Connecting the microtubule attachment status of each kinetochore to cell cycle arrest through the spindle assembly checkpoint

Chromosoma

Volumn 124, Issue 4, 2015, Pages 463-480

  Stukenberg, P Todd ^a   Burke, Daniel J ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Cell division; Chromosome segregation; Mitosis; Mitotic checkpoint

Indexed keywords

AURORA KINASE; PROTEIN MAD1;

CELL ADHESION; CELL CYCLE ARREST; CENTROMERE; CHROMOSOME; CHROMOSOME SEGREGATION; CYTOARCHITECTURE; DNA DAMAGE; HUMAN; M PHASE CELL CYCLE CHECKPOINT; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; PROMETAPHASE; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; EUKARYOTE; PHYSIOLOGY; SPINDLE APPARATUS;

ANIMALS; DNA DAMAGE; EUKARYOTA; HUMANS; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; MICROTUBULES; SPINDLE APPARATUS;

EID: 84949114021     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-015-0515-z     Document Type: Review

References (211)

1. Abrieu A, Magnaghi-Jaulin L, Kahana JA, Peter M, Castro A, Vigneron S, Lorca T, Cleveland DW, Labbe JC (2001) Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 106:83–93
2. Alushin GM, Musinipally V, Matson D, Tooley J, Stukenberg PT, Nogales E (2012) Multimodal microtubule binding by the Ndc80 kinetochore complex. Nat Struct Mol Biol 19:1161–1167
3. Amaro AC, Samora CP, Holtackers R, Wang E, Kingston IJ, Alonso M, Lampson M, McAinsh AD, Meraldi P (2010) Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nat Cell Biol 12:319–329
4. Bader JR, Kasuboski JM, Winding M, Vaughan PS, Hinchcliffe EH, Vaughan KT (2011) Polo-like kinase1 is required for recruitment of dynein to kinetochores during mitosis. J Biol Chem 286:20769–20777
5. Basilico F, Maffini S, Weir JR, Prumbaum D, Rojas AM, Zimniak T, De Antoni A, Jeganathan S, Voss B, van Gerwen S, Krenn V, Massimiliano L, Valencia A, Vetter IR, Herzog F, Raunser S, Pasqualato S, Musacchio A (2014) The pseudo GTPase CENP-M drives human kinetochore assembly. Elife 3:e02978
6. Basto R, Gomes R, Karess RE (2000) Rough deal and Zw10 are required for the metaphase checkpoint in Drosophila. Nat Cell Biol 2:939–943
7. Biggins S, Murray AW (2001) The budding yeast protein kinase Ipl1/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev 15:3118–3129
8. Biggins S, Severin FF, Bhalla N, Sassoon I, Hyman AA, Murray AW (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Dev 13:532–544
9. Bischoff JR, Anderson L, Zhu Y, Mossie K, Ng L, Souza B, Schryver B, Flanagan P, Clairvoyant F, Ginther C, Chan CS, Novotny M, Slamon DJ, Plowman GD (1998) A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J 17:3052–3065
10. Bolton M, Lan W, Powers S, McCleland M, Kuang J, Stukenberg P (2002) Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol Biol Cell 13(9):3064–3077
11. Boohaker RJ, Xu B (2014) The versatile functions of ATM kinase. Biomed J 37:3–9
12. Boyarchuk Y, Salic A, Dasso M, Arnaoutov A (2007) Bub1 is essential for assembly of the functional inner centromere. J Cell Biol 176:919–928
13. Buchler NE, Louis M (2008) Molecular titration and ultrasensitivity in regulatory networks. J Mol Biol 384:1106–1119
14. Buffin E, Lefebvre C, Huang J, Gagou ME, Karess RE (2005) Recruitment of Mad2 to the kinetochore requires the Rod/Zw10 complex. Curr Biol 15:856–861
15. Burke DJ, Stukenberg PT (2008) Linking kinetochore-microtubule binding to the spindle checkpoint. Dev Cell 14:474–479
16. Carmena M, Pinson X, Platani M, Salloum Z, Xu Z, Clark A, Macisaac F, Ogawa H, Eggert U, Glover DM, Archambault V, Earnshaw WC (2012) The chromosomal passenger complex activates Polo kinase at centromeres. PLoS Biol 10:e1001250
17. Chan GK, Jablonski SA, Starr DA, Goldberg ML, Yen TJ (2000) Human Zw10 and ROD are mitotic checkpoint proteins that bind to kinetochores. Nat Cell Biol 2:944–947
18. Chan YW, Jeyaprakash AA, Nigg EA, Santamaria A (2012) Aurora B controls kinetochore-microtubule attachments by inhibiting Ska complex-KMN network interaction. J Cell Biol 196:563–571
19. Chang L, Barford D (2014) Insights into the anaphase-promoting complex: a molecular machine that regulates mitosis. Curr Opin Struct Biol 29:1–9
20. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127:983–997
21. Chen RH, Waters JC, Salmon ED, Murray AW (1996) Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274:242–246
22. Chen RH, Murray AW, Waters JC (1998a) Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J Cell Biol 141:1193–1205
23. Chen RH, Shevchenko A, Mann M, Murray AW (1998b) Spindle checkpoint protein Xmad1 recruits Xmad2 to unattached kinetochores. J Cell Biol 143:283–295
24. Choi E, Lee H (2008) Chromosome damage in mitosis induces BubR1 activation and prometaphase arrest. FEBS Lett 582:1700–1706
