Walking, hopping, diffusing and braking modes of kinesin-5

Biochemical Society Transactions

Volumn 37, Issue 5, 2009, Pages 1045-1049

  Kaseda, Kuniyoshi ^a   McAinsh, Andrew D ^a   Cross, Robert A ^a  

^a MARIE CURIE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Bipolar spindle formation; Eg5; Kinesin 5; Molecular motor; Monastrol

Indexed keywords

EG 5 PROTEIN; KINESIN; KINESIN 5; UNCLASSIFIED DRUG;

CONFERENCE PAPER; IN VITRO STUDY; MEIOSIS; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; SPINDLE CELL;

ANIMALS; CELL CYCLE; HUMANS; KINESIN; MICROTUBULES; MITOTIC SPINDLE APPARATUS; PROTEIN ISOFORMS;

VERTEBRATA;

EID: 70350136402     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0371045     Document Type: Conference Paper

References (59)

1. Gadde, S. and Heald, R. (2004) Mechanisms and molecules of the mitotic spindle. Curr. Biol. 14, R797-R805
2. Mogilner, A., Wollman, R., Civelekoglu-Scholey, G. and Scholey, J. (2006) Modeling mitosis. Trends Cell Biol. 16, 88-96
3. O'Connell, C.B. and Khodjakov, A.L. (2007) Cooperative mechanisms of mitotic spindle formation. J. Cell Sci. 120, 1717-1722
4. Burbank, K.S., Mitchison, T.J. and Fisher, D.S. (2007) Slide-and-cluster models for spindle assembly. Curr. Biol. 17, 1373-1383
5. Goshima, G., Wollman, R., Goodwin, S.S., Zhang, N., Scholey, J.M., Vale, R.D. and Stuurman, N. (2007) Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421
6. Hoyt, M.A., He, L., Loo, K.K. and Saunders, W.S. (1992) Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly. J. Cell Biol. 118, 109-120
7. Roof, D.M., Meluh, P.B. and Rose, M.D. (1992) Kinesin-related proteins required for assembly of the mitotic spindle. J. Cell Biol. 118, 95-108
8. Castro, A., Mandart, E., Lorca, T. and Galas, S. (2003) Involvement of Aurora A kinase during meiosis I-II transition in Xenopus oocytes. J. Biol. Chem. 278, 2236-2241
9. Enos, A.P. and Morris, N.R. (1990) Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell 60, 1019-1027
10. Hagan, I. and Yanagida, M. (1990) Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene. Nature 347, 563-566
11. Blangy, A., Lane, H.A., d'Herin, P., Harper, M., Kress, M. and Nigg, E.A. (1995) Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell 83, 1159-1169
12. Sawin, K.E. and Mitchison, T.J. (1995) Mutations in the kinesin-like protein Eg5 disrupting localization to the mitotic spindle. Proc. Natl. Acad. Sci. U.S.A. 92, 4289-4293
13. Cahu, J., Olichon, A., Hentrich, C., Schek, H., Drinjakovic, J., Zhang, C., Doherty-Kirby, A., Lajoie, G. and Surrey, T. (2008) Phosphorylation by Cdk1 increases the binding of Eg5 to microtubules in vitro and in Xenopus egg extract spindles. PLoS ONE 3, e3936
14. van den Wildenberg, S.M., Tao, L., Kapitein, L.C., Schmidt, C.F., Scholey, J.M. and Peterman, E.J. (2008) The homotetrameric kinesin-5 KLP61F preferentially crosslinks microtubules into antiparallel orientations. Curr. Biol. 18, 1860-1864
15. Cole, D.G., Saxton, W.M., Sheehan, K.B. and Scholey, J.M. (1994) A "slow" homotetrameric kinesin-related motor protein purified from Drosophila embryos. J. Biol. Chem. 269, 22913-22916
16. Kashina, A.S., Baskin, R.J., Cole, D.G., Wedaman, K.P., Saxton, W.M. and Scholey, J.M. (1996) A bipolar kinesin. Nature 379, 270-272
17. Sawin, K.E., LeGuellec, K., Philippe, M. and Mitchison, T.J. (1992) Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359, 540-543
18. Kapitein, L.C., Peterman, E.J., Kwok, B.H., Kim, J.H., Kapoor, T.M. and Schmidt, C.F. (2005) The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 435, 114-118
