Rho GTPases as regulators of mitosis and cytokinesis in mammalian cells

Small GTPases

Volumn 5, Issue JUL, 2014, Pages

  Chircop, Megan ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Abscission; Actin; Cdc42; Cleavage furrow; Cytokinesis; Cytoskeleton; Metaphase; Microtubules; RhoA; Spindle assembly

Indexed keywords

CENTROMERE PROTEIN A; MYOSIN LIGHT CHAIN; P21 ACTIVATED KINASE 1; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

CELL CYCLE PROGRESSION; CELL STRUCTURE; CYTOKINESIS; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; MAMMAL CELL; MEMBRANE ABSCISSION; MEMBRANE BIOLOGY; MEMBRANE INGRESSION; METAPHASE; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; NONHUMAN; PROMETAPHASE; PROPHASE; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; ACTIN FILAMENT; ANIMAL; CENTROMERE; CHROMOSOME; METABOLISM; MITOSIS; PHYSIOLOGY; SPINDLE APPARATUS;

ACTIN CYTOSKELETON; ANIMALS; CDC42 GTP-BINDING PROTEIN; CHROMOSOMES; CYTOKINESIS; HUMANS; KINETOCHORES; MICROTUBULES; MITOSIS; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SPINDLE APPARATUS;

EID: 84922227318     PISSN: 21541248     EISSN: 21541256     Source Type: Journal    
DOI: 10.4161/sgtp.29770     Document Type: Review

References (160)

1. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629-35; PMID:12478284; http://dx.doi.org/10.1038/nature01148
2. Dransart E, Olofsson B, Cherfils J.RhoGDIs revisited: novel roles in Rho regulation. Traffic 2005; 6:957-66; PMID:16190977; http://dx.doi.org/10.1111/j.1600-0854.2005.00335.x
3. Oceguera-Yanez F, Kimura K, Yasuda S, Higashida C, Kitamura T, Hiraoka Y, Haraguchi T, Narumiya S. Ect2 and MgcRacGAP regulate the activation and function of Cdc42 in mitosis. J Cell Biol 2005; 168:221-32; PMID:15642749; http://dx.doi.org/10.1083/jcb.200408085
4. Yasuda S, Oceguera-Yanez F, Kato T, Okamoto M, Yonemura S, Terada Y, Ishizaki T, Narumiya S. Cdc42 and mDia3 regulate microtubule attachment to kinetochores. Nature 2004; 428:767-71; PMID:15085137; http://dx.doi.org/10.1038/nature02452
5. Jordan SN, Canman JC.Rho GTPases in animal cell cytokinesis: an occupation by the one percent. Cytoskeleton (Hoboken) 2012; 69:919-30; PMID:23047851; http://dx.doi.org/10.1002/cm.21071
6. Hirose K, Kawashima T, Iwamoto I, Nosaka T, Kitamura T. MgcRacGAP is involved in cytokinesis through associating with mitotic spindle and midbody. J Biol Chem 2001; 276:5821-8; PMID:11085985; http://dx.doi.org/10.1074/jbc.M007252200
7. Seguin L, Liot C, Mzali R, Harada R, Siret A, Nepveu A, Bertoglio J.CUX1 and E2F1 regulate coordinated expression of the mitotic complex genes Ect2, MgcRacGAP, and MKLP1 in S phase. Mol Cell Biol 2009; 29:570-81; PMID:19015243; http://dx.doi.org/10.1128/MCB.01275-08
8. Su L, Agati JM, Parsons SJ.p190RhoGAP is cell cycle regulated and affects cytokinesis. J Cell Biol 2003; 163:571-82; PMID:14610059; http://dx.doi.org/10.1083/jcb.200308007
9. Jiang YS, Maeda M, Okamoto M, Fujii M, Fukutomi R, Hori M, Tatsuka M, Ota T. Centrosomal localization of RhoGDIβ and its relevance to mitotic processes in cancer cells. Int J Oncol 2013; 42:460-8; PMID:23232495
10. Dao VT, Dupuy AG, Gavet O, Caron E, de Gunzburg J.Dynamic changes in Rap1 activity are required for cell retraction and spreading during mitosis. J Cell Sci 2009; 122:2996-3004; PMID:19638416; http://dx.doi.org/10.1242/jcs.041301
11. Kunda P, Pelling AE, Liu T, Baum B. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr Biol 2008; 18:91-101; PMID:18207738; http://dx.doi.org/10.1016/j.cub.2007.12.051
12. Matthews HK, Delabre U, Rohn JL, Guck J, Kunda P, Baum B. Changes in Ect2 localization couple actomyosin-dependent cell shape changes to mitotic progression. Dev Cell 2012; 23:371-83; PMID:22898780; http://dx.doi.org/10.1016/j.devcel.2012.06.003
13. Maddox AS, Burridge K. RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J Cell Biol 2003; 160:255-65; PMID:12538643; http://dx.doi.org/10.1083/jcb.200207130
14. Mali P, Wirtz D, Searson PC.Interplay of RhoA and motility in the programmed spreading of daughter cells postmitosis. Biophys J 2010; 99:3526-34; PMID:21112276; http://dx.doi.org/10.1016/j.bpj.2010.10.006
15. Gavet O, Pines J.Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev Cell 2010; 18:533-43; PMID:20412769; http://dx.doi.org/10.1016/j.devcel.2010.02.013
16. Hara T, Abe M, Inoue H, Yu LR, Veenstra TD, Kang YH, Lee KS, Miki T. Cytokinesis regulator ECT2 changes its conformation through phosphorylation at Thr-341 in G2/M phase. Oncogene 2006; 25:566-78; PMID:16170345
17. Niiya F, Tatsumoto T, Lee KS, Miki T. Phosphorylation of the cytokinesis regulator ECT2 at G2/M phase stimulates association of the mitotic kinase Plk1 and accumulation of GTP-bound RhoA. Oncogene 2006; 25:827-37; PMID:16247472; http://dx.doi.org/10.1038/sj.onc.1209124
