Depolymerizing kinesins Kip3 and MCAK shape cellular microtubule architecture by differential control of catastrophe

Cell

Volumn 147, Issue 5, 2011, Pages 1092-1103

  Gardner, Melissa K ^a,b   Zanic, Marija ^b   Gell, Christopher ^b   Bormuth, Volker ^b   Howard, Jonathon ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; KIP3 PROTEIN; MCAK PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL AGING; CELL DISRUPTION; CELL GROWTH; CONTROLLED STUDY; CYTOARCHITECTURE; DEPOLYMERIZATION; FREQUENCY ANALYSIS; MICROTUBULE; MOLECULAR DYNAMICS; PRIORITY JOURNAL;

EID: 81855189480     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.10.037     Document Type: Article

References (64)

1. S.F. Bakhoum, G. Genovese, and D.A. Compton Deviant kinetochore microtubule dynamics underlie chromosomal instability Curr. Biol. 19 2009 1937 1942
2. M. Caplow, and J. Shanks Evidence that a single monolayer tubulin-GTP cap is both necessary and sufficient to stabilize microtubules Mol. Biol. Cell 7 1996 663 675
3. M.F. Carlier, T.L. Hill, and Y. Chen Interference of GTP hydrolysis in the mechanism of microtubule assembly: an experimental study Proc. Natl. Acad. Sci. USA 81 1984 771 775
4. L.U. Cassimeris, P. Wadsworth, and E.D. Salmon Dynamics of microtubule depolymerization in monocytes J. Cell Biol. 102 1986 2023 2032
5. D. Chrétien, F. Metoz, F. Verde, E. Karsenti, and R.H. Wade Lattice defects in microtubules: protofilament numbers vary within individual microtubules J. Cell Biol. 117 1992 1031 1040
6. D. Chrétien, S.D. Fuller, and E. Karsenti Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates J. Cell Biol. 129 1995 1311 1328
7. A. Desai, S. Verma, T.J. Mitchison, and C.E. Walczak Kin I kinesins are microtubule-destabilizing enzymes Cell 96 1999 69 78
8. A. Dimitrov, M. Quesnoit, S. Moutel, I. Cantaloube, C. Poüs, and F. Perez Detection of GTP-tubulin conformation in vivo reveals a role for GTP remnants in microtubule rescues Science 322 2008 1353 1356
9. M. Dogterom, J.W. Kerssemakers, G. Romet-Lemonne, and M.E. Janson Force generation by dynamic microtubules Curr. Opin. Cell Biol. 17 2005 67 74
10. D.N. Drechsel, and M.W. Kirschner The minimum GTP cap required to stabilize microtubules Curr. Biol. 4 1994 1053 1061
11. Y. Du, C.A. English, and R. Ohi The kinesin-8 Kif18A dampens microtubule plus-end dynamics Curr. Biol. 20 2010 374 380
12. D. Foethke, T. Makushok, D. Brunner, and F. Nédélec Force-and length-dependent catastrophe activities explain interphase microtubule organization in fission yeast Mol. Syst. Biol. 5 2009 241
13. D.K. Fygenson, E. Braun, and A. Libchaber Phase diagram of microtubules Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 50 1994 1579 1588
14. M.K. Gardner, D.C. Bouck, L.V. Paliulis, J.B. Meehl, E.T. O'Toole, J. Haase, A. Soubry, A.P. Joglekar, M. Winey, and E.D. Salmon Chromosome congression by Kinesin-5 motor-mediated disassembly of longer kinetochore microtubules Cell 135 2008 894 906
15. C. Gell, V. Bormuth, G.J. Brouhard, D.N. Cohen, S. Diez, C.T. Friel, J. Helenius, B. Nitzsche, H. Petzold, and J. Ribbe Microtubule dynamics reconstituted in vitro and imaged by single-molecule fluorescence microscopy Methods Cell Biol. 95 2010 221 245
16. G. Goshima, R. Wollman, N. Stuurman, J.M. Scholey, and R.D. Vale Length control of the metaphase spindle Curr. Biol. 15 2005 1979 1988
17. M.L. Gupta Jr., P. Carvalho, D.M. Roof, and D. Pellman Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle Nat. Cell Biol. 8 2006 913 923
18. J. Helenius, G. Brouhard, Y. Kalaidzidis, S. Diez, and J. Howard The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends Nature 441 2006 115 119
19. J. Howard Mechanics of Motor Proteins and the Cytoskeleton 2001 Sinauer Associates, Inc. Sunderland, MA
20. A.W. Hunter, M. Caplow, D.L. Coy, W.O. Hancock, S. Diez, L. Wordeman, and J. Howard The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends Mol. Cell 11 2003 445 457