25. Ciferri C, De Luca J, Monzani S, Ferrari KJ, Ristic D, Wyman C, Stark H, Kilmartin J, Salmon ED, Musacchio A (2005) Architecture of the human ndc80-hec1 complex, a critical constituent of the outer kinetochore. J Biol Chem 280:29088–29095
26. Ciferri C, Pasqualato S, Screpanti E, Varetti G, Santaguida S, Dos Reis G, Maiolica A, Polka J, De Luca JG, De Wulf P, Salek M, Rappsilber J, Moores CA, Salmon ED, Musacchio A (2008) Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133:427–439
27. Civril F, Musacchio A (2008) Spindly attachments. Genes Dev 22:2302–2307
28. Cohen-Fix O, Peters JM, Kirschner MW, Koshland D (1996) Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev 10:3081–3093
29. Compton DA, Szilak I, Cleveland DW (1992) Primary structure of NuMA, an intranuclear protein that defines a novel pathway for segregation of proteins at mitosis. J Cell Biol 116:1395–1408
30. Daum JR, Wren JD, Daniel JJ, Sivakumar S, McAvoy JN, Potapova TA, Gorbsky GJ (2009) Ska3 is required for spindle checkpoint silencing and the maintenance of chromosome cohesion in mitosis. Curr Biol 19:1467–1472
31. De Antoni A, Pearson CG, Cimini D, Canman JC, Sala V, Nezi L, Mapelli M, Sironi L, Faretta M, Salmon ED, Musacchio A (2005) The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr Biol 15:214–225
32. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED (2006) Kinetochore microtubule dynamics and attachment stability are regulated by Hec1. Cell 127:969–982
33. DeLuca KF, Lens SM, DeLuca JG (2011) Temporal changes in Hec1 phosphorylation control kinetochore-microtubule attachment stability during mitosis. J Cell Sci 124:622–634
34. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T, Mortlock A, Keen N, Taylor SS (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 161:267–280
35. Dotiwala F, Harrison JC, Jain S, Sugawara N, Haber JE (2010) Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism. Curr Biol 20:328–332
36. Earnshaw WC, Migeon BR (1985) Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92:290–296
37. Echeverri CJ, Paschal BM, Vaughan KT, Vallee RB (1996) Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J Cell Biol 132:617–633
38. Espert A, Uluocak P, Bastos RN, Mangat D, Graab P, Gruneberg U (2014) PP2A-B56 opposes Mps1 phosphorylation of Knl1 and thereby promotes spindle assembly checkpoint silencing. J Cell Biol 206:833–842
39. Espeut J, Cheerambathur DK, Krenning L, Oegema K, Desai A (2012) Microtubule binding by KNL-1 contributes to spindle checkpoint silencing at the kinetochore. J Cell Biol 196:469–482
40. Eytan E, Sitry-Shevah D, Teichner A, Hershko A (2013) Roles of different pools of the mitotic checkpoint complex and the mechanisms of their disassembly. Proc Natl Acad Sci U S A 110:10568–10573
41. Eytan E, Wang K, Miniowitz-Shemtov S, Sitry-Shevah D, Kaisari S, Yen TJ, Liu ST, Hershko A (2014) Disassembly of mitotic checkpoint complexes by the joint action of the AAA-ATPase TRIP13 and p31(comet). Proc Natl Acad Sci U S A 111:12019–12024
42. Famulski JK, Vos L, Sun X, Chan G (2008) Stable hZW10 kinetochore residency, mediated by hZwint-1 interaction, is essential for the mitotic checkpoint. J Cell Biol 180:507–520
43. Fang G, Yu H, Kirschner MW (1998a) The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev 12:1871–1883
44. Fang G, Yu H, Kirschner MW (1998b) Direct binding of CDC20 protein family members activates the anaphase-promoting complex in mitosis and G1. Mol Cell 2:163–171
45. Fava LL, Kaulich M, Nigg EA, Santamaria A (2011) Probing the in vivo function of Mad1:C-Mad2 in the spindle assembly checkpoint. EMBO J 30:3322–3336
46. Fisk HA, Winey M (2001) The mouse Mps1p-like kinase regulates centrosome duplication. Cell 106:95–104
47. Fisk HA, Mattison CP, Winey M (2003) Human Mps1 protein kinase is required for centrosome duplication and normal mitotic progression. Proc Natl Acad Sci U S A 100:14875–14880
48. Foley EA, Maldonado M, Kapoor TM (2011) Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase. Nat Cell Biol 13:1265–1271
49. Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR 3rd, Cleveland DW (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8:458–469
50. Fraschini R, Beretta A, Sironi L, Musacchio A, Lucchini G, Piatti S (2001) Bub3 interaction with Mad2, Mad3 and Cdc20 is mediated by WD40 repeats and does not require intact kinetochores. EMBO J 20:6648–6659
51. Gascoigne KE, Takeuchi K, Suzuki A, Hori T, Fukagawa T, Cheeseman IM (2011) Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145:410–422
52. Gassmann R, Holland AJ, Varma D, Wan X, Civril F, Cleveland DW, Oegema K, Salmon ED, Desai A (2010) Removal of Spindly from microtubule-attached kinetochores controls spindle checkpoint silencing in human cells. Genes Dev 24:957–971
