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PMID: 12426374 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Spindle-kinetochore attachment requires the combined action of Kin I-like Klp5/6 and Alp14/Dis1-MAPs in fission yeast.

The EMBO journal ·Vol. 21 ·No. 22 ·2002-11-15 ·Pages 6015-24

Garcia MA, Koonrugsa N, Toda T

Abstract

Fission yeast Klp5 and Klp6 belong to the microtubule-destabilizing Kin I family. In klp5 mutants, spindle checkpoint proteins Mad2 and Bub1 are recruited to mitotic kinetochores for a prolonged duration, indicating that these kinetochores are unattached. Further analysis shows that there are kinetochores to which only Bub1, but not Mad2, localizes. These kinetochores are likely to have been captured, yet lack tension. Thus Klp5 and Klp6 play a role in a spindle- kinetochore interaction at dual steps, capture and generation of tension. The TOG/XMAP215 family, Alp14 and Dis1 are known to stabilize microtubules and be required for the bivalent attachment of the kinetochore to the spindle. Despite apparent opposing activities towards microtubule stability, Klp5/Klp6 and Alp14/Dis1 share an essential function, as either dis1klp or alp14klp mutants are synthetically lethal, like alp14dis1. Defective phenotypes are similar to each other, characteristic of attachment defects and chromosome mis-segregation. Furthermore Alp14 is of significance for kinetochore localization of Klp5. We propose that Klp5/Klp6 and Alp14/Dis1 play a collaborative role in bipolar spindle formation during prometaphase through producing spindle dynamism.

