Selective regulation of p38β protein and signaling by integrin-linked kinase mediates bladder cancer cell migration

Oncogene

Volumn 33, Issue 6, 2014, Pages 690-701

  Yu, L ^a   Yuan, X ^b   Wang, D ^a   Barakat, B ^a   Williams, E D ^a   Hannigan, G E ^a  

^a MONASH UNIVERSITY   (Australia)

^b XINHUA HOSPITAL AFFILIATED TO SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

bladder cancer; cell migration; heat shock protein 27; integrin linked kinase; p38b isoform; p38MAPK protein kinases

Indexed keywords

ACTINS; CASE-CONTROL STUDIES; CELL MOVEMENT; GENE KNOCKDOWN TECHNIQUES; HSP27 HEAT-SHOCK PROTEINS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 11; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; URINARY BLADDER NEOPLASMS;

EID: 84893729169     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.20     Document Type: Article

References (54)

1. Cuenda A, Rousseau S. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim Biophys Acta 2007; 1773: 1358-1375.
2. Coulthard LR, White DE, Jones DL, McDermott MF, Burchill SA. p38(MAPK): stress responses from molecular mechanisms to therapeutics. Trends Mol Med 2009; 15: 369-379.
3. del Barco Barrantes I, Coya JM, Maina F, Arthur JS, Nebreda AR. Genetic analysis of specific and redundant roles for p38alpha and p38beta MAPKs during mouse development. Proc Natl Acad Sci USA 2011; 108: 12764-12769.
4. Remy G, Risco AM, Inesta-Vaquera FA, Gonzalez-Teran B, Sabio G, Davis RJ et al. Differential activation of p38MAPK isoforms by MKK6 and MKK3. Cell Signal 2010; 22: 660-667.
5. Li Q, Zhang N, Zhang D, Wang Y, Lin T, Zhou H et al. Determinants that control the distinct subcellular localization of p38alpha-PRAK and p38beta-PRAK complexes. J Biol Chem 2008; 283: 11014-11023.
6. Cerezo-Guisado MI, del Reino P, Remy G, Kuma Y, Arthur JS, Gallego-Ortega D et al. Evidence of p38gamma and p38delta involvement in cell transformation processes. Carcinogenesis 2011; 32: 1093-1099.
7. Otto KB, Acharya SS, Robinson VL. Stress-activated kinase pathway alteration is a frequent event in bladder cancer. Urol Oncol 2011; 30: 415-420.
8. Herbsleb M, Christensen OF, Thykjaer T, Wiuf C, Borre M, Orntoft TF et al. Bioinformatic identification of FGF, p38-MAPK, and calcium signalling pathways associated with carcinoma in situ in the urinary bladder. BMC Cancer 2008; 8: 37.
9. Kumar B, Koul S, Petersen J, Khandrika L, Hwa JS, Meacham RB et al. p38 mitogenactivated protein kinase-driven MAPKAPK2 regulates invasion of bladder cancer by modulation of MMP-2 and MMP-9 activity. Cancer Res 2010; 70: 832-841.
10. Estrada Y, Dong J, Ossowski L. Positive crosstalk between ERK and p38 in melanoma stimulates migration and in vivo proliferation. Pigment Cell Melanoma Res 2009; 22: 66-76.
11. Yong HY, Koh MS, Moon A. The p38 MAPK inhibitors for the treatment of inflammatory diseases and cancer. Expert Opin Investig Drugs 2009; 18: 1893-1905.
12. Tan C, Mui A, Dedhar S. Integrin-linked kinase regulates inducible nitric oxide synthase and cyclooxygenase-2 expression in an NF-kappa B-dependent manner. J Biol Chem 2002; 277: 3109-3116.
13. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G, Filmus J et al. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 1996; 379: 91-96.
14. Zervas CG, Gregory SL, Brown NH. Drosophila integrin-linked kinase is required at sites of integrin adhesion to link the cytoskeleton to the plasma membrane. J Cell Biol 2001; 152: 1007-1018.
15. Mackinnon AC, Qadota H, Norman KR, Moerman DG, Williams BD. C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr Biol 2002; 12: 787-797.
16. Sakai T, Li S, Docheva D, Grashoff C, Sakai K, Kostka G et al. Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev 2003; 17: 926-940.
