Rac1-dependent recruitment of PAK2 to G2 phase centrosomes and their roles in the regulation of mitotic entry

Cell Cycle

Volumn 13, Issue 14, 2014, Pages 2210-2220

  May, Martin ^a   Schelle, Ilona ^a   Brakebusch, Cord ^b   Rottner, Klemens ^c,d   Genth, Harald ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Aurora; C. difficile toxin B; Cdc42; Cdk1; CyclinB; Mono O glucosylation; Rho

Indexed keywords

AURORA A KINASE; CLOSTRIDIUM DIFFICILE TOXIN B; CYCLIN B; CYCLIN DEPENDENT KINASE 1; GAMMA TUBULIN; HISTONE H1; HISTONE H3; LAMIN B; P21 ACTIVATED KINASE 1; P21 ACTIVATED KINASE 2; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PHOSPHOSPECIFIC ANTIBODY; POLO LIKE KINASE 1; PROTEIN CDC42; PROTEIN KINASE N; PROTEIN KINASE N2; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; AURKA PROTEIN, HUMAN; BACTERIAL PROTEIN; BACTERIAL TOXIN; CDK1 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE; NEUROPEPTIDE; P21 ACTIVATED KINASE; PAK2 PROTEIN, HUMAN; PAK2 PROTEIN, MOUSE; RAC1 PROTEIN, HUMAN; RAC1 PROTEIN, MOUSE; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE;

ANAPHASE; ANIMAL CELL; ANIMAL CELL CULTURE; ANTIBODY LABELING; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DIVISION; CELL MIGRATION; CENTROSOME; CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; DNA CONTENT; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME SUBSTRATE; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSFECTION; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; METAPHASE; MITOSIS; MITOSIS INDEX; MOUSE; NONHUMAN; PROMETAPHASE; PROPHASE; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN GLYCOSYLATION; REGULATORY MECHANISM; SPINDLE POLE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYMOLOGY; G2 PHASE CELL CYCLE CHECKPOINT; GENETICS; GLYCOSYLATION; METABOLISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR;

ANIMALS; AURORA KINASE A; BACTERIAL PROTEINS; BACTERIAL TOXINS; CENTROSOME; CYCLIN B; CYCLIN-DEPENDENT KINASES; ENZYME ACTIVATION; G2 PHASE CELL CYCLE CHECKPOINTS; GLYCOSYLATION; HELA CELLS; HUMANS; MICE; MITOSIS; NEUROPEPTIDES; P21-ACTIVATED KINASES; RAC1 GTP-BINDING PROTEIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84904512083     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.29279     Document Type: Article

References (29)

