MCAK activity at microtubule tips regulates spindle microtubule length to promote robust kinetochore attachment

Journal of Cell Biology

Volumn 197, Issue 2, 2012, Pages 231-237

  Domnitz, Sarah B ^a   Wagenbach, Michael ^a   Decarreau, Justin ^a   Wordeman, Linda ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; KINESIN; PROTEIN MITOTIC CENTROMERE ASSOCIATED KINESIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; KIF11 PROTEIN, HUMAN; KIF2C PROTEIN, HUMAN; MAD1L1 PROTEIN, HUMAN; MONASTROL; NUCLEAR PROTEIN; PHOSPHATASE; PYRIMIDINE DERIVATIVE; SKIP ENZYME, HUMAN; SMALL INTERFERING RNA; THIOKETONE;

ARTICLE; CELL SEPARATION; CENTROMERE; CENTROSOME; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; HUMAN; HUMAN CELL; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; PRIORITY JOURNAL; CELL CYCLE; DRUG ANTAGONISM; GENETICS; HELA CELL; METABOLISM; MITOSIS; PHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

CELL CYCLE; CELL CYCLE PROTEINS; CENTROMERE; CENTROSOME; HELA CELLS; HUMANS; KINESIN; KINETOCHORES; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; NUCLEAR PROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PYRIMIDINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THIONES;

EID: 84861949049     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201108147     Document Type: Article

References (31)

