The spindle checkpoint: A quality control mechanism which ensures accurate chromosome segregation

Chromosome Research

Volumn 12, Issue 6, 2004, Pages 599-616

  Taylor, Stephen S ^a   Scott, Maria I F ^a   Holland, Andrew J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Checkpoint; Kinetochore; Meiosis; Microtubule; Mitosis

Indexed keywords

BUB1 RELATED PROTEIN; BUB3 PROTEIN; CELL CYCLE PROTEIN 20; CHROMOSOME PROTEIN; COHESIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN MAD1; PROTEIN MAD2; SEPARASE; UVOMORULIN; BUB1 SPINDLE CHECKPOINT PROTEIN; CALCIUM BINDING PROTEIN; CELL CYCLE PROTEIN; MAD2L1 PROTEIN, HUMAN; PROTEIN KINASE; REPRESSOR PROTEIN;

ANAPHASE; ARTICLE; CELL CYCLE; CENTROMERE; CHROMOSOME ANALYSIS; CHROMOSOME SEGREGATION; DYNAMICS; HUMAN; MEIOSIS; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; ANIMAL; GENETICS; METABOLISM; MOLECULAR GENETICS; NEOPLASM; PHYSIOLOGY; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; HUMANS; KINETOCHORES; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROTEIN KINASES; REPRESSOR PROTEINS;

EID: 10344241869     PISSN: 09673849     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:CHRO.0000036610.78380.51     Document Type: Article

References (128)

