Catalytic assembly of the mitotic checkpoint inhibitor BubR1-Cdc20 by a Mad2-induced functional Switch in Cdc20

Molecular Cell

Volumn 51, Issue 1, 2013, Pages 92-104

  Han, Joo Seok ^a   Holland, Andrew J ^a,c   Fachinetti, Daniele ^a   Kulukian, Anita ^a,b   Cetin, Bulent ^a   Cleveland, Don W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BUB1 RELATED PROTEIN; CELL CYCLE PROTEIN 20; PROTEIN MAD2; UBIQUITIN PROTEIN LIGASE; BUB1 PROTEIN, HUMAN; BUB1 SPINDLE CHECKPOINT PROTEIN; CALCIUM BINDING PROTEIN; CDC20 PROTEIN, HUMAN; CELL CYCLE PROTEIN; MAD2L1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN;

ARTICLE; CENTROMERE; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; UBIQUITINATION; BINDING SITE; BIOLOGICAL MODEL; HELA CELL; METABOLISM; PHYSIOLOGY; HELA CELL LINE;

BINDING SITES; CALCIUM-BINDING PROTEINS; CDC20 PROTEINS; CELL CYCLE PROTEINS; HELA CELLS; HUMANS; KINETOCHORES; M PHASE CELL CYCLE CHECKPOINTS; MAD2 PROTEINS; MODELS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS;

EID: 84891719259     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.05.019     Document Type: Article

References (50)

