Skip to main content
SpringerLink
Log in

Dictyostelium cytokinesis: from molecules to mechanics

  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Abstract

Cytokinesis is the mechanical process that allows the simplest unit of life, the cell, to divide, propagating itself. To divide, the cell converts chemical energy into mechanical energy to produce force. This process is thought to be active, due in large part to the mechanochemistry of the myosin-II ATPase. The cell's viscoelasticity defines the context and perhaps the magnitude of the forces that are required for cytokinesis. The viscoelasticity may also guide the force-generating apparatus, specifying the cell shape change that results. Genetic, biochemical, and mechanical measurements are providing a quantitative view of how real proteins control this essential life process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adachi H, Takahashi Y, Hasebe T, Shirouzu M, Yokoyama S and Sutoh K (1997) Dictyostelium IQGAP-related protein specifically involved in the completion of cytokinesis. J Cell Biol 137: 891–898.

    Google Scholar 

  • Aizawa H, Fukui Y and Yahara I (1997) Live dynamics of Dictyostelium cofilin suggests a role in remodeling actin latticework into bundles. J Cell Sci 110: 2333–2344.

    Google Scholar 

  • Aizawa H, Sutoh K, Tsubuki S, Kawashima S, Ishii A and Yahara I (1995) Identification, characterization, and intracellular distribution of cofilin in Dictyostelium discoideum. J Biol Chem 270: 10,923–10,932.

    Google Scholar 

  • Bezanilla M, Forsburg SL and Pollard TD (1997) Identification of a second myosin-II in Schizosaccharomyces pombe: Myp2p is conditionally required for cytokinesis. Mol Biol Cell 8: 2693–2705.

    Google Scholar 

  • Breckler J and Burnside B (1994) Myosin I localizes to the midbody region during mammalian cytokinesis. Cell Motil Cytoskeleton 29: 312–320.

    Google Scholar 

  • Burton K and Taylor DL (1997) Traction forces of cytokinesis measured with optically modified elastic substrata. Nature 385: 450–454.

    Google Scholar 

  • Chung CY and Firtel RA (1999) PAKa, a putative PAK family member, is required for cytokinesis and the regulation of the cytoskeleton in Dictyostelium discoideum cells during chemotaxis. J Cell Biol 147: 559–575.

    Google Scholar 

  • Clarke M and Spudich JA (1974) Biochemical and structural studies of actimyosin-like proteins from non-muscle cells. J Mol Biol 86: 209–222.

    Google Scholar 

  • Clarke M and Spudich JA (1977) Nonmuscle contractile proteins: the role of actin and myosin in cell motility and shape determination. Ann Rev Biochem 46: 797–822.

    Google Scholar 

  • Dai J, Ting-Beall HP, Hockmuth RM, Sheetz MP and Titus MA (1999) Myosin I contributes to the generation of resting cortical tension. Biophys J 77: 1168–1176.

    Google Scholar 

  • deHostos EL, Bradtke B, Lottspeich F, Guggenheim R and Gerisch G (1991) Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein b subunits. EMBO J 10: 4097–4104.

    Google Scholar 

  • deHostos EL, Rehfueb C, Bradtke B, Waddell DR, Albrecht R, Murphy J and Gerisch G (1993) Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J Cell Biol 120: 163–173.

    Google Scholar 

  • DeLozanne A and Spudich JA (1987) Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236: 1086–1091.

    Google Scholar 

  • Devore JJ, Conrad GW and Rappaport R (1989) A model for astral stimulation of cytokinesis in animal cells. J Cell Biol 109: 2225–2232.

    Google Scholar 

  • Egelhoff TT, Lee RJ and Spudich JA (1993) Dictyostelium myosin heavy chain phosphorylation sites regulate myosin filament assembly and localization in vivo. Cell 75: 363–371.

    Google Scholar 

  • Evans E and Yeung A (1989) Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys J 56: 151–160.

    Google Scholar 

  • Faix J and Dittrich W (1996) DGAP1, a homologue of rasGTPase activating proteins that controls growth, cytokinesis, and development in Dictyostelium discoideum. FEBS Lett 394: 251–257.

    Google Scholar 

  • Faix J, Steinmetz M, Boves H, Kammerer RA, Lottspeich F, Mintert U, Murphy J, Stock A, Aebi U and Gerisch G (1996) Cortexillins, major determinants of cell shape and size, are actin-bundling proteins with a parallel coiled-coil tail. Cell 86: 631–642.

    Google Scholar 

  • Faix J, Weber I, Mintert U, Köhler J, Lottspeich F and Marriott G (2001) Recruitment of cortexillin into the cleavage-furrow is controlled by Rac1 and IQGAP-related proteins. EMBO J 20: 3705–3715.

    Google Scholar 

  • Finer JT, Simmons RM and Spudich JA (1994) Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368: 113–119.

    Google Scholar 

  • Fukui Y, Engler S, Inoue S and deHostos EL (1999) Architectural dynamics and gene replacement of coronin suggest its role in cytokinesis. Cell Motil Cytoskeleton 42: 204–217.

