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PMID: 15014440 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mechanism controlling perpendicular alignment of the spindle to the axis of cell division in fission yeast.

The EMBO journal ·Vol. 23 ·No. 6 ·2004-03-24 ·Pages 1289-300

Gachet Y, Tournier S, Millar JB, Hyams JS

Abstract

In animal cells, the mitotic spindle is aligned perpendicular to the axis of cell division. This ensures that sister chromatids are separated to opposite sides of the cytokinetic actomyosin ring (CAR). We show that, in fission yeast, spindle rotation is dependent on the interaction of astral microtubules with the cortical actin cytoskeleton. Interaction initially occurs with a region surrounding the nucleus, which we term the astral microtubule interaction zone (AMIZ). Simultaneous contact of astral microtubules from both poles with the AMIZ directs spindle rotation and this requires both actin and two type V myosins, Myo51 and Myo52. Astral microtubules from one pole only then contact the CAR, which is located at the centre of the AMIZ. We demonstrate that the anillin homologue Mid1, which dictates correct placement of the CAR, is necessary to stabilise the mitotic spindle perpendicular to the axis of cell division. Finally, we show that the position of the mitotic spindle is monitored by a checkpoint that regulates the timing of sister chromatid separation.

MeSH Terms
Actins/metabolism Anaphase/drug effects Bridged Bicyclo Compounds, Heterocyclic/pharmacology Cell Division/drug effects Contractile Proteins/metabolism Cytoskeleton/metabolism Microtubules/drug effects,metabolism Myosin Type V/metabolism Schizosaccharomyces/cytology,drug effects,metabolism Schizosaccharomyces pombe Proteins/metabolism Spindle Apparatus/drug effects,metabolism Thiazoles/pharmacology Thiazolidines
Chemicals
Actins Bridged Bicyclo Compounds, Heterocyclic Contractile Proteins Mid1 protein, S pombe Schizosaccharomyces pombe Proteins Thiazoles Thiazolidines anillin Myosin Type V latrunculin B
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Gachet Yannick
Department of Biology, University College London, London, UK.
Tournier Sylvie
Millar Jonathan B A
Hyams Jeremy S
References (54)
54 references, click to expand
  1. A mechanism for coupling exit from mitosis to partitioning of the nucleus.
    Cell. 2000 Jul 7;102(1):21-31 PMID: 10929710
  2. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A.
    J Cell Biol. 1997 Apr 21;137(2):399-416 PMID: 9128251
  3. Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis.
    J Cell Biol. 2000 Aug 7;150(3):539-52 PMID: 10931866
  4. Myosin V orientates the mitotic spindle in yeast.
    Nature. 2000 Aug 31;406(6799):1013-5 PMID: 10984058
  5. Bim1p/Yeb1p mediates the Kar9p-dependent cortical attachment of cytoplasmic microtubules.
    Mol Biol Cell. 2000 Sep;11(9):2949-59 PMID: 10982392
  6. Dynamic positioning of mitotic spindles in yeast: role of microtubule motors and cortical determinants.
    Mol Biol Cell. 2000 Nov;11(11):3949-61 PMID: 11071919
  7. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III.
    Nature. 2000 Nov 16;408(6810):331-6 PMID: 11099034
  8. tea1 and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell.
    Cell. 1997 Jun 13;89(6):939-49 PMID: 9200612
  9. Microtubules orient the mitotic spindle in yeast through dynein-dependent interactions with the cell cortex.
    J Cell Biol. 1997 Aug 11;138(3):629-41 PMID: 9245791
  10. Mitotic spindle positioning in Saccharomyces cerevisiae is accomplished by antagonistically acting microtubule motor proteins.
    J Cell Biol. 1997 Sep 8;138(5):1041-53 PMID: 9281582
  11. The spindle pole body of Schizosaccharomyces pombe enters and leaves the nuclear envelope as the cell cycle proceeds.
    Mol Biol Cell. 1997 Aug;8(8):1461-79 PMID: 9285819
  12. Evidence for cell cycle-specific, spindle pole body-mediated, nuclear positioning in the fission yeast Schizosaccharomyces pombe.
    J Cell Sci. 1997 Aug;110 ( Pt 16):1851-66 PMID: 9296386
  13. Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells.
    J Cell Sci. 1998 Mar;111 ( Pt 6):701-12 PMID: 9471999
  14. 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
  15. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast.
    J Cell Biol. 1998 Dec 14;143(6):1603-16 PMID: 9852154
  16. A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast.
    J Cell Biol. 1999 Jun 14;145(6):1233-49 PMID: 10366596
  17. The role of actin in spindle orientation changes during the Saccharomyces cerevisiae cell cycle.
    J Cell Biol. 1999 Sep 6;146(5):1019-32 PMID: 10477756
  18. Nud1p links astral microtubule organization and the control of exit from mitosis.
    EMBO J. 2000 Dec 1;19(23):6475-88 PMID: 11101520
  19. The role of the proteins Kar9 and Myo2 in orienting the mitotic spindle of budding yeast.
    Curr Biol. 2000 Nov 30;10(23):1497-506 PMID: 11114516
  20. Two type V myosins with non-overlapping functions in the fission yeast Schizosaccharomyces pombe: Myo52 is concerned with growth polarity and cytokinesis, Myo51 is a component of the cytokinetic actin ring.
    J Cell Sci. 2001 Jan;114(Pt 1):69-79 PMID: 11112691
  21. 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
  22. Dynein-dependent movements of the mitotic spindle in Saccharomyces cerevisiae Do not require filamentous actin.
