Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis

Journal of Cell Biology

Volumn 198, Issue 5, 2012, Pages 847-863

  Wandke, Cornelia ^a,b   Barisic, Marin ^a,c   Sigl, Reinhard ^a   Rauch, Veronika ^a   Wolf, Frank ^a   Amaro, Ana C ^b   Tan, Chia H ^b   Pereira, Antonio J ^c   Kutay, Ulrike ^b   Maiato, Helder ^c,d   Meraldi, Patrick ^b   Geley, Stephan ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF PORTO   (Portugal)

^d University of Porto   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOKINESIN; MOLECULAR MOTOR; NOCODAZOLE; PROTEIN HKID; PROTEIN KIF4A; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CENTROMERE; CHROMOSOME; CHROMOSOME ARM; CHROMOSOME CONGRESSION; CONTROLLED STUDY; HUMAN; HUMAN CELL; METAPHASE CHROMOSOME; MICROTUBULE; MITOSIS; MITOSIS INHIBITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA INTERFERENCE;

ANAPHASE; ANIMALS; CALCIUM-BINDING PROTEINS; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL LINE; CELL LINE, TUMOR; CHROMOSOME SEGREGATION; DNA-BINDING PROTEINS; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HUMANS; KINESIN; KINETOCHORES; METAPHASE; MICROTUBULES; MITOSIS; MITOTIC SPINDLE APPARATUS; NUCLEAR PROTEINS; REPRESSOR PROTEINS; XENOPUS; XENOPUS PROTEINS;

EID: 84866362654     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201110060     Document Type: Article

References (69)

1. Amaro, A.C., C.P. Samora, R. Holtackers, E. Wang, I.J. Kingston, M. Alonso, M. Lampson, A.D. McAinsh, and P. Meraldi. 2010. Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nat. Cell Biol. 12: 319-329. http://dx.doi.org/10.1038/ncb2033
2. Antonio, C., I. Ferby, H. Wilhelm, M. Jones, E. Karsenti, A.R. Nebreda, and I. Vernos. 2000. Xkid, a chromokinesin required for chromosome alignment on the metaphase plate. Cell. 102: 425-435. http://dx.doi.org/10.1016/S0092-8674(00)00048-9
3. Barisic, M., B. Sohm, P. Mikolcevic, C. Wandke, V. Rauch, T. Ringer, M. Hess, G. Bonn, and S. Geley. 2010. Spindly/CCDC99 is required for efficient chromosome congression and mitotic checkpoint regulation. Mol. Biol. Cell. 21: 1968-1981. http://dx.doi.org/10.1091/mbc.E09-04-0356
4. Bieling, P., I. Kronja, and T. Surrey. 2010a. Microtubule motility on reconstituted meiotic chromatin. Curr. Biol. 20:763-769. http://dx.doi.org/10.1016/j.cub.2010.02.067
5. Bieling, P., I.A. Telley, and T. Surrey. 2010b. A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell. 142:420-432. http://dx.doi.org/10.1016/j.cell.2010.06.033
6. Bringmann, H., G. Skiniotis, A. Spilker, S. Kandels-Lewis, I. Vernos, and T. Surrey. 2004. A kinesin-like motor inhibits microtubule dynamic instability. Science. 303: 1519-1522. http://dx.doi.org/10.1126/science.1094838
7. Brouhard, G.J., and A.J. Hunt. 2005. Microtubule movements on the arms of mitotic chromosomes: polar ejection forces quantified in vitro. Proc. Natl. Acad. Sci. USA. 102: 13903-13908. http://dx.doi.org/10.1073/pnas.0506017102
8. Buster, D.W., and D.J. Sharp. Chromokinesins Affect the Flux Rate of Mitotic Spindle Microtubules in Drosophila S2 Cells. 45th Meeting of the Americal Society of Cell Biology, San Francisco. 2005. Abstract.
9. Cassimeris, L., C.L. Rieder, and E.D. Salmon. 1994. Microtubule assembly and kinetochore directional instability in vertebrate monopolar spindles: implications for the mechanism of chromosome congression. J. Cell Sci. 107:285-297.
