1932

Abstract

Division of amoebas, fungi, and animal cells into two daughter cells at the end of the cell cycle depends on a common set of ancient proteins, principally actin filaments and myosin-II motors. Anillin, formins, IQGAPs, and many other proteins regulate the assembly of the actin filaments into a contractile ring positioned between the daughter nuclei by different mechanisms in fungi and animal cells. Interactions of myosin-II with actin filaments produce force to assemble and then constrict the contractile ring to form a cleavage furrow. Contractile rings disassemble as they constrict. In some cases, knowledge about the numbers of participating proteins and their biochemical mechanisms has made it possible to formulate molecularly explicit mathematical models that reproduce the observed physical events during cytokinesis by computer simulations.

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2019-06-20
2024-12-02
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Literature Cited

  1. 1. 
    Schroeder TE. 1970. The contractile ring. I. Fine structure of dividing mammalian (HeLa) cells and the effects of cytochalasin B. Z. Zellforsch. Mikrosk. Anat. 109:431–49
    [Google Scholar]
  2. 2. 
    Schroeder TE. 1973. Actin in dividing cells: contractile ring filaments bind heavy meromyosin. PNAS 70:1688–92
    [Google Scholar]
  3. 3. 
    Fujiwara K, Pollard TD. 1976. Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J. Cell Biol. 71:848–75
    [Google Scholar]
  4. 4. 
    Mabuchi I, Okuno M. 1977. The effect of myosin antibody on the division of starfish blastomeres. J. Cell Biol. 74:251–63
    [Google Scholar]
  5. 5. 
    Rappaport R. 1967. Cell division: direct measurement of maximum tension exerted by furrow of echinoderm eggs. Science 156:1241–43
    [Google Scholar]
  6. 6. 
    DeLozanne A, Spudich JA. 1987. Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236:1086–91
    [Google Scholar]
  7. 7. 
    Marks J, Hyams JS. 1985. Localization of F-actin through the cell division cycle of Schizosaccharomyces pombe. Eur. J. Cell Biol 39:27–32
    [Google Scholar]
  8. 8. 
    Kitayama C, Sugimoto A, Yamamoto M 1997. Type II myosin heavy chain encoded by the myo2 gene composes the contractile ring during cytokinesis in Schizosaccharomyces pombe. J. Cell Biol 137:1309–19
    [Google Scholar]
  9. 9. 
    Cheffings TH, Burroughs NJ, Balasubramanian MK 2016. Actomyosin ring formation and tension generation in eukaryotic cytokinesis. Curr. Biol. 26:R719–37
    [Google Scholar]
  10. 10. 
    Glotzer M. 2016. Cytokinesis in metazoa and fungi. Cold Spring Harb. Perspect. Biol 9:a022343
    [Google Scholar]
  11. 11. 
    Green RA, Paluch E, Oegema K 2012. Cytokinesis in animal cells. Annu. Rev. Cell Dev. Biol. 28:29–58
    [Google Scholar]
  12. 12. 
    Pollard TD. 2017. Nine unanswered questions about cytokinesis. J. Cell Biol. 216:3007–16
    [Google Scholar]
  13. 13. 
    Odronitz F, Kollmar M. 2007. Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol 8:R196
    [Google Scholar]
  14. 14. 
    Müller S, Jürgens G. 2016. Plant cytokinesis—no ring, no constriction but centrifugal construction of the partitioning membrane. Semin. Cell Dev. Biol. 53:10–18
    [Google Scholar]
  15. 15. 
    Hardin WR, Li R, Xu J, Shelton AM, Alas GCM et al. 2017. Myosin-independent cytokinesis in Giardia utilizes flagella to coordinate force generation and direct membrane trafficking. PNAS 114:E5854–63
    [Google Scholar]
  16. 16. 
    Mierzwa B, Gerlich DW. 2014. Cytokinetic abscission: molecular mechanisms and temporal control. Dev. Cell 31:525–38
    [Google Scholar]
  17. 17. 
    Freémont S, Echard A. 2018. Membrane traffic in the late steps of cytokinesis. Curr. Biol. 28:R458–70
    [Google Scholar]
  18. 18. 
    Xiao J, Goley ED. 2016. Redefining the roles of the FtsZ-ring in bacterial cytokinesis. Curr. Opin. Microbiol. 34:90–96
    [Google Scholar]
  19. 19. 
    Basant A, Glotzer M. 2018. Spatiotemporal regulation of RhoA during cytokinesis. Curr. Biol. 28:R570–80
    [Google Scholar]
  20. 20. 
    Rappaport R. 1996. Cytokinesis in Animal Cells Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  21. 21. 
    Cao LG, Wang YL. 1996. Signals from the spindle midzone are required for the stimulation of cytokinesis in cultured epithelial cells. Mol. Biol. Cell 7:225–32
    [Google Scholar]
  22. 22. 
    von Dassow G, Verbrugghe KJ, Miller AL, Sider JR, Bement WM 2009. Action at a distance during cytokinesis. J. Cell Biol. 187:831–45
    [Google Scholar]
  23. 23. 