53. Golsteyn RM, Mundt KE, Fry AM, Nigg EA (1995) Cell cycle regulation of the activity and subcellular localization of Plk1, a human protein kinase implicated in mitotic spindle function. J Cell Biol 129:1617–1628
54. Gorbsky GJ, Chen RH, Murray AW (1998) Microinjection of antibody to Mad2 protein into mammalian cells in mitosis induces premature anaphase. J Cell Biol 141:1193–1205
55. Goshima G, Nedelec F, Vale RD (2005) Mechanisms for focusing mitotic spindle poles by minus end-directed motor proteins. J Cell Biol 171:229–240
56. Grallert A, Boke E, Hagting A, Hodgson B, Connolly Y, Griffiths JR, Smith DL, Pines J, Hagan IM (2015) A PP1-PP2A phosphatase relay controls mitotic progression. Nature 517:94–98
57. Griffis ER, Stuurman N, Vale RD (2007) Spindly, a novel protein essential for silencing the spindle assembly checkpoint, recruits dynein to the kinetochore. J Cell Biol 177:1005–1015
58. Habu T, Kim SH, Weinstein J, Matsumoto T (2002) Identification of a MAD2-binding protein, CMT2, and its role in mitosis. EMBO J 21:6419–6428
59. Hanisch A, Sillje HH, Nigg EA (2006) Timely anaphase onset requires a novel spindle and kinetochore complex comprising Ska1 and Ska2. EMBO J 25:5504–5515
60. Hardwick KG, Johnston RC, Smith DL, Murray AW (2000) MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J Cell Biol 148:871–882
61. Hauf S, Cole RW, LaTerra S, Zimmer C, Schnapp G, Walter R, Heckel A, van Meel J, Rieder CL, Peters JM (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
62. Hayden JH, Bowser SS, Rieder CL (1990) Kinetochores capture astral microtubules during chromosome attachment to the mitotic spindle: direct visualization in live newt lung cells. J Cell Biol 111:1039–1045
63. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E (1996) Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 382:420–425
64. Heinrich S, Geissen EM, Kamenz J, Trautmann S, Widmer C, Drewe P, Knop M, Radde N, Hasenauer J, Hauf S (2013) Determinants of robustness in spindle assembly checkpoint signalling. Nat Cell Biol 15:1328–1339
65. Hewitt L, Tighe A, Santaguida S, White AM, Jones CD, Musacchio A, Green S, Taylor SS (2010) Sustained Mps1 activity is required in mitosis to recruit O-Mad2 to the Mad1-C-Mad2 core complex. J Cell Biol 190:25–34
66. Hoffman DB, Pearson CG, Yen TJ, Howell BJ, Salmon ED (2001) Microtubule-dependent changes in assembly of microtubule motor proteins and mitotic spindle checkpoint proteins at PtK1 kinetochores. Mol Biol Cell 12:1995–2009
67. Hori T, Amano M, Suzuki A, Backer CB, Welburn JP, Dong Y, McEwen BF, Shang WH, Suzuki E, Okawa K, Cheeseman IM, Fukagawa T (2008) CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135:1039–1052
68. Howell BJ, McEwen BF, Canman JC, Hoffman DB, Farrar EM, Rieder CL, Salmon ED (2001) Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 155:1159–1172
69. Hoyt MA, Totis L, Roberts BT (1991) S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66:507–517
70. Hsu KS, Toda T (2011) Ndc80 internal loop interacts with Dis1/TOG to ensure proper kinetochore-spindle attachment in fission yeast. Curr Biol 21:214–220
71. Huang H, Hittle J, Zappacosta F, Annan RS, Hershko A, Yen TJ (2008) Phosphorylation sites in BubR1 that regulate kinetochore attachment, tension, and mitotic exit. J Cell Biol 183:667–680
72. Hwang LH, Lau LF, Smith DL, Mistrot CA, Hardwick KG, Hwang ES, Amon A, Murray AW (1998) Budding yeast Cdc20: a target of the spindle checkpoint. Science 279:1041–1044
73. Irniger S, Piatti S, Michaelis C, Nasmyth K (1995) Genes involved in sister chromatid separation are needed for B-type cyclin proteolysis in budding yeast [published erratum appears in Cell 1998 May 1;93(3):487]. Cell 81:269–278
74. Izuta H, Ikeno M, Suzuki N, Tomonaga T, Nozaki N, Obuse C, Kisu Y, Goshima N, Nomura F, Nomura N, Yoda K (2006) Comprehensive analysis of the ICEN (Interphase Centromere Complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11:673–684
75. Jablonski SA, Chan GK, Cooke CA, Earnshaw WC, Yen TJ (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
76. Jablonski SA, Starr DA, Goldberg ML, Yen TJ (2000) Nat Cell Biol 2:944–947
77. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461:1071–1078
78. Jelluma N, Brenkman AB, van den Broek NJ, Cruijsen CW, van Osch MH, Lens SM, Medema RH, Kops GJ (2008) Mps1 phosphorylates Borealin to control Aurora B activity and chromosome alignment. Cell 132:233–246
79. Jeyaprakash AA, Santamaria A, Jayachandran U, Chan YW, Benda C, Nigg EA, Conti E (2012) Structural and functional organization of the ska complex, a key component of the kinetochore-microtubule interface. Mol Cell 46:274–286
