Septins promote F-actin ring formation by crosslinking actin filaments into curved bundles (original) (raw)

• Eggert, U. S., Mitchison, T. J. & Field, C. M. Animal cytokinesis: from parts list to mechanisms. Ann. Rev. Biochem. 75, 543–566 (2006).
  Article CAS PubMed Google Scholar
• Green, R. A., Paluch, E. & Oegema, K. Cytokinesis in animal cells. Ann. Rev. Cell Dev. Biol. 28, 29–58 (2012).
  Article CAS Google Scholar
• Murrell, M. P. & Gardel, M. L. F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex. Proc. Natl Acad. Sci. USA 109, 20820–20825 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Vogel, S. K., Petrasek, Z., Heinemann, F. & Schwille, P. Myosin motors fragment and compact membrane-bound actin filaments. eLife 2, e00116 (2013).
  Article PubMed PubMed Central Google Scholar
• Glotzer, M. The molecular requirements for cytokinesis. Science 307, 1735–1739 (2005).
  Article CAS PubMed Google Scholar
• Saarikangas, J. & Barral, Y. The emerging functions of septins in metazoans. EMBO Rep. 12, 1118–1126 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Bertin, A. et al. Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J. Mol. Biol. 404, 711–731 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, J. et al. Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr. Biol. 9, 1458–1467 (1999).
  Article CAS PubMed Google Scholar
• Field, C. M., Coughlin, M., Doberstein, S., Marty, T. & Sullivan, W. Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development 132, 2849–2860 (2005).
  Article CAS PubMed Google Scholar
• Kinoshita, M., Field, C. M., Coughlin, M. L., Straight, A. F. & Mitchison, T. J. Self- and actin-templated assembly of mammalian septins. Dev. Cell 3, 791–802 (2002).
  Article CAS PubMed Google Scholar
• Oegema, K., Savoian, M. S., Mitchison, T. J. & Field, C. M. Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J. Cell Biol. 150, 539–552 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Joo, E., Surka, M. C. & Trimble, W. S. Mammalian SEPT2 is required for scaffolding nonmuscle myosin II and its kinases. Dev. Cell 13, 677–690 (2007).
  Article CAS PubMed Google Scholar
• Mostowy, S. et al. Entrapment of intracytosolic bacteria by septin cage-like structures. Cell Host Microb. 8, 433–444 (2010).
  Article CAS Google Scholar
• Schmidt, K. & Nichols, B. J. A barrier to lateral diffusion in the cleavage furrow of dividing mammalian cells. Curr. Biol. 14, 1002–1006 (2004).
  Article CAS PubMed Google Scholar
• Caudron, F. & Barral, Y. Septins and the lateral compartmentalization of eukaryotic membranes. Dev. Cell 16, 493–506 (2009).
  Article CAS PubMed Google Scholar
• Liu, J., Fairn, G. D., Ceccarelli, D. F., Sicheri, F. & Wilde, A. Cleavage furrow organization requires PIP(2)-mediated recruitment of anillin. Curr. Biol. 22, 64–69 (2012).
  Article PubMed Google Scholar
• Kechad, A., Jananji, S., Ruella, Y. & Hickson, G. R. Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr. Biol. 22, 197–203 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Adam, J. C., Pringle, J. R. & Peifer, M. Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol. Biol. Cell 11, 3123–3135 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Field, C. M. & Alberts, B. M. Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131, 165–178 (1995).
  Article CAS PubMed Google Scholar
• Lecuit, T. & Wieschaus, E. Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo. J. Cell Biol. 150, 849–860 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Schejter, E. D. & Wieschaus, E. bottleneck acts as a regulator of the microfilament network governing cellularization of the Drosophila embryo. Cell 75, 373–385 (1993).
  Article CAS PubMed Google Scholar
• Thomas, J. H. & Wieschaus, E. src64 and tec29 are required for microfilament contraction during Drosophila cellularization. Development 131, 863–871 (2004).
  Article CAS PubMed Google Scholar
• Neufeld, T. P. & Rubin, G. M. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell 77, 371–379 (1994).
  Article CAS PubMed Google Scholar
• Field, C. M. et al. A purified Drosophila septin complex forms filaments and exhibits GTPase activity. J. Cell Biol. 133, 605–616 (1996).
