Inhibition of c-Src expression and activation in malignant pleural mesothelioma tissues leads to apoptosis, cell cycle arrest, and decreased migration and invasion

Molecular Cancer Therapeutics

Volumn 6, Issue 7, 2007, Pages 1962-1972

  Tsao, Anne S ^a   He, Dandan ^a   Saigal, Babita ^a   Liu, Suyu ^a   Lee, J Jack ^a   Bakkannagari, Srinivasa ^a   Ordonez, Nelson G ^a   Waun, Ki Hong ^a   Wistuba, Ignacio ^a   Johnson, Faye M ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DASATINIB; PROTEIN KINASE P60; PROTEIN TYROSINE KINASE INHIBITOR;

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CASE REPORT; CELL CYCLE ARREST; CELL INVASION; CELL LINE; CELL MEMBRANE; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; DOWNSTREAM PROCESSING; DRUG CYTOTOXICITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; METASTASIS; ONCOGENE SRC; PLEURA MESOTHELIOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL;

APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME ACTIVATION; EXONS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INHIBITORY CONCENTRATION 50; MALE; MESOTHELIOMA; MUTATION; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM STAGING; PLEURAL NEOPLASMS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS PP60(C-SRC); PYRIMIDINES; SIGNAL TRANSDUCTION; THIAZOLES;

EID: 34447316429     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-07-0052     Document Type: Article

References (66)

