Building an integrated model of chromosome congression

Journal of Cell Science

Volumn 128, Issue 18, 2015, Pages 3363-3374

  Auckland, Philip ^a   McAinsh, Andrew D ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Congression; Kinetochore; Mitosis; Spindle

Indexed keywords

CENTROMERE; CHROMOSOME; DEPOLYMERIZATION; DEPOLYMERIZATION COUPLED PULLING; FORCE; GENERATOR; HUMAN; METAPHASE; MICROTUBULE; MITOSIS; NONHUMAN; NOTE; PRIORITY JOURNAL; PROMETAPHASE; SPINDLE POLE; VERTEBRATE; ANIMAL; BIOLOGICAL MODEL; CHROMOSOME PAIRING; CHROMOSOME PUFF; CHROMOSOME SEGREGATION; HELA CELL LINE; PHYSIOLOGY; SPINDLE APPARATUS;

ANIMALS; CENTROMERE; CHROMOSOMAL PUFFS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; HELA CELLS; HUMANS; KINETOCHORES; MODELS, BIOLOGICAL; SPINDLE APPARATUS; VERTEBRATES;

EID: 84946031348     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.169367     Document Type: Note

References (127)

1. Abad, M.A., Medina, B., Santamaria, A., Zou, J., Plasberg-Hill, C., Madhumalar, A., Jayachandran, U., Redli, P. M., Rappsilber, J., Nigg, E. A. et al. (2014). Structural basis for microtubule recognition by the human kinetochore Ska complex. Nat. Commun. 5, 2964.
2. Alushin, G. M., Ramey, V. H., Pasqualato, S., Ball, D. A., Grigorieff, N., Musacchio, A. and Nogales, E. (2010). The Ndc80 kinetochore complex forms oligomeric arrays along microtubules. Nature 467, 805-810.
3. Alushin, G. M., Musinipally, V., Matson, D., Tooley, J., Stukenberg, P. T. and Nogales, E. (2012). Multimodal microtubule binding by the Ndc80 kinetochore complex. Nat. Struct. Mol. Biol. 19, 1161-1167.
4. Amaro, A. C., Samora, C. P., Holtackers, R., Wang, E., Kingston, I. J., Alonso, M., Lampson, M., McAinsh, A. D. and Meraldi, P. (2010). Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nat. Cell Biol. 12, 319-329.
5. Antonio, C., Ferby, I., Wilhelm, H., Jones, M., Karsenti, E., Nebreda, A. R. and Vernos, I. (2000). Xkid, a chromokinesin required for chromosome alignment on the metaphase plate. Cell 102, 425-435.
6. Armond, J. W., Vladimirou, E., Erent, M., McAinsh, A. D. and Burroughs, N. J. (2015). Probing microtubule polymerisation state at single kinetochores during metaphase chromosome motion. J. Cell Sci. 128, 1991-2001.
7. Ault, J. G., DeMarco, A. J., Salmon, E. D. and Rieder, C. L. (1991). Studies on the ejection properties of asters: astral microtubule turnover influences the oscillatory behaviour and positioning of monoorientated chromosomes. J. Cell Sci. 99, 701-710.
8. Bancroft, J., Auckland, P., Samora, C. P. and McAinsh, A. D. (2015). Chromosome congression is promoted by CENP-Q-and CENP-E-dependent pathways. J. Cell Sci. 128, 171-184.
9. Barisic, M., Aguiar, P., Geley, S. and Maiato, H. (2014). Kinetochore motors drive congression of peripheral polar chromosomes by overcoming random armejection forces. Nat. Cell Biol. 16, 1249-1256.
10. Barisic, M., Silva e Sousa, R., Tripathy, S. K., Magiera, M. M., Zaytsev, A. V., Pereira, A. L., Janke, C., Grishchuk, E. L. and Maiato, H. (2015). Microtubule detyrosination guides chromosomes during mitosis. Science 348, 799-803.
