Sorafenib inhibits non-small cell lung cancer cell growth by targeting B-RAF in KRAS wild-type cells and C-RAF in KRAS mutant cells

Cancer Research

Volumn 69, Issue 16, 2009, Pages 6515-6521

  Takezawa, Ken ^a   Okamoto, Isamu ^a   Yonesaka, Kimio ^a   Hatashita, Erina ^a   Yamada, Yuki ^a   Fukuoka, Masahiro ^a   Nakagawa, Kazuhiko ^a  

^a KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; C RAF KINASE; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; RAF PROTEIN; SORAFENIB; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; ONCOGENE K RAS; PRIORITY JOURNAL; PROTEIN TARGETING; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WILD TYPE;

ANTINEOPLASTIC AGENTS; BENZENESULFONATES; CARCINOMA, NON-SMALL-CELL LUNG; CELL PROLIFERATION; CYCLIN E; DRUG DELIVERY SYSTEMS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, RAS; GENOTYPE; HUMANS; LUNG NEOPLASMS; MUTATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-RAF; PYRIDINES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 69249132057     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-1076     Document Type: Article

References (46)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96.
2. Eccles SA. Parallels in invasion and angiogenesis provide pivotal points for therapeutic intervention. Int J Dev Biol 2004;48:583-98.
3. Sridhar SS, Hedley D, Siu LL. Raf kinase as a target for anticancer therapeutics. Mol Cancer Ther 2005;4: 677-85.
4. Adjei AA, Hillman SL. A front-line window of opportunity phase II study of sorafenib in patients with advanced non-small cell lung cancer: a North Central Cancer Treatment Group Study. Proc Am Soc Clin Oncol 2007;25:S18.
5. Gatzemeier U, Fosella F. Phase II trial of singe-agent sorafenib in patients with advanced non-small cell lung carcinoma. J Clin Oncol 2006;24:7002.
6. Gutierrez SKM, Allen D, Turkbey B, et al. A phase II study of multikinase inhibitor sorafenib in patients with relapsed non-small cell lung cancer [abstract 19084]. J Clin Oncol 2008;26:S712.
7. Schiller JH, Hanna NH, Traynor AM, Carbone DP. A randomized discontinuation phase II study of sorafenib versus placebo in patients with non-small cell lung cancer who have failed at least two prior chemotherapy regimens [abstract 8014]. J Clin Oncol 2008;26:S427.
8. Rodenhuis S, van de Wetering ML, Mooi WJ, Evers SG, van Zandwijk N, Bos JL. Mutational activation of the K-ras oncogene. Apossible pathogenetic factor in adenocarcinoma of the lung. N Engl J Med 1987;317:929-35.
9. Garnett MJ, Marais R. Guilty as charged: B-RAF is a human oncogene. Cancer Cell 2004;6:313-9.
10. Panka DJ, Wang W, Atkins MB, Mier JW. The Raf inhibitor BAY 43-9006 (sorafenib) induces caspase-independent apoptosis in melanoma cells. Cancer Res 2006;66:1611-9.
11. Molhoek KR, Brautigan DL, Slingluff CL, Jr. Synergistic inhibition of human melanoma proliferation by combination treatment with B-Raf inhibitor BAY43-9006 and mTOR inhibitor rapamycin. J Transl Med 2005;3:39.
12. Lasithiotakis KG, Sinnberg TW, Schittek B, et al. Combined inhibition of MAPK and mTOR signaling inhibits growth, induces cell death, and abrogates invasive growth of melanoma cells. J Invest Dermatol 2008;128:2013-23.
13. Henderson YC, Ahn SH, Kang Y, Clayman GL. Sorafenib potently inhibits papillary thyroid carcinomas harboring RET/PTC1 rearrangement. Clin Cancer Res 2008;14:4908-14.
14. Smalley KS, Xiao M, Villanueva J, et al. CRAF inhibition induces apoptosis in melanoma cells with non-V600E BRAF mutations. Oncogene 2009;28:85-94.
15. Okabe T, Okamoto I, Tamura K, et al. Differential constitutive activation of the epidermal growth factor receptor in non-small cell lung cancer cells bearing EGFR gene mutation and amplification.CancerRes 2007;67:2046-53.
16. Wilhelm SM, Carter C, Tang L, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004;64:7099-109.
17. Strumberg D, Clark JW, Awada A, et al. Safety, pharmacokinetics, and preliminary antitumor activity of sorafenib: a review of four phase I trials in patients with advanced refractory solid tumors. Oncologist 2007;12: 426-37.
18. Wojnowski L, Stancato LF, Larner AC, Rapp UR, Zimmer A. Overlapping and specific functions of Braf and Craf-1 proto-oncogenes during mouse embryogenesis. Mech Dev 2000;91:97-104.
19. Dobashi Y. Cell cycle regulation and its aberrations in human lung carcinoma. Pathol Int 2005;55:95-105.
20. Buttitta F, Barassi F, Fresu G, et al. Mutational analysis of the HER2 gene in lung tumors from Caucasian patients: mutations are mainly present in adenocarcinomas with bronchioloalveolar features. Int J Cancer 2006;119:2586-91.