80. Joglekar AP, Bouck D, Finley K, Liu X, Wan Y, Berman J, He X, Salmon ED, Bloom KS (2008a) Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J Cell Biol 181:587–594
81. Joglekar AP, Salmon ED, Bloom KS (2008b) Counting kinetochore protein numbers in budding yeast using genetically encoded fluorescent proteins. Methods Cell Biol 85:127–151
82. Kallio MJ, McCleland ML, Stukenberg PT, Gorbsky GJ (2002) Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr Biol 12:900–905
83. Kang YH, Park JE, Yu LR, Soung NK, Yun SM, Bang JK, Seong YS, Yu H, Garfield S, Veenstra TD, Lee KS (2006) Self-regulated Plk1 recruitment to kinetochores by the Plk1-PBIP1 interaction is critical for proper chromosome segregation. Mol Cell 24:409–422
84. Kang YH, Park CH, Kim TS, Soung NK, Bang JK, Kim BY, Park JE, Lee KS (2011) Mammalian polo-like kinase 1-dependent regulation of the PBIP1-CENP-Q complex at kinetochores. J Biol Chem 286:19744–19757
85. Kapoor TM, Mayer TU, Coughlin ML, Mitchison TJ (2000) Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J Cell Biol 150:975–988
86. Kapoor TM, Lampson MA, Hergert P, Cameron L, Cimini D, Salmon ED, McEwen BF, Khodjakov A (2006) Chromosomes can congress to the metaphase plate before biorientation. Science 311:388–391
87. Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432:316–323
88. Kasuboski JM, Bader JR, Vaughan PS, Tauhata SB, Winding M, Morrissey MA, Joyce MV, Boggess W, Vos L, Chan GK, Hinchcliffe EH, Vaughan KT (2011) Zwint-1 is a novel Aurora B substrate required for the assembly of a dynein-binding platform on kinetochores. Mol Biol Cell 22:3318–3330
89. Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y (2010) Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327:172–177
90. Khodjakov A, Copenagle L, Gordon MB, Compton DA, Kapoor TM (2003) Minus-end capture of preformed kinetochore fibers contributes to spindle morphogenesis. J Cell Biol 160:671–683
91. Kim EM, Burke DJ (2008) DNA damage activates the SAC in an ATM/ATR-dependent manner, independently of the kinetochore. PLoS Genet 4:e1000015
92. Kim S, Yu H (2015) Multiple assembly mechanisms anchor the KMN spindle checkpoint platform at human mitotic kinetochores. J Cell Biol 208:181–196
93. Kim SH, Lin DP, Matsumoto S, Kitazono A, Matsumoto T (1998) Fission yeast Slp1: an effector of the Mad2-dependent spindle checkpoint. Science 279:1045–1047
94. King RW, Peters JM, Tugendreich S, Rolfe M, Hieter P, Kirschner MW (1995) A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. Cell 81:279–288
95. Kitamura E, Tanaka K, Komoto S, Kitamura Y, Antony C, Tanaka TU (2010) Kinetochores generate microtubules with distal plus ends: their roles and limited lifetime in mitosis. Dev Cell 18:248–259
96. Kiyomitsu T, Obuse C, Yanagida M (2007) Human Blinkin/AF15q14 is required for chromosome alignment and the mitotic checkpoint through direct interaction with Bub1 and BubR1. Dev Cell 13:663–676
97. Kops GJ, Shah JV (2012) Connecting up and clearing out: how kinetochore attachment silences the spindle assembly checkpoint. Chromosoma 121:509–525
98. Kops GJ, Kim Y, Weaver BA, Mao Y, McLeod I, Yates JR 3rd, Tagaya M, Cleveland DW (2005) ZW10 links mitotic checkpoint signaling to the structural kinetochore. J Cell Biol 169:49–60
99. Krenn V, Overlack K, Primorac I, van Gerwen S, Musacchio A (2014) KI motifs of human Knl1 enhance assembly of comprehensive spindle checkpoint complexes around MELT repeats. Curr Biol 24:29–39
100. Kruse T, Zhang G, Larsen MS, Lischetti T, Streicher W, Kragh Nielsen T, Bjorn SP, Nilsson J (2013) Direct binding between BubR1 and B56-PP2A phosphatase complexes regulate mitotic progression. J Cell Sci 126:1086–1092
101. Kwiatkowski N, Jelluma N, Filippakopoulos P, Soundararajan M, Manak MS, Kwon M, Choi HG, Sim T, Deveraux QL, Rottmann S, Pellman D, Shah JV, Kops GJ, Knapp S, Gray NS (2010) Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat Chem Biol 6:359–368
102. Lawrimore J, Bloom KS, Salmon ED (2011) Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J Cell Biol 195:573–582
103. Lenart P, Petronczki M, Steegmaier M, Di Fiore B, Lipp JJ, Hoffmann M, Rettig WJ, Kraut N, Peters JM (2007) The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr Biol 17:304–315
104. Li Y, Benezra R (1996) Identification of a human mitotic checkpoint gene: hsMAD2. Science 274:246–248
105. Li R, Murray AW (1991) Feedback control of mitosis in budding yeast. Cell 66:519–531
106. Liu ST, Chan GK, Hittle JC, Fujii G, Lees E, Yen TJ (2003a) Human MPS1 kinase is required for mitotic arrest induced by the loss of CENP-E from kinetochores. Mol Biol Cell 14:1638–1651