11. Bieling, P., Kronja, I. and Surrey, T. (2010). Microtubule motility on reconstituted meiotic chromatin. Curr. Biol. 20, 763-769.
12. Bomont, P., Maddox, P., Shah, J. V., Desai, A. B. and Cleveland, D. W. (2005). Unstable microtubule capture at kinetochores depleted of the centromereassociated protein CENP-F. EMBO J. 24, 3927-3939.
13. Braun, M., Drummond, D. R., Cross, R. A. and McAinsh, A. D. (2009). The kinesin-14 Klp2 organizes microtubules into parallel bundles by an ATPdependent sorting mechanism. Nat. Cell Biol. 11, 724-730.
14. Brouhard, G. J. and Hunt, A. J. (2005). Microtubule movements on the arms of mitotic chromosomes: polar ejection forces quantified in vitro. Proc. Natl. Acad. Sci. USA 102, 13903-13908.
15. Brust-Mascher, I. and Scholey, J. M. (2002). Microtubule flux and sliding in mitotic spindles of Drosophila embryos. Mol. Biol. Cell 13, 3967-3975.
16. Cai, S., O'Connell, C. B., Khodjakov, A. and Walczak, C. E. (2009). Chromosome congression in the absence of kinetochore fibres. Nat. Cell Biol. 11, 832-838.
17. Cane, S., Ye, A. A., Luks-Morgan, S. J. and Maresca, T. J. (2013). Elevated polar ejection forces stabilize kinetochore-microtubule attachments. J. Cell Biol. 200, 203-218.
18. Cassimeris, L. and Salmon, E. D. (1991). Kinetochore microtubules shorten by loss of subunits at the kinetochores of prometaphase chromosomes. J. Cell Sci. 98, 151-158.
19. Centonze, V. E. and Borisy, G. G. (1991). Pole-to-chromosome movements induced at metaphase: sites of microtubule disassembly. J. Cell Sci. 100, 205-211.
20. Chan, Y. W., Jeyaprakash, A. A., Nigg, E. A. and Santamaria, A. (2012). Aurora B controls kinetochore-microtubule attachments by inhibiting Ska complex-KMN network interaction. J. Cell Biol. 196, 563-571.
21. Cheerambathur, D. K. and Desai, A. (2014). Linked in: formation and regulation of microtubule attachments during chromosome segregation. Curr. Opin. Cell Biol. 26, 113-122.
22. Cheerambathur, D. K., Gassmann, R., Cook, B., Oegema, K. and Desai, A. (2013). Crosstalk between microtubule attachment complexes ensures accurate chromosome segregation. Science 342, 1239-1242.
23. Cheeseman, I. M. (2014). The kinetochore. Cold Spring Harbor perspectives in biology 6, a015826.
24. Cheeseman, I. M. and Desai, A. (2008). Molecular architecture of the kinetochore-microtubule interface. Nat. Rev. Mol. Cell Biol. 9, 33-46.
25. Cheeseman, I. M., Enquist-Newman, M., Müller-Reichert, T., Drubin, D. G. and Barnes, G. (2001). Mitotic spindle integrity and kinetochore function linked by the Duo1p/Dam1p complex. J. Cell Biol. 152, 197-212.
26. 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, 4213-4225.
27. Cross, R. A. and McAinsh, A. (2014). Prime movers: the mechanochemistry of mitotic kinesins. Nat. Rev. Mol. Cell Biol. 15, 257-271.
28. Czaban, B. B., Forer, A. and Bajer, A. S. (1993). Ultraviolet microbeam irradiation of chromosomal spindle fibres in Haemanthus katherinae endosperm I. Behaviour of the irradiated region. J. Cell Sci. 105, 571-578.
29. Czechanski, A., Kim, H., Byers, C., Greenstein, I., Stumpff, J. and Reinholdt, L. G. (2015). Kif18a is specifically required for mitotic progression during germ line development. Dev. Biol. 402, 253-262.