1. Bakhoum, S.F., S.L. Thompson, A.L. Manning, and D.A. Compton. 2009. Genome stability is ensured by temporal control of kinetochore-microtubule dynamics. Nat. Cell Biol. 11:27-35. http://dx.doi.org/10.1038/ncb1809.
2. Buster, D.W., D. Zhang, and D.J. Sharp. 2007. Poleward tubulin flux in spindles: Regulation and function in mitotic cells. Mol. Biol. Cell. 18:3094-3104. http://dx.doi.org/10.1091/mbc.E06-11-0994.
3. Cai, S., C.B. O'Connell, A. Khodjakov, and C.E. Walczak. 2009. Chromosome congression in the absence of kinetochore fibres. Nat. Cell Biol. 11:832-838. http://dx.doi.org/10.1038/ncb1890.
4. Chen, R.H., A. Shevchenko, M. Mann, and A.W. Murray. 1998. Spindle checkpoint protein Xmad1 recruits Xmad2 to unattached kinetochores. J. Cell Biol. 143:283-295. http://dx.doi.org/10.1083/jcb.143.2.283.
5. Cross, M.K., and M.A. Powers. 2011. Nup98 regulates bipolar spindle assembly through association with microtubules and opposition of MCAK. Mol. Biol. Cell. 22:661-672. http://dx.doi.org/10.1091/mbc.E10-06-0478.
6. Ganem, N.J., K. Upton, and D.A. Compton. 2005. Efficient mitosis in human cells lacking poleward microtubule flux. Curr. Biol. 15:1827-1832. http://dx.doi.org/10.1016/j.cub.2005.08.065.
7. Honnappa, S., S.M. Gouveia, A. Weisbrich, F.F. Damberger, N.S. Bhavesh, H. Jawhari, I. Grigoriev, F.J. van Rijssel, R.M. Buey, A. Lawera, et al. 2009. An EB1-binding motif acts as a microtubule tip localization signal. Cell. 138:366-376. http://dx.doi.org/10.1016/j.cell.2009.04.065.
8. Hunter, A.W., M. Caplow, D.L. Coy, W.O. Hancock, S. Diez, L. Wordeman, and J. Howard. 2003. The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends. Mol. Cell. 11:445-457. http://dx.doi.org/10.1016/S1097-2765(03)00049-2.
9. Kapoor, T.M., T.U. Mayer, M.L. Coughlin, and T.J. Mitchison. 2000. Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol. 150:975-988. http://dx.doi.org/10.1083/jcb.150.5.975.
10. Kapoor, T.M., M.A. Lampson, P. Hergert, L. Cameron, D. Cimini, E.D. Salmon, B.F. McEwen, and A. Khodjakov. 2006. Chromosomes can congress to the metaphase plate before biorientation. Science. 311:388-391. http://dx.doi.org/10.1126/science.1122142.
11. Kim, Y., J.E. Heuser, C.M. Waterman, and D.W. Cleveland. 2008. CENP-E combines a slow, processive motor and a flexible coiled coil to produce an essential motile kinetochore tether. J. Cell Biol. 181:411-419. http://dx.doi.org/10.1083/jcb.200802189.
12. Kollu, S., S.F. Bakhoum, and D.A. Compton. 2009. Interplay of microtubule dynamics and sliding during bipolar spindle formation in mammalian cells. Curr. Biol. 19:2108-2113. http://dx.doi.org/10.1016/j.cub.2009.10.056.
13. Loughlin, R., J.D. Wilbur, F.J. McNally, F.J. Nédélec, and R. Heald. 2011. Katanin contributes to interspecies spindle length scaling in Xenopus. Cell. 147:1397-1407. http://dx.doi.org/10.1016/j.cell.2011.11.014.
14. Magidson, V., C.B. O'Connell, J. Lončarek, R. Paul, A. Mogilner, and A. Khodjakov. 2011. The spatial arrangement of chromosomes during prometaphase facilitates spindle assembly. Cell. 146:555-567. http://dx.doi.org/10.1016/j.cell.2011.07.012.
15. Maney, T., M. Wagenbach, and L. Wordeman. 2001. Molecular dissection of the microtubule depolymerizing activity of mitotic centromere-associated kinesin. J. Biol. Chem. 276:34753-34758. http://dx.doi.org/10.1074/jbc.M106626200.
16. Manning, A.L., N.J. Ganem, S.F. Bakhoum, M. Wagenbach, L. Wordeman, and D.A. Compton. 2007. The kinesin-13 proteins Kif2a, Kif2b, and Kif2c/ MCAK have distinct roles during mitosis in human cells. Mol. Biol. Cell. 18:2970-2979. http://dx.doi.org/10.1091/mbc.E07-02-0110.
17. McNally, K., A. Audhya, K. Oegema, and F.J. McNally. 2006. Katanin controls mitotic and meiotic spindle length. J. Cell Biol. 175:881-891. http://dx.doi.org/10.1083/jcb.200608117.
18. Mitchison, T.J., P. Maddox, J. Gaetz, A. Groen, M. Shirasu, A. Desai, E.D. Salmon, and T.M. Kapoor. 2005. Roles of polymerization dynamics, opposed motors, and a tensile element in governing the length of Xenopus extract meiotic spindles. Mol. Biol. Cell. 16:3064-3076. http://dx.doi.org/10.1091/mbc.E05-02-0174.
19. Montenegro Gouveia, S., K. Leslie, L.C. Kapitein, R.M. Buey, I. Grigoriev, M. Wagenbach, I. Smal, E. Meijering, C.C. Hoogenraad, L. Wordeman, et al. 2010. In vitro reconstitution of the functional interplay between MCAK and EB3 at microtubule plus ends. Curr. Biol. 20:1717-1722. http://dx.doi.org/10.1016/j.cub.2010.08.020.
20. Moore, A.T., K.E. Rankin, G. von Dassow, L. Peris, M. Wagenbach, Y. Ovechkina, A. Andrieux, D. Job, and L. Wordeman. 2005. MCAK associates with the tips of polymerizing microtubules. J. Cell Biol. 169:391-397. http://dx.doi.org/10.1083/jcb.200411089.
21. Ohi, R., K. Burbank, Q. Liu, and T.J. Mitchison. 2007. Nonredundant functions of Kinesin-13s during meiotic spindle assembly. Curr. Biol. 17:953-959. http://dx.doi.org/10.1016/j.cub.2007.04.057.
22. Ovechkina, Y., M. Wagenbach, and L. Wordeman. 2002. K-loop insertion restores microtubule depolymerizing activity of a " neckless" MCAK mutant. J. Cell Biol. 159:557-562. http://dx.doi.org/10.1083/jcb.200205089.
23. Rankin, K.E., and L. Wordeman. 2010. Long astral microtubules uncouple mitotic spindles from the cytokinetic furrow. J. Cell Biol. 190:35-43. http://dx.doi.org/10.1083/jcb.201004017.
24. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Vol. 3. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 1659 pp..
25. Tanenbaum, M.E., L. Macůrek, A. Janssen, E.F. Geers, M. Alvarez-Fernández, and R.H. Medema. 2009. Kif15 cooperates with eg5 to promote bipolar spindle assembly. Curr. Biol. 19:1703-1711. http://dx.doi.org/10.1016/j.cub.2009.08.027.
26. Toso, A., J.R. Winter, A.J. Garrod, A.C. Amaro, P. Meraldi, and A.D. McAinsh. 2009. Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly. J. Cell Biol. 184:365-372. http://dx.doi.org/10.1083/jcb.200809055.
27. Tulu, U.S., N.M. Rusan, and P. Wadsworth. 2003. Peripheral, non-centrosomeassociated microtubules contribute to spindle formation in centrosomecontaining cells. Curr. Biol. 13:1894-1899. http://dx.doi.org/10.1016/j.cub.2003.10.002.
28. Walczak, C.E., E.C. Gan, A. Desai, T.J. Mitchison, and S.L. Kline-Smith. 2002. The microtubule-destabilizing kinesin XKCM1 is required for chromosome positioning during spindle assembly. Curr. Biol. 12:1885-1889. http://dx.doi.org/10.1016/S0960-9822(02)01227-7.
29. Wordeman, L., and T.J. Mitchison. 1995. Identification and partial characterization of mitotic centromere-associated kinesin, a kinesin-related protein that associates with centromeres during mitosis. J. Cell Biol. 128:95-104. http://dx.doi.org/10.1083/jcb.128.1.95.
30. Wordeman, L., M. Wagenbach, and G. von Dassow. 2007. MCAK facilitates chromosome movement by promoting kinetochore microtubule turnover. J. Cell Biol. 179:869-879. http://dx.doi.org/10.1083/jcb.200707120.
31. Yang, Z., U.S. Tulu, P. Wadsworth, and C.L. Rieder. 2007. Kinetochore dynein is required for chromosome motion and congression independent of the spindle checkpoint. Curr. Biol. 17:973-980. http://dx.doi.org/10.1016/j.cub.2007.04.056.