On the cutting edge: Post-translational modifications in cytokinesis

Trends in Cell Biology

Volumn 21, Issue 5, 2011, Pages 283-292

  Bohnert, K Adam ^a   Gould, Kathleen L ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTRACTILE PROTEIN;

CELL DIVISION; CYTOKINESIS; DAUGHTER CELL; GLYCOSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SUMOYLATION; UBIQUITINATION;

ANIMALS; CONTRACTILE PROTEINS; CYTOKINESIS; CYTOSKELETAL PROTEINS; CYTOSKELETON; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; YEASTS;

EID: 79955542287     PISSN: 09628924     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tcb.2011.01.006     Document Type: Review

References (110)

1. Pollard T.D. Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 2010, 22:50-56.
2. Pollard T.D., Wu J.Q. Understanding cytokinesis: lessons from fission yeast. Nat. Rev. Mol. Cell Biol. 2010, 11:149-155.
3. King R.W., et al. How proteolysis drives the cell cycle. Science 1996, 274:1652-1659.
4. Hunter T. A thousand and one protein kinases. Cell 1987, 50:823-829.
5. Coffman V.C., et al. Roles of formin nodes and myosin motor activity in Mid1p-dependent contractile-ring assembly during fission yeast cytokinesis. Mol. Biol. Cell 2009, 20:5195-5210.
6. Vavylonis D., et al. Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 2008, 319:97-100.
7. Almonacid M., et al. Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export. Curr. Biol. 2009, 19:961-966.
8. Bahler J., et al. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast. J. Cell Biol. 1998, 143:1603-1616.
9. Martin S.G., Berthelot-Grosjean M. Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle. Nature 2009, 459:852-856.
10. Huang Y., et al. Polarity determinants Tea1p Tea4p, and Pom1p inhibit division-septum assembly at cell ends in fission yeast. Dev. Cell 2007, 12:987-996.
11. Moseley J.B., et al. A spatial gradient coordinates cell size and mitotic entry in fission yeast. Nature 2009, 459:857-860.
12. Zhou M., Wang Y.L. Distinct pathways for the early recruitment of myosin II and actin to the cytokinetic furrow. Mol. Biol. Cell 2008, 19:318-326.
13. Werner M., et al. Astral signals spatially bias cortical myosin recruitment to break symmetry and promote cytokinesis. Curr. Biol. 2007, 17:1286-1297.
14. Huang Y., et al. Assembly of normal actomyosin rings in the absence of Mid1p and cortical nodes in fission yeast. J. Cell Biol. 2008, 183:979-988.
15. Kamasaki T., et al. Three-dimensional arrangement of F-actin in the contractile ring of fission yeast. J. Cell Biol. 2007, 178:765-771.
16. Hachet O., Simanis V. Mid1p/anillin and the septation initiation network orchestrate contractile ring assembly for cytokinesis. Genes Dev. 2008, 22:3205-3216.
17. Mohl D.A., et al. Dbf2-Mob1 drives relocalization of protein phosphatase Cdc14 to the cytoplasm during exit from mitosis. J. Cell Biol. 2009, 184:527-539.
18. Chen C.T., et al. The SIN kinase Sid2 regulates cytoplasmic retention of the S. pombe Cdc14-like phosphatase Clp1. Curr. Biol. 2008, 18:1594-1599.
19. Glotzer M. The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat. Rev. Mol. Cell Biol. 2009, 10:9-20.
20. Wolf F., et al. The end of the beginning': cdk1 thresholds and exit from mitosis. Cell Cycle 2007, 6:1408-1411.
21. Wolfe B.A., et al. Phospho-regulation of the Cdc14/Clp1 phosphatase delays late mitotic events in S. pombe. Dev. Cell 2006, 11:423-430.
22. Clifford D.M., et al. The Clp1/Cdc14 phosphatase contributes to the robustness of cytokinesis by association with anillin-related Mid1. J. Cell Biol. 2008, 181:79-88.
23. Roberts-Galbraith R.H., et al. Dephosphorylation of F-BAR protein Cdc15 modulates its conformation and stimulates its scaffolding activity at the cell division site. Mol. Cell 2010, 39:86-99.
24. Li C.R., et al. The IQGAP Iqg1 is a regulatory target of CDK for cytokinesis in Candida albicans. EMBO J. 2008, 27:2998-3010.
25. Yoshida S., et al. Polo-like kinase Cdc5 controls the local activation of Rho1 to promote cytokinesis. Science 2006, 313:108-111.