1. Herndon JE, Green MR, Chahinian AP, Corson JM, Suzuki Y, Vogelzang NJ. Factors predictive of survival among 337 patients with mesothelioma treated between 1984 and 1994 by the Cancer and Leukemia Group B. Chest 1998;113:723-31.
2. Rusch VW, Rosenzweig K, Venkatraman E, et al. A phase II trial of surgical resection and adjuvant high-dose hemithoracic radiation for malignant pleural mesothelioma. J Thorac Cardiovasc Surg 2001;122:788-95.
3. Vogelzang NJ, Rusthoven JJ, Symanowski J, et al. Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. J Clin Oncol 2003;21:2636-44.
4. Irby RB, Yeatman TJ. Role of Src expression and activation in human cancer. Oncogene 2000;19:5636-42.
5. Levin VA. Basis and importance of Src as a target in cancer. Cancer Treat Res 2004;119:89-119.
6. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54.
7. Thompson EW, Newgreen DF, Tarin D. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Cancer Res 2005;65:5991-5; discussion 5995.
8. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 1999;4:915-24.
9. Yezhelyev MV, Koehl G, Guba M, et al. Inhibition of SRC tyrosine kinase as treatment for human pancreatic cancer growing orthotopically in nude mice. Clin Cancer Res 2004;10:8028-36.
10. Summy JM, Trevino JG, Lesslie DP, et al. AP23846, a novel and highly potent Src family kinase inhibitor, reduces vascular endothelial growth factor and interleukin-8 expression in human solid tumor cell lines and abrogates downstream angiogenic processes. Mol Cancer Ther 2005;4:1900-11.
11. Trevino JG, Summy JM, Gray MJ, et al. Expression and activity of SRC regulate interleukin-8 expression in pancreatic adenocarcinoma cells: implications for angiogenesis. Cancer Res 2005;65:7214-22.
12. Gray MJ, Zhang J, Ellis LM, et al. HIF-1α, STAT3, CBP/p300 and Ref-1/APE are components of a transcriptional complex that regulates Src-dependent hypoxia-induced expression of VEGF in pancreatic and prostate carcinomas. Oncogene 2005;24:3110-20.
13. Summy JM, Trevino JG, Baker CH, Gallick GE. c-Src regulates constitutive and EGF-mediated VEGF expression in pancreatic tumor cells through activation of phosphatidyl inositol-3 kinase and p38 MAPK. Pancreas 2005;31:263-74.
14. Trevino JG, Summy JM, Lesslie DP, et al. Inhibition of SRC expression and activity inhibits tumor progression and metastasis of human pancreatic adenocarcinoma cells in an orthotopic nude mouse model. Am J Pathol 2006;168:962-72.
15. Johnson FM, Gallick GE. Src Family Nonreceptor Tyrosine Kinases as Molecular Targets for Cancer Therapy. Curr Med Chem. In press 2007.
16. Turkson J, Bowman T, Garcia R, Caldenhoven E, De Groot RP, Jove R. Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol Cell Biol 1998;18:2545-52.
17. Karni R, Jove R, Levitzki A. Inhibition of pp60c-Src reduces Bcl-XL expression and reverses the transformed phenotype of cells overexpressing EGF and HER-2 receptors. Oncogene 1999;18:4654-62.
18. Yeatman TJ. A renaissance for SRC. Nat Rev Cancer 2004;4:470-80.
19. Tan YX, Wang HT, Zhang P, et al. c-Src activating mutation analysis in Chinese patients with colorectal cancer. World J Gastroenterol 2005;11:2351-3.
20. Irby RB, Mao W, Coppola D, et al. Activating SRC mutation in a subset of advanced human colon cancers. Nat Genet 1999;21:187-90.
21. Laghi L, Bianchi P, Orbetegli O, Gennari L, Roncalli M, Malesci A. Lack of mutation at codon 531 of SRC in advanced colorectal cancers from Italian patients. Br J Cancer 2001;84:196-8.
22. Ohta Y, Shridhar V, Bright RK, et al. VEGF and VEGF type C play an important role in angiogenesis and lymphangiogenesis in human malignant mesothelioma tumours. Br J Cancer 1999;81:54-61.
23. Kumar-Singh S, Vermeulen PB, Weyler J, et al. Evaluation of tumour angiogenesis as a prognostic marker in malignant mesothelioma. J Pathol 1997;182:211-6.
24. Langerak AW, De Laat PA, Van Der Linden-Van Beurden CA, et al. Expression of platelet-derived growth factor (PDGF) and PDGF receptors in human malignant mesothelioma in vitro and in vivo. J Pathol 1996;178:151-60.
25. Konig JE, Tolnay E, Wiethege T, Muller KM. Expression of vascular endothelial growth factor in diffuse malignant pleural mesothelioma. Virchows Arch 1999;435:8-12.
26. Strizzi L, Catalano A, Vianale G, et al. Vascular endothelial growth factor is an autocrine growth factor in human malignant mesothelioma. J Pathol 2001;193:468-75.
27. Kumar-Singh S, Weyler J, Martin MJ, Vermeulen PB, Van Marck E. Angiogenic cytokines in mesothelioma: a study of VEGF, FGF-1 and -2, and TGF h expression. J Pathol 1999;189:72-8.
28. Zebrowski BK, Yano S, Liu W, et al. Vascular endothelial growth factor levels and induction of permeability in malignant pleural effusions. Clin Cancer Res 1999;5:3364-8.
29. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983;219:983-5.
30. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-76.
31. Kindler HL. Movingbeyond chemotherapy: novel cytostatic agents for malignant mesothelioma. Lung Cancer 2004;45 Suppl 1:S125-7.
32. England JM, Panella MJ, Ewert DL, Halpern MS. Induction of a diffuse mesothelioma in chickens by intraperitoneal inoculation of v-src DNA. Virology 1991;182:423-9.
33. Miura Y, Nishimura Y, Katsuyama H, et al. Involvement of IL-10 and Bcl-2 in resistance against an asbestos-induced apoptosis of T cells. Apoptosis 2006;11:1825-35.
34. Poulikakos PI, Xiao GH, Gallagher R, Jablonski S, Jhanwar SC, Testa JR. Re-expression of the tumor suppressor NF2/merlin inhibits invasiveness in mesothelioma cells and negatively regulates FAK. Oncogene 2006; 25:5960-8.
35. Lombardo LJ, Lee FY, Chen P, et al. Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)- piperazin-1-yl)-2-methylpyrimidin-4-ylamino) thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 2004;47:6658-61.
