Elevated polar ejection forces stabilize kinetochore-microtubule attachments

Journal of Cell Biology

Volumn 200, Issue 2, 2013, Pages 203-218

  Cane, Stuart ^a   Ye, Anna A ^a   Luks Morgan, Sasha J ^a   Maresca, Thomas J ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; KINESIN; NOD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL ASSAY; CELL FUNCTION; CELL INTERACTION; CELL MOTILITY; CENTROMERE; CHIMERA; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; DROSOPHILA; FORCE; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; POLAR EJECTION FORCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; SPINDLE CELL; SPINDLE POLE BODY;

ANIMALS; CELL CYCLE PROTEINS; CELL POLARITY; CELLS, CULTURED; CHROMOSOME POSITIONING; CHROMOSOMES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; KINESIN; KINETOCHORES; MICROTUBULES; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES;

EID: 84873046642     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201211119     Document Type: Article

References (65)

1. Adams, R.R., H. Maiato, W.C. Earnshaw, and M. Carmena. 2001. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J. Cell Biol. 153: 865-880. http://dx.doi.org/10.1083/jcb.153.4.865
2. Afshar, K., N.R. Barton, R.S. Hawley, and L.S. Goldstein. 1995a. DNA binding and meiotic chromosomal localization of the Drosophila nod kinesin-like protein. Cell. 81:129-138. http://dx.doi.org/10.1016/0092-8674(95)90377-1
3. Afshar, K., J. Scholey, and R.S. Hawley. 1995b. Identification of the chromosome localization domain of the Drosophila nod kinesin-like protein. J. Cell Biol. 131:833-843. http://dx.doi.org/10.1083/jcb.131.4.833
4. Akiyoshi, B., K.K. Sarangapani, A.F. Powers, C.R. Nelson, S.L. Reichow, H. Arellano-Santoyo, T. Gonen, J.A. Ranish, C.L. Asbury, and S. Biggins. 2010. Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature. 468:576-579. http://dx.doi.org/10.1038/nature09594
5. 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
6. Bieling, P., L. Laan, H. Schek, E.L. Munteanu, L. Sandblad, M. Dogterom, D. Brunner, and T. Surrey. 2007. Reconstitution of a microtubule plusend tracking system in vitro. Nature. 450:1100-1105. http://dx.doi.org/10.1038/nature06386
7. 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
8. 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
9. Block, S.M., L.S. Goldstein, and B.J. Schnapp. 1990. Bead movement by single kinesin molecules studied with optical tweezers. Nature. 348:348-352. http://dx.doi.org/10.1038/348348a0
10. 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
11. 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
12. Carvalho, P., M.L. Gupta Jr., M.A. Hoyt, and D. Pellman. 2004. Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Dev. Cell. 6:815-829. http://dx.doi.org/10.1016/j.devcel.2004.05.001
13. 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.
14. 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
15. 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
16. Cui, W., L.R. Sproul, S.M. Gustafson, H.J. Matthies, S.P. Gilbert, and R.S. Hawley. 2005. Drosophila Nod protein binds preferentially to the plus ends of microtubules and promotes microtubule polymerization in vitro. Mol. Biol. Cell. 16:5400-5409. http://dx.doi.org/10.1091/mbc.E05-06-0582
17. Ditchfield, C., V.L. Johnson, A. Tighe, R. Ellston, C. Haworth, T. Johnson, A. Mortlock, N. Keen, and S.S. Taylor. 2003. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161:267-280. http://dx.doi.org/10.1083/jcb.200208091
18. Dogterom, M., and B. Yurke. 1997. Measurement of the force-velocity relation for growing microtubules. Science. 278:856-860. http://dx.doi.org/10.1126/science.278.5339.856
19. Domnitz, S.B., M. Wagenbach, J. Decarreau, and L. Wordeman. 2012. MCAK activity at microtubule tips regulates spindle microtubule length to promote robust kinetochore attachment. J. Cell Biol. 197:231-237. http://dx.doi.org/10.1083/jcb.201108147
20. Dumont, J., K. Oegema, and A. Desai. 2010. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat. Cell Biol. 12:894-901. http://dx.doi.org/10.1038/ncb2093
21. 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
22. Giet, R., and D.M. Glover. 2001. Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152:669-682. http://dx.doi.org/10.1083/jcb.152.4.669
23. 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
24. Goshima, G., R. Wollman, S.S. Goodwin, N. Zhang, J.M. Scholey, R.D. Vale, and N. Stuurman. 2007. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science. 316:417-421. http://dx.doi.org/10.1126/science.1141314
25. Goshima, G., M. Mayer, N. Zhang, N. Stuurman, and R.D. Vale. 2008. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 181:421-429. http://dx.doi.org/10.1083/jcb.200711053
26. Hackney, D.D. 1995. Highly processive microtubule-stimulated ATP hydrolysis by dimeric kinesin head domains. Nature. 377:448-450. http://dx.doi.org/10.1038/377448a0
27. Hauf, S., R.W. Cole, S. LaTerra, C. Zimmer, G. Schnapp, R. Walter, A. Heckel, J. van Meel, C.L. Rieder, and J.M. Peters. 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. http://dx.doi.org/10.1083/jcb.200208092
28. Howard, J., A.J. Hudspeth, and R.D. Vale. 1989. Movement of microtubules by single kinesin molecules. Nature. 342:154-158. http://dx.doi.org/10.1038/342154a0
29. 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
