PAK4 kinase activity and somatic mutation promote carcinoma cell motility and influence inhibitor sensitivity

Oncogene

Volumn 32, Issue 16, 2013, Pages 2114-2120

  Whale, A D ^a,b   Dart, A ^b   Holt, M ^a   Jones, G E ^a   Wells, C M ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

cancer; motility; prostate

Indexed keywords

GLUTAMINE; GLYCINE; LIM KINASE 1; LYSINE; P21 ACTIVATED KINASE 4; P21 ACTIVATED KINASE 4 INHIBITOR; PROTEIN CDC42; PROTEIN SERINE THREONINE KINASE INHIBITOR; PURVALANOL A; SCATTER FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CARCINOMA CELL; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SOMATIC MUTATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATE; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CELL MOVEMENT; HEPATOCYTE GROWTH FACTOR; HUMANS; LIM KINASES; MALE; MUTATION; P21-ACTIVATED KINASES; PHOSPHORYLATION; PROSTATIC NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 84876695177     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.233     Document Type: Article

References (37)

1. Cecchi F, Rabe DC, Bottaro DP. Targeting the HGF/Met signalling pathway in cancer. Eur J Cancer 2010; 46: 1260-1270.
2. Knudsen BS, Woude GV. Showering c-MET-dependent cancers with drugs. Curr opin Genetics Dev 2008; 18: 87-96.
3. Lai AZ, Abella JV, Park M. Crosstalk in Met receptor oncogenesis. Trends Cell Biol 2009; 19: 542-551.
4. Paliouras GN, Naujokas MA, Park M. Pak4, a novel Gab1 binding partner, modulates cell migration and invasion by the Met receptor. Mol Cell Biol 2009; 29: 3018-3032.
5. Abo A, Qu J, Cammarano MS, Dan C, Fritsch A, Baud V et al. PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO J 1998; 17: 6527-6540.
6. Callow MG, Zozulya S, Gishizky ML, Jallal B, Smeal T. PAK4 mediates morphological changes through the regulation of GEF-H1. J Cell Sci 2005; 118: 1861-1872.
7. Wells CM, Whale AD, Parsons M, Masters JR, Jones GE. PAK4: a pluripotent kinase that regulates prostate cancer cell adhesion. J Cell Sci 2010; 123: 1663-1673.
8. Li Z, Zhang H, Lundin L, Thullberg M, Liu Y, Wang Y et al. p21-activated kinase 4 phosphorylation of integrin b5 Ser-759 and Ser-762 regulates cell migration. J Biol Chem 2010; 285: 23699-23710.
9. Dan C, Kelly A, Bernard O, Minden A. Cytoskeletal changes regulated by the PAK4 serine/threonine kinase are mediated by LIM kinase 1 and cofilin. J Biol Chem 2001; 276: 32115-32121.
10. Soosairajah J, Maiti S, Wiggan O, Sarmiere P, Moussi N, Sarcevic B et al. Interplay between components of a novel LIM kinase-slingshot phosphatase complex regulates cofilin. EMBO J 2005; 24: 473-486.
11. Lai FPL, Szczodrak M, Block J, Faix J, Breitsprecher D, Mannherz HG et al. Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J 2008; 27: 982-992.
12. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS et al. Cofilin promotes actin polymerization and defines the direction of cell motility. Science 2004; 304: 743-746.
13. Callow MG, Clairvoyant F, Zhu S, Schryver B, Whyte DB, Bischoff JR et al. Requirement for PAK4 in the anchorage-independent growth of human cancer cell lines. J Biol Chem 2002; 277: 550-558.
14. Liu Y, Xiao H, Tian Y, Nekrasova T, Hao X, Lee HJ et al. The pak4 protein kinase plays a key role in cell survival and tumorigenesis in athymic mice. Mol Cancer Res 2008; 6: 215-224.
15. Whale A, Hashim FN, Fram S, Jones GE, Wells CM. Signalling to cancer cell invasion through PAK family kinases. Front Biosci 2011; 16: 849-864.
16. Parsons DW, Wang TL, Samuels Y, Bardelli A, Cummins JM, DeLong L et al. Colorectal cancer: mutations in a signalling pathway. Nature 2005; 436: 792.
17. Kimmelman AC, Hezel AF, Aguirre AJ, Zheng H, Paik J, Ying H et al. Genomic alterations link Rho family of GTPases to the highly invasive phenotype of pancreas cancer. Proc Natl Acad Sci USA 2008; 105: 19372-19377.