36. Talpaz M, Shah NP, Kantarjian H, et al. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med 2006;354:2531-41.
37. Mujoo K, Maneval DC, Anderson SC, Gutterman JU. Adenoviral-mediated p53 tumor suppressor gene therapy of human ovarian carcinoma. Oncogene 1996;12:1617-23.
38. 1 transit following brief starvation for serum factors. Exp Cell Res 1984;152:459-62.
39. Kong-Beltran M, Stamos J, Wickramasinghe D. The Sema domain of Met is necessary for receptor dimerization and activation. Cancer Cell 2004;6:75-84.
40. Michieli P, Mazzone M, Basilico C, et al. Targeting the tumor and its microenvironment by a dual-function decoy Met receptor. Cancer Cell 2004;6:61-73.
41. Beaudry P, Force J, Naumov GN, et al. Differential effects of vascular endothelial growth factor receptor-2 inhibitor ZD6474 on circulating endothelial progenitors and mature circulating endothelial cells: implications for use as a surrogate marker of antiangiogenic activity. Clin Cancer Res 2005;11:3514-22.
42. Albini A, Iwamoto Y, Kleinman HK, et al. A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res 1987;47:3239-45.
43. Zhang J, Kalyankrishna S, Wislex M, et al. Src-family kinases are activated in non-small cell lung cancer and promote the survival of epidermal growth factor receptor-dependent cell lines. Am J Pathol 2007;170:1-11.
44. Johnson FM, Saigal B, Talpaz M, Donato NJ. Dasatinib (BMS-354825) tyrosine kinase inhibitor suppresses invasion and induces cell cycle arrest and apoptosis of head and neck squamous cell carcinoma and non-small cell lung cancer cells. Clin Cancer Res 2005;11:6924-32.
45. Nam S, Kim D, Cheng JQ, et al. Action of the Src family kinase inhibitor, dasatinib (BMS-354825), on human prostate cancer cells. Cancer Res 2005;65:9185-9.
46. Wakeling AE, Guy SP, Woodburn JR, et al. ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res 2002;62:5749-54.
47. Janmaat ML, Kruyt FA, Rodriguez JA, Giaccone G. Response to epidermal growth factor receptor inhibitors in non-small cell lung cancer cells: limited antiproliferative effects and absence of apoptosis associated with persistent activity of extracellular signal-regulated kinase or Akt kinase pathways. Clin Cancer Res 2003;9:2316-26.
48. Le Chevalier T, Lynch T. Adjuvant treatment of lung cancer: current status and potential applications of new regimens. Lung Cancer 2004;46 Suppl 2:S33-9.
49. Paez JG, Janne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500.
50. Massarelli E, Onn A, Herbst R, et al. The time of tissue processing for human surgical specimens influences the level of epidermal growth factor receptor phosphorylation [Abstract 430]. In: Proceedings of the American Association of Cancer Research; 2005.
51. Stevens C, Rice D, Forster K, et al. Extrapleural pneumonectomy followed by IMRT: results of a phase I/II study [abstract 7178]. In: Proceedings of the American Society of Clinical Oncology; 2005.
52. Allen A, Den R, Wong J, et al. The influence of radiotherapy technique and dose on the patterns of failure for mesothelioma patients following extrapleural pneumonectomy [abstract #7094]. ASCO Annual Meeting Proceedings. J Clin Oncol 2006;24:7094.
53. Criscuoli ML, Nguyen M, Eliceiri BP. Tumor metastasis but not tumor growth is dependent on Src-mediated vascular permeability. Blood 2005;105:1508-14.
54. Masood R, Kundra A, Zhu S, et al. Malignant mesothelioma growth inhibition by agents that target the VEGF and VEGF-C autocrine loops. Int J Cancer 2003;104:603-10.
55. Roberts F, Harper CM, Downie I, Burnett RA. Immunohistochemical analysis still has a limited role in the diagnosis of malignant mesothelioma. A study of thirteen antibodies. Am J Clin Pathol 2001;116:253-62.
56. Nowak AK, Lake RA, Kindler HL, Robinson BW. New approaches for mesothelioma: biologics, vaccines, gene therapy, and other novel agents. Semin Oncol 2002;29:82-96.
57. Gerwin BI, Lechner JF, Reddel RR, et al. Comparison of production of transforming growth factor-β and platelet-derived growth factor by normal human mesothelial cells and mesothelioma cell lines. Cancer Res 1987;47:6180-4.
58. Dorai T, Kobayashi H, Holland JF, Ohnuma T. Modulation of platelet-derived growth factor-β mRNA expression and cell growth in a human mesothelioma cell line by a hammerhead ribozyme. Mol Pharmacol 1994;46:437-44.
59. Mutsaers SE, McAnulty RJ, Laurent GJ, Versnel MA, Whitaker D, Papadimitriou JM. Cytokine regulation of mesothelial cell proliferation in vitro and in vivo. Eur J Cell Biol 1997;72:24-9.
60. Dodelet VC, Pasquale EB. Eph receptors and ephrin ligands: embryogenesis to tumorigenesis. Oncogene 2000;19:5614-9.
61. Pandey A, Shao H, Marks RM, Polverini PJ, Dixit VM. Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-α-induced angiogenesis. Science 1995;268:567-9.
62. Miao H, Burnett E, Kinch M, Simon E, Wang B. Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat Cell Biol 2000;2:62-9.
63. Andres AC, Reid HH, Zurcher G, Blaschke RJ, Albrecht D, Ziemiecki A. Expression of two novel eph-related receptor protein tyrosine kinases in mammary gland development and carcinogenesis. Oncogene 1994;9:1461-7.
64. Gerety SS, Wang HU, Chen ZF, Anderson DJ. Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell 1999;4:403-14.
65. Xia G, Kumar SR, Masood R, et al. Up-regulation of EphB4 in mesothelioma and its biological significance. Clin Cancer Res 2005;11:4305-15.
66. Catalano A, Rodilossi S, Rippo MR, Caprari P, Procopio A. Induction of stem cell factor/c-Kit/slugsig nal transduction in multidrug-resistant malignant mesothelioma cells. J Biol Chem 2004;279:46706-14.