10. Castoldi, M., and I. Vernos. 2006. Chromokinesin Xklp1 contributes to the regulation of microtubule density and organization during spindle assembly. Mol. Biol. Cell. 17: 1451-1460. http://dx.doi.org/10.1091/mbc.E05-04-0271
11. Cochran, J.C., C.V. Sindelar, N.K. Mulko, K.A. Collins, S.E. Kong, R.S. Hawley, and F.J. Kull. 2009. ATPase cycle of the nonmotile kinesin NOD allows microtubule end tracking and drives chromosome movement. Cell. 136: 110-122. http://dx.doi.org/10.1016/j.cell.2008.11.048
12. Daum, J.R., T.A. Potapova, S. Sivakumar, J.J. Daniel, J.N. Flynn, S. Rankin, and G.J. Gorbsky. 2011. Cohesion fatigue induces chromatid separation in cells delayed at metaphase. Curr. Biol. 21: 1018-1024. http://dx.doi.org/10.1016/j.cub.2011.05.032
13. Du, Y., C.A. English, and R. Ohi. 2010. The kinesin-8 Kif18A dampens microtubule plus-end dynamics. Curr. Biol. 20: 374-380. http://dx.doi.org/10.1016/j.cub.2009.12.049
14. Funabiki, H., and A.W. Murray. 2000. The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell. 102: 411-424. http://dx.doi.org/10.1016/S0092-8674(00)00047-7
15. 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
16. Gao, J., N. Sai, C. Wang, X. Sheng, Q. Shao, C. Zhou, Y. Shi, S. Sun, X. Qu, and C. Zhu. 2011. Overexpression of chromokinesin KIF4 inhibits proliferation of human gastric carcinoma cells both in vitro and in vivo. Tumour Biol. 32: 53-61. http://dx.doi.org/10.1007/s13277-010-0090-0
17. Garcia, M.A., N. Koonrugsa, and T. Toda. 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. http://dx.doi.org/10.1016/S0960-9822(02)00761-3
18. Gordon, D.J., B. Resio, and D. Pellman. 2012. Causes and consequences of aneuploidy in cancer. Nat. Rev. Genet. 13:189-203.
19. Goshima, G., and R.D. Vale. 2003. The roles of microtubule-based motor proteins in mitosis: comprehensive RNAi analysis in the Drosophila S2 cell line. J. Cell Biol. 162: 1003-1016. http://dx.doi.org/10.1083/jcb.200303022
20. Gupta, M.L. Jr., P. Carvalho, D.M. Roof, and D. Pellman. 2006. Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle. Nat. Cell Biol. 8: 913-923. http://dx.doi.org/10.1038/ncb1457
21. Hu, C.K., M. Coughlin, C.M. Field, and T.J. Mitchison. 2011. KIF4 regulates midzone length during cytokinesis. Curr. Biol. 21: 815-824. http://dx.doi.org/10.1016/j.cub.2011.04.019
22. Hu, C.K., M. Coughlin, and T.J. Mitchison. 2012. Midbody assembly and its regulation during cytokinesis. Mol. Biol. Cell. 23: 1024-1034. http://dx.doi.org/10.1091/mbc.E11-08-0721
23. Jaqaman, K., E.M. King, A.C. Amaro, J.R. Winter, J.F. Dorn, H.L. Elliott, N. McHedlishvili, S.E. McClelland, I.M. Porter, M. Posch, et al. 2010. Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases. J. Cell Biol. 188: 665-679. http://dx.doi.org/10.1083/jcb.200909005
24. Jordan, M.A., D. Thrower, and L. Wilson. 1992. Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles. Implications for the role of microtubule dynamics in mitosis. J. Cell Sci. 102:401-416.