18. Li Z, Lock JG, Olofsson H, Kowalewski JM, Teller S, Liu Y et al. Integrin-mediated cell attachment induces a PAK4-dependent feedback loop regulating cell adhesion through modified integrin avb5 clustering and turnover. Mol Biol Cell 2010; 21: 3317-3329.
19. Siu MKY, Chan HY, Konga DSH, Wong ESY, Wong OGW, Ngan HYS et al. p21-activated kinase 4 regulates ovarian cancer cell proliferation, migration, and invasion and contributes to poor prognosis in patients. Proc Natl Acad Sci USA 2010; 107: 18622-18627.
20. Eswaran J, Soundararajan M, Knapp S. Targeting group II PAKs in cancer and metastasis. Cancer Metastasis Rev 2009; 28: 209-217.
21. Zhao Z, Manser E. Do PAKs make good drug targets? Faculty of 1000 2010 2: 70.
22. Murray BW, Guoa C, Piraino J, Westwick JK, Zhang C, Lamerdin J et al. Small-molecule p21-activated kinase inhibitor PF-3758309 is a potent inhibitor of oncogenic signaling and tumor growth. Proc Natl Acad Sci USA 2010; 107: 9446-9451.
23. Finkelstein E, Chang W, Chao P-HG, Gruber D, Minden A, Hung CT et al. Roles of microtubules, cell polarity and adhesion in electric-field-mediated motility of 3T3 fibroblasts. J Cell Sci 2004; 117: 1533-1545.
24. Ahmed T, Shea K, Masters JR, Jones GE, Wells CMA. PAK4-LIMK1 pathway drives prostate cancer cell migration downstream of HGF. Cell Signal 2008; 20: 1320-1328.
25. Scott RW, Hooper S, Crighton D, Li A, König I, Munro J et al. LIM kinases are required for invasive path generation by tumor and tumor-associated stromal cells. J Cell Biol 2010; 191: 169-185.
26. Yoshioka K, Foletta V, Bernard O, Itoh K. A role for LIM kinase in cancer invasion. Proc Natl Acad Sci USA 2003; 100: 7247-7252.
27. Baldassa S, Calogero AM, Colombo G, Zippel R, Gnesutta N. N-Terminal interaction domain implicates PAK4 in translational regulation and reveals novel cellular localization signals. J Cell Physiol 2010; 224: 722-733.
28. Eswaran J, Lee WH, Debreczeni JE, Filippakopoulos P, Turnbull A, Fedorov O et al. Crystal structures of the p21-activated kinases PAK4, PAK5, and PAK6 reveal catalytic domain plasticity of active group II PAKs. Structure 2007; 15: 201-213.
29. Grant BD, Hemmer W, Tsigelny I, Adams JA, Taylor SS. Kinetic analyses of mutations in the glycine-rich loop of cAMP-dependent protein kinase. Biochemistry 1998; 37: 7708-7715.
30. Barouch-Bentov R, Che J, Lee CC, Yang Y, Herman A, Jia Y et al. A conserved salt bridge in the G loop of multiple protein kinases is important for catalysis and for in vivo Lyn function. Mol Cell 2009; 33: 43-52.
31. Griswold IJ, MacPartlin M, Bumm T, Goss VL, O'Hare T, Lee KA et al. Kinase domain mutants of Bcr-Abl exhibit altered transformation potency, kinase activity, and substrate utilization, irrespective of sensitivity to imatinib. Mol Cell Biol 2006; 26: 6082-6093.
32. Yamamoto M, Kurosu T, Kakihana K, Mizuchi D, Miura O. The two major imatinib resistance mutations E255K and T315I enhance the activity of BCR/ABL fusion kinase. Biochem Biophys Res Commun 2004; 319: 1272-1275.
33. Skaggs BJ, Gorre ME, Ryvkin A, Burgess MR, Xie Y, Han Y et al. Phosphorylation of the ATP-binding loop directs oncogenicity of drug-resistant BCR-ABL mutants. Proc Natl Acad Sci USA 2006; 103: 19466-19471.
34. Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, Kuriyan J et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2002; 2: 117-125.
35. Pavlovsky C, Kantarjian H, Cortes JE. First-line therapy for chronic myeloid leukemia: past, present, and future. Am J Hematol 2009; 84: 287-293.
36. Girdler F, Sessa F, Patercoli S, Villa F, Musacchio A, Taylor S et al. Molecular basis of drug resistance in aurora kinases. Chem Biol 2008; 15: 552-562.
37. Zicha D, Dunn G, Jones G. Analyzing chemotaxis using the Dunn direct-viewing chamber. Methods Mol Biol 1997; 75: 449-57.