107. Liu ST, Hittle JC, Jablonski SA, Campbell MS, Yoda K, Yen TJ (2003b) Human CENP-I specifies localization of CENP-F, MAD1 and MAD2 to kinetochores and is essential for mitosis. Nat Cell Biol 5:341–345
108. Liu D, Vader G, Vromans MJ, Lampson MA, Lens SM (2009) Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323:1350–1353
109. Liu D, Vleugel M, Backer CB, Hori T, Fukagawa T, Cheeseman IM, Lampson MA (2010) Regulated targeting of protein phosphatase 1 to the outer kinetochore by KNL1 opposes Aurora B kinase. J Cell Biol 188:809–820
110. London N, Biggins S (2014) Mad1 kinetochore recruitment by Mps1-mediated phosphorylation of Bub1 signals the spindle checkpoint. Genes Dev 28:140–152
111. London N, Ceto S, Ranish JA, Biggins S (2012) Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores. Curr Biol 22:900–906
112. Luo X, Fang G, Coldiron M, Lin Y, Yu H, Kirschner MW, Wagner G (2000) Structure of the Mad2 spindle assembly checkpoint protein and its interaction with Cdc20. Nat Struct Biol 7:224–229
113. Luo X, Tang Z, Rizo J, Yu H (2002) The Mad2 spindle checkpoint protein undergoes similar major conformational changes upon binding to either Mad1 or Cdc20. Mol Cell 9:59–71
114. Luo X, Tang Z, Xia G, Wassmann K, Matsumoto T, Rizo J, Yu H (2004) The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat Struct Mol Biol 11:338–345
115. Maciejowski J, George KA, Terret ME, Zhang C, Shokat KM, Jallepalli PV (2010) Mps1 directs the assembly of Cdc20 inhibitory complexes during interphase and mitosis to control M phase timing and spindle checkpoint signaling. J Cell Biol 190:89–100
116. Magidson V, O’Connell CB, Loncarek J, Paul R, Mogilner A, Khodjakov A (2011) The spatial arrangement of chromosomes during prometaphase facilitates spindle assembly. Cell 146:555–567
117. Maldonado M, Kapoor TM (2011) Constitutive Mad1 targeting to kinetochores uncouples checkpoint signalling from chromosome biorientation. Nat Cell Biol 13:475–482
118. Mapelli M, Filipp FV, Rancati G, Massimiliano L, Nezi L, Stier G, Hagan RS, Confalonieri S, Piatti S, Sattler M, Musacchio A (2006) Determinants of conformational dimerization of Mad2 and its inhibition by p31comet. EMBO J 25:1273–1284
119. Maresca TJ, Salmon ED (2009) Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J Cell Biol 184:373–381
120. Mariani L, Chiroli E, Nezi L, Muller H, Piatti S, Musacchio A, Ciliberto A (2012) Role of the Mad2 dimerization interface in the spindle assembly checkpoint independent of kinetochores. Curr Biol 22:1900–1908
121. Martin-Lluesma S, Stucke VM, Nigg EA (2002) Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science 297:2267–2270
122. Matson DR, Stukenberg PT (2012) Cdt1 throws kinetochore-microtubule attachments for a loop. Nat Cell Biol 14:561–563
123. Matson DR, Stukenberg PT (2014) CENP-I and Aurora B act as a molecular switch that ties RZZ/Mad1 recruitment to kinetochore attachment status. J Cell Biol 205:541–554
124. Matson DR, Demirel PB, Stukenberg PT, Burke DJ (2012) A conserved role for COMA/CENP-H/I/N kinetochore proteins in the spindle checkpoint. Genes Dev 26:542–547
125. Maure JF, Komoto S, Oku Y, Mino A, Pasqualato S, Natsume K, Clayton L, Musacchio A, Tanaka TU (2011) The Ndc80 loop region facilitates formation of kinetochore attachment to the dynamic microtubule plus end. Curr Biol 21:207–213
126. McCleland ML, Gardner RD, Kallio MJ, Daum JR, Gorbsky GJ, Burke DJ, Stukenberg PT (2003) The highly conserved Ndc80 complex is required for kinetochore assembly, chromosome congression, and spindle checkpoint activity. Genes Dev 17:101–114
127. McEwen BF, Chan GK, Zubrowski B, Savoian MS, Sauer MT, Yen TJ (2001) CENP-E is essential for reliable bioriented spindle attachment, but chromosome alignment can be achieved via redundant mechanisms in mammalian cells. Mol Biol Cell 12:2776–2789
128. McKenney RJ, Huynh W, Tanenbaum ME, Bhabha G, Vale RD (2014) Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science 345:337–341
129. Meraldi P, Draviam VM, Sorger PK (2004) Timing and checkpoints in the regulation of mitotic progression. Dev Cell 7:45–60
130. Miller SA, Johnson ML, Stukenberg PT (2008) Kinetochore attachments require an interaction between unstructured tails on microtubules and Ndc80(Hec1). Curr Biol 18:1785–1791
131. Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BM, Dasso M (2010) The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 12:164–169
132. Morrow CJ, Tighe A, Johnson VL, Scott MI, Ditchfield C, Taylor SS (2005) Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J Cell Sci 118:3639–3652
133. Moyle MW, Kim T, Hattersley N, Espeut J, Cheerambathur DK, Oegema K, Desai A (2014) A Bub1-Mad1 interaction targets the Mad1-Mad2 complex to unattached kinetochores to initiate the spindle checkpoint. J Cell Biol 204:647–657
