Spindle checkpoint function requires Mad2-dependent Cdc20 binding to the Mad3 homology domain of BubR1

Experimental Cell Research

Volumn 312, Issue 10, 2006, Pages 1831-1842

  Davenport, James ^a   Harris, Loleta D ^a   Goorha, Rakesh ^a,b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Bub1; Bub3; BubR1; Cdc20; HeLa cell; Mad2; MCC; Mitotic checkpoint; Mitotic checkpoint complex; Spindle assembly checkpoint

Indexed keywords

BUB1 RELATED PROTEIN; CELL CYCLE PROTEIN 20; GLUTATHIONE TRANSFERASE; LYSINE; NOCODAZOLE; PROTEIN MAD2;

ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; SEQUENCE HOMOLOGY;

EID: 33646851446     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.02.018     Document Type: Article

References (41)

1. Rieder C.L., Cole R.W., Khodjakov A., and Sluder G. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130 (1995) 941-948
2. Li R., and Murray A.W. Feedback control of mitosis in budding yeast. Cell 66 (1991) 519-531
3. Hoyt M.A., Totis L., and Roberts B.T. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66 (1991) 507-517
4. King R.W., Deshaies R.J., Peters J.M., and Kirschner M.W. How proteolysis drives the cell cycle. Science 274 (1996) 1652-1659
5. Peters J.M. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9 (2002) 931-943
6. Li Y., Gorbea C., Mahaffey D., Rechsteiner M., and Benezra R. MAD2 associates with the cyclosome/anaphase-promoting complex and inhibits its activity. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 12431-12436
7. He X., Patterson T.E., and Sazer S. The Schizosaccharomyces pombe spindle checkpoint protein mad2p blocks anaphase and genetically interacts with the anaphase-promoting complex. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 7965-7970
8. Hwang L.H., Lau L.F., Smith D.L., Mistrot C.A., Hardwick K.G., Hwang E.S., Amon A., and Murray A.W. Budding yeast Cdc20: a target of the spindle checkpoint. Science 279 (1998) 1041-1044
9. Kim S.H., Lin D.P., Matsumoto S., Kitazono A., and Matsumoto T. Fission yeast Slp1: an effector of the Mad2-dependent spindle checkpoint. Science 279 (1998) 1045-1047
10. Yu H. Regulation of APC-Cdc20 by the spindle checkpoint. Curr. Opin. Cell Biol. 14 (2002) 706-714
11. Cleveland D.W., Mao Y., and Sullivan K.F. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112 (2003) 407-421
12. Bharadwaj R., and Yu H. The spindle checkpoint, aneuploidy, and cancer. Oncogene 23 (2004) 2016-2027
13. Tang Z., Bharadwaj R., Li B., and Yu H. Mad2-independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev. Cell 1 (2001) 227-237
14. Taylor S.S., Ha E., and McKeon F. The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase. J. Cell Biol. 142 (1998) 1-11
15. Hardwick K.G., Johnston R.C., Smith D.L., and Murray A.W. MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J. Cell Biol. 148 (2000) 871-882
16. Fraschini R., Beretta A., Sironi L., Musacchio A., Lucchini G., and Piatti S. Bub3 interaction with Mad2, Mad3 and Cdc20 is mediated by WD40 repeats and does not require intact kinetochores. EMBO J. 20 (2001) 6648-6659
17. Millband D.N., and Hardwick K.G. 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 (2002) 2728-2742
18. Fang G., Yu H., and Kirschner M.W. 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 (1998) 1871-1883
19. Fang G. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol. Biol. Cell 13 (2002) 755-766
20. Mao Y., Abrieu A., and Cleveland D.W. Activating and silencing the mitotic checkpoint through CENP-E-dependent activation/inactivation of BubR1. Cell 114 (2003) 87-98