30. 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
31. Khodjakov, A., and C.L. Rieder. 1996. Kinetochores moving away from their associated pole do not exert a significant pushing force on the chromosome. J. Cell Biol. 135:315-327. http://dx.doi.org/10.1083/jcb.135.2.315
32. King, J.M., and R.B. Nicklas. 2000. Tension on chromosomes increases the number of kinetochore microtubules but only within limits. J. Cell. Sci. 113:3815-3823.
33. Kitajima, T.S., M. Ohsugi, and J. Ellenberg. 2011. Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell. 146:568-581. http://dx.doi.org/10.1016/j.cell.2011.07.031
34. 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
35. Lampson, M.A., K. Renduchitala, A. Khodjakov, and T.M. Kapoor. 2004. Correcting improper chromosome-spindle attachments during cell division. Nat. Cell Biol. 6:232-237. http://dx.doi.org/10.1038/ncb1102
36. Lee, L., J.S. Tirnauer, J. Li, S.C. Schuyler, J.Y. Liu, and D. Pellman. 2000. Positioning of the mitotic spindle by a cortical-microtubule capture mechanism. Science. 287:2260-2262. http://dx.doi.org/10.1126/science .287.5461.2260
37. 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
38. Li, X., and R.B. Nicklas. 1995. Mitotic forces control a cell-cycle checkpoint. Nature. 373:630-632. http://dx.doi.org/10.1038/373630a0
39. Li, W., T. Miki, T. Watanabe, M. Kakeno, I. Sugiyama, K. Kaibuchi, and G. Goshima. 2011. EB1 promotes microtubule dynamics by recruiting Sentin in Drosophila cells. J. Cell Biol. 193:973-983. http://dx.doi.org/ 10.1083/jcb.201101108
40. Magidson, V., C.B. O'Connell, J. Lonçarek, 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
41. Maresca, T.J., and E.D. Salmon. 2009. Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J. Cell Biol. 184:373-381. http://dx.doi.org/10 .1083/jcb.200808130
42. Maresca, T.J., and E.D. Salmon. 2010. Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J. Cell Sci. 123:825-835. http://dx.doi.org/10.1242/jcs.064790
43. Markus, S.M., K.M. Plevock, B.J. St Germain, J.J. Punch, C.W. Meaden, and W.L. Lee. 2011. Quantitative analysis of Pac1/LIS1-mediated dynein targeting: implications for regulation of dynein activity in budding yeast. Cytoskeleton (Hoboken). 68:157-174.
44. 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
45. Matthies, H.J., R.J. Baskin, and R.S. Hawley. 2001. Orphan kinesin NOD lacks motile properties but does possess a microtubule-stimulated ATPase activity. Mol. Biol. Cell. 12:4000-4012.
46. Nicklas, R.B., and C.A. Koch. 1969. Chromosome micromanipulation. III. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J. Cell Biol. 43:40-50. http://dx.doi.org/10.1083/jcb.43.1.40
47. Nicklas, R.B., J.C. Waters, E.D. Salmon, and S.C. Ward. 2001. Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential. J. Cell Sci. 114:4173-4183.
48. 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
49. Rasooly, R.S., C.M. New, P. Zhang, R.S. Hawley, and B.S. Baker. 1991. The lethal(1)TW-6cs mutation of Drosophila melanogaster is a dominant antimorphic allele of nod and is associated with a single base change in the putative ATP-binding domain. Genetics. 129:409-422.
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. Rieder, C.L., R.W. Cole, A. Khodjakov, and G. Sluder. 1995. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130:941-948. http://dx.doi.org/10.1083/jcb.130.4.941
53. Rogers, S.L., G.C. Rogers, D.J. Sharp, and R.D. Vale. 2002. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 158:873-884. http://dx.doi.org/10.1083/jcb.200202032
54. Shah, J.V., E. Botvinick, Z. Bonday, F. Furnari, M. Berns, and D.W. Cleveland. 2004. Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr. Biol. 14:942-952.
55. Skibbens, R.V., V.P. Skeen, and E.D. Salmon. 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. http://dx.doi.org/10.1083/jcb.122.4.859
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. Tirnauer, J.S., S. Grego, E.D. Salmon, and T.J. Mitchison. 2002. EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol. Biol. Cell. 13:3614-3626. http://dx.doi.org/10.1091/mbc.02-04-0210
59. 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
60. Visscher, K., M.J. Schnitzer, and S.M. Block. 1999. Single kinesin molecules studied with a molecular force clamp. Nature. 400:184-189. http://dx.doi .org/10.1038/22146
61. Wandke, C., M. Barisic, R. Sigl, V. Rauch, F. Wolf, A.C. Amaro, C.H. Tan, A.J. Pereira, U. Kutay, H. Maiato, et al. 2012. Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis. J. Cell Biol. 198:847-863. http://dx.doi.org/10.1083/jcb.201110060
62. Wignall, S.M., and A.M. Villeneuve. 2009. Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat. Cell Biol. 11:839-844. http://dx.doi.org/10.1038/ncb1891
63. Yajima, J., M. Edamatsu, J. Watai-Nishii, N. Tokai-Nishizumi, T. Yamamoto, and Y.Y. Toyoshima. 2003. The human chromokinesin Kid is a plus enddirected microtubule-based motor. EMBO J. 22:1067-1074. http://dx.doi .org/10.1093/emboj/cdg102
64. Zhang, P., and R.S. Hawley. 1990. The genetic analysis of distributive segregation in Drosophila melanogaster. II. Further genetic analysis of the nod locus. Genetics. 125:115-127.
65. Zhang, P., B.A. Knowles, L.S. Goldstein, and R.S. Hawley. 1990. A kinesin-like protein required for distributive chromosome segregation in Drosophila. Cell. 62:1053-1062. http://dx.doi.org/10.1016/0092-8674(90)90383-P