    Google Scholar 

  • Furukawa R and Fechheimer M (1994) Differential localization of α-actinin and the 30 kD actin-binding protein in the cleavage-furrow, phagocytic cup, and contractile vacuole of Dictyostelium discoideum. Cell Motil Cyto 29: 46–56.

    Google Scholar 

  • Gerald N, Dai J, Ting-Beall HP and DeLozanne A (1998) A role for Dictyostelium RacE in cortical tension and cleavage-furrow progression. J Cell Biol 141: 483–492.

    Google Scholar 

  • Goode BL, Wong JJ, Butty A-C, Peter M, McCormick AL, Yates JR, Drubin DG and Barnes G (1999) Coronin promotes the rapid assembly and cross-linking of actin filaments and may link the actin and microtubule cytoskeletons in yeast. J Cell Biol 144: 83–98.

    Google Scholar 

  • Greenspan HP (1977) On the dynamics of cell cleavage. J Theor Biol 65: 79–99.

    Google Scholar 

  • Gunsalus KC, Bonaccorsi S, Williams E, Verni F, Gatti M and Goldberg ML (1995) Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, results in defects in centrosome migration and cytokinesis. J Cell Biol 131: 1243–1259.

    Google Scholar 

  • Haugwitz M, Noegel AA, Karakesisoglou J and Schleicher M (1994) Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell 79: 303–314.

    Google Scholar 

  • He X and Dembo M (1997) On the mechanics of the first cleavage division of the sea urchin egg. Exp Cell Res 233: 252–273.

    Google Scholar 

  • Higgs HN and Pollard TD (1999) Regulation of actin polymerization by Arp2/3 complex and WASp/Scar proteins. J Biol Chem 274: 32,531–32,534.

    Google Scholar 

  • Howard J (2001) Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Ishizaka S (1966) Surface characters of dividing cells II. Isotropy and uniformity of surface membrane. J Exp Biol 44: 225–232.

    Google Scholar 

  • Knecht DA and Loomis WF (1987) Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum. Science 236: 1081–1086.

    Google Scholar 

  • Larochelle DA, Vithalani KK and DeLozanne A (1996) A novel member of the rho family of small GTP-binding proteins is specifically required for cytokinesis. J Cell Biol 133: 1321–1329.

    Google Scholar 

  • Larochelle DA, Vithalani KK and DeLozanne A (1997) Role of Dictyostelium racE in cytokinesis: mutational analysis and localization studies by the use of green fluorescent protein. Mol Biol Cell 8: 935–944.

    Google Scholar 

  • Maniak M, Rauchenberger R, Albrecht R, Murphy J and Gerisch G (1995) Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein tag. Cell 83: 915–924.

    Google Scholar 

  • Matzke R, Jacobson K and Radmacher M (2001) Direct, high-resolution measurement of furrow stiffening during division of adherent cells. Nature Cell Biol 3: 607–610.

    Google Scholar 

  • May KM, Watts FZ, Jones N and Hyams JS (1997) Type II myosin involved in cytokinesis in the fission yeast, Schizosaccharomyces pombe. Cell Motil Cytoskeleton 38: 385–396.

    Google Scholar 

  • Merkel R, Simson R, Simson DA, Hohenadl M, Boulbitch A, Wallra, E and Sackmann E (2000) A micromechanic study of cell polarity and plasma membrane cell body coupling in Dictyostelium. Biophys J 79: 707–719.

    Google Scholar 

  • Murphy CT, Rock RS and Spudich JA (2001) A myosin II mutation uncouples ATPase activity from motility and shortens step size. Nat Cell Biol 3: 311–315.

    Google Scholar 

  • Nagasaki A, Hostos ELd and Uyeda TQP (2002) Genetic and morphological evidence for two parallel pathways of cell-cycle-coupled cytokinesis in Dictyostelium. J Cell Sci 115: 2241–2251.

    Google Scholar 

  • Nakamura F, Osborn E, Janmey PA and Stossel TP (2002) Comparison of filamen A-induced cross-linking and Arp2/3 complex-mediated branching on the mechanics of actin filaments. J Biol Chem 277: 9148–9154.

    Google Scholar 

  • Pasternak C, Spudich JA and Elson EL (1989) Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 341: 549–551.

    Google Scholar 

  • Rappaport R (1964) Geometrical relations of the cleavage stimulus in constricted sand dollar eggs. J Exp Zool 155: 225–230.

    Google Scholar 

  • Rappaport R (1967) Cell division: direct measurement of maximum tension exerted by furrow of echinoderm eggs. Science 156: 1241–1243.

    Google Scholar 

  • Rappaport R (1996) Cytokinesis in Animal Cells. Cambridge University Press, Cambridge.

    Google Scholar 

  • Robinson DN (2001) Cell division: biochemically controlled mechanics. Curr Biol 11: R737-R740.

