Force and premature binding of ADP can regulate the processivity of individual Eg5 dimers

Biophysical Journal

Volumn 97, Issue 6, 2009, Pages 1671-1677

  Valentine, Megan T ^a   Block, Steven M ^b  

^a University of California   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DIMER; KINESIN; KINESIN EG5; MOLECULAR MOTOR; NUCLEOTIDE; PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; CONTROLLED STUDY; ENZYME INHIBITION; FORCE; HIGH RESOLUTION COMPUTER TOMOGRAPHY; HUMAN; MICROTUBULE ASSEMBLY; MOLECULAR MODEL; NONHUMAN; OPTICAL TWEEZERS; PROTEIN DOMAIN; PROTEIN PROCESSING;

EID: 70350011897     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.07.013     Document Type: Article

References (28)

1. Kapitein, L. C., E. J. G. Peterman, B. H. Kwok, J. H. Kim, T. M. Kapoor, et al. 2005. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature. 435:114-118.
2. Korneev, M., S. Lakämper, and C. Schmidt. 2007. Load-dependent release limits the processive stepping of the tetrameric Eg5 motor. Eur. Biophys. J. 36:675-681.
3. Valentine, M. T., P. M. Fordyce, T. C. Krzysiak, S. P. Gilbert, and S. M. Block. 2006. Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat. Cell Biol. 8:470-476.
4. Cochran, J. C., T. C. Krzysiak, and S. P. Gilbert. 2006. Pathway of ATP hydrolysis by monomeric kinesin Eg5. Biochemistry. 45:12334-12344.
5. Krzysiak, T. C., and S. P. Gilbert. 2006. Dimeric Eg5 maintains processivity through alternating-site catalysis with rate-limiting ATP hydrolysis. J. Biol. Chem. 281:39444-39454.
6. Krzysiak, T. C., M. Grabe, and S. P. Gilbert. 2008. Getting in sync with dimeric Eg5: initiation and regulation of the processive run. J. Biol. Chem. 283:2078-2087.
7. Gilbert, S. P., and A. T. Mackey. 2000. Kinetics: a tool to study molecular motors. Methods. 22:337-354.
8. Lang, M. J., P. M. Fordyce, A. M. Engh, K. C. Neuman, and S. M. Block. 2004. Simultaneous, coincident optical trapping and single-molecule fluorescence. Nat. Methods. 1:133-139.
9. Block, S. M., C. L. Asbury, J. W. Shaevitz, and M. J. Lang. 2003. Probing the kinesin reaction cycle with a 2D optical force clamp. Proc. Natl. Acad. Sci. USA. 100:2351-2356.
10. Lang, M. J., C. L. Asbury, J. W. Shaevitz, and S. M. Block. 2002. An automated two-dimensional optical force clamp for single molecule studies. Biophys. J. 83:491-501. (Pubitemid 34694752)
11. Neuman, K. C., and S. M. Block. 2004. Optical trapping. Rev. Sci. Instrum. 75:2787-2809.
12. Schnitzer, M. J., and S. M. Block. 1997. Kinesin hydrolyses one ATP per 8-nm step. Nature. 388:386-390.
13. Colquhoun, D., and A. G. Hawkes. 1995. The principles of stochastic interpretation of ion-channel mechanisms. In Single Channel Recording. B. Sakmann and E. Neher, editors. Plenum, New York. 397-482.
14. Rosenfeld, S. S., P. M. Fordyce, G. M. Jefferson, P. H. King, and S. M. Block. 2003. Stepping and stretching: how kinesin uses internal strain to walk processively. J. Biol. Chem. 278:18550-18556.
15. Carter, N., and R. Cross. 2005. Mechanics of the kinesin step. Nature. 435:308-312.
16. Cochran, J. C., and S. P. Gilbert. 2005. ATPase mechanism of Eg5 in the absence of microtubules: insight into microtubule activation and allosteric inhibition by monastrol. Biochemistry. 44:16633-16648.
17. Hackney, D. D. 1988. Kinesin ATPase: rate-limiting ADP release. Proc. Natl. Acad. Sci. USA. 85:6314-6318.
18. Shimizu, T., E. Sablin, R. D. Vale, R. Fletterick, E. Pechatnikova, et al. 2002. Expression, purification, ATPase properties, and microtubule-binding properties of the ncd motor domain. Biochemistry. 34:13259-13266.
19. Asenjo, A. B., N. Krohn, and H. Sosa. 2003. Configuration of the two kinesin motor domains during ATP hydrolysis. Nat. Struct. Biol. 10:836-842.
20. Asenjo, A. B., and H. Sosa. 2009. A mobile kinesin-head intermediate during the ATP-waiting state. Proc. Natl. Acad. Sci. USA. 106:5657-5662.
21. Mori, T., R. D. Vale, and M. Tomishige. 2007. How kinesin waits between steps. Nature. 450:750-754.
22. Guydosh, N. R., and S. M. Block. 2009. Direct observation of the binding state of the kinesin head to the microtubule. Nature. 10.1038/nature08259.
23. Klumpp, L. M., A. Hoenger, and S. P. Gilbert. 2004. Kinesin's second step. Proc. Natl. Acad. Sci. USA. 101:3444-3449.
24. Sosa, H., E. J. G. Peterman, W. E. Moerner, and L. S. B. Goldstein. 2001. ADP-induced rocking of the kinesin motor domain revealed by single-molecule fluorescence polarization microscopy. Nat. Struct. Mol. Biol. 8:540-544.
25. Krzysiak, T. C., T. Wendt, L. R. Sproul, P. Tittmann, H. Gross, S. P. Gilbert, and A. Hoenger. 2006. A structural model for monastrol inhibition of dimeric kinesin Eg5. EMBO J. 25:2263-2273.
26. Rosenfeld, S. S., J. Xing, G. M. Jefferson, and P. H. King. 2005. Docking and rolling, a model of how the mitotic motor Eg5 works. J. Biol. Chem. 280:35684-35695.
27. Kapitein, L. C., B. H. Kwok, J. S. Weinger, C. F. Schmidt, T. M. Kapoor, et al. 2008. Microtubule cross-linking triggers the directional motility of kinesin-5. J. Cell Biol. 182:421-428.
28. Kwok, B. H., L. C. Kapitein, J. H. Kim, E. J. G. Peterman, C. F. Schmidt, et al. 2006. Allosteric inhibition of kinesin-5 modulates its processive directional motility. Nat. Chem. Biol. 2:480-485.