RAF1-MEK1-ERK/AKT axis may confer NSCLC cell lines resistance to erlotinib

International Journal of Clinical and Experimental Pathology

Volumn 6, Issue 8, 2013, Pages 1493-1504

  Xu, Zhi Hong ^a   Hang, Jun Biao ^a   Hu, Jia An ^a   Gao, Bei Li ^a  

^a SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

Author keywords

AKT; EGFR; ERK; Erlotinib; MAP2K1; Microarray; Non small cell lung cancer; NSCLC; RAF1

Indexed keywords

ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; MAP2K1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PROTEIN KINASE B; QUINAZOLINE DERIVATIVE; RAF PROTEIN; TRANSCRIPTOME; TUMOR MARKER;

AKT; ARTICLE; CELL SURVIVAL; DNA MICROARRAY; DRUG EFFECT; DRUG RESISTANCE; EGFR; ERK; GENETICS; HUMAN; LUNG NON SMALL CELL CANCER; LUNG TUMOR; MAP2K1; METABOLISM; MICROARRAY; NON-SMALL CELL LUNG CANCER; NSCLC; PHYSIOLOGY; RAF1; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; WESTERN BLOTTING;

AKT; EGFR; ERK; ERLOTINIB; MAP2K1; MICROARRAY; NON-SMALL CELL LUNG CANCER; NSCLC; RAF1;

ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; HUMANS; LUNG NEOPLASMS; MAP KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-RAF; QUINAZOLINES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSCRIPTOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84882950933     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (41)

