CYK4 inhibits Rac1-dependent PAK1 and ARHGEF7 effector pathways during cytokinesis

Journal of Cell Biology

Volumn 198, Issue 5, 2012, Pages 865-880

  Bastos, Ricardo Nunes ^a   Penate, Xenia ^a,c   Bates, Michelle ^a,d   Hammond, Dean ^a,b   Barr, Francis A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF SEVILLE   (Spain)

^d LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARHGEF7 PROTEIN; CYK4 PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; P21 ACTIVATED KINASE 1; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VINCULIN;

ANAPHASE; ARTICLE; CELL ADHESION; CELL DIVISION; CELL SPREADING; CONTROLLED STUDY; CYTOKINESIS; HUMAN; HUMAN CELL; MITOSIS; PRIORITY JOURNAL;

ANAPHASE; CDC42 GTP-BINDING PROTEIN; CELL ADHESION; CELL LINE, TUMOR; CYTOKINESIS; GTPASE-ACTIVATING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HELA CELLS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; P21-ACTIVATED KINASES; RAC1 GTP-BINDING PROTEIN; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; VINCULIN;

ANIMALIA;

EID: 84866378190     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201204107     Document Type: Article

References (53)

1. Barr F.A., and U. Gruneberg. 2007. Cytokinesis: placing and making the final cut. Cell. 131:847-860. http://dx.doi.org/10.1016/j.cell.2007.11.011
2. Bassi, Z.I., K.J. Verbrugghe, L. Capalbo, S. Gregory, E. Montembault, D.M. Glover, and P.P. D'Avino. 2011. Sticky/Citron kinase maintains proper RhoA localization at the cleavage site during cytokinesis. J. Cell Biol. 195:595-603. http://dx.doi.org/10.1083/jcb.201105136
3. Canman, J.C., L. Lewellyn, K. Laband, S.J. Smerdon, A. Desai, B. Bowerman, and K. Oegema. 2008. Inhibition of Rac by the GAP activity of centralspindlin is essential for cytokinesis. Science. 322:1543-1546. http://dx.doi.org/10.1126/science.1163086
4. Castrillon, D.H., and S.A. Wasserman. 1994. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development. 120:3367-3377.
5. Chesneau, L., D. Dambournet, M. Machicoane, I. Kouranti, M. Fukuda, B. Goud, and A. Echard. 2012. An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr. Biol. 22:147-153. http://dx.doi.org/10.1016/j.cub.2011.11.058
6. Cox, J., and M. Mann. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26:1367-1372. http://dx.doi.org/10.1038/nbt.1511
7. Cox, J., I. Matic, M. Hilger, N. Nagaraj, M. Selbach, J.V. Olsen, and M. Mann. 2009. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4:698-705. http://dx.doi.org/10.1038/nprot.2009.36
8. D'Avino, P.P., M.S. Savoian, and D.M. Glover. 2004. 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. 166:61-71. http://dx.doi.org/10.1083/jcb.200402157
9. D'Avino, P.P., M.S. Savoian, and D.M. Glover. 2005. Cleavage furrow formation and ingression during animal cytokinesis: a microtubule legacy. J. Cell Sci. 118:1549-1558. http://dx.doi.org/10.1242/jcs.02335
10. Frank, S.R., and S.H. Hansen. 2008. The PIX-GIT complex: a G protein signaling cassette in control of cell shape. Semin. Cell Dev. Biol. 19:234-244. http://dx.doi.org/10.1016/j.semcdb.2008.01.002
11. Fuchs, E., A.K. Haas, R.A. Spooner, S. Yoshimura, J.M. Lord, and F.A. Barr. 2007. Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways. J. Cell Biol. 177:1133-1143. http://dx.doi.org/10.1083/jcb.200612068
12. Glotzer, M. 2005. The molecular requirements for cytokinesis. Science. 307:1735-1739. http://dx.doi.org/10.1126/science.1096896
13. Glotzer, M. 2009. Cytokinesis: GAP gap. Curr. Biol. 19:R162-R165. http://dx.doi.org/10.1016/j.cub.2008.12.028
14. Goldstein, A.Y., Y.N. Jan, and L. Luo. 2005. Function and regulation of Tumbleweed (RacGAP50C) in neuroblast proliferation and neuronal morphogenesis. Proc. Natl. Acad. Sci. USA. 102:3834-3839. http://dx.doi.org/10.1073/pnas.0500748102
15. Gregory, S.L., S. Ebrahimi, J. Milverton, W.M. Jones, A. Bejsovec, and R. Saint. 2008. Cell division requires a direct link between microtubule-bound RacGAP and Anillin in the contractile ring. Curr. Biol. 18:25-29. http://dx.doi.org/10.1016/j.cub.2007.11.050