30. Darlington, C. D. (1937). Recent Advances in Cytology. 2nd edn. Philadelphia: Blackston Co.
31. Daum, J. R., Wren, J. D., Daniel, J. J., Sivakumar, S., McAvoy, J. N., Potapova, T. A. and Gorbsky, G. J. (2009). Ska3 is required for spindle checkpoint silencing and the maintenance of chromosome cohesion in mitosis. Curr. Biol. 19, 1467-1472.
32. Desai, A. and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
33. De Wulf, P., McAinsh, A. D. and Sorger, P. K. (2003). Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes & development 17, 2902-2921.
34. Du, Y., English, C. A. and Ohi, R. (2010). The kinesin-8 Kif18A dampens microtubule plus-end dynamics. Curr. Biol. 20, 374-380.
35. Dumont, S., Salmon, E. D. and Mitchison, T. J. (2012). Deformations within moving kinetochores reveal different sites of active and passive force generation. Science 337, 355-358.
36. Ems-McClung, S. C., Hainline, S. G., Devare, J., Zong, H., Cai, S., Carnes, S. K., Shaw, S. L. and Walczak, C. E. (2013). Aurora B inhibits MCAK activity through a phosphoconformational switch that reduces microtubule association. Curr. Biol. 23, 2491-2499.
37. Feng, J., Huang, H. and Yen, T. J. (2006). CENP-F is a novel microtubule-binding protein that is essential for kinetochore attachments and affects the duration of the mitotic checkpoint delay. Chromosoma 115, 320-329.
38. Ferreira, J. G., Pereira, A. L. and Maiato, H. (2014). Microtubule plus-end tracking proteins and their roles in cell division. Int. Rev. Cell Mol. Biol. 309, 59-140.
39. Foley, E. A. and Kapoor, T. M. (2013). Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol. 14, 25-37.
40. Funabiki, H. and Murray, A. W. (2000). The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell 102, 411-424.
41. Gaitanos, T. N., Santamaria, A., Jeyaprakash, A. A., Wang, B., Conti, E. and Nigg, E. A. (2009). Stable kinetochore-microtubule interactions depend on the Ska complex and its new component Ska3/C13Orf3. EMBO J. 28, 1442-1452.
42. Ganem, N. J., Upton, K. and Compton, D. A. (2005). Efficient mitosis in human cells lacking poleward microtubule flux. Curr. Biol. 15, 1827-1832.
43. Godek, K. M., Kabeche, L. and Compton, D. A. (2015). Regulation of kinetochore-microtubule attachments through homeostatic control during mitosis. Nat. Rev. Mol. Cell Biol. 16, 57-64.
44. Gorbsky, G. J., Sammak, P. J. and Borisy, G. G. (1987). Chromosomes move poleward in anaphase along stationary microtubules that coordinately disassemble from their kinetochore ends. J. Cell Biol. 104, 9-18.
45. Grishchuk, E. L., Molodtsov, M. I., Ataullakhanov, F. I. and McIntosh, J. R. (2005). Force production by disassembling microtubules. Nature 438, 384-388.
46. Grishchuk, E. L., Spiridonov, I. S., Volkov, V. A., Efremov, A., Westermann, S., Drubin, D., Barnes, G., Ataullakhanov, F. I. and McIntosh, J. R. (2008). Different assemblies of the DAM1 complex follow shortening microtubules by distinct mechanisms. Proc. Natl. Acad. Sci. USA 105, 6918-6923.
47. Gudimchuk, N., Vitre, B., Kim, Y., Kiyatkin, A., Cleveland, D. W., Ataullakhanov, F. I. and Grishchuk, E. L. (2013). Kinetochore kinesin CENP-E is a processive bidirectional tracker of dynamic microtubule tips. Nat. Cell Biol. 15, 1079-1088.
