Spindle checkpoint signaling requires the Mis6 kinetochore subcomplex, which interacts with Mad2 and mitotic spindles

Molecular Biology of the Cell

Volumn 16, Issue 8, 2005, Pages 3666-3677

  Saitoh, Shigeaki ^a   Ishii, Kojiro ^a   Kobayashi, Yasuyo ^a   Takahashi, Kohta ^a,b  

^a KURUME UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; PROTEIN BUB1; PROTEIN MAD2; PROTEIN MIS6; PROTEIN NUF2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANAPHASE; ARTICLE; CELL CYCLE; CENTROMERE; CHROMATIN; CHROMOSOME SEGREGATION; COMPLEX FORMATION; MICROTUBULE; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; YEAST;

AUTOANTIGENS; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; KINETOCHORES; MITOSIS; MITOTIC SPINDLE APPARATUS; MUTATION; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCES POMBE;

EID: 23044475524     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-01-0014     Document Type: Article

References (60)

1. Appelgren, H., Kniola, B., and Ekwall, K. (2003). Distinct centromere domain structures with separate functions demonstrated in live fission yeast cells. J. Cell Sci. 116, 4035-4042.
2. Bernard, P., Hardwick, K., and Javerzat, J. P. (1998). Fission yeast bub1 is a mitoric centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis. J. Cell Biol. 143, 1775-1787.
3. Cahill, D. P., Lengauer, C., Yu, J., Riggins, G. J., Willson, J. K., Markowitz, S. D., Kinzler, K. W., and Vogelstein, B. (1998). Mutations of mitotic checkpoint genes in human cancers. Nature 392, 300-303.
4. Cheeseman, I. M., Anderson, S., Jwa, M., Green, E. M., Kang, J., Yates, J, R., 3rd, Chan, C. S., Drubin, D. G., and Barnes, G. (2002a). Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ip11p. Cell 111, 163-172.
5. Cheeseman, I. M., Drubin, D. G., and Barnes, G. (2002b). Simple centromere, complex kinetochore: linking spindle microtubules and centromeric DNA in budding yeast. J. Cell Biol. 257, 199-203.
6. Chen, R. H., Brady, D. M., Smith, D., Murray, A. W., and Hardwick, K. G. (1999). The spindle checkpoint of budding yeast depends on a tight complex between the Mad1 and Mad2 proteins. Mol. Biol. Cell 30, 2607-2618.
7. Chen, R. H., Shevchenko, A., Mann, M., and Murray, A. W. (1998). Spindle checkpoint protein Xmadl recruits Xmad2 to unattached kinetochores. J. Cell Biol. 143, 283-295.
8. Chen, R. H., Waters, J. C., Salmon, E. D., and Murray, A. W. (1996). Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores. Science 274, 242-246.
9. Chen, Y., Riley, D. J., Chen, P. L., and Lee, W. H. (1997). HEC, a novel nuclear protein rich in leucine heptad repeats specifically involved in mitosis. Mol. Cell. Biol. 17, 6049-6056.
10. Cleveland, D. W., Mao, Y., and Sullivan, K. F. (2003). Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421.
11. De Wulf, P., McAinsh, A. D., and Sorger, P. K. (2003). Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev. 17, 2902-2921.
12. Deluca, J. G., Dong, Y., Hergert, P., Strauss, J., Hickey, J. M., Salmon, E. D., and McEwen, B. F. (2005). Hec1 and Nuf2 are core components of the kinetochore outer plate essential for organizing microtubule attachment sites. Mol. Biol. Cell, 16, 519-531.
13. DeLuca, J. G., Howell, B. J., Canman, J. C., Hickey, J. M., Fang, G., and Salmon, E. D. (2003). Nuf2 and Hec1 are required for retention of the checkpoint proteins Mad1 and Mad2 to kinetochores. Curr. Biol. 13, 2103-2109.
14. Funabiki, H., Hagan, I., Uzawa, S., and Yanagida, M. (1993). Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol. 121, 961-976.
15. Garcia, M. A., Koonrugsa, N., and Toda, T. (2002). Spindle-kinetochore attachment requires the combined action of Kin I-like Klp5/6 and Alp14/Dis1-MAPs in fission yeast. EMBO J. 21, 6015-6024.
16. Goshima, G., Kiyomitsu, T., Yoda, K., and Yanagida, M. (2003). Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J. Cell Biol. 160, 25-39.