    Su KC, Bement WM, Petronczki M, von Dassow G 2014. An astral simulacrum of the central spindle accounts for normal, spindle-less, and anucleate cytokinesis in echinoderm embryos. Mol. Biol. Cell 25:4049–62
    [Google Scholar]
  24. 24. 
    Swan KA, Severson AF, Carter JC, Martin PR, Schnabel H et al. 1998. cyk-1: a C. elegans FH gene required for a late step in embryonic cytokinesis. J. Cell Sci. 111:2017–27
    [Google Scholar]
  25. 25. 
    Bement WM, Benink HA, von Dassow G 2005. A microtubule-dependent zone of active RhoA during cleavage plane specification. J. Cell Biol. 170:91–101
    [Google Scholar]
  26. 26. 
    Miller AL, Bement WM. 2009. Regulation of cytokinesis by Rho GTPase flux. Nat. Cell Biol. 11:71–77
    [Google Scholar]
  27. 27. 
    Rogers SL, Wiedemann U, Stuurman N, Vale RD 2003. Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162:1079–88
    [Google Scholar]
  28. 28. 
    Nguyen PA, Groen AC, Loose M, Ishihara K, Wühr M et al. 2014. Spatial organization of cytokinesis signaling reconstituted in a cell-free system. Science 346:244–47
    [Google Scholar]
  29. 29. 
    Niiya F, Xie X, Lee KS, Inoue H, Miki T 2005. Inhibition of cyclin-dependent kinase 1 induces cytokinesis without chromosome segregation in an ECT2 and MgcRacGAP-dependent manner. J. Biol. Chem. 280:36502–9
    [Google Scholar]
  30. 30. 
    Potapova TA, Daum JR, Pittman BD, Hudson JR, Jones TN et al. 2006. The reversibility of mitotic exit in vertebrate cells. Nature 440:954–58
    [Google Scholar]
  31. 31. 
    Canman JC, Hoffman DB, Salmon ED 2000. The role of pre- and post-anaphase microtubules in the cytokinesis phase of the cell cycle. Curr. Biol. 10:611–14
    [Google Scholar]
  32. 32. 
    Mishima M, Pavicic V, Gruneberg U, Nigg EA, Glotzer M 2004. Cell cycle regulation of central spindle assembly. Nature 430:908–13
    [Google Scholar]
  33. 33. 
    Hara T, Abe M, Inoue H, Yu LR, Veenstra TD et al. 2006. Cytokinesis regulator ECT2 changes its conformation through phosphorylation at Thr-341 in G2/M phase. Oncogene 25:566–78
    [Google Scholar]
  34. 34. 
    Yüce Ö, Piekny A, Glotzer M 2005. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J. Cell Biol. 170:571–82
    [Google Scholar]
  35. 35. 
    Su KC, Takaki T, Petronczki M 2011. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev. Cell 21:1104–15
    [Google Scholar]
  36. 36. 
    Hu CK, Ozlü N, Coughlin M, Steen JJ, Mitchison TJ 2012. Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis. Mol. Biol. Cell 23:2702–11
    [Google Scholar]
  37. 37. 
    Kim H, Guo F, Brahma S, Xing Y, Burkard ME 2014. Centralspindlin assembly and 2 phosphorylations on MgcRacGAP by Polo-like kinase 1 initiate Ect2 binding in early cytokinesis. Cell Cycle 13:2952–61
    [Google Scholar]
  38. 38. 
    Mishima M, Kaitna S, Glotzer M 2002. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell 2:41–54
    [Google Scholar]
  39. 39. 
    White EA, Raghuraman H, Perozo E, Glotzer M 2013. Binding of the CYK-4 subunit of the centralspindlin complex induces a large scale conformational change in the kinesin subunit. J. Biol. Chem. 288:19785–95
    [Google Scholar]
  40. 40. 
    Nislow C, Lombillo VA, Kuriyama R, McIntosh JR 1992. A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature 359:543–47
    [Google Scholar]
  41. 41. 
    Toure A, Dorseuil O, Morin L, Timmons P, Jegou B et al. 1998. MgcRacGAP, a new human GTPase-activating protein for Rac and Cdc42 similar to Drosophila rotundRacGAP gene product, is expressed in male germ cells. J. Biol. Chem. 273:6019–23
    [Google Scholar]
  42. 42. 
    Kimura K, Tsuji T, Takada Y, Miki T, Narumiya S 2000. Accumulation of GTP-bound RhoA during cytokinesis and a critical role of ECT2 in this accumulation. J. Biol. Chem. 275:17233–36
    [Google Scholar]
  43. 43. 
    Lekomtsev S, Su KC, Pye VE, Blight K, Sundaramoorthy S et al. 2012. Centralspindlin links the mitotic spindle to the plasma membrane during cytokinesis. Nature 492:276–79
    [Google Scholar]
  44. 44. 
    Somers WG, Saint R. 2003. A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev. Cell 4:29–39
    [Google Scholar]
  45. 45. 
    Zhang D, Glotzer M. 2015. The RhoGAP activity of CYK-4/MgcRacGAP functions non-canonically by promoting RhoA activation during cytokinesis. eLife 4:e08898
    [Google Scholar]
  46. 46. 