48. Hanisch, A., Silljé, H. H. W. and Nigg, E. A. (2006). Timely anaphase onset requires a novel spindle and kinetochore complex comprising Ska1 and Ska2. EMBO J. 25, 5504-5515.
49. Hays, T. S. and Salmon, E. D. (1990). Poleward force at the kinetochore in metaphase depends on the number of kinetochore microtubules. J. Cell Biol. 110, 391-404.
50. Hays, T. S., Wise, D. and Salmon, E. D. (1982). Traction force on a kinetochore at metaphase acts as a linear function of kinetochore fiber length. J. Cell Biol. 93, 374-382.
51. Hill, T. L. (1985). Theoretical problems related to the attachment of microtubules to kinetochores. Proc. Natl. Acad. Sci. USA 82, 4404-4408.
52. Hochegger, H., Hegarat, N. and Pereira-Leal, J. B. (2013). Aurora at the pole and equator: overlapping functions of Aurora kinases in the mitotic spindle. Open Biol. 3, 120185.
53. Holt, S. V., Vergnolle, M. A. S., Hussein, D., Wozniak, M. J., Allan, V. J. and Taylor, S. S. (2005). Silencing Cenp-F weakens centromeric cohesion, prevents chromosome alignment and activates the spindle checkpoint. J. Cell Sci. 118, 4889-4900.
54. Honnappa, S., Gouveia, S. M., Weisbrich, A., Damberger, F. F., Bhavesh, N. S., Jawhari, H., Grigoriev, I., van Rijssel, F. J. A., Buey, R. M., Lawera, A. et al. (2009). An EB1-binding motif acts as a microtubule tip localization signal. Cell 138, 366-376.
55. Hori, T., Okada, M., Maenaka, K. and Fukagawa, T. (2008). CENP-O class proteins form a stable complex and are required for proper kinetochore function. Mol. Biol. Cell 19, 843-854.
56. 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.
57. Iemura, K. and Tanaka, K. (2015). Chromokinesin Kid and kinetochore kinesin CENP-E differentially support chromosome congression without end-on attachment to microtubules. Nat. Commun. 6, 6447.
58. Jaqaman, K., King, E. M., Amaro, A. C., Winter, J. R., Dorn, J. F., Elliott, H. L., McHedlishvili, N., McClelland, S. E., Porter, I. M., Posch, M. et al. (2010). Kinetochore alignment within the metaphase plate is regulated by centromere stiffness and microtubule depolymerases. J. Cell Biol. 188, 665-679.
59. Jeyaprakash, A. A., Santamaria, A., Jayachandran, U., Chan, Y. W., Benda, C., Nigg, E. A. and Conti, E. (2012). Structural and functional organization of the Ska complex, a key component of the kinetochore-microtubule interface. Mol. Cell 46, 274-286.
60. Johnston, K., Joglekar, A., Hori, T., Suzuki, A., Fukagawa, T. and Salmon, E. D. (2010). Vertebrate kinetochore protein architecture: protein copy number. J. Cell Biol. 189, 937-943.
61. Kapoor, T. M., Lampson, M. A., Hergert, P., Cameron, L., Cimini, D., Salmon, E. D., McEwen, B. F. and Khodjakov, A. (2006). Chromosomes can congress to the metaphase plate before biorientation. Science 311, 388-391.
62. Kettenbach, A. N., Schweppe, D. K., Faherty, B. K., Pechenick, D., Pletnev, A. A. and Gerber, S. A. (2011). Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-Like kinase activities in mitotic cells. Sci. Signal. 4, rs5.
63. Khodjakov, A. and Rieder, C. L. (1996). Kinetochores moving away from their associated pole do not exert a significant pushing force on the chromosome. J. Cell Biol. 135, 315-327.
64. 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.