1. Brugger W, Triller N, Blasinska-Morawiec M, Curescu S, Sakalauskas R, Manikhas GM, Mazieres J, Whittom R, Ward C, Mayne K, Trunzer K and Cappuzzo F. Prospective molecular marker analyses of EGFR and KRAS from a randomized, placebo-controlled study of erlotinib maintenance therapy in advanced non-small-cell lung cancer. J Clin Oncol 2011; 29: 4113-4120.
2. Janne PA, Engelman JA, and Johnson BE. Epidermal growth factor receptor mutations in non-small-cell lung cancer: implications for treatment, and tumor biology. J Clin Oncol 2005; 23: 3227-3234.
3. Ji H, Li D, Chen L, Shimamura T, Kobayashi S, McNamara K, Mahmood U, Mitchell A, Sun Y, Al-Hashem R, Chirieac LR, Padera R, Bronson RT, Kim W, Janne PA, Shapiro GI, Tenen D, Johnson BE, Weissleder R, Sharpless NE, and Wong KK. The impact of human EGFR kinase domain mutations on lung tumorigenesis, and in vivo sensitivity to EGFR-targeted therapies. Cancer Cell 2006; 9: 485-495.
4. Zhou C, Wu YL, Chen G, Feng J, Liu XQ, Wang C, Zhang S, Wang J, Zhou S, Ren S, Lu S, Zhang L, Hu C, Hu C, Luo Y, Chen L, Ye M, Huang J, Zhi X, Zhang Y, Xiu Q, Ma J, Zhang L, and You C. Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study. Lancet Oncol 2011; 12: 735-742.
5. Rosell R, Carcereny E, Gervais R, Vergnenegre A, Massuti B, Felip E, Palmero R, Garcia-Gomez R, Pallares C, Sanchez JM, Porta R, Cobo M, Garrido P, Longo F, Moran T, Insa A, De Marinis F, Corre R, Bover I, Illiano A, Dansin E, De Castro J, Milella M, Reguart N, Altavilla G, Jimenez U, Provencio M, Moreno MA, Terrasa J, Munoz-Langa J, Valdivia J, Isla D, Domine M, Molinier O, Mazieres J, Baize N, Garcia-Campelo R, Robinet G, Rodriguez-Abreu D, Lopez-Vivanco G, Gebbia V, Ferrera-Delgado L, Bombaron P, Bernabe R, Bearz A, Artal A, Cortesi E, Rolfo C, Sanchez-Ronco M, Drozdowskyj A, Queralt C, De Aguirre I, Ramirez JL, Sanchez JJ, Molina MA, Taron M, Paz-Ares L; Spanish Lung Cancer Group in collaboration with Groupe Francais De Pneumo-Cancérologie, and Associazione Italiana Oncologia T. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol 2012; 13: 239-246.
6. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, Kris MG, and Varmus H. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005; 2: e73.
7. Shigematsu H, Lin L, Takahashi T, Nomura M, Suzuki M, Wistuba II, Fong KM, Lee H, Toyooka S, Shimizu N, Fujisawa T, Feng Z, Roth JA, Herz J, Minna JD, and Gazdar AF. Clinical, and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst 2005; 97: 339-346.
8. Sharma SV, Bell DW, Settleman J, and Haber DA. Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 2007; 7: 169-181.
9. Engelman JA, and Janne PA. Factors predicting response to EGFR tyrosine kinase inhibitors. Semin Respir Crit Care Med 2005; 26: 314-322.
10. Giaccone G. Epidermal growth factor receptor inhibitors in the treatment of non-small-cell lung cancer. J Clin Oncol 2005; 23: 3235-3242.
11. Wang SE, Narasanna A, Perez-Torres M, Xiang B, Wu FY, Yang S, Carpenter G, Gazdar AF, Muthuswamy SK, and Arteaga CL. HER2 kinase domain mutation results in constitutive phosphorylation, and activation of HER2, and EGFR, and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell 2006; 10: 25-38.
12. Prahallad A, Sun C, Huang S, Di Nicolantonio F, Salazar R, Zecchin D, Beijersbergen RL, Bardelli A, and Bernards R. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 2012; 483: 100-103.
13. Gusenbauer S, Vlaicu P, and Ullrich A. HGF induces novel EGFR functions involved in resistance formation to tyrosine kinase inhibitors. Oncogene 2012; doi: 10.1038/onc.2012.396. [Epub ahead of print].
14. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, Kosaka T, Holmes AJ, Rogers AM, Cappuzzo F, Mok T, Lee C, Johnson BE, Cantley LC, and Janne PA. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-1043.