26. Yoshida S., et al. Mechanisms for concentrating Rho1 during cytokinesis. Genes Dev. 2009, 23:810-823.
27. Wolfe B.A., et al. Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol. 2009, 7:e1000110.
28. Burkard M.E., et al. Plk1 self-organization and priming phosphorylation of HsCYK-4 at the spindle midzone regulate the onset of division in human cells. PLoS Biol. 2009, 7:e1000111.
29. Douglas M.E., et al. Aurora B and 14-3-3 coordinately regulate clustering of centralspindlin during cytokinesis. Curr. Biol. 2010, 20:927-933.
30. Mishima M., et al. Cell cycle regulation of central spindle assembly. Nature 2004, 430:908-913.
31. Miller A.L., Bement W.M. Regulation of cytokinesis by Rho GTPase flux. Nat. Cell Biol. 2009, 11:71-77.
32. Toure A., et al. Phosphoregulation of MgcRacGAP in mitosis involves Aurora B and Cdk1 protein kinases and the PP2A phosphatase. FEBS Lett. 2008, 582:1182-1188.
33. Asiedu M., et al. Phosphorylation of MyoGEF on Thr-574 by Plk1 promotes MyoGEF localization to the central spindle. J. Biol. Chem. 2008, 283:28392-28400.
34. Birkenfeld J., et al. GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev. Cell 2007, 12:699-712.
35. Rosario C.O., et al. Plk4 is required for cytokinesis and maintenance of chromosomal stability. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:6888-6893.
36. Minoshima Y., et al. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev. Cell 2003, 4:549-560.
37. Matsumura F. Regulation of myosin II during cytokinesis in higher eukaryotes. Trends Cell Biol. 2005, 15:371-377.
38. Mizutani T., et al. Diphosphorylation of the myosin regulatory light chain enhances the tension acting on stress fibers in fibroblasts. J. Cell Physiol. 2006, 209:726-731.
39. Mizutani T., et al. Regulation of cellular contractile force in response to mechanical stretch by diphosphorylation of myosin regulatory light chain via RhoA signaling cascade. Cell Motil. Cytoskeleton 2009, 66:389-397.
40. Wu Q., et al. Deficiency in myosin light-chain phosphorylation causes cytokinesis failure and multipolarity in cancer cells. Oncogene 2010, 29:4183-4193.
41. Uehara R., et al. Determinants of myosin II cortical localization during cytokinesis. Curr. Biol. 2010, 20:1080-1085.
42. Beach J.R., Egelhoff T.T. Myosin II recruitment during cytokinesis independent of centralspindlin-mediated phosphorylation. J. Biol. Chem. 2009, 284:27377-27383.
43. Joo E., et al. Mammalian SEPT2 is required for scaffolding nonmuscle myosin II and its kinases. Dev. Cell 2007, 13:677-690.
44. Lordier L., et al. Megakaryocyte endomitosis is a failure of late cytokinesis related to defects in the contractile ring and Rho/Rock signaling. Blood 2008, 112:3164-3174.
45. Gruneberg U., et al. KIF14 and citron kinase act together to promote efficient cytokinesis. J. Cell Biol. 2006, 172:363-372.
46. Lucero A., et al. A global, myosin light chain kinase-dependent increase in myosin II contractility accompanies the metaphase-anaphase transition in sea urchin eggs. Mol. Biol. Cell 2006, 17:4093-4104.
47. Chew T.L., et al. A fluorescent resonant energy transfer-based biosensor reveals transient and regional myosin light chain kinase activation in lamella and cleavage furrows. J. Cell Biol. 2002, 156:543-553.
48. Loo T.H., Balasubramanian M. Schizosaccharomyces pombe Pak-related protein Pak1p/Orb2p, phosphorylates myosin regulatory light chain to inhibit cytokinesis. J. Cell Biol. 2008, 183:785-793.
49. Bosgraaf L., van Haastert P.J. The regulation of myosin II in Dictyostelium. Eur. J. Cell Biol. 2006, 85:969-979.
50. Sladewski T.E., et al. Regulation of fission yeast myosin-II function and contractile ring dynamics by regulatory light-chain and heavy-chain phosphorylation. Mol. Biol. Cell 2009, 20:3941-3952.
51. Saurin A.T., et al. The regulated assembly of a PKCepsilon complex controls the completion of cytokinesis. Nat. Cell Biol. 2008, 10:891-901.
52. Echard A. Membrane traffic and polarization of lipid domains during cytokinesis. Biochem. Soc. Trans. 2008, 36:395-399.
