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PMID: 8265603 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Kinesin swivels to permit microtubule movement in any direction.

Hunt AJ, Howard J

Abstract

Kinesin is a motor protein that uses the energy derived from ATP hydrolysis to transport organelles along microtubules. By analyzing the thermal fluctuation of microtubules tethered to glass surfaces by single molecules of kinesin, we have measured the torsional flexibility of the motor protein. The torsional stiffness of kinesin, (117 +/- 19) x 10(-24) N.m.rad-1 (mean +/- SEM), is so low that one kT of energy (approximately 4.1 x 10(-21) J at room temperature) is sufficient to twist a kinesin molecule through more than 360 degrees from its resting orientation. Consistent with this flexibility, motility assays show that one or more kinesin molecules can move a microtubule equally well in any direction. These results explain how a motor on the surface of an organelle can rapidly bind to and capture a microtubule irrespective of the organelle's orientation. Furthermore, the flexibility ensures that several motors can efficiently work together even though they are randomly oriented on the surface of an organelle rather than being in precise arrays like the motors of muscle and cilia.

MeSH Terms
Cilia/physiology Kinesins/chemistry,physiology Mathematics Microtubules/physiology Models, Biological Movement Muscles/physiology Thermodynamics
Chemicals
Kinesins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Hunt A J
Department of Physiology and Biophysics, University of Washington, Seattle 98195.
Howard J
References (27)
27 references, click to expand
  1. The mechanism of muscular contraction.
    Science. 1969 Jun 20;164(3886):1356-65 PMID: 4181952
  2. Assay of microtubule movement driven by single kinesin molecules.
    Methods Cell Biol. 1993;39:137-47 PMID: 8246794
  3. Segmental flexibility of the S-1 moiety of myosin.
    Biochemistry. 1973 Jun 5;12(12):2250-5 PMID: 4575787
  4. Motion of subfragment-1 in myosin and its supramolecular complexes: saturation transfer electron paramagnetic resonance.
    Proc Natl Acad Sci U S A. 1975 May;72(5):1729-33 PMID: 168572
  5. Can a myosin molecule bind to two actin filaments?
    Nature. 1978 Jan 26;271(5643):325-9 PMID: 622172
  6. Electron microscopy of thin filaments decorated with a Ca2+-regulated myosin.
    J Mol Biol. 1980 Jun 15;140(1):35-55 PMID: 6997502
  7. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility.
    Cell. 1985 Aug;42(1):39-50 PMID: 3926325
  8. A novel brain ATPase with properties expected for the fast axonal transport motor.
    Nature. 1985 Sep 5-11;317(6032):73-5 PMID: 2412134
  9. Cross-bridges mediate anterograde and retrograde vesicle transport along microtubules in squid axoplasm.
    J Cell Biol. 1985 Dec;101(6):2181-93 PMID: 2415536
  10. Myosin movement in vitro: a quantitative assay using oriented actin cables from Nitella.
    Methods Enzymol. 1986;134:531-44 PMID: 3821577
  11. Hindered diffusion of inert tracer particles in the cytoplasm of mouse 3T3 cells.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4910-3 PMID: 3474634
  12. Microtubule structure at 18 A resolution.
    J Mol Biol. 1987 Mar 20;194(2):257-64 PMID: 3612805
  13. Kinesin from pig brain studied by electron microscopy.
    J Cell Sci. 1987 Feb;87 ( Pt 1):105-11 PMID: 3117808
  14. 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):589-95 PMID: 2521221
  15. Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains.
    J Cell Biol. 1988 Dec;107(6 Pt 2):2657-67 PMID: 2974459
  16. Identification of globular mechanochemical heads of kinesin.
    Nature. 1989 Mar 23;338(6213):355-7 PMID: 2493586
  17. Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration.
    Cell. 1989 Mar 10;56(5):867-78 PMID: 2522351
  18. A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses.
    Cell. 1989 Mar 10;56(5):879-89 PMID: 2522352
  19. Bidirectional movement of actin filaments along tracks of myosin heads.
    Nature. 1989 Sep 14;341(6238):154-6 PMID: 2674720
  20. Movement of microtubules by single kinesin molecules.
    Nature. 1989 Nov 9;342(6246):154-8 PMID: 2530455
  21. Evidence that the head of kinesin is sufficient for force generation and motility in vitro.
    Science. 1990 Jul 6;249(4964):42-7 PMID: 2142332
  22. Polarity and velocity of sliding filaments: control of direction by actin and of speed by myosin.
    Science. 1990 Jul 27;249(4967):406-8 PMID: 2377894
  23. Bead movement by single kinesin molecules studied with optical tweezers.
    Nature. 1990 Nov 22;348(6299):348-52 PMID: 2174512
  24. Preparation of modified tubulins.
    Methods Enzymol. 1991;196:478-85 PMID: 2034137
  25. What is the pitch of the alpha-helical coiled coil?
    Proteins. 1992 Dec;14(4):425-9 PMID: 1438180
  26. Force-velocity relationships in kinesin-driven motility.
    Nature. 1993 Jul 29;364(6436):457-9 PMID: 8332217
  27. Segmental flexibility in an antibody molecule.
    J Mol Biol. 1970 Aug;51(3):573-90 PMID: 5492607
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1993-12-15
Pages
11653-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC48042
Subset
IM
Grants
NIAMS NIH HHS · AR40593 · United States
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