Home LiteratureArticle Details
PMID: 17825050 Published · ppublish English Journal Article Research Support, N.I.H., Intramural

Condensin function at centromere chromatin facilitates proper kinetochore tension and ensures correct mitotic segregation of sister chromatids.

Genes to cells : devoted to molecular & cellular mechanisms ·Vol. 12 ·No. 9 ·2007-09-00 ·Pages 1075-90

Yong-Gonzalez V, Wang BD, Butylin P, Ouspenski I, Strunnikov A

Abstract

The condensin complex is essential for sister chromatid segregation in eukaryotic mitosis. Nevertheless, in budding yeast, condensin mutations result in massive mis-segregation of chromosomes containing the nucleolar organizer, while other chromosomes, which also contain condensin binding sites, remain genetically stable. To investigate this phenomenon we analyzed the mechanism of the cell-cycle arrest elicited by condensin mutations. Under restrictive conditions, the majority of condensin-deficient cells arrest in metaphase. This metaphase arrest is mediated by the spindle checkpoint, particularly by the spindle-kinetochore tension-controlling pathway. Inactivation of the spindle checkpoint in condensin mutants resulted in frequent chromosome non-disjunction, eliminating the bias in chromosome mis-segregation towards rDNA-containing chromosomes. The spindle tension defect in condensin-impaired cells is likely mediated by structural defects in centromere chromatin reflected by the partial loss of the centromere histone Cse4p. These findings show that, in addition to its essential role in rDNA segregation, condensin mediates segregation of the whole genome by maintaining the centromere structure in Saccharomyces cerevisiae.

