Home LiteratureArticle Details
PMID: 18256284 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Sister kinetochore recapture in fission yeast occurs by two distinct mechanisms, both requiring Dam1 and Klp2.

Molecular biology of the cell ·Vol. 19 ·No. 4 ·2008-04-00 ·Pages 1646-62

Gachet Y, Reyes C, Courthéoux T, Goldstone S, Gay G, Serrurier C, Tournier S

Abstract

In eukaryotic cells, proper formation of the spindle is necessary for successful cell division. We have studied chromosome recapture in the fission yeast Schizosaccharomyces pombe. We show by live cell analysis that lost kinetochores interact laterally with intranuclear microtubules (INMs) and that both microtubule depolymerization (end-on pulling) and minus-end-directed movement (microtubule sliding) contribute to chromosome retrieval to the spindle pole body (SPB). We find that the minus-end-directed motor Klp2 colocalizes with the kinetochore during its transport to the SPB and contributes to the effectiveness of retrieval by affecting both end-on pulling and lateral sliding. Furthermore, we provide in vivo evidence that Dam1, a component of the DASH complex, also colocalizes with the kinetochore during its transport and is essential for its retrieval by either of these mechanisms. Finally, we find that the position of the unattached kinetochore correlates with the size and orientation of the INMs, suggesting that chromosome recapture may not be a random process.