65. Khodjakov, A., Gabashvili, I. S. and Rieder, C. L. (1999). "Dumb" versus "Smart" kinetochore models for chromosome congression during mitosis in vertebrate somatic cells. Cell Motil. Cytoskeleton 43, 179-185.
66. Kim, Y., Heuser, J. E., Waterman, C. M. and Cleveland, D. W. (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.
67. Kim, Y., Holland, A. J., Lan, W. and Cleveland, D. W. (2010). Aurora kinases and protein phosphatase 1 mediate chromosome congression through regulation of CENP-E. Cell 142, 444-455.
68. Kiyomitsu, T. and Cheeseman, I. M. (2012). Chromosome-and spindle-polederived signals generate an intrinsic code for spindle position and orientation. Nat. Cell Biol. 14, 311-317.
69. Kline-Smith, S. L., Khodjakov, A., Hergert, P. and Walczak, C. E. (2004). Depletion of centromeric MCAK leads to chromosome congression and segregation defects due to improper kinetochore attachments. Mol. Biol. Cell 15, 1146-1159.
70. Lampert, F., Hornung, P. and Westermann, S. (2010). The Dam1 complex confers microtubule plus end-tracking activity to the Ndc80 kinetochore complex. J. Cell Biol. 189, 641-649.
71. Lampson, M. A. and Cheeseman, I. M. (2011). Sensing centromere tension: Aurora B and the regulation of kinetochore function. Trends Cell Biol. 21, 133-140.
72. Levesque, A. A. and Compton, D. A. (2001). The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles. J. Cell Biol. 154, 1135-1146.
73. Li, Y., Yu, W., Liang, Y. and Zhu, X. (2007). Kinetochore dynein generates a poleward pulling force to facilitate congression and full chromosome alignment. Cell Res. 17, 701-712.
74. Liu, X.-S., Zhao, X.-D., Wang, X., Yao, Y.-X., Zhang, L.-L., Shu, R.-Z., Ren, W.-H., Huang, Y., Huang, L., Gu, M.-M. et al. (2010). Germinal cell aplasia in Kif18a mutant male mice due to impaired chromosome congression and dysregulated BubR1 and CENP-E. Genes Cancer 1, 26-39.
75. Maffini, S., Maia, A. R. R., Manning, A. L., Maliga, Z., Pereira, A. L., Junqueira, M., Shevchenko, A., Hyman, A., Yates, J. R., III, Galjart, N. et al. (2009). Motorindependent targeting of CLASPs to kinetochores by CENP-E promotes microtubule turnover and poleward flux. Curr. Biol. 19, 1566-1572.
76. Magidson, V., O'Connell, C. B., Lončarek, J., Paul, R., Mogilner, A. and Khodjakov, A. (2011). The spatial arrangement of chromosomes during prometaphase facilitates spindle assembly. Cell 146, 555-567.
77. Magidson, V., Paul, R., Yang, N., Ault, J. G., O'Connell, C. B., Tikhonenko, I., McEwen, B. F., Mogilner, A. and Khodjakov, A. (2015). Adaptive changes in the kinetochore architecture facilitate proper spindle assembly. Nat. Cell Biol., (in press). doi:10.1038/ncb3223.
78. Mayr, M. I., Hümmer, S., Bormann, J., Grüner, T., Adio, S., Woehlke, G. and Mayer, T. U. (2007). The human kinesin Kif18A is a motile microtubule depolymerase essential for chromosome congression. Curr. Biol. 17, 488-498.
79. Mazumdar, M., Sundareshan, S. and Misteli, T. (2004). Human chromokinesin KIF4A functions in chromosome condensation and segregation. J. Cell Biol. 166, 613-620.
80. McIntosh, J. R., Grishchuk, E. L., Morphew, M. K., Efremov, A. K., Zhudenkov, K., Volkov, V. A., Cheeseman, I. M., Desai, A., Mastronarde, D. N. and Ataullakhanov, F. I. (2008). Fibrils connect microtubule tips with kinetochores: a mechanism to couple tubulin dynamics to chromosome motion. Cell 135, 322-333.
