Determinants of conformational dimerization of Mad2 and its inhibition by p31comet

EMBO Journal

Volumn 25, Issue 6, 2006, Pages 1273-1284

  Mapelli, Marina ^a,b   Filipp, Fabian V ^c   Rancati, Giulia ^d   Massimiliano, Lucia ^a,b   Nezi, Luigi ^a   Stier, Gunter ^c   Hagan, Robert S ^e   Confalonieri, Stefano ^b   Piatti, Simonetta ^d   Sattler, Michael ^c   Musacchio, Andrea ^a,b  

^a EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY OF MILANO BICOCCA   (Italy)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cdc20; Centromere; Kinetochore; Mitosis; Mitotic arrest deficient; Spindle assembly checkpoint

Indexed keywords

BINDING PROTEIN; CELL CYCLE PROTEIN 20; P31 PROTEIN; PROTEIN MAD1; PROTEIN MAD2; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CENTROMERE; DIMERIZATION; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; BINDING SITES; CALCIUM-BINDING PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; DIMERIZATION; HUMANS; KINETOCHORES; MITOTIC SPINDLE APPARATUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID;

SACCHAROMYCES CEREVISIAE;

EID: 33645315214     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601033     Document Type: Article

References (44)

1. Aravind L, Koonin EV (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23: 284-280
2. Bharadwaj R, Yu H (2004) The spindle checkpoint, aneuploidy, and cancer. Oncogene 23: 2016-2027
3. Chan GK, Liu ST, Yen TJ (2005) Kinetochore structure and function. Trends Cell Biol 15: 589-598
4. 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
5. Chen RH, Brady DM, Smith D, Murray AW, Hardwick KG (1999) The spindle checkpoint of budding yeast depends on a tight complex between the Mad1 and Mad2 proteins. Mol Biol Cell 10: 2007-2618
6. Chen RH, Shevchenko A, Mann M, Murray AW (1998) Spindle checkpoint protein Xmad1 recruits Xmad2 to unattached kinetochores. J Cell Biol 143: 283-295
7. Chung E, Chen R-H (2002) Spindle checkpoint requires Mad1-bound and Mad1-free Mad2. Mol Biol Cell 13: 1501-1511
8. Cleveland DW, Mao Y, Sullivan KF (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112: 407-421
9. De Antoni A, Pearson CG, Cimini D, Canman JC, Sala V, Nezi L, Mapelli M, Sironi L, Faretta M, Salmon ED, Musacchio A (2005a) The madl/mad2 complex as a template for mad2 activation in the spindle assembly checkpoint. Curr Biol 15: 214-225
10. De Antoni A, Sala V, Musacchio A (2005b) Explaining the oligomerization properties of the spindle assembly checkpoint protein Mad2. Philos Trans R Soc Lond B Biol Sci 360: 637-647, discussion 447-638
11. Epstein CB, Cross FR (1992) CLB5: a novel B cyclin from budding yeast with a role in S phase. Genes Dev 6: 1695-1706
12. Fang G (2002) Checkpoint protein BubR1 acts synergistically with Mad2 to inhibit anaphase-promoting complex. Mol Biol Cell 13: 755-766
13. Fang G, Yu H, Kirschner MW (1998) 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: 1871-1883
14. Fraschini R, Beretta A, Sironi L, Musacchio A, Lucchini G, Piatti S (2001) Bub3 interaction with Mad2, Mad3 and Cdc20 is mediated by WD40 repeats and does not require intact kinetochores. EMBO J 20: 6648-6659
15. Habu T, Kim SH, Weinstein J, Matsumoto T (2002) Identification of a MAD2-binding protein, CMT2, and its role in mitosis. EMBO J 21: 6419-6428
16. Hagan RS, Sorger PK (2005) Cell biology: the more MAD, the merrier. Nature 434: 575-577
17. Hardwick KG (2005) Checkpoint signalling: Mad2 conformers and signal propagation. Curr Biol 15: R122-R124
18. Hardwick KG, Johnston RC, Smith DL, Murray AW (2000) MAD3 encodes a novel component of the spindle checkpoint which interacts with Bub3p, Cdc20p, and Mad2p. J Cell Biol 148: 871-882
