Bub1-Mediated Adaptation of the Spindle Checkpoint
During cell division, the spindle checkpoint ensures accurate chromosome segregation by monitoring the kinetochore–microtubule interaction and delaying the onset of anaphase until each pair of sister chromosomes is properly attached to microtubules. The spindle checkpoint is deactivated as chromosomes start moving toward the spindles in anaphase, but the mechanisms by which this deactivation and adaptation to prolonged mitotic arrest occur remain obscure. Our results strongly suggest that Cdc28-mediated phosphorylation of Bub1 at T566 plays an important role for the degradation of Bub1 in anaphase, and the phosphorylation is required for adaptation of the spindle checkpoint to prolonged mitotic arrest.
Vyšlo v časopise:
Bub1-Mediated Adaptation of the Spindle Checkpoint. PLoS Genet 7(1): e32767. doi:10.1371/journal.pgen.1001282
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001282
Souhrn
During cell division, the spindle checkpoint ensures accurate chromosome segregation by monitoring the kinetochore–microtubule interaction and delaying the onset of anaphase until each pair of sister chromosomes is properly attached to microtubules. The spindle checkpoint is deactivated as chromosomes start moving toward the spindles in anaphase, but the mechanisms by which this deactivation and adaptation to prolonged mitotic arrest occur remain obscure. Our results strongly suggest that Cdc28-mediated phosphorylation of Bub1 at T566 plays an important role for the degradation of Bub1 in anaphase, and the phosphorylation is required for adaptation of the spindle checkpoint to prolonged mitotic arrest.
Zdroje
1. InoueS
SalmonED
1995 Force generation by microtubule assembly/disassembly in mitosis and related movements. Mol Biol Cell 6 1619 1640
2. MichaelisC
CioskR
NasmythK
1997 Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91 35 45
3. RiederCL
SchultzA
ColeR
SluderG
1994 Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J Cell Biol 127 1301 1310
4. SchaarBT
ChanGK
MaddoxP
SalmonED
YenTJ
1997 CENP-E function at kinetochores is essential for chromosome alignment. J Cell Biol 139 1373 1382
5. SkibbensRV
SkeenVP
SalmonED
1993 Directional instability of kinetochore motility during chromosome congression and segregation in mitotic newt lung cells: a push-pull mechanism. J Cell Biol 122 859 875
6. SkibbensRV
RiederCL
SalmonED
1995 Kinetochore motility after severing between sister centromeres using laser microsurgery: evidence that kinetochore directional instability and position is regulated by tension. J Cell Sci 108 Pt 7 2537 2548
7. WoodKW
SakowiczR
GoldsteinLS
ClevelandDW
1997 CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment. Cell 91 357 366
8. GuacciV
HoganE
KoshlandD
1994 Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol 125 517 530
9. CioskR
ZachariaeW
MichaelisC
ShevchenkoA
MannM
1998 An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93 1067 1076
10. UhlmannF
LottspeichF
NasmythK
1999 Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400 37 42
11. UhlmannF
WernicD
PoupartMA
KooninEV
NasmythK
2000 Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103 375 386
12. Cohen-FixO
PetersJM
KirschnerMW
KoshlandD
1996 Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev 10 3081 3093
13. RudnerAD
MurrayAW
1996 The spindle assembly checkpoint. Curr Opin Cell Biol 8 773 780
14. LiR
MurrayAW
1991 Feedback control of mitosis in budding yeast. Cell 66 519 531
15. HoytMA
TotisL
RobertsBT
1991 S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66 507 517
16. WellsWA
MurrayAW
1996 Aberrantly segregating centromeres activate the spindle assembly checkpoint in budding yeast. J Cell Biol 133 75 84
17. PalframanWJ
MeehlJB
JaspersenSL
WineyM
MurrayAW
2006 Anaphase inactivation of the spindle checkpoint. Science 313 680 684
18. VanoosthuyseV
HardwickKG
2009 A novel protein phosphatase 1-dependent spindle checkpoint silencing mechanism. Curr Biol 19 1176 1181
19. PinskyBA
NelsonCR
BigginsS
2009 Protein phosphatase 1 regulates exit from the spindle checkpoint in budding yeast. Curr Biol 19 1182 1187
20. KungAL
SherwoodSW
SchimkeRT
