Home LiteratureArticle Details
PMID: 11014800 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Saccharomyces cerevisiae BUB2 prevents mitotic exit in response to both spindle and kinetochore damage.

Genetics ·Vol. 156 ·No. 2 ·2000-10-00 ·Pages 489-500

Krishnan R, Pangilinan F, Lee C, Spencer F

Abstract

The spindle assembly checkpoint-mediated mitotic arrest depends on proteins that signal the presence of one or more unattached kinetochores and prevents the onset of anaphase in the presence of kinetochore or spindle damage. In the presence of either damage, bub2 cells initiate a preanaphase delay but do not maintain it. Inappropriate sister chromatid separation in nocodazole-treated bub2 cells is prevented when mitotic exit is blocked using a conditional tem1(c) mutant, indicating that the preanaphase failure in bub2 cells is a consequence of events downstream of TEM1 in the mitotic exit pathway. Using a conditional bub2(tsd) mutant, we demonstrate that the continuous presence of Bub2 protein is required for maintaining spindle damage-induced arrest. BUB2 is not required to maintain a DNA damage checkpoint arrest, revealing a specificity for spindle assembly checkpoint function. In a yeast two-hybrid assay and in vitro, Bub2 protein interacts with the septin protein Cdc3, which is essential for cytokinesis. These data support the view that the spindle assembly checkpoint encompasses regulation of distinct mitotic steps, including a MAD2-directed block to anaphase initiation and a BUB2-directed block to TEM1-dependent exit.

