. and Schiefelbein, J. (1994) Molecular analysis of the myosin gene family in Arabidopsis thaliana. Plant Mol. Biol. 26, 1139-1153.
19. Kojima, H., Muto, E., Higuchi, H. and Yanagida, T. (1997) Mechanics of single kinesin molecules measured by optical trapping nanometry. Biophys. J., 73, 2012-2022.
20. Kron, S.J., Toyoshima, Y.Y., Uyeda, T.Q.P. and Spudich, J.A. (1991) Assays for actin sliding movement over myosin-coated surfaces. Methods Enzymol., 196, 399-416.
21. Leibler, S. and Huse, D.A. (1993) Porters versus rowers: a unified stochastic model of motor proteins. J. Cell Biol., 121, 1357-1368.
22. Lupas, A. (1996) Prediction and analysis of coiled-coil structures. Methods Enzymol., 266, 513-525.
23. Mabuchi, K. (1991) Heavy-meromyosin-decorated actin filaments: a simple method to preserve actin filaments for rotary shadowing. J. Struct. Biol., 107, 22-28.
24. Mehta, A. (2001) Myosin learns to walk. J. Cell Sci., 114, 1981-1998.
25. Morimatsu, M., Nakamura, A., Sumiyoshi, H., Sakaba, N., Taniguchi, H., Kohama, K. and Higashi-Fujime, S. (2000) The molecular structure of the fastest myosin from green algae, Chara. Biochem. Biophys. Res. Commun., 270, 147-152.
26. Nishikawa, S. et al. (2002) Class VI myosin moves processively along actin filaments backward with large steps. Biochem. Biophys. Res. Commun., 290, 311-317.
27. Oiwa, K. et al. (2000) Comparative single-molecule and ensemble myosin enzymology: sulfoindocyanine ATP and ADP derivatives. Biophys. J., 78, 3048-3071.
28. Reddy, A.S. (2001) Molecular motors and their functions in plants. Int. Rev. Cytol., 204, 97-178.
29. Rief, M., Rock, R.S., Mehta, A.D., Mooseker, M.S., Cheney, R.E. and Spudich, J.A. (2000) Myosin-V stepping kinetics: a molecular model for processivity. Proc. Natl Acad. Sci. USA, 97, 9482-9486.
30. Rock, R.S., Rice, S.E., Wells, A.L., Purcell, T.J., Spudich, J.A and Sweeney, H.L. (2001) Myosin VI is a processive motor with a large step size. Proc. Natl Acad. Sci. USA, 98, 13655-13659.
31. Sakakibara, H., Kojima, H., Sakai, Y., Katayama, E. and Oiwa, K. (1999) Inner-arm dynein c of Chlamydomonas flagella is a single-headed processive motor. Nature, 400, 586-590.
32. Sakamoto, T., Amitani, I., Yokota, E. and Ando, T. (2000) Direct observation of processive movement by individual myosin V molecules. Biochem. Biophys. Res. Commun., 272, 586-590.
33. Shimmen, T. and Yokota, E. (1994) Physiological and biochemical aspects of cytoplasmic streaming. Int. Rev. Cytol., 155, 97-139.
34. Svoboda, K., Schmidt, C.F., Schnapp, B.J. and Block, S.M. (1993) Direct observation of kinesin stepping by optical trapping interferometry. Nature, 365, 721-727.
35. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.
36. Toyoshima, Y.Y., Kron, S.J. and Spudich, J.A. (1990) The myosin step size: measurement of the unit displacement per ATP hydrolyzed in an in vitro assay. Proc. Natl Acad. Sci. USA, 87, 7130-7134.
37. Trybus, K.M., Krementsova, E. and Freyzon, Y. (1999) Kinetic characterization of a monomeric unconventional myosin V construct. J. Biol. Chem., 274, 27448-27456.
38. Veigel, C., Wang, F. Bartoo, M.L., Sellers, J.R. and Molloy, J.E. (2002) The gated gait of the processive molecular motor, myosin V. Nature Cell Biol., 4, 59-65.
39. Walker, M.L., Burgess, S.A., Sellers, J.R., Wang, F., Hammer, J.A., III, Trinick, J. and Knight, P.J. (2000) Two-headed binding of a processive myosin to F-actin. Nature, 405, 804-807.
40. Warshaw, D.M., Desrosiers, J.M., Work, S.S. and Trybus, K.M. (1991) Effects of MgATP, MgADP, and Pi on actin movement by smooth muscle myosin. J. Biol. Chem., 266, 24339-24343.
41. Wells, A.L., Lin, A.W., Chen, L.Q., Safer, D., Cain, S.M., Hasson, T., Carragher, B.O., Milligan, R.A. and Sweeney, H.L. (1999) Myosin VI is an actin-based motor that moves backwards. Nature, 401, 505-508.
42. Yamamoto, K., Kikuyama, M., Sutoh-Yamamoto, N. and Kamitsubo, E. (1994) Purification of actin-based motor protein from Chara corallina. Proc. Jap. Acad., 70, 175-180.
43. Yamamoto, K., Kikuyama, M., Sutoh-Yamamoto, N., Kamitsubo, E. and Katayama, E. (1995) Myosin from alga Chara: unique structure revealed by electron microscopy. J. Mol. Biol., 254, 109-112.
44. Yokota,E. and Shimmen, T. (1994) Isolation and characterization of plant myosin from pollen tubes of lily. Protoplasma, 177, 153-162.
45. Yokota, E., Yukawa, C., Muto, S., Sonobe, S. and Shimmen, T. (1999) Biochemical and immunocytochemical characterization of two types of myosins in cultured tobacco bright yellow-2 cells. Plant Physiol., 121, 525-534.
46. Yokota, E., Sonobe, S., Orii, H., Yuasa, T., Inada, S. and Shimmen, T. (2001) The type and the localization of 175-kDa myosin in tobacco cultured cells BY-2. J. Plant Res., 114, 115-116.
47. Yoneda, M. and Nagai, R. (1988) Structural basis of cytoplasmic streaming in Characean internodal cells. A hydrodynamic analysis. Protoplasma, 147, 64-76.