19. Lockhart, A. and Cross, R.A. (1994) Origins of reversed directionality in the ncd molecular motor. EMBO J. 13, 751-757
20. Cochran, J.C., Sontag, C.A., Maliga, Z., Kapoor, T.M., Correia, J.J. and Gilbert, S.P. (2004) Mechanistic analysis of the mitotic kinesin Eg5. J. Biol. Chem. 279, 38861-38870
21. Rosenfeld, S.S., Xing, J., Jefferson, G.M. and King, P.H. (2005) Docking and rolling, a model of how the mitotic motor Eg5 works. J. Biol. Chem. 280, 35684-35695
22. Turner, J., Anderson, R., Guo, J., Beraud, C., Fletterick, R. and Sakowicz, R. (2001) Crystal structure of the mitotic spindle kinesin Eg5 reveals a novel conformation of the neck-linker. J. Biol. Chem. 276, 25496-25502
23. Hirose, K., Henningsen, U., Schliwa, M., Toyoshima, C., Shimizu, T., Alonso, M., Cross, R.A. and Amos, L.A. (2000) Structural comparison of dimeric Eg5, Neurospora kinesin (Nkin) and Ncd head-Nkin neck chimera with conventional kinesin. EMBO J. 19, 5308-5314
24. Bodey, A.J., Kikkawa, M. and Moores, C.A. (2009) 9-Angstrom structure of a microtubule-bound mitotic motor. J. Mol. Biol. 388, 218-224
25. Valentine, M.T., Fordyce, P.M., Krzysiak, T.C., Gilbert, S.P. and Block, S.M. (2006) Individual dimers of the mitotic kinesin motor Eg5 step processively and support substantial loads in vitro. Nat. Cell Biol. 8, 470-476
26. Kaseda, K., Crevel, I., Hirose, K. and Cross, R.A. (2008) Single-headed mode of kinesin-5. EMBO Rep. 9, 761-765
27. Yajima, J., Mizutani, K. and Nishizaka, T. (2008) A torque component present in mitotic kinesin Eg5 revealed by three-dimensional tracking. Nat. Struct. Mol. Biol. 15, 1119-1121
28. Mayer, T.U., Kapoor, T.M., Haggarty, S.J., King, R.W., Schreiber, S.L. and Mitchison, T.J. (1999) Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971-974
29. Crevel, I.M., Alonso, M.C. and Cross, R.A. (2004) Monastrol stabilises an attached low-friction mode of Eg5. Curr. Biol. 14, R411-R412
30. Sarli, V. and Giannis, A. (2008) Targeting the kinesin spindle protein: basic principles and clinical implications. Clin. Cancer Res. 14, 7583-7587
31. Korneev, M.J., Lakamper, S. and Schmidt, C.F. (2007) Load-dependent release limits the processive stepping of the tetrameric Eg5 motor. Eur. Biophys. J. 36, 675-681
32. Sharp, D.J., Yu, K.R., Sisson, J.C., Sullivan, W. and Scholey, J.M. (1999) Antagonistic microtubule-sliding motors position mitotic centrosomes in Drosophila early embryos. Nat. Cell Biol. 1, 51-54
33. Hancock, W.O. and Howard, J. (1998) Processivity of the motor protein kinesin requires two heads. J. Cell Biol. 140, 1395-1405
34. Crevel, I.M., Lockhart, A. and Cross, R.A. (1997) Kinetic evidence for low chemical processivity in ncd and Eg5. J. Mol. Biol. 273, 160-170
35. Okada, Y. and Hirokawa, N. (1999) A processive single-headed motor: kinesin superfamily protein KIF1A. Science 283, 1152-1157
36. Furuta, K. and Toyoshima, Y.Y. (2008) Minus-end-directed motor Ncd exhibits processive movement that is enhanced by microtubule bundling in vitro. Curr. Biol. 18, 152-157
37. Krzysiak, T.C. and Gilbert, S.P. (2006) Dimeric Eg5 maintains processivity through alternating-site catalysis with rate-limiting ATP hydrolysis. J. Biol. Chem. 281, 39444-39454
38. Kwok, B.H., Kapitein, L.C., Kim, J.H., Peterman, E.J., Schmidt, C.F. and Kapoor, T.M. (2006) Allosteric inhibition of kinesin-5 modulates its processive directional motility. Nat. Chem. Biol. 2, 480-485
39. Kapitein, L.C., Kwok, B.H., Weinger, J.S., Schmidt, C.F., Kapoor, T.M. and Peterman, E.J. (2008) Microtubule cross-linking triggers the directional motility of kinesin-5. J. Cell Biol. 182, 421-428
