Active bio-systems: From single motor molecules to cooperative cargo transport

Biophysical Reviews and Letters

Volumn 4, Issue 1-2, 2009, Pages 77-137

  Lipowsky, Reinhard ^a   Beeg, Janina ^a   Dimova, Rumiana ^a   Klumpp, Stefan ^a,b   Liepelt, Steffen ^a   Müller, Melanie J I ^a   Valleriani, Angelo ^a  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bi directional transport; Chemomechanical coupling; Composite motor walks; Force generation; Molecular motors; Motor traffic; Nonequilibrium processes; Uni directional transport

Indexed keywords

ADENOSINE TRIPHOSPHATE; DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; MYOSIN;

ACTIN FILAMENT; BINDING KINETICS; CELL DIVISION; CELL MIGRATION; CELL MOTILITY; CONFORMATIONAL TRANSITION; CYTOSKELETON; DIFFUSION COEFFICIENT; ENERGY BALANCE; ENERGY CONVERSION; ENZYME ACTIVITY; FORCE; HYDROLYSIS; INTRACELLULAR TRANSPORT; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PHASE TRANSITION; PRIORITY JOURNAL; REVIEW; THERMODYNAMICS; VELOCITY;

EID: 66949169605     PISSN: 17930480     EISSN: None     Source Type: Journal    
DOI: 10.1142/s1793048009000946     Document Type: Review

References (99)