  Article CAS PubMed Google Scholar
• Royou, A., Field, C., Sisson, J. C., Sullivan, W. & Karess, R. Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol. Biol. Cell 15, 838–850 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Fullilove, S. L. & Jacobson, A. G. Nuclear elongation and cytokinesis in Drosophila montana. Dev. Biol. 26, 560–577 (1971).
  Article CAS PubMed Google Scholar
• Carvalho, A., Desai, A. & Oegema, K. Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size. Cell 137, 926–937 (2009).
  Article CAS PubMed Google Scholar
• Padash Barmchi, M., Rogers, S. & Hacker, U. DRhoGEF2 regulates actin organization and contractility in the Drosophila blastoderm embryo. J. Cell Biol. 168, 575–585 (2005).
  Article PubMed PubMed Central Google Scholar
• Grosshans, J. et al. RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development 132, 1009–1020 (2005).
  Article CAS PubMed Google Scholar
• Wenzl, C., Yan, S., Laupsien, P. & Grosshans, J. Localization of RhoGEF2 during Drosophila cellularization is developmentally controlled by Slam. Mech. Dev. 127, 371–384 (2010).
  Article CAS PubMed Google Scholar
• Zhang, L. & Ward, R. E. Distinct tissue distributions and subcellular localizations of differently phosphorylated forms of the myosin regulatory light chain in Drosophila. Gene Expression Patterns 11, 93–104 (2011).
  Article CAS PubMed Google Scholar
• Kress, A. et al. Mapping the local organization of cell membranes using excitation-polarization-resolved confocal fluorescence microscopy. Biophys. J. 105, 127–136 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Sirajuddin, M. et al. Structural insight into filament formation by mammalian septins. Nature 449, 311–315 (2007).
  Article CAS PubMed Google Scholar
• Garcia, G. 3rd. et al. Subunit-dependent modulation of septin assembly: budding yeast septin Shs1 promotes ring and gauze formation. J. Cell Biol. 195, 993–1004 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Farkasovsky, M., Herter, P., Voss, B. & Wittinghofer, A. Nucleotide binding and filament assembly of recombinant yeast septin complexes. Biol. Chem. 386, 643–656 (2005).
  Article CAS PubMed Google Scholar
• Weirich, C. S., Erzberger, J. P. & Barral, Y. The septin family of GTPases: architecture and dynamics. Nat. Rev. 9, 478–489 (2008).
  Article CAS Google Scholar
• Holmes, K. C. Structural biology: actin in a twist. Nature 457, 389–390 (2009).
  Article CAS PubMed Google Scholar
• Jansen, S. et al. Mechanism of actin filament bundling by fascin. J. Biol. Chem. 286, 30087–30096 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Faix, J. et al. Cortexillins, major determinants of cell shape and size, are actin-bundling proteins with a parallel coiled-coil tail. Cell 86, 631–642 (1996).
  Article CAS PubMed Google Scholar
• Bertin, A. et al. Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc. Natl Acad. Sci. USA 105, 8274–8279 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Frazier, J. A. et al. Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. J. Cell Biol. 143, 737–749 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Hickson, G. R. & O’Farrell, P. H. Rho-dependent control of anillin behavior during cytokinesis. J. Cell Biol. 180, 285–294 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• D’Avino, P. P. et al. Interaction between Anillin and RacGAP50C connects the actomyosin contractile ring with spindle microtubules at the cell division site. J. Cell Sci. 121, 1151–1158 (2008).
  Article PubMed Google Scholar
• Estey, M. P., Di Ciano-Oliveira, C., Froese, C. D., Bejide, M. T. & Trimble, W. S. Distinct roles of septins in cytokinesis: SEPT9 mediates midbody abscission. J. Cell Biol. 191, 741–749 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Gilden, J. K., Peck, S., Chen, Y. C. & Krummel, M. F. The septin cytoskeleton facilitates membrane retraction during motility and blebbing. J. Cell Biol. 196, 103–114 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Sedzinski, J. et al. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 476, 462–466 (2011).
  Article CAS PubMed Google Scholar
• Guillot, C. & Lecuit, T. Adhesion disengagement uncouples intrinsic and extrinsic forces to drive cytokinesis in epithelial tissues. Dev. Cell 24, 227–241 (2013).
  Article CAS PubMed Google Scholar
• Founounou, N., Loyer, N. & Le Borgne, R. Septins regulate the contractility of the actomyosin ring to enable adherens junction remodelling during cytokinesis of epithelial cells. Dev. Cell 24, 242–255 (2013).