    Carmena M, Wheelock M, Funabiki H, Earnshaw WC 2012. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat. Rev. Mol. Cell. Biol. 13:789–803
    [Google Scholar]
  47. 47. 
    Basant A, Lekomtsev S, Tse YC, Zhang D, Longhini KM et al. 2015. Aurora B kinase promotes cytokinesis by inducing centralspindlin oligomers that associate with the plasma membrane. Dev. Cell 33:204–15
    [Google Scholar]
  48. 48. 
    Prokopenko SN, Brumby A, O'Keefe L, Prior L, He Y et al. 1999. A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. . Genes Dev 13:2301–14
    [Google Scholar]
  49. 49. 
    Tatsumoto T, Xie X, Blumenthal R, Okamoto I, Miki T 1999. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J. Cell Biol. 147:921–28
    [Google Scholar]
  50. 50. 
    Wagner E, Glotzer M. 2016. Local RhoA activation induces cytokinetic furrows independent of spindle position and cell cycle stage. J. Cell Biol. 213:641–49
    [Google Scholar]
  51. 51. 
    Kim J-E, Billadeau DD, Chen J 2005. The tandem BRCT domains of Ect2 are required for both negative and positive regulation of Ect2 in cytokinesis. J. Biol. Chem. 280:5733–39
    [Google Scholar]
  52. 52. 
    Nishimura Y, Yonemura S. 2006. Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J. Cell Sci. 119:104–14
    [Google Scholar]
  53. 53. 
    Schmutz C, Stevens J, Spang A 2007. Functions of the novel RhoGAP proteins RGA-3 and RGA-4 in the germ line and in the early embryo of C. elegans. . Development 134:3495–505
    [Google Scholar]
  54. 54. 
    Schonegg S, Constantinescu AT, Hoege C, Hyman AA 2007. The Rho GTPase-activating proteins RGA-3 and RGA-4 are required to set the initial size of PAR domains in Caenorhabditis elegans one-cell embryos. PNAS 104:14976–81
    [Google Scholar]
  55. 55. 
    Zanin E, Desai A, Poser I, Toyoda Y, Andree C et al. 2013. A conserved RhoGAP limits M phase contractility and coordinates with microtubule asters to confine RhoA during cytokinesis. Dev. Cell 26:496–510
    [Google Scholar]
  56. 56. 
    Tse YC, Werner M, Longhini KM, Labbé J-C, Goldstein B, Glotzer M 2012. RhoA activation during polarization and cytokinesis of the early Caenorhabditis elegans embryo is differentially dependent on NOP-1 and CYK-4. Mol. Biol. Cell 23:4020–31
    [Google Scholar]
  57. 57. 
    Carvalho A, Desai A, Oegema K 2009. Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size. Cell 137:926–37
    [Google Scholar]
  58. 58. 
    Canman JC, Lewellyn L, Laband K, Smerdon SJ, Desai A et al. 2008. Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science 322:1543–46
    [Google Scholar]
  59. 59. 
    Zhuravlev Y, Hirsch SM, Jordan SN, Dumont J, Shirasu-Hiza M, Canman JC 2017. CYK-4 regulates Rac, but not Rho, during cytokinesis. Mol. Biol. Cell 28:1258–70
    [Google Scholar]
  60. 60. 
    Hutterer A, Glotzer M, Mishima M 2009. Clustering of centralspindlin is essential for its accumulation to the central spindle and the midbody. Curr. Biol. 19:2043–49
    [Google Scholar]
  61. 61. 
    Subramanian R, Wilson-Kubalek EM, Arthur CP, Bick MJ, Campbell EA et al. 2010. Insights into antiparallel microtubule crosslinking by PRC1, a conserved nonmotor microtubule binding protein. Cell 142:433–43
    [Google Scholar]
  62. 62. 
    Verbrugghe KJC, White JG. 2004. SPD-1 is required for the formation of the spindle midzone but is not essential for the completion of cytokinesis in C. elegans embryos. Curr. Biol. 14:1755–60
    [Google Scholar]
  63. 63. 
    Kotynkova K, Su KC, West SC, Petronczki M 2016. Plasma membrane association but not midzone recruitment of RhoGEF ECT2 is essential for cytokinesis. Cell Rep 17:2672–86
    [Google Scholar]
  64. 64. 
    Rodrigues NT, Lekomtsev S, Jananji S, Kriston-Vizi J, Hickson GR, Baum B 2015. Kinetochore-localized PP1–Sds22 couples chromosome segregation to polar relaxation. Nature 524:489–92
    [Google Scholar]
  65. 65. 
    Bieling P, Telley IA, Surrey T 2010. A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell 142:420–32
    [Google Scholar]
  66. 66. 
    Mangal S, Sacher J, Kim T, Osório DS, Motegi F et al. 2018. TPXL-1 activates Aurora A to clear contractile ring components from the polar cortex during cytokinesis. J. Cell Biol. 217:837–48
    [Google Scholar]
  67. 67. 
    Akamatsu MS, Berro J, Pu K-M, Tebbs IR, Pollard TD 2014. Cytokinetic nodes in fission yeast arise from two distinct types of nodes that merge during interphase. J. Cell Biol. 204:977–88
    [Google Scholar]
  68. 68. 
