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: 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

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa