Characterization of the Kinetochore Binding Domain of CENP-E Reveals Interactions with the Kinetochore Proteins CENP-F and hBUBR1

doi:10.1083/jcb.143.1.49

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J. Cell Biol., Volume 143, Number 1, October 5, 1998 49-63

Characterization of the Kinetochore Binding Domain of CENP-E Reveals Interactions with the Kinetochore Proteins CENP-F and hBUBR1

G.K.T. Chan, B.T. Schaar, and T.J. Yen

Institute for Cancer Research, Fox Chase Cancer Center, Philadelphia, Pennsylvania 19111

We have identified a 350-amino acid domain in the kinetochore motor CENP-E that specifies kinetochore binding in mitosis butnot during interphase. The kinetochore binding domain was usedin a yeast two-hybrid screen to isolate interacting proteins thatincluded the kinetochore proteins CENP-E, CENP-F, and hBUBR1,a BUB1-related kinase that was found to be mutated in some colorectalcarcinomas (Cahill, D.P., C. Lengauer, J. Yu, G.J. Riggins, J.K.Wilson, S.D. Markowitz, K.W. Kinzler, and B. Vogelstein. 1998.Nature. 392:300-303). CENP-F, hBUBR1, and CENP-E assembled ontokinetochores in sequential order during late stages of the cellcycle. These proteins therefore define discrete steps along thekinetochore assembly pathway.

Kinetochores of unaligned chromosome exhibited stronger hBUBR1 and CENP-E staining than those of aligned chromosomes. CENP-Eand hBUBR1 remain colocalized at kinetochores until mid-anaphasewhen hBUBR1 localized to portions of the spindle midzone thatdid not overlap with CENP-E. As CENP-E and hBUBR1 can coimmunoprecipitatewith each other from HeLa cells, they may function as a motor-kinasecomplex at kinetochores. However, the complex distribution patternof hBUBR1 suggests that it may regulate multiple functions thatinclude the kinetochore and the spindle midzone.

