An elastically tethered viscous load imposes a regular gait on the motion of myosin-V. Simulation of the effect of transient force relaxation on a stochastic process

Journal of the Royal Society Interface

Volumn 3, Issue 6, 2006, Pages 153-165

  Schilstra, Maria J ^a   Martin, Stephen R ^b  

^a UNIVERSITY OF HERTFORDSHIRE   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Force dependent kinetics; Hybrid simulation; Modelling; Myosin V; Non Markov process; Stochastic

Indexed keywords

MYOSIN V; ACTIN; MOLECULAR MOTOR;

ARTICLE; ELASTICITY; KINETICS; MATHEMATICAL COMPUTING; MUSCLE RELAXATION; SIMULATION; STATISTICS; VISCOSITY; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; MECHANICAL STRESS; METHODOLOGY; MOTION; OSCILLOMETRY; PERIODICITY; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE;

ACTINS; COMPUTER SIMULATION; ELASTICITY; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; MOTION; MYOSIN TYPE V; OSCILLOMETRY; PERIODICITY; PROTEIN CONFORMATION; STOCHASTIC PROCESSES; STRESS, MECHANICAL; STRUCTURE-ACTIVITY RELATIONSHIP; VISCOSITY;

EID: 33746132537     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2005.0098     Document Type: Article

References (34)