1990 Cell line-specific differences in the control of cell cycle progression in the absence of mitosis. Proc Natl Acad Sci U S A 87 9553 9557
21. RiederCL
PalazzoRE
1992 Colcemid and the mitotic cycle. J Cell Sci 102 Pt 3 387 392
22. MinshullJ
StraightA
RudnerAD
DernburgAF
BelmontA
1996 Protein phosphatase 2A regulates MPF activity and sister chromatid cohesion in budding yeast. Curr Biol 6 1609 1620
23. UbersaxJA
WoodburyEL
QuangPN
ParazM
BlethrowJD
2003 Targets of the cyclin-dependent kinase Cdk1. Nature 425 859 864
24. FarrKA
HoytMA
1998 Bub1p kinase activates the Saccharomyces cerevisiae spindle assembly checkpoint. Mol Cell Biol 18 2738 2747
25. De BrabanderMJ
Van de VeireRM
AertsFE
BorgersM
JanssenPA
1976 The effects of methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) carbamate, (R 17934; NSC 238159), a new synthetic antitumoral drug interfering with microtubules, on mammalian cells cultured in vitro. Cancer Res 36 905 916
26. FerniusJ
HardwickKG
2007 Bub1 kinase targets Sgo1 to ensure efficient chromosome biorientation in budding yeast mitosis. PLoS Genet 3 e213 doi:10.1371/journal.pgen.0030213
27. KoshlandD
HieterP
1987 Visual assay for chromosome ploidy. Methods Enzymol 155 351 372
28. SheroJH
KovalM
SpencerF
PalmerRE
HieterP
1991 Analysis of chromosome segregation in Saccharomyces cerevisiae. Methods Enzymol 194 749 773
29. MontpetitB
HazbunTR
FieldsS
HieterP
2006 Sumoylation of the budding yeast kinetochore protein Ndc10 is required for Ndc10 spindle localization and regulation of anaphase spindle elongation. J Cell Biol 174 653 663
30. QiW
YuH
2007 KEN-box-dependent degradation of the Bub1 spindle checkpoint kinase by the anaphase-promoting complex/cyclosome. J Biol Chem 282 3672 3679
31. TaylorSS
HusseinD
WangY
ElderkinS
MorrowCJ
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
32. BradyDM
HardwickKG
2000 Complex formation between Mad1p, Bub1p and Bub3p is crucial for spindle checkpoint function. Curr Biol 10 675 678
33. RudnerAD
HardwickKG
MurrayAW
2000 Cdc28 activates exit from mitosis in budding yeast. J Cell Biol 149 1361 1376
34. RudnerAD
MurrayAW
2000 Phosphorylation by Cdc28 activates the Cdc20-dependent activity of the anaphase-promoting complex. J Cell Biol 149 1377 1390
35. YamaguchiS
DecottigniesA
NurseP
2003 Function of Cdc2p-dependent Bub1p phosphorylation and Bub1p kinase activity in the mitotic and meiotic spindle checkpoint. EMBO J 22 1075 1087
36. KangJ
YangM
LiB
QiW
ZhangC
2008 Structure and substrate recruitment of the human spindle checkpoint kinase Bub1. Mol Cell 32 394 405
37. KitagawaK
NiikuraY
2008 Caspase-independent mitotic death (CIMD). Cell Cycle 7 1001 1005
38. NiikuraY
DixitA
ScottR
PerkinsG
KitagawaK
2007 BUB1 mediation of caspase-independent mitotic death determines cell fate. J Cell Biol 178 283 296
39. RoseMD
WinstonF
HieterP
1990 Methods in Yeast Genetics: Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
40. LongtineMS
McKenzieA3rd
DemariniDJ
ShahNG
WachA
1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 953 961
41. KitagawaK
AbdulleR
2002 In vivo site-directed mutagenesis of yeast plasmids using a three-fragment homologous recombination system. Biotechniques 33 288, 290, 292 passim
42. BurtonJL
SolomonMJ
2007 Mad3p, a pseudosubstrate inhibitor of APCCdc20 in the spindle assembly checkpoint. Genes Dev 21 655 667
43. GerringSL
SpencerF
HieterP
1990 The CHL 1 (CTF 1) gene product of Saccharomyces cerevisiae is important for chromosome transmission and normal cell cycle progression in G2/M. EMBO J 9 4347 4358
44. YuenKW
WarrenCD
ChenO
KwokT
HieterP
2007 Systematic genome instability screens in yeast and their potential relevance to cancer. Proc Natl Acad Sci U S A 104 3925 3930
45. KitagawaK
AbdulleR
BansalPK
CagneyG
FieldsS
2003 Requirement of Skp1-Bub1 interaction for kinetochore-mediated activation of the spindle checkpoint. Mol Cell 11 1201 1213
46. KitagawaK
SkowyraD
ElledgeSJ
HarperJW
HieterP
1999 SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol Cell 4 21 33
47. BansalPK
AbdulleR
KitagawaK
2004 Sgt1 associates with Hsp90: an initial step of assembly of the core kinetochore complex. Mol Cell Biol 24 8069 8079
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