1. Abrieu A, Kahana JA, Wood KW, Cleveland DW (2000) CENP-E as an essential component of the mitotic checkpoint in vitro. Cell 102: 817-826.
2. Abrieu A, Magnaghi-Jaulin L, Kahana JA et al. (2001) Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 106: 83-93.
3. Amon A (1999) The spindle checkpoint. Curr Opin Genet Dev 9: 69-75.
4. Anand S, Penrhyn-Lowe S, Venkitaraman AR (2003) AURORA-A amplification overrides the mitotic spindle assembly checkpoint, inducing resistance to Taxol. Cancer Cell 3: 51-62.
5. Arnaoutov A, Dasso M (2003) The Ran GTPase regulates kinetochore function. Dev Cell 5: 99-111.
6. Babu JR, Jeganathan KB, Baker DJ, Wu X, Kang-Decker N, van Deursen JM (2003) Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J Cell Biol 160: 341-353.
7. Bailer SM, Siniossoglou S, Podtelejnikov A, Hellwig A, Mann M, Hurt E (1998) Nup116p and nup100p are interchangeable through a conserved motif which constitutes a docking site for the mRNA transport factor gle2p. Embo J 17: 1107-1119.
8. Basu J, Logarinho E, Herrmann S et al. (1998) Localization of the Drosophila checkpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod. Chromosoma 107: 376-385.
9. Belgareh N, Rabut G, Bai SW et al. (2001) An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J Cell Biol 154: 1147-1160.
10. Bernard P, Hardwick K, Javerzat JP (1998) Fission yeast bub1 is a mitotic centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis. J Cell Biol 143: 1775-1787.
11. Biggins S, Murray AW (2001) The budding yeast protein kinase Ip11/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev 15: 3118-3129.
12. Bischoff JR, Anderson L, Zhu Y et al. (1998) A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. Embo J 17: 3052-3065.
13. Cahill DP, Lengauer C, Yu J et al. (1998) Mutations of mitotic checkpoint genes in human cancers. Nature 392: 300-303.
14. Callan HG, Jacobs PA (1957) The meiotic process in Mantis religiosa L. males. J Genet 55: 200-217.
15. Campbell MS, Chan GK, Yen TJ (2001) Mitotic checkpoint proteins HsMAD1 and HsMAD2 are associated with nuclear pore complexes in interphase. J Cell Sci 114: 953-963.
16. Canman JC, Sharma N, Straight A, Shannon KB, Fang G, Salmon ED (2002) Anaphase onset does not require the microtubule-dependent depletion of kinetochore and centromere-binding proteins. J Cell Sci 115: 3787-3795.
17. Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP (2003) Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 116: 2987-2998.
18. Chan GK, Schaar BT, Yen TJ (1998) Characterization of the kinetochore binding domain of CENP-E reveals interactions with the kinetochore proteins CENP-F and hBUBR1. J Cell Biol 143: 49-63.
19. Chen RH (2002) BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1. J Cell Biol 158: 487-496.
20. Chen RH, Waters JC, Salmon ED, Murray AW (1996) Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274: 242-246.
21. Chen RH, Shevchenko A, Mann M, Murray AW (1998) Spindle checkpoint protein Xmad1 recruits Xmad2 to unattached kinetochores. J Cell Biol 143: 283-295.
22. Chung E, Chen RH (2003) Phosphorylation of Cdc20 is required for its inhibition by the spindle checkpoint. Nat Cell Biol 5: 748-753.
23. Ciosk R, Zachariae W, Michaelis C, Shevchenko A, Mann M, Nasmyth K (1998) An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93: 1067-1076.
24. Cleveland DW, Mao Y, Sullivan KF (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112: 407-421.
25. DeLuca JG, Howell BJ, Canman JC, Hickey JM, Fang G, Salmon ED (2003) Nuf2 and Hec1 are required for retention of the checkpoint proteins Mad1 and Mad2 to kinetochores. Curr Biol 13: 2103-2109.
26. Dewar H, Tanaka K, Nasmyth K, Tanaka TU (2004) Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle. Nature 428: 93-97.
27. Dikovskaya D, Newton IP, Nathke IS (2004) The adenomatous polyposis coli protein is required for the formation of robust spindles formed in CSF Xenopus extracts. Mol Biol Cell 15: 2978-2991.
28. Ditchfield C, Johnson VL, Tighe A et al. (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 161: 267-280.
29. Dobles M, Liberal V, Scott ML, Benezra R, Sorger PK (2000) Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101: 635-645.
30. Ewart-Toland A, Briassouli P, de Koning JP et al. (2003) Identification of Stk6/STK15 as a candidate low-penetrance tumor-susceptibility gene in mouse and human. Nat Genet 34: 403-412.
31. Fang G (2002) Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol Biol Cell 13: 755-766.
32. Fang G, Yu H, Kirschner MW (1998) 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.
33. Farr KA, Hoyt MA (1998) Bub1p kinase activates the Saccharomyces cerevisiae spindle assembly checkpoint. Mol Cell Biol 18: 2738-2747.
34. Farruggio DC, Townsley FM, Ruderman JV (1999) Cdc20 associates with the kinase aurora2/Aik. Proc Natl Acad Sci USA 96: 7306-7311.
35. Fisk HA, Winey M (2001) The mouse Mps1p-like kinase regulates centrosome duplication. Cell 106: 95-104.
36. Fisk HA, Mattison CP, Winey M (2003) Human Mps1 protein kinase is required for centrosome duplication and normal mitotic progression. Proc Natl Acad Sci USA 100: 14875-14880.
37. Fodde R, Kuipers J, Rosenberg C et al. (2001) Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 3: 433-438.
38. 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.
39. Gardner RD, Poddar A, Yellman C, Tavormina PA, Monteagudo MC, Burke DJ (2001) The spindle checkpoint of the yeast Saccharomyces cerevisiae requires kinetochore function and maps to the CBF3 domain. Genetics 157: 1493-1502.
