To step or not to step? How biochemistry and mechanics influence processivity in Kinesin and Eg5

Current Opinion in Cell Biology

Volumn 19, Issue 1, 2007, Pages 75-81

  Valentine, Megan T ^a   Gilbert, Susan P ^b  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; MOLECULAR MOTOR; PROTEIN EG5; UNCLASSIFIED DRUG;

BINDING AFFINITY; DISSOCIATION; ENERGY; KINETICS; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; STEADY STATE;

ANIMALS; BIOMECHANICS; DIMERIZATION; KINESIN; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PROTEIN BINDING;

EID: 33846350208     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2006.12.011     Document Type: Review

References (56)

1. Miki H., Okada Y., and Hirokawa N. Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol 15 (2005) 467-476
2. Schnitzer M.J., and Block S.M. Kinesin hydrolyses one ATP per 8-nm step. Nature 388 (1997) 386-390
3. Hua W., Young E.C., Fleming M.L., and Gelles J. Coupling of kinesin steps to ATP hydrolysis. Nature 388 (1997) 390-393
4. Valentine M.T., Fordyce P.M., Krzysiak T.C., Gilbert S.P., and Block S.M. Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat Cell Biol 8 (2006) 470-476. This study is the first single molecule analysis of a processive mitotic kinesin. The paper demonstrates biophysical and biochemical characterization of Eg5.
5. Asbury C.L. Kinesin: world's tiniest biped. Curr Opin Cell Biol 17 (2005) 89-97. A thoughtful and balanced review of Kinesin-1 processivity via asymmetric hand-over-hand walking.
6. Yildiz A., and Selvin P.R. Kinesin: walking, crawling or sliding along?. Trends Cell Biol 15 (2005) 112-120
7. Carter N.J., and Cross R.A. Kinesin's moonwalk. Curr Opin Cell Biol 18 (2006) 61-67
8. Cross R.A. The kinetic mechanism of kinesin. Trends Biochem Sci 29 (2004) 301-309. A thoughtful and balanced minireview of the ATPase mechanism of Kinesin-1.
9. Block SM: Kinesin motor mechanics: binding, stepping, tracking, gating, limping... and some newly discovered rotational states. In Molecular Motors: point counterpoint. 2006 Biophysical Society Discussions. URL: http://www.biophysics.org/discussions/2006/study-book.pdf, Block, p. SP13-A.
10. Kapitein L.C., Peterman E.J., Kwok B.H., Kim J.H., Kapoor T.M., and Schmidt C.F. The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 435 (2005) 114-118. An exciting report which shows that purified tetrameric Eg5 can crosslink two parallel microtubules and slide two anti-parallel microtubules relative to one another in vitro.
11. Krzysiak T.C., Wendt T., Sproul L.R., Tittmann P., Gross H., Gilbert S.P., and Hoenger A. A structural model for monastrol inhibition of dimeric kinesin Eg5. EMBO J 25 (2006) 2263-2273. This study shows that AMPPNP promotes an Eg5 two-heads-bound configuration on single microtubule protofilaments.
12. Vale R.D., Reese T.S., and Sheetz M.P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42 (1985) 39-50
13. Howard J., Hudspeth A.J., and Vale R.D. Movement of microtubules by single kinesin molecules. Nature 342 (1989) 154-158
14. Block S.M., Goldstein L.S.B., and Schnapp B.J. Bead movement by single kinesin molecules studied with optical tweezers. Nature 348 (1990) 348-352
15. Hackney D.D. Kinesin ATPase: rate-limiting ADP release. Proc Natl Acad Sci USA 85 (1988) 6314-6318
16. Hackney D.D. Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc Natl Acad Sci USA 91 (1994) 6865-6869
17. Ma Y.-Z., and Taylor E.W. Interacting head mechanism of microtubule-kinesin ATPase. J Biol Chem 272 (1997) 724-730
18. Gilbert S.P., Moyer M.L., and Johnson K.A. Alternating site mechanism of the kinesin ATPase. Biochemistry 37 (1998) 792-799