81. Miller, S. A., Johnson, M. L. and Stukenberg, P. T. (2008). Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80Hec1. Curr. Biol. 18, 1785-1791.
82. Miranda, J. J. L., De Wulf, P., Sorger, P. K. and Harrison, S. C. (2005). The yeast DASH complex forms closed rings on microtubules. Nat. Struct. Mol. Biol. 12, 138-143.
83. Mitchison, T. J. (1989). Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence. J. Cell Biol. 109, 637-652.
84. Mitchison, T. J. and Salmon, E. D. (1992). Poleward kinetochore fiber movement occurs during both metaphase and anaphase-A in newt lung cell mitosis. J. Cell Biol. 119, 569-582.
85. Mitchison, T., Evans, L., Schulze, E. and Kirschner, M. (1986). Sites of microtubule assembly and disassembly in the mitotic spindle. Cell 45, 515-527.
86. Nicklas, R. B. (1988). The forces that move chromosomes in mitosis. Annu. Rev. Biophys. Chem. 17, 431-449.
87. Nunes Bastos, R., Gandhi, S. R., Baron, R. D., Gruneberg, U., Nigg, E. A. and Barr, F. A. (2013). Aurora B suppresses microtubule dynamics and limits central spindle size by locally activating KIF4A. J. Cell Biol. 202, 605-621.
88. Oguchi, Y., Uchimura, S., Ohki, T., Mikhailenko, S. V. and Ishiwata, S. (2011). The bidirectional depolymerizer MCAK generates force by disassembling both microtubule ends. Nat. Cell Biol. 13, 846-852.
89. Östergren, G. (1945). Equilibrium of trivalents and the mechanism of chromosome movements. Hereditas 31, 498.
90. Östergren, G. (1951). The mechanism of co-orientation in bivalents and multivalents. The theory of orientation by pulling. Hereditas 37, 85-156.
91. Park, C. H., Park, J.-E., Kim, T.-S., Kang, Y. H., Soung, N. K., Zhou, M., Kim, N.-H., Bang, J. K. and Lee, K. S. (2015). Mammalian Polo-like Kinase 1 (Plk1) promotes proper chromosome segregation by phosphorylating and delocalizing the PBIP1-CENP-Q complex from kinetochores. J. Biol. Chem. 290, 8569-8581.
92. Pereira, A. J. and Maiato, H. (2012). Maturation of the kinetochore-microtubule interface and the meaning of metaphase. Chromosome Res. 20, 563-577.
93. Powers, A. F., Franck, A. D., Gestaut, D. R., Cooper, J., Gracyzk, B., Wei, R. R., Wordeman, L., Davis, T. N. and Asbury, C. L. (2009). The Ndc80 kinetochore complex forms load-bearing attachments to dynamic microtubule tips via biased diffusion. Cell 136, 865-875.
94. Rieder, C. L., Davison, E. A., Jensen, L. C., Cassimeris, L. and Salmon, E. D. (1986). Oscillatory movements of monooriented chromosomes and their position relative to the spindle pole result from the ejection properties of the aster and halfspindle. J. Cell Biol. 103, 581-591.
95. Rogers, G. C., Rogers, S. L., Schwimmer, T. A., Ems-McClung, S. C., Walczak, C. E., Vale, R. D., Scholey, J. M. and Sharp, D. J. (2004). Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature 427, 364-370.
96. Savoian, M. S., Goldberg, M. L. and Rieder, C. L. (2000). The rate of poleward chromosome motion is attenuated in Drosophila zw10 and rod mutants. Nat. Cell Biol. 2, 948-952.
97. Schmidt, J. C., Kiyomitsu, T., Hori, T., Backer, C. B., Fukagawa, T. and Cheeseman, I. M. (2010). Aurora B kinase controls the targeting of the AstrinSKAP complex to bioriented kinetochores. J. Cell Biol. 191, 269-280.