21. Suzuki M, Shigematsu H, Iizasa T, et al. Exclusive mutation in epidermal growth factor receptor gene, HER-2, and KRAS, and synchronous methylation of nonsmall cell lung cancer. Cancer 2006;106:2200-7.
22. Graziano SL, Gamble GP, Newman NB, et al. Prognostic significance of K-ras codon 12 mutations in patients with resected stage I and II non-small-cell lung cancer. J Clin Oncol 1999;17:668-75.
23. Slebos RJ, Kibbelaar RE, Dalesio O, et al. K-ras oncogene activation as a prognostic marker in adenocarcinoma of the lung. N Engl J Med 1990;323:561-5.
24. Winton T, Livingston R, Johnson D, et al. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med 2005;352:2589-97.
25. Pao W, Wang TY, Riely GJ, et al. KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2005;2:e17.
26. Massarelli E, Varella-Garcia M, Tang X, et al. KRAS mutation is an important predictor of resistance to therapy with epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. Clin Cancer Res 2007;13:2890-6.
27. Marks JL, Broderick S, Zhou Q, et al. Prognostic and therapeutic implications of EGFR and KRAS mutations in resected lung adenocarcinoma. J Thorac Oncol 2008; 3:111-6.
28. Baselga J, Rosen N. Determinants of RASistance to anti-epidermal growth factor receptor agents. J Clin Oncol 2008;26:1582-4.
29. Hao H, Muniz-Medina VM, Mehta H, et al. Contextdependent roles of mutant B-Raf signaling in melanoma and colorectal carcinoma cell growth. Mol Cancer Ther 2007;6:2220-9.
30. Jane EP, Premkumar DR, Pollack IF. Coadministration of sorafenib with rottlerin potently inhibits cell proliferation and migration in human malignant glioma cells. J Pharmacol Exp Ther 2006;319:1070-80.
31. Ambrosini G, Cheema HS, Seelman S, et al. Sorafenib inhibits growth and mitogen-activated protein kinase signaling in malignant peripheral nerve sheath cells. Mol Cancer Ther 2008;7:890-6.
32. Villanueva J, Yung Y, Walker JL, Assoian RK. ERK activity and G1 phase progression: identifying dispensable versus essential activities and primary versus secondary targets. Mol Biol Cell 2007;18:1457-63.
33. Jones SM, Kazlauskas A. Growth-factor-dependent mitogenesis requires two distinct phases of signalling. Nat Cell Biol 2001;3:165-72.
34. Yamamoto T, Ebisuya M, Ashida F, Okamoto K, Yonehara S, Nishida E. Continuous ERK activation downregulates antiproliferative genes throughout G1 phase to allow cell-cycle progression. Curr Biol 2006;16:1171-82.
35. Fassett JT, Tobolt D, Nelsen CJ, Albrecht JH, Hansen LK. The role of collagen structure in mitogen stimulation of ERK, cyclin D1 expression, and G1-S progression in rat hepatocytes. J Biol Chem 2003;278: 31691-700.
36. Smalley KS, Lioni M, Dalla Palma M, et al. Increased cyclin D1 expression can mediate BRAF inhibitor resistance in BRAF V600E-mutated melanomas. Mol Cancer Ther 2008;7:2876-83.
37. King AJ, Patrick DR, Batorsky RS, et al. Demonstration of a genetic therapeutic index for tumors expressing oncogenic BRAF by the kinase inhibitor SB-590885. Cancer Res 2006;66:11100-5.
38. Huser M, Luckett J, Chiloeches A, et al. MEK kinase activity is not necessary for Raf-1 function. EMBO J 2001;20:1940-51.
39. Mikula M, Schreiber M, Husak Z, et al. Embryonic lethality and fetal liver apoptosis in mice lacking the c-raf-1 gene. EMBO J 2001;20:1952-62.
40. Salgia R, Skarin AT. Molecular abnormalities in lung cancer. J Clin Oncol 1998;16:1207-17.
41. Montagut C, Sharma SV, Shioda T, et al. Elevated CRAF as a potential mechanism of acquired resistance to BRAF inhibition in melanoma. Cancer Res 2008;68: 4853-61.
42. Baumann B, Weber CK, Troppmair J, et al. Raf induces NF-nB by membrane shuttle kinase MEKK1, a signaling pathway critical for transformation. Proc Natl Acad Sci U S A 2000;97:4615-20.
43. Galaktionov K, Jessus C, Beach D. Raf1 interaction with Cdc25 phosphatase ties mitogenic signal transduction to cell cycle activation. Genes Dev 1995;9:1046-58.
44. Kerkhoff E, Rapp UR. Cell cycle targets of Ras/Raf signalling. Oncogene 1998;17:1457-62.
45. Hindley A, Kolch W. Extracellular signal regulated kinase (ERK)/mitogen activated protein kinase (MAPK)-independent functions of Raf kinases. J Cell Sci 2002;115: 1575-81.
46. Liu L, Cao Y, Chen C, et al. Sorafenib blocks the RAF/MEK/ERK pathway, inhibits tumor angiogenesis, and induces tumor cell apoptosis in hepatocellular carcinoma model PLC/PRF/5. Cancer Res 2006;66: 11851-8.