Home LiteratureArticle Details
PMID: 17620411 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Molecular mechanisms of microtubule-dependent kinetochore transport toward spindle poles.

The Journal of cell biology ·Vol. 178 ·No. 2 ·2007-07-16 ·Pages 269-81

Tanaka K, Kitamura E, Kitamura Y, Tanaka TU

Abstract

In mitosis, kinetochores are initially captured by the lateral sides of single microtubules and are subsequently transported toward spindle poles. Mechanisms for kinetochore transport are not yet known. We present two mechanisms involved in microtubule-dependent poleward kinetochore transport in Saccharomyces cerevisiae. First, kinetochores slide along the microtubule lateral surface, which is mainly and probably exclusively driven by Kar3, a kinesin-14 family member that localizes at kinetochores. Second, kinetochores are tethered at the microtubule distal ends and pulled poleward as microtubules shrink (end-on pulling). Kinetochore sliding is often converted to end-on pulling, enabling more processive transport, but the opposite conversion is rare. The establishment of end-on pulling is partly hindered by Kar3, and its progression requires the Dam1 complex. We suggest that the Dam1 complexes, which probably encircle a single microtubule, can convert microtubule depolymerization into the poleward kinetochore-pulling force. Thus, microtubule-dependent poleward kinetochore transport is ensured by at least two distinct mechanisms.