25. Kapoor, T.M., and D.A. Compton. 2002. Searching for the middle ground: mechanisms of chromosome alignment during mitosis. J. Cell Biol. 157: 551-556. http://dx.doi.org/10.1083/jcb.200202073
26. 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
27. Ke, K., J. Cheng, and A.J. Hunt. 2009. The distribution of polar ejection forces determines the amplitude of chromosome directional instability. Curr. Biol. 19: 807-815. http://dx.doi.org/10.1016/j.cub.2009.04.036
28. Kim, Y., A.J. Holland, W. Lan, and D.W. Cleveland. 2010. Aurora kinases and protein phosphatase 1 mediate chromosome congression through regulation of CENP-E. Cell. 142: 444-455. http://dx.doi.org/10.1016/j.cell.2010.06.039
29. Kurasawa, Y., W.C. Earnshaw, Y. Mochizuki, N. Dohmae, and K. Todokoro. 2004. Essential roles of KIF4 and its binding partner PRC1 in organized central spindle midzone formation. EMBO J. 23: 3237-3248. http://dx.doi.org/10.1038/sj.emboj.7600347
30. Kwon, M., S. Morales-Mulia, I. Brust-Mascher, G.C. Rogers, D.J. Sharp, and J.M. Scholey. 2004. The chromokinesin, KLP3A, dives mitotic spindle pole separation during prometaphase and anaphase and facilitates chromatid motility. Mol. Biol. Cell. 15: 219-233. http://dx.doi.org/10.1091/mbc.E03-07-0489
31. Levesque, A.A., and D.A. Compton. 2001. The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles. J. Cell Biol. 154: 1135-1146. http://dx.doi.org/10.1083/jcb.200106093
32. Levesque, A.A., L. Howard, M.B. Gordon, and D.A. Compton. 2003. A functional relationship between NuMA and kid is involved in both spindle organization and chromosome alignment in vertebrate cells. Mol. Biol. Cell. 14: 3541-3552. http://dx.doi.org/10.1091/mbc.E03-02-0082
33. Logarinho, E., S. Maffini, M. Barisic, A. Marques, A. Toso, P. Meraldi, and H. Maiato. 2012. CLASPs prevent irreversible multipolarity by ensuring spindle-pole resistance to traction forces during chromosome alignment. Nat. Cell Biol. 14: 295-303. http://dx.doi.org/10.1038/ncb2423
34. 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
35. Marshall, W.F., J.F. Marko, D.A. Agard, and J.W. Sedat. 2001. Chromosome elasticity and mitotic polar ejection force measured in living Drosophila embryos by four-dimensional microscopy-based motion analysis. Curr. Biol. 11: 569-578. http://dx.doi.org/10.1016/S0960-9822(01)00180-4
36. Martin-Lluesma, S., V.M. Stucke, and E.A. Nigg. 2002. Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science. 297: 2267-2270. http://dx.doi.org/10.1126/science.1075596
37. Matos, I., A.J. Pereira, M. Lince-Faria, L.A. Cameron, E.D. Salmon, and H. Maiato. 2009. Synchronizing chromosome segregation by flux-dependent force equalization at kinetochores. J. Cell Biol. 186: 11-26. http://dx.doi.org/10.1083/jcb.200904153
38. Mayr, M.I., S. Hümmer, J. Bormann, T. Grüner, S. Adio, G. Woehlke, and T.U. Mayer. 2007. The human kinesin Kif18A is a motile microtubule depolymerase essential for chromosome congression. Curr. Biol. 17: 488-498. http://dx.doi.org/10.1016/j.cub.2007.02.036
39. Mazumdar, M., and T. Misteli. 2005. Chromokinesins: multitalented players in mitosis. Trends Cell Biol. 15: 349-355. http://dx.doi.org/10.1016/j.tcb.2005.05.006
40. Mazumdar, M., S. Sundareshan, and T. Misteli. 2004. Human chromokinesin KIF4A functions in chromosome condensation and segregation. J. Cell Biol. 166: 613-620. http://dx.doi.org/10.1083/jcb.200401142