1. B. Alberts, D. Bray, A. Johnson, J. Lewis, M. Raff, K. Roberts and P. Walter, Essential Cell Biology: An Introduction to the Molecular Biology of the Cell. Garland, New York, 1998.
2. D. Bray, Cell Movements. Garland Publ., New York, 2001.
3. J. Howard, Mechanics of Motor Proteins and the Cytoskeleton. Sinauer, New York, 1 edition, 2001.
4. M. Schliwa and G. Woehlke, Molecular motors, Nature 422, 759-765 (2003).
5. R.D. Vale, The Molecular Motor Toolbox for Intracellular Transport, Cell 112, 467-480 (2003).
6. R. Lipowsky and S. Klumpp, Life is Motion - Multiscale Motility of Molecular Motors, Physica A 352, 53-112 (2005).
7. R. Lipowsky, Y. Chai, S. Klumpp, S. Liepelt and M. J. I. Müller, Molecular motor traffic: From biological nanomachines to macroscopic transport, Physica A 372, 34-51 (2006).
8. K. Svoboda, Ch. F. Schmidt, B. J. Schnapp and St. M. Block, Direct observation of kinesin stepping by optical trapping interferometry, Nature 365, 721-727 (1993).
9. A. Yildiz, M. Tomishige, R. D. Vale and P. R. Selvin, Kinesin walks hand-over-hand, Science 303, 676-678 (2004).
10. N. J. Carter and R. A. Cross, Mechanics of the kinesin step, Nature 435, 308-312 (2005).
11. M. J. Schnitzer and St. M. Block, Kinesin hydrolyses one ATP per 8-nm step, Nature 388, 386-390 (1997).
12. D. D. Hackney, The tethered motor domain of a kinesin-microtubule complex catalyzes reversible synthesis of bound ATP, PNAS 102 18338-18343 (2005).
13. S. P. Gilbert, M. L. Moyer and K. A. Johnson, Alternating Site Mechanism of the Kinesin ATPase, Biochemistry 37, 792-799 (1998).
14. L. Romberg and R. D. Vale, Chemomechanical cycle of kinesin differs from that of myosin, Nature 361, 168-170 (1993).
15. I. Crevel, A. Lockhart and R. A. Cross, Weak and strong states of kinesin and ncd, J. Mol. Biol. 257, 66-76 (1996).
16. N. R. Guydosh and S. M. Block, Backsteps induced by nucleotide analogs suggest the front head of kinesin is gated by strain, Proc. Nat. Acad. Scie. USA 103, 8054-8059 (2006).
17. S. Liepelt and R. Lipowsky, Steady-state balance conditions for molecular motor cycles and stochastic nonequilibrium processes, EPL 77:50002, 2007.
18. R. Lipowsky and S. Liepelt, Chemomechanical coupling of molecular motors: Thermodynamics, network representations, and balance conditions, J. Stat. Phys. 130, 39-67 (2008).
19. S. Liepelt and R. Lipowsky, Kinesin's network of chemomechanical motor cycles, Phys. Rev. Lett. 98, 258102 (2007).
20. A. Valleriani, S. Liepelt and R. Lipowsky, Dwell time distributions for kinesin's mechanical steps, EPL 82, 28011 (2008).
21. K. Visscher, M. J. Schnitzer and S. M. Block, Single kinesin molecules studied with a molecular force clamp, Nature 400, 184-189 (1999).
22. M. Nishiyama, H. Higuchi and T. Yanagida, Chemomechanical coupling of the forward and backward steps of single kinesin molecules, Nature Cell Biol. 4, 790-797 (2002).
23. M. J. Schnitzer, K. Visscher and S. M. Block, Force production by single kinesin motors, Nature Cell Biology 2, 718-723 (2000).
24. W. R. Schief, R., H. Clark, A. H. Crevenna and J. Howard, Inhibition of kinesin motility by ADP and phosphate supports a hand-over-hand mechanism, PNAS 101, 1183-1188 (2004).
25. S. M. Block, L. S. B. Goldstein and B. J. Schnapp, Bead movement by single kinesin molecules studied with optical tweezers, Nature 348, 348-352 (1990).
26. A. Ajdari, Transport by active filaments, Europhys. Lett. 31 69-74 (1995).
27. R. Lipowsky, S. Klumpp and T. M. Nieuwenhuizen, Random walks of cytoskeletal motors in open and closed compartments, Phys. Rev. Lett. 87, 108101 (2001).
28. T. M. Nieuwenhuizen, S. Klumpp and R. Lipowsky, Movements of molecular motors in two and three dimensions, Europhys. Lett. 58, 468-474 (2002).
29. S. Klumpp and R. Lipowsky, Active diffusion of motor particles, Phys. Rev. Lett. 95, 268102 (2005).