19. Crevel I., Carter N., Schliwa M., and Cross R.A. Coupled chemical and mechanical reaction steps in a processive Neurospora kinesin. EMBO J 18 (1999) 5863-5872
20. Rice S., Lin A.W., Safer D., Hart C.L., Naber N., Carragher B.O., Cain S.M., Pechatnikova E., Wilson-Kubalek E.M., Whittaker M., et al. A structural change in the kinesin motor protein that drives motility. Nature 402 (1999) 778-784
21. Rosenfeld S.S., Jefferson G.M., and King P.H. ATP reorients the neck linker of kinesin in two sequential steps. J Biol Chem 276 (2001) 40167-40174
22. Rosenfeld S.S., Xing J., Jefferson G.M., Cheung H.C., and King P.H. Measuring kinesin's first step. J Biol Chem 277 (2002) 36731-36739
23. Block S.M., Asbury C.L., Shaevitz J.W., and Lang M.J. Probing the kinesin reaction cycle with a 2D optical force clamp. Proc Natl Acad Sci USA 100 (2003) 2351-2356
24. Klumpp L.M., Hoenger A., and Gilbert S.P. Kinesin's second step. Proc Natl Acad Sci USA 101 (2004) 3444-3449
25. Asbury C.L., Fehr A.N., and Block S.M. Kinesin moves by an asymmetric hand-over-hand mechanism. Science 302 (2003) 2130-2134
26. Kaseda K., Higuchi H., and Hirose K. Alternate fast and slow stepping of a heterodimeric kinesin molecule. Nat Cell Biol 5 (2003) 1079-1082
27. Yildiz A., Tomishige M., Vale R.D., and Selvin P.R. Kinesin walks hand-over-hand. Science 303 (2004) 676-678
28. Hancock W.O., and Howard J. Kinesin's processivity results from mechanical and chemical coordination between the ATP hydrolysis cycles of the two motor domains. Proc Natl Acad Sci USA 96 (1999) 13147-13152
29. Schief W.R., Clark R.H., Crevenna A.H., and Howard J. Inhibition of kinesin motility by ADP and phosphate supports a hand-over-hand mechanism. Proc Natl Acad Sci USA 101 (2004) 1183-1188
30. Rosenfeld S.S., Fordyce P.M., Jeffereson G.M., King P.H., and Block S.M. Stepping and stretching: how kinesin uses internal strain to walk processively. J Biol Chem 278 (2003) 18550-18556
31. Klumpp L.M., Brendza K.M., Rosenberg J.M., Hoenger A., and Gilbert S.P. Motor domain mutation traps kinesin as a microtubule rigor complex. Biochemistry 42 (2003) 2595-2606
32. Crevel I.M., Nyitrai M., Alonso M.C., Weiss S., Geeves M.A., and Cross R.A. What kinesin does at roadblocks: the coordination mechanism for molecular walking. EMBO J 23 (2004) 23-32
33. Guydosh N.R., and Block S.M. Backsteps induced by nucleotide analogs suggest the front head of kinesin is gated by strain. Proc Natl Acad Sci USA 103 (2006) 8054-8059. A careful and thorough analysis of kinesin backstepping induced by nucleotide analogs. The results provide evidence for a gated front head mechanism.
34. Moyer M.L., Gilbert S.P., and Johnson K.A. Purification and characterization of two monomeric kinesin constructs. Biochemistry 35 (1996) 6321-6329
35. Ma Y.-Z., and Taylor E.W. Kinetic mechanism of a monomeric kinesin construct. J Biol Chem 272 (1997) 717-723
36. Gilbert S.P., and Johnson K.A. Pre-steady-state kinetics of the microtubule-kinesin ATPase. Biochemistry 33 (1994) 1951-1960
37. Skiniotis G., Surrey T., Altmann S., Gross H., Song Y.H., Mandelkow E., and Hoenger A. Nucleotide-induced conformations in the neck region of dimeric kinesin. EMBO J 22 (2003) 1518-1528
38. Asenjo A.B., Krohn N., and Sosa H. Configuration of the two kinesin motor domains during ATP hydrolysis. Nat Struct Biol 10 (2003) 836-842
39. i state) with the neck-linker region close to parallel to the microtubule axis.
40. Tomishige M., Stuurman N., and Vale R.D. Single-molecule observations of neck linker conformational changes in the kinesin motor protein. Nat Struct Mol Biol 13 (2006) 887-894
