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PMID: 16687577 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Cell cycle-dependent roles for the FCH-domain protein Cdc15p in formation of the actomyosin ring in Schizosaccharomyces pombe.

Molecular biology of the cell ·Vol. 17 ·No. 7 ·2006-07-00 ·Pages 3254-66

Wachtler V, Huang Y, Karagiannis J, Balasubramanian MK

Abstract

Cell division in the fission yeast Schizosaccharomyces pombe requires the formation and constriction of an actomyosin ring at the division site. The actomyosin ring is assembled in metaphase and anaphase A, is maintained throughout mitosis, and constricts after completion of anaphase. Maintenance of the actomyosin ring during late stages of mitosis depends on the septation initiation network (SIN), a signaling cascade that also regulates the deposition of the division septum. However, SIN is not active in metaphase and is not required for the initial assembly of the actomyosin ring early in mitosis. The FER/CIP4-homology (FCH) domain protein Cdc15p is a component of the actomyosin ring. Mutations in cdc15 lead to failure in cytokinesis and result in the formation of elongated, multinucleate cells without a division septum. Here we present evidence that the requirement of Cdc15p for actomyosin ring formation is dependent on the stage of mitosis. Although cdc15 mutants are competent to assemble actomyosin rings in metaphase, they are unable to maintain actomyosin rings late in mitosis when SIN is active. In the absence of functional Cdc15p, ring formation upon metaphase arrest depends on the anillin-like Mid1p. Interestingly, when cytokinesis is delayed due to perturbations to the division machinery, Cdc15p is maintained in a hypophosphorylated form. The dephosphorylation of Cdc15p, which occurs transiently in unperturbed cytokinesis, is partially dependent on the phosphatase Clp1p/Flp1p. This suggests a mechanism where both SIN and Clp1p/Flp1p contribute to maintenance of the actomyosin ring in late mitosis through Cdc15p, possibly by regulating its phosphorylation status.