    Google Scholar 

  • Robinson DN, Cavet G, Warrick HM and Spudich JA (2002a) Quantitation of the distribution and flux of myosin-II during cytokinesis. BMC Cell Biology 3: 4.

    Google Scholar 

  • Robinson DN, Ocon SS, Rock RS and Spudich JA (2002b) Dynacortin is a novel actin bundling protein that localizes to dynamic actin structures. J Biol Chem 277: 9088–9095.

    Google Scholar 

  • Robinson DN and Spudich JA (2000a) Dynacortin, a genetic link between equatorial contractility and global shape control discovered by library complementation of a Dictyostelium discoideum cytokinesis mutant. J Cell Biol 150: 823–838.

    Google Scholar 

  • Robinson DN and Spudich JA (2000b) Towards a molecular understanding of cytokinesis. Trends Cell Biol 10: 228–237.

    Google Scholar 

  • Sabry JH, Moores SL, Ryan S, Zang J-H and Spudich JA (1997) Myosin heavy chain phosphorylation sites regulate myosin localization during cytokinesis in live cells. Mol Biol Cell 8: 2647–2657.

    Google Scholar 

  • Simson R, Wallra. E, Faix J, Niewöhner J, Gerisch G and Sackmann E (1998) Membrane bending modulus and adhesion energy of wild-type and mutant cells of Dictyostelium lacking talin or cortexillins. Biophys J 74: 514–522.

    Google Scholar 

  • Stock A, Steinmetz MO, Janmey PA, Aebi U, Gerisch G, Kammerer RA, Weber I and Faix J (1999) Domain analysis of cortexillin I: actin-bundling, PIP2-binding and the rescue of cytokinesis. EMBO J 18: 5274–5284.

    Google Scholar 

  • Uyeda TQP, Kitayama C and Yumura S (2000) Myosin II-Independent cytokinesis in Dictyostelium: its mechanism and implications. Cell Struct Function 25: 1–10.

    Google Scholar 

  • Wachsstock DH, Schwarz WH and Pollard TD (1993) Affinity of α-actinin determines the structure and mechanical properties of actin filament gels. Biophys J 65: 205–214.

    Google Scholar 

  • Wachsstock DH, Schwarz WH and Pollard TD (1994) Cross-linker dynamics determine the mechanical properties of actin gels. Biophys J 66: 801–809.

    Google Scholar 

  • Wagner MC, Barylko B and Albanesi JP (1992) Tissue distribution and subcellular localization of mammalian myosin I. J Cell Biol 119: 163–170.

    Google Scholar 

  • Weber I (2001) On the mechanism of cleavage-furrow ingression in Dictyostelium. Cell Struct Function 26: 577–584.

    Google Scholar 

  • Weber I, Gerisch G, Heizer C, Murphy J, Badelt K, Stock A, Schwartz J-M and Faix J (1999) Cytokinesis mediated through the recruitment of cortexillins into the cleavage-furrow. EMBO J 18: 586–594.

    Google Scholar 

  • Weber I, Neujahr R, Du A, Köler J, Faix J and Gerisch G (2000) Two-step positioning of a cleavage-furrow by cortexillin and myosin II. Curr Biol 10: 501–506.

    Google Scholar 

  • Welch MD (1999) The world according to Arp: regulation of actin nucleation by the Arp2/3 complex. Trends Cell Biol 9: 423–427.

    Google Scholar 

  • White JG and Borisy GG (1983) On the mechanisms of cytokinesis in animal cells. J Theor Biol 101: 289–316.

    Google Scholar 

  • Xu J, Wirtz D and Pollard TD (1998) Dynamic cross-linking by α-actinin determines the mechanical properties of actin filament networks. J Biol Chem 273: 9570–9576.

    Google Scholar 

  • Yoneda M and Dan K (1972) Tension at the surface of the dividing sea-urchin egg. J Exp Biol 57: 575–587.

    Google Scholar 

  • Yumura S (2001) Myosin II dynamics and cortical flow during contractile ring formation in Dictyostelium cells. J Cell Biol 154: 137–145.

    Google Scholar 

  • Zang J-H, Cavet G, Sabry JH, Wagner P, Moores SL and Spudich JA (1997) On the role of myosin-II in cytokinesis: division of Dictyostelium cells under adhesive and nonadhesive conditions. Mol Biol Cell 8: 2617–2629.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell Biology, Johns Hopkins University School of Medicine, 725 N. Wolfe St., Baltimore, MD, 21205, USA

    Douglas N. Robinson, Kristine D. Girard, Edelyn Octtaviani & Elizabeth M. Reichl

Authors
  1. Douglas N. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristine D. Girard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edelyn Octtaviani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elizabeth M. Reichl
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Robinson, D.N., Girard, K.D., Octtaviani, E. et al. Dictyostelium cytokinesis: from molecules to mechanics. J Muscle Res Cell Motil 23, 719–727 (2002). https://doi.org/10.1023/A:1024419510314

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024419510314

Keywords

Search

Navigation