15. Pao W, and Girard N. New driver mutations in non-small-cell lung cancer. Lancet Oncol 2011; 12: 175-180.
16. Cheng L, Alexander RE, Maclennan GT, Cummings OW, Montironi R, Lopez-Beltran A, Cramer HM, Davidson DD, and Zhang S. Molecular pathology of lung cancer: key to personalized medicine. Mod Pathol 2012; 25: 347-369.
17. Yauch RL, Januario T, Eberhard DA, Cavet G, Zhu W, Fu L, Pham TQ, Soriano R, Stinson J, Seshagiri S, Modrusan Z, Lin CY, O'Neill V, and Amler LC. Epithelial versus mesenchymal phenotype determines in vitro sensitivity, and predicts clinical activity of erlotinib in lung cancer patients. Clin Cancer Res 2005; 11: 8686-8698.
18. Sos ML, Michel K, Zander T, Weiss J, Frommolt P, Peifer M, Li D, Ullrich R, Koker M, Fischer F, Shimamura T, Rauh D, Mermel C, Fischer S, Stuckrath I, Heynck S, Beroukhim R, Lin W, Winckler W, Shah K, LaFramboise T, Moriarty WF, Hanna M, Tolosi L, Rahnenfuhrer J, Verhaak R, Chiang D, Getz G, Hellmich M, Wolf J, Girard L, Peyton M, Weir BA, Chen TH, Greulich H, Barretina J, Shapiro GI, Garraway LA, Gazdar AF, Minna JD, Meyerson M, Wong KK, and Thomas RK. Predicting drug susceptibility of non-small cell lung cancers based on genetic lesions. J Clin Invest 2009; 119: 1727-1740.
19. Yao Z, Fenoglio S, Gao DC, Camiolo M, Stiles B, Lindsted T, Schlederer M, Johns C, Altorki N, Mittal V, Kenner L, and Sordella R. TGF-beta IL-6 axis mediates selective, and adaptive mechanisms of resistance to molecular targeted therapy in lung cancer. Proc Natl Acad Sci USA 2010; 107: 15535-15540.
20. Frederick BA, Helfrich BA, Coldren CD, Zheng D, Chan D, Bunn PA Jr, and Raben D. Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head, and neck squamous cell carcinoma, and non-small cell lung carcinoma. Mol Cancer Ther 2007; 6: 1683-1691.
21. Balko JM, Potti A, Saunders C, Stromberg A, Haura EB, and Black EP. Gene expression patterns that predict sensitivity to epidermal growth factor receptor tyrosine kinase inhibitors in lung cancer cell lines, and human lung tumors. BMC Genomics 2006; 7: 289.
22. Yonesaka K, Zejnullahu K, Lindeman N, Homes AJ, Jackman DM, Zhao F, Rogers AM, Johnson BE, and Janne PA. Autocrine production of amphiregulin predicts sensitivity to both gefitinib, and cetuximab in EGFR wild-type cancers. Clin Cancer Res 2008; 14: 6963-6973.
23. Petty WJ, Voelzke WR, Urbanic JJ, Varela VA, Waller LL, Swift CB, Graham RM, Memoli VA, and Dragnev KH. High cyclin D3 expression confers erlotinib resistance in aerodigestive tract cancer. Lung Cancer 2011; 74: 384-391.
24. Tusher VG, Tibshirani R, and Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001; 98: 5116-5121.
25. McDermott U, Sharma SV, Dowell L, Greninger P, Montagut C, Lamb J, Archibald H, Raudales R, Tam A, Lee D, Rothenberg SM, Supko JG, Sordella R, Ulkus LE, Iafrate AJ, Maheswaran S, Njauw CN, Tsao H, Drew L, Hanke JH, Ma XJ, Erlander MG, Gray NS, Haber DA, and Settleman J. Identification of genotype-correlated sensitivity to selective kinase inhibitors by using high-throughput tumor cell line profiling. Proc Natl Acad Sci USA 2007; 104: 19936-19941.
26. Xuan YT, Guo Y, Zhu Y, Wang OL, Rokosh G, Messing RO, and Bolli R. Role of the protein kinase C-epsilon-Raf-1-MEK-1/2-p44/42 MAPK signaling cascade in the activation of signal transducers, and activators of transcription 1, and 3, and induction of cyclooxygenase-2 after ischemic preconditioning. Circulation 2005; 112: 1971-1978.
27. Li D, Lin HH, McMahon M, Ma H, and Ann DK. Oncogenic raf-1 induces the expression of non-histone chromosomal architectural protein HMGI-C via a p44/p42 mitogen-activated protein kinase-dependent pathway in salivary epithelial cells. J Biol Chem 1997; 272: 25062-25070.
