Rho GTPases regulate PRK2/PKN2 to control entry into mitosis and exit from cytokinesis

EMBO Journal

Volumn 26, Issue 6, 2007, Pages 1624-1636

  Schmidt, Anja ^a   Durgan, Joanne ^a,b   Magalhaes, Ana ^a,b   Hall, Alan ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cdc25B; Cdk1; Cell cycle; PRK; Rho GTPase

Indexed keywords

CYCLIN DEPENDENT KINASE 1; PROTEIN; PROTEIN PKN2; PROTEIN PRK2; PROTEIN TYROSINE PHOSPHATASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ABSCISSION; ARTICLE; CELL CYCLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIVISION; CONTROLLED STUDY; CYTOKINESIS; HUMAN; HUMAN CELL; MAMMAL CELL; MITOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

CDC25 PHOSPHATASE; CELL CYCLE PROTEINS; CYTOKINESIS; FLOW CYTOMETRY; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; MITOSIS; PHOSPHORYLATION; PROTEIN KINASE C; RHO GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 33947591759     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601637     Document Type: Article

References (52)

1. Bakal CJ, Finan D, LaRose J, Wells CD, Gish G, Kulkarni S, DeSepulveda P, Wilde A, Rottapel R (2005) The Rho GTP exchange factor Lfc promotes spindle assembly in early mitosis. Proc Natl Acad Sci USA 102: 9529-9534
2. Cazales M, Schmitt E, Montembault E, Dozier C, Prigent C, Ducommun B (2005) CDC25B phosphorylation by Aurora-A occurs at the G2/M transition and is inhibited by DNA damage. Cell Cycle 4: 1233-1238
3. Coleman ML, Marshall CJ, Olson MF (2004) RAS and RHO GTPases in G1-phase cell-cycle regulation. Nat Rev Mol Cell Biol 5: 355-366
4. De Souza CP, Ellem KA, Gabrielli BG (2000) Centrosomal and cytoplasmic Cdc2/cyclin B1 activation precedes nuclear mitotic events. Exp Cell Res 257: 11-21
5. Di Cunto F, Imarisio S, Hirsch E, Broccoli V, Bulfone A, Migheli A, Atzori C, Turco E, Triolo R, Dotto GP, Silengo L, Altruda F (2000) Defective neurogenesis in citron kinase knockout mice by altered cytokinesis and massive apoptosis. Neuron 28: 115-127
6. Du J, Hannon GJ (2004) Suppression of p160ROCK bypasses cell cycle arrest after Aurora-A/STK15 depletion. Proc Natl Acad Sci USA 101: 8975-8980
7. Dutertre S, Cazales M, Quaranta M, Froment C, Trabut V, Dozier C, Mirey G, Bouche JP, Theis-Febvre N, Schmitt E, Monsarrat B, Prigent C, Ducommun B (2004) Phosphorylation of CDC25B by Aurora-A at the centrosome contributes to the G2-M transition. J Cell Sci 117: 2523-2531
8. Eda M, Yonemura S, Kato T, Watanabe N, Ishizaki T, Madaule P, Narumiya S (2001) Rho-dependent transfer of Citron-kinase to the cleavage furrow of dividing cells. J Cell Sci 114: 3273-3284
9. Ferguson AM, White LS, Donovan PJ, Piwnica-Worms H (2005) Normal cell cycle and checkpoint responses in mice and cells lacking Cdc25B and Cdc25C protein phosphatases. Mol Cell Biol 25: 2853-2860
10. Flynn P, Mellor H, Palmer R, Panayotou G, Parker PJ (1998) Multiple interactions of PRK1 with RhoA. Functional assignment of the Hr1 repeat motif. J Biol Chem 273: 2698-2705
11. Gabrielli BG, De Souza CP, Tonks ID, Clark JM, Hayward NK, Ellem KA (1996) Cytoplasmic accumulation of cdc25B phosphatase in mitosis triggers centrosomal microtubule nucleation in HeLa cells. J Cell Sci 109 (Part 5): 1081-1093
12. Glotzer M (2005) The molecular requirements for cytokinesis. Science 307: 1735-1739
13. Gotta M, Abraham MC, Ahringer J (2001) CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr Biol 11: 482-488
14. Gould KL, Nurse P (1989) Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 342: 39-45
15. Gross C, Heumann R, Erdmann KS (2001) The protein kinase C-related kinase PRK2 interacts with the protein tyrosine phosphatase PTP-BL via a novel PDZ domain binding motif. FEBS Lett 496: 101-104
16. Gruneberg U, Neef R, Li X, Chan EH, Chalamalasetty RB, Nigg EA, Barr FA (2006) KIF14 and citron kinase act together to promote efficient cytokinesis. J Cell Biol 172: 363-372
17. Herrmann L, Dittmar T, Erdmann KS (2003) The protein tyrosine phosphatase PTP-BL associates with the midbody and is involved in the regulation of cytokinesis. Mol Biol Cell 14: 230-240
18. Hirota T, Kunitoku N, Sasayama T, Marumoto T, Zhang D, Nitta M, Hatakeyama K, Saya H (2003) Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114: 585-598
19. Jackman M, Lindon C, Nigg EA, Pines J (2003) Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 5: 143-148
20. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21: 247-269
21. Kamijo K, Ohara N, Abe M, Uchimura T, Hosoya H, Lee JS, Miki T (2006) Dissecting the role of Rho-mediated signaling in contractile ring formation. Mol Biol Cell 17: 43-55
22. Karlsson-Rosenthal C, Millar JB (2006) Cdc25: mechanisms of checkpoint inhibition and recovery. Trends Cell Biol 16: 285-292
