Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1995 Apr;68(4 Suppl):245S–255S.

The mechanics of force generation by kinesin.

J Howard 1
PMCID: PMC1281936  PMID: 7787085

Abstract

Several laboratories have developed highly sensitive mechanical techniques for studying the movement of purified motor proteins along their associated filaments. The aim of these experiments is to test models for force generation, such as the powerstroke model and "ratchet" or diffusional models, by 1) directly visualizing the path on the filament along which the motor moves, 2) measuring the force exerted by the motor against the filament, and 3) characterizing the passive mechanical properties (elasticity) of the motor. This paper focuses on recently published work on the microtubule-based motor kinesin taking this mechanical approach. Related work on myosin is mentioned for comparison.

Full text

PDF
245s

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Amos L., Klug A. Arrangement of subunits in flagellar microtubules. J Cell Sci. 1974 May;14(3):523–549. doi: 10.1242/jcs.14.3.523. [DOI] [PubMed] [Google Scholar]
  2. Block S. M., Goldstein L. S., Schnapp B. J. Bead movement by single kinesin molecules studied with optical tweezers. Nature. 1990 Nov 22;348(6299):348–352. doi: 10.1038/348348a0. [DOI] [PubMed] [Google Scholar]
  3. Craig R., Szent-Györgyi A. G., Beese L., Flicker P., Vibert P., Cohen C. Electron microscopy of thin filaments decorated with a Ca2+-regulated myosin. J Mol Biol. 1980 Jun 15;140(1):35–55. doi: 10.1016/0022-2836(80)90355-1. [DOI] [PubMed] [Google Scholar]
  4. Eisenberg E., Hill T. L. A cross-bridge model of muscle contraction. Prog Biophys Mol Biol. 1978;33(1):55–82. doi: 10.1016/0079-6107(79)90025-7. [DOI] [PubMed] [Google Scholar]
  5. Finer J. T., Simmons R. M., Spudich J. A. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature. 1994 Mar 10;368(6467):113–119. doi: 10.1038/368113a0. [DOI] [PubMed] [Google Scholar]
  6. Gelles J., Schnapp B. J., Sheetz M. P. Tracking kinesin-driven movements with nanometre-scale precision. Nature. 1988 Feb 4;331(6155):450–453. doi: 10.1038/331450a0. [DOI] [PubMed] [Google Scholar]
  7. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  8. Hackney D. D. Kinesin ATPase: rate-limiting ADP release. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6314–6318. doi: 10.1073/pnas.85.17.6314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hackney D. D., Levitt J. D., Suhan J. Kinesin undergoes a 9 S to 6 S conformational transition. J Biol Chem. 1992 Apr 25;267(12):8696–8701. [PubMed] [Google Scholar]
  10. Hall K., Cole D. G., Yeh Y., Scholey J. M., Baskin R. J. Force-velocity relationships in kinesin-driven motility. Nature. 1993 Jul 29;364(6436):457–459. doi: 10.1038/364457a0. [DOI] [PubMed] [Google Scholar]
  11. Harrison B. C., Marchese-Ragona S. P., Gilbert S. P., Cheng N., Steven A. C., Johnson K. A. Decoration of the microtubule surface by one kinesin head per tubulin heterodimer. Nature. 1993 Mar 4;362(6415):73–75. doi: 10.1038/362073a0. [DOI] [PubMed] [Google Scholar]
  12. Higuchi H., Goldman Y. E. Sliding distance between actin and myosin filaments per ATP molecule hydrolysed in skinned muscle fibres. Nature. 1991 Jul 25;352(6333):352–354. doi: 10.1038/352352a0. [DOI] [PubMed] [Google Scholar]
  13. Howard J., Hudspeth A. J., Vale R. D. Movement of microtubules by single kinesin molecules. Nature. 1989 Nov 9;342(6246):154–158. doi: 10.1038/342154a0. [DOI] [PubMed] [Google Scholar]
  14. Huang T. G., Hackney D. D. Drosophila kinesin minimal motor domain expressed in Escherichia coli. Purification and kinetic characterization. J Biol Chem. 1994 Jun 10;269(23):16493–16501. [PubMed] [Google Scholar]
  15. Huang T. G., Suhan J., Hackney D. D. Drosophila kinesin motor domain extending to amino acid position 392 is dimeric when expressed in Escherichia coli. J Biol Chem. 1994 Jun 10;269(23):16502–16507. [PubMed] [Google Scholar]
  16. Hunt A. J., Gittes F., Howard J. The force exerted by a single kinesin molecule against a viscous load. Biophys J. 1994 Aug;67(2):766–781. doi: 10.1016/S0006-3495(94)80537-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hunt A. J., Howard J. Kinesin swivels to permit microtubule movement in any direction. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11653–11657. doi: 10.1073/pnas.90.24.11653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Huxley A. F., Simmons R. M. Proposed mechanism of force generation in striated muscle. Nature. 1971 Oct 22;233(5321):533–538. doi: 10.1038/233533a0. [DOI] [PubMed] [Google Scholar]
  19. Huxley H. E. The mechanism of muscular contraction. Science. 1969 Jun 20;164(3886):1356–1365. doi: 10.1126/science.164.3886.1356. [DOI] [PubMed] [Google Scholar]
  20. Ishijima A., Harada Y., Kojima H., Funatsu T., Higuchi H., Yanagida T. Single-molecule analysis of the actomyosin motor using nano-manipulation. Biochem Biophys Res Commun. 1994 Mar 15;199(2):1057–1063. doi: 10.1006/bbrc.1994.1336. [DOI] [PubMed] [Google Scholar]