40. Tao, L., Mogilner, A., Civelekoglu-Scholey, G., Wollman, R., Evans, J., Stahlberg, H. and Scholey, J.M. (2006) A homotetrameric kinesin-5, KLP61F, bundles microtubules and antagonizes Ncd in motility assays. Curr. Biol. 16, 2293-2302
41. Saunders, A.M., Powers, J., Strome, S. and Saxton, W.M. (2007) Kinesin-5 acts as a brake in anaphase spindle elongation. Curr. Biol. 17, R453-454
42. Tikhonenko, I., Nag, D.K., Martin, N. and Koonce, M.P. (2008) Kinesin-5 is not essential for mitotic spindle elongation in Dictyostelium. Cell Motil. Cytoskeleton 65, 853-862
43. Myers, K.A. and Baas, P.W. (2007) Kinesin-5 regulates the growth of the axon by acting as a brake on its microtubule array. J. Cell Biol. 178, 1081-1091
44. Saunders, W.S. and Hoyt, M.A. (1992) Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell 70, 451-458
45. Heck, M.M., Pereira, A., Pesavento, P., Yannoni, Y., Spradling, A.C. and Goldstein, L.S. (1993) The kinesin-like protein KLP61F is essential for mitosis in Drosophila. J. Cell Biol. 123, 665-679
46. Saunders, W., Lengyel, V. and Hoyt, M.A. (1997) Mitotic spindle function in Saccharomyces cerevisiae requires a balance between different types of kinesin-related motors. Mol. Biol. Cell 8, 1025-1033
47. Straight, A.F., Sedat, J.W. and Murray, A.W. (1998) Time-lapse microscopy reveals unique roles for kinesins during anaphase in budding yeast. J. Cell Biol. 143, 687-694
48. Walczak, C.E., Vernos, I., Mitchison, T.J., Karsenti, E. and Heald, R. (1998) A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity. Curr. Biol. 8, 903-913
49. Sharp, D.J., Rogers, G.C. and Scholey, J.M. (2000) Roles of motor proteins in building microtubule-based structures: a basic principle of cellular design. Biochim. Biophys. Acta 1496, 128-141
50. Brust-Mascher, I., Civelekoglu-Scholey, G., Kwon, M., Mogilner, A. and Scholey, J.M. (2004) Model for anaphase B: role of three mitotic motors in a switch from poleward flux to spindle elongation. Proc. Natl. Acad. Sci. U.S.A. 101, 15938-15943
51. Tanenbaum, M.E., Macurek, L., Galjart, N. and Medema, R.H. (2008) Dynein, Lis1 and CLIP-170 counteract Eg5-dependent centrosome separation during bipolar spindle assembly. EMBO J. 27, 3235-3245
52. Toso, A., Winter, J.R., Garrod, A.J., Amaro, A.C., Meraldi, P. and McAinsh, A.D. (2009) Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly. J. Cell Biol. 184, 365-372
53. Sharp, D.J., McDonald, K.L., Brown, H.M., Matthies, H.J., Walczak, C., Vale, R.D., Mitchison, T.J. and Scholey, J.M. (1999) The bipolar kinesin, KLP61F, cross-links microtubules within interpolar microtubule bundles of Drosophila embryonic mitotic spindles. J. Cell Biol. 144, 125-138
54. Brust-Mascher, I., Sommi, P., Cheerambathur, D.K. and Scholey, J.M. (2009) Kinesin-5-dependent poleward flux and spindle length control in Drosophila embryo mitosis. Mol. Biol. Cell 20, 1749-1762
55. Goshima, G., Wollman, R., Stuurman, N., Scholey, J.M. and Vale, R.D. (2005) Length control of the metaphase spindle. Curr. Biol. 15, 1979-1988
56. Cameron, L.A., Yang, G., Cimini, D., Canman, J.C., Kisurina-Evgenieva, O., Khodjakov, A., Danuser, G. and Salmon, E.D. (2006) Kinesin 5-independent poleward flux of kinetochore microtubules in PtK1 cells. J. Cell Biol. 173, 173-179
57. Miyamoto, D.T., Perlman, Z.E., Burbank, K.S., Groen, A.C. and Mitchison, T.J. (2004) The kinesin Eg5 drives poleward microtubule flux in Xenopus laevis egg extract spindles. J. Cell Biol. 167, 813-818
58. Braun, M., Drummond, D.R., Cross, R.A. and McAinsh, A.D. (2009) The kinesin-14 Klp2 organizes microtubules into parallel bundles by an ATP-dependent sorting mechanism. Nat. Cell Biol. 11, 724-730
59. 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