Two kinesins transport cargo primarily via the action of one motor: Implications for intracellular transport

Biophysical Journal

Volumn 99, Issue 9, 2010, Pages 2967-2977

  Jamison, D Kenneth ^a   Driver, Jonathan W ^a   Rogers, Arthur R ^b   Constantinou, Pamela E ^a   Diehl, Michael R ^a,b  

^a Rice University   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78349232437     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.08.025     Document Type: Article

References (34)

1. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Sunderland, MA.
2. Carter, N. J., and R. A. Cross. 2005. Mechanics of the kinesin step. Nature. 435:308-312.
3. Hancock, W. O., and J. Howard. 1998. Processivity of the motor protein kinesin requires two heads. J. Cell Biol. 140:1395-1405.
4. Schnitzer, M. J., K. Visscher, and S. M. Block. 2000. Force production by single kinesin motors. Nat. Cell Biol. 2:718-723.
5. Gennerich, A., and D. Schild. 2006. Finite-particle tracking reveals submicroscopic-size changes of mitochondria during transport in mitral cell dendrites. Phys. Biol. 3:45-53.
6. Hirokawa, N. 1998. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science. 279:519-526. (Pubitemid 28067273)
7. Kulic, I. M., A. E. X. Brown., V. I. Gelfand. 2008. The role of microtubule movement in bidirectional organelle transport. Proc. Natl. Acad. Sci. USA. 105:10011-10016.
8. Soppina, V., A. K. Rai., R. Mallik. 2009. Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc. Natl. Acad. Sci. USA. 106:19381-19386.
9. Levi, V., A. S. Serpinskaya., V. Gelfand. 2006. Organelle transport along microtubules in Xenopus melanophores: evidence for cooperation between multiple motors. Biophys. J. 90:318-327.
10. Shubeita, G. T., S. L. Tran., S. P. Gross. 2008. Consequences of motor copy number on the intracellular transport of kinesin-1-driven lipid droplets. Cell. 135:1098-1107.
11. Holzbaur, E. L., and Y. E. Goldman. 2010. Coordination of molecular motors: from in vitro assays to intracellular dynamics. Curr. Opin. Cell Biol. 22:4-13.
12. Beeg, J., S. Klumpp., R. Lipowsky. 2008. Transport of beads by several kinesin motors. Biophys. J. 94:532-541.
13. Vershinin, M., B. C. Carter., S. P. Gross. 2007. Multiple-motor based transport and its regulation by Tau. Proc. Natl. Acad. Sci. USA. 104:87-92.
14. Schweller, R. M., P. E. Constantinou., M. R. Diehl. 2008. Design of DNA-conjugated polypeptide-based capture probes for the anchoring of proteins to DNA matrices. Bioconjug. Chem. 19:2304-2307.
15. Diehl, M. R., K. Zhang., D. A. Tirrell. 2006. Engineering cooperativity in biomotor-protein assemblies. Science. 311:1468-1471.
16. Rogers, A. R., J. W. Driver., M. R. Diehl. 2009. Negative interference dominates collective transport of kinesin motors in the absence of load. Phys. Chem. Chem. Phys. 11:4882-4889.
17. Sims, P. A., and X. S. Xie. 2009. Probing dynein and kinesin stepping with mechanical manipulation in a living cell. ChemPhysChem. 10:1511-1516.
18. Coppin, C. M., D. W. Pierce., R. D. Vale. 1997. The load dependence of kinesin's mechanical cycle. Proc. Natl. Acad. Sci. USA. 94:8539-8544.
19. Kojima, H., E. Muto., T. Yanagida. 1997. Mechanics of single kinesin molecules measured by optical trapping nanometry. Biophys. J. 73:2012-2022.
20. Leduc, C., F. Ruhnow., S. Diez. 2007. Detection of fractional steps in cargo movement by the collective operation of kinesin-1 motors. Proc. Natl. Acad. Sci. USA. 104:10847-10852.
21. Fehr, A. N., C. L. Asbury, and S. M. Block. 2008. Kinesin steps do not alternate in size. Biophys. J. 94: L20-L22.
22. Gittes, F., E. Meyhöfer., J. Howard. 1996. Directional loading of the kinesin motor molecule as it buckles a microtubule. Biophys. J. 70:418-429.
23. Yildiz, A., M. Tomishige., P. R. Selvin. 2004. Kinesin walks hand-over-hand. Science. 303:676-678.
24. Klumpp, S., and R. Lipowsky. 2005. Cooperative cargo transport by several molecular motors. Proc. Natl. Acad. Sci. USA. 102:17284-17289.
25. Lan, G., and S. X. Sun. 2005. Dynamics of myosin-driven skeletal muscle contraction: I. Steady-state force generation. Biophys. J. 88:4107-4117.
26. Constantinou, P. E., and M. R. Diehl. 2010. The mechanochemistry of integrated motor protein complexes. J. Biomech. 43:31-37.
27. Kunwar, A., M. Vershinin., S. P. Gross. 2008. Stepping, strain gating, and an unexpected force-velocity curve for multiplemotor-based transport. Curr. Biol. 18:1173-1183.
28. Driver, J. W., A. R. Rogers., M. R. Diehl. 2010. Coupling between motor proteins determines dynamic behaviors of motor protein assemblies. Phys. Chem. Chem. Phys. 12:10398-10405.
29. Kawaguchi, K., S. Uemura, and S. Ishiwata. 2003. Equilibrium and transition between single-and double-headed binding of kinesin as revealed by single-molecule mechanics. Biophys. J. 84:1103-1113.
30. Bruno, L., M. M. Echarte, and V. Levi. 2008. Exchange of microtubule molecular motors during melanosome transport in Xenopus laevis melanophores is triggered by collisions with intracellular obstacles. Cell Biochem. Biophys. 52:191-201.
31. Laney, D. E., R. A. Garcia., H. G. Hansma. 1997. Changes in the elastic properties of cholinergic synaptic vesicles as measured by atomic force microscopy. Biophys. J. 72:806-813.
32. Mallik, R., B. C. Carter., S. P. Gross. 2004. Cytoplasmic dynein functions as a gear in response to load. Nature. 427:649-652.
33. King, S. J., and T. A. Schroer. 2000. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat. Cell Biol. 2:20-24.
34. Ross, J. L., H. Shuman., Y. E. Goldman. 2008. Kinesin and dyneindynactin at intersecting microtubules: motor density affects dynein function. Biophys. J. 94:3115-3125.