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. 1996 Feb;70(2):637–653. doi: 10.1016/S0006-3495(96)79605-4

Mechanochemical coupling of the motion of molecular motors to ATP hydrolysis.

R D Astumian 1, M Bier 1
PMCID: PMC1224965  PMID: 8789082

Abstract

The typical biochemical paradigm for coupling between hydrolysis of ATP and the performance of chemical or mechanical work involves a well-defined sequence of events (a kinetic mechanism) with a fixed stoichiometry between the number of ATP molecules hydrolyzed and the turnover of the output reaction. Recent experiments show, however, that such a deterministic picture of coupling may not be adequate to explain observed behavior of molecular motor proteins in the presence of applied forces. Here we present a general model in which the binding of ATP and release of ADP serve to modulate the binding energy of a motor protein as it travels along a biopolymer backbone. The mechanism is loosely coupled--the average number of ATPs hydrolyzed to cause a single step from one binding site to the next depends strongly on the magnitude of an applied force and on the effective viscous drag force. The statistical mechanical perspective described here offers insight into how local anisotrophy along the "track" for a molecular motor, combined with an energy-releasing chemical reaction to provide a source of nonequilibrium fluctuations, can lead to macroscopic motion.

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Selected References

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

  1. Astumian R. D., Chock P. B., Tsong T. Y., Chen Y. D., Westerhoff H. V. Can free energy be transduced from electric noise? Proc Natl Acad Sci U S A. 1987 Jan;84(2):434–438. doi: 10.1073/pnas.84.2.434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Astumian RD, Bier M. Fluctuation driven ratchets: Molecular motors. Phys Rev Lett. 1994 Mar 14;72(11):1766–1769. doi: 10.1103/PhysRevLett.72.1766. [DOI] [PubMed] [Google Scholar]
  3. Astumian RD, Chock PB, Tsong TY, Westerhoff HV. Effects of oscillations and energy-driven fluctuations on the dynamics of enzyme catalysis and free-energy transduction. Phys Rev A Gen Phys. 1989 Jun 15;39(12):6416–6435. doi: 10.1103/physreva.39.6416. [DOI] [PubMed] [Google Scholar]
  4. Faucheux LP, Bourdieu LS, Kaplan PD, Libchaber AJ. Optical thermal ratchet. Phys Rev Lett. 1995 Feb 27;74(9):1504–1507. doi: 10.1103/PhysRevLett.74.1504. [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. 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 Apr 6;374(6522):555–559. doi: 10.1038/374555a0. [DOI] [PubMed] [Google Scholar]
  7. Gilbert S. P., Johnson K. A. Expression, purification, and characterization of the Drosophila kinesin motor domain produced in Escherichia coli. Biochemistry. 1993 May 4;32(17):4677–4684. doi: 10.1021/bi00068a028. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. 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]
  11. Kabata H., Kurosawa O., Arai I., Washizu M., Margarson S. A., Glass R. E., Shimamoto N. Visualization of single molecules of RNA polymerase sliding along DNA. Science. 1993 Dec 3;262(5139):1561–1563. doi: 10.1126/science.8248804. [DOI] [PubMed] [Google Scholar]
  12. Kamp F., Astumian R. D., Westerhoff H. V. Coupling of vectorial proton flow to a biochemical reaction by local electric interactions. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3792–3796. doi: 10.1073/pnas.85.11.3792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Liu D. S., Astumian R. D., Tsong T. Y. Activation of Na+ and K+ pumping modes of (Na,K)-ATPase by an oscillating electric field. J Biol Chem. 1990 May 5;265(13):7260–7267. [PubMed] [Google Scholar]
  16. Magnasco MO. Forced thermal ratchets. Phys Rev Lett. 1993 Sep 6;71(10):1477–1481. doi: 10.1103/PhysRevLett.71.1477. [DOI] [PubMed] [Google Scholar]
  17. McDonald H. B., Stewart R. J., Goldstein L. S. The kinesin-like ncd protein of Drosophila is a minus end-directed microtubule motor. Cell. 1990 Dec 21;63(6):1159–1165. doi: 10.1016/0092-8674(90)90412-8. [DOI] [PubMed] [Google Scholar]
  18. Meister M., Caplan S. R., Berg H. C. Dynamics of a tightly coupled mechanism for flagellar rotation. Bacterial motility, chemiosmotic coupling, protonmotive force. Biophys J. 1989 May;55(5):905–914. doi: 10.1016/S0006-3495(89)82889-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Peskin C. S., Odell G. M., Oster G. F. Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys J. 1993 Jul;65(1):316–324. doi: 10.1016/S0006-3495(93)81035-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Prost J, Chauwin JF, Peliti L, Ajdari A. Asymmetric pumping of particles. Phys Rev Lett. 1994 Apr 18;72(16):2652–2655. doi: 10.1103/PhysRevLett.72.2652. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Robertson B., Astumian R. D. Michaelis-Menten equation for an enzyme in an oscillating electric field. Biophys J. 1990 Oct;58(4):969–974. doi: 10.1016/S0006-3495(90)82441-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rousselet J., Salome L., Ajdari A., Prost J. Directional motion of brownian particles induced by a periodic asymmetric potential. Nature. 1994 Aug 11;370(6489):446–448. doi: 10.1038/370446a0. [DOI] [PubMed] [Google Scholar]
  24. Serpersu E. H., Tsong T. Y. Activation of electrogenic Rb+ transport of (Na,K)-ATPase by an electric field. J Biol Chem. 1984 Jun 10;259(11):7155–7162. [PubMed] [Google Scholar]
  25. 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]
  26. Svoboda K., Mitra P. P., Block S. M. Fluctuation analysis of motor protein movement and single enzyme kinetics. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11782–11786. doi: 10.1073/pnas.91.25.11782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Tsong T. Y., Astumian R. D. Electroconformational coupling: how membrane-bound ATPase transduces energy from dynamic electric fields. Annu Rev Physiol. 1988;50:273–290. doi: 10.1146/annurev.ph.50.030188.001421. [DOI] [PubMed] [Google Scholar]
  29. Vale R. D., Oosawa F. Protein motors and Maxwell's demons: does mechanochemical transduction involve a thermal ratchet? Adv Biophys. 1990;26:97–134. doi: 10.1016/0065-227x(90)90009-i. [DOI] [PubMed] [Google Scholar]
  30. Walker R. A., Salmon E. D., Endow S. A. The Drosophila claret segregation protein is a minus-end directed motor molecule. Nature. 1990 Oct 25;347(6295):780–782. doi: 10.1038/347780a0. [DOI] [PubMed] [Google Scholar]
  31. Westerhoff H. V., Tsong T. Y., Chock P. B., Chen Y. D., Astumian R. D. How enzymes can capture and transmit free energy from an oscillating electric field. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4734–4738. doi: 10.1073/pnas.83.13.4734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Xie T. D., Marszalek P., Chen Y. D., Tsong T. Y. Recognition and processing of randomly fluctuating electric signals by Na,K-ATPase. Biophys J. 1994 Sep;67(3):1247–1251. doi: 10.1016/S0006-3495(94)80594-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

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