Depletion of Centromeric MCAK Leads to Chromosome Congression and Segregation Defects Due to Improper Kinetochore Attachments

Molecular Biology of the Cell

Volumn 15, Issue 3, 2004, Pages 1146-1159

  Kline Smith, Susan L ^a   Khodjakov, Alexey ^b   Hergert, Polla ^b   Walczak, Claire E ^a  

^a INDIANA UNIVERSITY   (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KINESIN; MITOTIC CENTROMERE ASSOCIATED KINESIN; PROTEIN KIN IS; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CENTROMERE; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; DEPOLYMERIZATION; METAPHASE; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ANIMALS; CELL CYCLE; CELLS, CULTURED; CHROMOSOME SEGREGATION; CHROMOSOMES; HUMANS; KINESIN; KINETOCHORES; MICROSCOPY, ELECTRON; MICROTUBULES; MITOTIC SPINDLE APPARATUS; XENOPUS;

ANIMALIA;

EID: 1542373746     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-08-0581     Document Type: Article

References (52)

1. Biggins, S., Severin, F.F., Bhalla, N., Sassoon, I., Hyman, A.A., and Murray, A.W. (1999). The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev. 13, 532-544.
2. Cassimeris, L., Rieder, C.L., Rupp, G., and Salmon, E.D. (1990). Stability of microtubule attachment to metaphase kinetochores in FtK1 cells. J. Cell Sci. 96, 9-15.
3. Cassimeris, L., Rieder, C.L., and Salmon, E.D. (1994). Microtubule assembly and kinetochore directional instability in vertebrate monopolar spindles: implications for the mechanism of chromosome congression. J. Cell Sci. 107, 285-297.
4. Cimini, D., Howell, B., Maddox, P., Khodjakov, A., Degrassi, F., and Salmon, E.D. (2001). Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J. Cell Biol. 153, 517-527.
5. Cimini, D., Fioravanti, D., Salmon, E.D., and Degrassi, F. (2002). Merotelic kinetochore orientation versus chromosome mono-orientation in the origin of lagging chromosomes in human primary cells. J. Cell Sci. 115, 507-515.
6. Cimini, D., Moree, B., Canman, J.C., and Salmon, E.D. (2003). Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms. J. Cell Sci. 116, 4213-25.
7. Cohen, M.W., Hoffstrom, B.G., and DeSimone, D.W. (2000). Active zones on motor nerve terminals contain alpha 3beta 1 integrin. J. Neurosci. 20, 4912-4921.
8. De Brabander, M., Geuens, G., De Mey, J., and Joniau, M. (1981). Nucleated assembly of mitotic microtubules in living PTK2 cells after release from nocodazole treatment. Cell Motil. 1, 469-483.
9. Desai, A., Verma, S., Mitchison, T.J., and Walczak, C.E. (1999). Kin I kinesins are microtubule-destabilizing enzymes. Cell. 96, 69-78.
10. Ditchfield, C., Johnson, V.L., Tighe, A., Ellston, R., Haworth, C., Johnson, T., Mortlock, A., Keen, N., and Taylor, S.S. (2003). Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161, 267-280.
11. Garcia, M.A., Koonrugsa, N., and Toda, T. (2002). Two kinesin-like Kin I family proteins in fission yeast regulate the establishment of metaphase and the onset of anaphase A. Curr. Biol. 12, 610-621.
12. Gorbsky, G.J., and Ricketts, W.A. (1993). Differential expression of a phosphoepitope at the kinetochores of moving chromosomes. J. Cell Biol. 122, 1311-1321.
13. Gordon, M.B., Howard, L., and Compton, D.A. (2001). Chromosome movement in mitosis requires microtubule anchorage at spindle poles. J. Cell Biol. 152, 425-434.
14. Goshima, G., and Vale, R.D. (2003). The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162, 1003-16.
15. Hauf, S., Cole, R.W., LaTerra, S., Zimmer, C., Schnapp, G., Walter, R., Heckel, A., Van Meel, J., Rieder, C.L., and Peters, J.M. (2003). The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J. Cell Biol. 161, 281-294.
16. Hoffman, D.B., Pearson, C.G., Yen, T.J., Howell, B.J., and Salmon, E.D. (2001). Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol. Biol. Cell. 12, 1995-2009.
17. Hunter, A.W., Caplow, M., Coy, D.L., Hancock, W.O., Diez, S., Wordeman, L., and Howard, J. (2003). The kinesin-related protein MCAK is a microtubule depolymerase that forms an ATP-hydrolyzing complex at microtubule ends. Mol. Cell. 11, 445-457.
18. Inoue, S., and Salmon, E.D. (1995). Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol. Biol. Cell. 6, 1619-1640.
19. Jablonski, S.A., Chan, G.K., Cooke, C.A., Earnshaw, W.C., and Yen, T.J. (1998). The hBUB1 and hBUBR1 kinases sequentially assemble onto kinetochores during prophase with hBUBR1 concentrating at the kinetochore plates in mitosis. Chromosoma 107, 386-396.
20. Kapoor, T.M., Mayer, T.U., Coughlin, M.L., and Mitchison, T.J. (2000). Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol. 150, 975-988.
21. Khodjakov, A., Cole, R.W., McEwen, B.F., Buttle, K.F., and Rieder, C.L. (1997). Chromosome fragments possessing only one kinetochore can congress to the spindle equator. J. Cell Biol. 136, 229-240.
22. King, J.M., and Nicklas, R.B. (2000). Tension on chromosomes increases the number of kinetochore microtubules but only within limits. J. Cell Sci. 113 Pt 21, 3815-3823.