MeSH Terms
Adenosine Triphosphatases/genetics,metabolism Cell Cycle Proteins/genetics,metabolism Centromere/physiology Chromatin/metabolism DNA, Ribosomal/metabolism DNA-Binding Proteins/genetics,metabolism Kinetochores/physiology Mitosis/physiology Models, Biological Multiprotein Complexes/genetics,metabolism Mutation Saccharomyces cerevisiae/metabolism Saccharomyces cerevisiae Proteins/genetics,metabolism Sister Chromatid Exchange/physiology
Chemicals
Cell Cycle Proteins Chromatin DNA, Ribosomal DNA-Binding Proteins Multiprotein Complexes Saccharomyces cerevisiae Proteins condensin complexes Adenosine Triphosphatases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Yong-Gonzalez Vladimir
NIH, NICHD, LGRD, Bethesda, Maryland, USA.
Wang Bi-Dar
Butylin Pavel
Ouspenski Ilia
Strunnikov Alexander
References (69)
69 references, click to expand
  1. Cdc14 phosphatase induces rDNA condensation and resolves cohesin-independent cohesion during budding yeast anaphase.
    Cell. 2004 May 14;117(4):471-82 PMID: 15137940
  2. Spindle checkpoint protein dynamics at kinetochores in living cells.
    Curr Biol. 2004 Jun 8;14(11):953-64 PMID: 15182668
  3. Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells.
    Mol Biol Cell. 2004 Jul;15(7):3296-308 PMID: 15146063
  4. Cell and molecular biology of nucleolar assembly and disassembly.
    Int Rev Cytol. 2004;239:99-178 PMID: 15464853
  5. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe.
    Cell. 1987 Sep 11;50(6):917-25 PMID: 3040264
  6. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1.
    Nature. 1999 Jul 1;400(6739):37-42 PMID: 10403247
  7. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4.
    Genes Dev. 1999 Sep 1;13(17):2271-83 PMID: 10485849
  8. Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant.
    Curr Biol. 2004 Nov 9;14(21):1968-72 PMID: 15530401
  9. Cdc14p/FEAR pathway controls segregation of nucleolus in S. cerevisiae by facilitating condensin targeting to rDNA chromatin in anaphase.
    Cell Cycle. 2004 Jul;3(7):960-7 PMID: 15190202
  10. The centromeric protein Sgo1 is required to sense lack of tension on mitotic chromosomes.
    Science. 2005 Jan 7;307(5706):130-3 PMID: 15637284
  11. Spindle-independent condensation-mediated segregation of yeast ribosomal DNA in late anaphase.
    J Cell Biol. 2005 Jan 17;168(2):209-19 PMID: 15657393
  12. Kinetochore-spindle microtubule interactions during mitosis.
    Curr Opin Cell Biol. 2005 Feb;17(1):35-46 PMID: 15661517
  13. Essential tension and constructive destruction: the spindle checkpoint and its regulatory links with mitotic exit.
    Biochem J. 2005 Feb 15;386(Pt 1):1-13 PMID: 15521820
  14. The Drosophila melanogaster condensin subunit Cap-G interacts with the centromere-specific histone H3 variant CID.
    Chromosoma. 2005 Feb;113(7):350-61 PMID: 15592865
  15. Ran GTPase regulates Mad2 localization to the nuclear pore complex.
    Eukaryot Cell. 2005 Feb;4(2):274-80 PMID: 15701789
  16. Condensins: organizing and segregating the genome.
    Curr Biol. 2005 Apr 12;15(7):R265-75 PMID: 15823530
  17. Visual assay for chromosome ploidy.
    Methods Enzymol. 1987;155:351-72 PMID: 3431466
  18. 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
  19. Feedback control of mitosis in budding yeast.
    Cell. 1991 Aug 9;66(3):519-31 PMID: 1651172
  20. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair.
    Genes Dev. 1994 Mar 15;8(6):652-65 PMID: 7926756
  21. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis.
    EMBO J. 1994 Oct 17;13(20):4938-52 PMID: 7957061
  22. 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
  23. Mitotic chromosome condensation requires Brn1p, the yeast homologue of Barren.
    Mol Biol Cell. 2000 Apr;11(4):1293-304 PMID: 10749930
  24. Chromosome condensation factor Brn1p is required for chromatid separation in mitosis.
    Mol Biol Cell. 2000 Apr;11(4):1305-13 PMID: 10749931
  25. Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast.
    Cell. 2000 Mar 17;100(6):619-33 PMID: 10761928
  26. The condensin complex governs chromosome condensation and mitotic transmission of rDNA.
    J Cell Biol. 2000 May 15;149(4):811-24 PMID: 10811823
  27. Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast.
    Cell. 2000 Jun 23;101(7):763-75 PMID: 10892747
  28. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation.
    Nat Cell Biol. 2000 Aug;2(8):492-9 PMID: 10934469
  29. The Bfa1/Bub2 GAP complex comprises a universal checkpoint required to prevent mitotic exit.
    Curr Biol. 2000 Nov 2;10(21):1379-82 PMID: 11084339
  30. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family.
    Genes Dev. 1995 Mar 1;9(5):587-99 PMID: 7698648
  31. Cell cycle checkpoints: preventing an identity crisis.
    Science. 1996 Dec 6;274(5293):1664-72 PMID: 8939848
  32. 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
  33. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae.
    Cell. 1997 Oct 3;91(1):47-57 PMID: 9335334
  34. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications.
    Yeast. 1998 Jan 30;14(2):115-32 PMID: 9483801
  35. Cse4p is a component of the core centromere of Saccharomyces cerevisiae.
    Cell. 1998 Sep 4;94(5):607-13 PMID: 9741625
  36. Merotelic kinetochores in mammalian tissue cells.
    Philos Trans R Soc Lond B Biol Sci. 2005 Mar 29;360(1455):553-68 PMID: 15897180