Key words: kinetochore; mitotic checkpoint; CENP-E; CENP-F; hBubR1 kinase

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Kanta, H., Laprade, L., Almutairi, A., Pinto, I. (2006). Suppressor Analysis of a Histone Defect Identifies a New Function for the Hda1 Complex in Chromosome Segregation. Genetics 173: 435-450 [Abstract] [Full Text]
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Perez-Mongiovi, D., Malmanche, N., Bousbaa, H., Sunkel, C. (2005). Maternal expression of the checkpoint protein BubR1 is required for synchrony of syncytial nuclear divisions and polar body arrest in Drosophila melanogaster. Development 132: 4509-4520 [Abstract] [Full Text]
Bolanos-Garcia, V. M., Beaufils, S., Renault, A., Grossmann, J. G., Brewerton, S., Lee, M., Venkitaraman, A., Blundell, T. L. (2005). The Conserved N-Terminal Region of the Mitotic Checkpoint Protein BUBR1: A Putative TPR Motif of High Surface Activity. Biophys. J 89: 2640-2649 [Abstract] [Full Text]
Mao, Y., Desai, A., Cleveland, D. W. (2005). Microtubule capture by CENP-E silences BubR1-dependent mitotic checkpoint signaling. J. Cell Biol. 170: 873-880 [Abstract] [Full Text]
Zhu, C., Zhao, J., Bibikova, M., Leverson, J. D., Bossy-Wetzel, E., Fan, J.-B., Abraham, R. T., Jiang, W. (2005). Functional Analysis of Human Microtubule-based Motor Proteins, the Kinesins and Dyneins, in Mitosis/Cytokinesis Using RNA Interference. Mol. Biol. Cell 16: 3187-3199 [Abstract] [Full Text]
Oikawa, T., Okuda, M., Ma, Z., Goorha, R., Tsujimoto, H., Inokuma, H., Fukasawa, K. (2005). Transcriptional Control of BubR1 by p53 and Suppression of Centrosome Amplification by BubR1. Mol. Cell. Biol. 25: 4046-4061 [Abstract] [Full Text]
Yang, Z., Guo, J., Chen, Q., Ding, C., Du, J., Zhu, X. (2005). Silencing Mitosin Induces Misaligned Chromosomes, Premature Chromosome Decondensation before Anaphase Onset, and Mitotic Cell Death. Mol. Cell. Biol. 25: 4062-4074 [Abstract] [Full Text]
Encalada, S. E., Willis, J., Lyczak, R., Bowerman, B. (2005). A Spindle Checkpoint Functions during Mitosis in the Early Caenorhabditis elegans Embryo. Mol. Biol. Cell 16: 1056-1070 [Abstract] [Full Text]
Tsurumi, C., Hoffmann, S., Geley, S., Graeser, R., Polanski, Z. (2004). The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J. Cell Biol. 167: 1037-1050 [Abstract] [Full Text]
Zhang, D., Ma, W., Li, Y.-H., Hou, Y., Li, S.-W., Meng, X.-Q., Sun, X.-F., Sun, Q.-Y., Wang, W.-H. (2004). Intra-oocyte Localization of MAD2 and Its Relationship with Kinetochores, Microtubules, and Chromosomes in Rat Oocytes During Meiosis. Biol. Reprod. 71: 740-748 [Abstract] [Full Text]
Tanudji, M., Shoemaker, J., L'Italien, L., Russell, L., Chin, G., Schebye, X. M. (2004). Gene Silencing of CENP-E by Small Interfering RNA in HeLa Cells Leads to Missegregation of Chromosomes after a Mitotic Delay. Mol. Biol. Cell 15: 3771-3781 [Abstract] [Full Text]
Johnson, V. L., Scott, M. I. F., Holt, S. V., Hussein, D., Taylor, S. S. (2004). Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression. J. Cell Sci. 117: 1577-1589 [Abstract] [Full Text]
Koon, N, Schneider-Stock, R, Sarlomo-Rikala, M, Lasota, J, Smolkin, M, Petroni, G, Zaika, A, Boltze, C, Meyer, F, Andersson, L, Knuutila, S, Miettinen, M, El-Rifai, W (2004). Molecular targets for tumour progression in gastrointestinal stromal tumours. Gut 53: 235-240 [Abstract] [Full Text]
Voet, T., Liebe, B., Labaere, C., Marynen, P., Scherthan, H. (2003). Telomere-independent homologue pairing and checkpoint escape of accessory ring chromosomes in male mouse meiosis. J. Cell Biol. 162: 795-808 [Abstract] [Full Text]
Weaver, B. A.A., Bonday, Z. Q., Putkey, F. R., Kops, G. J.P.L., Silk, A. D., Cleveland, D. W. (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 [Abstract] [Full Text]
Liu, S.-T., Chan, G. K.T., Hittle, J. C., Fujii, G., Lees, E., Yen, T. J. (2003). Human MPS1 Kinase Is Required for Mitotic Arrest Induced by the Loss of CENP-E from Kinetochores. Mol. Biol. Cell 14: 1638-1651 [Abstract] [Full Text]
Campbell, L., Hardwick, K. G. (2003). Analysis of Bub3 spindle checkpoint function in Xenopus egg extracts. J. Cell Sci. 116: 617-628 [Abstract] [Full Text]