41. Mazumdar, M., J.H. Lee, K. Sengupta, T. Ried, S. Rane, and T. Misteli. 2006. Tumor formation via loss of a molecular motor protein. Curr. Biol. 16: 1559-1564. http://dx.doi.org/10.1016/j.cub.2006.06.029
42. McKinney, S.A., C.S. Murphy, K.L. Hazelwood, M.W. Davidson, and L.L. Looger. 2009. A bright and photostable photoconvertible fluorescent protein. Nat. Methods. 6: 131-133. http://dx.doi.org/10.1038/nmeth.1296
43. Midorikawa, R., Y. Takei, and N. Hirokawa. 2006. KIF4 motor regulates activity-dependent neuronal survival by suppressing PARP-1 enzymatic activity. Cell. 125: 371-383. http://dx.doi.org/10.1016/j.cell.2006.02.039
44. Nasmyth, K. 2002. Segregating sister genomes: the molecular biology of chromosome separation. Science. 297: 559-565. http://dx.doi.org/10.1126/science.1074757
45. Ohsugi, M., K. Adachi, R. Horai, S. Kakuta, K. Sudo, H. Kotaki, N. Tokai-Nishizumi, H. Sagara, Y. Iwakura, and T. Yamamoto. 2008. Kid-mediated chromosome compaction ensures proper nuclear envelope formation. Cell. 132: 771-782. http://dx.doi.org/10.1016/j.cell.2008.01.029
46. Oshimori, N., M. Ohsugi, and T. Yamamoto. 2006. The Plk1 target Kizuna stabilizes mitotic centrosomes to ensure spindle bipolarity. Nat. Cell Biol. 8: 1095-1101. http://dx.doi.org/10.1038/ncb1474
47. Powers, J., D.J. Rose, A. Saunders, S. Dunkelbarger, S. Strome, and W.M. Saxton. 2004. Loss of KLP-19 polar ejection force causes misorientation and missegregation of holocentric chromosomes. J. Cell Biol. 166: 991-1001. http://dx.doi.org/10.1083/jcb.200403036
48. Ribeiro, S.A., J.C. Gatlin, Y. Dong, A. Joglekar, L. Cameron, D.F. Hudson, C.J. Farr, B.F. McEwen, E.D. Salmon, W.C. Earnshaw, and P. Vagnarelli. 2009. Condensin regulates the stiffness of vertebrate centromeres. Mol. Biol. Cell. 20: 2371-2380. http://dx.doi.org/10.1091/mbc.E08-11-1127
49. Rieder, C.L., and G.G. Borisy. 1981. The attachment of kinetochores to the prometaphase spindle in PtK1 cells. Recovery from low temperature treatment. Chromosoma. 82: 693-716. http://dx.doi.org/10.1007/BF00285776
50. Rieder, C.L., and E.D. Salmon. 1994. Motile kinetochores and polar ejection forces dictate chromosome position on the vertebrate mitotic spindle. J. Cell Biol. 124: 223-233. http://dx.doi.org/10.1083/jcb.124.3.223
51. Rieder, C.L., E.A. Davison, L.C. Jensen, L. Cassimeris, and E.D. Salmon. 1986. Oscillatory movements of monooriented chromosomes and their position relative to the spindle pole result from the ejection properties of the aster and half-spindle. J. Cell Biol. 103: 581-591. http://dx.doi.org/10.1083/jcb.103.2.581
52. Santamaria, A., S. Nagel, H.H. Sillje, and E.A. Nigg. 2008. The spindle protein CHICA mediates localization of the chromokinesin Kid to the mitotic spindle. Curr. Biol. 18: 723-729. http://dx.doi.org/10.1016/j.cub.2008.04.041
53. Stevens, D., R. Gassmann, K. Oegema, and A. Desai. 2011. Uncoordinated loss of chromatid cohesion is a common outcome of extended metaphase arrest. PLoS ONE. 6:e22969. http://dx.doi.org/10.1371/journal.pone.0022969
54. Stumpff, J., G. von Dassow, M. Wagenbach, C. Asbury, and L. Wordeman. 2008. The kinesin-8 motor Kif18A suppresses kinetochore movements to control mitotic chromosome alignment. Dev. Cell. 14: 252-262. http://dx.doi.org/10.1016/j.devcel.2007.11.014