21. Weaver B.A., Bonday Z.Q., Putkey F.R., Kops G.J., Silk A.D., and Cleveland D.W. Centromere-associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to single chromosome loss. J. Cell Biol. 162 (2003) 551-563
22. Lampson M.A., and Kapoor T.M. The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7 (2005) 93-98
23. Warren C.D., Brady D.M., Johnston R.C., Hanna J.S., Hardwick K.G., and Spencer F.A. Distinct chromosome segregation roles for spindle checkpoint proteins. Mol. Biol. Cell 13 (2002) 3029-3041
24. Meraldi P., and Sorger P.K. A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J. 24 (2005) 1621-1633
25. Harris L., Davenport J., Neale G., and Goorha R. The mitotic checkpoint gene BubR1 has two distinct functions in mitosis. Exp. Cell Res. 308 (2005) 85-100
26. Davenport J.W., Fernandes E.R., Harris L.D., Neale G.A., and Goorha R. The mouse mitotic checkpoint gene bub1b, a novel bub1 family member, is expressed in a cell cycle-dependent manner. Genomics 55 (1999) 113-117
27. Davenport J., Neale G.A., and Goorha R. Identification of genes potentially involved in LMO2-induced leukemogenesis. Leukemia 14 (2000) 1986-1996
28. Juan G., Traganos F., James W.M., Ray J.M., Roberge M., Sauve D.M., Anderson H., and Darzynkiewicz Z. Histone H3 phosphorylation and expression of cyclins A and B1 measured in individual cells during their progression through G2 and mitosis. Cytometry 32 (1998) 71-77
29. Wang X., Babu J.R., Harden J.M., Jablonski S.A., Gazi M.H., Lingle W.L., de Groen P.C., Yen T.J., and van Deursen J.M. The mitotic checkpoint protein hBUB3 and the mRNA export factor hRAE1 interact with GLE2p-binding sequence (GLEBS)-containing proteins. J. Biol. Chem. 276 (2001) 26559-26567
30. Frangioni J.V., and Neel B.G. Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem. 210 (1993) 179-187
31. Zhang Y., and Lees E. Identification of an overlapping binding domain on Cdc20 for Mad2 and anaphase-promoting complex: model for spindle checkpoint regulation. Mol. Cell. Biol. 21 (2001) 5190-5199
32. Kraft C., Vodermaier H.C., Maurer-Stroh S., Eisenhaber F., and Peters J.M. The WD40 propeller domain of Cdh1 functions as a destruction box receptor for APC/C substrates. Mol. Cell 18 (2005) 543-553
33. Schwab M., Neutzner M., Mocker D., and Seufert W. Yeast Hct1 recognizes the mitotic cyclin Clb2 and other substrates of the ubiquitin ligase APC. EMBO J. 20 (2001) 5165-5175
34. Sironi L., Mapelli M., Knapp S., Antoni A.D., Jeang K.T., and Musacchio A. Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a 'safety belt' binding mechanism for the spindle checkpoint. EMBO J. 21 (2002) 2496-2506
35. Sudakin V., Chan G.K., and Yen T.J. Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J. Cell Biol. 154 (2001) 925-936
36. Chen R.H. BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1. J. Cell Biol. 158 (2002) 487-496
37. Morrow C.J., Tighe A., Johnson V.L., Scott M.I., Ditchfield C., and Taylor S.S. Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J. Cell Sci. 118 (2005) 3639-3652
38. Logarinho E., Bousbaa H., Dias J.M., Lopes C., Amorim I., Antunes-Martins A., and Sunkel C.E. Different spindle checkpoint proteins monitor microtubule attachment and tension at kinetochores in Drosophila cells. J. Cell Sci. 117 (2004) 1757-1771
39. Skoufias D.A., Andreassen P.R., Lacroix F.B., Wilson L., and Margolis R.L. Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 4492-4497
40. Kops G.J., Foltz D.R., and Cleveland D.W. Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 8699-8704
41. Baker D.J., Jeganathan K.B., Cameron J.D., Thompson M., Juneja S., Kopecka A., Kumar R., Jenkins R.B., de Groen P.C., Roche P., and van Deursen J.M. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat. Genet. 36 (2004) 744-749