The loop 5 element structurally and kinetically coordinates dimers of the human kinesin-5, Eg5

Biophysical Journal

Volumn 101, Issue 11, 2011, Pages 2760-2769

  Waitzman, Joshua S ^a   Larson, Adam G ^b   Cochran, Jared C ^c   Naber, Nariman ^b   Cooke, Roger ^b   Jon Kull, F ^c   Pate, Edward ^d   Rice, Sarah E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Dartmouth College   (United States)

^d Washington State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3' O (N METHYLANTHRANILOYL)ADENOSINE 5' DIPHOSPHATE; 3'-O-(N-METHYLANTHRANILOYL)ADENOSINE 5'-DIPHOSPHATE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ANTHRANILIC ACID DERIVATIVE; DRUG DERIVATIVE; KIF11 PROTEIN, HUMAN; KINESIN; MUTANT PROTEIN; NUCLEOTIDE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON SPIN RESONANCE; GENETICS; HUMAN; KINETICS; METABOLISM; MICROTUBULE; MOLECULAR PROBE; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; SOLUTION AND SOLUBILITY; STRUCTURE ACTIVITY RELATION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ANTHRANILIC ACIDS; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; KINESIN; KINETICS; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR PROBES; MUTANT PROTEINS; MUTATION; NUCLEOTIDES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; SOLUTIONS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 82955194449     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.10.032     Document Type: Article

References (39)