40. Gillett ES, Espelin CW, Sorger PK (2004) Spindle checkpoint proteins and chromosome-microtubule attachment in budding yeast. J Cell Biol 164: 535-546.
41. Goh PY, Kilmartin JV (1993) NDC10: a gene involved in chromosome segregation in Saccharomyces cerevisiae. J Cell Biol 121: 503-512.
42. 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.
43. Green RA, Kaplan KB (2003) Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J Cell Biol 163: 949-961.
44. Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112: 765-777.
45. 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.
46. Haccard O, Sarcevic B, Lewellyn A et al. (1993) Induction of metaphase arrest in cleaving Xenopus embryos by MAP kinase. Science 262: 1262-1265.
47. Hardwick KG, Murray AW (1995) Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast. J Cell Biol 131: 709-720.
48. Hardwick KG, Weiss E, Luca FC, Winey M, Murray AW (1996) Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 273: 953-956.
49. 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.
50. Harrington EA, Bebbington D, Moore J et al. (2004) VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 10: 262-267.
51. Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure the order of cell cycle events. Science 246: 629-634.
52. Hauf S, Cole RW, LaTerra S et al. (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.
53. He X, Jones MH, Winey M, Sazer S (1998) Mph1, a member of the Mps1-like family of dual specificity protein kinases, is required for the spindle checkpoint in S. pombe. J Cell Sci 111 (Pt 12): 1635-1647.
54. Howell BJ, Hoffman DB, Fang G, Murray AW, Salmon ED (2000) Visualization of Mad2 dynamics at kinetochores, along spindle fibers, and at spindle poles in living cells. J Cell Biol 150: 1233-1250.
55. 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.
56. Hussein D, Taylor SS (2002) Farnesylation of Cenp-F is required for G2/M progression and degradation after mitosis. J Cell Sci 115: 3403-3414.
57. Hwang LH, Lau LF, Smith DL et al. (1998) Budding yeast Cdc20: a target of the spindle checkpoint. Science 279: 1041-1044.
58. 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.
59. Johnson VL, Scott MI, Holt SV, Hussein D, Taylor SS (2004) Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression. J Cell Sci 117: 1577-1589.
60. Joseph J, Liu ST, Jablonski SA, Yen TJ, Dasso M (2004) The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr Biol 14: 611-617.
61. Kalitsis P, Earle E, Fowler KJ, Choo KH (2000) Bub3 gene disruption in mice reveals essential mitotic spindle checkpoint function during early embryogenesis. Genes Dev 14: 2277-2282.
62. 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.
63. Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS (2001) A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 3: 429-432.
64. Karsenti E, Vernos I (2001) The mitotic spindle: a self-made machine. Science 294: 543-547.
65. Kelling J, Sullivan K, Wilson L, Jordan MA (2003) Suppression of centromere dynamics by Taxol in living osteosarcoma cells. Cancer Res 63: 2794-2801.
66. 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.
67. Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427: 510-517.
68. Lengauer C, Kinzler KW, Vogelstein B (1997) Genetic instability in colorectal cancers. Nature 386: 623-627.
69. Lens SM, Wolthuis RM, Klompmaker R et al. (2003) Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension. Embo J 22: 2934-2947.
70. Lew DJ, Burke DJ (2003) The spindle assembly and spindle position checkpoints. Annu Rev Genet 37: 251-282.
71. Li Y, Benezra R (1996) Identification of a human mitotic checkpoint gene: hsMAD2. Science 274: 246-248.
72. Li R, Murray AW (1991) Feedback control of mitosis in budding yeast. Cell 66: 519-531.
73. Li X, Nicklas RB (1995) Mitotic forces control a cell-cycle checkpoint. Nature 373: 630-632.
74. Li HY, Zheng Y (2004) Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev 18: 512-527.
75. Liao H, Winkfein RJ, Mack G, Rattner JB, Yen TJ (1995) CENP-F is a protein of the nuclear matrix that assembles onto kinetochores at late G2 and is rapidly degraded after mitosis. J Cell Biol 130: 507-518.
76. Mao Y, Abrieu A, Cleveland DW (2003) Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/inactivation of BubR1. Cell 114: 87-98.
77. 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.
78. McIntosh JR (1991) Structural and mechanical control of mitotic progression. Cold Spring Harb Symp Quant Biol 56: 613-619.
79. Michel LS, Liberal V, Chatterjee A et al. (2001) MAD2 haploinsufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409: 355-359.
80. Millband DN, Hardwick KG (2002) Fission yeast Mad3p is required for Mad2p to inhibit the anaphase-promoting complex and localizes to kinetochores in a Bub1p-, Bub3p-, and Mph1p-dependent manner. Mol Cell Biol 22: 2728-2742.
81. Minshull J, Sun H, Tonks NK, Murray AW (1994) A MAP kinase-dependent spindle assembly checkpoint in Xenopus egg extracts. Cell 79: 475-486.
82. Murata-Hori M, Wang YL (2002) The kinase activity of aurora B is required for kinetochore-microtubule interactions during mitosis. Curr Biol 12: 894-899.
83. Murray AW (2004) Recycling the cell cycle: cyclins revisited. Cell 116: 221-234.
84. Musacchio A, Hardwick KG (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731-741.
85. Nasmyth K (2002) Segregating sister genomes: the molecular biology of chromosome separation. Science 297: 559-565.
86. Nicklas RB (1997) How cells get the right chromosomes. Science 275: 632-637.
87. Nicklas RB, Koch CA (1969) Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol 43: 40-50.
