Mimicking Ndc80 phosphorylation triggers spindle assembly checkpoint signalling

EMBO Journal

Volumn 28, Issue 8, 2009, Pages 1099-1110

  Kemmler, Stefan ^a,c   Stach, Manuel ^a   Knapp, Maria ^a   Ortiz, Jennifer ^a   Pfannstiel, Jens ^a,d   Ruppert, Thomas ^b   Lechner, Johannes ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b P   (Germany)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

Centromere; Kinetochore; Mps1; Ndc80; Spindle assembly checkpoint

Indexed keywords

ALANINE; ASPARTIC ACID; NDC80 COMPLEX; NOCODAZOLE; PROTEIN KINASE; PROTEIN KINASE MPS1; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE ARREST; CENTROMERE; IN VITRO STUDY; IN VIVO STUDY; METAPHASE; MICROTUBULE ASSEMBLY; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SPINDLE ASSEMBLY CHECKPOINT; WILD TYPE;

SACCHAROMYCES CEREVISIAE;

EID: 67349247484     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.62     Document Type: Article

References (38)

1. Ahonen LJ, Kallio MJ, Daum JR, Bolton M, Manke IA, Yaffe MB, Stukenberg PT, Gorbsky GJ (2005) Polo-like kinase 1 creates the tension-sensing 3F3/2 phosphoepitope and modulates the asso- ciation of spindle-checkpoint proteins at kinetochores. Curr Biol15: 1078-1089
2. Biggins S, Murray AW (2001) The budding yeast protein kinase Ipll/ Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev 15: 3118-3129
3. Castillo AR, Meehl JB, Morgan G, Schutz-Geschwender A, Winey M (2002) The yeast protein kinase Mpslp is required for assembly of the integral spindle pole body component Spc42p. J Cell Biol 156:453-465
4. Chan GK, Liu ST, Yen TJ (2005) Kinetochore structure and function. Trends Cell Biol 15: 589-598
5. Cheeseman IM, Anderson S, Jwa M, Green EM, Rang J, Yates III JR, Chan CS, Drubin DG, Barnes G (2002) Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipllp. Cell 111: 163-172
6. Cheeseman IM, Chappie JS, Wilson-Rubalek EM, Desai A (2006) The conserved RMN network constitutes the core microtubule- binding site of the kinetochore. Cell 127: 983-997
7. Ciferri C, De Luca J, Monzani S, Ferrari RJ, Ristic D, Wyman C, Stark H, Kilmartin J, Salmon ED, Musacchio A (2005) Architecture of the human ndc80-hecl complex, a critical con- stituent of the outer kinetochore. J Biol Chem 280: 29088-29095
8. Ciferri C, Pasqualato S, Screpanti E, Varetti G, Santaguida S, Dos Reis G, Maiolica A, Polka J, De Luca JG, De Wulf P, Salek M, Rappsilber J, Moores CA, Salmon ED, Musacchio A (2008) Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex. Cell 133: 427-439
9. DeLuca JG, Gall WE, Ciferri C, Cimini D, Musacchio A, Salmon ED (2006) Rinetochore microtubule dynamics and attachment stabi- lity are regulated by Hecl. Cell 127: 969-982
10. DeLuca JG, Howell BJ, Canman JC, Hickey JM, Fang G, Salmon ED (2003) Nuf2 and Hecl are required for retention of the checkpoint proteins Madl and Mad2 to kinetochores. Curr Biol 13: 2103-2109
11. Fraschini R, Beretta A, Lucchini G, Piatti S (2001) Role of the kinetochore protein Ndcl0 in mitotic checkpoint activation in Saccharomyces cerevisiae. Mol Genet Genomics 266: 115-125
12. Gillett ES, Espelin CW, Sorger PR (2004) Spindle checkpoint pro- teins and chromosome-microtubule attachment in budding yeast. J Cell Biol 164: 535-546
13. Goshima G, Yanagida M (2000) Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell100: 619-633
14. Hardwick KG, Weiss E, Luca FC, Winey M, Murray AW (1996) Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 273: 953-956
15. Janke C, Ortiz J, Lechner J, Shevchenko A, Magiera MM, Schramm C, 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
16. Janke C, Ortiz J, Tanaka TU, Lechner J, Schiebel E (2002) Four new subunits of the Daml-Duol complex reveal novel functions in sister kinetochore biorientation. EMBO J 21: 181-193