16. Heasman, S.J., and A.J. Ridley. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9:690-701. http://dx.doi.org/10.1038/nrm2476
17. Hickson, G.R., and P.H. O'Farrell. 2008. Rho-dependent control of anillin behavior during cytokinesis. J. Cell Biol. 180:285-294. http://dx.doi.org/10.1083/jcb.200709005
18. Hickson, G.R., A. Echard, and P.H. O'Farrell. 2006. Rho-kinase controls cell shape changes during cytokinesis. Curr. Biol. 16:359-370. http://dx.doi.org/10.1016/j.cub.2005.12.043
19. Jantsch-Plunger, V., P. Gönczy, A. Romano, H. Schnabel, D. Hamill, R. Schnabel, A.A. Hyman, and M. Glotzer. 2000. CYK-4: A Rho family GTPase activating protein (GAP) required for central spindle formation and cytokinesis. J. Cell Biol. 149:1391-1404. http://dx.doi.org/10.1083/jcb.149.7.1391
20. Jenkins, N., J.R. Saam, and S.E. Mango. 2006. CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science. 313:1298-1301. http://dx.doi.org/10.1126/science.1130291
21. Kechad, A., S. Jananji, Y. Ruella, and G.R. Hickson. 2012. Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr. Biol. 22:197-203. http://dx.doi.org/10.1016/j.cub.2011.11.062
22. Kimura, K., T. Tsuji, Y. Takada, T. Miki, and S. Narumiya. 2000. Accumulation of GTP-bound RhoA during cytokinesis and a critical role of ECT2 in this accumulation. J. Biol. Chem. 275:17233-17236. http://dx.doi.org/10.1074/jbc.C000212200
23. Lin, D., A.S. Edwards, J.P. Fawcett, G. Mbamalu, J.D. Scott, and T. Pawson. 2000. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2:549-547. http://dx.doi.org/10.1038/35019582
24. Loria, A., K.M. Longhini, and M. Glotzer. 2012. The RhoGAP domain of CYK-4 has an essential role in RhoA activation. Curr. Biol. 22:213-219. http://dx.doi.org/10.1016/j.cub.2011.12.019
25. Madaule, P., M. Eda, N. Watanabe, K. Fujisawa, T. Matsuoka, H. Bito, T. Ishizaki, and S. Narumiya. 1998. Role of citron kinase as a target of the small GTPase Rho in cytokinesis. Nature. 394:491-494. http://dx.doi.org/10.1038/28873
26. Mandato, C.A., H.A. Benink, and W.M. Bement. 2000. Microtubule-actomyosin interactions in cortical flow and cytokinesis. Cell Motil. Cytoskeleton. 45:87-92. http://dx.doi.org/10.1002/(SICI)1097-0169(200002)45:2<87::AID-CM1>3.0.CO;2-0
27. Manser, E., T.H. Loo, C.G. Koh, Z.S. Zhao, X.Q. Chen, L. Tan, I. Tan, T. Leung, and L. Lim. 1998. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell. 1:183-192. http://dx.doi.org/10.1016/S1097-2765(00)80019-2
28. Miller, A.L., and W.M. Bement. 2009. Regulation of cytokinesis by Rho GTPase flux. Nat. Cell Biol. 11:71-77. http://dx.doi.org/10.1038/ncb1814
29. Minoshima, Y., T. Kawashima, K. Hirose, Y. Tonozuka, A. Kawajiri, Y.C. Bao, X. Deng, M. Tatsuka, S. Narumiya, W.S. May Jr., et al. 2003. Phosphorylation by aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev. Cell. 4:549-560. http://dx.doi.org/10.1016/S1534-5807(03)00089-3
30. Mishima, M., S. Kaitna, and M. Glotzer. 2002. Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell. 2:41-54. http://dx.doi.org/10.1016/S1534-5807(01)00110-1
31. Neef, R., C. Preisinger, J. Sutcliffe, R. Kopajtich, E.A. Nigg, T.U. Mayer, and F.A. Barr. 2003. Phosphorylation of mitotic kinesin-like protein 2 by polo-like kinase 1 is required for cytokinesis. J. Cell Biol. 162:863-875. http://dx.doi.org/10.1083/jcb.200306009
32. Neef, R., U.R. Klein, R. Kopajtich, and F.A. Barr. 2006. Cooperation between mitotic kinesins controls the late stages of cytokinesis. Curr. Biol. 16:301-307. http://dx.doi.org/10.1016/j.cub.2005.12.030
33. Neef, R., U. Gruneberg, R. Kopajtich, X. Li, E.A. Nigg, H. Sillje, and F.A. Barr. 2007. Choice of Plk1 docking partners during mitosis and cytokinesis is controlled by the activation state of Cdk1. Nat. Cell Biol. 9:436-444. http://dx.doi.org/10.1038/ncb1557
34. Niiya, F., T. Tatsumoto, K.S. Lee, and T. Miki. 2006. Phosphorylation of the cytokinesis regulator ECT2 at G2/M phase stimulates association of the mitotic kinase Plk1 and accumulation of GTP-bound RhoA. Oncogene. 25:827-837. http://dx.doi.org/10.1038/sj.onc.1209124