134. Nam EA, Cortez D (2011) ATR signalling: more than meeting at the fork. Biochem J 436:527–536
135. Nijenhuis W, von Castelmur E, Littler D, De Marco V, Tromer E, Vleugel M, van Osch MH, Snel B, Perrakis A, Kops GJ (2013) A TPR domain-containing N-terminal module of MPS1 is required for its kinetochore localization by Aurora B. J Cell Biol 201:217–231
136. Nijenhuis W, Vallardi G, Teixeira A, Kops GJ, Saurin AT (2014) Negative feedback at kinetochores underlies a responsive spindle checkpoint signal. Nat Cell Biol 16:1257–1264
137. Nishino T, Takeuchi K, Gascoigne KE, Suzuki A, Hori T, Oyama T, Morikawa K, Cheeseman IM, Fukagawa T (2012) CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell 148:487–501
138. Obuse C, Yang H, Nozaki N, Goto S, Okazaki T, Yoda K (2004) Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localized with the centromeric region in interphase. Genes Cells 9:105–120
139. Ohta S, Bukowski-Wills JC, Sanchez-Pulido L, Alves Fde L, Wood L, Chen ZA, Platani M, Fischer L, Hudson DF, Ponting CP, Fukagawa T, Earnshaw WC, Rappsilber J (2010) The protein composition of mitotic chromosomes determined using multiclassifier combinatorial proteomics. Cell 142:810–821
140. Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX, Yates JR 3rd, Desai A, Fukagawa T (2006) The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat Cell Biol 8:446–457
141. Overlack K, Primorac I, Vleugel M, Krenn V, Maffini S, Hoffmann I, Kops GJ, Musacchio A (2015) A molecular basis for the differential roles of Bub1 and BubR1 in the spindle assembly checkpoint. Elife 4
142. Paul R, Wollman R, Silkworth WT, Nardi IK, Cimini D, Mogilner A (2009) Computer simulations predict that chromosome movements and rotations accelerate mitotic spindle assembly without compromising accuracy. Proc Natl Acad Sci U S A 106:15708–15713
143. Peddibhotla S, Rosen JM (2009) Chking and executing cell division to prevent genomic instability. Cell Cycle 8:2339–2342
144. Peddibhotla S, Lam MH, Gonzalez-Rimbau M, Rosen JM (2009) The DNA-damage effector checkpoint kinase 1 is essential for chromosome segregation and cytokinesis. Proc Natl Acad Sci U S A 106:5159–5164
145. Petrovic A, Pasqualato S, Dube P, Krenn V, Santaguida S, Cittaro D, Monzani S, Massimiliano L, Keller J, Tarricone A, Maiolica A, Stark H, Musacchio A (2010) The MIS12 complex is a protein interaction hub for outer kinetochore assembly. J Cell Biol 190:835–852
146. Pinsky BA, Kung C, Shokat KM, Biggins S (2006) The Ipl1-Aurora protein kinase activates the spindle checkpoint by creating unattached kinetochores. Nat Cell Biol 8:78–83
147. Pinsky BA, Nelson CR, Biggins S (2009) Protein phosphatase 1 regulates exit from the spindle checkpoint in budding yeast. Curr Biol 19:1182–1187
148. Poddar A, Stukenberg PT, Burke DJ (2005) Two complexes of spindle checkpoint proteins containing Cdc20 and Mad2 assemble during mitosis independently of the kinetochore in Saccharomyces cerevisiae. Eukaryot Cell 4:867–878
149. Primorac I, Weir JR, Chiroli E, Gross F, Hoffmann I, van Gerwen S, Ciliberto A, Musacchio A (2013) Bub3 reads phosphorylated MELT repeats to promote spindle assembly checkpoint signaling. Elife 2:e01030
150. Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J, Dadlez M, Glover DM (2011) CENP-C is a structural platform for kinetochore assembly. Curr Biol 21:399–405
151. Rago F, Gascoigne KE, Cheeseman IM (2015) Distinct organization and regulation of the outer kinetochore KMN network downstream of CENP-C and CENP-T. Curr Biol 25(5):671–677
152. Rieder CL, Borisy GG (1981) The attachment of kinetochores to the pro-metaphase spindle in PtK1 cells. Recovery from low temperature treatment. Chromosoma 82:693–716
153. Rodriguez-Bravo V, Maciejowski J, Corona J, Buch HK, Collin P, Kanemaki MT, Shah JV, Jallepalli PV (2014) Nuclear pores protect genome integrity by assembling a premitotic and Mad1-dependent anaphase inhibitor. Cell 156:1017–1031
154. Rosenberg JS, Cross FR, Funabiki H (2011) KNL1/Spc105 recruits PP1 to silence the spindle assembly checkpoint. Curr Biol 21:942–947
155. Sacristan C, Kops GJ (2015) Joined at the hip: kinetochores, microtubules, and spindle assembly checkpoint signaling. Trends Cell Biol 25(1):21–28
156. Santaguida S, Tighe A, D’Alise AM, Taylor SS, Musacchio A (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J Cell Biol 190:73–87
157. Santaguida S, Vernieri C, Villa F, Ciliberto A, Musacchio A (2011) Evidence that Aurora B is implicated in spindle checkpoint signalling independently of error correction. EMBO J 30:1508–1519
158. Saurin AT, van der Waal MS, Medema RH, Lens SM, Kops GJ (2011) Aurora B potentiates Mps1 activation to ensure rapid checkpoint establishment at the onset of mitosis. Nat Commun 2:316
