Force generation by cellular motors

• Autorzy: Wanka F , Van Zoelen E.J.J.
• Języki publikacji: EN

Abstrakty

EN

Cell motility processes in non-muscle cells depend on the activity of motor proteins that bind to either microtubules or actin filaments. From presently available data it must be concluded that the driving force is generated by transient interaction of the respective motors with microtubules or actin filaments which then activates the binding and hydrolysis of ATP. This reaction results in an abrupt discharge of the motor molecule, the direction of which is determined by the spatial orientation of its binding to the helical and polar vehicle. The latter is thereby propelled in its length direction and simultaneously undergoes an axial rotation, while the expelled motor exerts an oppositely directed current in the surrounding fluid, comparable to jet propulsion. Force production, propulsion velocities and energy requirements known from in vitro studies comply with those derived from the theory. The theory opens new ways for the understanding of cellular activities such as particle transport, mitosis and morphodynamics.

Słowa kluczowe

EN

muscle contraction; plasma; non-muscle cell; actin filament; microtubule; chromosome segregation; kinesin; cell motility; myosin

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2003
• Tom: 08
• Numer: 4
• Opis fizyczny: p.1017-1033,fig.

Twórcy

autor

Wanka F

• University of Nijmegen, Toernooiveld 1, 6225 ED Nijmegen, The Netherlands

autor

Van Zoelen E.J.J.