    Moseley JB, Mayeux A, Paoletti A, Nurse P 2009. A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 459:857–60
    [Google Scholar]
  69. 69. 
    Martin SG, Berthelot-Grosjean M. 2009. Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 459:852–56
    [Google Scholar]
  70. 70. 
    Akamatsu M, Lin Y, Bewersdorf J, Pollard TD 2017. Analysis of interphase node proteins in fission yeast by quantitative and super resolution fluorescence microscopy. Mol. Biol. Cell 28:3203–14
    [Google Scholar]
  71. 71. 
    Paoletti A, Chang F. 2000. 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 11:2757–73
    [Google Scholar]
  72. 72. 
    Sun L, Guan R, Lee IJ, Liu Y, Chen M et al. 2015. Mechanistic insights into the anchorage of the contractile ring by anillin and Mid1. Dev. Cell 33:413–26
    [Google Scholar]
  73. 73. 
    Huang Y, Chew TG, Ge W, Balasubramanian MK 2007. Polarity determinants Tea1p, Tea4p, and Pom1p inhibit division-septum assembly at cell ends in fission yeast. Dev. Cell 12:987–96
    [Google Scholar]
  74. 74. 
    Hersch M, Hachet O, Dalessi S, Ullal P, Bhatia P et al. 2015. Pom1 gradient buffering through intermolecular auto-phosphorylation. Mol. Syst. Biol. 11:818
    [Google Scholar]
  75. 75. 
    Rincon SA, Bhatia P, Bicho C, Guzman-Vendrell M, Fraisier V et al. 2014. Pom1 regulates the assembly of Cdr2-Mid1 cortical nodes for robust spatial control of cytokinesis. J. Cell Biol. 206:61–77
    [Google Scholar]
  76. 76. 
    Celton-Morizur S, Bordes N, Fraisier V, Tran PT, Paoletti A 2004. C-terminal anchoring of mid1p to membranes stabilizes cytokinetic ring position in early mitosis in fission yeast. Mol. Cell. Biol. 24:10621–35
    [Google Scholar]
  77. 77. 
    Padte NN, Martin SG, Howard M, Chang F 2006. The cell-end factor pom1p inhibits mid1p in specification of the cell division plane in fission yeast. Curr. Biol. 16:2480–87
    [Google Scholar]
  78. 78. 
    Lee ME, Rusin SF, Jenkins N, Kettenbach AN, Moseley JB 2018. Mechanisms connecting the conserved protein kinases Ssp1, Kin1, and Pom1 in fission yeast cell polarity and division. Curr. Biol. 28:84–92
    [Google Scholar]
  79. 79. 
    Tran PT, Doye V, Inoué S, Chang F 2001. A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J. Cell Biol. 153:397–411
    [Google Scholar]
  80. 80. 
    Daga RR, Chang F. 2005. Dynamic positioning of the fission yeast cell division plane. PNAS 102:8228–32
    [Google Scholar]
  81. 81. 
    Tolic-Norrelykke IM, Sacconi L, Stringari C, Raabe I, Pavone FS 2005. Nuclear and division-plane positioning revealed by optical micromanipulation. Curr. Biol. 15:1212–16
    [Google Scholar]
  82. 82. 
    Chang F, Wollard A, Nurse P 1996. Isolation and characterization of fission yeast mutants defective in the assembly and placement of the contractile actin ring. J. Cell Sci. 109:131–42
    [Google Scholar]
  83. 83. 
    Sohrmann M, Fankhauser C, Brodbeck C, Simanis V 1996. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast. Genes Dev 10:2707–19
    [Google Scholar]
  84. 84. 
    Wu JQ, Kuhn JR, Kovar DR, Pollard TD 2003. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev. Cell 5:723–34
    [Google Scholar]
  85. 85. 
    Almonacid M, Celton-Morizur S, Jakubowski J, Dingli F, Loew D et al. 2011. Temporal control of contractile ring assembly by Plo1 regulation of myosin II recruitment by Mid1/anillin. Curr. Biol. 21:473–79
    [Google Scholar]
  86. 86. 
    Almonacid M, Moseley JB, Janvore J, Mayeux A, Fraisier V et al. 2009. Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export. Curr. Biol. 19:961–66
    [Google Scholar]
  87. 87. 
    Rincon SA, Paoletti A. 2012. Mid1/anillin and the spatial regulation of cytokinesis in fission yeast. Cytoskeleton 69:764–77
    [Google Scholar]
  88. 88. 
    Simanis V. 2015. Pombe's thirteen—control of fission yeast cell division by the septation initiation network. J. Cell Sci. 128:1465–74
    [Google Scholar]
  89. 89. 
    Rincon SA, Estravis M, Dingli F, Loew D, Tran PT, Paoletti A 2017. SIN-dependent dissociation of the SAD kinase Cdr2 from the cell cortex resets the division plane. Curr. Biol. 27:534–42
    [Google Scholar]
  90. 90. 
    Pu K-M, Akamatsu M, Pollard TD 2015. The fission yeast septation initiation network controls type 1 cytokinesis nodes. J. Cell Sci. 128:441–46
    [Google Scholar]
  91. 91. 
