The functions and consequences of force at kinetochores

Journal of Cell Biology

Volumn 200, Issue 5, 2013, Pages 557-565

  Rago, Florencia ^a,b   Cheeseman, Iain M ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CHROMOSOME SEGREGATION; DEPOLYMERIZATION; DNA BINDING; FORCE; HUMAN; MICROTUBULE; MOLECULAR INTERACTION; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; MITOSIS; MITOSIS SPINDLE; PHYSIOLOGY; REVIEW;

DNA; NUCLEAR PROTEIN;

ANIMALS; CHROMOSOME SEGREGATION; DNA; HUMANS; KINETOCHORES; MECHANOTRANSDUCTION, CELLULAR; MITOSIS; MITOTIC SPINDLE APPARATUS; NUCLEAR PROTEINS; STRESS, MECHANICAL;

MLCS; MLOWN;

EID: 84874970891     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201211113     Document Type: Article

References (88)

1. Akiyoshi, B., C.R. Nelson, J.A. Ranish, and S. Biggins. 2009. Quantitative proteomic analysis of purified yeast kinetochores identifies a PP1 regulatory subunit. Genes Dev. 23:2887-2899. http://dx.doi.org/10.1101/gad.1865909
2. 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
3. Al-Bassam, J., and F. Chang. 2011. Regulation of microtubule dynamics by TOG-domain proteins XMAP215/Dis1 and CLASP. Trends Cell Biol. 21:604-614. http://dx.doi.org/10.1016/j.tcb.2011.06.007
4. Bader, J.R., and K.T. Vaughan. 2010. Dynein at the kinetochore: Timing, interactions and functions. Semin. Cell Dev. Biol. 21:269-275. http://dx.doi.org/ 10.1016/j.semcdb.2009.12.015
5. Bayless, B.A., T.H. Giddings Jr., M. Winey, and C.G. Pearson. 2012. Bld10/ Cep135 stabilizes basal bodies to resist cilia-generated forces. Mol. Biol. Cell. 23:4820-4832. http://dx.doi.org/10.1091/mbc.E12-08-0577
6. Bennink, M.L., S.H. Leuba, G.H. Leno, J. Zlatanova, B.G. de Grooth, and J. Greve. 2001. Unfolding individual nucleosomes by stretching single chromatin fibers with optical tweezers. Nat. Struct. Biol. 8:606-610. http://dx.doi.org/10.1038/89646
7. Bloom, K.S. 2008. Beyond the code: the mechanical properties of DNA as they relate to mitosis. Chromosoma. 117:103-110. http://dx.doi.org/ 10.1007/s00412-007-0138-0
8. Bock, L.J., C. Pagliuca, N. Kobayashi, R.A. Grove, Y. Oku, K. Shrestha, C. Alfieri, C. Golfieri, A. Oldani, M. Dal Maschio, et al. 2012. Cnn1 inhibits the interactions between the KMN complexes of the yeast kinetochore. Nat. Cell Biol. 14:614-624. http://dx.doi.org/10.1038/ncb2495
9. Bouck, D.C., and K. Bloom. 2007. Pericentric chromatin is an elastic component of the mitotic spindle. Curr. Biol. 17:741-748. http://dx.doi .org/10.1016/j.cub.2007.03.033
10. Brower-Toland, B.D., C.L. Smith, R.C. Yeh, J.T. Lis, C.L. Peterson, and M.D. Wang. 2002. Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc. Natl. Acad. Sci. USA. 99:1960-1965. http://dx.doi.org/10.1073/pnas.022638399
11. Cheeseman, I.M., and A. Desai. 2008. Molecular architecture of the kinetochoremicrotubule interface. Nat. Rev. Mol. Cell Biol. 9:33-46. http://dx.doi.org/ 10.1038/nrm2310
12. Cheeseman, I.M., J.S. Chappie, E.M. Wilson-Kubalek, and A. Desai. 2006. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell. 127:983-997. http://dx.doi.org/10.1016/ j.cell.2006.09.039
13. Chen, W., and D. Zhang. 2004. Kinetochore fibre dynamics outside the context of the spindle during anaphase. Nat. Cell Biol. 6:227-231.
14. Cottingham, F.R., L. Gheber, D.L. Miller, and M.A. Hoyt. 1999. Novel roles for Saccharomyces cerevisiae mitotic spindle motors. J. Cell Biol. 147:335- 350. http://dx.doi.org/10.1083/jcb.147.2.335
15. Coue, M., V.A. Lombillo, and J.R. McIntosh. 1991. Microtubule depolymerization promotes particle and chromosome movement in vitro. J. Cell Biol. 112:1165-1175. http://dx.doi.org/10.1083/jcb.112.6.1165
16. Cui, Y., and C. Bustamante. 2000. Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. Proc. Natl. Acad. Sci. USA. 97:127-132. http://dx.doi.org/10.1073/pnas.97.1.127
17. Desai, A., and T.J. Mitchison. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13:83-117. http://dx.doi.org/10.1146/annurev .cellbio.13.1.83
18. Dumont, S., E.D. Salmon, and T.J. Mitchison. 2012. Deformations within moving kinetochores reveal different sites of active and passive force generation. Science. 337:355-358. http://dx.doi.org/10.1126/science.1221886
19. Evans, E. 2001. Probing the relation between force-lifetime-and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30:105-128. http://dx.doi.org/10.1146/annurev.biophys.30.1.105
20. Finan, K., P.R. Cook, and D. Marenduzzo. 2011. Non-specific (entropic) forces as major determinants of the structure of mammalian chromosomes. Chromosome Res. 19:53-61. http://dx.doi.org/10.1007/s10577-010-9150-y
21. Fisher, J.K., M. Ballenger, E.T. O'Brien, J. Haase, R. Superfine, and K. Bloom. 2009. DNA relaxation dynamics as a probe for the intracellular environment. Proc. Natl. Acad. Sci. USA. 106:9250-9255. http://dx.doi.org/10.1073/pnas.0812723106
22. Franck, A.D., A.F. Powers, D.R. Gestaut, T. Gonen, T.N. Davis, and C.L. Asbury. 2007. Tension applied through the Dam1 complex promotes microtubule elongation providing a direct mechanism for length control in mitosis. Nat. Cell Biol. 9:832-837. http://dx.doi.org/10.1038/ncb1609
23. Gascoigne, K.E., and I.M. Cheeseman. 2011. Kinetochore assembly: if you build it, they will come. Curr. Opin. Cell Biol. 23:102-108. http://dx.doi.org/ 10.1016/j.ceb.2010.07.007
24. Gascoigne, K.E., K. Takeuchi, A. Suzuki, T. Hori, T. Fukagawa, and I.M. Cheeseman. 2011. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell. 145:410-422. http://dx.doi.org/ 10.1016/j.cell.2011.03.031
25. Gennerich, A., A.P. Carter, S.L. Reck-Peterson, and R.D. Vale. 2007. Forceinduced bidirectional stepping of cytoplasmic dynein. Cell. 131:952-965. http://dx.doi.org/10.1016/j.cell.2007.10.016
26. Gregan, J., S. Polakova, L. Zhang, I.M. Tolíc-Nørrelykke, and D. Cimini. 2011. Merotelic kinetochore attachment: causes and effects. Trends Cell Biol. 21:374-381. http://dx.doi.org/10.1016/j.tcb.2011.01.003
27. Grishchuk, E.L., and J.R. McIntosh. 2006. Microtubule depolymerization can drive poleward chromosome motion in fission yeast. EMBO J. 25:4888- 4896. http://dx.doi.org/10.1038/sj.emboj.7601353
28. Grishchuk, E.L., M.I. Molodtsov, F.I. Ataullakhanov, and J.R. McIntosh. 2005. Force production by disassembling microtubules. Nature. 438:384-388. http://dx.doi.org/10.1038/nature04132
29. Guse, A., C.W. Carroll, B. Moree, C.J. Fuller, and A.F. Straight. 2011. In vitro centromere and kinetochore assembly on defined chromatin templates. Nature. 477:354-358. http://dx.doi.org/10.1038/nature10379
30. Hill, T.L. 1985. Theoretical problems related to the attachment of microtubules to kinetochores. Proc. Natl. Acad. Sci. USA. 82:4404-4408. http://dx.doi .org/10.1073/pnas.82.13.4404
31. Hunt, A.J., and J.R. McIntosh. 1998. The dynamic behavior of individual microtubules associated with chromosomes in vitro. Mol. Biol. Cell. 9: 2857-2871.
32. Inoué, S., and E.D. Salmon. 1995. Force generation by microtubule assembly/ disassembly in mitosis and related movements. Mol. Biol. Cell. 6: 1619-1640.
33. Joglekar, A.P., D.C. Bouck, J.N. Molk, K.S. Bloom, and E.D. Salmon. 2006. Molecular architecture of a kinetochore-microtubule attachment site. Nat. Cell Biol. 8:581-585. http://dx.doi.org/10.1038/ncb1414