159. Savoian MS, Goldberg ML, Rieder CL (2000) The rate of poleward chromosome motion is attenuated in Drosophila zw10 and rod mutants. Nat Cell Biol 2:948–952
160. Scaerou F, Starr DA, Piano F, Papoulas O, Karess RE, Goldberg ML (2001) The ZW10 and Rough Deal checkpoint proteins function together in a large, evolutionarily conserved complex targeted to the kinetochore. J Cell Sci 114:3103–3114
161. Schaar BT, Chan GK, Maddox P, Salmon ED, Yen TJ (1997) CENP-E function at kinetochores is essential for chromosome alignment. J Cell Biol 139:1373–1382
162. Schleiffer A, Maier M, Litos G, Lampert F, Hornung P, Mechtler K, Westermann S (2012) CENP-T proteins are conserved centromere receptors of the Ndc80 complex. Nat Cell Biol 14:604–613
163. Screpanti E, De Antoni A, Alushin GM, Petrovic A, Melis T, Nogales E, Musacchio A (2011) Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr Biol 21:391–398
164. Shepperd LA, Meadows JC, Sochaj AM, Lancaster TC, Zou J, Buttrick GJ, Rappsilber J, Hardwick KG, Millar JB (2012) Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint. Curr Biol 22:891–899
165. Shevchenko A, Mann M, Murray AW, Gorbsky GJ (1998) Microinjection of antibody to Mad2 protein into mammalian cells in mitosis induces premature anaphase. J Cell Biol 143:283–295
166. Sironi L, Mapelli M, Knapp S, De Antoni A, Jeang KT, Musacchio A (2002) Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a ‘safety belt’ binding mechanism for the spindle checkpoint. EMBO J 21:2496–2506
167. Starr DA, Saffery R, Li Z, Simpson AE, Choo KH, Yen TJ, Goldberg ML (2000) HZwint-1, a novel human kinetochore component that interacts with HZW10. J Cell Sci 113:1939–1950
168. Starr DA, Piano F, Papoulas O, Karess RE, Goldberg ML, Chan GK (2001) Human Zw10 and ROD are mitotic checkpoint proteins that bind to kinetochores. J Cell Sci 114:3103–3114
169. Stucke VM, Sillje HH, Arnaud L, Nigg EA (2002) Human Mps1 kinase is required for the spindle assembly checkpoint but not for centrosome duplication. EMBO J 21:1723–1732
170. Stukenberg PT, Foltz DR (2010) Kinetochores: orchestrating the chromosomal minuet. Curr Biol 20:R522–R525
171. Su TT (2011) Safeguarding genetic information in Drosophila. Chromosoma 120:547–555
172. Sudakin V, Chan GK, Yen TJ (2001) Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 154:925–936
173. Suijkerbuijk SJ, Vleugel M, Teixeira A, Kops GJ (2012) Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev Cell 23:745–755
174. Suzuki A, Badger BL, Wan X, DeLuca JG, Salmon ED (2014) The architecture of CCAN proteins creates a structural integrity to resist spindle forces and achieve proper intrakinetochore stretch. Dev Cell 30:717–730
175. Tai CY, Dujardin DL, Faulkner NE, Vallee RB (2002) Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. J Cell Biol 156:959–968
176. Takeuchi K, Nishino T, Mayanagi K, Horikoshi N, Osakabe A, Tachiwana H, Hori T, Kurumizaka H, Fukagawa T (2014) The centromeric nucleosome-like CENP-T-W-S-X complex induces positive supercoils into DNA. Nucleic Acids Res 42:1644–1655
177. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, Stark MJ, Nasmyth K (2002) Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108:317–329
178. Taylor SS, McKeon F (1997) Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell 89:727–735
179. Taylor SS, Ha E, McKeon F (1998) The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase. J Cell Biol 142:1–11
180. Taylor SS, Hussein D, Wang Y, Elderkin S, Morrow CJ (2001) Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells. J Cell Sci 114:4385–4395
181. Tooley JG, Miller SA, Stukenberg PT (2011) The Ndc80 complex employs a tripartite attachment point to couple microtubule depolymerization to chromosome movement. Mol Biol Cell 22(8):1217–1226
182. Uchida KS, Takagaki K, Kumada K, Hirayama Y, Noda T, Hirota T (2009) Kinetochore stretching inactivates the spindle assembly checkpoint. J Cell Biol 184:383–390
183. van der Waal MS, Saurin AT, Vromans MJ, Vleugel M, Wurzenberger C, Gerlich DW, Medema RH, Kops GJ, Lens SM (2012) Mps1 promotes rapid centromere accumulation of Aurora B. EMBO Rep 13:847–854
184. Vanoosthuyse V, Hardwick KG (2009) A novel protein phosphatase 1-dependent spindle checkpoint silencing mechanism. Curr Biol 19:1176–1181
185. Varma D, Chandrasekaran S, Sundin LJ, Reidy KT, Wan X, Chasse DA, Nevis KR, DeLuca JG, Salmon ED, Cook JG (2012) Recruitment of the human Cdt1 replication licensing protein by the loop domain of Hec1 is required for stable kinetochore-microtubule attachment. Nat Cell Biol 14:593–603
186. Vergnolle MA, Taylor SS (2007) Cenp-F links kinetochores to Ndel1/Nde1/Lis1/dynein microtubule motor complexes. Curr Biol 17:1173–1179