88. Nystul TG, Goldmark JP, Padilla PA, Roth MB (2003) Suspended animation in C. elegans requires the spindle checkpoint. Science 302: 1038-1041.
89. Peters JM (2002) The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol Cell 9: 931-943.
90. Pritchard CE, Fornerod M, Kasper LH, van Deursen JM (1999) RAE1 is a shuttling mRNA export factor that binds to a GLEBS-like NUP98 motif at the nuclear pore complex through multiple domains. J Cell Biol 145: 237-254.
91. Rieder CL, Schultz A, Cole R, Sluder G (1994) Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J Cell Biol 127: 1301-1310.
92. Rieder CL, Cole RW, Khodjakov A, Sluder G (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.
93. Roberts BT, Farr KA, Hoyt MA (1994) The Saccharomyces cerevisiae checkpoint gene BUB1 encodes a novel protein kinase. Mol Cell Biol 14: 8282-8291.
94. Salina D, Enarson P, Rattner JB, Burke B (2003) Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J Cell Biol 162: 991-1001.
95. Shah JV, Cleveland DW (2000) Waiting for anaphase: Mad2 and the spindle assembly checkpoint. Cell 103: 997-1000.
96. Shannon KB, Canman JC, Salmon ED (2002) Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol Biol Cell 13: 3706-3719.
97. Shapiro PS, Vaisberg E, Hunt AJ et al. (1998) Activation of the MKK/ERK pathway during somatic cell mitosis: direct interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen. J Cell Biol 142: 1533-1545.
98. Sharp-Baker H, Chen RH (2001) Spindle checkpoint protein Bub1 is required for kinetochore localization of Mad1, Mad2, Bub3, and CENP-E, independently of its kinase activity. J Cell Biol 153: 1239-1250.
99. Sironi L, Melixetian M, Faretta M, Prosperini E, Helin K, Musacchio A (2001) Mad2 binding to Mad1 and Cdc20, rather than oligomerization, is required for the spindle checkpoint. EMBO J 20: 6371-6382.
100. 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.
101. Skoufias DA, Andreassen PR, Lacroix FB, Wilson L, Margolis RL (2001) Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc Natl Acad Sci USA 98: 4492-4497.
102. 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.
103. 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.
104. Takenaka K, Moriguchi T, Nishida E (1998) Activation of the protein kinase p38 in the spindle assembly checkpoint and mitotic arrest. Science 280: 599-602.
105. Tanaka TU, Rachidi N, Janke C et al. (2002) Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108: 317-329.
106. Tang Z, Bharadwaj R, Li B, Yu H (2001) Mad2-Independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev Cell 1: 227-237.
107. 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.
108. 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.
109. Taylor SS, Hussein D, Wang Y, Elderkin S, Morrow CJ (2001) Kinetochore localization 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.
110. Tighe A, Johnson VL, Albertella M, Taylor SS (2001) Aneuploid colon cancer cells have a robust spindle checkpoint. EMBO Rep 2: 609-614.
111. Tirnauer JS, Bierer BE (2000) EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability. J Cell Biol 149: 761-766.
112. Tunquist BJ, Maller JL (2003) Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev 17: 683-710.
113. Tunquist BJ, Eyers PA, Chen LG, Lewellyn AL, Maller JL (2003) Spindle checkpoint proteins Mad1 and Mad2 are required for cytostatic factor-mediated metaphase arrest. J Cell Biol 163: 1231-1242.
114. Uhlmann F, Lottspeich F, Nasmyth K (1999) Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400: 37-42.
115. Uhlmann F, Wernic D, Poupart MA, Koonin EV, Nasmyth K (2000) Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103: 375-386.
116. Wang XM, Zhai Y, Ferrell JE Jr. (1997) A role for mitogen-activated protein kinase in the spindle assembly checkpoint in XTC cells. J Cell Biol 137: 433-443.
117. Wang X, Babu JR, Harden JM et al. (2001) The mitotic checkpoint protein hBUB3 and the mRNA export factor hRAE1 interact with GLE2p-binding sequence (GLEBS)-containing proteins. J Biol Chem 276: 26559-26567.
118. Warren CD, Brady DM, Johnston RC, Hanna JS, Hardwick KG, Spencer FA (2002) Distinct chromosome segregation roles for spindle checkpoint proteins. Mol Biol Cell 13: 3029-3041.
119. Wassmann K, Liberal V, Benezra R (2003) Mad2 phosphorylation regulates its association with Mad1 and the APC/C. EMBO J 22: 797-806.
120. Waters JC, Chen RH, Murray AW, Salmon ED (1998) Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J Cell Biol 141: 1181-1191.
121. Weaver BA, Bonday ZQ, Putkey FR, Kops GJ, Silk AD, Cleveland DW (2003) Centromere-associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to single chromosome loss. J Cell Biol 162: 551-563.
122. 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.
123. Wu L, Osmani SA, Mirabito PM (1998) A role for NIMA in the nuclear localization of cyclin B in Aspergillus nidulans. J Cell Biol 141: 1575-1587.
124. Yamaguchi S, Decottignies A, Nurse P (2003) Function of Cdc2p-dependent Bub1p phosphorylation and Bub1p kinase activity in the mitotic and meiotic spindle checkpoint. EMBO J 22: 1075-1087.
125. Yao X, Abrieu A, Zheng Y, Sullivan KF, Cleveland DW (2000) CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint. Nat Cell Biol 2: 484-491.
126. Zecevic M, Catling AD, Eblen ST et al. (1998) Active MAP kinase in mitosis: localization at kinetochores and association with the motor protein CENP-E. J Cell Biol 142: 1547-1558.
127. Zhou H, Kuang J, Zhong L et al. (1998) Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat Genet 20: 189-193.
128. Zirkle RE (1970) Involvement of the prometaphase kinetochore in prevention of a precocious anaphase. J Cell Biol 47: 235a.