21. A.A. Hyman, S. Salser, D.N. Drechsel, N. Unwin, and T.J. Mitchison Role of GTP hydrolysis in microtubule dynamics: information from a slowly hydrolyzable analogue, GMPCPP Mol. Biol. Cell 3 1992 1155 1167
22. M.E. Janson, M.E. de Dood, and M. Dogterom Dynamic instability of microtubules is regulated by force J. Cell Biol. 161 2003 1029 1034
23. K. Jaqaman, E.M. King, A.C. Amaro, J.R. Winter, J.F. Dorn, H.L. Elliott, N. McHedlishvili, S.E. McClelland, I.M. Porter, and M. Posch Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases J. Cell Biol. 188 2010 665 679
24. K. Kinoshita, B. Habermann, and A.A. Hyman XMAP215: a key component of the dynamic microtubule cytoskeleton Trends Cell Biol. 12 2002 267 273
25. S.L. Kline-Smith, and C.E. Walczak The microtubule-destabilizing kinesin XKCM1 regulates microtubule dynamic instability in cells Mol. Biol. Cell 13 2002 2718 2731
26. S.L. Kline-Smith, and C.E. Walczak Mitotic spindle assembly and chromosome segregation: refocusing on microtubule dynamics Mol. Cell 15 2004 317 327
27. T. Maney, A.W. Hunter, M. Wagenbach, and L. Wordeman Mitotic centromere-associated kinesin is important for anaphase chromosome segregation J. Cell Biol. 142 1998 787 801
28. S.P. Maurer, P. Bieling, J. Cope, A. Hoenger, and T. Surrey GTPgammaS microtubules mimic the growing microtubule end structure recognized by end-binding proteins (EBs) Proc. Natl. Acad. Sci. USA 108 2011 3988 3993
29. M.I. Mayr, S. Hümmer, J. Bormann, T. Grüner, S. Adio, G. Woehlke, and T.U. Mayer The human kinesin Kif18A is a motile microtubule depolymerase essential for chromosome congression Curr. Biol. 17 2007 488 498
30. B. Mickey, and J. Howard Rigidity of microtubules is increased by stabilizing agents J. Cell Biol. 130 1995 909 917
31. T. Mitchison, and M. Kirschner Dynamic instability of microtubule growth Nature 312 1984 237 242
32. S. Montenegro Gouveia, K. Leslie, L.C. Kapitein, R.M. Buey, I. Grigoriev, M. Wagenbach, I. Smal, E. Meijering, C.C. Hoogenraad, and L. Wordeman In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends Curr. Biol. 20 2010 1717 1722
33. C.A. Moores, and R.A. Milligan Lucky 13-microtubule depolymerisation by kinesin-13 motors J. Cell Sci. 119 2006 3905 3913
34. A.M. Mulder, A. Glavis-Bloom, C.A. Moores, M. Wagenbach, B. Carragher, L. Wordeman, and R.A. Milligan A new model for binding of kinesin 13 to curved microtubule protofilaments J. Cell Biol. 185 2009 51 57
35. C.N. Newton, M. Wagenbach, Y. Ovechkina, L. Wordeman, and L. Wilson MCAK, a Kin I kinesin, increases the catastrophe frequency of steady-state HeLa cell microtubules in an ATP-dependent manner in vitro FEBS Lett. 572 2004 80 84
36. E. Nogales, and H.W. Wang Structural mechanisms underlying nucleotide-dependent self-assembly of tubulin and its relatives Curr. Opin. Struct. Biol. 16 2006 221 229
37. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the alpha beta tubulin dimer by electron crystallography Nature 391 1998 199 203
38. D.J. Odde, L. Cassimeris, and H.M. Buettner Kinetics of microtubule catastrophe assessed by probabilistic analysis Biophys. J. 69 1995 796 802
39. D.J. Odde, H.M. Buettner, and L. Cassimeris Spectral analysis of microtubule assembly dynamics AIChE J. 42 1996 1434 1442
40. R. Phillips, J. Kondev, and J. Theriot Physical Biology of the Cell 2008 Taylor & Francis Group London
41. K.E. Rankin, and L. Wordeman Long astral microtubules uncouple mitotic spindles from the cytokinetic furrow J. Cell Biol. 190 2010 35 43
42. J.A. Rice Mathematical Statistics and Data Analysis 1995 Duxbury Press Belmont, CA
43. R.S. Rizk, K.P. Bohannon, L.A. Wetzel, J. Powers, S.L. Shaw, and C.E. Walczak MCAK and paclitaxel have differential effects on spindle microtubule organization and dynamics Mol. Biol. Cell 20 2009 1639 1651