17. Jelluma N, Brenkman AB, van den Broek NJ, Cruijsen CW, van Osch MH, Lens SM, Medema RH, Kops GJ (2008) Mpsl phos- phorylates Borealin to control Aurora B activity and chromosome alignment. Cell 132: 233-246
18. Joglekar AP, Bouck DC, Molk JN, Bloom KS, Salmon ED (2006) Molecular architecture of a kinetochore-microtubule attachment site. Nat Cell Biol 8: 581-585
19. Jones MH, Huneycutt BJ, Pearson CG, Zhang C, Morgan G, Shokat K, Bloom K, Winey M (2005) Chemical genetics reveals a role for Mpsl kinase in kinetochore attachment during mitosis. Curr Biol15: 160-165
20. Kerscher 0, Crotti LB, Basrai MA (2003) Recognizing chromosomes in trouble: association of the spindle checkpoint protein Bub3p with altered kinetochores and a unique defective centromere. Mol Cell Biol 23: 6406-6418
21. Lauze E, Stoelcker B, Luca FC, Weiss E, Schutz AR, Winey M (1995) Yeast spindle pole body duplication gene MPS1 encodes an essential dual specificity protein kinase. EMBO J 14:1655-1663
22. Li Y, Bachant J, Alcasabas AA, Wang Y, Qin J, Elledge SJ (2002) The mitotic spindle is required for loading of the DASH complex onto the kinetochore. Genes Dev 16: 183-197
23. Martin-Lluesma S, Stucke VM, Nigg EA (2002) Role of Hecl in spindle checkpoint signaling and kinetochore recruitment of Madl/Mad2. Science 297: 2267-2270
24. Maure JF, Kitamura E, Tanaka TU (2007) Mpsl kinase promotes sister-kinetochore bi-orientation by a tension-dependent mechan- ism. Curr Biol 17: 2175-2182
25. McCleland ML, Gardner RD, Kallio MJ, Daum JR, Gorbsky GJ, Burke DJ, Stukenberg PT (2003) The highly conserved Ndc80 complex is required for kinetochore assembly, chromo- some congression, and spindle checkpoint activity. Genes Dev 17: 101-114
26. Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393
27. Nakajima H, Toyoshima-Morimoto F, Taniguchi E, Nishida E (2003) Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Mytl as a Plk1 substrate. J Biol Chem 278: 25277-25280
28. Nicklas RB, Ward SC, Gorbsky GJ (1995) Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J Cell Biol 130: 929-939
29. Palframan WJ, Meehl JB, Jaspersen SL, Winey M, Murray AW (2006) Anaphase inactivation of the spindle checkpoint. Science 313: 680-684
30. Sandall S, Severin F, McLeod IX, Yates III JR, Oegema K, Hyman A, Desai A (2006) A Birl-Slil5 complex connects centromeres to microtubules and is required to sense kinetochore tension. Cell 127: 1179-1191
31. Shimogawa MM, Graczyk B, Gardner MK, Francis SE, White EA, Ess M, Molk JN, Ruse C, Niessen S, Yates III JR, Muller EG, Bloom K, Odde DJ, Davis TN (2006) Mpsl phosphorylation of Daml couples kinetochores to microtubule plus ends at metaphase. Curr Biol 16: 1489-1501
32. Tanaka TU, Rachidi N, Janke C, Pereira G, Galova M, Schiebel E, Stark MJ, Nasmyth K (2002) Evidence that the Ipll-Slil5 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell 108: 317-329
33. Vigneron S, Prieto S, Bernis C, Labbe JC, Castro A, Lorca T (2004) Kinetochore localization of spindle checkpoint proteins: who controls whom? Mol Biol Cell 15: 4584-4596
34. Wei RR, Al-Bassam J, Harrison SC (2007) The Ndc80/HEC1 com- plex is a contact point for kinetochore-microtubule attachment. Nat Struct Mol Biol 14: 54-59
35. Wei RR, Sorger PK, Harrison SC (2005) Molecular organization of the Ndc80 complex, an essential kinetochore component. Proc Natl Acad Sci USA 102: 5363-5367
36. Weiss E, Winey M (1996) The Saccharomyces cerevisiae spindle pole body duplication gene MPS1 is part of a mitotic checkpoint. J Cell Biol 132: 111-123
37. Winey M, Goetsch L, Baum P, Byers B (1991) MPS1 and MPS2: novel yeast genes defining distinct steps of spindle pole body duplication. J Cell Biol 114: 745-754
38. Wong OK, Fang G (2005) Plxl is the 3F3/2 kinase responsible for targeting spindle checkpoint proteins to kinetochores. J Cell Biol 170: 709-719