1. Burton J.L., Solomon M.J. Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev. 2007, 21:655-667.
2. Chao W.C., Kulkarni K., Zhang Z., Kong E.H., Barford D. Structure of the mitotic checkpoint complex. Nature 2012, 484:208-213.
3. Choi E., Choe H., Min J., Choi J.Y., Kim J., Lee H. BubR1 acetylation at prometaphase is required for modulating APC/C activity and timing of mitosis. EMBO J. 2009, 28:2077-2089.
4. Cordingley M.G., Callahan P.L., Sardana V.V., Garsky V.M., Colonno R.J. Substrate requirements of human rhinovirus 3C protease for peptide cleavage invitro. J.Biol. Chem. 1990, 265:9062-9065.
5. Davenport J., Harris L.D., Goorha R. Spindle checkpoint function requires Mad2-dependent Cdc20 binding to the Mad3 homology domain of BubR1. Exp. Cell Res. 2006, 312:1831-1842.
6. De Antoni A., Pearson C.G., Cimini D., Canman J.C., Sala V., Nezi L., Mapelli M., Sironi L., Faretta M., Salmon E.D., Musacchio A. The Mad1/Mad2 complex as a template for Mad2 activation in the spindle assembly checkpoint. Curr. Biol. 2005, 15:214-225.
7. Doncic A., Ben-Jacob E., Barkai N. Evaluating putative mechanisms of the mitotic spindle checkpoint. Proc. Natl. Acad. Sci. USA 2005, 102:6332-6337.
8. Fang G. Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol. Biol. Cell 2002, 13:755-766.
9. Fang G., Yu H., 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. 1998, 12:1871-1883.
10. Gassmann R., Holland A.J., Varma D., Wan X., Civril F., Cleveland D.W., Oegema K., Salmon E.D., Desai A. Removal of Spindly from microtubule-attached kinetochores controls spindle checkpoint silencing in human cells. Genes Dev. 2010, 24:957-971.
11. Herzog F., Peters J.M. Large-scale purification of the vertebrate anaphase-promoting complex/cyclosome. Methods Enzymol. 2005, 398:175-195.
12. Holland A.J., Fachinetti D., Han J.S., Cleveland D.W. Inducible, reversible system for the rapid and complete degradation of proteins in mammalian cells. Proc. Natl. Acad. Sci. USA 2012, 109:E3350-E3357.
13. Hoyt M.A., Totis L., Roberts B.T. S.cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 1991, 66:507-517.
14. Izawa D., Pines J. Mad2 and the APC/C compete for the same site on Cdc20 to ensure proper chromosome segregation. J.Cell Biol. 2012, 199:27-37.
15. Jia L., Li B., Warrington R.T., Hao X., Wang S., Yu H. Defining pathways of spindle checkpoint silencing: functional redundancy between Cdc20 ubiquitination and p31(comet). Mol. Biol. Cell 2011, 22:4227-4235.
16. King E.M., van der Sar S.J., Hardwick K.G. Mad3 KEN boxes mediate both Cdc20 and Mad3 turnover, and are critical for the spindle checkpoint. PLoS ONE 2007, 2:e342.
17. Kulukian A., Han J.S., Cleveland D.W. Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding. Dev. Cell 2009, 16:105-117.
18. Lara-Gonzalez P., Scott M.I., Diez M., Sen O., Taylor S.S. BubR1 blocks substrate recruitment to the APC/C in a KEN-box-dependent manner. J.Cell Sci. 2011, 124:4332-4345.
19. Lara-Gonzalez P., Westhorpe F.G., Taylor S.S. The spindle assembly checkpoint. Curr. Biol. 2012, 22:R966-R980.
20. Lau D.T., Murray A.W. Mad2 and Mad3 cooperate to arrest budding yeast in mitosis. Curr. Biol. 2012, 22:180-190. Published online December 29, 2011. 10.1016/j.cub.2011.12.029.
21. Li R., Murray A.W. Feedback control of mitosis in budding yeast. Cell 1991, 66:519-531.
22. Luo X., Fang G., Coldiron M., Lin Y., Yu H., Kirschner M.W., Wagner G. Structure of the Mad2 spindle assembly checkpoint protein and its interaction with Cdc20. Nat. Struct. Biol. 2000, 7:224-229.
23. Luo X., Tang Z., Rizo J., Yu H. The Mad2 spindle checkpoint protein undergoes similar major conformational changes upon binding to either Mad1 or Cdc20. Mol. Cell 2002, 9:59-71.
24. Luo X., Tang Z., Xia G., Wassmann K., Matsumoto T., Rizo J., Yu H. The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat. Struct. Mol. Biol. 2004, 11:338-345.
25. Mapelli M., Filipp F.V., Rancati G., Massimiliano L., Nezi L., Stier G., Hagan R.S., Confalonieri S., Piatti S., Sattler M., Musacchio A. Determinants of conformational dimerization of Mad2 and its inhibition by p31comet. EMBO J. 2006, 25:1273-1284.
26. Mapelli M., Massimiliano L., Santaguida S., Musacchio A. The Mad2 conformational dimer: structure and implications for the spindle assembly checkpoint. Cell 2007, 131:730-743.