1. Gavet O, Pines J. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J Cell Biol 2010; 189:247-59; PMID:20404109; http://dx.doi.org/10.1083/jcb.200909144
2. Santos SD, Wollman R, Meyer T, Ferrell JE Jr. Spatial positive feedback at the onset of mitosis. Cell 2012; 149:1500-13; PMID:22726437; http://dx.doi.org/10.1016/j.cell.2012.05.028
3. Jackman M, Lindon C, Nigg EA, Pines J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 2003; 5:143-8; PMID:12524548; http://dx.doi.org/10.1038/ncb918
4. 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
5. Doxsey S, Zimmerman W, Mikule K. Centrosome control of the cell cycle. Trends Cell Biol 2005; 15:303-11; PMID:15953548; http://dx.doi.org/10.1016/j. tcb.2005.04.008
6. Lindqvist A, Rodríguez-Bravo V, Medema RH. The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J Cell Biol 2009; 185:193-202; PMID:19364923; http://dx.doi.org/10.1083/jcb.200812045
7. Macůrek L, Lindqvist A, Lim D, Lampson MA, Klompmaker R, Freire R, Clouin C, Taylor SS, Yaffe MB, Medema RH. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 2008; 455:119-23; PMID:18615013; http://dx.doi.org/10.1038/nature07185
8. Seki A, Coppinger JA, Jang CY, Yates JR, Fang G. Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science 2008; 320:1655-8; PMID:18566290; http://dx.doi.org/10.1126/science. 1157425
9. Bokoch GM. Biology of the p21-activated kinases. Annu Rev Biochem 2003; 72:743-81; PMID:12676796; http://dx.doi.org/10.1146/annurev.biochem.72.121801. 161742
10. Dummler B, Ohshiro K, Kumar R, Field J. Pak protein kinases and their role in cancer. Cancer Metastasis Rev 2009; 28:51-63; PMID:19165420; http://dx.doi.org/10.1007/s10555-008-9168-1
11. 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
12. Zhao ZS, Lim JP, Ng YW, Lim L, Manser E. The GIT-associated kinase PAK targets to the centrosome and regulates Aurora-A. Mol Cell 2005; 20:237-49; PMID:16246726; http://dx.doi.org/10.1016/j.molcel.2005.08.035
13. Schmidt A, Durgan J, Magalhaes A, Hall A. Rho GTPases regulate PRK2/PKN2 to control entry into mitosis and exit from cytokinesis. EMBO J 2007; 26:1624-36; PMID:17332740; http://dx.doi.org/10.1038/sj.emboj.7601637
14. Bornens M, Moudjou M. Studying the composition and function of centrosomes in vertebrates. Methods Cell Biol 1999; 61:13-34; PMID:9891307; http://dx.doi.org/10.1016/S0091-679X(08)61973-1
15. Ando Y, Yasuda S, Oceguera-Yanez F, Narumiya S. Inactivation of Rho GTPases with Clostridium difficile toxin B impairs centrosomal activation of Aurora-A in G2/M transition of HeLa cells. Mol Biol Cell 2007; 18:3752-63; PMID:17634283; http://dx.doi.org/10.1091/mbc.E07-03-0281
16. Huelsenbeck J, Dreger S, Gerhard R, Barth H, Just I, Genth H. Difference in the cytotoxic effects of toxin B from Clostridium difficile strain VPI 10463 and toxin B from variant Clostridium difficile strain 1470. Infect Immun 2007; 75:801-9; PMID:17145947; http://dx.doi.org/10.1128/IAI.01705-06
17. Genth H, Dreger SC, Huelsenbeck J, Just I. Clostridium difficile toxins: more than mere inhibitors of Rho proteins. Int J Biochem Cell Biol 2008; 40:592-7; PMID:18289919; http://dx.doi.org/10.1016/j.biocel.2007.12.014
18. Genth H, Huelsenbeck J, Hartmann B, Hofmann F, Just I, Gerhard R. Cellular stability of Rho-GTPases glucosylated by Clostridium difficile toxin B. FEBS Lett 2006; 580:3565-9; PMID:16730714; http://dx.doi.org/10.1016/j.febslet. 2006.04.100
19. Steffen A, Ladwein M, Dimchev GA, Hein A, Schwenkmezger L, Arens S, Ladwein KI, Margit Holleboom J, Schur F, Victor Small J, et al. Rac function is crucial for cell migration but is not required for spreading and focal adhesion formation. J Cell Sci 2013; 126:4572-88; PMID:23902686; http://dx.doi.org/10. 1242/jcs.118232
20. Czuchra A, Wu X, Meyer H, van Hengel J, Schroeder T, Geffers R, Rottner K, Brakebusch C. Cdc42 is not essential for filopodium formation, directed migration, cell polarization, and mitosis in fibroblastoid cells. Mol Biol Cell 2005; 16:4473-84; PMID:16014609; http://dx.doi.org/10.1091/mbc.E05-01-0061
21. Woodcock SA, Rushton HJ, Castañeda-Saucedo E, Myant K, White GR, Blyth K, Sansom OJ, Malliri A. Tiam1-Rac signaling counteracts Eg5 during bipolar spindle assembly to facilitate chromosome congression. Curr Biol 2010; 20:669-75; PMID:20346677; http://dx.doi.org/10.1016/j.cub.2010.02.033
22. Herrmann C, Ahmadian MR, Hofmann F, Just I. Functional consequences of monoglucosylation of Ha-Ras at effector domain amino acid threonine 35. J Biol Chem 1998; 273:16134-9; PMID:9632667; http://dx.doi.org/10.1074/jbc.273.26.16134
23. Sehr P, Joseph G, Genth H, Just I, Pick E, Aktories K. Glucosylation and ADP ribosylation of rho proteins: effects on nucleotide binding, GTPase activity, and effector coupling. Biochemistry 1998; 37:5296-304; PMID:9548761; http://dx.doi.org/10.1021/bi972592c
24. Genth H, Aktories K, Just I. Monoglucosylation of RhoA at threonine 37 blocks cytosol-membrane cycling. J Biol Chem 1999; 274:29050-6; PMID:10506156; http://dx.doi.org/10.1074/jbc.274.41.29050
25. Rossman KL, Der CJ, Sondek J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat Rev Mol Cell Biol 2005; 6:167-80; PMID:15688002; http://dx.doi.org/10.1038/nrm1587
26. Banerjee M, Worth D, Prowse DM, Nikolic M. Pak1 phosphorylation on t212 affects microtubules in cells undergoing mitosis. Curr Biol 2002; 12:1233-9; PMID:12176334; http://dx.doi.org/10.1016/S0960-9822(02)00956-9
27. ten Klooster JP, Jaffer ZM, Chernoff J, Hordijk PL. Targeting and activation of Rac1 are mediated by the exchange factor beta-Pix. J Cell Biol 2006; 172:759-69; PMID:16492808; http://dx.doi.org/10.1083/jcb.200509096
28. Cotteret S, Chernoff J. Pak GITs to Aurora-A. Dev Cell 2005; 9:573-4; PMID:16256730; http://dx.doi.org/10.1016/j.devcel.2005.10.005
29. Pugacheva EN, Roegiers F, Golemis EA. Interdependence of cell attachment and cell cycle signaling. Curr Opin Cell Biol 2006; 18:507-15; PMID:16919436; http://dx.doi.org/10.1016/j.ceb.2006.08.014