53. Emoto K., et al. Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis. J. Biol. Chem. 2005, 280:37901-37907.
54. Field S.J., et al. PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr. Biol. 2005, 15:1407-1412.
55. Kouranti I., et al. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr. Biol. 2006, 16:1719-1725.
56. Janetopoulos C., et al. Temporal and spatial regulation of phosphoinositide signaling mediates cytokinesis. Dev. Cell 2005, 8:467-477.
57. Wilson G.M., et al. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol. Biol. Cell 2005, 16:849-860.
58. Fielding A.B., et al. Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J. 2005, 24:3389-3399.
59. Polevoy G., et al. Dual roles for the Drosophila PI 4-kinase four wheel drive in localizing Rab11 during cytokinesis. J. Cell Biol. 2009, 187:847-858.
60. Sagona A.P., et al. PtdIns(3)P controls cytokinesis through KIF13A-mediated recruitment of FYVE-CENT to the midbody. Nat. Cell Biol. 2010, 12:362-371.
61. Hanson P.I., et al. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J. Cell Biol. 2008, 180:389-402.
62. Yakir-Tamang L., Gerst J.E. A phosphatidylinositol-transfer protein and phosphatidylinositol-4-phosphate 5-kinase control Cdc42 to regulate the actin cytoskeleton and secretory pathway in yeast. Mol. Biol. Cell 2009, 20:3583-3597.
63. Mendoza M., et al. A mechanism for chromosome segregation sensing by the NoCut checkpoint. Nat. Cell Biol. 2009, 11:477-483.
64. Norden C., et al. The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 2006, 125:85-98.
65. Steigemann P., et al. Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 2009, 136:473-484.
66. Pereira G., Schiebel E. Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14. Science 2003, 302:2120-2124.
67. Hummer S., Mayer T.U. Cdk1 negatively regulates midzone localization of the mitotic kinesin Mklp2 and the chromosomal passenger complex. Curr. Biol. 2009, 19:607-612.
68. Fuller B.G., et al. Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature 2008, 453:1132-1136.
69. Sumara I., et al. A Cul3-based E3 ligase removes Aurora B from mitotic chromosomes, regulating mitotic progression and completion of cytokinesis in human cells. Dev. Cell 2007, 12:887-900.
70. Maerki S., et al. The Cul3-KLHL21 E3 ubiquitin ligase targets aurora B to midzone microtubules in anaphase and is required for cytokinesis. J. Cell Biol. 2009, 187:791-800.
71. Floyd S., et al. APC/C Cdh1 targets aurora kinase to control reorganization of the mitotic spindle at anaphase. Curr. Biol. 2008, 18:1649-1658.
72. Wu J.Q., Pollard T.D. Counting cytokinesis proteins globally and locally in fission yeast. Science 2005, 310:310-314.
73. Carvalho A., et al. Structural memory in the contractile ring makes the duration of cytokinesis independent of cell size. Cell 2009, 137:926-937.
74. Tully G.H., et al. The anaphase-promoting complex promotes actomyosin-ring disassembly during cytokinesis in yeast. Mol. Biol. Cell 2009, 20:1201-1212.
75. Blondel M., et al. Degradation of Hof1 by SCF(Grr1) is important for actomyosin contraction during cytokinesis in yeast. EMBO J. 2005, 24:1440-1452.
76. Albuquerque C.P., et al. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol. Cell Proteomics 2008, 7:1389-1396.
77. Zhao W.M., Fang G. Anillin is a substrate of anaphase-promoting complex/cyclosome (APC/C) that controls spatial contractility of myosin during late cytokinesis. J. Biol. Chem. 2005, 280:33516-33524.
78. Tasto J.J., et al. An anillin homologue Mid2p, acts during fission yeast cytokinesis to organize the septin ring and promote cell separation. J. Cell Biol. 2003, 160:1093-1103.
79. Watanabe S., et al. mDia2 induces the actin scaffold for the contractile ring and stabilizes its position during cytokinesis in NIH 3T3 cells. Mol. Biol. Cell 2008, 19:2328-2338.
80. DeWard A.D., Alberts A.S. Ubiquitin-mediated degradation of the formin mDia2 upon completion of cell division. J. Biol. Chem. 2009, 284:20061-20069.