  Article CAS PubMed Google Scholar
• Mostowy, S. et al. A role for septins in the interaction between the Listeria monocytogenes INVASION PROTEIN InlB and the Met receptor. Biophys. J. 100, 1949–1959 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Tooley, A. J. et al. Amoeboid T lymphocytes require the septin cytoskeleton for cortical integrity and persistent motility. Nat. Cell Biol. 11, 17–26 (2009).
  Article CAS PubMed Google Scholar
• Dagdas, Y. F. et al. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science 336, 1590–1595 (2012).
  Article CAS PubMed Google Scholar
• Pan, F., Malmberg, R. L. & Momany, M. Analysis of septins across kingdoms reveals orthology and new motifs. BMC Evol. Biol. 7, 103 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Sellin, M. E., Sandblad, L., Stenmark, S. & Gullberg, M. Deciphering the rules governing assembly order of mammalian septin complexes. Mol. Biol. Cell 22, 3152–3164 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, M. S., Froese, C. D., Estey, M. P. & Trimble, W. S. SEPT9 occupies the terminal positions in septin octamers and mediates polymerization-dependent functions in abscission. J. Cell Biol. 195, 815–826 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Gittes, F., Mickey, B., Nettleton, J. & Howard, J. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120, 923–934 (1993).
  Article CAS PubMed Google Scholar
• Tang, J. X., Kas, J. A., Shah, J. V. & Janmey, P. A. Counterion-induced actin ring formation. Eur. Biophys. J. 30, 477–484 (2001).
  Article CAS PubMed Google Scholar
• Taylor, K. A., Taylor, D. W. & Schachat, F. Isoforms of α-actinin from cardiac, smooth, and skeletal muscle form polar arrays of actin filaments. J. Cell Biol. 149, 635–646 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Surka, M. C., Tsang, C. W. & Trimble, W. S. The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis. Mol. Biol. Cell 13, 3532–3545 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Kinoshita, M. et al. Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes Dev. 11, 1535–1547 (1997).
  Article CAS PubMed Google Scholar
• Mostowy, S. & Cossart, P. Septins: the fourth component of the cytoskeleton. Nature reviews. Mol. Cell Biol. 13, 183–194 (2012).
  Article CAS Google Scholar
• Lecuit, T. & Pilot, F. Developmental control of cell morphogenesis: a focus on membrane growth. Nat. Cell Biol. 5, 103–108 (2003).
  Article CAS PubMed Google Scholar
• Murthy, M., Teodoro, R. O., Miller, T. P. & Schwarz, T. L. Sec5, a member of the exocyst complex, mediates Drosophila embryo cellularization. Development 137, 2773–2783 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Mavrakis, M., Rikhy, R. & Lippincott-Schwartz, J. Plasma membrane polarity and compartmentalization are established before cellularization in the fly embryo. Dev. Cell 16, 93–104 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Rauzi, M., Lenne, P. F. & Lecuit, T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110–1114 (2010).
  Article CAS PubMed Google Scholar
• Mavrakis, M., Rikhy, R., Lilly, M. & Lippincott-Schwartz, J. in Current Protocols in Cell Biology (eds Bonifacino, J.S. et al.) (ed Bonifacino, J.S.et al.) Ch. 4, Unit 4.18 (John Wiley, (2008).
  Google Scholar
• Levayer, R., Pelissier-Monier, A. & Lecuit, T. Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 13, 529–540 (2011).
  Article CAS PubMed Google Scholar
• Diebold, M. L., Fribourg, S., Koch, M., Metzger, T. & Romier, C. Deciphering correct strategies for multiprotein complex assembly by co-expression: application to complexes as large as the histone octamer. J. Struct. Biol. 175, 178–188 (2011).
  Article CAS PubMed Google Scholar
• Pardee, J. D. & Spudich, J. A. Purification of muscle actin. Methods Enzymol. 85 Pt B, 164–181 (1982).
  Article CAS PubMed Google Scholar
• Pollard, T. D. A guide to simple and informative binding assays. Mol. Biol. Cell 21, 4061–4067 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Gentry, B. S. et al. Multiple actin binding domains of Ena/VASP proteins determine actin network stiffening. Eur. Biophys. J. 41, 979–990 (2012).
  Article CAS PubMed Google Scholar