MeSH Terms
Biological Transport, Active Dyneins/genetics,metabolism Genes, Fungal Green Fluorescent Proteins/genetics,metabolism Kinetochores/metabolism Microtubule-Associated Proteins/genetics,metabolism Microtubules/metabolism Models, Biological Molecular Motor Proteins/genetics,metabolism Multiprotein Complexes Recombinant Proteins/genetics,metabolism Schizosaccharomyces/genetics,metabolism Schizosaccharomyces pombe Proteins/genetics,metabolism Sister Chromatid Exchange/genetics,physiology Spindle Apparatus/genetics,metabolism
Chemicals
Cyan Fluorescent Protein Dam1 protein, S pombe Klp2 protein, S pombe Microtubule-Associated Proteins Molecular Motor Proteins Multiprotein Complexes Recombinant Proteins Schizosaccharomyces pombe Proteins Green Fluorescent Proteins Dhc1 protein, S pombe Dyneins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Gachet Yannick
Laboratoire de Biologie Cellulaire et Moléculaire du Controle de la Prolifération (LBCMCP), Centre National de la Recherche Scientifique, Université de Toulouse, 31062 Toulouse, France.
Reyes Céline
Courthéoux Thibault
Goldstone Sherilyn
Gay Guillaume
Serrurier Céline
Tournier Sylvie
References (38)
38 references, click to expand
  1. Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles.
    J Cell Biol. 2007 Jul 16;178(2):269-81 PMID: 17620411
  2. Chromosomes can congress to the metaphase plate before biorientation.
    Science. 2006 Jan 20;311(5759):388-91 PMID: 16424343
  3. Intra-nuclear microtubules and a mitotic spindle orientation checkpoint.
    Nat Cell Biol. 2004 Dec;6(12):1245-6 PMID: 15573098
  4. The yeast DASH complex forms closed rings on microtubules.
    Nat Struct Mol Biol. 2005 Feb;12(2):138-43 PMID: 15640796
  5. Kinetochores are transported poleward along a single astral microtubule during chromosome attachment to the spindle in newt lung cells.
    J Cell Biol. 1990 Jan;110(1):81-95 PMID: 2295685
  6. Architecture of the Dam1 kinetochore ring complex and implications for microtubule-driven assembly and force-coupling mechanisms.
    Nat Struct Mol Biol. 2007 Aug;14(8):721-6 PMID: 17643123
  7. The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends.
    Nature. 2006 Mar 23;440(7083):565-9 PMID: 16415853
  8. Mechanism controlling perpendicular alignment of the spindle to the axis of cell division in fission yeast.
    EMBO J. 2004 Mar 24;23(6):1289-300 PMID: 15014440
  9. Rings, bracelets, sleeves, and chevrons: new structures of kinetochore proteins.
    Trends Cell Biol. 2007 Aug;17(8):377-82 PMID: 17766118
  10. Molecular analysis of kinetochore architecture in fission yeast.
    EMBO J. 2005 Aug 17;24(16):2919-30 PMID: 16079914
  11. Dynein participates in chromosome segregation in fission yeast.
    Biol Cell. 2007 Nov;99(11):627-37 PMID: 17561805
  12. Simple centromere, complex kinetochore: linking spindle microtubules and centromeric DNA in budding yeast.
    J Cell Biol. 2002 Apr 15;157(2):199-203 PMID: 11956223
  13. Motor proteins at the microtubule plus-end.
    Trends Cell Biol. 2006 Mar;16(3):135-43 PMID: 16469495
  14. The dynamic kinetochore-microtubule interface.
    J Cell Sci. 2004 Nov 1;117(Pt 23):5461-77 PMID: 15509863
  15. The rate of poleward chromosome motion is attenuated in Drosophila zw10 and rod mutants.
    Nat Cell Biol. 2000 Dec;2(12):948-52 PMID: 11146661
  16. Gradients in the self-organization of the mitotic spindle.
    Trends Cell Biol. 2006 Mar;16(3):125-34 PMID: 16478663
  17. Mitotic chromosome biorientation in fission yeast is enhanced by dynein and a minus-end-directed, kinesin-like protein.
    Mol Biol Cell. 2007 Jun;18(6):2216-25 PMID: 17409356
  18. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1991;194:795-823 PMID: 2005825
  19. Mal3, the fission yeast homologue of the human APC-interacting protein EB-1 is required for microtubule integrity and the maintenance of cell form.
    J Cell Biol. 1997 Nov 3;139(3):717-28 PMID: 9348288
  20. The mitotic spindle is required for loading of the DASH complex onto the kinetochore.
    Genes Dev. 2002 Jan 15;16(2):183-97 PMID: 11799062
  21. The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules.
    Curr Biol. 2004 Apr 6;14(7):548-59 PMID: 15062095
  22. Influence of M-phase chromatin on the anisotropy of microtubule asters.
    J Cell Biol. 1996 Apr;133(1):125-40 PMID: 8601601
  23. Positioning and elongation of the fission yeast spindle by microtubule-based pushing.
    Curr Biol. 2004 Jul 13;14(13):1181-6 PMID: 15242615
  24. The DASH complex and Klp5/Klp6 kinesin coordinate bipolar chromosome attachment in fission yeast.
    EMBO J. 2005 Aug 17;24(16):2931-43 PMID: 16079915
  25. Disruption of astral microtubule contact with the cell cortex activates a Bub1, Bub3, and Mad3-dependent checkpoint in fission yeast.
    Mol Biol Cell. 2004 Jul;15(7):3345-56 PMID: 15146064
  26. Microtubule depolymerization can drive poleward chromosome motion in fission yeast.
    EMBO J. 2006 Oct 18;25(20):4888-96 PMID: 17036054
  27. Long-range communication between chromatin and microtubules in Xenopus egg extracts.
    Curr Biol. 2003 Sep 30;13(19):1728-33 PMID: 14521840
  28. Targeted movement of cell end factors in fission yeast.
    Nat Cell Biol. 2003 Sep;5(9):812-8 PMID: 12894167
  29. Analysis of a RanGTP-regulated gradient in mitotic somatic cells.
    Nature. 2006 Mar 30;440(7084):697-701 PMID: 16572176
  30. Molecular mechanisms of kinetochore capture by spindle microtubules.
    Nature. 2005 Apr 21;434(7036):987-94 PMID: 15846338
  31. Cytoplasmic dynein is required for poleward chromosome movement during mitosis in Drosophila embryos.
    Nat Cell Biol. 2000 Dec;2(12):922-30 PMID: 11146657
  32. Four new subunits of the Dam1-Duo1 complex reveal novel functions in sister kinetochore biorientation.
    EMBO J. 2002 Jan 15;21(1-2):181-93 PMID: 11782438
  33. Effects of {gamma}-tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast.
    Mol Biol Cell. 2005 Jun;16(6):2719-33 PMID: 15772152
  34. The Dam1/DASH complex is required for the retrieval of unclustered kinetochores in fission yeast.
    J Cell Sci. 2007 Oct 1;120(Pt 19):3345-51 PMID: 17881496
  35. The mechanism of kinetochore-spindle attachment and polewards movement analyzed in PtK2 cells at the prophase-prometaphase transition.
    Eur J Cell Biol. 1990 Dec;53(2):313-25 PMID: 2081546
  36. Genetic analysis of the kinetochore DASH complex reveals an antagonistic relationship with the ras/protein kinase A pathway and a novel subunit required for Ask1 association.
    Mol Cell Biol. 2005 Jan;25(2):767-78 PMID: 15632076
  37. Implication of a novel multiprotein Dam1p complex in outer kinetochore function.
    J Cell Biol. 2001 Dec 24;155(7):1137-45 PMID: 11756468
  38. Chromosome-microtubule interactions during mitosis.
    Annu Rev Cell Dev Biol. 2002;18:193-219 PMID: 12142285
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
Published
2008-04-00
Epub
2008-00-06
Pages
1646-62
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2291439
Subset
IM
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: product@genelibs.com