18. Chalamalasetty RB, Hümmer S, Nigg EA, Silljé HH. Influence of human Ect2 depletion and overexpression on cleavage furrow formation and abscission. J Cell Sci 2006; 119:3008-19; PMID:16803869; http://dx.doi.org/10.1242/jcs.03032
19. Kamijo K, Ohara N, Abe M, Uchimura T, Hosoya H, Lee JS, Miki T. Dissecting the role of Rho-mediated signaling in contractile ring formation. Mol Biol Cell 2006; 17:43-55; PMID:16236794; http://dx.doi.org/10.1091/mbc.E05-06-0569
20. Kim JE, Billadeau DD, Chen J.The tandem BRCT domains of Ect2 are required for both negative and positive regulation of Ect2 in cytokinesis. J Biol Chem 2005; 280:5733-9; PMID:15545273; http://dx.doi.org/10.1074/jbc.M409298200
21. Tatsumoto T, Xie X, Blumenthal R, Okamoto I, Miki T. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J Cell Biol 1999; 147:921-8; PMID:10579713; http://dx.doi.org/10.1083/jcb.147.5.921
22. Yüce O, Piekny A, Glotzer M. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 2005; 170:571-82; PMID:16103226; http://dx.doi.org/10.1083/jcb.200501097
23. Saito S, Liu XF, Kamijo K, Raziuddin R, Tatsumoto T, Okamoto I, Chen X, Lee CC, Lorenzi MV, Ohara N, et al. Deregulation and mislocalization of the cytokinesis regulator ECT2 activate the Rho signaling pathways leading to malignant transformation. J Biol Chem 2004; 279:7169-79; PMID:14645260; http://dx.doi.org/10.1074/jbc.M306725200
24. Frenette P, Haines E, Loloyan M, Kinal M, Pakarian P, Piekny A. An anillin-Ect2 complex stabilizes central spindle microtubules at the cortex during cytokinesis. PLoS One 2012; 7:e34888; PMID:22514687; urlhttp://dx.doi.org/10.1371/journal.pone.0034888
25. Su KC, Takaki T, Petronczki M. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev Cell 2011; 21:1104-15; PMID:22172673; http://dx.doi.org/10.1016/j.devcel.2011.11.003
26. Helmke KJ, Heald R, Wilbur JD. Interplay between spindle architecture and function. Int Rev Cell Mol Biol 2013; 306:83-125; PMID:24016524; http://dx.doi.org/10.1016/B978-0-12-407694-5.00003-1
27. Rieder CL. Kinetochore fiber formation in animal somatic cells: dueling mechanisms come to a draw. Chromosoma 2005; 114:310-8; PMID:16270218; http://dx.doi.org/10.1007/s00412-005-0028-2
28. Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 2007; 8:379-93; PMID:17426725; http://dx.doi.org/10.1038/nrm2163
29. Rodriguez-Fraticelli AE, Vergarajauregui S, Eastburn DJ, Datta A, Alonso MA, Mostov K, Martín-Belmonte F. The Cdc42 GEF Intersectin 2 controls mitotic spindle orientation to form the lumen during epithelial morphogenesis. J Cell Biol 2010; 189:725-38; PMID:20479469; http://dx.doi.org/10.1083/jcb.201002047
30. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005; 21:247-69; PMID:16212495; http://dx.doi.org/10.1146/annurev.cellbio.21.020604.150721
31. Jaffe AB, Kaji N, Durgan J, Hall A. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J Cell Biol 2008; 183:625-33; PMID:19001128; http://dx.doi.org/10.1083/jcb.200807121
32. Kotak S, Gönczy P. Mechanisms of spindle positioning: cortical force generators in the limelight. Curr Opin Cell Biol 2013; 25:741-8; PMID:23958212; http://dx.doi.org/10.1016/j.ceb.2013.07.008
33. Sütterlin C, Colanzi A. The Golgi and the centrosome: building a functional partnership. J Cell Biol 2010; 188:621-8; PMID:20212314; http://dx.doi.org/10.1083/jcb.200910001
34. Sütterlin C, Polishchuk R, Pecot M, Malhotra V. The Golgi-associated protein GRASP65 regulates spindle dynamics and is essential for cell division. Mol Biol Cell 2005; 16:3211-22; PMID:15888544; http://dx.doi.org/10.1091/mbc.E04-12-1065
35. Kodani A, Sütterlin C.The Golgi protein GM130 regulates centrosome morphology and function. Mol Biol Cell 2008; 19:745-53; PMID:18045989; http://dx.doi.org/10.1091/mbc.E07-08-0847
36. Kodani A, Kristensen I, Huang L, Sütterlin C.GM130-dependent control of Cdc42 activity at the Golgi regulates centrosome organization. Mol Biol Cell 2009; 20:1192-200; PMID:19109421; http://dx.doi.org/10.1091/mbc.E08-08-0834
37. Ban R, Irino Y, Fukami K, Tanaka H. Human mitotic spindle-associated protein PRC1 inhibits MgcRacGAP activity toward Cdc42 during the metaphase. J Biol Chem 2004; 279:16394-402; PMID:14744859; http://dx.doi.org/10.1074/jbc.M313257200
38. Gundersen GG. Evolutionary conservation of microtubule-capture mechanisms. Nat Rev Mol Cell Biol 2002; 3:296-304; PMID:11994749; http://dx.doi.org/10.1038/nrm777
39. Bader JR, Vaughan KT. Dynein at the kinetochore: Timing, Interactions and Functions. Semin Cell Dev Biol 2010; 21:269-75; PMID:20045078; http://dx.doi.org/10.1016/j.semcdb.2009.12.015
40. Lin SL, Qi ST, Sun SC, Wang YP, Schatten H, Sun QY. PAK1 regulates spindle microtubule organization during oocyte meiotic maturation. Front Biosci. (Elite.Ed) 2010; 2:1254-1264.