    Mol Biol Cell. 2000 Mar;11(3):863-72 PMID: 10712505
  23. Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion.
    Mol Biol Cell. 2000 May;11(5):1765-74 PMID: 10793150
  24. Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae.
    J Cell Biol. 2000 May 15;149(4):863-74 PMID: 10811827
  25. It's a kar9ochore to capture microtubules.
    Nat Cell Biol. 2000 Jun;2(6):E96-8 PMID: 10854334
  26. Fission yeast living mitosis visualized by GFP-tagged gene products.
    Micron. 2001 Jan;32(1):67-74 PMID: 10900382
  27. The surveillance mechanism of the spindle position checkpoint in yeast.
    J Cell Biol. 2001 Apr 2;153(1):159-68 PMID: 11285282
  28. Control of spindle polarity and orientation in Saccharomyces cerevisiae.
    Trends Cell Biol. 2001 Apr;11(4):160-6 PMID: 11306295
  29. Identification of two type V myosins in fission yeast, one of which functions in polarized cell growth and moves rapidly in the cell.
    Mol Biol Cell. 2001 May;12(5):1367-80 PMID: 11359928
  30. A MAP kinase-dependent actin checkpoint ensures proper spindle orientation in fission yeast.
    Nature. 2001 Jul 19;412(6844):352-5 PMID: 11460168
  31. The Bub2-dependent mitotic pathway in yeast acts every cell cycle and regulates cytokinesis.
    J Cell Sci. 2001 Jun;114(Pt 12):2345-54 PMID: 11493673
  32. S. pombe cdc11p, together with sid4p, provides an anchor for septation initiation network proteins on the spindle pole body.
    Curr Biol. 2001 Oct 16;11(20):1559-68 PMID: 11676915
  33. Animal cell cytokinesis.
    Annu Rev Cell Dev Biol. 2001;17:351-86 PMID: 11687493
  34. Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division.
    Curr Biol. 2001 Oct 30;11(21):1656-65 PMID: 11696322
  35. Localization of fission yeast type II myosin, Myo2, to the cytokinetic actin ring is regulated by phosphorylation of a C-terminal coiled-coil domain and requires a functional septation initiation network.
    Mol Biol Cell. 2001 Dec;12(12):4044-53 PMID: 11739799
  36. The 14-kDa dynein light chain-family protein Dlc1 is required for regular oscillatory nuclear movement and efficient recombination during meiotic prophase in fission yeast.
    Mol Biol Cell. 2002 Mar;13(3):930-46 PMID: 11907273
  37. Microtubule capture by the cleavage apparatus is required for proper spindle positioning in yeast.
    Genes Dev. 2002 Jul 1;16(13):1627-39 PMID: 12101122
  38. Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation.
    Dev Cell. 2003 Mar;4(3):333-44 PMID: 12636915
  39. A fiber apparatus in the nucleus of the yeast cell.
    J Cell Biol. 1966 Apr;29(1):129-51 PMID: 5331666
  40. Identification of the pleiotropic cell division cycle gene NDA2 as one of two different alpha-tubulin genes in Schizosaccharomyces pombe.
    Cell. 1984 May;37(1):233-42 PMID: 6327053
  41. Mitosis in the fission yeast Schizosaccharomyces pombe as revealed by freeze-substitution electron microscopy.
    J Cell Sci. 1986 Feb;80:253-68 PMID: 3522614
  42. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1991;194:795-823 PMID: 2005825
  43. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway.
    Cell. 1991 Jun 28;65(7):1203-12 PMID: 2065354
  44. Direct experimental evidence for the existence, structural basis and function of astral forces during anaphase B in vivo.
    J Cell Sci. 1991 Oct;100 ( Pt 2):279-88 PMID: 1757488
  45. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, Schizosaccharomyces pombe.
    J Cell Biol. 1993 Jan;120(1):141-51 PMID: 8416984
  46. A yeast actin-related protein homologous to that in vertebrate dynactin complex is important for spindle orientation and nuclear migration.
    Cell. 1994 Aug 26;78(4):669-79 PMID: 8069915
  47. The S. pombe cdc15 gene is a key element in the reorganization of F-actin at mitosis.
    Cell. 1995 Aug 11;82(3):435-44 PMID: 7634333
  48. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex.
    J Cell Biol. 1995 Oct;131(1):165-78 PMID: 7559773
  49. The BUD4 protein of yeast, required for axial budding, is localized to the mother/BUD neck in a cell cycle-dependent manner.
    J Cell Biol. 1996 Jul;134(2):413-27 PMID: 8707826
  50. An actin point-mutation neighboring the 'hydrophobic plug' causes defects in the maintenance of cell polarity and septum organization in the fission yeast Schizosaccharomyces pombe.
    FEBS Lett. 1996 Sep 2;392(3):237-41 PMID: 8774852
  51. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring.
    J Cell Sci. 1996 Jan;109 ( Pt 1):131-42 PMID: 8834798
  52. Forces acting on the fission yeast anaphase spindle.
    Cell Motil Cytoskeleton. 1996;34(1):69-75 PMID: 8860233
  53. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast.
    Genes Dev. 1996 Nov 1;10(21):2707-19 PMID: 8946912
  54. Analysis of mid1p, a protein required for placement of the cell division site, reveals a link between the nucleus and the cell surface in fission yeast.
    Mol Biol Cell. 2000 Aug;11(8):2757-73 PMID: 10930468
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1038/sj.emboj.7600156
Published
2004-03-24
Epub
2004-00-11
Pages
1289-300
Language
English
Region
England
NLM ID
8208664
PMCID
PMC381420
Subset
IM
Grants
Medical Research Council · MC_U117531948 · United Kingdom
Wellcome Trust · United Kingdom
External Links
PubMed source DOI: 10.1038/sj.emboj.7600156 PMC Full Text View journal details
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