Bibliografia

• 1. Huxley, H.E. The mechanism of muscular contraction. Science 164 (1969) 1356-1365.
• 2. Harada, Y., Sukurada, K., Aoki, T., Thomas, D.D. and Yanagida, T. Mechanochemical coupling in actomyosin energy transduction studies by in vitro movement assay. J. Mol. Biol. 216 (1990) 49-68.
• 3. Paschal, B.M., Shpetner, H.S. and Vallee, R.B. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dyneinlike properties. J. Cell Biol. 105 (1987) 1273-1282.
• 4. Paschal, B.M. and Vallee, R.B. Retrograde transport by microtubule-associated protein MAP 1C. Nature 330 (1987) 181-183.
• 5. Pollack, G.H. The cross-bridge theory. Physiol. Rev. 63 (1983) 1049-1113.
• 6. Kersey, Y., Hepler, P.H., Palewitz, B.A. and Wessels, N.K. Polarity of actin filaments in Characean algae. Proc. Natl. Acad. Sci. U.S.A. 73 (1976) 165-167.
• 7. Tanaka, E.M. and Kirschner, M.W. Microtubule behaviour in the growth cones of living neurons during axon elongation. J. Cell Biol. 115 (1991) 345-363.
• 8. Vale, R.D., Reese, T.S. and Sheetz, P.M. Identification of a novel forcegenerating protein, kinesin, involved in microtubule based motility. Cell 42 (1985) 39-50.
• 9. Kron, S.J. and Spudich, J.A. Fluorescent actin filaments move on myosin fixed to a glass surface. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 6272-6276.
• 10. Toyoshima, Y.Y., Kron, S.J., Mcnally, E.M., Niebling, K.R.N., Toyoshima, C. and Spudich, J.A. Myosin subfragment-1 is sufficient to move actin filaments in vitro. Nature 328 (1987) 536-539.
• 11. Yang, J.T., Laymon, R.A. and Goldstein. L.S.B. A three-domain structure of kinesin heavy chain, revealed by DNA sequence and microtubule binding analysis. Cell 56 (1989) 879-889.
• 12. Kuznetsov, S.A., Vaisberg, E.A., Shanina, N.A., Magretova, N.N., Chernak, V.Y. and Gelfand, V.I. The quaternary structure of bovine kinesin. EMBO-J. 7 (1988) 353-356.
• 13. Kuznetsov, S.A., Vaisberg, E.A., Rothwell, S.W., Murphy, D.B. and Gelfand, V.I. Isolation of a 45-kDa fragment from kinesin heavy chain with enhanced ATPase and microtubule binding activities. J. Biol. Chem. 264 (1989) 589-595.
• 14. Rayment, I., Holden, H.M., Whittaker, M., Yohn, C.B., Lorenz, M., Holmes, K.C. and Milligan, A.R. Structure of the atin-myosin complex and its implications for muscle contraction, Science 261 (1993) 58-65.
• 15. Rayment, I., Rypniewski, W.R., Schmidt-Bläse, K., Smith, R., Tomchik, D.R., Benning, M.M., Winkelmann, D.A., Wesenberg, G. and Holden, H.M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261 (1993) 50-58.
• 16. Kull, F.J., Sablin, E.P., Lace, R., Fletterich, R.J. and Vale R.D. Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 380 (1996) 550-555.
• 17. Conzelman, K.A. and Mooseker, M.S. The 110-kD protein-calmodulin complex of the intestinal microvillus is an activated MgATPase. J. Cell Biol. 105 (1987) 13-324.
• 18. Song, Y. -H. and Mandelkow, E. Recombinant kinesin motor domain binds to β-tubulin and decorates microtubules with a B surface lattice. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 1671-1675.
• 19. Huxley, H.E. Electron microscope studies of the structure of natural and synthetic protein filaments from striated muscle. J. Mol. Biol. 7 (1963) 281-308.
• 20. Porter, M.E., Scholey, J.M., Stemple, D.L., Vigers, G.P.A., Vale, R.D. Sheetz, M.P. and Mcintosh, J.R. Characterization of the microtubule movement produced by sea urchin egg kinesin. J. Biol. Chem. 262 (1987) 2794-2802.
• 21. Clarke, M. and Spudich, J.A. Biochemical and structural studies of actomyosin-like proteins from amoebae of Dictyostelium discoideum. J. Mol. Biol. 86 (1974) 209-222.
• 22. Kuznetsov, S.A. and Gelfand, V.I. Bovine brain kinesin is a microtubule-activated ATPase. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 8530-8534.
• 23. Pfister, K.K., Wagner, M.C., Bloom, G.S. and Brady, S.T. Modification of the microtubule-binding and ATPase activities of kinesin by N-ethylmaleimide [NEM] suggests a role for sulfhydryls in fast axonal transport. Biochemistry 28 (1989) 9006-9012.
• 24. Cross, R.A., Cross, K.K. and Sobiszek, A. ATP-linked monomer-polymer equilibrium of smooth muscle myosin: the free folded monomer trap ADP- Pi. EMBO-J. 5 (1986) 2637-2641.
• 25. Hackney, D.D. Kinesin ATPase: rate-limiting ADP release. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 6314-6318.
• 26. Gilbert, S.P. and Johnson, K.A. Pre-steady-state kinetics of the microtubule- kinesin ATPase. Biochemistry 33 (1994) 1951-1960.
• 27. Lockhart, A. and Cross, A.R. Origins of reversed directionality in the ncd molecular motor. EMBO-J. 13 (1994) 751-757.
• 28. Gibbons, I.R., Cosson, M.P., Evans, J.A., Gibbons, B.H., Houk, B., Martinson, K.M., Sale, W.S. and Tang, W.-J.Y. Potent inhibition of dynein adenosinetriphosphatase and motility of cilia and sperm flagella by vanadate Proc. Natl. Acad. Sci. U.S.A. 75 (1978) 2220-2224.
• 29. Beckerle, M. and Porter K.R. Analysis of the role of microtubules and actin in erythrophore intracellular motility. J. Cell Biol. 96 (1983) 354-362.
• 30. Fisher, A.J., Smith, C.A., Thoden, J., Smith, R., Sutoh, K., Holden, H.M. and Rayment, J. Structural studies of myosin: nucleotide complexes: a revised model for the molecular basis of muscle contraction. Biophys. J. 68 (1995) 19S-28S.
• 31. Fisher, A.J., Smith, C.A., Thoden, J.B., Smith, R., Sutoh, K., Holden, H.M. and Rayment, I. X-ray structures of myosin motor domain of Dictyostelium discoideum complexed with MgADP∙BeFx and MgADP∙ A1F4. Biochemistry 34 (1995) 8960-8972.
• 32. Crevel, I.M., Lockhart, A. and Cross, R.A. Weak and strong states of kinesin and ncd. J. Mol. Biol. 257 (1996) 66-76.