41. Maroto B, Ye MB, von Lohneysen K, Schnelzer A, Knaus UG. P21-activated kinase is required for mitotic progression and regulates Plk1. Oncogene 2008; 27:4900-8; PMID:18427546; http://dx.doi.org/10.1038/onc.2008.131
42. Lagana A, Dorn JF, De Rop V, Ladouceur AM, Maddox AS, Maddox PS. A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A. Nat Cell Biol 2010; 12:1186-93; PMID:21102442; http://dx.doi.org/10.1038/ncb2129
43. Glotzer M. The molecular requirements for cytokinesis. Science 2005; 307:1735-9; PMID:15774750; http://dx.doi.org/10.1126/science.1096896
44. rd, Meyer BJ, Heald R. Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 2004; 305:61-6; PMID:15166316; http://dx.doi.org/10.1126/science.1097931
45. Julian M, Tollon Y, Lajoie-Mazenc I, Moisand A, Mazarguil H, Puget A, Wright M. gamma-Tubulin participates in the formation of the midbody during cytokinesis in mammalian cells. J Cell Sci 1993; 105:145-56; PMID:8360269
46. Gromley A, Jurczyk A, Sillibourne J, Halilovic E, Mogensen M, Groisman I, Blomberg M, Doxsey S. A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase. J Cell Biol 2003; 161:535-45; PMID:12732615; http://dx.doi.org/10.1083/jcb.200301105
47. Gromley A, Yeaman C, Rosa J, Redick S, Chen CT, Mirabelle S, Guha M, Sillibourne J, Doxsey SJ.Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 2005; 123:75-87; PMID:16213214; http://dx.doi.org/10.1016/j.cell.2005.07.027
48. Lordier L, Jalil A, Aurade F, Larbret F, Larghero J, Debili N, Vainchenker W, Chang Y. Megakaryocyte endomitosis is a failure of late cytokinesis related to defects in the contractile ring and Rho/Rock signaling. Blood 2008; 112:3164-74; PMID:18684864; http://dx.doi.org/10.1182/blood-2008-03-144956
49. Gao Y, Smith E, Ker E, Campbell P, Cheng EC, Zou S, Lin S, Wang L, Halene S, Krause DS. Role of RhoA-specific guanine exchange factors in regulation of endomitosis in megakaryocytes. Dev Cell 2012; 22:573-84; PMID:22387001; http://dx.doi.org/10.1016/j.devcel.2011.12.019
50. Burgess DR, Chang F. Site selection for the cleavage furrow at cytokinesis. Trends Cell Biol 2005; 15:156-62; PMID:15752979; http://dx.doi.org/10.1016/j.tcb.2005.01.006
51. Glotzer M. Cleavage furrow positioning. J Cell Biol 2004; 164:347-51; PMID:14757750; http://dx.doi.org/10.1083/jcb.200310112
52. Danowski BA. Fibroblast contractility and actin organization are stimulated by microtubule inhibitors. J Cell Sci 1989; 93:255-66; PMID:2482296
53. Pletjushkina OJ, Rajfur Z, Pomorski P, Oliver TN, Vasiliev JM, Jacobson KA. Induction of cortical oscillations in spreading cells by depolymerization of microtubules. Cell Motil Cytoskeleton 2001; 48:235-44; PMID:11276073; http://dx.doi.org/10.1002/cm.1012
54. Ren XD, Kiosses WB, Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 1999; 18:578-85; PMID:9927417; http://dx.doi.org/10.1093/emboj/18.3.578
55. Canman JC, Bement WM. Microtubules suppress actomyosin-based cortical flow in Xenopus oocytes. J Cell Sci 1997; 110:1907-17; PMID:9296390
56. Werner M, Munro E, Glotzer M. Astral signals spatially bias cortical myosin recruitment to break symmetry and promote cytokinesis. Curr Biol 2007; 17:1286-97; PMID:17669650; http://dx.doi.org/10.1016/j.cub.2007.06.070
57. Canman JC, Cameron LA, Maddox PS, Straight A, Tirnauer JS, Mitchison TJ, Fang G, Kapoor TM, Salmon ED. Determining the position of the cell division plane. Nature 2003; 424:1074-8; PMID:12904818; http://dx.doi.org/10.1038/nature01860
58. Rappaport R. Establishment of the mechanism of cytokinesis in animal cells. Int Rev Cytol 1986; 105:245-81; PMID:3539854; http://dx.doi.org/10.1016/S0074-7696(08)61065-7
59. Bringmann H, Hyman AA. A cytokinesis furrow is positioned by two consecutive signals. Nature 2005; 436:731-4; PMID:16079852; http://dx.doi.org/10.1038/nature03823
60. Dechant R, Glotzer M. Centrosome separation and central spindle assembly act in redundant pathways that regulate microtubule density and trigger cleavage furrow formation. Dev Cell 2003; 4:333-44; PMID:12636915; http://dx.doi.org/10.1016/S1534-5807(03)00057-1
61. Drechsel DN, Hyman AA, Hall A, Glotzer M. A requirement for Rho and Cdc42 during cytokinesis in Xenopus embryos. Curr Biol 1997; 7:12-23; PMID:8999996; http://dx.doi.org/10.1016/S0960-9822(06)00023-6