1. L. Luo, and J.D. Carson R.A. Copeland Conformation-dependent ligand regulation of ATP hydrolysis by human KSP: activation of basal hydrolysis and inhibition of microtubule-stimulated hydrolysis by a single, small molecule modulator J. Am. Chem. Soc. 130 2008 7584 7591
2. L. Luo, and C.A. Parrish K.R. Auger ATP-competitive inhibitors of the mitotic kinesin KSP that function via an allosteric mechanism Nat. Chem. Biol. 3 2007 722 726
3. A.C. Groen, and D. Needleman T.J. Mitchison A novel small-molecule inhibitor reveals a possible role of kinesin-5 in anastral spindle-pole assembly J. Cell Sci. 121 2008 2293 2300
4. T.M. Kapoor, and T.U. Mayer T.J. Mitchison Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5 J. Cell Biol. 150 2000 975 988
5. T.C. Krzysiak, M. Grabe, and S.P. Gilbert Getting in sync with dimeric Eg5. Initiation and regulation of the processive run J. Biol. Chem. 283 2008 2078 2087
6. T.C. Krzysiak, and S.P. Gilbert Dimeric Eg5 maintains processivity through alternating-site catalysis with rate-limiting ATP hydrolysis J. Biol. Chem. 281 2006 39444 39454
7. Y.Z. Ma, and E.W. Taylor Interacting head mechanism of microtubule-kinesin ATPase J. Biol. Chem. 272 1997 724 730
8. M.T. Valentine, and P.M. Fordyce S.M. Block Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro Nat. Cell Biol. 8 2006 470 476
9. R.D. Vale, and T. Funatsu T. Yanagida Direct observation of single kinesin molecules moving along microtubules Nature 380 1996 451 453
10. L.M. Klumpp, and K.M. Brendza S.P. Gilbert Microtubule-kinesin interface mutants reveal a site critical for communication Biochemistry 43 2004 2792 2803
11. Y. Yan, and V. Sardana L.C. Kuo Inhibition of a mitotic motor protein: where, how, and conformational consequences J. Mol. Biol. 335 2004 547 554
12. L. Liu, and S. Parameswaran E.J. Wojcik Loop 5-directed compounds inhibit chimeric kinesin-5 motors: implications for conserved allosteric mechanisms J. Biol. Chem. 286 2011 6201 6210
13. E.D. Kim, and R. Buckley S. Kim Allosteric drug discrimination is coupled to mechanochemical changes in the kinesin-5 motor core J. Biol. Chem. 285 2010 18650 18661
14. W.M. Behnke-Parks, and J. Vendome S.S. Rosenfeld Loop L5 acts as a conformational latch in the mitotic kinesin Eg5 J. Biol. Chem. 286 2011 5242 5253
15. A.G. Larson, and N. Naber S.E. Rice The conserved L5 loop establishes the pre-powerstroke conformation of the Kinesin-5 motor, Eg5 Biophys. J. 98 2010 2619 2627
16. S.S. Rosenfeld, and J. Xing P.H. King Docking and rolling, a model of how the mitotic motor Eg5 works J. Biol. Chem. 280 2005 35684 35695
17. T.D. Harrington, and N. Naber E. Pate Analysis of the interaction of the Eg5 Loop5 with the nucleotide site J. Theor. Biol. 289 2011 107 115
18. Z. Maliga, T.M. Kapoor, and T.J. Mitchison Evidence that monastrol is an allosteric inhibitor of the mitotic kinesin Eg5 Chem. Biol. 9 2002 989 996
19. T.C. Krzysiak, and T. Wendt A. Hoenger A structural model for monastrol inhibition of dimeric kinesin Eg5 EMBO J. 25 2006 2263 2273
20. M. Leonard, and B.D. Song S.L. Schmid Robust colorimetric assays for dynamin's basal and stimulated GTPase activities Methods Enzymol. 404 2005 490 503
21. J.C. Cochran, and C.A. Sontag S.P. Gilbert Mechanistic analysis of the mitotic kinesin Eg5 J. Biol. Chem. 279 2004 38861 38870
22. M.S. Crowder, and R. Cooke Orientation of spin-labeled nucleotides bound to myosin in glycerinated muscle fibers Biophys. J. 51 1987 323 333
23. C.V. Sindelar, and M.J. Budny R. Cooke Two conformations in the human kinesin power stroke defined by x-ray crystallography and EPR spectroscopy Nat. Struct. Biol. 9 2002 844 848
24. A.G. Larson, E.C. Landahl, and S.E. Rice Mechanism of cooperative behavior in systems of slow and fast molecular motors Phys. Chem. Chem. Phys. 11 2009 4890 4898
25. C.L. Parke, and E.J. Wojcik D.K. Worthylake ATP hydrolysis in Eg5 kinesin involves a catalytic two-water mechanism J. Biol. Chem. 285 2010 5859 5867
26. J.C. Cochran, T.C. Krzysiak, and S.P. Gilbert Pathway of ATP hydrolysis by monomeric kinesin Eg5 Biochemistry 45 2006 12334 12344
27. J.C. Cochran, and S.P. Gilbert ATPase mechanism of Eg5 in the absence of microtubules: insight into microtubule activation and allosteric inhibition by monastrol Biochemistry 44 2005 16633 16648
28. Z. Maliga, and J. Xing S.S. Rosenfeld A pathway of structural changes produced by monastrol binding to Eg5 J. Biol. Chem. 281 2006 7977 7982
29. D.D. Hackney Highly processive microtubule-stimulated ATP hydrolysis by dimeric kinesin head domains Nature 377 1995 448 450
30. L.C. Kapitein, and E.J. Peterman C.F. Schmidt The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks Nature 435 2005 114 118
31. B.H. Kwok, and L.C. Kapitein T.M. Kapoor Allosteric inhibition of kinesin-5 modulates its processive directional motility Nat. Chem. Biol. 2 2006 480 485
32. N. Naber, and A. Larson E. Pate Multiple conformations of the nucleotide site of Kinesin family motors in the triphosphate state J. Mol. Biol. 408 2011 628 642
33. N. Naber, and T.J. Minehardt E. Pate Closing of the nucleotide pocket of kinesin-family motors upon binding to microtubules Science 300 2003 798 801
34. S. Brier, and D. Lemaire F. Kozielski Molecular dissection of the inhibitor binding pocket of mitotic kinesin Eg5 reveals mutants that confer resistance to antimitotic agents J. Mol. Biol. 360 2006 360 376
35. C.V. Sindelar, and K.H. Downing The beginning of kinesin's force-generating cycle visualized at 9- resolution J. Cell Biol. 177 2007 377 385
36. S. Rice, and A.W. Lin R.D. Vale A structural change in the kinesin motor protein that drives motility Nature 402 1999 778 784
37. S.S. Rosenfeld, G.M. Jefferson, and P.H. King ATP reorients the neck linker of kinesin in two sequential steps J. Biol. Chem. 276 2001 40167 40174
38. A.J. Bodey, M. Kikkawa, and C.A. Moores 9-ngström structure of a microtubule-bound mitotic motor J. Mol. Biol. 388 2009 218 224
39. H.M. Kantarjian, and S. Padmanabhan M. Minden Phase I/II multicenter study to assess the safety, tolerability, pharmacokinetics and pharmacodynamics of AZD4877 in patients with refractory acute myeloid leukemia Invest. New Drugs 2011 10.1007/s10637-011-9660-2 Epub ahead of print