MeSH Terms
Chromosomes, Fungal/physiology Kinesins/genetics,physiology Kinetochores/physiology,ultrastructure Macromolecular Substances Metaphase Microtubule-Associated Proteins/genetics,physiology Microtubules/chemistry,ultrastructure Phenotype Protein Interaction Mapping Schizosaccharomyces/cytology,genetics,physiology Schizosaccharomyces pombe Proteins/genetics,physiology Spindle Apparatus/physiology
Chemicals
Macromolecular Substances Microtubule-Associated Proteins Schizosaccharomyces pombe Proteins alp14 protein, S pombe dis1 protein, S pombe Klp5 protein, S pombe Klp6 protein, S pombe Kinesins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Garcia Miguel Angel
Laboratory of Cell Regulation, Cancer Research UK, London Research Institute, Lincoln's Inn Fields Laboratories, 44 Lincoln's Inn Fields, London WC2A 3PX, UK.
Koonrugsa Nirada
Toda Takashi
References (54)
54 references, click to expand
  1. Dis1/TOG universal microtubule adaptors - one MAP for all?
    J Cell Sci. 2001 Nov;114(Pt 21):3805-12 PMID: 11719547
  2. Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores.
    Science. 1996 Oct 11;274(5285):242-6 PMID: 8824188
  3. Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells.
    Dev Cell. 2001 Dec;1(6):759-70 PMID: 11740938
  4. The S. pombe aurora-related kinase Ark1 associates with mitotic structures in a stage dependent manner and is required for chromosome segregation.
    J Cell Sci. 2001 Dec;114(Pt 24):4371-84 PMID: 11792803
  5. Kinetochore localisation and phosphorylation of the mitotic checkpoint components Bub1 and BubR1 are differentially regulated by spindle events in human cells.
    J Cell Sci. 2001 Dec;114(Pt 24):4385-95 PMID: 11792804
  6. 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
  7. Schizosaccharomyces pombe Bir1p, a nuclear protein that localizes to kinetochores and the spindle midzone, is essential for chromosome condensation and spindle elongation during mitosis.
    Genetics. 2002 Feb;160(2):445-56 PMID: 11861551
  8. XKCM1 acts on a single protofilament and requires the C terminus of tubulin.
    J Mol Biol. 2002 Feb 22;316(3):817-28 PMID: 11866534
  9. Kinesins klp5(+) and klp6(+) are required for normal chromosome movement in mitosis.
    J Cell Sci. 2002 Mar 1;115(Pt 5):931-40 PMID: 11870212
  10. Requirement of chromatid cohesion proteins rad21/scc1 and mis4/scc2 for normal spindle-kinetochore interaction in fission yeast.
    Curr Biol. 2002 Mar 5;12(5):347-58 PMID: 11882285
  11. Fission yeast Mad3p is required for Mad2p to inhibit the anaphase-promoting complex and localizes to kinetochores in a Bub1p-, Bub3p-, and Mph1p-dependent manner.
    Mol Cell Biol. 2002 Apr;22(8):2728-42 PMID: 11909965
  12. Control of localization of a spindle checkpoint protein, Mad2, in fission yeast.
    J Cell Sci. 2002 Apr 15;115(Pt 8):1603-10 PMID: 11950879
  13. The Schizosaccharomyces pombe aurora-related kinase Ark1 interacts with the inner centromere protein Pic1 and mediates chromosome segregation and cytokinesis.
    Mol Biol Cell. 2002 Apr;13(4):1132-43 PMID: 11950927
  14. A switch in microtubule dynamics at the onset of anaphase B in the mitotic spindle of Schizosaccharomyces pombe.
    Curr Biol. 1999 Dec 2;9(23):1423-6 PMID: 10607565
  15. Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts.
    Nat Cell Biol. 2000 Jan;2(1):13-9 PMID: 10620801
  16. 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
  17. Mammalian mad2 and bub1/bubR1 recognize distinct spindle-attachment and kinetochore-tension checkpoints.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4492-7 PMID: 11274370
  18. Stu2 promotes mitotic spindle elongation in anaphase.
    J Cell Biol. 2001 Apr 16;153(2):435-42 PMID: 11309422
  19. 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
  20. Fission yeast ch-TOG/XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint.
    EMBO J. 2001 Jul 2;20(13):3389-401 PMID: 11432827
  21. Bir1/Cut17 moving from chromosome to spindle upon the loss of cohesion is required for condensation, spindle elongation and repair.
    Genes Cells. 2001 Sep;6(9):743-63 PMID: 11554922
  22. Reconstitution of physiological microtubule dynamics using purified components.
    Science. 2001 Nov 9;294(5545):1340-3 PMID: 11701928
  23. The gamma-tubulin complex protein Alp4 provides a link between the metaphase checkpoint and cytokinesis in fission yeast.
    Genes Cells. 2002 Apr;7(4):365-73 PMID: 11952833
  24. Two kinesin-like Kin I family proteins in fission yeast regulate the establishment of metaphase and the onset of anaphase A.
    Curr Biol. 2002 Apr 16;12(8):610-21 PMID: 11967147
  25. A mechanism for microtubule depolymerization by KinI kinesins.
    Mol Cell. 2002 Apr;9(4):903-9 PMID: 11983180
  26. Minor alteration of microtubule dynamics causes loss of tension across kinetochore pairs and activates the spindle checkpoint.
    J Biol Chem. 2002 May 10;277(19):17200-8 PMID: 11864974
  27. Bi-orienting chromosomes on the mitotic spindle.
    Curr Opin Cell Biol. 2002 Jun;14(3):365-71 PMID: 12067660
  28. XMAP215: a key component of the dynamic microtubule cytoskeleton.
    Trends Cell Biol. 2002 Jun;12(6):267-73 PMID: 12074886
  29. The microtubule-destabilizing kinesin XKCM1 regulates microtubule dynamic instability in cells.
    Mol Biol Cell. 2002 Aug;13(8):2718-31 PMID: 12181341
  30. Attachment and tension in the spindle assembly checkpoint.
    J Cell Sci. 2002 Sep 15;115(Pt 18):3547-55 PMID: 12186941
  31. Cold-sensitive and caffeine-supersensitive mutants of the Schizosaccharomyces pombe dis genes implicated in sister chromatid separation during mitosis.
    EMBO J. 1988 May;7(5):1465-73 PMID: 3409871
  32. Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their centromere.
    EMBO J. 1989 Oct;8(10):3045-52 PMID: 2583093
  33. S. pombe gene sds22+ essential for a midmitotic transition encodes a leucine-rich repeat protein that positively modulates protein phosphatase-1.
    Cell. 1991 Jan 11;64(1):149-57 PMID: 1846086
  34. Identification and partial characterization of mitotic centromere-associated kinesin, a kinesin-related protein that associates with centromeres during mitosis.
    J Cell Biol. 1995 Jan;128(1-2):95-104 PMID: 7822426
  35. Mitotic forces control a cell-cycle checkpoint.
    Nature. 1995 Feb 16;373(6515):630-2 PMID: 7854422
  36. The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability.
    J Cell Biol. 1995 May;129(4):1033-47 PMID: 7744953
  37. p93dis1, which is required for sister chromatid separation, is a novel microtubule and spindle pole body-associating protein phosphorylated at the Cdc2 target sites.
    Genes Dev. 1995 Jul 1;9(13):1572-85 PMID: 7628693
  38. XKCM1: a Xenopus kinesin-related protein that regulates microtubule dynamics during mitotic spindle assembly.
    Cell. 1996 Jan 12;84(1):37-47 PMID: 8548824
  39. Identification of a human mitotic checkpoint gene: hsMAD2.
    Science. 1996 Oct 11;274(5285):246-8 PMID: 8824189
  40. 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
  41. How cells get the right chromosomes.
    Science. 1997 Jan 31;275(5300):632-7 PMID: 9005842
  42. Meiotic nuclear reorganization: switching the position of centromeres and telomeres in the fission yeast Schizosaccharomyces pombe.
    EMBO J. 1997 Jan 2;16(1):193-202 PMID: 9009280
  43. Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage.
    Cell. 1997 May 30;89(5):727-35 PMID: 9182760
  44. Centromere position in budding yeast: evidence for anaphase A.
    Mol Biol Cell. 1997 Jun;8(6):957-72 PMID: 9201708
  45. Isolation of a Schizosaccharomyces pombe rad21ts mutant that is aberrant in chromosome segregation, microtubule function, DNA repair and sensitive to hydroxyurea: possible involvement of Rad21 in ubiquitin-mediated proteolysis.
    Genetics. 1998 Jan;148(1):49-57 PMID: 9475720
  46. Mutations of mitotic checkpoint genes in human cancers.
    Nature. 1998 Mar 19;392(6673):300-3 PMID: 9521327
  47. The fission yeast SPB component Cut12 links bipolar spindle formation to mitotic control.
    Genes Dev. 1998 Apr 1;12(7):927-42 PMID: 9531532
  48. Localization of Mad2 to kinetochores depends on microtubule attachment, not tension.
    J Cell Biol. 1998 Jun 1;141(5):1181-91 PMID: 9606210
  49. Mitotic centromere-associated kinesin is important for anaphase chromosome segregation.
    J Cell Biol. 1998 Aug 10;142(3):787-801 PMID: 9700166
  50. Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle.
    Mol Biol Cell. 1998 Nov;9(11):3211-25 PMID: 9802907
  51. Fission yeast bub1 is a mitotic centromere protein essential for the spindle checkpoint and the preservation of correct ploidy through mitosis.
    J Cell Biol. 1998 Dec 28;143(7):1775-87 PMID: 9864354
  52. Kin I kinesins are microtubule-destabilizing enzymes.
    Cell. 1999 Jan 8;96(1):69-78 PMID: 9989498
  53. The spindle checkpoint.
    Curr Opin Genet Dev. 1999 Feb;9(1):69-75 PMID: 10072359
  54. 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
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/cdf611
Published
2002-11-15
Pages
6015-24
Language
English
Region
England
NLM ID
8208664
PMCID
PMC137203
Subset
IM
External Links
PubMed source DOI: 10.1093/emboj/cdf611 PMC Full Text View journal details
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