30. S. Klumpp and R. Lipowsky, Cooperative cargo transport by several molecular motors, Proc. Nat. Acad. Sci. USA 102, 17284-17289 (2005).
31. M. Vershinin, B. C. Carter, D. S. Razafsky, S. J. King and S. P. Gross, Multiple-motor based transport and its regulation by Tau, Proc. Nat. Acad. Sci. USA 104, 87-92 (2007).
32. J. Beeg, S. Klumpp, R. Dimova, R. S. Gracia, E. Unger and R. Lipowsky, Transport of beads by several kinesin motors, Biophys. J. 94 532-541 (2008).
33. S. P. Gross, Hither and yon: A review of bi-directional microtubule-based transport, Phys. Biol. 1, R1-R11 (2004).
34. M. A. Welte, Bidirectional Transport along Microtubules, Current Biology 14, R525-R537 (2004).
35. M. J. I. Müller, S. Klumpp and R. Lipowsky, Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors, Proc. Nat. Acad. Sci. USA 105, 4609-4614 (2008).
36. M. A. Welte and S. P. Gross, Molecular motors: A traffic cop within? HFSP J. 2, 178-182 (2008).
37. S. Klumpp and R. Lipowsky, Traffic of molecular motors through open tube-like compartments, J. Stat. Phys. 113, 233-268 (2003).
38. M. J. I. Müuller, S. Klumpp and R. Lipowsky, Molecular motor traffic in a half-open tube, J. Phys. Cond. Mat. 17, S3839-S3850 (2005).
39. S. Klumpp, M. J. I. Müuller and R. Lipowsky, Traffic of Molecular Motors, in A. Schadschneider, T. Pöschel, R. Kühne, M. Schreckenberg and D. E. Wolf, editors, Traffic and Granular Flow 05 pages 251-261. Springer, Berlin, 2007.
40. D. D. Hurd and W. M. Saxton, Kinesin mutations cause motor neuron desease phenotypes by disrupting fast axonal transport in drosophila, Genetics 144, 1075-1085 (1996).
41. M. A. Martin, S. J. Iyadurai, A. Gassman, Jr. J. G. Gindhart, T. S. Hays and W. M. Saxton, Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport, Mol. Biol. Cell 10, 3717-3728 (1999).
42. S. Konzack, Funktion des Kinesin Motorproteins KipA bei der Organisation des Mikrotubuli-Cytoskeletts und beim polaren Wachstum von Aspergillus nidulans, doctoral thesis, University of Marburg (2004).
43. S. Konzack, P. E. Rischitor, C. Enke and R. Fischer, The role of the kinesin motor KipA in microtubule organization and polarized growth of Aspergillus nidulans, Mol. Biol. Cell 16, 497-506 (2005).
44. I. M.-T. C. Crevel, M. Nyitrai, M. C. Alonso, S. Weiss, M. A. Geeves and R. A. Cross, What kinesin does at roadblocks: The coordination mechanism for molecular walking, EMBO Journal 23, 23-32 (2004).
45. C. Leduc, O. Campas, K. B. Zeldovich, A. Roux, P. Jolimaitre, L. Bourel-Bonnet, B. Goud, J.-F. Joanny, P. Bassereau and J. Frost, Cooperative extraction of membrane nanotubes by molecular motors, PNAS 101, 17096-17101 (2004).
46. K. Nishinari, Y. Okada, A. Schadschneider and D. Chowdhury, Intracellular Transport of Single-Headed Molecular Motors KIF1A, Phys. Rev. Lett. 95 118101 (2005).
47. A. Seitz and T. Surrey, Processive movement of single kinesins on crowded microtubules visualized using quantum dots, EMBO Journal 25, 267-277 (2006).
48. S. Klumpp and R. Lipowsky, Phase transitions in systems with two species of molecular motors, Europhys. Lett. 66, 90-96 (2004).
49. P. Kraikivski, R. Lipowsky and J. Kierfeld, Enhanced Ordering of Interacting Filaments by Molecular Motors, Phys. Rev. Lett. 96 258103 (2006).
50. J. Kierfeld, P. Gutjahr, T. Kühne, P. Kraikivski and R. Lipowsky. Buckling, bundling, and pattern formation: From semi-flexible polymers to assemblies of interacting filaments, J. Comp. Theo. Nanosci. 3, 898-911 (2006).
51. R. A. Alberty, Thermodynamics of the Hydrolysis of ATP as a Function of Temperature, pH, pMg, and Ionic Strength, J. Phys. Chem. B 107 12324-12330 (2003).
52. T. L. Hill, Free Energy Transduction and Biochemical Cycle Kinetics Springer Verlag, New York, 1 edition, 1989.
53. A. Yildiz, J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldmann and P. R. Selvin, Myosin V walks handover-hand: Single fluorophore imaging with 1.5-nm localization, Science 300, 2061-2065 (2003).