62. Jantsch-Plunger V, Gönczy P, Romano A, Schnabel H, Hamill D, Schnabel R, Hyman AA, Glotzer M. CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis. J Cell Biol 2000; 149:1391-404; PMID:10871280; http://dx.doi.org/10.1083/jcb.149.7.1391
63. Kishi K, Sasaki T, Kuroda S, Itoh T, Takai Y. Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI). J Cell Biol 1993; 120:1187-95; PMID:8436590; http://dx.doi.org/10.1083/jcb.120.5.1187
64. Piekny A, Werner M, Glotzer M. Cytokinesis: welcome to the Rho zone. Trends Cell Biol 2005; 15:651-8; PMID:16243528; http://dx.doi.org/10.1016/j.tcb.2005.10.006
65. Bement WM, Benink HA, von Dassow G. A microtubule-dependent zone of active RhoA during cleavage plane specification. J Cell Biol 2005; 170:91-101; PMID:15998801; http://dx.doi.org/10.1083/jcb.200501131
66. Nishimura Y, Yonemura S. Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J Cell Sci 2006; 119:104-14; PMID:16352658; http://dx.doi.org/10.1242/jcs.02737
67. Yonemura S, Hirao-Minakuchi K, Nishimura Y. Rho localization in cells and tissues. Exp Cell Res 2004; 295:300-14; PMID:15093731; http://dx.doi.org/10.1016/j.yexcr.2004.01.005
68. Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T, Mochizuki N, Nagashima K, Matsuda M. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J Cell Biol 2003; 162:223-32; PMID:12860967; http://dx.doi.org/10.1083/jcb.200212049
69. Mishima M, Kaitna S, Glotzer M. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2002; 2:41-54; PMID:11782313; http://dx.doi.org/10.1016/S1534-5807(01)00110-1
70. Somers WG, Saint R. A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev Cell 2003; 4:29-39; PMID:12530961; http://dx.doi.org/10.1016/S1534-5807(02)00402-1
71. Matuliene J, Kuriyama R. Role of the midbody matrix in cytokinesis: RNAi and genetic rescue analysis of the mammalian motor protein CHO1. Mol Biol Cell 2004; 15:3083-94; PMID:15075367; http://dx.doi.org/10.1091/mbc.E03-12-0888
72. Mollinari C, Kleman JP, Jiang W, Schoehn G, Hunter T, Margolis RL. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J Cell Biol 2002; 157:1175-86; PMID:12082078; http://dx.doi.org/10.1083/jcb.200111052
73. Lekomtsev S, Su KC, Pye VE, Blight K, Sundaramoorthy S, Takaki T, Collinson LM, Cherepanov P, Divecha N, Petronczki M. Centralspindlin links the mitotic spindle to the plasma membrane during cytokinesis. Nature 2012; 492:276-9; PMID:23235882; http://dx.doi.org/10.1038/nature11773
74. Birkenfeld J, Nalbant P, Bohl BP, Pertz O, Hahn KM, Bokoch GM. GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev Cell 2007; 12:699-712; PMID:17488622; http://dx.doi.org/10.1016/j.devcel.2007.03.014
75. Asiedu M, Wu D, Matsumura F, Wei Q. Centrosome/spindle pole-associated protein regulates cytokinesis via promoting the recruitment of MyoGEF to the central spindle. Mol Biol Cell 2009; 20:1428-40; PMID:19129481; http://dx.doi.org/10.1091/mbc.E08-01-0001
76. Asiedu M, Wu D, Matsumura F, Wei Q. Phosphorylation of MyoGEF on Thr-574 by Plk1 promotes MyoGEF localization to the central spindle. J Biol Chem 2008; 283:28392-400; PMID:18694934; http://dx.doi.org/10.1074/jbc.M801801200
77. Wu D, Asiedu M, Adelstein RS, Wei Q. A novel guanine nucleotide exchange factor MyoGEF is required for cytokinesis. Cell Cycle 2006; 5:1234-9; PMID:16721066; http://dx.doi.org/10.4161/cc.5.11.2815
78. Loria A, Longhini KM, Glotzer M. The RhoGAP domain of CYK-4 has an essential role in RhoA activation. Curr Biol 2012; 22:213-9; PMID:22226748; http://dx.doi.org/10.1016/j.cub.2011.12.019
79. Miller AL, Bement WM. Regulation of cytokinesis by Rho GTPase flux. Nat Cell Biol 2009; 11:71-7 PMID:19060892; http://dx.doi.org/10.1038/ncb1814
80. Burkard ME, Maciejowski J, Rodriguez-Bravo V, Repka M, Lowery DM, Clauser KR, Zhang C, Shokat KM, Carr SA, Yaffe MB, 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; PMID:19468302; urlhttp://dx.doi.org/10.1371/journal.pbio.1000111
81. Wolfe BA, Takaki T, Petronczki M, Glotzer M. Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol 2009; 7:e1000110; PMID:19468300; http://dx.doi.org/10.1371/journal.pbio.1000110
82. Touré A, Dorseuil O, Morin L, Timmons P, Jégou B, Reibel L, Gacon G. 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 1998; 273:6019-23; PMID:9497316; http://dx.doi.org/10.1074/jbc.273.11.6019