  21. Kamimura S., Mandelkow E. Tubulin protofilaments and kinesin-dependent motility. J Cell Biol. 1992 Aug;118(4):865–875. doi: 10.1083/jcb.118.4.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kuo S. C., Sheetz M. P. Force of single kinesin molecules measured with optical tweezers. Science. 1993 Apr 9;260(5105):232–234. doi: 10.1126/science.8469975. [DOI] [PubMed] [Google Scholar]
  23. Kuznetsov S. A., Vaisberg Y. A., Rothwell S. W., Murphy D. B., Gelfand V. I. Isolation of a 45-kDa fragment from the kinesin heavy chain with enhanced ATPase and microtubule-binding activities. J Biol Chem. 1989 Jan 5;264(1):589–595. [PubMed] [Google Scholar]
  24. Leibler S., Huse D. A. Porters versus rowers: a unified stochastic model of motor proteins. J Cell Biol. 1993 Jun;121(6):1357–1368. doi: 10.1083/jcb.121.6.1357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lombardi V., Piazzesi G., Linari M. Rapid regeneration of the actin-myosin power stroke in contracting muscle. Nature. 1992 Feb 13;355(6361):638–641. doi: 10.1038/355638a0. [DOI] [PubMed] [Google Scholar]
  26. Lymn R. W., Taylor E. W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry. 1971 Dec 7;10(25):4617–4624. doi: 10.1021/bi00801a004. [DOI] [PubMed] [Google Scholar]
  27. Malik F., Brillinger D., Vale R. D. High-resolution tracking of microtubule motility driven by a single kinesin motor. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4584–4588. doi: 10.1073/pnas.91.10.4584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meyhöfer E., Howard J. The force generated by a single kinesin molecule against an elastic load. Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):574–578. doi: 10.1073/pnas.92.2.574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nishizaka T., Yagi T., Tanaka Y., Ishiwata S. Right-handed rotation of an actin filament in an in vitro motile system. Nature. 1993 Jan 21;361(6409):269–271. doi: 10.1038/361269a0. [DOI] [PubMed] [Google Scholar]
  30. Ray S., Meyhöfer E., Milligan R. A., Howard J. Kinesin follows the microtubule's protofilament axis. J Cell Biol. 1993 Jun;121(5):1083–1093. doi: 10.1083/jcb.121.5.1083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rayment I., Holden H. M., Whittaker M., Yohn C. B., Lorenz M., Holmes K. C., Milligan R. A. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 1993 Jul 2;261(5117):58–65. doi: 10.1126/science.8316858. [DOI] [PubMed] [Google Scholar]
  32. Rayment I., Rypniewski W. R., Schmidt-Bäse K., Smith R., Tomchick D. R., Benning M. M., Winkelmann D. A., Wesenberg G., Holden H. M. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993 Jul 2;261(5117):50–58. doi: 10.1126/science.8316857. [DOI] [PubMed] [Google Scholar]
  33. Saito K., Aoki T., Aoki T., Yanagida T. Movement of single myosin filaments and myosin step size on an actin filament suspended in solution by a laser trap. Biophys J. 1994 Mar;66(3 Pt 1):769–777. doi: 10.1016/s0006-3495(94)80853-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sellers J. R., Kachar B. Polarity and velocity of sliding filaments: control of direction by actin and of speed by myosin. Science. 1990 Jul 27;249(4967):406–408. doi: 10.1126/science.2377894. [DOI] [PubMed] [Google Scholar]
  35. Song Y. H., Mandelkow E. Recombinant kinesin motor domain binds to beta-tubulin and decorates microtubules with a B surface lattice. Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1671–1675. doi: 10.1073/pnas.90.5.1671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stewart R. J., Thaler J. P., Goldstein L. S. Direction of microtubule movement is an intrinsic property of the motor domains of kinesin heavy chain and Drosophila ncd protein. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5209–5213. doi: 10.1073/pnas.90.11.5209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Svoboda K., Block S. M. Force and velocity measured for single kinesin molecules. Cell. 1994 Jun 3;77(5):773–784. doi: 10.1016/0092-8674(94)90060-4. [DOI] [PubMed] [Google Scholar]
  38. Svoboda K., Schmidt C. F., Schnapp B. J., Block S. M. Direct observation of kinesin stepping by optical trapping interferometry. Nature. 1993 Oct 21;365(6448):721–727. doi: 10.1038/365721a0. [DOI] [PubMed] [Google Scholar]
  39. Toyoshima Y. Y., Toyoshima C., Spudich J. A. Bidirectional movement of actin filaments along tracks of myosin heads. Nature. 1989 Sep 14;341(6238):154–156. doi: 10.1038/341154a0. [DOI] [PubMed] [Google Scholar]
  40. Vale R. D., Reese T. S., Sheetz M. P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 1985 Aug;42(1):39–50. doi: 10.1016/s0092-8674(85)80099-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wade R. H., Chrétien D. Cryoelectron microscopy of microtubules. J Struct Biol. 1993 Jan-Feb;110(1):1–27. doi: 10.1006/jsbi.1993.1001. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES