Survivin is required for a sustained spindle checkpoint arrest in response to lack of tension

EMBO Journal

Volumn 22, Issue 12, 2003, Pages 2934-2947

  Lens, Susanne M A ^a   Wolthuis, Rob M F ^a   Klompmaker, Rob ^a   Kauw, Jos ^a   Agami, Reuven ^a   Brummelkamp, Thijn ^a   Kops, Geert ^b   Medema, René H ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Checkpoint; Mitosis; Survivin

Indexed keywords

PROTEIN MAD2; SURVIVIN;

ANIMAL CELL; ARTICLE; CELL DIVISION; CENTROMERE; CHROMOSOME; DEPOLYMERIZATION; HUMAN; HUMAN CELL; MAMMAL CELL; MITOSIS INHIBITION; MITOSIS SPINDLE; MOUSE; NONHUMAN; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CELL LINE; CHROMOSOMES, HUMAN; CHROMOSOMES, MAMMALIAN; CYSTEINE PROTEINASE INHIBITORS; GENES, REPORTER; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; NEOPLASM PROTEINS; PACLITAXEL; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PYRIMIDINES; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SPECTRIN; STRESS, MECHANICAL; THIONES;

ANIMALIA; MAMMALIA;

EID: 0038376119     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg307     Document Type: Article

References (48)