55. Stumpff, J., Y. Du, C.A. English, Z. Maliga, M. Wagenbach, C.L. Asbury, L. Wordeman, and R. Ohi. 2011. A tethering mechanism controls the processivity and kinetochore-microtubule plusend enrichment of the kinesin-8 Kif18A. Mol. Cell. 43: 764-775. http://dx.doi.org/10.1016/j.molcel.2011.07.022
56. Stumpff, J., M. Wagenbach, A. Franck, C.L. Asbury, and L. Wordeman. 2012. Kif18A and chromokinesins confine centromere movements via microtubule growth suppression and spatial control of kinetochore tension. Dev. Cell. 22: 1017-1029. http://dx.doi.org/10.1016/j.devcel.2012.02.013
57. Theurkauf, W.E., and R.S. Hawley. 1992. Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J. Cell Biol. 116: 1167-1180. http://dx.doi.org/10.1083/jcb.116.5.1167
58. Tokai-Nishizumi, N., M. Ohsugi, E. Suzuki, and T. Yamamoto. 2005. The chromokinesin Kid is required for maintenance of proper metaphase spindle size. Mol. Biol. Cell. 16: 5455-5463. http://dx.doi.org/10.1091/mbc.E05-03-0244
59. Varga, V., J. Helenius, K. Tanaka, A.A. Hyman, T.U. Tanaka, and J. Howard. 2006. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner. Nat. Cell Biol. 8: 957-962. http://dx.doi.org/10.1038/ncb1462
60. Vernos, I., J. Raats, T. Hirano, J. Heasman, E. Karsenti, and C. Wylie. 1995. Xklp1, a chromosomal Xenopus kinesin-like protein essential for spindle organization and chromosome positioning. Cell. 81: 117-127. http://dx.doi.org/10.1016/0092-8674(95)90376-3
61. Wan, X., D. Cimini, L.A. Cameron, and E.D. Salmon. 2012. The coupling between sister kinetochore directional instability and oscillations in centromere stretch in metaphase PtK1 cells. Mol. Biol. Cell. 23: 1035-1046. http://dx.doi.org/10.1091/mbc.E11-09-0767
62. Wandke, C., and S. Geley. 2006. Generation and characterization of an hKidspecific monoclonal antibody. Hybridoma (Larchmt). 25: 41-43. http://dx.doi.org/10.1089/hyb.2006.25.41
63. Wargacki, M.M., J.C. Tay, E.G. Muller, C.L. Asbury, and T.N. Davis. 2010. Kip3, the yeast kinesin-8, is required for clustering of kinetochores at metaphase. Cell Cycle. 9: 2581-2588. http://dx.doi.org/10.4161/cc.9.13.12076
64. West, R.R., T. Malmstrom, and J.R. McIntosh. 2002. Kinesins klp5(+) and klp6(+) are required for normal chromosome movement in mitosis. J. Cell Sci. 115:931-940.
65. Williams, B.C., M.F. Riedy, E.V. Williams, M. Gatti, and M.L. Goldberg. 1995. The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis. J. Cell Biol. 129: 709-723. http://dx.doi.org/10.1083/jcb.129.3.709
66. Wolf, F., C. Wandke, N. Isenberg, and S. Geley. 2006. Dose-dependent effects of stable cyclin B1 on progression through mitosis in human cells. EMBO J. 25: 2802-2813. http://dx.doi.org/10.1038/sj.emboj.7601163
67. Yajima, J., M. Edamatsu, J. Watai-Nishii, N. Tokai-Nishizumi, T. Yamamoto, and Y.Y. Toyoshima. 2003. The human chromokinesin Kid is a plus end-directed microtubule-based motor. EMBO J. 22: 1067-1074. http://dx.doi.org/10.1093/emboj/cdg102
68. Zhu, C., and W. Jiang. 2005. Cell cycle-dependent translocation of PRC1 on the spindle by Kif4 is essential for midzone formation and cytokinesis. Proc. Natl. Acad. Sci. USA. 102: 343-348. http://dx.doi.org/10.1073/pnas.0408438102
69. Zhu, C., J. Zhao, M. Bibikova, J.D. Leverson, E. Bossy-Wetzel, J.B. Fan, R.T. Abraham, and W. Jiang. 2005. Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference. Mol. Biol. Cell. 16: 3187-3199. http://dx.doi.org/10.1091/mbc.E05-02-0167