54. C. Veigel, F. Wang, M. L. Bartoo, J. R. Sellers and J. E. Molloy, The gated gait of the processive molecular motor, myosin V, Nat. Cell Biol. 4, 59-65 (2002).
55. G. Cappello, P. Pierobon, C. Symonds, L. Busoni, J. Gebhardt, M. Rief and J. Frost, Myosin V stepping mechanism, Proc. Nat. Acad. Sci. USA 104, 15328-15333 (2007).
56. R. Lipowsky, Universal aspects of the chemo-mechanical coupling for molecular motors, Phys. Rev. Lett. 85, 4401-4404 (2000).
57. R. Lipowsky and N. Jaster, Molecular motor cycles: From ratchets to networks, J. Stat. Phys. 110, 1141-1167 (2003).
58. U. Seifert, Entropy production along a stochastic trajectory and an integral fluctuation theorem, Phys. Rev. Lett. 95, 040602 (2005).
59. D. J. Evans, E. G. D. Cohen and G. P. Morris, Probability of Second Law Violations in Shearing Steady States, Phys. Rev. Lett. 71, 2401-2404 (1993).
60. G. E. Crooks, Entropy production fluctuation theorem and the nonequilibrium work relation for free energy differences, Phys. Rev. E 60, 2721-2726 (1999).
61. J. L. Lebowitz and H. Spohn, A Gallavotti-Cohen-Type Symmetry in the Large Deviation Functional for Stochastic Dynamics, J. Stat. Phys. 95, 333-365 (1999).
62. C. Jarzynski, Hamiltonian Derivation of a Detailed Fluctuation Theorem, J. Stat. Phys. 98, 77-102 (2000).
63. S. Liepelt and R. Lipowsky, Operation modes of the molecular motor kinesin, Phys. Rev. E (submitted), 2008.
64. St. J. King and T. A. Schroer, Dynactin increases the processivity of the cytoplasmic dynein motor, Nat. Cell Biol. 2, 20-24 (2000).
65. A. D. Mehta, R. S. Rock, M. Rief, J. A. Spudich, M. S. Mooseker and R. E. Cheney, Myosin-V is a processive actin-based motor, Nature 400, 590-593 (1999).
66. Z. Ökten, L. S. Churchman, R. S. Rock and J. A. Spudich, Myosin VI walks hand-over-hand along actin, Nature Struct. Molecular Biol. 11, 884-887 (2004).
67. T. M. Nieuwenhuizen, S. Klumpp and R. Lipowsky, Random Walks of molecular motors arising from diffusional encounters with immobilized filaments, Phys. Rev. E, 69:061911, 2004.
68. S. Klumpp, T. M. Nieuwenhuizen and R. Lipowsky, Self-organized density patterns of molecular motors in arrays of cytoskeletal filaments, Biophys. J. 88, 3118-3132 (2005).
69. T. M. Nieuwenhuizen, S. Klumpp and R. Lipowsky, Walks of molecular motors interacting with immobilized filaments, Physica A 350 122-130 (2005).
70. S. Klumpp, Y. Chai and R. Lipowsky, Effects of the chemomechanical stepping cycle on the traffic of molecular motors, Phys. Rev. E 78, 041909 (2008).
71. D. C. Turner, C. Chang, K. Fang, S. L. Brandow and D. B. Murphy, Selective Adhesion of Functional Microtubules to Patterned Silane Surfaces, Biophys. J. 69, 2782-2789 (1995).
72. H. Suzuki, A. Yamada, K. Oiwa, H. Nakayama and S. Mashiko, Control of Actin Moving Trajectory by Patterned Poly(methylmethacrylate) Tracks, Biophys. J. 72, 1997-2001 (1997).
73. D. Riveline, A. Ott, F. Jülicher, D. A. Winkelmann, O. Cardoso, J.-J. Lacapere, S. Magnusdottir, J.-L. Viovy, L. Gorre-Talini and J. Prost, Acting on actin: The electric motility assay, Eur. Biophys. J. 27, 403-408 (1998).
74. H. Hess, J. Clemmens, D. Qin, J. Howard and V. Vogel, Light-Controlled Molecular Shuttles Made from Motor Proteins Carrying Cargo on Engineered Surfaces, Nano Lett. 1, 235-239 (2001).
75. Y. Hiratsuka, T. Tada, K. Oiwa, T. Kanayama and T. Q. P. Uyeda, Controlling the Direction of Kinesin-Driven Microtubule Movements along Microlithographic Tracks, Biophys. J. 81, 1555-1561 (2001).
76. K. J. Böhm, R. Stracke, P. Mühling and E. Unger, Motor protein-driven unidirectional transport of micrometer-sized cargoes across isopolar microtubule arrays, Nanotechnology 12, 238-244 (2001).