• 33. Omoto, C.K. and Johnson, K.A. Activation of the dynein adenosinetriphosphatase by microtubules. Biochemistry 25 (1986) 419-427.
• 34. Shimizu, T., Marchese-Ragona, S.P. and Johnson, K.A. Activation of dynein adenine triphosphatase by cross-linking to microtubules. Biochemistry 28 (1989) 7016-7021.
• 35. Shimizu, T., Toyoshima, Y., Edamatsu, M. and Vale, R.D. Comparison of the motile and enzymatic properties of two microtubule minus-end-directed motors, ncd and cytoplasmic dynein. Biochemistry 43 (1995) 1575-1582.
• 36. Sablin, E.P., Kull, F.J., Cooke, R., Vale, R.D. and Fletterich, R.J. Crystal structure of the motor domain of the kinesin-related motor ncd. Nature 380 (1996) 555-559.
• 37. Kull. F.J. and Endow, S.A. Kinesin: swich I & II and the motor mechanism. J. Cell Sci. 115 (2002) 15-23.
• 38. Hackney, D.D. Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 6865-6869.
• 39. Offer, G. Skip residues correlate with bends in the myosin tail. J. Mol. Biol. 216 (1990) 213-218.
• 40. Burke, M. and Reisler, E. Effect of nucleotide binding on the proximity of the essential sulfhydryl groups of myosin. Chemical probing of movement of residues during conformational transitions. Biochemistry 16 (1977) 5559-5563.
• 41. Huston, E.E., Grammer, J.C. and Yount, R.G. Flexibility of the myosin heavy chain: direct evidence that the region containing SH1 and SH2 can move 10Å under the influence of nucleotide binding. Biochemistry 72 (1988) 8945-8952.
• 42. Onishi, H., Maita, T., Matsuka, G. and Fujiwara, K. Lys-65 and Glu-168 are the residues for carbodiimide-catalysed cross-linking between the two heads of rigor smooth muscle heavy meromyosin. J. Biol. Chem. 265 (1990) 19362-19368.
• 43. Olney, J.J., Sellers, J.R. and Cremo, C.R. Structure and function of the 10S conformation of smooth muscle myosin. J. Biol. Chem. 217 (1996) 20375-20384.
• 44. Rosenfeld, S.S., Xing, J., Rener, B., Lebowitz, J., Karr, S. and Cheung, H.C. Structural and kinetic studies of the 10S↔6S transition in smooth muscle myosin. J. Biol. Chem. 269 (1994) 30187-30194.
• 45. Mendelson, R. and Morris, E.P. The structure of the acto-myosin subfragment 1 complex: Results of searches using data from electron microscopy and X-ray crystallography. Proc. Natl. Acad. Sci. 94 (1997) 8533-8538.
• 46. Reedy, M.K., Lucaveche, C., Naber, N. and Cooke, R. Insect cross-bridges, relaxed by spin-labeled nucleotide, show well-ordered 90° state by X-Ray diffraction and electron microscopy but spectra of electron paramagnetic resonance probes report disorder. J. Mol. Biol. 227 (1992) 678-697.
• 47. Zhao, L., Naber, N. and Cooke, R. Muscle cross-bridges bound to actin are disordered in the presence of 2,3-butanedione monoxime. Biochem. J. 68 (1995) 1980-1990.
• 48. Nishizaka, T., Yagi, T., Tanaka, Y. and Ishiwata, S. Right handed rotation of an actin filament in an in vitro motile system. Nature 361 (1993) 269-271.
• 49. Sase, I., Miyata, H., Ishiwata, S. and Kinosita, K. jr. Axial rotation of sliding actin filaments revealed by single-fluorophore imaging. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 5646-5650.
• 50. Ray, S., Meyhover, E., Milligan, R.A. and Howard, J. Kinesin follows the microtubule’s protofilament axes. J. Cell Biol. 121 (1993) 1083-1093.
• 51. Henningsen, U. and Schliwa, M. Reversion in the direction of movement of a molecular motor. Nature 389 (1997) 93-96.
• 52. Harada, Y., Noguchi, A., Kishino, A. and Yanagida, T. Sliding movement of single actin filaments on one-headed myosin filaments. Nature 326 (1987) 805-808.
• 53. Waller, G.S., Ouyang, G., Swafford, J., Vibert, P. and Lowey, S. A minimal motor domain from chicken skeletal muscle myosin. J. Biol. Chem. 270 (1995) 15348-15352.
• 54. Stewart, R.J., Thaler, J.P. and Goldstein, L.S.B. Direction of microtubule movement is an itrinsic property of the motor domains of kinesin heavy chain and Drosophila ncd protein. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 5209-5213.
• 55. Ansow, M. Geeves, M.A. Kurozava, S.E. and Manstein, D.J. Myosin motors with artificial lever arms. EMBO-J. 15 (1996) 6069-6074.
• 56. Wolenski, J.S., Hayden, M.S., Forscher, P. and Mooseker, M.S. Calcium- calmodulin and regulation of brush border myosin-I MgATPase and mechanochemistry. J. Cell Biol. 122 (1993) 613-621.
• 57. Cheney, R.E., O’Shea, M., Heuser J.E., Coelho, M.V., Wolenski, J.S. Espreatico, E.M. Forscher, F., Larson, R.E. and Mooseker, M.S. Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell 75 (1993) 13-23.
• 58. Lowey, S., Waller, G.S. and Trybus, K.M. Skeletal muscle myosin light chains are essential for physiological speeds of shortening. Nature 365 (1993) 454-456.
• 59. Van Buren, P., Waller, G.S., Harris, D.E., Trybus, K.M., Warshaw, D.M. and Lowey, S. The essential light chain is required for full force production by skeletal muscle myosin. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 12403- 12407.
• 60. Xie, X., Harrison, D.H., Schlichting, I., Sweet, R.-M., Kalabokis, V.N., Szent-Györgyi, A.G. and Cohen, C. Structure and regulatory domain of scallop myosin at 28Å resolution. Nature 368 (1994) 306-312.
• 61. Ishijima, A., Doi, T., Sakurada, K. and Yanagida, T. Sub-piconewton force fluctuations of actomyosin in vitro. Nature 352 (1991) 301-306.
• 62. Visscher, K., Schnitzer, M.J. and Black, S.-M. Single kinesin molecules studied with a molecular force clamp. Nature 400 (1999) 184-189.
• 63. Bajer, A. and Molé-Bajer, J. Spindle dynamics and chromosome movement. Int. Rev. Cytol. 3 (1972) Supl. 3, 1-217.
• 64. Williamson, R.E. Cytoplasmic streaming in Chara: A cell model activated by ATP and inhibited by cytochalasin. J. Cell Sci. 17 (1975) 655-668.