23. Kosako H, Yoshida T, Matsumura F, Ishizaki T, Narumiya S, Inagaki M (2000) 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 19: 6059-6064
24. Lammer C, Wagerer S, Saffrich R, Mertens D, Ansorge W, Hoffmann I (1998) The cdc25B phosphatase is essential for the G2/M phase transition in human cells. J Cell Sci 111 (Part 16): 2445-2453
25. Lindqvist A, Kallstrom H, Karlsson Rosenthal C (2004) Characterisation of Cdc25B localisation and nuclear export during the cell cycle and in response to stress. J Cell Sci 117: 4979-4990
26. Lindqvist A, Kallstrom H, Lundgren A, Barsoum E, Rosenthal CK (2005) Cdc25B cooperates with Cdc25A to induce mitosis but has a unique role in activating cyclin B1-Cdk1 at the centrosome. J Cell Biol 171: 35-45
27. Mabuchi I, Hamaguchi Y, Fujimoto H, Morii N, Mishima M, Narumiya S (1993) A rho-like protein is involved in the organisation of the contractile ring in dividing sand dollar eggs. Zygote 1: 325-331
28. Madaule P, Eda M, Watanabe N, Fujisawa K, Matsuoka T, Bito H, Ishizaki T, Narumiya S (1998) Role of citron kinase as a target of the small GTPase Rho in cytokinesis. Nature 394: 491-494
29. Maddox AS, Burridge K (2003) RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J Cell Biol 160: 255-265
30. Mailand N, Podtelejnikov AV, Groth A, Mann M, Bartek J, Lukas J (2002) Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J 21: 5911-5920
31. Mettouchi A, Klein S, Guo W, Lopez-Lago M, Lemichez E, Westwick JK, Giancotti FG (2001) Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell 8: 115-127
32. Millar JB, Blevitt J, Gerace L, Sadhu K, Featherstone C, Russell P (1991) p55CDC25 is a nuclear protein required for the initiation of mitosis in human cells. Proc Natl Acad Sci USA 88: 10500-10504
33. Misaki K, Mukai H, Yoshinaga C, Oishi K, Isagawa T, Takahashi M, Ohsumi K, Kishimoto T, Ono Y (2001) PKN delays mitotic timing by inhibition of Cdc25C: possible involvement of PKN in the regulation of cell division. Proc Natl Acad Sci USA 98: 125-129
34. Mukai H (2003) The structure and function of PKN, a protein kinase having a catalytic domain homologous to that of PKC. J Biochem (Tokyo) 133: 17-27
35. Niiya F, Tatsumoto T, Lee KS, Miki T (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
36. Nishimura Y, Yonemura S (2006) Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J Cell Sci 119: 104-114
37. Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144: 1235-1244
38. Oceguera-Yanez F, Kimura K, Yasuda S, Higashida C, Kitamura T, Hiraoka Y, Haraguchi T, Narumiya S (2005) Ect2 and MgcRacGAP regulate the activation and function of Cdc42 in mitosis. J Cell Biol 168: 221-232
39. Olson MF, Ashworth A, Hall A (1995) An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science 269: 1270-1272
40. Olson MF, Paterson HF, Marshall CJ (1998) Signals from Ras and Rho GTPases interact to regulate expression of p21Waf1/Cip1. Nature 394: 295-299
41. Palmer RH, Ridden J, Parker PJ (1995) Cloning and expression patterns of two members of a novel protein-kinase-C-related kinase family. Eur J Biochem 227: 344-351
42. Piekny A, Werner M, Glotzer M (2005) Cytokinesis: welcome to the Rho zone. Trends Cell Biol 15: 651-658
43. Schmidt A, Hall A (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 16: 1587-1609
44. Schweitzer JK, D'Souza-Schorey C (2004) Finishing the job: cytoskeletal and membrane events bring cytokinesis to an end. Exp Cell Res 295: 1-8
45. Shandala T, Gregory SL, Dalton HE, Smallhorn M, Saint R (2004) Citron kinase is an essential effector of the Pbl-activated Rho signalling pathway in Drosophila melanogaster. Development 131: 5053-5063
46. Takahashi M, Shibata H, Shimakawa M, Miyamoto M, Mukai H, Ono Y (1999) Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the golgi apparatus. J Biol Chem 274: 17267-17274
47. 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: 921-928
48. Vincent S, Settleman J (1997) The PRK2 kinase is a potential effector target of both Rho and Rac GTPases and regulates actin cytoskeletal organization. Mol Cell Biol 17: 2247-2256
49. Welsh CF, Roovers K, Villanueva J, Liu Y, Schwartz MA, Assoian RK (2001) Timing of cyclin D1 expression within G1 phase is controlled by Rho. Nat Cell Biol 3: 950-957
50. Yamamoto M, Marui N, Sakai T, Morii N, Kozaki S, Ikai K, Imamura S, Narumiya S (1993) ADP-ribosylation of the rhoA gene product by botulinum C3 exoenzyme causes Swiss 3T3 cells to accumulate in the G1 phase of the cell cycle. Oncogene 8: 1449-1455
51. Yasuda S, Oceguera-Yanez F, Kato T, Okamoto M, Yonemura S, Terada Y, Ishizaki T, Narumiya S (2004) Cdc42 and mDia3 regulate microtubule attachment to kinetochores. Nature 428: 767-771
52. Yuce O, Piekny A, Glotzer M (2005) An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 170: 571-582