1. Adams, R.R., Wheatley, S.P., Gouldsworthy, A.M., Kandels-Lewis, S.E., Carmena, M., Smythe, C., Gerloff, D.L. and Earnshaw, W.C. (2000) INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow. Curr. Biol., 10, 1075-1078.
2. Adams, R.R., Carmena, M. and Earnshaw, W.C. (2001) Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol., 11, 49-54.
3. Biggins, S. and Murray, A.W. (2001) The budding yeast protein kinase Ip11/Aurora allows the absence of tension to activate the spindle checkpoint. Genes Dev., 15, 3118-3129.
4. Bolton, M.A., Lan, W., Powers, S.E., McCleland, M.L., Kuang, J. and Stukenberg, P.T. (2002) Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol. Biol. Cell, 13, 3064-3077.
5. Brummelkamp, T.R., Bernards, R. and Agami, R. (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science, 296, 550-553.
6. Chen, J. et al. (2003) Survivin enhances Aurora-B kinase activity and localizes Aurora-B in human cells. J. Biol. Chem., 278, 486-490.
7. 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.
8. Cutts, S.M. et al. (1999) Defective chromosome segregation, microtubule bundling and nuclear bridging in inner centromere protein gene (Incenp)-disrupted mice. Hum. Mol. Genet., 8, 1145-1155.
9. Deveraux, Q.L. and Reed, J.C. (1999) IAP family proteins - suppressors of apoptosis. Genes Dev., 13, 239-252.
10. Fraser, A.G., James, C., Evan, G.I. and Hengartner, M.O. (1999) Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr. Biol., 9, 292-301.
11. Hauf, S., Waizenegger, I.C. and Peters, J.M. (2001) Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science, 293, 1320-1323.
12. Hoyt, M.A. (2000) Exit from mitosis: spindle pole power. Cell, 102, 267-270.
13. Kalejta, R.F., Shenk, T. and Beavis, A.J. (1997) Use of a membrane-localized green fluorescent protein allows simultaneous identification of transfected cells and cell cycle analysis by flow cytometry. Cytometry, 29, 286-291.
14. Kanda, T., Sullivan, K.F. and Wahl, G.M. (1998) Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol., 8, 377-385.
15. Kapoor, T.M., Mayer, T.U., Coughlin, M.L. and Mitchison, T.J. (2000) Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol., 150, 975-988.
16. Li, F., Ambrosini, G., Chu, E.Y., Plescia, J., Tognin, S., Marchisio, P.C. and Altieri, D.C. (1998) Control of apoptosis and mitotic spindle checkpoint by survivin. Nature, 396, 580-584.
17. Li, F., Ackermann, E.J., Bennett, C.F., Rothermel, A.L., Plescia, J., Tognin, S., Villa, A., Marchisio, P.C. and Altieri, D.C. (1999) Pleiotropic cell-division defects and apoptosis induced by interference with survivin function. Nat. Cell Biol., 1, 461-466.
18. Li, F., Flanary, P.L., Altieri, D.C. and Dohlman, H.G. (2000) Cell division regulation by BIR1, a member of the inhibitor of apoptosis family in yeast. J. Biol. Chem., 275, 6707-6711.
19. Martin-Lluesma, S., Stucke, V.M. and Nigg, E.A. (2002) Role of Hec1 in spindle checkpoint signaling and kinetochore recruitment of Mad1/Mad2. Science, 297, 2267-2270.
20. Mayer, T.U., Kapoor, T.M., Haggarty, S.J., King, R.W., Schreiber, S.L. and Mitchison, T.J. (1999) Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science, 286, 971-974.
21. McEwen, B.F., Heagle, A.B., Cassels, G.O., Buttle, K.F. and Rieder, C.L. (1997) Kinetochore fiber maturation in PtK1 cells and its implications for the mechanisms of chromosome congression and anaphase onset. J. Cell Biol., 137, 1567-1580.
22. kip1. Nature, 404, 782-787.
23. Michaelis, C., Ciosk, R. and Nasmyth, K. (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell, 91, 35-45.
24. Miller, L.K. (1999) An exegesis of IAPs: salvation and surprises from BIR motifs. Trends Cell Biol., 9, 323-328.
25. Musacchio, A. and Hardwick, K.G. (2002) The spindle checkpoint: structural insights into dynamic signalling. Nat. Rev. Mol. Cell Biol., 3, 731-741.
26. Nasmyth, K., Peters, J.M. and Uhlmann, F. (2000) Splitting the chromosome: cutting the ties that bind sister chromatids. Science, 288, 1379-1385.
27. Nicklas, R.B. (1997) How cells get the right chromosomes. Science, 275, 632-637.
28. Peters, J.M. (2002) The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell, 9, 931-943.
29. Pines, J. (1997) Localization of cell cycle regulators by immunofluorescence. Methods Enzymol., 283, 99-113.
30. Shah, J.V. and Cleveland, D.W. (2000) Waiting for anaphase: Mad2 and the spindle assembly checkpoint. Cell, 103, 997-1000.
31. Shannon, K.B., Canman, J.C. and Salmon, E.D. (2002) Mad2 and BubR1 function in a single checkpoint pathway that responds to a loss of tension. Mol. Biol. Cell, 13, 3706-3719.
32. Skoufias, D.A., Mollinari, C., Lacroix, F.B. and Margolis, R.L. (2000) Human survivin is a kinetochore-associated passenger protein. J. Cell Biol., 151, 1575-1582.
33. Skoufias, D.A., Andreassen, P.R., Lacroix, F.B., Wilson, L. and Margolis, R.L. (2001) Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints. Proc. Natl Acad. Sci. USA, 98, 4492-4497.
34. Smits, V.A., Klompmaker, R., Arnaud, L., Rijksen, G., Nigg, E.A. and Medema, R.H. (2000) Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat. Cell Biol., 2, 672-676.
35. Speliotes, E.K., Uren, A., Vaux, D. and Horvitz, H.R. (2000) The survivin-like C. elegans BIR-1 protein acts with the Aurora-like kinase AIR-2 to affect chromosomes and the spindle midzone. Mol. Cell, 6, 211-223.
36. Stemmann, O., Zou, H., Gerber, S.A., Gygi, S.P. and Kirschner, M.W. (2001) Dual inhibition of sister chromatid separation at metaphase. Cell, 107, 715-726.
37. Stern, B.M. (2002) Mitosis: aurora gives chromosomes a healthy stretch. Curr. Biol., 12, R316-R318.
38. Tanaka, T.U. (2002) Bi-orienting chromosomes on the mitotic spindle. Curr. Opin. Cell Biol., 14, 365-371.
39. Tanaka, T.U., Rachidi, N., Janke, C., Pereira, G., Galova, M., Schiebel, E., Stark, M.J. and Nasmyth, K. (2002) Evidence that the Ip11-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell, 108, 317-329.
40. Taylor, S.S., Hussein, D., Wang, Y., Elderkin, S. and Morrow, C.J. (2001) Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells. J. Cell Sci., 114, 4385-4395.
41. Uhlmann, F., Wernic, D., Poupart, M.A., Koonin, E.V. and Nasmyth, K. (2000) Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell, 103, 375-386.
42. Uren, A.G., Beilharz, T., O'Connell, M.J., Bugg, S.J., van Driel, R., Vaux, D.L. and Lithgow, T. (1999) Role for yeast inhibitor of apoptosis (IAP)-like proteins in cell division. Proc. Natl Acad. Sci. USA, 96, 10170-10175.
43. Uren, A.G., Wong, L., Pakusch, M., Fowler, K.J., Burrows, F.J., Vaux, D.L. and Choo, K.H. (2000) Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr. Biol., 10, 1319-1328.
44. van den Heuvel, S. and Harlow, E. (1993) Distinct roles for cyclin-dependent kinases in cell cycle control. Science, 262, 2050-2054.
45. Waters, J.C., Chen, R.H., Murray, A.W. and Salmon, E.D. (1998) Localization of Mad2 to kinetochores depends on microtubule attachment, not tension. J. Cell Biol., 141, 1181-1191.
46. Wheatley, S.P., Carvalho, A., Vagnarelli, P. and Earnshaw, W.C. (2001) INCENP is required for proper targeting of Survivin to the centromeres and the anaphase spindle during mitosis. Curr. Biol., 11, 886-890.
47. Yoon, H.J. and Carbon, J. (1999) Participation of Bir1p, a member of the inhibitor of apoptosis family, in yeast chromosome segregation events. Proc. Natl Acad. Sci. USA, 96, 13208-13213.
48. Zhou, J., Panda, D., Landen, J.W., Wilson, L. and Joshi, H.C. (2002) Minor alteration of microtubule dynamics causes loss of tension across kinetochore pairs and activates the spindle checkpoint. J. Biol. Chem., 277, 17200-17208.