98. Schmidt, J. C., Arthanari, H., Boeszoermenyi, A., Dashkevich, N. M., WilsonKubalek, E. M., Monnier, N., Markus, M., Oberer, M., Milligan, R. A., Bathe, M. et al. (2012). The kinetochore-bound Ska1 complex tracks depolymerizing microtubules and binds to curved protofilaments. Dev. Cell 23, 968-980.
99. Shelden, E. and Wadsworth, P. (1992). Microinjection of biotin-tubulin into anaphase cells induces transient elongation of kinetochore microtubules and reversal of chromosome-to-pole motion. J. Cell Biol. 116, 1409-1420.
100. Shrestha, R. L. and Draviam, V. M. (2013). Lateral to end-on conversion of chromosome-microtubule attachment requires kinesins CENP-E and MCAK. Curr. Biol. 23, 1514-1526.
101. Simon, J. R. and Salmon, E. D. (1990). The structure of microtubule ends during the elongation and shortening phases of dynamic instability examined by negative-stain electron microscopy. J. Cell Sci. 96, 571-582.
102. Sivakumar, S., Daum, J. R., Tipton, A. R., Rankin, S. and Gorbsky, G. J. (2014). The Spindle and Kinetochore-associated (Ska) complex enhances binding of the Anaphase-Promoting Complex/Cyclosome (APC/C) to chromosomes and promotes mitotic exit. Mol. Biol. Cell 25, 594-605.
103. 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.
104. Spurck, T. P., Stonington, O. G., Snyder, J. A., Pickett-Heaps, J. D., Bajer, A. and Mole-Bajer, J. (1990). UV microbeam irradiations of the mitotic spindle. II. Spindle fiber dynamics and force production. J. Cell Biol. 111, 1505-1518.
105. Stumpff, J., von Dassow, G., Wagenbach, M., Asbury, C. and Wordeman, L. (2008). The kinesin-8 motor Kif18A suppresses kinetochore movements to control mitotic chromosome alignment. Dev. Cell 14, 252-262.
106. Stumpff, J., Du, Y., English, C. A., Maliga, Z., Wagenbach, M., Asbury, C. L., Wordeman, L. and Ohi, R. (2011). A tethering mechanism controls the processivity and kinetochore-microtubule plus-end enrichment of the kinesin-8 Kif18A. Mol. Cell 43, 764-775.
107. Stumpff, J., Wagenbach, M., Franck, A., Asbury, C. L. and Wordeman, L. (2012). Kif18A and chromokinesins confine centromere movements via microtubule growth suppression and spatial control of kinetochore tension. Dev. Cell 22, 1017-1029.
108. Theis, M., Slabicki, M., Junqueira, M., Paszkowski-Rogacz, M., Sontheimer, J., Kittler, R., Heninger, A.-K., Glatter, T., Kruusmaa, K., Poser, I. et al. (2009). Comparative profiling identifies C13orf3 as a component of the Ska complex required for mammalian cell division. EMBO J. 28, 1453-1465.
109. Tien, J. F., Umbreit, N. T., Gestaut, D. R., Franck, A. D., Cooper, J., Wordeman, L., Gonen, T., Asbury, C. L. and Davis, T. N. (2010). Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B. J. Cell Biol. 189, 713-723.
110. Tirnauer, J. S., Canman, J. C., Salmon, E. D. and Mitchison, T. J. (2002). EB1 targets to kinetochores with attached, polymerizing microtubules. Mol. Biol. Cell 13, 4308-4316.
111. Tooley, J. G., Miller, S. A. and Stukenberg, P. T. (2011). The Ndc80 complex uses a tripartite attachment point to couple microtubule depolymerization to chromosome movement. Mol. Biol. Cell 22, 1217-1226.
112. Umbreit, N. T., Miller, M. P., Tien, J. F., Cattin Ortolá, J., Gui, L., Lee, K. K., Biggins, S., Asbury, C. L. and Davis, T. N. (2014). Kinetochores require oligomerization of Dam1 complex to maintain microtubule attachments against tension and promote biorientation. Nat. Commun. 5, 4951.
113. VandenBeldt, K. J., Barnard, R. M., Hergert, P. J., Meng, X., Maiato, H. and McEwen, B. F. (2006). Kinetochores use a novel mechanism for coordinating the dynamics of individual microtubules. Curr. Biol. 16, 1217-1223.
114. Vergnolle, M. A. S. and Taylor, S. S. (2007). Cenp-F links kinetochores to Ndel1/Nde1/Lis1/dynein microtubule motor complexes. Curr. Biol. 17, 1173-1179.
115. Vladimirou, E., Harry, E., Burroughs, N. and McAinsh, A. D. (2011). Springs, clutches and motors: driving forward kinetochore mechanism by modelling. Chromosome Res. 19, 409-421.
116. Volkov, V. A., Grissom, P. M., Arzhanik, V. K., Zaytsev, A. V., Renganathan, K., McClure-Begley, T., Old, W. M., Ahn, N. and McIntosh, J. R. (2015). Centromere protein F includes two sites that couple efficiently to depolymerizing microtubules. J. Cell Biol. 209, 813-828.
117. Wandke, C., Barisic, M., Sigl, R., Rauch, V., Wolf, F., Amaro, A. C., Tan, C. H., Pereira, A. J., Kutay, U., Maiato, H. et al. (2012). Human chromokinesins promote chromosome congression and spindle microtubule dynamics during mitosis. J. Cell Biol. 198, 847-863.
118. Welburn, J. P. I., Grishchuk, E. L., Backer, C. B., Wilson-Kubalek, E. M., Yates, J. R., 3rd and Cheeseman, I. M. (2009). The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev. Cell 16, 374-385.
119. Westermann, S., Avila-Sakar, A., Wang, H.-W., Niederstrasser, H., Wong, J., Drubin, D. G., Nogales, E. and Barnes, G. (2005). Formation of a dynamic kinetochore-microtubule interface through assembly of the Dam1 ring complex. Mol. Cell 17, 277-290.
120. Westhorpe, F. G. and Straight, A. F. (2013). Functions of the centromere and kinetochore in chromosome segregation. Curr. Opin. Cell Biol. 25, 334-340.
121. 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.
122. Wood, K. W., Sakowicz, R., Goldstein, L. S. B. and Cleveland, D. W. (1997). CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment. Cell 91, 357-366.
123. Wordeman, L., Wagenbach, M. and von Dassow, G. (2007). MCAK facilitates chromosome movement by promoting kinetochore microtubule turnover. J. Cell Biol. 179, 869-879.
124. Yajima, J., Edamatsu, M., Watai-Nishii, N., Tokai-Nishizumi, N., Yamamoto, T. and Toyoshima, Y. Y. (2003). The human chromokinesin Kid is a plus enddirected microtubule-based motor. EMBO J. 22, 1067-1074.
125. Yang, Z., Guo, J., Chen, Q., Ding, C., Du, J. and Zhu, X. (2005). Silencing mitosin induces misaligned chromosomes, premature chromosome decondensation before anaphase onset, and mitotic cell death. Mol. Cell. Biol. 25, 4062-4074.
126. Yang, Z., Tulu, U. S., Wadsworth, P. and Rieder, C. L. (2007). Kinetochore dynein is required for chromosome motion and congression independent of the spindle checkpoint. Curr. Biol. 17, 973-980.
127. Ye, A. A., Deretic, J., Hoel, C. M., Hinman, A. W., Cimini, D., Welburn, J. P. and Maresca, T. J. (2015). Aurora A Kinase Contributes to a Pole-Based Error Correction Pathway. Curr. Biol. 25, 1842-1851.