17. Goshima, G., Saitoh, S., and Yanagida, M. (1999). Proper metaphase spindle length is determined by centromere proteins Mis12 and Mis6 required for faithful chromosome segregation. Genes Dev. 13, 1664-1677.
18. 7+ gene. Nature 347, 563-566.
19. Hayashi, T., Fujita, Y., Iwasaki, O., Adachi, Y., Takahashi, K., and Yanagida, M. (2004). Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118, 715-729.
20. Holland, S., Ioannou, D., Haines, S., and Brown, W. R. (2005). Comparison of Dam tagging and chromatin immunoprecipitation as tools for the identification of the binding sites for S. pombe CENP-C. Chromosome Res. 13, 73-83.
21. Hori, T., Haraguchi, T., Hiraoka, Y., Kimura, H., and Fukagawa, T. (2003). Dynamic behavior of Nuf2-Hec1 complex that localizes to the centrosome and centromere and is essential for mitotic progression in vertebrate cells. J. Cell Sci. 116, 3347-3362.
22. Howe, M., McDonald, K. L., Albertson, D. G., and Meyer, B. J, (2001). HIM-10 is required for kinetochore structure and function on Caenorhahditis elegans holocentric chromosomes. J. Cell Biol. 153, 1227-1238.
23. Ikui, A. E., Furuya, K., Yanagida, M., and Matsumoto, T. (2002). Control of localization of a spindle checkpoint protein, Mad2, in fission yeast. J. Cell Sci. 115, 1603-1610.
24. Janke, C., Ortiz, J., Lechner, J., Shevchenko, A., Magiera, M. M., Schramm, C., and Schiebel, E. (2001). The budding yeast proteins Spc24p and Spc25p interact with Ndc80p and Nuf2p at the kinetochore and are important for kinetochore clustering and checkpoint control. EMBO J. 20, 777-791.
25. Jin, D. Y., Spencer, F., and Jeang, K. T. (1998). Human T cell leukemia virus type 1 oncoprotein Tax targets the human mitotic checkpoint protein MAD1. Cell 93, 81-91.
26. Kim, S. H., Lin, D. P., Matsumoto, S., Kitazono, A., and Matsumoto, T. (1998). Fission yeast Slp 1, an effector of the Mad2-dependent spindle checkpoint. Science 279, 1045-1047.
27. Krawchuk, M. D., and Wahls, W. P. (1999). High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast 15, 1419-1427.
28. Li, Y., and Benezra, R. (1996). Identification of a human mitotic checkpoint gene: hsMAD2. Science 274, 246-248.
29. Liu, S. T., Hittle, J. C., Jablonski, S. A., Campbell, M. S., Yoda, K., and Yen, T. J. (2003). Human CENP-I specifies localization of CENP-F, MAD1 and MAD2 to kinetochores and is essential for mitosis. Nat. Cell Biol. 5, 341-345.
30. Martin-Lluesma, S., Stucke, V. M., and Nigg, E. A. (2002). Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science 297, 2267-2270.
31. Maundrell, K. (1993). Thiamine-repressible expression vectors pREP and pRIP for fission yeast. Gene 123, 127-130.
32. Mellone, B. G., and Allshire, R. C. (2003). Stretching it: putting the CEN(P-A) in centromere. Curr. Opin. Genet. Dev. 13, 191-198.
33. Meluh, P. B., and Koshland, D. (1995). Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol. Biol. Cell 6, 793-807.
34. Mikami, Y., Hori, T., Kimura, H., and Fukagawa, T. (2005). The functional region of CENP-H interacts with the Nuf2 complex that localizes to centromere during mitosis. Mol. Cell. Biol. 25, 1958-1970.
35. Millband, D. N., and 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.
36. Minoda, A., Saitoh, S., Takahashi, K., and Toda, T. (2005). BAF53/Arp4 homolog Alp5 in fission yeast is required for histone H4 acetylation, kinetochore-spindle attachment, and gene silencing at centromere. Mol. Biol. Cell 16, 316-327.
37. Moreno, S., Klar, A., and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
38. Nabeshima, K., Saitoh, S., and Yanagida, M. (1997). Use of green fluorescent protein for intracellular protein localization in living fission yeast cells. Methods Enzymol. 283, 459-471.
39. Nabetani, A., Koujin, T., Tsutsumi, C., Haraguchi, T., and Hiraoka, Y. (2001). A conserved protein, Nuf2, is implicated in connecting the centromere to the spindle during chromosome segregation: a link between the kinetochore function and the spindle checkpoint. Chromosoma 110, 322-334.