23. Kline-Smith, S.L., and Walczak, C.E. (2002). The microtubule-destabilizing kinesin XKCM1 regulates microtubule dynamic instability in cells. Mol. Biol. Cell. 13, 2718-2731.
24. Maddox, P., Straight, A., Coughlin, P., Mitchison, T.J., and Salmon, E.D. (2003). Direct observation of microtubule dynamics at kinetochores in Xenopus extract spindles: implications for spindle mechanics. J. Cell Biol. 162, 377-382.
25. Maney, T., Hunter, A.W., Wagenbach, M., and Wordeman, L. (1998). Mitotic centromere-associated kinesin is important for anaphase chromosome segregation. J. Cell Biol. 142, 787-801.
26. Marko, M., and Leith, A. (1996). Sterecon-three-dimensional reconstructions from stereoscopic contouring. J. Struct. Biol. 116, 93-98.
27. McEwen, B.F., Heagle, A.B., Cassels, G.O., Buttle, K.F., and Rieder, C.L. (1997). Kinetochore fiber maturation in PtK1 cells and its implications for the mechanisms of chromosome congression and anaphase onset. J. Cell Biol. 137, 1567-1580.
28. McIntosh, J.R., Grishchuk, E.L., and West, R.R. (2002). Chromosome-microtubule interactions during mitosis. Annu. Rev. Cell Dev. Biol. 18, 193-219.
29. Musacchio, A., and Hardwick, K.G. (2002). The spindle checkpoint: structural insights into dynamic signalling. Nat. Rev. Mol. Cell. Biol. 3, 731-41.
30. Nicklas, R.B., Ward, S.C., and Gorbsky, G.J. (1995). Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J. Cell Biol. 130, 929-939.
31. Nicklas, R.B. (1997). How cells get the right chromosomes. Science. 275, 632-637.
32. Ohi, R., Coughlin, M.L., Lane, W.S., and Mitchison, T.J. (2003). An inner centromere protein that stimulates the microtubule depolymerizing activity of a KinI kinesin. Dev. Cell. 5, 309-321.
33. Ovechkina, Y., and Wordeman, L. (2003). Unconventional motoring: an overview of the kin C and kin I kinesins. Traffic. 4, 367-375.
34. Rieder, C.L. (1982). The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int. Rev. Cytol. 79, 1-58.
35. Rieder, C.L., and Cassels, G. (1999). Correlative light and electron microscopy of mitotic cells in monolayer cultures. Methods Cell Biol. 61, 297-315.
36. Rieder, C.L., and Salmon, E.D. (1998). The vertebrate cell kinetochore and its roles during mitosis. Trends Cell Biol. 8, 310-318.
37. Roos, U.P. (1973). Light and electron microscopy of rat kangaroo cells in mitosis. II. Kinetochore structure and function. Chromosoma 41, 195-220.
38. Salmon, E.D., Inoue, T., Desai, A., and Murray, A.W. (1994). High resolution multimode digital imaging system for mitosis studies in vivo and in vitro. Biol. Bull. 187, 231-232.
39. Shannon, K.B., Canman, J.C., and Salmon, E.D. (2002). Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol. Biol. Cell. 13, 3706-3719.
40. Shannon, K.B., and Salmon, E.D. (2002). Chromosome dynamics: new light on Aurora B kinase function. Curr. Biol. 12, R458-460.
41. Skibbens, R.V., Skeen, V.P., and Salmon, E.D. (1993). Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism. J. Cell Biol. 122, 859-875.
42. Skibbens, R.V., and Salmon, E.D. (1997). Micromanipulation of chromosomes in mitotic vertebrate tissue cells: tension controls the state of kinetochore movement. Exp. Cell Res. 235, 314-24.
43. Tanaka, T.U. (2002). Bi-orienting chromosomes on the mitotic spindle. Curr. Opin. Cell Biol. 14, 365-371.
44. Thrower, D.A., Jordan, M.A., and Wilson, L. (1996). Modulation of CENP-E organization at kinetochores by spindle microtubule attachment. Cell Motil. Cytoskeleton. 35, 121-133.
45. Walczak, C.E., Mitchison, T.J., and Desai, A. (1996). XKCM1, a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly. Cell. 84, 37-47.
46. Walczak, C.E., Gan, E.C., Desai, A., Mitchison, T.J., and Kline-Smith, S.L. (2002). The microtubule-destabilizing kinesin XKCM1 is required for chromosome positioning during spindle assembly. Curr. Biol. 12, 1885-1889.
47. Waters, J.C., Mitchison, T.J., Rieder, C.L., and Salmon, E.D. (1996a). The kinetochore microtubule minus-end disassembly associated with poleward flux produces a force that can do work. Mol. Biol. Cell. 7, 1547-1558.
48. Waters, J.C., Skibbens, R.V., and Salmon, E.D. (1996b). Oscillating mitotic newt lung cell kinetochores are, on average, under tension and rarely push. J. Cell Sci. 109, 2823-2831.
49. West, R.R., Malmstrom, T., and McIntosh, J.R. (2002). Kinesins klp5(+) and klp6(+) are required for normal chromosome movement in mitosis. J. Cell Sci. 115, 931-940.
50. Wise, D., Cassimeris, L., Rieder, C.L., Wadsworth, P., and Salmon, E.D. (1991). Chromosome fiber dynamics and congression oscillations in metaphase PtK2 cells at 23 degrees C. Cell Motil. Cytoskeleton. 18, 131-142.
51. Wordeman, L., and Mitchison, T.J. (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.
52. Zhou, J., Yao, J., and Joshi, H.C. (2002). Attachment and tension in the spindle assembly checkpoint. J. Cell Sci. 115, 3547-3555.