Kar3Vik1 mechanochemistry is inhibited by mutation or deletion of the C terminus of the Vik1 subunit

Journal of Biological Chemistry

Volumn 288, Issue 52, 2013, Pages 36957-36970

  Joshi, Monika ^a   Duan, Da ^a   Drew, Doran ^a   Jia, Zhimeng ^a   Davis, Darlene ^a   Campbell, Robert L ^a   Allingham, John S ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

ALLOSTERIC COMMUNICATION; C TERMINUS; KINESINS; MECHANO-CHEMISTRY; MOTOR DOMAIN; STRUCTURAL MOTIFS; STRUCTURAL REARRANGEMENT;

STRUCTURAL DYNAMICS;

ADENOSINE TRIPHOSPHATE; KINESIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; KINETICS; MICROTUBULE; MOLECULAR DYNAMICS; MOTOR HOMOLOGY DOMAIN; NUCLEOTIDE METABOLISM; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; PROTEIN SUBUNIT;

EID: 84891427785     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.492264     Document Type: Article

References (55)

1. Wickstead, B., and Gull, K. (2006) A "holistic" kinesin phylogeny reveals new kinesin families and predicts protein functions. Mol. Biol. Cell 17, 1734-1743
2. Amos, L. A., and Hirose, K. (2007) A cool look at the structural changes in kinesin motor domains. J. Cell Sci. 120, 3919-3927
3. 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., Pate, E., Cooke, R., Taylor, E. W., Milligan, R. A., and Vale, R. D. (1999)Astructural change in the kinesin motor protein that drives motility. Nature 402, 778-784
4. Endres, N. F., Yoshioka, C., Milligan, R. A., and Vale, R. D. (2006) A leverarm rotation drives motility of the minus-end-directed kinesin Ncd. Nature 439, 875-878
5. Kikkawa, M., Sablin, E. P., Okada, Y., Yajima, H., Fletterick, R. J., and Hirokawa, N. (2001) Switch-based mechanism of kinesin motors. Nature 411, 439-445
6. Hwang, W., Lang, M. J., and Karplus, M. (2008) Force generation in kinesin hinges on cover-neck bundle formation. Structure 16, 62-71
7. Khalil, A. S., Appleyard, D. C., Labno, A. K., Georges, A., Karplus, M., Belcher, A. M., Hwang, W., and Lang, M. J. (2008) Kinesin's cover-neck bundle folds forward to generate force. Proc. Natl. Acad. Sci. U.S.A. 105, 19247-19252
8. Sindelar, C. V., and Downing, K. H. (2007) The beginning of kinesin's force-generating cycle visualized at 9-Å resolution. J. Cell Biol. 177, 377-385
9. Heuston, E., Bronner, C. E., Kull, F. J., and Endow, S. A. (2010) A kinesin motor in a force-producing conformation. BMC Struct. Biol. 10, 19
10. Vinogradova, M. V., Malanina, G. G., Reddy, A. S., and Fletterick, R. J. (2009) Structure of the complex of a mitotic kinesin with its calcium binding regulator. Proc. Natl. Acad. Sci. U.S.A. 106, 8175-8179
11. Szczȩsna, E., and Kasprzak, A. A. (2012) The C-terminus of kinesin-14 Ncd is a crucial component of the force generating mechanism. FEBS Lett. 586, 854-858
12. Hahlen, K., Ebbing, B., Reinders, J., Mergler, J., Sickmann, A., and Woehlke, G. (2006) Feedback of the kinesin-1 neck-linker position on the catalytic site. J. Biol. Chem. 281, 18868-18877
13. Yildiz, A., Tomishige, M., Gennerich, A., and Vale, R. D. (2008) Intramolecular strain coordinates kinesin stepping behavior along microtubules. Cell 134, 1030-1041
14. Rosenfeld, S. S., Fordyce, P. M., Jefferson, G. M., King, P. H., and Block, S. M. (2003) Stepping and stretching. How kinesin uses internal strain to walk processively. J. Biol. Chem. 278, 18550-18556