27. Mariani L., Chiroli E., Nezi L., Muller H., Piatti S., Musacchio A., Ciliberto A. Role of the Mad2 dimerization interface in the spindle assembly checkpoint independent of kinetochores. Curr. Biol. 2012, 22:1900-1908.
28. Nezi L., Rancati G., De Antoni A., Pasqualato S., Piatti S., Musacchio A. Accumulation of Mad2-Cdc20 complex during spindle checkpoint activation requires binding of open and closed conformers of Mad2 in Saccharomyces cerevisiae. J.Cell Biol. 2006, 174:39-51.
29. Nilsson J., Yekezare M., Minshull J., Pines J. The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat. Cell Biol. 2008, 10:1411-1420.
30. Nishimura K., Fukagawa T., Takisawa H., Kakimoto T., Kanemaki M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 2009, 6:917-922.
31. Pan J., Chen R.H. Spindle checkpoint regulates Cdc20p stability in Saccharomyces cerevisiae. Genes Dev. 2004, 18:1439-1451.
32. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
33. Reddy S.K., Rape M., Margansky W.A., Kirschner M.W. Ubiquitination by the anaphase-promoting complex drives spindle checkpoint inactivation. Nature 2007, 446:921-925.
34. Shah J.V., Botvinick E., Bonday Z., Furnari F., Berns M., Cleveland D.W. Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr. Biol. 2004, 14:942-952.
35. Sironi L., Melixetian M., Faretta M., Prosperini E., Helin K., Musacchio A. Mad2 binding to Mad1 and Cdc20, rather than oligomerization, is required for the spindle checkpoint. EMBO J. 2001, 20:6371-6382.
36. Sironi L., Mapelli M., Knapp S., De Antoni A., Jeang K.T., Musacchio A. Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a 'safety belt' binding mechanism for the spindle checkpoint. EMBO J. 2002, 21:2496-2506.
37. Sudakin V., Chan G.K., 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. 2001, 154:925-936.
38. Tang Z., Yu H. Functional analysis of the spindle-checkpoint proteins using an invitro ubiquitination assay. Methods Mol. Biol. 2004, 281:227-242.
39. Tang Z., Bharadwaj R., Li B., Yu H. Mad2-Independent inhibition of APCCdc20 by the mitotic checkpoint protein BubR1. Dev. Cell 2001, 1:227-237.
40. Teichner A., Eytan E., Sitry-Shevah D., Miniowitz-Shemtov S., Dumin E., Gromis J., Hershko A. p31comet Promotes disassembly of the mitotic checkpoint complex in an ATP-dependent process. Proc. Natl. Acad. Sci. USA 2011, 108:3187-3192.
41. Tighe A., Johnson V.L., Taylor S.S. Truncating APC mutations have dominant effects on proliferation, spindle checkpoint control, survival and chromosome stability. J.Cell Sci. 2004, 117:6339-6353.
42. Tipton A.R., Wang K., Link L., Bellizzi J.J., Huang H., Yen T., Liu S.T. BUBR1 and closed MAD2 (C-MAD2) interact directly to assemble a functional mitotic checkpoint complex. J.Biol. Chem. 2011, 286:21173-21179.
43. Tugendreich S., Tomkiel J., Earnshaw W., Hieter P. CDC27Hs colocalizes with CDC16Hs to the centrosome and mitotic spindle and is essential for the metaphase to anaphase transition. Cell 1995, 81:261-268.
44. Varetti G., Guida C., Santaguida S., Chiroli E., Musacchio A. Homeostatic control of mitotic arrest. Mol. Cell 2011, 44:710-720.
45. Vink M., Simonetta M., Transidico P., Ferrari K., Mapelli M., De Antoni A., Massimiliano L., Ciliberto A., Faretta M., Salmon E.D., Musacchio A. Invitro FRAP identifies the minimal requirements for Mad2 kinetochore dynamics. Curr. Biol. 2006, 16:755-766.
46. Weiss E., Winey M. The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J.Cell Biol. 1996, 132:111-123.
47. Westhorpe F.G., Tighe A., Lara-Gonzalez P., Taylor S.S. p31comet-mediated extraction of Mad2 from the MCC promotes efficient mitotic exit. J.Cell Sci. 2011, 124:3905-3916.
48. Wu H., Lan Z., Li W., Wu S., Weinstein J., Sakamoto K.M., Dai W. p55CDC/hCDC20 is associated with BUBR1 and may be a downstream target of the spindle checkpoint kinase. Oncogene 2000, 19:4557-4562.
49. Yang M., Li B., Tomchick D.R., Machius M., Rizo J., Yu H., Luo X. p31comet blocks Mad2 activation through structural mimicry. Cell 2007, 131:744-755.
50. Yang M., Li B., Liu C.J., Tomchick D.R., Machius M., Rizo J., Yu H., Luo X. Insights into mad2 regulation in the spindle checkpoint revealed by the crystal structure of the symmetric mad2 dimer. PLoS Biol. 2008, 6:e50.