MeSH Terms
Actomyosin/metabolism Anaphase Cell Cycle Cell Cycle Proteins/analysis,genetics,metabolism Cytokinesis Cytoplasm/enzymology GTP-Binding Proteins/genetics,metabolism Metaphase Mutation Phosphorylation Protein Structure, Tertiary/genetics Protein Tyrosine Phosphatases/analysis,metabolism Schizosaccharomyces/cytology,enzymology,physiology Schizosaccharomyces pombe Proteins/analysis,genetics,metabolism
Chemicals
CDC15 protein Cell Cycle Proteins Mid1 protein, S pombe Schizosaccharomyces pombe Proteins Actomyosin Clp1 protein, S. pombe Protein Tyrosine Phosphatases GTP-Binding Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Wachtler Volker
Cell Division Laboratory, Temasek Life Sciences Laboratory, Singapore 117604, Singapore.
Huang Yinyi
Karagiannis Jim
Balasubramanian Mohan K
References (42)
42 references, click to expand
  1. Asymmetric segregation on spindle poles of the Schizosaccharomyces pombe septum-inducing protein kinase Cdc7p.
    Genes Dev. 1998 Jan 1;12(1):84-94 PMID: 9420333
  2. Drc1p/Cps1p, a 1,3-beta-glucan synthase subunit, is essential for division septum assembly in Schizosaccharomyces pombe.
    Genetics. 1999 Nov;153(3):1193-203 PMID: 10545452
  3. The 14-3-3 protein rad24p modulates function of the cdc14p family phosphatase clp1p/flp1p in fission yeast.
    Curr Biol. 2005 Aug 9;15(15):1376-83 PMID: 16085489
  4. Flp1, a fission yeast orthologue of the s. cerevisiae CDC14 gene, is not required for cyclin degradation or rum1p stabilisation at the end of mitosis.
    J Cell Sci. 2001 Jul;114(Pt 14):2649-64 PMID: 11683392
  5. 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
  6. SIN and the art of splitting the fission yeast cell.
    Curr Biol. 2004 Sep 7;14(17):R722-30 PMID: 15341766
  7. Myosin-II reorganization during mitosis is controlled temporally by its dephosphorylation and spatially by Mid1 in fission yeast.
    J Cell Biol. 2004 Jun 7;165(5):685-95 PMID: 15184401
  8. 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
  9. Degradation of Hof1 by SCF(Grr1) is important for actomyosin contraction during cytokinesis in yeast.
    EMBO J. 2005 Apr 6;24(7):1440-52 PMID: 15775961
  10. Schizosaccharomyces pombe cdc4+ gene encodes a novel EF-hand protein essential for cytokinesis.
    J Cell Biol. 1995 Aug;130(3):651-60 PMID: 7622565
  11. F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe.
    J Cell Sci. 2002 Mar 1;115(Pt 5):887-98 PMID: 11870208
  12. The Clp1p/Flp1p phosphatase ensures completion of cytokinesis in response to minor perturbation of the cell division machinery in Schizosaccharomyces pombe.
    J Cell Sci. 2004 Aug 1;117(Pt 17):3897-910 PMID: 15265986
  13. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis.
    Dev Cell. 2003 Nov;5(5):723-34 PMID: 14602073
  14. The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe.
    J Cell Biol. 2003 Sep 1;162(5):851-62 PMID: 12939254
  15. 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
  16. The Schizosaccharomyces pombe actin-related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin.
    EMBO J. 1996 Dec 2;15(23):6438-46 PMID: 8978671
  17. The S. pombe cdc16 gene is required both for maintenance of p34cdc2 kinase activity and regulation of septum formation: a link between mitosis and cytokinesis?
    EMBO J. 1993 Jul;12(7):2697-704 PMID: 8334988
  18. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1991;194:795-823 PMID: 2005825
  19. Involvement of PCH family proteins in cytokinesis and actin distribution.
    Microsc Res Tech. 2000 Apr 15;49(2):168-72 PMID: 10816256
  20. Isolation and characterization of new fission yeast cytokinesis mutants.
    Genetics. 1998 Jul;149(3):1265-75 PMID: 9649519
  21. Split decisions: coordinating cytokinesis in yeast.
    Trends Cell Biol. 2005 Jan;15(1):10-8 PMID: 15653073
  22. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin.
    J Cell Biol. 1997 Apr 7;137(1):169-82 PMID: 9105045
  23. Analysis of the cps1 gene provides evidence for a septation checkpoint in Schizosaccharomyces pombe.
    Mol Gen Genet. 1999 Aug;262(1):163-72 PMID: 10503548
  24. Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe.
    Mol Gen Genet. 1976 Jul 23;146(2):167-78 PMID: 958201
  25. Fission yeast Clp1p phosphatase regulates G2/M transition and coordination of cytokinesis with cell cycle progression.
    Curr Biol. 2001 Jun 26;11(12):931-40 PMID: 11448769
  26. Evidence for F-actin-dependent and -independent mechanisms involved in assembly and stability of the medial actomyosin ring in fission yeast.
    EMBO J. 1999 Feb 15;18(4):854-62 PMID: 10022828
  27. Importance of a myosin II-containing progenitor for actomyosin ring assembly in fission yeast.
    Curr Biol. 2002 Apr 30;12(9):724-9 PMID: 12007415
  28. Organization of a sterol-rich membrane domain by cdc15p during cytokinesis in fission yeast.
    Nat Cell Biol. 2004 Nov;6(11):1142-4 PMID: 15517003
  29. Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe.
    J Mol Biol. 1983 Aug 5;168(2):251-70 PMID: 6887244
  30. Cytokinesis in fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1997;283:494-506 PMID: 9251043
  31. Uncontrolled septation in a cell division cycle mutant of the fission yeast Schizosaccharomyces pombe.
    J Bacteriol. 1979 Jan;137(1):440-6 PMID: 762020
  32. Timing is everything: regulation of mitotic exit and cytokinesis by the MEN and SIN.
    Trends Cell Biol. 2001 Feb;11(2):89-95 PMID: 11166217
  33. The Spg1p GTPase is an essential, dosage-dependent inducer of septum formation in Schizosaccharomyces pombe.
    Genes Dev. 1997 Jun 15;11(12):1519-34 PMID: 9203579
  34. Genetic interactions in the control of septation in Schizosaccharomyces pombe.
    J Cell Sci. 1992 Apr;101 ( Pt 4):801-8 PMID: 1527180
  35. The Schizosaccharomyces pombe spindle checkpoint protein mad2p blocks anaphase and genetically interacts with the anaphase-promoting complex.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7965-70 PMID: 9223296
  36. A checkpoint that monitors cytokinesis in Schizosaccharomyces pombe.
    J Cell Sci. 2000 Apr;113 ( Pt 7):1223-30 PMID: 10704373
  37. The role of the sid1p kinase and cdc14p in regulating the onset of cytokinesis in fission yeast.
    EMBO J. 2000 Apr 17;19(8):1803-15 PMID: 10775265
  38. Cytokinesis in fission yeast: a story of rings, rafts and walls.
    Trends Genet. 2003 Jul;19(7):403-8 PMID: 12850446
  39. Equatorial retention of the contractile actin ring by microtubules during cytokinesis.
    Science. 2003 Jun 6;300(5625):1569-74 PMID: 12791993
  40. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells.
    Curr Biol. 2004 Sep 21;14(18):R806-18 PMID: 15380095
  41. 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
  42. Fission yeast Clp1p phosphatase affects G2/M transition and mitotic exit through Cdc25p inactivation.
    EMBO J. 2004 Feb 25;23(4):919-29 PMID: 14765109
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2006-07-00
Epub
2006-00-10
Pages
3254-66
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1483054
Subset
IM
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