187. Vink M, Simonetta M, Transidico P, Ferrari K, Mapelli M, De Antoni A, Massimiliano L, Ciliberto A, Faretta M, Salmon ED, Musacchio A (2006) In vitro FRAP identifies the minimal requirements for Mad2 kinetochore dynamics. Curr Biol 16:755–766
188. Vleugel M, Tromer E, Omerzu M, Groenewold V, Nijenhuis W, Snel B, Kops GJ (2013) Arrayed BUB recruitment modules in the kinetochore scaffold KNL1 promote accurate chromosome segregation. J Cell Biol 203:943–955
189. Vorozhko VV, Emanuele MJ, Kallio MJ, Stukenberg PT, Gorbsky GJ (2008) Multiple mechanisms of chromosome movement in vertebrate cells mediated through the Ndc80 complex and dynein/dynactin. Chromosoma 117:169–179
190. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, Stukenberg PT, Gorbsky GJ, Higgins JM (2010) Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330:231–235
191. Wang K, Sturt-Gillespie B, Hittle JC, Macdonald D, Chan GK, Yen TJ, Liu ST (2014) Thyroid hormone receptor interacting protein 13 (TRIP13) AAA-ATPase is a novel mitotic checkpoint-silencing protein. J Biol Chem 289:23928–23937
192. Waters JC, Chen RH, Murray AW, Gorbsky GJ, Salmon ED, Nicklas RB (1999) Mad2 binding by phosphorylated kinetochores links error detection and checkpoint action in mitosis. Curr Biol 9:649–652
193. Wei RR, Al-Bassam J, Harrison SC (2007) The Ndc80/HEC1 complex is a contact point for kinetochore-microtubule attachment. Nat Struct Mol Biol 14:54–59
194. Weiss E, Winey M (1996) The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J Cell Biol 132:111–123
195. Welburn JP, Grishchuk EL, Backer CB, Wilson-Kubalek EM, Yates JR 3rd, Cheeseman IM (2009) The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev Cell 16:374–385
196. Westhorpe FG, Tighe A, Lara-Gonzalez P, Taylor SS (2011) p31comet-mediated extraction of Mad2 from the MCC promotes efficient mitotic exit. J Cell Sci 124:3905–3916
197. Wilde A, Lizarraga SB, Zhang L, Wiese C, Gliksman NR, Walczak CE, Zheng Y (2001) Ran stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nat Cell Biol 3:221–227
198. Williams BC, Li Z, Liu S, Williams EV, Leung G, Yen TJ, Goldberg ML (2003) Zwilch, a new component of the ZW10/ROD complex required for kinetochore functions. Mol Biol Cell 14:1379–1391
199. Xia G, Luo X, Habu T, Rizo J, Matsumoto T, Yu H (2004) Conformation-specific binding of p31(comet) antagonizes the function of Mad2 in the spindle checkpoint. EMBO J 23:3133–3143
200. Yamagishi Y, Honda T, Tanno Y, Watanabe Y (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330:239–243
201. Yamagishi Y, Yang CH, Tanno Y, Watanabe Y (2012) MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components. Nat Cell Biol 14:746–752
202. Yang M, Li B, Tomchick DR, Machius M, Rizo J, Yu H, Luo X (2007) p31comet blocks Mad2 activation through structural mimicry. Cell 131:744–755
203. Yang Y, Wu F, Ward T, Yan F, Wu Q, Wang Z, McGlothen T, Peng W, You T, Sun M, Cui T, Hu R, Dou Z, Zhu J, Xie W, Rao Z, Ding X, Yao X (2008) Phosphorylation of HsMis13 by Aurora B kinase is essential for assembly of functional kinetochore. J Biol Chem 283:26726–26736
204. Yang C, Tang X, Guo X, Niikura Y, Kitagawa K, Cui K, Wong ST, Fu L, Xu B (2011) Aurora-B mediated ATM serine 1403 phosphorylation is required for mitotic ATM activation and the spindle checkpoint. Mol Cell 44:597–608
205. Yang C, Wang H, Xu Y, Brinkman KL, Ishiyama H, Wong ST, Xu B (2012) The kinetochore protein Bub1 participates in the DNA damage response. DNA Repair 11:185–191
206. Yang C, Hao J, Kong D, Cui X, Zhang W, Wang H, Guo X, Ma S, Liu X, Pu P, Xu B (2014a) ATM-mediated Mad1 Serine 214 phosphorylation regulates Mad1 dimerization and the spindle assembly checkpoint. Carcinogenesis 35:2007–2013
207. Yang X, Xu W, Hu Z, Zhang Y, Xu N (2014b) Chk1 is required for the metaphase-anaphase transition via regulating the expression and localization of Cdc20 and Mad2. Life Sci 106:12–18
208. Yun M, Han YH, Yoon SH, Kim HY, Kim BY, Ju YJ, Kang CM, Jang SH, Chung HY, Lee SJ, Cho MH, Yoon G, Park GH, Kim SH, Lee KH (2009) p31comet induces cellular senescence through p21 accumulation and Mad2 disruption. Mol Cancer Res 7:371–382
209. Zachos G, Black EJ, Walker M, Scott MT, Vagnarelli P, Earnshaw WC, Gillespie DA (2007) Chk1 is required for spindle checkpoint function. Dev Cell 12:247–260
210. Zaytsev AV, Sundin LJ, DeLuca KF, Grishchuk EL, DeLuca JG (2014) Accurate phosphoregulation of kinetochore-microtubule affinity requires unconstrained molecular interactions. J Cell Biol 206:45–59
211. Zou H, McGarry TJ, Bernal T, Kirschner MW (1999) Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis [see comments]. Science 285:418–422