Phosphorylation regulates the p31comet-mitotic arrest-deficient 2 (Mad2) interaction to promote spindle assembly checkpoint (SAC) activity

Journal of Biological Chemistry

Volumn 289, Issue 16, 2014, Pages 11367-11373

  Date, Dipali A ^a   Burrows, Amy C ^a   Summers, Matthew K ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

MITOTIC PROGRESSION; SPINDLE-ASSEMBLY;

PHOSPHORYLATION;

CELL PROTEIN; PROTEIN MAD2; PROTEIN P31; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; BINDING KINETICS; CELL CYCLE ASSAY; CELL CYCLE REGULATION; COMET ASSAY; COMPLEX FORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; M PHASE CELL CYCLE CHECKPOINT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANAPHASE-PROMOTING COMPLEX; CELL CYCLE; CELL DIVISION; MAD2; MITOSIS; MITOTIC CHECKPOINT COMPLEX; P31COMET; PROTEIN COMPLEXES; PROTEIN PHOSPHORYLATION; SPINDLE ASSEMBLY CHECKPOINT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE PROTEINS; HELA CELLS; HUMANS; M PHASE CELL CYCLE CHECKPOINTS; MAD2 PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING;

EID: 84899022679     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.520841     Document Type: Article

References (28)

1. Sudakin, V., Chan, G. K., and 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
2. Luo, X., Tang, Z., Xia, G., Wassmann, K., Matsumoto, T., Rizo, J., and Yu, H. (2004) The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat. Struct. Mol. Biol. 11, 338-345
3. Luo, X., Fang, G., Coldiron, M., Lin, Y., Yu, H., Kirschner, M. W., and Wagner, G. (2000) Structure of the Mad2 spindle assembly checkpoint protein and its interaction with Cdc20. Nat Struct Biol 7, 224-229
4. Luo, X., Tang, Z., Rizo, J., and 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
5. Sironi, L., Melixetian, M., Faretta, M., Prosperini, E., Helin, K., and Musacchio A. (2001) Mad2 binding to Mad1 and Cdc20, rather than oligomerization, is required for the spindle checkpoint. EMBO J. 20, 6371-6382
6. Sironi, L., Mapelli, M., Knapp, S., De Antoni, A., Jeang, K. T., and 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
7. De Antoni, A., Pearson, C. G., Cimini, D., Canman, J. C., Sala, V., Nezi, L., Mapelli, M., Sironi, L., Faretta, M., Salmon, E. D., and Musacchio, A. (2005) The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 15, 214-225
8. Nezi, L., Rancati, G., De Antoni, A., Pasqualato, S., Piatti, S., and Musacchio, A. (2006) Accumulation of Mad2-Cdc20 complex during spindle checkpoint activation requires binding of open and closed conformers of Mad2 in Saccharomyces cerevisiae. J. Cell Biol. 174, 39-51
9. Mapelli, M., Massimiliano, L., Santaguida, S., and Musacchio, A. (2007) The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint. Cell 131, 730-743
10. Mariani, L., Chiroli, E., Nezi, L., Muller, H., Piatti, S., Musacchio, A., and Ciliberto, A. (2012) Role of the Mad2 dimerization interface in the spindle assembly checkpoint independent of kinetochores. Curr. Biol. 22, 1900-1908
11. Kulukian, A., Han, J. S., and Cleveland, D. W. (2009) Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell 16, 105-117
12. Xia, G., Luo, X., Habu, T., Rizo, J., Matsumoto, T., and Yu, H. (2004) Conformation-specific binding of p31(comet) antagonizes the function of Mad2 in the spindle checkpoint. EMBO J. 23, 3133-3143
13. Jia, L., Li, B., Warrington, R. T., Hao, X., Wang, S., and Yu, H. (2011) Defining pathways of spindle checkpoint silencing: functional redundancy between Cdc20 ubiquitination and p31(comet). Mol. Biol. Cell 22, 4227-4235
14. Hagan, R. S., Manak, M. S., Buch, H. K., Meier, M. G., Meraldi, P., Shah, J. V., and Sorger, P. K. (2011) p31comet acts to ensure timely spindle checkpoint silencing subsequent to kinetochore attachment. Mol. Biol. Cell 22, 4236-4246
15. Westhorpe, F. G., Tighe, A., Lara-Gonzalez, P., and Taylor, S. S. (2011) p31comet-mediated extraction of Mad2 from the MCC promotes efficient mitotic exit. J. Cell Sci. 124, 3905-3916
16. Fava, L. L., Kaulich, M., Nigg, E. A., and Santamaria, A. (2011) Probing the in vivo function of Mad1:C-Mad2 in the spindle assembly checkpoint. EMBO J. 30, 3322-3336
17. Mapelli, M., Filipp, F. V., Rancati, G., Massimiliano, L., Nezi, L., Stier, G., Hagan, R. S., Confalonieri, S., Piatti, S., Sattler, M., and Musacchio, A. (2006) Determinants of conformational dimerization of Mad2 and its inhibition by p31comet. EMBO J. 25, 1273-1284
18. Yang, M., Li, B., Tomchick, D. R., Machius, M., Rizo, J., Yu, H., and Luo, X. (2007) p31comet blocks Mad2 activation through structural mimicry. Cell 131, 744-755
19. Varetti, G., Guida, C., Santaguida, S., Chiroli, E., and Musacchio, A. (2011) Homeostatic control of mitotic arrest. Mol. Cell 44, 710-720
20. Summers, M. K., Pan, B., Mukhyala, K., and Jackson, P. K. (2008) The unique N terminus of the UbcH10 E2 enzyme controls the threshold for APC activation and enhances checkpoint regulation of the APC. Mol. Cell 31, 544-556
21. Reddy, S. K., Rape, M., Margansky, W. A., and Kirschner, M. W. (2007) Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 446, 921-925
22. Miniowitz-Shemtov, S., Teichner, A., Sitry-Shevah, D., and Hershko, A. (2010) ATP is required for the release of the anaphase-promoting complex/ cyclosome from inhibition by the mitotic checkpoint. Proc. Natl. Acad. Sci. U.S.A. 107, 5351-5356
23. Teichner, A., Eytan, E., Sitry-Shevah, D., Miniowitz-Shemtov, S., Dumin, E., Gromis, J., and Hershko, A. (2011) p31comet Promotes disassembly of the mitotic checkpoint complex in an ATP-dependent process. Proc. Natl. Acad. Sci. U.S.A. 108, 3187-3192
24. Torres, J. Z., Miller, J. J., and Jackson, P. K. (2009) High-Throughput generation of tagged stable cell lines for proteomic analysis. Proteomics 9, 2888-2891
25. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K., and Koike, T. (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell Proteomics 5, 749-757
26. Tipton, A. R., Wang, K., Link, L., Bellizzi, J. J., Huang, H., Yen, T., and Liu, S. T. (2011) BUBR1 and closed MAD2 (C-MAD2) interact directly to assemble a functional mitotic checkpoint complex. J. Biol. Chem. 286, 21173-21179
27. Miniowitz-Shemtov, S., Eytan, E., Ganoth, D., Sitry-Shevah, D., Dumin, E., and Hershko, A. (2012) Role of phosphorylation of Cdc20 in p31(comet)-stimulated disassembly of the mitotic checkpoint complex. Proc. Natl. Acad. Sci. U.S.A. 109, 8056-8060
28. Kim, S., Sun, H., Ball, H. L., Wassmann, K., Luo, X., and Yu, H. (2010) Phosphorylation of the spindle checkpoint protein Mad2 regulates its conformational transition. Proc. Natl. Acad. Sci. U.S.A. 107, 19772-19777