83. D'Avino PP, Savoian MS, Glover DM. Mutations in sticky lead to defective organization of the contractile ring during cytokinesis and are enhanced by Rho and suppressed by Rac.J Cell Biol 2004; 166:61-71; PMID:15240570; http://dx.doi.org/10.1083/jcb.200402157
84. Bastos RN, Penate X, Bates M, Hammond D, Barr FA. CYK4 inhibits Rac1-dependent PAK1 and ARHGEF7 effector pathways during cytokinesis. J Cell Biol 2012; 198:865-80; PMID:22945935; http://dx.doi.org/10.1083/jcb.201204107
85. Zanin E, Desai A, Poser I, Toyoda Y, Andree C, Moebius C, Bickle M, Conradt B, Piekny A, Oegema K. A conserved RhoGAP limits M phase contractility and coordinates with microtubule asters to confine RhoA during cytokinesis. Dev Cell 2013; 26:496-510; PMID:24012485; http://dx.doi.org/10.1016/j.devcel.2013.08.005
86. Maupin P, Pollard TD. 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 1986; 94:92-103; PMID:3772181; http://dx.doi.org/10.1016/0889-1605(86)90055-8
87. Ikebe M, Koretz J, Hartshorne DJ.Effects of phosphorylation of light chain residues threonine 18 and serine 19 on the properties and conformation of smooth muscle myosin. J Biol Chem 1988; 263:6432-7; PMID:2966156
88. Komatsu S, Yano T, Shibata M, Tuft RA, Ikebe M. Effects of the regulatory light chain phosphorylation of myosin II on mitosis and cytokinesis of mammalian cells. J Biol Chem 2000; 275:34512-20; PMID:10944522; http://dx.doi.org/10.1074/jbc.M003019200
89. Yamakita Y, Yamashiro S, Matsumura F. In vivo phosphorylation of regulatory light chain of myosin II during mitosis of cultured cells. J Cell Biol 1994; 124:129-37; PMID:8294496; http://dx.doi.org/10.1083/jcb.124.1.129
90. Scholey JM, Taylor KA, Kendrick-Jones J.Regulation of non-muscle myosin assembly by calmodulin-dependent light chain kinase. Nature 1980; 287:233-5; PMID:6893621; http://dx.doi.org/10.1038/287233a0
91. Field CM, al-Awar O, Rosenblatt J, Wong ML, Alberts B, Mitchison TJ.A purified Drosophila septin complex forms filaments and exhibits GTPase activity. J Cell Biol 1996; 133:605-16; PMID:8636235; http://dx.doi.org/10.1083/jcb.133.3.605
92. Kinoshita M, Kumar S, Mizoguchi A, Ide C, Kinoshita A, Haraguchi T, Hiraoka Y, Noda M. Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes Dev 1997; 11:1535-47; PMID:9203580; http://dx.doi.org/10.1101/gad.11.12.1535
93. Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ.Self-and actin-templated assembly of Mammalian septins. Dev Cell 2002; 3:791-802; PMID:12479805; http://dx.doi.org/10.1016/S1534-5807(02)00366-0
94. Nagata K, Kawajiri A, Matsui S, Takagishi M, Shiromizu T, Saitoh N, Izawa I, Kiyono T, Itoh TJ, Hotani H, et al. Filament formation of MSF-A, a mammalian septin, in human mammary epithelial cells depends on interactions with microtubules. J Biol Chem 2003; 278:18538-43; PMID:12626509; http://dx.doi.org/10.1074/jbc.M205246200
95. Surka MC, Tsang CW, Trimble WS. The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis. Mol Biol Cell 2002; 13:3532-45; PMID:12388755; http://dx.doi.org/10.1091/mbc.E02-01-0042
96. Xie H, Surka M, Howard J, Trimble WS. Characterization of the mammalian septin H5: distinct patterns of cytoskeletal and membrane association from other septin proteins. Cell Motil Cytoskeleton 1999; 43:52-62; PMID:10340703; http://dx.doi.org/10.1002/(SICI)1097-0169(1999)43:152::AID-CM63.0.CO;2-5
97. Zhang J, Kong C, Xie H, McPherson PS, Grinstein S, Trimble WS. Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr Biol 1999; 9:1458-67; PMID:10607590; http://dx.doi.org/10.1016/S0960-9822(00)80115-3
98. Neufeld TP, Rubin GM. The Drosophila peanut gene is required for cytokinesis and encodes a protein similar to yeast putative bud neck filament proteins. Cell 1994; 77:371-9; PMID:8181057; http://dx.doi.org/10.1016/0092-8674(94)90152-X
99. Nguyen TQ, Sawa H, Okano H, White JG. The C.elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis. J Cell Sci 2000; 113:3825-37; PMID:11034910
100. Kinoshita M. The septins. Genome Biol 2003; 4:236; PMID:14611653; http://dx.doi.org/10.1186/gb-2003-4-11-236
101. Oegema K, Savoian MS, Mitchison TJ, Field CM. Functional analysis of a human homologue of the Drosophila actin binding protein anillin suggests a role in cytokinesis. J Cell Biol 2000; 150:539-52; PMID:10931866; http://dx.doi.org/10.1083/jcb.150.3.539
102. El Amine N, Kechad A, Jananji S, Hickson GR. Opposing actions of septins and Sticky on Anillin promote the transition from contractile to midbody ring. J Cell Biol 2013; 203:487-504; PMID:24217622; http://dx.doi.org/10.1083/jcb.201305053