35. Parsons, J.T., A.R. Horwitz, and M.A. Schwartz. 2010. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11:633-643. http://dx.doi.org/10.1038/nrm2957
36. Petronczki, M., M. Glotzer, N. Kraut, and J.M. Peters. 2007. Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. Dev. Cell. 12:713-725. http://dx.doi.org/10.1016/j.devcel.2007.03.013
37. Piekny, A.J., and M. Glotzer. 2008. Anillin is a scaffold protein that links RhoA, actin, and myosin during cytokinesis. Curr. Biol. 18:30-36. http://dx.doi.org/10.1016/j.cub.2007.11.068
38. Piekny, A., M. Werner, and M. Glotzer. 2005. Cytokinesis: welcome to the Rho zone. Trends Cell Biol. 15:651-658. http://dx.doi.org/10.1016/ j.tcb.2005.10.006
39. Portereiko, M.F., J. Saam, and S.E. Mango. 2004. ZEN-4/MKLP1 is required to polarize the foregut epithelium. Curr. Biol. 14:932-941. http://dx.doi .org/10.1016/j.cub.2004.05.052
40. Rittinger, K., P.A. Walker, J.F. Eccleston, K. Nurmahomed, D. Owen, E. Laue, S.J. Gamblin, and S.J. Smerdon. 1997a. Crystal structure of a small G protein in complex with the GTPase-activating protein rhoGAP. Nature. 388:693-697. http://dx.doi.org/10.1038/41805
41. Rittinger, K., P.A. Walker, J.F. Eccleston, S.J. Smerdon, and S.J. Gamblin. 1997b. Structure at 1.65 A of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature. 389:758-762. http://dx.doi.org/10.1038/39651
42. Somers, W.G., and R. Saint. 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. http://dx.doi.org/10.1016/S1534-5807(02)00402-1
43. Su, K.C., T. Takaki, and M. Petronczki. 2011. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev. Cell. 21:1104-1115. http://dx.doi.org/10.1016/j.devcel.2011.11.003
44. Tatsumoto, T., X. Xie, R. Blumenthal, I. Okamoto, and T. Miki. 1999. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J. Cell Biol. 147:921-928. http://dx.doi.org/10.1083/jcb.147.5.921
45. Touré, A., O. Dorseuil, L. Morin, P. Timmons, B. Jégou, L. Reibel, and G. Gacon. 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. 273:6019-6023. http://dx.doi.org/10.1074/jbc.273.11.6019
46. Vitale, N., W.A. Patton, J. Moss, M. Vaughan, R.J. Lefkowitz, and R.T. Premont. 2000. GIT proteins, A novel family of phosphatidylinositol 3,4, 5-trisphosphate-stimulated GTPase-activating proteins for ARF6. J. Biol. Chem. 275:13901-13906. http://dx.doi.org/10.1074/jbc.275.18.13901
47. Wodarz, A. 2005. Molecular control of cell polarity and asymmetric cell division in Drosophila neuroblasts. Curr. Opin. Cell Biol. 17:475-481. http://dx.doi.org/10.1016/j.ceb.2005.08.005
48. Wolfe, B.A., T. Takaki, M. Petronczki, and M. Glotzer. 2009. Polo-like kinase 1 directs assembly of the HsCyk-4 RhoGAP/Ect2 RhoGEF complex to initiate cleavage furrow formation. PLoS Biol. 7:e1000110. http://dx.doi.org/10.1371/journal.pbio.1000110
49. Yamada, T., M. Hikida, and T. Kurosaki. 2006. Regulation of cytokinesis by mgcRacGAP in B lymphocytes is independent of GAP activity. Exp. Cell Res. 312:3517-3525. http://dx.doi.org/10.1016/j.yexcr.2006.07.026
50. Yoshizaki, H., Y. Ohba, K. Kurokawa, R.E. Itoh, T. Nakamura, N. Mochizuki, K. Nagashima, and M. Matsuda. 2003. Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J. Cell Biol. 162:223-232. http://dx.doi.org/10.1083/jcb.200212049
51. Yoshizaki, H., Y. Ohba, M.C. Parrini, N.G. Dulyaninova, A.R. Bresnick, N. Mochizuki, and M. Matsuda. 2004. Cell type-specific regulation of RhoA activity during cytokinesis. J. Biol. Chem. 279:44756-44762. http://dx.doi.org/10.1074/jbc.M402292200
52. Yüce, O., A. Piekny, and M. Glotzer. 2005. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J. Cell Biol. 170:571582. http://dx.doi.org/10.1083/jcb.200501097
53. Zavortink, M., N. Contreras, T. Addy, A. Bejsovec, and R. Saint. 2005. Tum/RacGAP50C provides a critical link between anaphase microtubules and the assembly of the contractile ring in Drosophila melanogaster. J. Cell Sci. 118:5381-5392. http://dx.doi.org/10.1242/jcs.02652