Actin dynamics in the contractile ring during cytokinesis in fission yeast

Cytokinesis in many eukaryotes requires a contractile ring of actin and myosin that cleaves the cell in two. Little is known about how actin filaments and other components assemble into this ring structure and generate force. Here we show that the contractile ring in the fission yeast Schizosaccharomyces pombe is an active site of actin assembly. This actin polymerization activity requires Arp3, the formin Cdc12, profilin and WASP, but not myosin II or IQGAP proteins. Both newly polymerized actin filaments and pre-existing actin cables can contribute to the initial assembly of the ring. Once formed, the ring remains a dynamic structure in which actin and other ring components continuously assemble and disassemble from the ring every minute. The rate of actin polymerization can influence the rate of cleavage. Thus, actin polymerization driven by the Arp2/3 complex and formins is a central process in cytokinesis. Our studies show that cytokinesis is a more dynamic process than previously thought and provide a perspective on the mechanism of cell division.

[1]  Rong Li,et al.  Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[2]  I. Mabuchi,et al.  F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe. , 2002, Journal of cell science.

[3]  Y. Wang,et al.  Mechanism of the formation of contractile ring in dividing cultured animal cells. I. Recruitment of preexisting actin filaments into the cleavage furrow , 1990, The Journal of cell biology.

[4]  K. Gould,et al.  The Schizosaccharomyces pombe actin‐related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin. , 1996, The EMBO journal.

[5]  F. Chang,et al.  Cytokinesis and the contractile ring in fission yeast. , 2001, Current opinion in microbiology.

[6]  R. Rappaport,et al.  Cytokinesis in animal cells. , 1996, International Review of Cytology.

[7]  T. Pollard,et al.  Fission Yeast Myosin-I, Myo1p, Stimulates Actin Assembly by Arp2/3 Complex and Shares Functions with Wasp , 2000, The Journal of cell biology.

[8]  David G. Drubin,et al.  Activation of the Arp2/3 Complex by the Actin Filament Binding Protein Abp1p , 2001, The Journal of cell biology.

[9]  J A Theriot,et al.  The Polymerization Motor , 2000, Traffic.

[10]  K. Gould,et al.  A mutant of Arp2p causes partial disassembly of the Arp2/3 complex and loss of cortical actin function in fission yeast. , 1999, Molecular biology of the cell.

[11]  K. Nakano,et al.  Subcellular localization and possible function of actin, tropomyosin and actin-related protein 3 (Arp3) in the fission yeast Schizosaccharomyces pombe. , 1998, European journal of cell biology.

[12]  K. Gould,et al.  Isolation and characterization of new fission yeast cytokinesis mutants. , 1998, Genetics.

[13]  K. Gould,et al.  Schizosaccharomyces pombe cdc4+ gene encodes a novel EF-hand protein essential for cytokinesis , 1995, The Journal of cell biology.

[14]  K. Gould,et al.  Cytokinesis in fission yeast Schizosaccharomyces pombe. , 1997, Methods in enzymology.

[15]  S. Wasserman,et al.  FH proteins as cytoskeletal organizers. , 1998, Trends in cell biology.

[16]  Fred Chang,et al.  cdc12p, a Protein Required for Cytokinesis in Fission Yeast, Is a Component of the Cell Division Ring and Interacts with Profilin , 1997, The Journal of cell biology.

[17]  Fred Chang,et al.  Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division , 2001, Current Biology.

[18]  K L Gould,et al.  The Arp2/3 complex: a multifunctional actin organizer. , 1999, Current opinion in cell biology.

[19]  P. Nurse,et al.  Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. , 1996, Journal of cell science.

[20]  T D Pollard,et al.  Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. , 2001, Annual review of biochemistry.

[21]  Charles Boone,et al.  Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast , 2002, Nature Cell Biology.

[22]  K. Gould,et al.  The Schizosaccharomyces pombe cdc3+ gene encodes a profilin essential for cytokinesis , 1994, The Journal of cell biology.

[23]  K. Sawin.  Cell Polarity: Following Formin Function , 2002, Current Biology.

[24]  Paul J. McLaughlin,et al.  Latrunculin alters the actin-monomer subunit interface to prevent polymerization , 2000, Nature Cell Biology.

[25]  David Pellman,et al.  Yeast formins regulate cell polarity by controlling the assembly of actin cables , 2002, Nature Cell Biology.

[26]  R. Pelham,et al.  Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe , 2001, Nature Cell Biology.

[27]  J. Spudich,et al.  Towards a molecular understanding of cytokinesis. , 2000, Trends in cell biology.

[28]  R. Rappaport,et al.  Cytokinesis in Animal Cells: Cytokinesis in Animal Cells , 1996 .

[29]  T. Noguchi,et al.  Reorganization of actin cytoskeleton at the growing end of the cleavage furrow of Xenopus egg during cytokinesis. , 2000, Journal of cell science.

[30]  D. Drubin,et al.  Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast , 1995, The Journal of cell biology.

[31]  Y. Fukui,et al.  Myosin II-independent F-actin flow contributes to cell locomotion in dictyostelium. , 1999, Journal of cell science.