MeSH Terms
Cell Cycle/genetics Cell Cycle Proteins DNA Damage Fungal Proteins/genetics,metabolism Genotype Kinetochores/ultrastructure Mitosis/genetics Monomeric GTP-Binding Proteins/genetics,metabolism Nocodazole/pharmacology Saccharomyces cerevisiae/cytology,drug effects,genetics Saccharomyces cerevisiae Proteins Spindle Apparatus/genetics,ultrastructure
Chemicals
BUB2 protein, S cerevisiae Cell Cycle Proteins Fungal Proteins Saccharomyces cerevisiae Proteins TEM1 protein, S cerevisiae Monomeric GTP-Binding Proteins Nocodazole
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Krishnan R
Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
Pangilinan F
Lee C
Spencer F
References (44)
44 references, click to expand
  1. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex.
    Cell. 1999 Apr 16;97(2):233-44 PMID: 10219244
  2. Kinetochores and the checkpoint mechanism that monitors for defects in the chromosome segregation machinery.
    Annu Rev Genet. 1998;32:307-37 PMID: 9928483
  3. A Bub2p-dependent spindle checkpoint pathway regulates the Dbf2p kinase in budding yeast.
    EMBO J. 1999 May 4;18(9):2424-34 PMID: 10228157
  4. Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage.
    EMBO J. 1999 May 17;18(10):2707-21 PMID: 10329618
  5. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences.
    FEMS Microbiol Lett. 1999 May 15;174(2):247-50 PMID: 10339815
  6. Lesions in many different spindle components activate the spindle checkpoint in the budding yeast Saccharomyces cerevisiae.
    Genetics. 1999 Jun;152(2):509-18 PMID: 10353895
  7. RAD53, DUN1 and PDS1 define two parallel G2/M checkpoint pathways in budding yeast.
    EMBO J. 1999 Jun 1;18(11):3173-85 PMID: 10357828
  8. The unstable F-box protein p58-Ctf13 forms the structural core of the CBF3 kinetochore complex.
    J Cell Biol. 1999 May 31;145(5):933-50 PMID: 10352012
  9. Budding yeast Bub2 is localized at spindle pole bodies and activates the mitotic checkpoint via a different pathway from Mad2.
    J Cell Biol. 1999 May 31;145(5):979-91 PMID: 10352016
  10. Pds1 and Esp1 control both anaphase and mitotic exit in normal cells and after DNA damage.
    Genes Dev. 1999 Aug 1;13(15):1936-49 PMID: 10444592
  11. Pds1p of budding yeast has dual roles: inhibition of anaphase initiation and regulation of mitotic exit.
    Genes Dev. 1999 Aug 1;13(15):1950-9 PMID: 10444593
  12. Septins: cytoskeletal polymers or signalling GTPases?
    Trends Cell Biol. 1999 Oct;9(10):387-94 PMID: 10481176
  13. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms.
    Science. 1999 Nov 5;286(5442):1166-71 PMID: 10550056
  14. Uncontrolled septation in a cell division cycle mutant of the fission yeast Schizosaccharomyces pombe.
    J Bacteriol. 1979 Jan;137(1):440-6 PMID: 762020
  15. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  16. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site.
    J Cell Biol. 1991 Feb;112(4):535-44 PMID: 1993729
  17. S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function.
    Cell. 1991 Aug 9;66(3):507-17 PMID: 1651171
  18. Identification of essential components of the S. cerevisiae kinetochore.
    Cell. 1993 May 21;73(4):761-74 PMID: 8500169
  19. The S. pombe cdc16 gene is required both for maintenance of p34cdc2 kinase activity and regulation of septum formation: a link between mitosis and cytokinesis?
    EMBO J. 1993 Jul;12(7):2697-704 PMID: 8334988
  20. Heat-inducible degron: a method for constructing temperature-sensitive mutants.
    Science. 1994 Mar 4;263(5151):1273-6 PMID: 8122109
  21. Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint.
    J Cell Biol. 1995 Aug;130(4):929-39 PMID: 7642708
  22. The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores.
    J Cell Biol. 1995 Aug;130(4):941-8 PMID: 7642709
  23. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint.
    Mol Cell Biol. 1995 Nov;15(11):6128-38 PMID: 7565765
  24. Checkpoint genes required to delay cell division in response to nocodazole respond to impaired kinetochore function in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1995 Dec;15(12):6838-44 PMID: 8524250
  25. Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s).
    J Cell Biol. 1996 Apr;133(1):99-110 PMID: 8601617
  26. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast.
    Genetics. 1996 Dec;144(4):1425-36 PMID: 8978031
  27. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p.
    Genes Dev. 1996 Dec 15;10(24):3081-93 PMID: 8985178
  28. GFP tagging of budding yeast chromosomes reveals that protein-protein interactions can mediate sister chromatid cohesion.
    Curr Biol. 1996 Dec 1;6(12):1599-608 PMID: 8994824
  29. Cdc20, a beta-transducin homologue, links RAD9-mediated G2/M checkpoint control to mitosis in Saccharomyces cerevisiae.
    Mol Gen Genet. 1996 Nov 27;253(1-2):138-48 PMID: 9003297
  30. Gene identification using the yeast two-hybrid system.
    Methods Enzymol. 1997;283:141-56 PMID: 9251017
  31. CDC20 and CDH1: a family of substrate-specific activators of APC-dependent proteolysis.
    Science. 1997 Oct 17;278(5337):460-3 PMID: 9334304
  32. The anaphase inhibitor of Saccharomyces cerevisiae Pds1p is a target of the DNA damage checkpoint pathway.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14361-6 PMID: 9405617
  33. Budding yeast Cdc20: a target of the spindle checkpoint.
    Science. 1998 Feb 13;279(5353):1041-4 PMID: 9461437
  34. Mitotic arrest: Mad2 prevents sleepy from waking up the APC.
    Science. 1998 Feb 13;279(5353):999-1000 PMID: 9490488
  35. Cdc20 is essential for the cyclosome-mediated proteolysis of both Pds1 and Clb2 during M phase in budding yeast.
    Curr Biol. 1998 Feb 12;8(4):231-4 PMID: 9501986
  36. Dominant alleles of Saccharomyces cerevisiae CDC20 reveal its role in promoting anaphase.
    Genetics. 1998 Feb;148(2):599-610 PMID: 9504909
  37. Cell cycle arrest in cdc20 mutants of Saccharomyces cerevisiae is independent of Ndc10p and kinetochore function but requires a subset of spindle checkpoint genes.
    Genetics. 1998 Apr;148(4):1701-13 PMID: 9560388
  38. Mammalian p55CDC mediates association of the spindle checkpoint protein Mad2 with the cyclosome/anaphase-promoting complex, and is involved in regulating anaphase onset and late mitotic events.
    J Cell Biol. 1998 Jun 15;141(6):1393-406 PMID: 9628895
  39. The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation.
    Genes Dev. 1998 Jun 15;12(12):1871-83 PMID: 9637688
  40. The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities.
    Curr Biol. 1998 Jul 2;8(14):831-4 PMID: 9663392
  41. Byr4 and Cdc16 form a two-component GTPase-activating protein for the Spg1 GTPase that controls septation in fission yeast.
    Curr Biol. 1998 Aug 27;8(17):947-54 PMID: 9742395
  42. A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae.
    Mol Biol Cell. 1998 Oct;9(10):2803-17 PMID: 9763445
  43. Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function.
    J Cell Biol. 1998 Nov 2;143(3):719-36 PMID: 9813093
  44. Subunits and substrates of the anaphase-promoting complex.
    Exp Cell Res. 1999 May 1;248(2):339-49 PMID: 10222126
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2000-10-00
Pages
489-500
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1461296
Subset
IM
Grants
NIGMS NIH HHS · GM50842 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]