15. Guydosh, N. R., and Block, S. M. (2006) Backsteps induced by nucleotide analogs suggest the front head of kinesin is gated by strain. Proc. Natl. Acad. Sci. U.S.A. 103, 8054-8059
16. Thoresen, T., and Gelles, J. (2008) Processive movement by a kinesin heterodimer with an inactivating mutation in one head. Biochemistry 47, 9514-9521
17. Shastry, S., and Hancock, W. O. (2011) Interhead tension determines processivity across diverse N-terminal kinesins. Proc. Natl. Acad. Sci. U.S.A. 108, 16253-16258
18. Hesse, W. R., Steiner, M., Wohlever, M. L., Kamm, R. D., Hwang, W., and Lang, M. J. (2013) Modular aspects of kinesin force generation machinery. Biophys. J. 104, 1969-1978
19. Duan, D., Jia, Z., Joshi, M., Brunton, J., Chan, M., Drew, D., Davis, D., and Allingham, J. S. (2012) Neck rotation and neck mimic docking in the noncatalytic Kar3-associated protein Vik1. J. Biol. Chem. 287, 40292-40301
20. Ambrose, J. C., Li, W., Marcus, A., Ma, H., and Cyr, R. (2005) A minusend-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol. Biol. Cell 16, 1584-1592
21. Cai, S., Weaver, L. N., Ems-McClung, S. C., and Walczak, C. E. (2009) Kinesin-14 family proteins HSET/XCTK2 control spindle length by crosslinking and sliding microtubules. Mol. Biol. Cell 20, 1348-1359
22. Braun, M., Drummond, D. R., Cross, R. A., and McAinsh, A. D. (2009) The kinesin-14 Klp2 organizes microtubules into parallel bundles by an ATPdependent sorting mechanism. Nat. Cell Biol. 11, 724-730
23. Fink, G., Hajdo, L., Skowronek, K. J., Reuther, C., Kasprzak, A. A., and Diez, S. (2009) The mitotic kinesin-14 Ncd drives directional microtubule-microtubule sliding. Nat. Cell Biol. 11, 717-723
24. Allingham, J. S., Sproul, L. R., Rayment, I., and Gilbert, S. P. (2007) Vik1 modulates microtubule-Kar3 interactions through a motor domain that lacks an active site. Cell 128, 1161-1172
25. Duan, D., Hnatchuk, D. J., Brenner, J., Davis, D., and Allingham, J. S. (2012) Crystal structure of the Kar3-like kinesin motor domain from the filamentous fungus Ashbya gossypii. Proteins 80, 1016-1027
26. Sproul, L. R., Anderson, D. J., Mackey, A. T., Saunders, W. S., and Gilbert, S. P. (2005) Cik1 targets the minus-end kinesin depolymerase Kar3 to microtubule plus ends. Curr. Biol. 15, 1420-1427
27. Huang, T. G., and Hackney, D. D. (1994) Drosophila kinesin minimal motor domain expressed in Escherichia coli. Purification and kinetic characterization. J. Biol. Chem. 269, 16493-16501
28. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815
29. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
30. Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701-1718
31. MacKerell, A. D., Jr., Bashford, D., Dunbrack, R. L., Jr., Evanseck, J. D., Field, M. J., Fischer, S., Gao, J., Guo, H., and Ha, S., Joseph-McCarthy, D., Kuchnir, L., Kuczera, K., Lau, F. T. K., Mattos, C., Michnick, S., Ngo, T., Nguyen, D. T., Prodhom, B., Reiher, W. E., 3rd, Roux, B., Schlenkrich, M., Smith, J. C., Stote, R., Straub, J., Watanabe, M., Wiórkiewicz-Kuczera, J., Yin, D., and Karplus, M. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616
32. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Phys. Chem. 79, 926-935
33. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-38
34. Schrödinger, LLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1, Schrödinger, LLC, Portland, OR
35. Rank, K. C., Chen, C. J., Cope, J., Porche, K., Hoenger, A., Gilbert, S. P., and Rayment, I. (2012) Kar3Vik1, a member of the kinesin-14 superfamily, shows a novel kinesin microtubule binding pattern. J. Cell Biol. 197, 957-970