40. Nishihashi, A., Haraguchi, T., Hiraoka, Y., Ikemura, T., Regnier, V., Dodson, H., Earnshaw, W. C., and Fukagawa, T. (2002). CENP-I is essential for centromere function in vertebrate cells. Dev. Cell 2, 463-476.
41. Obuse, C., Iwasaki, O., Kiyomitsu, T., Goshima, G., Toyoda, Y., and Yanagida, M. (2004). A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nat. Cell Biol. 6, 1135-1141.
42. Osborne, M. A., Schlenstedt, G., Jinks, T., and Silver, P. A. (1994). Nuf2, a spindle pole body-associated protein required for nuclear division in yeast. J. Cell Biol. 125, 853-866.
43. Pidoux, A. L., Richardson, W., and Allshire, R. C. (2003). Sim 4, a novel fission yeast kinetochore protein required for centromeric silencing and chromosome segregation. J. Cell Biol. 161, 295-307.
44. Rizzo, M. A., Springer, G. H., Granada, B., and Piston, D. W. (2004). An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 22, 445-449.
45. Saitoh, H., Tomkiel, J., Cooke, C. A., Ratrie, H., 3rd, Maurer, M., Rothfield, N. F., and Earnshaw, W. C. (1992). CENP-C, an autoantigen in scleroderma, is a component of the human inner kinetochore plate. Cell 70, 115-125.
46. Saitoh, S., Takahashi, K., and Yanagida, M. (1997). Mis6, a fission yeast inner centromere protein, acts during G1/S and forms specialized chromatin required for equal segregation. Cell 90, 131-143.
47. Skoufias, D. A., Andreassen, P. R., Lacroix, F. B., Wilson, L., and 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.
48. Takahashi, K., Chen, E. S., and Yanagida, M. (2000). Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288, 2215-2219.
49. Takahashi, K., Murakami, S., Chikashige, Y., Funabiki, H., Niwa, O., and Yanagida, M. (1992). A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol. Biol. Cell 3, 819-835.
50. Takahashi, K., Yamada, H., and Yanagida, M. (1994). Fission yeast minichromosome loss mutants mis cause lethal aneuploidy and replication abnormality. Mol. Biol. Cell 5, 1145-1158.
51. Taylor, S. S., Ha, E., and 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. 342, 1-11.
52. Taylor, S. S., and McKeon, F. (1997). Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell 89, 727-735.
53. Toyoda, Y., Furuya, K., Goshima, G., Nagao, K., Takahashi, K., and Yanagida, M. (2002). Requirement of chromarid cohesion proteins rad21/scc1 and mis4/ scc2 for normal spindle-kinetochore interaction in fission yeast. Curr. Biol. 12, 347-358.
54. Vanoosthuyse, V., Valsdottir, R., Javerzat, J. P., and Hardwick, K. G. (2004). Kinetochore targeting of fission yeast Mad and Bub proteins is essential for spindle checkpoint function but not for all chromosome segregation roles of Bub1p. Mol. Cell. Biol. 24, 9786-9801.
55. Waters, J. C., Chen, R. H., Murray, A. W., and Salmon, E. D. (1998). Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J. Cell Biol. 141, 1181-1191.
56. Westermann, S., Cheeseman, I. M., Anderson, S., Yates, J. R., 3rd, Drubin, D. G., and Barnes, G. (2003). Architecture of the budding yeast kinetochore reveals a conserved molecular core. J. Cell Biol. 163, 215-222.
57. Wigge, P. A., Jensen, O. N., Holmes, S., Soues, S., Mann, M., and Kilmartin, J. V. (1998). Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry. J. Cell Biol. 141, 967-977.
58. Wigge, P. A., and Kilmartin, J. V. (2001). The Ndc80p complex from Saccharomyces cerevisiae contains conserved centromere components and has a function in chromosome segregation. J. Cell Biol. 152, 349-360.
59. Yamada, H., Kumada, K., and Yanagida, M. (1997). Distinct subunit functions and cell cycle regulated phosphorylation of 20S APC/cyclosome required for anaphase in fission yeast. J. Cell Sci. 110, 1793-1804.
60. Zhou, H., and Thiele, D. J. (2001). Identification of a novel high affinity copper transport complex in the fission yeast Schizosaccharomyces pombe. J. Biol. Chem. 276, 20529-20535.