17. Cabodi S, del Pilar Camacho-Leal M, Di Stefano P, Defilippi P. Integrin signalling adaptors: not only figurants in the cancer story. Nat Rev Cancer 2010; 10: 858-870.
18. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer 2005; 5: 51-63.
19. Gao J, Zhu J, Li HY, Pan XY, Jiang R, Chen JX. Small interfering RNA targeting integrin-linked kinase inhibited the growth and induced apoptosis in human bladder cancer cells. Int J Biochem Cell Biol 2011; 43: 1294-1304.
20. Matsui YAK, Ogawa O, Raven PA, Dedhar S, Gleave ME, Salh B et al. The importance of integrin-linked kinase in the regulation of bladder cancer invasion. Int J Cancer 2012; 130: 521-531.
21. Qian Y, Zhong X, Flynn DC, Zheng JZ, Qiao M, Wu C et al. ILK mediates actin filament rearrangements and cell migration and invasion through PI3K/Akt/Rac1 signaling. Oncogene 2005; 24: 3154-3165.
22. Lu H, Fedak PW, Dai X, Du C, Zhou YQ, Henkelman M et al. Integrin-linked kinase expression is elevated in human cardiac hypertrophy and induces hypertrophy in transgenic mice. Circulation 2006; 114: 2271-2279.
23. Leung-Hagesteijn C, Hu MC, Mahendra AS, Hartwig S, Klamut HJ, Rosenblum ND et al. Integrin-linked kinase mediates bone morphogenetic protein 7-dependent renal epithelial cell morphogenesis. Mol Cell Biol 2005; 25: 3648-3657.
24. Smeeton J, Zhang X, Bulus N, Mernaugh G, Lange A, Karner CM et al. Integrinlinked kinase regulates p38 MAPK-dependent cell cycle arrest in ureteric bud development. Development 2010; 137: 3233-3243.
25. Esfandiarei M, Yazdi SA, Gray V, Dedhar S, van Breemen C. Integrin-linked kinase functions as a downstream signal of platelet-derived growth factor to regulate actin polymerization and vascular smooth muscle cell migration. BMC Cell Biol 2010; 11: 16.
26. Chaffer CL, Dopheide B, McCulloch DR, Lee AB, Moseley JM, Thompson EW et al. Upregulated MT1-MMP/TIMP-2 axis in the TSU-Pr1-B1/B2 model of metastatic progression in transitional cell carcinoma of the bladder. Clin Exp Metastasis 2005; 22: 115-125.
27. Roussos ET, Condeelis JS, Patsialou A. Chemotaxis in cancer. Nat Rev Cancer 2011; 11: 573-587.
28. Filipenko NR, Attwell S, Roskelley C, Dedhar S. Integrin-linked kinase activity regulates Rac-and Cdc42-mediated actin cytoskeleton reorganization via a-PIX. Oncogene 2005; 24: 5837-5849.
29. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA 2004; 20: 7618-7623.
30. Jones TJ, Adapala RK, Geldenhuys WJ, Bursley C, AbouAlaiwi WA, Nauli SM et al. Primary cilia regulates the directional migration and barrier integrity of endothelial cells through the modulation of hsp27 dependent actin cytoskeletal organization. J Cell Physiol 2012; 227: 70-76.
31. Zhu Z, Xu X, Yu Y, Graham M, Prince ME, Carey TE et al. Silencing heat shock protein 27 decreases metastatic behavior of human head and neck squamous cell cancer cells in vitro. Mol Pharmacol 2010; 7: 1283-1290.
32. Shyu YJ, Hiatt SM, Duren HM, Ellis RE, Kerppola TK, Hu CD. Visualization of protein interactions in living Caenorhabditis elegans using bimolecular fluorescence complementation analysis. Nat Protoc 2008; 3: 588-596.
33. Mongroo PS, Johnstone CN, Naruszewicz I, Leung-Hagesteijn C, Sung RK, Carnio L et al. Beta-parvin inhibits integrin-linked kinase signaling and is downregulated in breast cancer. Oncogene 2004; 23: 8959-8970.
34. New L, Jiang Y, Zhao M, Liu K, Zhu W, Flood LJ et al. PRAK, a novel protein kinase regulated by the p38 MAP kinase. EMBO J 1998; 17: 3372-3384.
35. Jarvius M, Paulsson J, Weibrecht I, Leuchowius KJ, Andersson AC, Wahlby C et al. In situ detection of phosphorylated platelet-derived growth factor receptor beta using a generalized proximity ligation method. Mol Cell Proteomics 2007; 6: 1500-1509.
36. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 2006; 3: 995-1000.
37. Maydan M, McDonald PC, Sanghera J, Yan J, Rallis C, Pinchin S et al. Integrinlinked kinase is a functional Mn-dependent protein kinase that regulates glycogen synthase kinase-3b (GSK-3b) phosphorylation. PLoS ONE 2010; 5: e12356.
38. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9: 537-549.
39. Hui L, Bakiri L, Mairhorfer A, Schweifer N, Haslinger C, Kenner L et al. p38alpha suppresses normal and cancer cell proliferation by antagonizing the JNK-c-Jun pathway. Nat Genet 2007; 39: 741-749.
40. Dolado I, Swat A, Ajenjo N, De Vita G, Cuadrado A, Nebreda AR. p38alpha MAP kinase as a sensor of reactive oxygen species in tumorigenesis. Cancer Cell 2007; 11: 191-205.
41. Ventura JJ, Tenbaum S, Perdiguero E, Huth M, Guerra C, Barbacid M et al. p38alpha MAP kinase is essential in lung stem and progenitor cell proliferation and differentiation. Nat Genet 2007; 39: 750-758.
42. Junttila MR, Ala-Aho R, Jokilehto T, Peltonen J, Kallajoki M, Grenman R et al. p38alpha and p38delta mitogen-activated protein kinase isoforms regulate invasion and growth of head and neck squamous carcinoma cells. Oncogene 2007; 26: 5267-5279.
43. Schindler EM, Hindes A, Gribben EL, Burns CJ, Yin Y, Lin MH et al. p38delta Mitogen-activated protein kinase is essential for skin tumor development in mice. Cancer Res 2009; 69: 4648-4655.
44. Fukuda T, Chen K, Shi X, Wu C. PINCH-1 is an obligate partner of integrin-linked kinase (ILK) functioning in cell shape modulation, motility, and survival. J Biol Chem 2003; 278: 51324-51333.
45. Silva G, Cunha A, Gregoire IP, Seldon MP, Soares MP. The antiapoptotic effect of heme oxygenase-1 in endothelial cells involves the degradation of p38 alpha MAPK isoform. J Immunol 2006; 177: 1894-1903.
46. Montanez E, Wickström SA, Altstätter J, Chu H, Fässler R. Alpha-parvin controls vascular mural cell recruitment to vessel wall by regulating RhoA/ROCK signalling. EMBO J 2009; 28: 3132-3144.
47. Nakrieko KA, Welch I, Dupuis H, Bryce D, Pajak A, Arnaud RS et al. Impaired hair follicle morphogenesis and polarized keratinocyte movement upon conditional inactivation of integrin-linked kinase in the epidermis. Mol Biol Cell 2008; 19: 1462-1473.
48. New L, Jiang Y, Han J. Regulation of PRAK subcellular location by p38 MAP kinases. Mol Biol Cell 2003; 14: 2603-2616.
49. Cornford PA, Dodson AR, Parsons KF, Desmond AD, Woolfenden A, Fordham M et al. Heat shock protein expression independently predicts clinical outcome in prostate cancer. Cancer Res 2000; 60: 7099-7105.
50. Song HY, Liu YK, Feng JT, Cui JF, Dai Z, Zhang LJ et al. Proteomic analysis on metastasis-associated proteins of human hepatocellular carcinoma tissues. J Cancer Res Clin Oncol 2006; 132: 92-98.
51. Wang A, Liu X, Sheng S, Ye H, Peng T, Shi F et al. Dysregulation of heat shock protein 27 expression in oral tongue squamous cell carcinoma. BMC Cancer 2009; 9: 167-174.
52. Djakiew D, Pflug BR, Delsite R, Onoda M, Lynch JH, Arand G et al. Chemotaxis and chemokinesis of human prostate tumor cell lines in response to human prostate stromal cell secretory proteins containing a nerve growth factor-like protein. Cancer Res 1993; 53: 1416-1420.
53. Coso S, Zeng Y, Sooraj D, Williams ED. Conserved signaling through vascular endothelial growth (VEGF) receptor family members in murine lymphatic endothelial cells. Exp Cell Res 2011; 317: 2397-2407.
54. Irving Aaron T, Wang D, Vasilevski O, Latchoumanin O, Kozer N, Clayton Andrew HA et al. Regulation of actin dynamics by protein kinase R control of gelsolin enforces basal innate immune defense. Immunity 2012; 36: 795-806.