Bub1 Maintains Centromeric Cohesion by Activation of the Spindle Checkpoint

Developmental Cell

Volumn 13, Issue 4, 2007, Pages 566-579

  Perera, David ^a   Tilston, Valerie ^a   Hopwood, Jane A ^a   Barchi, Marco ^b   Boot Handford, Raymond P ^a   Taylor, Stephen S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

CELLCYCLE

Indexed keywords

BUB1 PROTEIN; NUCLEAR PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE REGULATION; CELL PROLIFERATION; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FIBROBLAST; HOMEOSTASIS; MALE; MALE INFERTILITY; MITOSIS INHIBITION; MITOSIS SPINDLE; MOUSE; MOUSE STRAIN; NIDATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SEMINIFEROUS TUBULE; SPERMATOGENESIS; TISSUE METABOLISM;

ANIMALS; BLASTOCYST; CELL PROLIFERATION; CELLS, CULTURED; CENTROMERE; CHROMOSOME SEGREGATION; EMBRYO LOSS; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FIBROBLASTS; INFERTILITY, MALE; KINETOCHORES; MALE; MICE; MITOTIC SPINDLE APPARATUS; PROTEIN-SERINE-THREONINE KINASES; SPERMATOGENESIS;

EID: 34848910184     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2007.08.008     Document Type: Article

References (46)