36. Cope, J., Rank, K. C., Gilbert, S. P., Rayment, I., and Hoenger, A. (2013) Kar3Vik1 uses a minus-end directed powerstroke for movement along microtubules. PLoS ONE 8, e53792
37. Chen, C. J., Porche, K., Rayment, I., and Gilbert, S. P. (2012) The ATPase pathway that drives the kinesin-14 Kar3Vik1 powerstroke. J. Biol. Chem. 287, 36673-36682
38. Gonzalez, M. A., Cope, J., Rank, K. C., Chen, C. J., Tittmann, P., Rayment, I., Gilbert, S. P., and Hoenger, A. (2013) Common mechanistic themes for the powerstroke of kinesin-14 motors. J. Struct. Biol. 184, 335-344
39. Rank, K. C., and Rayment, I. (2013) Functional asymmetry in kinesin and dynein dimers. Biol. Cell 105, 1-13
40. Hackney, D. D. (1994) Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis. Proc. Natl. Acad. Sci. U.S.A. 91, 6865-6869
41. Hancock, W. O., and Howard, J. (1998) Processivity of the motor protein kinesin requires two heads. J. Cell Biol. 140, 1395-1405
42. Yun, M., Bronner, C. E., Park, C. G., Cha, S. S., Park, H. W., and Endow, S. A. (2003) Rotation of the stalk/neck and one head in a new crystal structure of the kinesin motor protein, Ncd. EMBO J. 22, 5382-5389
43. Vale, R. D., and Milligan, R. A. (2000) The way things move: looking under the hood of molecular motor proteins. Science 288, 88-95
44. Block, S. M. (2007) Kinesin motor mechanics: binding, stepping, tracking, gating, and limping. Biophys. J. 92, 2986-2995
45. Carter, N. J., and Cross, R. A. (2005) Mechanics of the kinesin step. Nature 435, 308-312
46. Crevel, I. M., Nyitrai, M., Alonso, M. C., Weiss, S., Geeves, M. A., and Cross, R. A. (2004) What kinesin does at roadblocks: the coordination mechanism for molecular walking. EMBO J. 23, 23-32
47. Hackney, D. D. (2002) Pathway of ADP-stimulated ADP release and dissociation of tethered kinesin from microtubules. Implications for the extent of processivity. Biochemistry 41, 4437-4446
48. Tomishige, M., Stuurman, N., and Vale, R. D. (2006) Single-molecule observations of neck linker conformational changes in the kinesin motor protein. Nat. Struct. Mol. Biol. 13, 887-894
49. Martin, D. S., Fathi, R., Mitchison, T. J., and Gelles, J. (2010) FRET measurements of kinesin neck orientation reveal a structural basis for processivity and asymmetry. Proc. Natl. Acad. Sci. U.S.A. 107, 5453-5458
50. Subramanian, R., and Gelles, J. (2007) Two distinct modes of processive kinesin movement in mixtures of ATP and AMP-PNP. J. Gen. Physiol. 130, 445-455
51. Ebbing, B., Mann, K., Starosta, A., Jaud, J., Schöls, L., Schüle, R., and Woehlke, G. (2008) Effect of spastic paraplegia mutations in KIF5A kinesin on transport activity. Hum. Mol. Genet. 17, 1245-1252
52. Kull, F. J., Sablin, E. P., Lau, R., Fletterick, R. J., and Vale, R. D. (1996) Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 380, 550-555
53. Sindelar, C. V., Budny, M. J., Rice, S., Naber, N., Fletterick, R., and Cooke, R. (2002) Two conformations in the human kinesin power stroke defined by x-ray crystallography and EPR spectroscopy. Nat. Struct. Biol. 9, 844-848
54. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., and Barton, G. J. (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191
55. Higgins, D. G., Thompson, J. D., and Gibson, T. J. (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266, 383-402