Preuss, U., Landsberg, G., Scheidtmann, K. H. (2003). Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res 31: 878-885 [Abstract] [Full Text]
Shannon, K. B., Canman, J. C., Salmon, E. D. (2002). Mad2 and BubR1 Function in a Single Checkpoint Pathway that Responds to a Loss of Tension. Mol. Biol. Cell 13: 3706-3719 [Abstract] [Full Text]
Zhou, J., Yao, J., Joshi, H. C. (2002). Attachment and tension in the spindle assembly checkpoint. J. Cell Sci. 115: 3547-3555 [Abstract] [Full Text]
Harper, J. W., Burton, J. L., Solomon, M. J. (2002). The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16: 2179-2206 [Full Text]
Chen, R.-H. (2002). BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1. J. Cell Biol. 158: 487-496 [Abstract] [Full Text]
Zhou, J., Panda, D., Landen, J. W., Wilson, L., Joshi, H. C. (2002). Minor Alteration of Microtubule Dynamics Causes Loss of Tension across Kinetochore Pairs and Activates the Spindle Checkpoint. J. Biol. Chem. 277: 17200-17208 [Abstract] [Full Text]
Millband, D. N., Hardwick, K. G. (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 [Abstract] [Full Text]
Taylor, S. S., Hussein, D., Wang, Y., Elderkin, S., Morrow, C. J. (2002). 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 [Abstract] [Full Text]
Chaturvedi, P., Sudakin, V., Bobiak, M. L., Fisher, P. W., Mattern, M. R., Jablonski, S. A., Hurle, M. R., Zhu, Y., Yen, T. J., Zhou, B.-B. S. (2002). Chfr Regulates a Mitotic Stress Pathway through its RING-Finger Domain with Ubiquitin Ligase Activity. Cancer Res. 62: 1797-1801 [Abstract] [Full Text]
Fang, G. (2002). Checkpoint Protein BubR1 Acts Synergistically with Mad2 to Inhibit Anaphase-promoting Complex. Mol. Biol. Cell 13: 755-766 [Abstract] [Full Text]
Hussein, D., Taylor, S. S. (2002). Farnesylation of Cenp-F is required for G2/M progression and degradation after mitosis. J. Cell Sci. 115: 3403-3414 [Abstract] [Full Text]
Jullien, D., Vagnarelli, P., Earnshaw, W. C., Adachi, Y. (2002). Kinetochore localisation of the DNA damage response component 53BP1 during mitosis. J. Cell Sci. 115: 71-79 [Abstract] [Full Text]
Belgareh, N., Rabut, G., Bai, S. W., van Overbeek, M., Beaudouin, J., Daigle, N., Zatsepina, O. V., Pasteau, F., Labas, V., Fromont-Racine, M., Ellenberg, J., Doye, V. (2001). An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154: 1147-1160 [Abstract] [Full Text]
Hoyt, M. A. (2001). A new view of the spindle checkpoint. J. Cell Biol. 154: 909-912 [Abstract] [Full Text]
Sudakin, V., Chan, G. K.T., Yen, T. J. (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 [Abstract] [Full Text]
Sutherland, H. G.E., Mumford, G. K., Newton, K., Ford, L. V., Farrall, R., Dellaire, G., Caceres, J. F., Bickmore, W. A. (2001). Large-scale identification of mammalian proteins localized to nuclear sub-compartments. Hum Mol Genet 10: 1995-2011 [Abstract] [Full Text]
Sun, F., Yin, H., Eichenlaub-Ritter, U. (2001). Differential chromosome behaviour in mammalian oocytes exposed to the tranquilizer diazepam in vitro. Mutagenesis 16: 407-417 [Abstract] [Full Text]
McEwen, B. F., Chan, G. K.T., Zubrowski, B., Savoian, M. S., Sauer, M. T., Yen, T. J. (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 [Abstract] [Full Text]
Hoffman, D. B., Pearson, C. G., Yen, T. J., Howell, B. J., Salmon, E.D. (2001). Microtubule-dependent Changes in Assembly of Microtubule Motor Proteins and Mitotic Spindle Checkpoint Proteins at PtK1 Kinetochores. Mol. Biol. Cell 12: 1995-2009 [Abstract] [Full Text]
Sharp-Baker, H., Chen, R.-H. (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 [Abstract] [Full Text]
Olesen, S. H., Thykjaer, T., Orntoft, T. F. (2001). Mitotic checkpoint genes hBUB1, hBUB1B, hBUB3 and TTK in human bladder cancer, screening for mutations and loss of heterozygosity. Carcinogenesis 22: 813-815 [Abstract] [Full Text]
Skoufias, D. A., Andreassen, P. R., Lacroix, F. B., Wilson, L., Margolis, R. L. (2001). Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc. Natl. Acad. Sci. USA 10.1073/pnas.081076898v1 [Abstract] [Full Text]