41. Hahlen K., Ebbing B., Reinders J., Mergler J., Sickmann A., and Woehlke G. Feedback of the kinesin-1 neck-linker position on the catalytic site. J Biol Chem 281 (2006) 18868-18877
42. Hackney D.D. The tethered motor domain of a kinesin-microtubule complex catalyzes reversible synthesis of bound ATP. Proc Natl Acad Sci USA 102 (2005) 18338-18343
43. Uemura S., Kawaguchi K., Yajima J., Edamatsu M., Toyoshima Y.Y., and Ishiwata S. Kinesin-microtubule binding depends on both nucleotide state and loading direction. Proc Natl Acad Sci USA 99 (2002) 5977-5981
44. Carter N.J. Cross RA: Mechanics of the kinesin step. Nature 435 (2005) 308-312. This study shows processive backstepping by kinesin under superstall backward loads at an ATP-dependent rate with no indication of substeps.
45. Auerbach S.D., and Johnson K.A. Alternating site ATPase pathway of rat conventional kinesin. J Biol Chem 280 (2005) 37048-37060
46. Svoboda K., Mitra P.P., and Block S.M. Fluctuation analysis of motor protein movement and single enzyme kinetics. Proc Natl Acad Sci USA 91 (1994) 11782-11786
47. Kwok B.H., Yang J.G., and Kapoor T.M. The rate of bipolar spindle assembly depends on the microtubule-gliding velocity of the mitotic kinesin Eg5. Curr Biol 14 (2004) 1783-1788
48. Sharp D.J., McDonald K.L., Brown H.M., Matthies H.J., Walczak C., Vale R., Mitchison T.J., and Scholey J.M. The bipolar kinesin, KLP61F, cross-links microtubules within interpolar microtubule bundles of Drosophila embryonic mitotic spindles. J Cell Biol 144 (1999) 125-138
49. Hildebrandt E.R., Gheber L., Kingsbury T., and Hoyt M.A. Homotetrameric form of Cin8p, a Saccharomyces cerevisiae kinesin-5 motor, is essential for its in vivo function. J Biol Chem 281 (2006) 26004-26013
50. Wilde A., Lizarraga S.B., Zhang L., Wiese C., Gliksman N.R., Walczak C.E., and Zheng Y. Ran stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nat Cell Biol 3 (2001) 221-227
51. Krzysiak T.C., and Gilbert S.P. Dimeric Eg5 maintains processivity through alternating-site catalysis with rate-limiting ATP hydrolysis. J Biol Chem 281 (2006) 39444-39454. This transient-state kinetic analysis identifies Eg5 as the first kinesin motor to have a rate-limiting ATP hydrolysis step. In addition, this study shows a requirement for a slow structural transition upon collision with the microtubule that is required for ATP binding.
52. Rosenfeld S.S., Xing J., Jefferson G.M., and King P.H. Docking and rolling, a model of how the mitotic motor Eg5 works. J Biol Chem 280 (2005) 35684-35695. Fluorescence resonance energy transfer (FRET) is used to measure the structural transitions at the neck linker and other domains of monomeric Eg5 as a function of ATP. This study also documents the requirement for a slow conformational change of the neck linker upon collision with the microtubule and before ATP binding.
53. Turner J., Anderson R., Guo J., Beraud C., Fletterick R., and Sakowicz R. Crystal structure of the mitotic spindle kinesin Eg5 reveals a novel conformation of the neck-linker. J Biol Chem 276 (2001) 25496-25502
54. Yan Y., Sardana V., Xu B., Homnick C., Halczenko W., Buser C.A., Schaber M., Hartman G.D., Huber H.E., and Kuo L.C. Inhibition of a mitotic motor protein: where, how, and conformational consequences. J Mol Biol 335 (2004) 547-554
55. Kwok B.H., Kapitein L.C., Kim J.H., Peterman E.J., Schmidt C.F., and Kapoor T.M. Allosteric inhibition of kinesin-5 modulates its processive directional motility. Nat Chem Biol. 2 (2006) 480-485
56. Klumpp L.M., Mackey A.T., Farrell C.M., Rosenberg J.M., and Gilbert S.P. A kinesin switch I arginine to lysine mutation rescues microtubule function. J Biol Chem 278 (2003) 39059-39067