    Chiou JG, Balasubramanian MK, Lew DJ 2017. Cell polarity in yeast. Annu. Rev. Cell Dev. Biol. 33:77–101
    [Google Scholar]
  92. 92. 
    Goryachev AB, Pokhilko AV. 2008. Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. FEBS Lett 582:1437–43
    [Google Scholar]
  93. 93. 
    Witte K, Strickland D, Glotzer M 2017. Cell cycle entry triggers a switch between two modes of Cdc42 activation during yeast polarization. eLife 6:e26722
    [Google Scholar]
  94. 94. 
    Miyazaki M, Chiba M, Eguchi H, Ohki T, Ishiwata S 2015. Cell-sized spherical confinement induces the spontaneous formation of contractile actomyosin rings in vitro. Nat. Cell Biol. 17:480–89
    [Google Scholar]
  95. 95. 
    Wu JQ, Pollard TD. 2005. Counting cytokinesis proteins globally and locally in fission yeast. Science 310:310–14
    [Google Scholar]
  96. 96. 
    Laplante C, Huang F, Tebbs IR, Bewersdorf J, Pollard TD 2016. Molecular organization of cytokinesis nodes and contractile rings by super-resolution fluorescence microscopy of live fission yeast. PNAS 113:E5876–85
    [Google Scholar]
  97. 97. 
    Willet AH, McDonald NA, Bohnert KA, Baird MA, Allen JR et al. 2015. The F-BAR Cdc15 promotes contractile ring formation through the direct recruitment of the formin Cdc12. J. Cell Biol. 208:391–99
    [Google Scholar]
  98. 98. 
    Kovar DR, Kuhn JR, Tichy AL, Pollard TD 2003. The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J. Cell Biol. 161:875–87
    [Google Scholar]
  99. 99. 
    Courtemanche N, Pollard TD, Chen Q 2016. Avoiding artefacts when counting polymerized actin in live cells with LifeAct fused to fluorescent proteins. Nat. Cell Biol. 18:676–83
    [Google Scholar]
  100. 100. 
    Vavylonis D, Wu J-Q, Hao S, O'Shaughnessy B, Pollard TD 2008. Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 319:97–100
    [Google Scholar]
  101. 101. 
    Wang N, Lo Presti L, Zhu YH, Kang M, Wu Z et al. 2014. The novel proteins Rng8 and Rng9 regulate the myosin-V Myo51 during fission yeast cytokinesis. J. Cell Biol. 205:357–75
    [Google Scholar]
  102. 102. 
    Laplante C, Berro J, Karatekin E, Lee R, Hernandez-Leyva A, Pollard TD 2015. Three myosins contribute uniquely to the assembly and constriction of the cytokinetic contractile ring in fission yeast. Curr. Biol. 25:1955–65
    [Google Scholar]
  103. 103. 
    Chen Q, Pollard TD. 2011. Actin filament severing by cofilin is more important for assembly than constriction of the cytokinetic contractile ring. J. Cell Biol. 195:485–98
    [Google Scholar]
  104. 104. 
    Bidone TC, Tang H, Vavylonis D 2014. Dynamic network morphology and tension buildup in 3D model of cytokinetic ring assembly. Biophys. J. 107:2618–28
    [Google Scholar]
  105. 105. 
    Bhavsar-Jog YP, Bi E. 2017. Mechanics and regulation of cytokinesis in budding yeast. Semin. Cell Dev. Biol. 66:107–18
    [Google Scholar]
  106. 106. 
    Matsumura F. 2005. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol 15:371–77
    [Google Scholar]
  107. 107. 
    Watanabe S, Ando Y, Yasuda S, Hosoya H, Watanabe N et al. 2008. mDia2 induces the actin scaffold for the contractile ring and stabilizes its position during cytokinesis in NIH 3T3 cells. Mol. Biol. Cell 19:2328–38
    [Google Scholar]
  108. 108. 
    Beach JR, Shao L, Remmert K, Li D, Betzig E, Hammer JA III 2014. Nonmuscle myosin II isoforms coassemble in living cells. Curr. Biol. 24:1160–66
    [Google Scholar]
  109. 109. 
    Henson JH, Ditzler CE, Germain A, Irwin PM, Vogt ET et al. 2017. The ultrastructural organization of actin and myosin II filaments in the contractile ring: new support for an old model of cytokinesis. Mol. Biol. Cell 28:613–23
    [Google Scholar]
  110. 110. 
    Schroeder TE, Otto J. 1988. Association of actin and myosin in the contractile ring. Zool. Sci. 5:713–25
    [Google Scholar]
  111. 111. 
    Dean SO, Rogers SL, Stuurman N, Vale RD, Spudich JA 2005. Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis. PNAS 102:13473–78
    [Google Scholar]
  112. 112. 
    Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ et al. 2003. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science 299:1743–47
    [Google Scholar]
  113. 113. 
    Castrillon D, Wasserman S. 1994. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120:3367–77
    [Google Scholar]
  114. 114. 