19. Howell BJ, McEwen BF, Canman JC, Hoffman DB, Farrar EM, Rieder CL, Salmon ED (2001) Cytoplasmic dynein/dynactin drives kinetochore protein transport to the spindle poles and has a role in mitotic spindle checkpoint inactivation. J Cell Biol 155: 1159-1172
20. Hoyt MA, Totis L, Roberts BT (1991) S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66: 507-517
21. Hwang LH, Lau LF, Smith DL, Mistrot CA, Hardwick KG, Hwang ES, Amon A, Murray AW (1998) Budding yeast Cdc20: a target of the spindle checkpoint. Science 279: 1041-1044
22. Kallio M, Weinstein J, Daum JR, Burke DJ, Gorbsky GJ (1998) Mammalian p55CDC mediates association of the spindle checkpoint protein Mad2 with the cyclosome/anaphase-promoting complex, and is involved in regulating anaphase onset and late mitotic events. J Cell Biol 141: 1393-1406
23. Kim SH, Lin DP, Matsumoto S, Kitazono A, Matsumoto T (1998) Fission yeast Slp1: an effector of the Mad2-dependent spindle checkpoint. Science 279: 1045-1047
24. Li R, Murray A (1991) Feedback control of mitosis in budding yeast. Cell 66: 519-531
25. Luo X, Fang G, Coldiron M, Lin Y, Yu H, Kirschner MW, Wagner G (2000) Structure of the mad2 spindle assembly checkpoint protein and its interaction with cdc20. Nat Struct Biol 7: 224-229
26. Luo X, Tang Z, Rizo J, 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
27. Luo X, Tang Z, Xia G, Wassmann K, Matsumoto T, Rizo J, Yu H (2004) The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat Struct Mol Biol 11: 338-345
28. Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91: 35-45
29. Morrow CJ, Tighe A, Johnson VL, Scott MI, Ditchfield C, Taylor SS (2005) Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J Cell Sci 118: 3639-3652
30. Musacchio A, Hardwick KG (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat Rev Mol Cell Biol 3: 731-741
31. Nasmyth K (2005) How do so few control so many? Cell 120: 739-746
32. Pinsky BA, Biggins S (2005) The spindle checkpoint: tension versus attachment. Trends Cell Biol 15: 486-493
33. Poddar A, Stukenberg PT, Burke DJ (2005) Two complexes of spindle checkpoint proteins containing Cdc20 and Mad2 assemble during mitosis independently of the kinetochore in Saccharomyces cerevisiae. Eukaryot Cell 4: 867-878
34. Sattler M, Schleucher J, Griesinger C (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog NMR Spectrosc 34: 93-158
35. Shah JV, Botvinick E, Bonday Z, Furnari F, Berns M, Cleveland DW (2004) Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr Biol 14: 942-952
36. Shannon KB, Canman JC, Salmon ED (2002) Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol Biol Cell 13: 3706-3719
37. Sherman F (2002) Getting started with yeast. Methods Enzymol 350: 3-41
38. Sironi L, Mapelli M, Knapp S, Antoni AD, Jeang K-T, Musacchio A (2002) Crystal structure of the tetrameric Madl-Mad2 core complex: implications of a 'safety belt' binding mechanism for the spindle checkpoint. EMBO J 21: 2496-2506
39. Sironi L, Melixetian M, Faretta M, Prosperini E, Helin K, Musacchio A (2001) Mad2 binding to Mad1 and Cdc20, rather than oligomerization, is required for the spindle checkpoint. EMBO J 20: 6371-6382
40. Sudakin V, Chan GK, Yen TJ (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
41. Tang Z, Bharadwaj R, Li B, Yu H (2001) Mad2-independent inhibition of APC-Cdc20 by the mitotic checkpoint protein Bub1R. Dev Cell 1: 227-237
42. Wassmann K, Benezra R (1998) Mad2 transiently associates with an APC/p55Cdc complex during mitosis. Proc Natl Acad Sci USA 95: 11193-11198
43. Wassmann K, Liberal V, Benezra R (2003) Mad2 phosphorylation regulates its association with Mad1 and the APC/C. EMBO J 22: 797-806
44. Xia G, Luo X, Habu T, Rizo J, Matsumoto T, Yu H (2004) Conformation-specific binding of p31(comet) antagonizes the function of Mad2 in the spindle checkpoint. EMBO J 23: 3133-3143