77. L. Limberis, J. J. Magda and R. J. Steward, Polarized Alignment and Surface Immobilization og Microtubules for Kinesin-Powered Nanodevices, Nano Lett. 1, 277-280 (2001).
78. W. H. Roos, A. Roth, J. Konle, H. Presting, E. Sackmann and J. P. Spatz, Freely Suspended Actin Cortex Models on Arrays of Microfabricated Pillars, Chem. Phys. Chem. 4, 872 (2003).
79. R. H. Miller and R. J. Lasek, Cross-bridges Mediate Anterograde and Retrograde Vesicle Transport along Microtubules in Squid Axoplasm, J. Cell Biol. 101, 2181-2193 (1985).
80. A. Ashkin, K. Schütze, J. M. Dziedzic, U. Euteneuer and M. Schliwa, Force generation of organelle transport measured in vivo by an infrared laser trap, Nature 348, 346-348 (1990).
81. S. P. Gross, M. A. Welte, S. M. Block and E. F. Wieschaus, Coordination of opposite-polarity microtubule motors, J. Cell Biol. 156, 715-724 (2002).
82. D. B. Hill, M. J. Plaza, K. Bonin and G. Holzwarth, Fast vesicle transport in PC12 neurites: Velocities and forces, Eur. Biophys. J. 33, 623-632 (2004).
83. C. Kural, H. Kim, S. Syed, G. Goshima, V. I. Gelfand and P. R. Selvin, Kinesin and Dynein Move a Peroxisome in Vivo: A Tug-of-War or Coordinated Movement? Science 308, 1469-1472 (2005).
84. V. Levi, A. S. Serpinskaya, E. Gratton and V. Gelfand, Organelle Transport along Microtubules in Xenopus Melanophores: Evidence for Cooperation between Multiple Motors, Biophys. J. 90, 318-327 (2006).
85. M. J. I. Müller, S. Klumpp and R. Lipowsky, Motility states of molecular motors performing a tug-of-war, J. Stat. Phys. (submitted) 2008.
86. C. T. MacDonald, J. H. Gibbs and A. C. Pipkin, Kinetics of biopolymerization on nucleic acid templates, Biopolymers 6, 1-25 (1968).
87. F. Spitzer, Interaction of Markov Processes, Adv. Math. 5, 246-290 (1970).
88. S. Katz, J. L. Lebowitz and H. Spohn, Nonequilibrium steady-states of stochastic lattice gas models of fast ionic conductors, J. Stat. Phys. 34, 497-537 (1984).
89. J. Krug, Boundary-induced phase transitions in driven diffusive systems, Phys. Rev. Lett. 67, 1882-1885 (1991).
90. A. B. Kolomeisky, G. M. Schütz, E. B. Kolomeisky and J. P. Straley, Phase diagram of one-dimensional driven lattice gases with open boundaries, J. Phys. A: Math. Gen. 31, 6911-6919 (1998).
91. R. K. P. Zia, L. B. Shaw, B. Schmittmann and R. J. Astalos, Contrasts between equilibrium and nonequilibrium steady states: Computer aided discoveries in simple lattice gases, Computer Phys. Commun. 127 23-31 (2000).
92. G.M. Schütz, Exactly solvable models for many-body systems far from equilibrium, in C. Domb and J. L. Lebowitz, editors, Phase Transisions and Critical Phenomena, volume 19, pages 3-251. Academic Press, London, 2001.
93. A. Parmeggiani, T. Franosch and E. Frey, Phase Coexistence in Driven One-Dimensional Transport, Phys. Rev. Lett. 90, 086601/ 1-086601/4 (2003).
94. V. Popkov, A. Rakos, R. D. Willmann, A. B. Kolomeisky and G. M. Schütz, Localization of shocks in driven diffusive systems without particle number conservation, Phys. Rev. E 67, 066117/ 1-066117/6 (2003).
95. M. R. Evans, R. Juhasz and L. Santen, Shock formation in an exclusion process with creation and annihilation, Phys. Rev. E 68, 026117/1-066117/8 (2003).
96. D. T. Woodrum, S. A. Rich and T. D. Pollard, Evidence for biased bidirectional polymerization of actin filaments using heavy meromyosin prepared by an improved method, J. Cell Biol. 67, 231-237 (1975).
97. A. Orlova and E. H. Egelman, Cooperative rigor binding of myosin to actin is a function of F-actin structure, J. Mol. Biol. 265, 469-474 (1997).
98. A. Vilfan, E. Frey, F. Schwabl, M. Thormählen, Y.-H. Song and E. Mandelkow, Dynamics and Cooperativity of Microtubule, Decoration by the Motor Protein Kinesin, J. Mol.Biol. 312, 1011-1026 (2001).
99. E. Muto, H. Sakai and K. Kaseda. Long-range cooperative binding of kinesin to a microtubule in the presence of ATP, J. Cell Biol. 168, 691-696 (2005).