1. Atkins, P. W. 1994 Physical chemistry, 7th edn. Oxford, UK: Oxford University Press.
2. Baker, J. E., Krementsova, E. B., Kennedy, G. G., Armstrong, A., Trybus, K. M. & Warshaw, D. M. 2004 Myosin V processivity: multiple kinetic pathways for head-to-head coordination. PNAS 101, 5542-5546. (doi:10. 1073/pnas.0307247101)
3. Bausch, A. R., Möller, W. & Sackmann, E. 1999 Measurement of local viscoelasticity and forces in living cells by magnetic tweezers. Biophys. J. 76, 573-579.
4. Bortz, A. B., Kalos, M. H. & Lebowitz, J. L. 1975 A new algorithm for Monte Carlo simulation of Ising spin systems. J. Comput. Phys. 17, 10-18. (doi:10.1016/0021-9991(75)90060-1)
5. Bustamante, C., Marko, J. F., Siggia, E. D. & Smith, S. 1994 Entropic elasticity of lambda-phage DNA. Science 265, 1599-1600.
6. Clemen, A. E. M., Vilfan, M., Jaud, J., Zhang, J., Barmann, M. & Rief, M. 2005 Force-dependent stepping kinetics of myosin-V. Biophys. J. 88, 4402-4410. (doi:10.1529/biophysj.104.053504)
7. De La Cruz, E. M., Wells, A. L., Rosenfeld, S. S., Ostap, E. M. & Sweeney, H. L. 1999 The kinetic mechanism of myosin V. PNAS 96, 13 726-13 731. (doi:10.1073/pnas.96.24. 13726)
8. De La Cruz, E. M., Ostap, E. M. & Sweeney, H. L. 2001 Kinetic mechanism and regulation of myosin VI. J. Biol. Chem. 276, 32 373-32 381. (doi:10.1074/jbc. M104136200)
9. Duke, T. A. J. 1999 Molecular model of muscle contraction. Proc. Natl. Acad. Sci. USA 96, 2770-2775. (doi:10.1073/ pnas.96.6.2770)
10. Espreafico, E. M., Cheney, R. E., Matteoli, M., Nascimento, A. A., De Camilli, P. V., Larson, R. E. & 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. (doi:10.1083/jcb.119.6.1541)
11. Evans, L., Lee, A., Bridgman, P. & Mooseker, M. 1998 Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell Sci. 111, 2055-2066.
12. Freitas, R. A. 1999 Nanomedicine. Basic capabilities, vol. I, 1st edn. Austin, TX: Landes Bioscience.
13. Gibson, M. A. & Bruck, J. 2000 Efficient exact stochastic simulation of chemical systems with many species and many channels. J. Phys. Chem. A 104, 1876-1889. (doi:10. 1021/jp993732q)
14. Gillespie, D. T. 1977 Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81, 2340-2361. (doi:10. 1021/j100540a008)
15. Happel, J. & Brenner, H. 1983 Low Reynolds number hydrodynamics with special applications to particulate media, pp. 40-49. Dordrecht: Kluwer Press.
16. Kolomeisky, A. B. & Fisher, M. E. 2003 A simple kinetic model describes the processivity of myosin-V. Biophys. J. 84, 1642-1650.
17. Lan, G. & Sun, S. X. 2005 Dynamics of myosin-V processivity. Biophys. J. 88, 999-1008. (doi:10.1529/biophysj.104. 047662)
18. Maita, T., Yajima, E., Nagata, S., Miyanishi, T., Nakayama, S. & Matsuda, G. 1991 The primary structure of skeletal muscle myosin heavy chain: IV. Sequence of the rod, and the complete 1,938-residue sequence of the heavy chain. J. Biochem. (Tokyo) 110, 75-87.
19. Mehta, A. 2001 Myosin learns to walk. J. Cell Sci. 114, 1981-1998.
20. Mehta, A. D., Rock, R. S., Rief, M., Spudich, J. A., Mooseker, M. S. & Cheney, R. E. 1999 Myosin-V is a processive actin-based motor. Nature 400, 590-593. (doi:10.1038/23072)
21. Press, W. H., Flannery, B. P., Teukolsky, B. P. & Vetterling, W. T. 1989 Numerical recipes. The art of scientific computing Fortran version. Cambridge, UK: Cambridge University Press.
22. Reck-Peterson, S. L., Provance Jr, D. W., Mooseker, M. S. & Mercer, J. A. 2000 Class V myosins. Biochim. Biophys. Acta (BBA) - Mol. Cell Res. 1496, 36-51. (doi:10.1016/ S0167-4889(00)00007-0)
23. Rief, M., Fernandez, J. M. & Gaub, H. E. 1998 Elastically coupled two-level systems as a model for biopolymer extensibility. Phys. Rev. Lett. 81, 4764-4767. (doi:10. 1103/PhysRevLett.81.4764)
24. Rief, M., Rock, R. S., Mehta, A. D., Mooseker, M. S., Cheney, R. E. & Spudich, J. A. 2000 Myosin-V stepping kinetics: a molecular model for processivity. PNAS 97, 9482-9486. (doi:10.1073/pnas.97.17.9482)
25. Schwaiger, I., Sattler, C., Hostetter, D. R. & Rief, M. 2002 The myosin coiled-coil is a truly elastic protein structure. Nat. Mat. 1, 232-235. (doi:10.1038/nmat776)
26. Sellers, J. R. 2000 Myosins: a diverse superfamily. Biochim. Biophys. Acta (BBA) - Mol. Cell Res. 1496, 3-22. (doi:10. 1016/S0167-4889(00) 00005-7)
27. Tabb, J., Molyneaux, B., Cohen, D., Kuznetsov, S. & Langford, G. 1998 Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 111, 3221-3234.
28. Titus, M. A. 1997 Motor proteins: myosin V - the multipurpose transport motor. Curr. Biol. 7, R301-R304. (doi:10.1016/S0960-9822(06)00143- 6)
29. Trybus, K. M., Krementsova, E. & Freyzon, Y. 1999 Kinetic characterization of a monomeric unconventional myosin V construct. J. Biol. Chem. 274, 27 448-27 456. (doi:10. 1074/jbc.274.39.27448)
30. Uemura, S., Higuchi, H., Olivares, A. O., De La Cruz, E. M. & Ishiwata, S. 2004 Mechanochemical coupling of two substeps in a single myosin V motor. Nat. Struct. Mol. Biol. 11, 877-883. (doi:10.1038/nsmb806)
31. Vale, R. D. 2003 Myosin V motor proteins: marching stepwise towards a mechanism. J. Cell Biol. 163, 445-450. (doi:10. 1083/jcb.200308093)
32. Veigel, C., Wang, F., Bartoo, M. L., Sellers, J. R. & Molloy, J. E. 2001 The gated gait of the processive molecular motor, myosin V. Nat. Cell Biol. 4, 59-65. (doi:10.1038/ ncb732)
33. Veigel, C., Schmitz, S., Wang, F. & Sellers, J. R. 2005 Load-dependent kinetics of myosin-V can explain its high processivity. Nat. Cell Biol. 7, 861-869. (doi:10.1038/ ncb1287)
34. Vilfan, A. 2005 Elastic lever-arm model for myosin V. Biophys. J. 88, 3792-3805. (doi:10.1529/biophysj.104. 046763)