    Watanabe S, De Zan T, Ishizaki T, Yasuda S, Kamijo H et al. 2013. Loss of a Rho-regulated actin nucleator, mDia2, impairs cytokinesis during mouse fetal erythropoiesis. Cell Rep 5:926–32
    [Google Scholar]
  115. 115. 
    Chalut KJ, Paluch EK. 2016. The actin cortex: a bridge between cell shape and function. Dev. Cell 38:571–73
    [Google Scholar]
  116. 116. 
    Reymann AC, Staniscia F, Erzberger A, Salbreux G, Grill SW 2016. Cortical flow aligns actin filaments to form a furrow. eLife 5:e17807
    [Google Scholar]
  117. 117. 
    Hiramoto Y. 1970. Rheological properties of sea urchin eggs. Biorheology 6:201–34
    [Google Scholar]
  118. 118. 
    Hiramoto Y. 1975. Force exerted by the cleavage furrow of sea urchin eggs. Dev. Growth Differ. 17:27–38
    [Google Scholar]
  119. 119. 
    Yoneda M, Dan K. 1972. Tension at the surface of the dividing sea-urchin egg. J. Exp. Biol. 57:575–87
    [Google Scholar]
  120. 120. 
    Stachowiak MR, Laplante C, Chin HF, Guirao B, Karatekin E et al. 2014. Mechanism of cytokinetic contractile ring constriction in fission yeast. Dev. Cell 29:547–61
    [Google Scholar]
  121. 121. 
    Schroeder TE. 1972. The contractile ring. II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs. J. Cell Biol. 53:419–34
    [Google Scholar]
  122. 122. 
    Kamasaki T, Osumi M, Mabuchi I 2007. Three-dimensional arrangement of F-actin in the contractile ring of fission yeast. J. Cell Biol. 178:765–71
    [Google Scholar]
  123. 123. 
    Swulius MT, Nguyen LT, Ladinsky MS, Ortega DR, Aich S et al. 2018. Structure of the fission yeast actomyosin ring during constriction. PNAS 115:E1455–64
    [Google Scholar]
  124. 124. 
    McDonald NA, Lind AL, Smith SE, Li R, Gould KL 2017. Nanoscale architecture of the Schizosaccharomyces pombe contractile ring. eLife 6:e28865
    [Google Scholar]
  125. 125. 
    Takaine M, Numata O, Nakano K 2015. An actin–myosin-II interaction is involved in maintaining the contractile ring in fission yeast. J. Cell Sci. 128:2903–18
    [Google Scholar]
  126. 126. 
    Lord M, Pollard TD. 2004. UCS protein Rng3p activates actin filament gliding by fission yeast myosin-II. J. Cell Biol. 167:315–25
    [Google Scholar]
  127. 127. 
    Molloy JE, Burns JE, Kendrick-Jones J, Tregear RT, White DC 1995. Movement and force produced by a single myosin head. Nature 378:209–12
    [Google Scholar]
  128. 128. 
    Stark BC, Sladewski TE, Pollard LW, Lord M 2010. Tropomyosin and myosin-II cellular levels promote actomyosin ring assembly in fission yeast. Mol. Biol. Cell 21:989–1000
    [Google Scholar]
  129. 129. 
    Thiyagarajan S, Wang S, O'Shaughnessy B 2017. A node organization in the actomyosin contractile ring generates tension and aids stability. Mol. Biol. Cell 28:3286–97
    [Google Scholar]
  130. 130. 
    Thiyagarajan S, Munteanu EL, Arasada R, Pollard TD, O'Shaughnessy B 2015. The fission yeast cytokinetic contractile ring regulates septum shape and closure. J. Cell Sci. 28:3672–81
    [Google Scholar]
  131. 131. 
    Stachowiak MR, McCall PM, Thoresen T, Balcioglu HE, Kasiewicz L et al. 2012. Self-organization of myosin II in reconstituted actomyosin bundles. Biophys. J. 103:1265–74
    [Google Scholar]
  132. 132. 
    Wollrab V, Thiagarajan R, Wald A, Kruse K, Riveline D 2016. Still and rotating myosin clusters determine cytokinetic ring constriction. Nat. Commun. 7:11860
    [Google Scholar]
  133. 133. 
    Nguyen LT, Swulius MT, Aich S, Mishra M, Jensen GJ 2018. Coarse-grained simulations of actomyosin rings point to a nodeless model involving both unipolar and bipolar myosins. Mol. Biol. Cell 29:1318–31
    [Google Scholar]
  134. 134. 
    Cortés JC, Konomi M, Martins IM, Muñoz J, Moreno MB et al. 2007. The (1,3)β-d-glucan synthase subunit Bgs1p is responsible for the fission yeast primary septum formation. Mol. Microbiol. 65:201–17
    [Google Scholar]
  135. 135. 
    Muñoz J, Cortés J, Sipiczki M, Ramos M, Clemente-Ramos JA et al. 2013. Extracellular cell wall β(1,3)glucan is required to couple septation to actomyosin ring contraction. J. Cell Biol. 203:265–82
    [Google Scholar]
  136. 136. 
    Atilgan E, Magidson V, Khodjakov A, Chang F 2015. Morphogenesis of the fission yeast cell through cell wall expansion. Curr. Biol. 25:2150–57
    [Google Scholar]
  137. 137. 