103. Kechad A, Jananji S, Ruella Y, Hickson GR. Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr Biol 2012; 22:197-203; PMID:22226749; http://dx.doi.org/10.1016/j.cub.2011.11.062
104. Dobbelaere J, Barral Y. Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 2004; 305:393-6; PMID:15256669; http://dx.doi.org/10.1126/science.1099892
105. Schmidt K, Nichols BJ.A barrier to lateral diffusion in the cleavage furrow of dividing mammalian cells. Curr Biol 2004; 14:1002-6; PMID:15182674; http://dx.doi.org/10.1016/j.cub.2004.05.044
106. Li F, Higgs HN. The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 2003; 13:1335-40; PMID:12906795; http://dx.doi.org/10.1016/S0960-9822(03)00540-2
107. Alberts AS. Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J Biol Chem 2001; 276:2824-30; PMID:11035012; http://dx.doi.org/10.1074/jbc.M006205200
108. Otomo T, Otomo C, Tomchick DR, Machius M, Rosen MK. Structural basis of Rho GTPase-mediated activation of the formin mDia1. Mol Cell 2005; 18:273-81; PMID:15866170; http://dx.doi.org/10.1016/j.molcel.2005.04.002
109. Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, Wittinghofer A. Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 2005; 435:513-8; PMID:15864301; http://dx.doi.org/10.1038/nature03604
110. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 1997; 16:3044-56; PMID:9214622; http://dx.doi.org/10.1093/emboj/16.11.3044
111. Tominaga T, Sahai E, Chardin P, McCormick F, Courtneidge SA, Alberts AS. Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell 2000; 5:13-25; PMID:10678165; http://dx.doi.org/10.1016/S1097-2765(00)80399-8
112. Kasahara K, Nakayama Y, Nakazato Y, Ikeda K, Kuga T, Yamaguchi N. Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J Biol Chem 2007; 282:5327-39; PMID:17189253; http://dx.doi.org/10.1074/jbc.M608396200
113. Guha M, Zhou M, Wang YL. Cortical actin turnover during cytokinesis requires myosin II. Curr Biol 2005; 15:732-6; PMID:15854905; http://dx.doi.org/10.1016/j.cub.2005.03.042
114. Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, Sellers JR, Mitchison TJ.Dissecting temporal and spatial control of cytokinesis with a myosin II Inhibitor. Science 2003; 299:1743-7; PMID:12637748; http://dx.doi.org/10.1126/science.1081412
115. Zang JH, Spudich JA. Myosin II localization during cytokinesis occurs by a mechanism that does not require its motor domain. Proc Natl Acad Sci U S A 1998; 95:13652-7; PMID:9811855; http://dx.doi.org/10.1073/pnas.95.23.13652
116. Dean SO, Rogers SL, Stuurman N, Vale RD, Spudich JA. Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis. Proc Natl Acad Sci U S A 2005; 102:13473-8; PMID:16174742; http://dx.doi.org/10.1073/pnas.0506810102
117. Dean SO, Spudich JA. Rho kinase's role in myosin recruitment to the equatorial cortex of mitotic Drosophila S2 cells is for myosin regulatory light chain phosphorylation. PLoS One 2006; 1:e131; PMID:17205135; http://dx.doi.org/10.1371/journal.pone.0000131
118. Madaule P, Eda M, Watanabe N, Fujisawa K, Matsuoka T, Bito H, Ishizaki T, Narumiya S. Role of citron kinase as a target of the small GTPase Rho in cytokinesis. Nature 1998; 394:491-4; PMID:9697773; http://dx.doi.org/10.1038/28873
119. Kosako H, Yoshida T, Matsumura F, Ishizaki T, Narumiya S, Inagaki M. Rho-kinase/ROCK is involved in cytokinesis through the phosphorylation of myosin light chain and not ezrin/radixin/moesin proteins at the cleavage furrow. Oncogene 2000; 19:6059-64; PMID:11146558; http://dx.doi.org/10.1038/sj.onc.1203987
120. Yamashiro S, Totsukawa G, Yamakita Y, Sasaki Y, Madaule P, Ishizaki T, Narumiya S, Matsumura F. Citron kinase, a Rho-dependent kinase, induces di-phosphorylation of regulatory light chain of myosin II. Mol Biol Cell 2003; 14:1745-56; PMID:12802051; http://dx.doi.org/10.1091/mbc.E02-07-0427
121. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, et al. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 1996; 273:245-8; PMID:8662509; http://dx.doi.org/10.1126/science.273.5272.245
122. Kawano Y, Fukata Y, Oshiro N, Amano M, Nakamura T, Ito M, Matsumura F, Inagaki M, Kaibuchi K. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J Cell Biol 1999; 147:1023-38; PMID:10579722; http://dx.doi.org/10.1083/jcb.147.5.1023
