Abstract
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 force1,2. 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.
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References
Rappaport, R. Cytokinesis in Animal Cells 168–184 (Cambridge Univ. Press, Cambridge, 1996)
Robinson, D. N. & Spudich, J. A. Towards a molecular understanding of cytokinesis. Trends Cell Biol. 10, 228–237 (2000)
Feierbach, B. & Chang, F. Cytokinesis and the contractile ring in fission yeast. Curr. Opin. Microbiol. 4, 713–719 (2001)
Wasserman, S. FH proteins as cytoskeletal organizers. Trends Cell Biol. 8, 111–115 (1998)
Sawin, K. E. Cell polarity: following formin function. Curr. Biol. 12, R6–R8 (2002)
Chang, F., Drubin, D. & Nurse, P. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol. 137, 169–182 (1997)
Balasubramanian, M. K., Hirani, B. R., Burke, J. D. & Gould, K. L. The Schizosaccharomyces pombe cdc3+ gene encodes a profilin essential for cytokinesis. J. Cell Biol. 125, 1289–1301 (1994)
Higgs, H. N. & Pollard, T. D. Regulation of actin filament network formation through Arp2/3 complex: activation by a diverse array of proteins. Annu. Rev. Biochem. 70, 649–676 (2001)
Machesky, L. M. & Gould, K. L. The Arp2/3 complex: a multifunctional actin organizer. Curr. Opin. Cell Biol. 11, 117–121 (1999)
Arai, R., Nakano, K. & Mabuchi, I. Subcellular localization and possible function of actin, tropomyosin and actin-related protein 3 (Arp3) in the fission yeast Schizosaccharomyces pombe. Eur. J. Cell Biol. 76, 288–295 (1998)
Morrell, J. L., Morphew, M. & Gould, K. L. A mutant of arp2p causes partial disassembly of the Arp2/3 complex and loss of cortical actin function in fission yeast. Mol. Biol. Cell. 10, 4201–4215 (1999)
Pelham, R. J. & Chang, F. Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe. Nature Cell Biol. 3, 235–244 (2001)
Lee, W. L., Bezanilla, M. & Pollard, T. D. Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J. Cell Biol. 151, 789–800 (2000)
Goode, B. L., Rodal, A. A., Barnes, G. & Drubin, D. G. Activation of the Arp2/3 complex by the actin filament binding protein Abp1p. J. Cell Biol. 153, 627–634 (2001)
Morton, W. M., Ayscough, K. R. & McLaughlin, P. J. Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nature Cell Biol. 2, 376–378 (2000)
Li, R., Zheng, Y. & Drubin, D. G. Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J. Cell Biol. 128, 599–615 (1995)
Chang, F., Woollard, A. & Nurse, P. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J. Cell Sci. 109, 131–142 (1996)
Balasubramanian, M. K. et al. Isolation and characterization of new fission yeast cytokinesis mutants. Genetics 149, 1265–1275 (1998)
McCollum, D., Balasubramanian, M. K., Pelcher, L. E., Hemmingsen, S. M. & Gould, K. L. Schizosaccharomyces pombe cdc4+ gene encodes a novel EF-hand protein essential for cytokinesis. J. Cell Biol. 130, 651–660 (1995)
Cao, L. G. & Wang, Y. L. Mechanism of the formation of contractile ring in dividing cultured animal cells. I. Recruitment of preexisting actin filaments into the cleavage furrow. J. Cell Biol. 110, 1089–1095 (1990)
Fukui, Y., Kitanishi-Yumura, T. & Yumura, S. Myosin II-independent F-actin flow contributes to cell locomotion in Dictyostelium. J. Cell Sci. 112, 877–886 (1999)
Arai, R. & Mabuchi, I. F-actin ring formation and the role of F-actin cables in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 115, 887–898 (2002)
Feierbach, B. & Chang, F. Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr. Biol. 11, 1656–1665 (2001)
Winter, D. C., Choe, E. Y. & Li, R. Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc. Natl Acad. Sci. USA 96, 7288–7293 (1999)
McCollum, D., Feoktistova, A., Morphew, M., Balasubramanian, M. & Gould, K. L. The Schizosaccharomyces pombe actin-related protein, Arp3, is a component of the cortical actin cytoskeleton and interacts with profilin. EMBO J. 15, 6438–6446 (1996)
Theriot, J. A. The polymerization motor. Traffic 1, 19–28 (2000)
Sagot, I., Klee, S. K. & Pellman, D. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nature Cell Biol. 4, 42–50 (2002)
Evangelista, M., Pruyne, D., Amberg, D. C., Boone, C. & Bretscher, A. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nature Cell Biol. 4, 32–41 (2002)
Noguchi, T. & Mabuchi, I. Reorganization of actin cytoskeleton at the growing end of the cleavage furrow of Xenopus egg during cytokinesis. J. Cell Sci. 114, 401–412 (2001)
Balasubramanian, M. K., McCollum, D. & Gould, K. L. Cytokinesis in fission yeast Schizosaccharomyces pombe. Methods Enzymol. 283, 494–506 (1997)
Acknowledgements
We thank K. Gould for the Arc15–GFP construct, Arp3 reagents and communicating results before publication; D. Burgess, B. Feierbach, D. McCollum, A. Paoletti, R. Kessin and B. Goode for comments on the manuscript; T. Swayne and the Optical Imaging Facility of the Herbert Irving Cancer Center for use of their confocal microscope; T. Pollard for the wsp1Δ strain; and M. Balasubramanian for the GFP–Cdc4 and GFP–Cdc8 plasmids. This work was supported by research grants to F.C. from the NIH and the American Cancer Society.
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Pelham, R., Chang, F. Actin dynamics in the contractile ring during cytokinesis in fission yeast. Nature 419, 82–86 (2002). https://doi.org/10.1038/nature00999
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DOI: https://doi.org/10.1038/nature00999
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