    Proctor SA, Minc N, Boudaoud A, Chang F 2012. Contributions of turgor pressure, the contractile ring, and septum assembly to forces in cytokinesis in fission yeast. Curr. Biol. 22:1601–8
    [Google Scholar]
  138. 138. 
    Zhou Z, Munteanu EL, He J, Ursell T, Bathe M et al. 2015. The contractile ring coordinates curvature-dependent septum assembly during fission yeast cytokinesis. Mol. Biol. Cell 26:78–90
    [Google Scholar]
  139. 139. 
    Mishra M, Kashiwazaki J, Takagi T, Srinivasan R, Huang Y et al. 2013. In vitro contraction of cytokinetic ring depends on myosin II but not on actin dynamics. Nat. Cell Biol. 15:853–59
    [Google Scholar]
  140. 140. 
    Young BA, Buser C, Drubin DG 2010. Isolation and partial purification of the Saccharomyces cerevisiae cytokinetic apparatus. Cytoskeleton 67:13–22
    [Google Scholar]
  141. 141. 
    Ong K, Wloka C, Okada S, Svitkina T, Bi E 2014. Architecture and dynamic remodelling of the septin cytoskeleton during the cell cycle. Nat. Commun. 5:5698
    [Google Scholar]
  142. 142. 
    Wloka C, Vallen EA, Thé L, Fang X, Oh Y, Bi E 2013. Immobile myosin-II plays a scaffolding role during cytokinesis in budding yeast. J. Cell Biol. 200:271–86
    [Google Scholar]
  143. 143. 
    Tully GH, Nishihama R, Pringle JR, Morgan DO 2009. The anaphase-promoting complex promotes actomyosin-ring disassembly during cytokinesis in yeast. Mol. Biol. Cell 20:1201–12
    [Google Scholar]
  144. 144. 
    Bi E, Maddox P, Lew DJ, Salmon ED, McMillan JN et al. 1998. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 142:1301–12
    [Google Scholar]
  145. 145. 
    Lord M, Laves E, Pollard TD 2005. Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast. Mol. Biol. Cell 16:5346–55
    [Google Scholar]
  146. 146. 
    Mendes Pinto I, Rubinstein B, Kucharavy A, Unruh JR, Li R 2012. Actin depolymerization drives actomyosin ring contraction during budding yeast cytokinesis. Dev. Cell 22:1247–60
    [Google Scholar]
  147. 147. 
    Srivastava V, Iglesias PA, Robinson DN 2016. Cytokinesis: robust cell shape regulation. Semin. Cell Dev. Biol. 53:39–44
    [Google Scholar]
  148. 148. 
    Faix J, Weber I, Mintert U, Köhler J, Lottspeich F, Marriott G 2001. Recruitment of cortexillin into the cleavage furrow is controlled by Rac1 and IQGAP-related proteins. EMBO J 20:3705–15
    [Google Scholar]
  149. 149. 
    Yumura S, Fukui Y. 1985. Reversible cyclic AMP-dependent change in distribution of myosin thick filaments in Dictyostelium. . Nature 314:194–96
    [Google Scholar]
  150. 150. 
    Reichl EM, Ren Y, Morphew MK, Delannoy M, Effler JC et al. 2008. Interactions between myosin and actin crosslinkers control cytokinesis contractility dynamics and mechanics. Curr. Biol. 18:471–80
    [Google Scholar]
  151. 151. 
    Robinson DN, Cavet G, Warrick HM, Spudich JA 2002. Quantitation of the distribution and flux of myosin-II during cytokinesis. BMC Cell Biol 3:4
    [Google Scholar]
  152. 152. 
    Yumura S. 2001. Myosin II dynamics and cortical flow during contractile ring formation in Dictyostelium cells. J. Cell Biol. 154:137–45
    [Google Scholar]
  153. 153. 
    Poirier CC, Ng WP, Robinson DN, Iglesias PA 2012. Deconvolution of the cellular force-generating subsystems that govern cytokinesis furrow ingression. PLOS Comput. Biol. 8:e1002467
    [Google Scholar]
  154. 154. 
    Zhang WD, Robinson DN. 2005. Balance of actively generated contractile and resistive forces controls cytokinesis dynamics. PNAS 102:7186–91
    [Google Scholar]
  155. 155. 
    Sanger JM, Sanger JW. 1980. Banding and polarity of actin filaments in interphase and cleaving cells. J. Cell Biol. 86:568–75
    [Google Scholar]
  156. 156. 
    Maupin P, Pollard TD. 1986. Arrangement of actin filaments and myosin-like filaments in the contractile ring and of actin-like filaments in the mitotic spindle of dividing HeLa cells. J. Ultrastruct. Mol. Struct. Res. 94:92–103
    [Google Scholar]
  157. 157. 
    Maupin P, Phillips CL, Adelstein RS, Pollard TD 1994. Differential localization of myosin-II isozymes in human cultured cells and blood cells. J. Cell Sci. 107:3077–90
    [Google Scholar]
  158. 158. 
    Zhou M, Wang YL. 2008. Distinct pathways for the early recruitment of myosin II and actin to the cytokinetic furrow. Mol. Biol. Cell 19:318–26
    [Google Scholar]
  159. 159. 