81. Johnson A.E., Gould K.L. Dma1 ubiquitinates the SIN scaffold Sid4, to impede the mitotic localization of Plo1 kinase. EMBO J. 2011, 30:341-354.
82. Scolnick D.M., Halazonetis T.D. Chfr defines a mitotic stress checkpoint that delays entry into metaphase. Nature 2000, 406:430-435.
83. Tuttle R.L., et al. Defective in mitotic arrest 1/ring finger 8 is a checkpoint protein that antagonizes the human mitotic exit network. Mol. Cancer Res. 2007, 5:1304-1311.
84. Pohl C., Jentsch S. Final stages of cytokinesis and midbody ring formation are controlled by BRUCE. Cell 2008, 132:832-845.
85. Carlton J.G., Martin-Serrano J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 2007, 316:1908-1912.
86. Pohl C., Jentsch S. Midbody ring disposal by autophagy is a post-abscission event of cytokinesis. Nat. Cell Biol. 2009, 11:65-70.
87. Wang H., et al. The terminal phase of cytokinesis in the Caenorhabditis elegans early embryo requires protein glycosylation. Mol. Biol. Cell 2005, 16:4202-4213.
88. Zhang L., Ten Hagen K.G. Dissecting the biological role of mucin-type O-glycosylation using RNA interference in Drosophila cell culture. J. Biol. Chem. 2010, 285:34477-34484.
89. Slawson C., et al. Perturbations in O-linked beta-N-acetylglucosamine protein modification cause severe defects in mitotic progression and cytokinesis. J. Biol. Chem. 2005, 280:32944-32956.
90. Wang Z., et al. Extensive crosstalk between O-GlcNAcylation and phosphorylation regulates cytokinesis. Sci. Signal. 2010, 3:ra2.
91. Johnson E.S., Blobel G. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 1999, 147:981-994.
92. Makhnevych T., et al. The role of karyopherins in the regulated sumoylation of septins. J. Cell Biol. 2007, 177:39-49.
93. Klein U.R., et al. RanBP2 and SENP3 function in a mitotic SUMO2/3 conjugation-deconjugation cycle on Borealin. Mol. Biol. Cell 2009, 20:410-418.
94. Fernandez-Miranda G., et al. SUMOylation modulates the function of Aurora-B kinase. J. Cell Sci. 2010, 123:2823-2833.
95. Montpetit B., et al. Sumoylation of the budding yeast kinetochore protein Ndc10 is required for Ndc10 spindle localization and regulation of anaphase spindle elongation. J. Cell Biol. 2006, 174:653-663.
96. Shen Q., et al. NAT10, a nucleolar protein, localizes to the midbody and regulates cytokinesis and acetylation of microtubules. Exp. Cell Res. 2009, 315:1653-1667.
97. Zhou C., et al. Arl2 and Arl3 regulate different microtubule-dependent processes. Mol. Biol. Cell 2006, 17:2476-2487.
98. Wickstrom S.A., et al. CYLD negatively regulates cell-cycle progression by inactivating HDAC6 and increasing the levels of acetylated tubulin. EMBO J. 2010, 29:131-144.
99. Kraft C., et al. Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J. 2003, 22:6598-6609.
100. Lindon C., Pines J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J. Cell Biol. 2004, 164:233-241.
101. Chia W., et al. Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J. Cell Biol. 2008, 180:267-272.
102. Wirtz-Peitz F., et al. Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 2008, 135:161-173.
103. Atwood S.X., Prehoda K.E. aPKC phosphorylates Miranda to polarize fate determinants during neuroblast asymmetric cell division. Curr. Biol. 2009, 19:723-729.
104. Johnston C.A., et al. Identification of an Aurora-A/PinsLINKER/Dlg spindle orientation pathway using induced cell polarity in S2 cells. Cell 2009, 138:1150-1163.
105. Hao Y., et al. Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical pins. Curr. Biol. 2010, 20:1809-1818.
106. Cabernard C., et al. A spindle-independent cleavage furrow positioning pathway. Nature 2010, 467:91-94.
107. Ou G., et al. Polarized myosin produces unequal-size daughters during asymmetric cell division. Science 2010, 330:677-680.
108. Ang X.L., Wade Harper J. SCF-mediated protein degradation and cell cycle control. Oncogene 2005, 24:2860-2870.
109. Wilson-Grady J.T., et al. Phosphoproteome analysis of fission yeast. J. Proteome Res. 2008, 7:1088-1097.
110. Gnad, F. et al. (2011) PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res. 39, D253-260.