44. G.C. Rogers, S.L. Rogers, T.A. Schwimmer, S.C. Ems-McClung, C.E. Walczak, R.D. Vale, J.M. Scholey, and D.J. Sharp Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase Nature 427 2004 364 370
45. T. Stepanova, I. Smal, J. van Haren, U. Akinci, Z. Liu, M. Miedema, R. Limpens, M. van Ham, M. van der Reijden, and R. Poot History-dependent catastrophes regulate axonal microtubule behavior Curr. Biol. 20 2010 1023 1028
46. J. Stumpff, G. von Dassow, M. Wagenbach, C. Asbury, and L. Wordeman The kinesin-8 motor Kif18A suppresses kinetochore movements to control mitotic chromosome alignment Dev. Cell 14 2008 252 262
47. C. Tischer, D. Brunner, and M. Dogterom Force-and kinesin-8-dependent effects in the spatial regulation of fission yeast microtubule dynamics Mol. Syst. Biol. 5 2009 250
48. R. Tournebize, A. Popov, K. Kinoshita, A.J. Ashford, S. Rybina, A. Pozniakovsky, T.U. Mayer, C.E. Walczak, E. Karsenti, and A.A. Hyman Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts Nat. Cell Biol. 2 2000 13 19
49. V. Varga, J. Helenius, K. Tanaka, A.A. Hyman, T.U. Tanaka, and J. Howard Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner Nat. Cell Biol. 8 2006 957 962
50. V. Varga, C. Leduc, V. Bormuth, S. Diez, and J. Howard Kinesin-8 motors act cooperatively to mediate length-dependent microtubule depolymerization Cell 138 2009 1174 1183
51. W.A. Voter, E.T. O'Brien, and H.P. Erickson Dilution-induced disassembly of microtubules: relation to dynamic instability and the GTP cap Cell Motil. Cytoskeleton 18 1991 55 62
52. C.E. Walczak, T.J. Mitchison, and A. Desai XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly Cell 84 1996 37 47
53. R.A. Walker, E.T. O'Brien, N.K. Pryer, M.F. Soboeiro, W.A. Voter, H.P. Erickson, and E.D. Salmon Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies J. Cell Biol. 107 1988 1437 1448
54. R.A. Walker, S. Inoué, and E.D. Salmon Asymmetric behavior of severed microtubule ends after ultraviolet-microbeam irradiation of individual microtubules in vitro J. Cell Biol. 108 1989 931 937
55. R.A. Walker, N.K. Pryer, and E.D. Salmon Dilution of individual microtubules observed in real time in vitro: evidence that cap size is small and independent of elongation rate J. Cell Biol. 114 1991 73 81
56. M.M. Wargacki, J.C. Tay, E.G. Muller, C.L. Asbury, and T.N. Davis Kip3, the yeast kinesin-8, is required for clustering of kinetochores at metaphase Cell Cycle 9 2010 2581 2588
57. R. Wollman, E.N. Cytrynbaum, J.T. Jones, T. Meyer, J.M. Scholey, and A. Mogilner Efficient chromosome capture requires a bias in the 'search-and-capture' process during mitotic-spindle assembly Curr. Biol. 15 2005 828 832
58. L. Wordeman, M. Wagenbach, and G. von Dassow MCAK facilitates chromosome movement by promoting kinetochore microtubule turnover J. Cell Biol. 179 2007 869 879
59. M. Zanic, J.H. Stear, A.A. Hyman, and J. Howard EB1 recognizes the nucleotide state of tubulin in the microtubule lattice PLoS ONE 4 2009 e7585
60. Gell, C., Bormuth, V., Brouhard, G.J., Cohen, D.N., Diez, S., Friel, C.T., Helenius, J., Nitzsche, B., Petzold, H., Ribbe, J., et al. (2010). Microtubule dynamics reconstituted in vitro and imaged by single-molecule fluorescence microscopy. Methods Cell Biol. 95, 221-245.
61. Odde, D.J., and Buettner, H.M. (1998). Autocorrelation function and power spectrum of two-state random processes used in neurite guidance. Biophys. J. 75, 1189-1196.
62. Odde, D.J., Cassimeris, L., and Buettner, H.M. (1995). Kinetics of microtubule catastrophe assessed by probabilistic analysis. Biophys. J. 69, 796-802.
63. Varga, V., Helenius, J., Tanaka, K., Hyman, A.A., Tanaka, T.U., and Howard, J. (2006). Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nat. Cell Biol. 8, 957-962.
64. Varga, V., Leduc, C., Bormuth, V., Diez, S., and Howard, J. (2009). Kinesin-8 motors act cooperatively to mediate length-dependent microtubule depolymerization. Cell 138, 1174-1183.