1. Babu J.R., Jeganathan K.B., Baker D.J., Wu X., Kang-Decker N., and van Deursen J.M. Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J. Cell Biol. 160 (2003) 341-353
2. Baker D.J., Jeganathan K.B., Cameron J.D., Thompson M., Juneja S., Kopecka A., Kumar R., Jenkins R.B., de Groen P.C., Roche P., and van Deursen J.M. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat. Genet. 36 (2004) 744-749
3. Baker D.J., Jeganathan K.B., Malureanu L., Perez-Terzic C., Terzic A., and van Deursen J.M. Early aging-associated phenotypes in Bub3/Rae1 haploinsufficient mice. J. Cell Biol. 172 (2006) 529-540
4. Bernard P., Hardwick K., and Javerzat J.P. Fission yeast bub1 is a mitotic centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis. J. Cell Biol. 143 (1998) 1775-1787
5. Burds A.A., Lutum A.S., and Sorger P.K. Generating chromosome instability through the simultaneous deletion of Mad2 and p53. Proc. Natl. Acad. Sci. USA 102 (2005) 11296-11301
6. Dai W., Wang Q., Liu T., Swamy M., Fang Y., Xie S., Mahmood R., Yang Y.M., Xu M., and Rao C.V. Slippage of mitotic arrest and enhanced tumor development in mice with BubR1 haploinsufficiency. Cancer Res. 64 (2004) 440-445
7. Dobles M., Liberal V., Scott M.L., Benezra R., and Sorger P.K. Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101 (2000) 635-645
8. Fukagawa T., Nogami M., Yoshikawa M., Ikeno M., Okazaki T., Takami Y., Nakayama T., and Oshimura M. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat. Cell Biol. 6 (2004) 784-791
9. Gillett E.S., Espelin C.W., and Sorger P.K. Spindle checkpoint proteins and chromosome-microtubule attachment in budding yeast. J. Cell Biol. 164 (2004) 535-546
10. Gorbsky G.J., Chen R.H., and Murray A.W. Microinjection of antibody to Mad2 protein into mammalian cells in mitosis induces premature anaphase. J. Cell Biol. 141 (1998) 1193-1205
11. Hagting A., Den Elzen N., Vodermaier H.C., Waizenegger I.C., Peters J.M., and Pines J. Human securin proteolysis is controlled by the spindle checkpoint and reveals when the APC/C switches from activation by Cdc20 to Cdh1. J. Cell Biol. 157 (2002) 1125-1137
12. Hayashi S., and McMahon A.P. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: A tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244 (2002) 305-318
13. Hoyt M.A., Totis L., and Roberts B.T. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66 (1991) 507-517
14. Huang H., Feng J., Famulski J., Rattner J.B., Liu S.T., Kao G.D., Muschel R., Chan G.K., and Yen T.J. Tripin/hSgo2 recruits MCAK to the inner centromere to correct defective kinetochore attachments. J. Cell Biol. 177 (2007) 413-424
15. Hussein D., and Taylor S.S. Farnesylation of Cenp-F is required for G2/M progression and degradation after mitosis. J. Cell Sci. 115 (2002) 3403-3414
16. Iwanaga Y., Chi Y.H., Miyazato A., Sheleg S., Haller K., Peloponese Jr. J.M., Li Y., Ward J.M., Benezra R., and Jeang K.T. Heterozygous deletion of mitotic arrest-deficient protein 1 (MAD1) increases the incidence of tumors in mice. Cancer Res. 67 (2007) 160-166
17. Johnson V.L., Scott M.I., Holt S.V., Hussein D., and Taylor S.S. Bub1 is required for kinetochore localization of BubR1, Cenp-E, Cenp-F and Mad2, and chromosome congression. J. Cell Sci. 117 (2004) 1577-1589
18. Kalitsis P., Earle E., Fowler K.J., and Choo K.H. Bub3 gene disruption in mice reveals essential mitotic spindle checkpoint function during early embryogenesis. Genes Dev. 14 (2000) 2277-2282
19. Kalitsis P., Fowler K.J., Griffiths B., Earle E., Chow C.W., Jamsen K., and Choo K.H. Increased chromosome instability but not cancer predisposition in haploinsufficient Bub3 mice. Genes Chromosomes Cancer 44 (2005) 29-36
20. Kawashima S.A., Tsukahara T., Langegger M., Hauf S., Kitajima T.S., and Watanabe Y. Shugoshin enables tension-generating attachment of kinetochores by loading Aurora to centromeres. Genes Dev. 21 (2007) 420-435
21. Kitajima T.S., Hauf S., Ohsugi M., Yamamoto T., and Watanabe Y. Human Bub1 defines the persistent cohesion site along the mitotic chromosome by affecting Shugoshin localization. Curr. Biol. 15 (2005) 353-359
22. Kitajima T.S., Kawashima S.A., and Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427 (2004) 510-517
23. Kitajima T.S., Sakuno T., Ishiguro K., Iemura S., Natsume T., Kawashima S.A., and Watanabe Y. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441 (2006) 46-52
24. Kops G.J., Foltz D.R., and Cleveland D.W. Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc. Natl. Acad. Sci. USA 101 (2004) 8699-8704
25. Li R., and Murray A.W. Feedback control of mitosis in budding yeast. Cell 66 (1991) 519-531
26. Loonstra A., Vooijs M., Beverloo H.B., Allak B.A., van Drunen E., Kanaar R., Berns A., and Jonkers J. Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc. Natl. Acad. Sci. USA 98 (2001) 9209-9214
27. Meraldi P., Draviam V.M., and Sorger P.K. Timing and checkpoints in the regulation of mitotic progression. Dev. Cell 7 (2004) 45-60
28. Meraldi P., and Sorger P.K. A dual role for Bub1 in the spindle checkpoint and chromosome congression. EMBO J. 24 (2005) 1621-1633
29. Michel L.S., Liberal V., Chatterjee A., Kirchwegger R., Pasche B., Gerald W., Dobles M., Sorger P.K., Murty V.V., and Benezra R. MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409 (2001) 355-359
30. Morrow C.J., Tighe A., Johnson V.L., Scott M.I., Ditchfield C., and Taylor S.S. Bub1 and aurora B cooperate to maintain BubR1-mediated inhibition of APC/CCdc20. J. Cell Sci. 118 (2005) 3639-3652
31. Musacchio A., and Salmon E.D. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8 (2007) 379-393
32. Nagy A., Gertsenstein M., Vintersten K., and Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual. Third Edition (2003), Cold Spring Harbor Laboratory Press, New York
33. Peters J.M. The anaphase promoting complex/cyclosome: A machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7 (2006) 644-656
34. Putkey F.R., Cramer T., Morphew M.K., Silk A.D., Johnson R.S., McIntosh J.R., and Cleveland D.W. Unstable kinetochore-microtubule capture and chromosomal instability following deletion of CENP-E. Dev. Cell 3 (2002) 351-365
35. Riedel C.G., Katis V.L., Katou Y., Mori S., Itoh T., Helmhart W., Galova M., Petronczki M., Gregan J., Cetin B., et al. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441 (2006) 53-61
36. Salic A., Waters J.C., and Mitchison T.J. Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis. Cell 118 (2004) 567-578
37. Silver D.P., and Livingston D.M. Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol. Cell 8 (2001) 233-243
38. Tang Z., Shu H., Qi W., Mahmood N.A., Mumby M.C., and Yu H. PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation. Dev. Cell 10 (2006) 575-585
39. Tang Z., Sun Y., Harley S.E., Zou H., and Yu H. Human Bub1 protects centromeric sister-chromatid cohesion through Shugoshin during mitosis. Proc. Natl. Acad. Sci. USA 101 (2004) 18012-18017
40. Taylor S.S., Ha E., and McKeon F. The human homologue of Bub3 is required for kinetochore localization of Bub1 and a Mad3/Bub1-related protein kinase. J. Cell Biol. 142 (1998) 1-11
41. Taylor S.S., Hussein D., Wang Y., Elderkin S., and Morrow C.J. 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 (2001) 4385-4395
42. Taylor S.S., and McKeon F. Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell 89 (1997) 727-735
43. Vanoosthuyse V., Prykhozhij S., and Hardwick K.G. Shugoshin 2 regulates localization of the chromosomal passenger proteins in fission yeast mitosis. Mol. Biol. Cell 18 (2007) 1657-1669
44. Wang Q., Liu T., Fang Y., Xie S., Huang X., Mahmood R., Ramaswamy G., Sakamoto K.M., Darzynkiewicz Z., Xu M., and Dai W. BUBR1 deficiency results in abnormal megakaryopoiesis. Blood 103 (2004) 1278-1285
45. Warren C.D., Brady D.M., Johnston R.C., Hanna J.S., Hardwick K.G., and Spencer F.A. Distinct chromosome segregation roles for spindle checkpoint proteins. Mol. Biol. Cell 13 (2002) 3029-3041
46. Weaver B.A., Bonday Z.Q., Putkey F.R., Kops G.J., Silk A.D., and Cleveland D.W. Centromere-associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to single chromosome loss. J. Cell Biol. 162 (2003) 551-563