123. Yokoyama T, Goto H, Izawa I, Mizutani H, Inagaki M. Aurora-B and Rho-kinase/ROCK, the two cleavage furrow kinases, independently regulate the progression of cytokinesis: possible existence of a novel cleavage furrow kinase phosphorylates ezrin/radixin/moesin (ERM). Genes Cells 2005; 10:127-37; PMID:15676024; http://dx.doi.org/10.1111/j.1365-2443.2005.00824.x
124. Bassi ZI, Verbrugghe KJ, Capalbo L, Gregory S, Montembault E, Glover DM, D'Avino PP. Sticky/Citron kinase maintains proper RhoA localization at the cleavage site during cytokinesis. J Cell Biol 2011; 195:595-603; PMID:22084308; http://dx.doi.org/10.1083/jcb.201105136
125. Gai M, Camera P, Dema A, Bianchi F, Berto G, Scarpa E, Germena G, Di Cunto F. Citron kinase controls abscission through RhoA and anillin. Mol Biol Cell 2011; 22:3768-78; PMID:21849473; http://dx.doi.org/10.1091/mbc.E10-12-0952
126. Watanabe S, De Zan T, Ishizaki T, Narumiya S. Citron kinase mediates transition from constriction to abscission through its coiled-coil domain. J Cell Sci 2013; 126:1773-84; PMID:23444367; http://dx.doi.org/10.1242/jcs.116608
127. Hickson GR, O'Farrell PH. Rho-dependent control of anillin behavior during cytokinesis. J Cell Biol 2008; 180:285-94; PMID:18209105; http://dx.doi.org/10.1083/jcb.200709005
128. Piekny AJ, Glotzer M. Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr Biol 2008; 18:30-6; PMID:18158243; http://dx.doi.org/10.1016/j.cub.2007.11.068
129. Prokopenko SN, Brumby A, O'Keefe L, Prior L, He Y, Saint R, Bellen HJ.A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev 1999; 13:2301-14; PMID:10485851; http://dx.doi.org/10.1101/gad.13.17.2301
130. Zhao WM, 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; 280:33516-24; PMID:16040610; http://dx.doi.org/10.1074/jbc.M504657200
131. Gregory SL, Ebrahimi S, Milverton J, Jones WM, Bejsovec A, Saint R. Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr Biol 2008; 18:25-9; PMID:18158242; http://dx.doi.org/10.1016/j.cub.2007.11.050
132. Shu HB, Li Z, Palacios MJ, Li Q, Joshi HC.A transient association of gamma-tubulin at the midbody is required for the completion of cytokinesis during the mammalian cell division. J Cell Sci 1995; 108:2955-62; PMID:8537435
133. Ettinger AW, Wilsch-Bräuninger M, Marzesco AM, Bickle M, Lohmann A, Maliga Z, Karbanová J, Corbeil D, Hyman AA, Huttner WB. Proliferating versus differentiating stem and cancer cells exhibit distinct midbody-release behaviour. Nat Commun 2011; 2:503; PMID:22009035; http://dx.doi.org/10.1038/ncomms1511
134. Kuo TC, Chen CT, Baron D, Onder TT, Loewer S, Almeida S, Weismann CM, Xu P, Houghton JM, Gao FB, et al. Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity. Nat Cell Biol 2011; 13:1214-23; PMID:21909099; http://dx.doi.org/10.1038/ncb2332
135. Green RA, Mayers JR, Wang S, Lewellyn L, Desai A, Audhya A, Oegema K. The midbody ring scaffolds the abscission machinery in the absence of midbody microtubules. J Cell Biol 2013; 203:505-20; PMID:24217623; http://dx.doi.org/10.1083/jcb.201306036
136. Steigemann P, Gerlich DW. Cytokinetic abscission: cellular dynamics at the midbody. Trends Cell Biol 2009; 19:606-16; PMID:19733077; http://dx.doi.org/10.1016/j.tcb.2009.07.008
137. Mollinari C, Kleman JP, Saoudi Y, Jablonski SA, Perard J, Yen TJ, Margolis RL. Ablation of PRC1 by small interfering RNA demonstrates that cytokinetic abscission requires a central spindle bundle in mammalian cells, whereas completion of furrowing does not. Mol Biol Cell 2005; 16:1043-55; PMID:15616196; http://dx.doi.org/10.1091/mbc.E04-04-0346
138. Elia N, Sougrat R, Spurlin TA, Hurley JH, Lippincott-Schwartz J.Dynamics of endosomal sorting complex required for transport (ESCRT) machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci U S A 2011; 108:4846-51; PMID:21383202; http://dx.doi.org/10.1073/pnas.1102714108
139. Guizetti J, Schermelleh L, Mäntler J, Maar S, Poser I, Leonhardt H, Müller-Reichert T, Gerlich DW. Cortical constriction during abscission involves helices of ESCRT-III-dependent filaments. Science 2011; 331:1616-20; PMID:21310966; http://dx.doi.org/10.1126/science.1201847
140. Schiel JA, Park K, Morphew MK, Reid E, Hoenger A, Prekeris R. Endocytic membrane fusion and buckling-induced microtubule severing mediate cell abscission. J Cell Sci 2011; 124:1411-24; PMID:21486954; http://dx.doi.org/10.1242/jcs.081448
141. Schiel JA, Simon GC, Zaharris C, Weisz J, Castle D, Wu CC, Prekeris R. FIP3-endosome-dependent formation of the secondary ingression mediates ESCRT-III recruitment during cytokinesis. Nat Cell Biol 2012; 14:1068-78; PMID:23000966; http://dx.doi.org/10.1038/ncb2577
142. Minoshima Y, Kawashima T, Hirose K, Tonozuka Y, Kawajiri A, Bao YC, Deng X, Tatsuka M, Narumiya S, May WS Jr., et al. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev Cell 2003; 4:549-60; PMID:12689593; http://dx.doi.org/10.1016/S1534-5807(03)00089-3
143. Fielding AB, Schonteich E, Matheson J, Wilson G, Yu X, Hickson GR, Srivastava S, Baldwin SA, Prekeris R, Gould GW. Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J 2005; 24:3389-99; PMID:16148947; http://dx.doi.org/10.1038/sj.emboj.7600803
144. Wilson GM, Fielding AB, Simon GC, Yu X, Andrews PD, Hames RS, Frey AM, Peden AA, Gould GW, Prekeris R. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol Biol Cell 2005; 16:849-60; PMID:15601896; http://dx.doi.org/10.1091/mbc.E04-10-0927
145. Carlton JG, Agromayor M, Martin-Serrano J.Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release. Proc Natl Acad Sci U S A 2008; 105:10541-6; PMID:18641129; http://dx.doi.org/10.1073/pnas.0802008105
146. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP, Rodesch CK, Sundquist WI. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J 2007; 26:4215-27; PMID:17853893; http://dx.doi.org/10.1038/sj.emboj.7601850
147. Raiborg C, Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009; 458:445-52; PMID:19325624; http://dx.doi.org/10.1038/nature07961
148. Hanson PI, Roth R, Lin Y, Heuser JE. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments. J Cell Biol 2008; 180:389-402; PMID:18209100; http://dx.doi.org/10.1083/jcb.200707031
149. Carlton JG, Martin-Serrano J.Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science 2007; 316:1908-12; PMID:17556548; http://dx.doi.org/10.1126/science.1143422
150. Connell JW, Lindon C, Luzio JP, Reid E. Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 2009; 10:42-56; PMID:19000169; http://dx.doi.org/10.1111/j.1600-0854.2008.00847.x
151. Simon GC, Prekeris R. Mechanisms regulating targeting of recycling endosomes to the cleavage furrow during cytokinesis. Biochem Soc Trans 2008; 36:391-4; PMID:18481966; http://dx.doi.org/10.1042/BST0360391
152. Simon GC, Schonteich E, Wu CC, Piekny A, Ekiert D, Yu X, Gould GW, Glotzer M, Prekeris R. Sequential Cyk-4 binding to ECT2 and FIP3 regulates cleavage furrow ingression and abscission during cytokinesis. EMBO J 2008; 27:1791-803; PMID:18511905; http://dx.doi.org/10.1038/emboj.2008.112
153. Liot C, Seguin L, Siret A, Crouin C, Schmidt S, Bertoglio J.APC(cdh1) mediates degradation of the oncogenic Rho-GEF Ect2 after mitosis. PLoS One 2011; 6:e23676; PMID:21886810; http://dx.doi.org/10.1371/journal.pone.0023676
154. Keil R, Kiessling C, Hatzfeld M. Targeting of p0071 to the midbody depends on KIF3. J Cell Sci 2009; 122:1174-83; PMID:19339549; http://dx.doi.org/10.1242/jcs.045377
155. Martz MK, Grabocka E, Beeharry N, Yen TJ, Wedegaertner PB. Leukemia-associated RhoGEF (LARG) is a novel RhoGEF in cytokinesis and required for the proper completion of abscission. Mol Biol Cell 2013; 24:2785-94; PMID:23885121; http://dx.doi.org/10.1091/mbc.E12-07-0533
156. Wolf A, Keil R, Götzl O, Mun A, Schwarze K, Lederer M, Hüttelmaier S, Hatzfeld M. The armadillo protein p0071 regulates Rho signalling during cytokinesis. Nat Cell Biol 2006; 8:1432-40; PMID:17115030; http://dx.doi.org/10.1038/ncb1504
157. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992; 70:401-10; PMID:1643658; http://dx.doi.org/10.1016/0092-8674(92)90164-8
158. Pollard TD. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 2007; 36:451-77; PMID:17477841; http://dx.doi.org/10.1146/annurev.biophys.35.040405.101936
159. Yoshizaki H, Ohba Y, Parrini MC, Dulyaninova NG, Bresnick AR, Mochizuki N, Matsuda M. Cell type-specific regulation of RhoA activity during cytokinesis. J Biol Chem 2004; 279:44756-62; PMID:15308673; http://dx.doi.org/10.1074/jbc.M402292200
160. Canman JC, Lewellyn L, Laband K, Smerdon SJ, Desai A, Bowerman B, Oegema K. Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science 2008; 322:1543-6; PMID:19056985; http://dx.doi.org/10.1126/science.1163086