28. Goh LL, and Manser E. The RhoA GEF Syx is a target of Rnd3, and regulated via a Raf1-like ubiquitin-related domain. PLoS One 2010; 5: e12409.
29. Cardoso AP, Pinto ML, Pinto AT, Oliveira MI, Pinto MT, Goncalves R, Relvas JB, Figueiredo C, Seruca R, Mantovani A, Mareel M, Barbosa MA, and Oliveira MJ. Macrophages stimulate gastric, and colorectal cancer invasion through EGFY Y, c-Src, Erk1/2, and Akt phosphorylation, and smallGTPase activity. Oncogene 2013; doi:10.1038/onc.2013.154. [Epub ahead of print].
30. Humtsoe JO, and Kramer RH. Differential epidermal growth factor receptor signaling regulates anchorage-independent growth by modulation of the PI3K/AKT pathway. Oncogene 2010; 29: 1214-1226.
31. Bivona TG, Hieronymus H, Parker J, Chang K, Taron M, Rosell R, Moonsamy P, Dahlman K, Miller VA, Costa C, Hannon G, and Sawyers CL. FAS, and NF-kappaB signalling modulate dependence of lung cancers on mutant EGFR. Nature 2011; 471: 523-526.
32. Faber AC, Li D, Song Y, Liang MC, Yeap BY, Bronson RT, Lifshits E, Chen Z, Maira SM, Garcia-Echeverria C, Wong KK, and Engelman JA. Differential induction of apoptosis in HER2, and EGFR addicted cancers following PI3K inhibition. Proc Natl Acad Sci USA 2009; 106: 19503-19508.
33. Sos ML, Koker M, Weir BA, Heynck S, Rabinovsky R, Zander T, Seeger JM, Weiss J, Fischer F, Frommolt P, Michel K, Peifer M, Mermel C, Girard L, Peyton M, Gazdar AF, Minna JD, Garraway LA, Kashkar H, Pao W, Meyerson M, and Thomas RK. PTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt, and EGFR. Cancer Res 2009; 69: 3256-3261.
34. Wang YC, Kulp SK, Wang D, Yang CC, Sargeant AM, Hung JH, Kashida Y, Yamaguchi M, Chang GD, and Chen CS. Targeting endoplasmic reticulum stress, and Akt with OSU-03012, and gefitinib or erlotinib to overcome resistance to epidermal growth factor receptor inhibitors. Cancer Res 2008; 68: 2820-2830.
35. Eiseler T, Kohler C, Nimmagadda SC, Jamali A, Funk N, Joodi G, Storz P, and Seufferlein T. Protein kinase D1 mediates anchorage-dependent, and -independent growth of tumor cells via the zinc finger transcription factor Snail1. J Biol Chem 2012; 287: 32367-32380.
36. White GE, Tan TC, John AE, Whatling C, McPheat WL, and Greaves DR. Fractalkine has anti-apoptotic, and proliferative effects on human vascular smooth muscle cells via epidermal growth factor receptor signalling. Cardiovasc Res 2010; 85: 825-835.
37. Tardaguila M, Mira E, Garcia-Cabezas MA, Feijoo AM, Quintela-Fandino M, Azcoitia I, Lira SA, and Manes S. CX3CL1 promotes breast cancer via transactivation of the EGF pathway. Cancer Res 2013; [Epub ahead of print].
38. Volin MV, Huynh N, Klosowska K, Chong KK, and Woods JM. Fractalkine is a novel chemoattractant for rheumatoid arthritis fibroblast-like synoviocyte signaling through MAP kinases, and Akt. Arthritis Rheum 2007; 56: 2512-2522.
39. Ferretti E, Bertolotto M, Deaglio S, Tripodo C, Ribatti D, Audrito V, Blengio F, Matis S, Zupo S, Rossi D, Ottonello L, Gaidano G, Malavasi F, Pistoia V, and Corcione A. A novel role of the CX3CR1/CX3CL1 system in the cross-talk between chronic lymphocytic leukemia cells, and tumor microenvironment. Leukemia 2011; 25: 1268-1277.
40. Jarboe JS, Dutta S, Velu SE, and Willey CD. Mini-Review: Bmx Kinase Inhibitors for Cancer Therapy. Recent Pat Anticancer Drug Discov 2012; 8: 228-38.
41. Hur W, Velentza A, Kim S, Flatauer L, Jiang X, Valente D, Mason DE, Suzuki M, Larson B, Zhang J, Zagorska A, Didonato M, Nagle A, Warmuth M, Balk SP, Peters EC, and Gray NS. Clinical stage EGFR inhibitors irreversibly alkylate Bmx kinase. Bioorg Med Chem Lett 2008; 18: 5916-5919.