MeSH Terms
Biological Transport Cell Cycle Proteins/metabolism Kinetochores/metabolism Microtubule-Associated Proteins/metabolism Microtubules/metabolism Models, Biological Saccharomyces cerevisiae/cytology,genetics,metabolism Saccharomyces cerevisiae Proteins/metabolism Spindle Apparatus/metabolism
Chemicals
Cell Cycle Proteins DAM1 protein, S cerevisiae KAR3 protein, S cerevisiae Microtubule-Associated Proteins Saccharomyces cerevisiae Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Tanaka Kozo
College of Life Sciences, University of Dundee, Wellcome Trust Biocentre, Dundee, Scotland, UK.
Kitamura Etsushi
Kitamura Yoko
Tanaka Tomoyuki U
References (56)
56 references, click to expand
  1. Cik1 targets the minus-end kinesin depolymerase kar3 to microtubule plus ends.
    Curr Biol. 2005 Aug 9;15(15):1420-7 PMID: 16085496
  2. Chromosome bi-orientation on the mitotic spindle.
    Philos Trans R Soc Lond B Biol Sci. 2005 Mar 29;360(1455):581-9 PMID: 15897181
  3. The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae.
    Nat Cell Biol. 2000 Jan;2(1):36-41 PMID: 10620805
  4. Mitotic motors in Saccharomyces cerevisiae.
    Biochim Biophys Acta. 2000 Mar 17;1496(1):99-116 PMID: 10722880
  5. Dynein is a transient kinetochore component whose binding is regulated by microtubule attachment, not tension.
    J Cell Biol. 2000 Nov 13;151(4):739-48 PMID: 11076960
  6. The spindle cycle in budding yeast.
    Nat Cell Biol. 2001 Jan;3(1):E23-7 PMID: 11146646
  7. Mitotic spindle integrity and kinetochore function linked by the Duo1p/Dam1p complex.
    J Cell Biol. 2001 Jan 8;152(1):197-212 PMID: 11149931
  8. Budding yeast chromosome structure and dynamics during mitosis.
    J Cell Biol. 2001 Mar 19;152(6):1255-66 PMID: 11257125
  9. Stu2 promotes mitotic spindle elongation in anaphase.
    J Cell Biol. 2001 Apr 16;153(2):435-42 PMID: 11309422
  10. A structural pathway for activation of the kinesin motor ATPase.
    EMBO J. 2001 Jun 1;20(11):2611-8 PMID: 11387196
  11. Two related kinesins, klp5+ and klp6+, foster microtubule disassembly and are required for meiosis in fission yeast.
    Mol Biol Cell. 2001 Dec;12(12):3919-32 PMID: 11739790
  12. Implication of a novel multiprotein Dam1p complex in outer kinetochore function.
    J Cell Biol. 2001 Dec 24;155(7):1137-45 PMID: 11756468
  13. 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
  14. 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
  15. Evidence that the Ipl1-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections.
    Cell. 2002 Feb 8;108(3):317-29 PMID: 11853667
  16. Chromosome-microtubule interactions during mitosis.
    Annu Rev Cell Dev Biol. 2002;18:193-219 PMID: 12142285
  17. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p.
    Cell. 2002 Oct 18;111(2):163-72 PMID: 12408861
  18. Dynamics and mechanics of the microtubule plus end.
    Nature. 2003 Apr 17;422(6933):753-8 PMID: 12700769
  19. Kinetochore protein interactions and their regulation by the Aurora kinase Ipl1p.
    Mol Biol Cell. 2003 Aug;14(8):3342-55 PMID: 12925767
  20. The minus end-directed motor Kar3 is required for coupling dynamic microtubule plus ends to the cortical shmoo tip in budding yeast.
    Curr Biol. 2003 Aug 19;13(16):1423-8 PMID: 12932327
  21. Kinesin motors as molecular machines.
    Bioessays. 2003 Dec;25(12):1212-9 PMID: 14635256
  22. Aurora B regulates MCAK at the mitotic centromere.
    Dev Cell. 2004 Feb;6(2):253-68 PMID: 14960279
  23. Aurora B phosphorylates centromeric MCAK and regulates its localization and microtubule depolymerization activity.
    Curr Biol. 2004 Feb 17;14(4):273-86 PMID: 14972678
  24. Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle.
    Nature. 2004 Mar 4;428(6978):93-7 PMID: 14961024
  25. Differentiation of cytoplasmic and meiotic spindle assembly MCAK functions by Aurora B-dependent phosphorylation.
    Mol Biol Cell. 2004 Jun;15(6):2895-906 PMID: 15064354
  26. The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly.
    Cell. 2004 Jul 23;118(2):187-202 PMID: 15260989
  27. The dynamic kinetochore-microtubule interface.
    J Cell Sci. 2004 Nov 1;117(Pt 23):5461-77 PMID: 15509863
  28. 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
  29. 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
  30. Kar3 interaction with Cik1 alters motor structure and function.
    EMBO J. 2005 Sep 21;24(18):3214-23 PMID: 16107877
  31. Force production by disassembling microtubules.
    Nature. 2005 Nov 17;438(7066):384-8 PMID: 16292315
  32. Kinetochore capture and bi-orientation on the mitotic spindle.
    Nat Rev Mol Cell Biol. 2005 Dec;6(12):929-42 PMID: 16341079
  33. Analysis of kinesin motor function at budding yeast kinetochores.
    J Cell Biol. 2006 Mar 13;172(6):861-74 PMID: 16533946
  34. The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends.
    Nature. 2006 Mar 23;440(7083):565-9 PMID: 16415853
  35. Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins.
    Genome Biol. 2006;7(3):R23 PMID: 16563186
  36. The depolymerizing kinesin MCAK uses lattice diffusion to rapidly target microtubule ends.
    Nature. 2006 May 4;441(7089):115-9 PMID: 16672973
  37. The Dam1 kinetochore complex harnesses microtubule dynamics to produce force and movement.
    Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):9873-8 PMID: 16777964
  38. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner.
    Nat Cell Biol. 2006 Sep;8(9):957-62 PMID: 16906145
  39. Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle.
    Nat Cell Biol. 2006 Sep;8(9):913-23 PMID: 16906148
  40. The role of the kinesin-13 neck in microtubule depolymerization.
    Cell Cycle. 2006 Aug;5(16):1812-5 PMID: 16929184
  41. Kinesin-13s form rings around microtubules.
    J Cell Biol. 2006 Oct 9;175(1):25-31 PMID: 17015621
  42. Microtubule depolymerization can drive poleward chromosome motion in fission yeast.
    EMBO J. 2006 Oct 18;25(20):4888-96 PMID: 17036054
  43. KAR3, a kinesin-related gene required for yeast nuclear fusion.
    Cell. 1990 Mar 23;60(6):1029-41 PMID: 2138512
  44. Yeast Kar3 is a minus-end microtubule motor protein that destabilizes microtubules preferentially at the minus ends.
    EMBO J. 1994 Jun 1;13(11):2708-13 PMID: 7912193
  45. How cells get the right chromosomes.
    Science. 1997 Jan 31;275(5300):632-7 PMID: 9005842
  46. Single-particle tracking: applications to membrane dynamics.
    Annu Rev Biophys Biomol Struct. 1997;26:373-99 PMID: 9241424
  47. The Kar3p and Kip2p motors function antagonistically at the spindle poles to influence cytoplasmic microtubule numbers.
    J Cell Sci. 1998 Feb;111 ( Pt 3):295-301 PMID: 9427678
  48. Novel roles for saccharomyces cerevisiae mitotic spindle motors.
    J Cell Biol. 1999 Oct 18;147(2):335-50 PMID: 10525539
  49. Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase.
    Curr Biol. 2004 Nov 9;14(21):1962-7 PMID: 15530400
  50. Kinetochore-spindle microtubule interactions during mitosis.
    Curr Opin Cell Biol. 2005 Feb;17(1):35-46 PMID: 15661517
  51. Microtubule-depolymerizing kinesins.
    Curr Opin Cell Biol. 2005 Feb;17(1):82-8 PMID: 15661523
  52. Formation of a dynamic kinetochore- microtubule interface through assembly of the Dam1 ring complex.
    Mol Cell. 2005 Jan 21;17(2):277-90 PMID: 15664196
  53. The yeast DASH complex forms closed rings on microtubules.
    Nat Struct Mol Biol. 2005 Feb;12(2):138-43 PMID: 15640796
  54. Rings around kinetochore microtubules in yeast.
    Nat Struct Mol Biol. 2005 Mar;12(3):210-2 PMID: 15744320
  55. Molecular mechanisms of kinetochore capture by spindle microtubules.
    Nature. 2005 Apr 21;434(7036):987-94 PMID: 15846338
  56. Molecular analysis of kinetochore architecture in fission yeast.
    EMBO J. 2005 Aug 17;24(16):2919-30 PMID: 16079914
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2007-07-16
Epub
2007-00-09
Pages
269-81
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2064446
Subset
IM
Grants
Wellcome Trust · United Kingdom
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]