Scaerou, F., Starr, D. A., Piano, F., Papoulas, O., Karess, R. E., Goldberg, M. L. (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 [Abstract] [Full Text]
Yucel, J. K., Marszalek, J. D., McIntosh, J. R., Goldstein, L. S.B., Cleveland, D. W., Philp, A. V. (2000). CENP-meta, an Essential Kinetochore Kinesin Required for the Maintenance of Metaphase Chromosome Alignment in Drosophila. J. Cell Biol. 150: 1-12 [Abstract] [Full Text]
Ly, D. H., Lockhart, D. J., Lerner, R. A., Schultz, P. G. (2000). Mitotic Misregulation and Human Aging. Science 287: 2486-2492 [Abstract] [Full Text]
Hardwick, K. G., Johnston, R. C., Smith, D. L., Murray, A. W. (2000). MAD3 Encodes a Novel Component of the Spindle Checkpoint which Interacts with Bub3p, Cdc20p, and Mad2p. J. Cell Biol. 148: 871-882 [Abstract] [Full Text]
Futamura, M., Arakawa, H., Matsuda, K., Katagiri, T., Saji, S., Miki, Y., Nakamura, Y. (2000). Potential Role of BRCA2 in a Mitotic Checkpoint after Phosphorylation by hBUBR1. Cancer Res. 60: 1531-1535 [Abstract] [Full Text]
Saffery, R., Irvine, D. V., Griffiths, B., Kalitsis, P., Wordeman, L., Choo, K.H. A. (2000). Human centromeres and neocentromeres show identical distribution patterns of >20 functionally important kinetochore-associated proteins.. Hum Mol Genet 9: 175-185 [Abstract] [Full Text]
Starr, D., Saffery, R, Li, Z, Simpson, A., Choo, K., Yen, T., Goldberg, M. (2000). HZwint-1, a novel human kinetochore component that interacts with HZW10. J. Cell Sci. 113: 1939-1950 [Abstract]
Slater, H. R, Nouri, S., Earle, E., Lo, A. W I, Hale, L. G, Choo, K H A. (1999). Neocentromere formation in a stable ring 1p32-p36.1 chromosome. J. Med. Genet. 36: 914-918 [Abstract] [Full Text]
Li, W., Lan, Z., Wu, H., Wu, S., Meadows, J., Chen, J., Zhu, V., Dai, W. (1999). BUBR1 Phosphorylation Is Regulated during Mitotic Checkpoint Activation. Cell Growth Differ. 10: 769-775 [Abstract] [Full Text]
Chan, G.K.T., Jablonski, S.A., Sudakin, V., Hittle, J.C., Yen, T.J. (1999). Human BUBR1 Is a Mitotic Checkpoint Kinase that Monitors CENP-E Functions at Kinetochores and Binds the Cyclosome/APC. J. Cell Biol. 146: 941-954 [Abstract] [Full Text]
Chen, R.-H., Brady, D. M., Smith, D., Murray, A. W., Hardwick, K. G. (1999). The Spindle Checkpoint of Budding Yeast Depends on a Tight Complex between the Mad1 and Mad2 Proteins. Mol. Biol. Cell 10: 2607-2618 [Abstract] [Full Text]
Martinez-Exposito, M. J., Kaplan, K. B., Copeland, J., Sorger, P. K. (1999). Retention of the Bub3 checkpoint protein on lagging chromosomes. Proc. Natl. Acad. Sci. USA 96: 8493-8498 [Abstract] [Full Text]
Basu, J., Bousbaa, H., Logarinho, E., Li, Z., Williams, B. C., Lopes, C., Sunkel, C. E., Goldberg, M. L. (1999). Mutations in the Essential Spindle Checkpoint Gene bub1 Cause Chromosome Missegregation and Fail to Block Apoptosis in Drosophila. J. Cell Biol. 146: 13-28 [Abstract] [Full Text]
Goodwin, R. L., Pabon-Pena, L. M., Foster, G. C., Bader, D. (1999). The Cloning and Analysis of LEK1 Identifies Variations in the LEK/Centromere Protein F/Mitosin Gene Family. J. Biol. Chem. 274: 18597-18604 [Abstract] [Full Text]
Hardwick, K. G., Li, R., Mistrot, C., Chen, R.-H., Dann, P., Rudner, A., Murray, A. W. (1999). Lesions in Many Different Spindle Components Activate the Spindle Checkpoint in the Budding Yeast Saccharomyces cerevisiae. Genetics 152: 509-518 [Abstract] [Full Text]
Ashar, H. R., James, L., Gray, K., Carr, D., Black, S., Armstrong, L., Bishop, W. R., Kirschmeier, P. (2000). Farnesyl Transferase Inhibitors Block the Farnesylation of CENP-E and CENP-F and Alter the Association of CENP-E with the Microtubules. J. Biol. Chem. 275: 30451-30457 [Abstract] [Full Text]
Crespo, N. C., Ohkanda, J., Yen, T. J., Hamilton, A. D., Sebti, S. M. (2001). The Farnesyltransferase Inhibitor, FTI-2153, Blocks Bipolar Spindle Formation and Chromosome Alignment and Causes Prometaphase Accumulation during Mitosis of Human Lung Cancer Cells. J. Biol. Chem. 276: 16161-16167 [Abstract] [Full Text]
Skoufias, D. A., Andreassen, P. R., Lacroix, F. B., Wilson, L., Margolis, R. L. (2001). Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc. Natl. Acad. Sci. USA 98: 4492-4497 [Abstract] [Full Text]