    Khaliullin RN, Green RA, Shi LZ, Gomez-Cavazos JS, Berns MW et al. 2018. A positive-feedback-based mechanism for constriction rate acceleration during cytokinesis in Caenorhabditzs elegans. . eLife 7:e36073
    [Google Scholar]
  160. 160. 
    Hiramoto Y. 1967. Observations and measurements of sea urchin eggs with a centrifuge microscope. J. Am. Vet. Med. Assoc. 150:219–30
    [Google Scholar]
  161. 161. 
    Ma X, Kovacs M, Conti MA, Wang A, Zhang Y et al. 2012. Nonmuscle myosin II exerts tension but does not translocate actin in vertebrate cytokinesis. PNAS 109:4509–14
    [Google Scholar]
  162. 162. 
    Joanny JF, Kruse K, Ramaswamy S 2013. The actin cortex as an active wetting layer. Eur. Phys. J. E 36:52–58
    [Google Scholar]
  163. 163. 
    Turlier H, Audoly B, Prost J, Joanny JF 2014. Furrow constriction in animal cell cytokinesis. Biophys. J. 106:114–23
    [Google Scholar]
  164. 164. 
    Dorn JF, Zhang L, Phi TT, Lacroix B, Maddox PS et al. 2016. A theoretical model of cytokinesis implicates feedback between membrane curvature and cytoskeletal organization in asymmetric cytokinetic furrowing. Mol. Biol. Cell 27:1286–99
    [Google Scholar]
  165. 165. 
    Calvert ME, Wright GD, Leong FY, Chiam KH, Chen Y et al. 2011. Myosin concentration underlies cell size-dependent scalability of actomyosin ring constriction. J. Cell Biol. 195:799–813
    [Google Scholar]
  166. 166. 
    Zumdieck A, Kruse K, Bringmann H, Hyman AA, Jülicher F 2007. Stress generation and filament turnover during actin ring constriction. PLOS ONE 2:e696
    [Google Scholar]
  167. 167. 
    Lenz M, Thoresen T, Gardel ML, Dinner AR 2012. Contractile units in disordered actomyosin bundles arise from F-actin buckling. Phys. Rev. Lett. 108:238107
    [Google Scholar]
  168. 168. 
    Oelz D, Rubinstein B, Mogilner A 2015. A combination of actin treadmilling and cross-linking drives contraction of random actomyosin arrays. Biophys. J. 109:1818–29
    [Google Scholar]
  169. 169. 
    McDonald NA, Vander Kooi CW, Ohi MD, Gould KL 2015. Oligomerization but not membrane bending underlies the function of certain F-BAR proteins in cell motility and cytokinesis. Dev. Cell 35:725–36
    [Google Scholar]
  170. 170. 
    Snider CE, Willet AH, Chen JS, Arpağ G, Zanic M, Gould KL 2017. Phosphoinositide-mediated ring anchoring resists perpendicular forces to promote medial cytokinesis. J. Cell Biol. 216:3041–50
    [Google Scholar]
  171. 171. 
    Meitinger F, Palani S. 2016. Actomyosin ring driven cytokinesis in budding yeast. Semin. Cell Dev. Biol. 53:19–27
    [Google Scholar]
  172. 172. 
    Arasada R, Pollard TD. 2014. Contractile ring stability in S. pombe depends on F-BAR protein Cdc15p and Bgs1p transport from the Golgi complex. Cell Rep 8:1533–44
    [Google Scholar]
  173. 173. 
    Sethi K, Palani S, Cortés JC, Sato M, Sevugan M et al. 2016. A new membrane protein Sbg1 links the contractile ring apparatus and septum synthesis machinery in fission yeast. PLOS Genet 12:e1006383
    [Google Scholar]
  174. 174. 
    Hoffman BD, Yap AS. 2015. Towards a dynamic understanding of cadherin-based mechanobiology. Trends Cell Biol 25:803–14
    [Google Scholar]
  175. 175. 
    Mishra M, Huang Y, Srivastava P, Srinivasan R, Sevugan M et al. 2012. Cylindrical cellular geometry ensures fidelity of division site placement in fission yeast. J. Cell Sci. 125:3850–57
    [Google Scholar]
  176. 176. 
    Pelham RJ Jr, Chang F. 2001. Role of actin polymerization and actin cables in actin-patch movement in Schizosaccharomyces pombe. Nat. Cell Biol 3:235–44
    [Google Scholar]
  177. 177. 
    Sedzinski J, Biro M, Oswald A, Tinevez JY, Salbreux G, Paluch E 2011. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 476:462–66
    [Google Scholar]
  178. 178. 
    Tinevez JY, Schulze U, Salbreux G, Roensch J, Joanny JF, Paluch E 2009. Role of cortical tension in bleb growth. PNAS 106:18581–86
    [Google Scholar]
  179. 179. 
    Wang N, Lee IJ, Rask G, Wu JQ 2016. Roles of the TRAPP-II complex and the exocyst in membrane deposition during fission yeast cytokinesis. PLOS Biol 14:e1002437
    [Google Scholar]
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