  37. Drosophila CAP-D2 is required for condensin complex stability and resolution of sister chromatids.
    J Cell Sci. 2005 Jun 1;118(Pt 11):2529-43 PMID: 15923665
  38. Condensin binding at distinct and specific chromosomal sites in the Saccharomyces cerevisiae genome.
    Mol Cell Biol. 2005 Aug;25(16):7216-25 PMID: 16055730
  39. The condensin I subunit Barren/CAP-H is essential for the structural integrity of centromeric heterochromatin during mitosis.
    Mol Cell Biol. 2005 Oct;25(20):8971-84 PMID: 16199875
  40. De novo kinetochore assembly requires the centromeric histone H3 variant.
    Mol Biol Cell. 2005 Dec;16(12):5649-60 PMID: 16207811
  41. Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I.
    Nature. 2006 May 4;441(7089):53-61 PMID: 16541024
  42. The human CENP-A centromeric nucleosome-associated complex.
    Nat Cell Biol. 2006 May;8(5):458-69 PMID: 16622419
  43. Molecular architecture of a kinetochore-microtubule attachment site.
    Nat Cell Biol. 2006 Jun;8(6):581-5 PMID: 16715078
  44. Ribosomal DNA transcription-dependent processes interfere with chromosome segregation.
    Mol Cell Biol. 2006 Aug;26(16):6239-47 PMID: 16880532
  45. Condensin function in mitotic nucleolar segregation is regulated by rDNA transcription.
    Cell Cycle. 2006 Oct;5(19):2260-7 PMID: 16969110
  46. The overexpression of a Saccharomyces cerevisiae centromeric histone H3 variant mutant protein leads to a defect in kinetochore biorientation.
    Genetics. 2007 Feb;175(2):513-25 PMID: 17151247
  47. Degradation of a cohesin subunit by the N-end rule pathway is essential for chromosome stability.
    Nature. 2001 Apr 19;410(6831):955-9 PMID: 11309624
  48. M phase-specific kinetochore proteins in fission yeast: microtubule-associating Dis1 and Mtc1 display rapid separation and segregation during anaphase.
    Curr Biol. 2001 Apr 17;11(8):537-49 PMID: 11369198
  49. Mutation of YCS4, a budding yeast condensin subunit, affects mitotic and nonmitotic chromosome behavior.
    Mol Biol Cell. 2002 Feb;13(2):632-45 PMID: 11854418
  50. In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin.
    J Cell Biol. 2002 Mar 4;156(5):805-15 PMID: 11864994
  51. C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis.
    Genes Dev. 2002 Mar 15;16(6):729-42 PMID: 11914278
  52. Regulation of the Bfa1p-Bub2p complex at spindle pole bodies by the cell cycle phosphatase Cdc14p.
    J Cell Biol. 2002 Apr 29;157(3):367-79 PMID: 11970961
  53. Cnd2 has dual roles in mitotic condensation and interphase.
    Nature. 2002 May 9;417(6885):197-202 PMID: 12000964
  54. Requirement of Skp1-Bub1 interaction for kinetochore-mediated activation of the spindle checkpoint.
    Mol Cell. 2003 May;11(5):1201-13 PMID: 12769845
  55. The condensin complex is required for proper spindle assembly and chromosome segregation in Xenopus egg extracts.
    J Cell Biol. 2003 Jun 23;161(6):1041-51 PMID: 12821643
  56. Chromosome integrity in Saccharomyces cerevisiae: the interplay of DNA replication initiation factors, elongation factors, and origins.
    Genes Dev. 2003 Jul 15;17(14):1741-54 PMID: 12865298
  57. Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes.
    Dev Cell. 2003 Aug;5(2):323-36 PMID: 12919682
  58. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells.
    Cell. 2003 Oct 3;115(1):109-21 PMID: 14532007
  59. Global analysis of protein localization in budding yeast.
    Nature. 2003 Oct 16;425(6959):686-91 PMID: 14562095
  60. Condensin and biological role of chromosome condensation.
    Prog Cell Cycle Res. 2003;5:361-7 PMID: 14593730
  61. Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis.
    J Cell Sci. 2003 Dec 1;116(Pt 23):4763-76 PMID: 14600262
  62. An Mtw1 complex promotes kinetochore biorientation that is monitored by the Ipl1/Aurora protein kinase.
    Dev Cell. 2003 Nov;5(5):735-45 PMID: 14602074
  63. Spindle checkpoint component Mad2 contributes to biorientation of homologous chromosomes.
    Curr Biol. 2003 Nov 11;13(22):1979-84 PMID: 14614824
  64. Histone tail-independent chromatin binding activity of recombinant cohesin holocomplex.
    J Biol Chem. 2004 Jan 30;279(5):3382-8 PMID: 14613943
  65. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis.
    Nature. 2004 Feb 5;427(6974):510-7 PMID: 14730319
  66. Spindle checkpoint proteins and chromosome-microtubule attachment in budding yeast.
    J Cell Biol. 2004 Feb 16;164(4):535-46 PMID: 14769859
  67. Mechanisms involved in regulating DNA replication origins during the cell cycle and in response to DNA damage.
    Philos Trans R Soc Lond B Biol Sci. 2004 Jan 29;359(1441):31-8 PMID: 15065654
  68. Functional roles for evolutionarily conserved Spt4p at centromeres and heterochromatin in Saccharomyces cerevisiae.
    EMBO J. 2004 Apr 21;23(8):1804-14 PMID: 15057281
  69. Cdc14 and condensin control the dissolution of cohesin-independent chromosome linkages at repeated DNA.
    Cell. 2004 May 14;117(4):455-69 PMID: 15137939
Article Info
Journal
Genes to cells : devoted to molecular & cellular mechanisms
Abbr.
Genes Cells
ISSN
1356-9597
Published
2007-09-00
Pages
1075-90
Language
English
Region
England
NLM ID
9607379
PMCID
PMC2674963
Subset
IM
Grants
Intramural NIH HHS · Z01 HD001903-11 · United States
Intramural NIH HHS · Z99 AI999999 · 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]