34. Joglekar, A.P., D. Bouck, K. Finley, X. Liu, Y. Wan, J. Berman, X. He, E.D. Salmon, and K.S. Bloom. 2008. Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J. Cell Biol. 181:587-594. http://dx.doi.org/ 10.1083/jcb.200803027
35. Johnston, K., A. Joglekar, T. Hori, A. Suzuki, T. Fukagawa, and E.D. Salmon. 2010. Vertebrate kinetochore protein architecture: protein copy number. J. Cell Biol. 189:937-943. http://dx.doi.org/10.1083/jcb.200912022
36. Jun, S., and A. Wright. 2010. Entropy as the driver of chromosome segregation. Nat. Rev. Microbiol. 8:600-607. http://dx.doi.org/10.1038/ nrmicro2391
37. 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
38. Koshland, D.E., T.J. Mitchison, and M.W. Kirschner. 1988. Polewards chromosome movement driven by microtubule depolymerization in vitro. Nature. 331:499-504. http://dx.doi.org/10.1038/331499a0
39. Kumar, S., and M.S. Li. 2010. Biomolecules under mechanical force. Phys. Rep. 486:1-74. http://dx.doi.org/10.1016/j.physrep.2009.11.001
40. LaFountain, J.R., Jr., R. Oldenbourg, R.W. Cole, and C.L. Rieder. 2001. Microtubule flux mediates poleward motion of acentric chromosome fragments during meiosis in insect spermatocytes. Mol. Biol. Cell. 12: 4054-4065.
41. LaFountain, J.R., Jr., C.S. Cohan, A.J. Siegel, and D.J. LaFountain. 2004. Direct visualization of microtubule flux during metaphase and anaphase in crane-fly spermatocytes. Mol. Biol. Cell. 15:5724-5732. http://dx.doi .org/10.1091/mbc.E04-08-0750
42. Lampert, F., P. Hornung, and S. Westermann. 2010. The Dam1 complex confers microtubule plus end-tracking activity to the Ndc80 kinetochore complex. J. Cell Biol. 189:641-649. http://dx.doi.org/10.1083/jcb.200912021
43. Lawrimore, J., K.S. Bloom, and E.D. Salmon. 2011. Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J. Cell Biol. 195:573-582. http://dx.doi.org/10.1083/jcb.201106036
44. Leckband, D. 2000. Measuring the forces that control protein interactions. Annu. Rev. Biophys. Biomol. Struct. 29:1-26. http://dx.doi.org/10.1146/annurev .biophys.29.1.1
45. 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
46. Lin, S., J.-L. Chen, L.-S. Huang, and H.-W. Lin. 2005. Measurements of the forces in protein interactions with atomic force microscopy. Current Proteomics. 2:55-81. http://dx.doi.org/10.2174/1570164053507754
47. Liu, D., G. Vader, M.J.M. Vromans, M.A. Lampson, and S.M.A. Lens. 2009. Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science. 323:1350-1353. http://dx.doi .org/10.1126/science.1167000
48. Maddox, P., A. Straight, P. Coughlin, T.J. Mitchison, and E.D. Salmon. 2003. Direct observation of microtubule dynamics at kinetochores in Xenopus extract spindles: implications for spindle mechanics. J. Cell Biol. 162: 377-382. http://dx.doi.org/10.1083/jcb.200301088
49. Malvezzi, F., G. Litos, A. Schleiffer, A. Heuck, K. Mechtler, T. Clausen, and S. Westermann. 2013. A structural basis for kinetochore recruitment of the Ndc80 complex via two distinct centromere receptors. EMBO J. 32:409- 423. http://dx.doi.org/10.1038/emboj.2012.356
50. 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
51. Matos, I., and H. Maiato. 2011. Prevention and correction mechanisms behind anaphase synchrony: implications for the genesis of aneuploidy. Cytogenet. Genome Res. 133:243-253. http://dx.doi.org/10.1159/000323803
52. 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
53. McIntosh, J.R., E.L. Grishchuk, M.K. Morphew, A.K. Efremov, K. Zhudenkov, V.A. Volkov, I.M. Cheeseman, A. Desai, D.N. Mastronarde, and F.I. Ataullakhanov. 2008. Fibrils connect microtubule tips with kinetochores: a mechanism to couple tubulin dynamics to chromosome motion. Cell. 135:322-333. http://dx.doi.org/10.1016/j.cell.2008.08.038
54. Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:50-53. http://dx.doi.org/10.1038/16219
55. Mitchison, T.J., and E.D. Salmon. 1992. Poleward kinetochore fiber movement occurs during both metaphase and anaphase-A in newt lung cell mitosis. J. Cell Biol. 119:569-582. http://dx.doi.org/10.1083/jcb.119.3.569
56. Molodtsov, M.I., E.A. Ermakova, E.E. Shnol, E.L. Grishchuk, J.R. McIntosh, and F.I. Ataullakhanov. 2005. A molecular-mechanical model of the microtubule. Biophys. J. 88:3167-3179. http://dx.doi.org/10.1529/biophysj.104.051789
57. Nicklas, R.B. 1965. Chromosome velocity during mitosis as a function of chromosome size and position. J. Cell Biol. 25:119-135. http://dx.doi.org/ 10.1083/jcb.25.1.119
58. Nicklas, R.B. 1983. Measurements of the force produced by the mitotic spindle in anaphase. J. Cell Biol. 97:542-548. http://dx.doi.org/ 10.1083/jcb.97.2.542
59. Nicklas, R.B. 1988. The forces that move chromosomes in mitosis. Annu. Rev. Biophys. Biophys. Chem. 17:431-449. http://dx.doi.org/10.1146/annurev .bb.17.060188.002243
60. Nicklas, R.B., S.C. Ward, and G.J. Gorbsky. 1995. Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J. Cell Biol. 130:929-939. http://dx.doi.org/10.1083/jcb.130.4.929
61. Nishino, T., K. Takeuchi, K.E. Gascoigne, A. Suzuki, T. Hori, T. Oyama, K. Morikawa, I.M. Cheeseman, and T. Fukagawa. 2012. CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell. 148:487-501. http://dx.doi.org/10.1016/j.cell.2011.11.061
62. Nishino, T., F. Rago, T. Hori, K. Tomii, I.M. Cheeseman, and T. Fukagawa. 2013. CENP-T provides a structural platform for outer kinetochore assembly. EMBO J. 32:424-436. http://dx.doi.org/10.1038/emboj.2012.348
63. Nogales, E. 2000. Structural insights into microtubule function. Annu. Rev. Biochem. 69:277-302. http://dx.doi.org/10.1146/annurev.biochem.69.1.277
64. Nogales, E., and H.-W. Wang. 2006. Structural mechanisms underlying nucleotide- dependent self-assembly of tubulin and its relatives. Curr. Opin. Struct. Biol. 16:221-229. http://dx.doi.org/10.1016/j.sbi.2006.03.005
65. Pearson, C.G., P.S. Maddox, E.D. Salmon, and K. Bloom. 2001. Budding yeast chromosome structure and dynamics during mitosis. J. Cell Biol. 152:1255-1266. http://dx.doi.org/10.1083/jcb.152.6.1255
66. Powers, A.F., A.D. Franck, D.R. Gestaut, J. Cooper, B. Gracyzk, R.R. Wei, L. Wordeman, T.N. Davis, and C.L. Asbury. 2009. The Ndc80 kinetochore complex forms load-bearing attachments to dynamic microtubule tips via biased diffusion. Cell. 136:865-875. http://dx.doi.org/ 10.1016/j.cell.2008.12.045
67. Roca-Cusachs, P., T. Iskratsch, and M.P. Sheetz. 2012. Finding the weakest link: exploring integrin-mediated mechanical molecular pathways. J. Cell Sci. 125:3025-3038. http://dx.doi.org/10.1242/jcs.095794
68. Sandall, S., F. Severin, I.X. McLeod, J.R. Yates III, K. Oegema, A. Hyman, and A. Desai. 2006. A Bir1-Sli15 complex connects centromeres to microtubules and is required to sense kinetochore tension. Cell. 127:1179- 1191. http://dx.doi.org/10.1016/j.cell.2006.09.049
69. Santaguida, S., and A. Musacchio. 2009. The life and miracles of kinetochores. EMBO J. 28:2511-2531. http://dx.doi.org/10.1038/emboj.2009.173
70. Schleiffer, A., M. Maier, G. Litos, F. Lampert, P. Hornung, K. Mechtler, and S. Westermann. 2012. CENP-T proteins are conserved centromere receptors of the Ndc80 complex. Nat. Cell Biol. 14:604-613. http://dx.doi .org/10.1038/ncb2493
71. Schmidt, J.C., H. Arthanari, A. Boeszoermenyi, N.M. Dashkevich, E.M. Wilson- Kubalek, N. Monnier, M. Markus, M. Oberer, R.A. Milligan, M. Bathe, et al. 2012. The kinetochore-bound Ska1 complex tracks depolymerizing microtubules and binds to curved protofilaments. Dev. Cell. 23:968-980. http://dx.doi.org/10.1016/j.devcel.2012.09.012
72. Sekulic, N., E.A. Bassett, D.J. Rogers, and B.E. Black. 2010. The structure of (CENP-A-H4)(2) reveals physical features that mark centromeres. Nature. 467:347-351. http://dx.doi.org/10.1038/nature09323
73. Sharp, D.J., G.C. Rogers, and J.M. Scholey. 2000. Cytoplasmic dynein is required for poleward chromosome movement during mitosis in Drosophila embryos. Nat. Cell Biol. 2:922-930. http://dx.doi.org/10.1038/35046574
74. Suzuki, A., T. Hori, T. Nishino, J. Usukura, A. Miyagi, K. Morikawa, and T. Fukagawa. 2011. Spindle microtubules generate tension-dependent changes in the distribution of inner kinetochore proteins. J. Cell Biol. 193: 125-140. http://dx.doi.org/10.1083/jcb.201012050
75. Tanaka, T.U. 2002. Bi-orienting chromosomes on the mitotic spindle. Curr. Opin. Cell Biol. 14:365-371. http://dx.doi.org/10.1016/S0955-0674(02)00328-9
76. Taylor, E.W. 1965. Brownian and saltatory movements of cytoplasmic granules and the movement of anaphase chromosomes. In Proceedings of the fourth international congress on Rheology. Part 4-Symposium on Biorheology. A.L. Copley, editor. Interscience, New York. 175-191.
77. Tien, J.F., N.T. Umbreit, D.R. Gestaut, A.D. Franck, J. Cooper, L. Wordeman, T. Gonen, C.L. Asbury, and T.N. Davis. 2010. Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B. J. Cell Biol. 189:713-723. http://dx.doi.org/ 10.1083/jcb.200910142
78. Uchida, K.S.K., K. Takagaki, K. Kumada, Y. Hirayama, T. Noda, and T. Hirota. 2009. Kinetochore stretching inactivates the spindle assembly checkpoint. J. Cell Biol. 184:383-390. http://dx.doi.org/10.1083/jcb.200811028
79. Umbreit, N.T., D.R. Gestaut, J.F. Tien, B.S. Vollmar, T. Gonen, C.L. Asbury, and T.N. Davis. 2012. The Ndc80 kinetochore complex directly modulates microtubule dynamics. Proc. Natl. Acad. Sci. USA. 109:16113- 16118. http://dx.doi.org/10.1073/pnas.1209615109
80. Verdaasdonk, J.S., R. Gardner, A.D. Stephens, E. Yeh, and K. Bloom. 2012. Tension-dependent nucleosome remodeling at the pericentromere in yeast. Mol. Biol. Cell. 23:2560-2570. http://dx.doi.org/10.1091/mbc.E11- 07-0651
81. 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
82. Wan, X., R.P. O'Quinn, H.L. Pierce, A.P. Joglekar, W.E. Gall, J.G. DeLuca, C.W. Carroll, S.-T. Liu, T.J. Yen, B.F. McEwen, et al. 2009. Protein architecture of the human kinetochore microtubule attachment site. Cell. 137:672-684. http://dx.doi.org/10.1016/j.cell.2009.03.035
83. 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.E11-09-076
84. Weisel, J.W., H. Shuman, and R.I. Litvinov. 2003. Protein-protein unbinding induced by force: single-molecule studies. Curr. Opin. Struct. Biol. 13:227-235. http://dx.doi.org/10.1016/S0959-440X(03)00039-3
85. Welburn, J.P.I., E.L. Grishchuk, C.B. Backer, E.M. Wilson-Kubalek, J.R. Yates III, and I.M. Cheeseman. 2009. The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev. Cell. 16:374-385. http://dx.doi.org/10.1016/j.devcel.2009.01.011
86. Welburn, J.P.I., M. Vleugel, D. Liu, J.R. Yates III, M.A. Lampson, T. Fukagawa, and I.M. Cheeseman. 2010. Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface. Mol. Cell. 38:383-392. http://dx.doi.org/10.1016/j.molcel.2010.02.034
87. Yan, J., T.J. Maresca, D. Skoko, C.D. Adams, B. Xiao, M.O. Christensen, R. Heald, and J.F. Marko. 2007. Micromanipulation studies of chromatin fibers in Xenopus egg extracts reveal ATP-dependent chromatin assembly dynamics. Mol. Biol. Cell. 18:464-474. http://dx.doi.org/10.1091/mbc .E06-09-0800
88. 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