Mechanisms of resistance to reversible inhibitors of EGFR tyrosine kinase in non-small cell lung cancer

Wspolczesna Onkologia

Volumn 16, Issue 5, 2012, Pages 401-406

  Krawczyk, Paweł ^a   Mlak, Radosław ^a   Powrózek, Tomasz ^a   Nicoś, Marcin ^a   Kowalski, Dariusz M ^b   Wojas Krawczyk, Kamila ^a   Milanowski, Janusz ^a,c  

^a MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^b INSTITUTE OF ONCOLOGY   (Poland)

^c INSTITUTE OF AGRICULTURAL MEDICINE   (Poland)

Author keywords

EGFR gene mutations; Epidermal growth factor receptor; Resistance mechanisms; Tyrosine kinase inhibitors

Indexed keywords

AFATINIB; CANERTINIB; CETUXIMAB; CRIZOTINIB; DACOMITINIB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; EVEROLIMUS; FIGITUMUMAB; GEFITINIB; KERATINIB; LINSITINIB; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; NERATINIB; NEW DRUG; PANITUMUMAB; PELITINIB; PF 00299802; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RIDAFOROLIMUS; SCATTER FACTOR RECEPTOR; SOMATOMEDIN C RECEPTOR; TEMSIROLIMUS; TIVANTINIB; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER SURVIVAL; COLORECTAL CANCER; COPY NUMBER VARIATION; DIMERIZATION; DISORDERS OF CARBOHYDRATE METABOLISM; DISORDERS OF LIPID METABOLISM; DRUG EFFICACY; DRUG INDICATION; DRUG MECHANISM; DRUG SAFETY; EXON; GENE AMPLIFICATION; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; HEAD AND NECK CANCER; HUMAN; INDEL MUTATION; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; MUTATIONAL ANALYSIS; NUCLEIC ACID BASE SUBSTITUTION; ONCOGENE K RAS; PHARMACOGENOMICS; PROGRESSION FREE SURVIVAL; PROTEIN DOMAIN; RECEPTOR GENE; REVIEW; SIGNAL TRANSDUCTION; SMOKING; TREATMENT OUTCOME; TREATMENT PLANNING; TREATMENT RESPONSE; UNSPECIFIED SIDE EFFECT;

EID: 84870218433     PISSN: 14282526     EISSN: None     Source Type: Journal    
DOI: 10.5114/wo.2012.31768     Document Type: Review

References (57)

1. Jemal A, Bray F, Centem MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Jassem J, Biernat W, Drosik K, et al. Uaktualnione zalecenia dotycza̧ce systemowego leczenia niedrobnokomórkowego raka płuca i złośliwego miȩdzybłoniaka opłucnej. Pneumonol Alergol Pol 2010; 78: 418-31.
3. NSCLC Meta-Analysis Collaborative Group. Chemotherapy in addition to supportive care improves survival in advanced non-small-cell lung cancer. A systemic review and meta-analysis of individual patient data from 16 randomized controlled trials. J Clin Oncol 2008; 26: 4617-25.
4. Yun CH, Boggon TJ, Li Y, et al. Structures of lung cancer-derived EGFR mutants and inhibitor complexes: Mechanism of activation and insights into differential inhibitor sensitivity. Cancer Cell 2007; 11: 217-27. (Pubitemid 46349842)
5. Lynch TJ, Bell DW, Sordella R, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004; 350: 2129-39. (Pubitemid 38637993)
6. Shigematsu H, Lin L, Takahashi T, et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancer. J Natl Cancer Inst 2005; 97: 339-46. (Pubitemid 40425952)
7. Paez JG, Janne PA, Lee JC, et al. EGRF mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304: 1497-500. (Pubitemid 38720929)
8. Pao W, Miller V, Zakowski M, et al. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A 2004; 101: 13306-11. (Pubitemid 39209661)
9. Salgia R, Hensing T, Campbell N, Salama AK, Maitland M, Hoffman P, Villaflor V, Vokes EE. Personalized treatment of lung cancer. Semin Oncol 2011; 38: 274-83.
10. Shepherd FA, Rodrigues-Pereira J, Ciuleanu T, et al. National Cancer Institute of Canada Clinical Trials Group. Erlotinib in previously treated nonsmall-cell lung cancer. N Engl J Med 2005; 353: 123-32.
11. Douillard JY, Shepherd FA, Hirsh V, et al. Molecular predictors of outcome with gefitinib and docetaxel in previously treated non-small-cell lung cancer: data from the randomized phase III INTEREST trial. J Clin Oncol 2010; 28: 744-52.
12. Mok TS Wu YL, Thongprasert S, et al. Gefitinib or carboplatinpaclitaxel in pulmonary adenocarcinoma. N Engl J Med 2010; 361: 947-57.
13. Mitsudomi T, Morita S, Yatabe Y, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomized phase 3 trial. Lancet Oncol 2010; 11: 121-8.
14. Zhou C, Wu YL, Chen G, et al. Erlotinib versus chemotherapy as firstline 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: 735-42.
15. Rossel R, Gervias V, Vergnenegre A. Erlotinib vs chemotherapy (CT) in advanced non-small-cell lung cancer (NSCLC) patients (p) with epidermal growth factor receptor (EGFR) activating mutations: interim results of the European Tarceva vs Chemotherapy (EURTAC) phase III randomized trial. J Clin Oncol 2011; 29 (suppl.): abstr. 7503.
16. Paz-Ares L, Soulieres D, Melezinek I, et al. Clinical outcomes in non-small-cell lung cancer patients with EGFR mutations: pooled analysis. Cell Mol Med 2010; 14: 51-69.
17. Kosaka T, Yamaki E, Mogi A, Kuwano H. Mechanisms of resistance to EGFR TKIs and development of a new generation of drugs in non-small-cell lung cancer. J Biomed Biotechnol 2011; 2011: 165214.
18. Daub H, Specht K, Ullrich A. Strategies to overcome resistance to targeted protein kinase inhibitors. Nat Rev Cancer 2004; 3: 1001-10. (Pubitemid 39642363)
19. Avizienyte E, Ward RA, Garner AP. Comparison of the EGFR resistance mutation profiles generated by EGFR targeted tyrosine kinase inhibitors and the impact of drug combinations. Biochem J 2008; 415: 197-206.
20. Pao W, Miller VA, Politi KA, Riely GJ, Riely GJ, Somwar R, Zakowski MF, Kris MG, Varmus H. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Medicine 2005; 23: 225-35.
21. Maheswaran S, Sequist LV, Nagrath S, et al. Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 2008; 359: 366-77.
22. Doebele RC, Oton AB, Peled N, et al. New strategies to overcome limitations of reversible EGFR tyrosine kinase inhibitor therapy in non-small cell lung cancer. Lung Cancer 2010; 69: 1-12.
23. Kwak EL, Sordella R, Bell DW, et al. Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. Proc Natl Acad Sci U S A 2005; 102: 7665-70.
24. Hirsh V. Afatinib (BIBW 2992) development in non-small-cell lung cancer. Future Oncol 2011; 7: 817-25.
25. Li D, Ambrogio L, Shimamura T. BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene 2009; 27: 4702-11.
26. Zhou W, Ercan D, Chen L, et al. Novel mutant-selective EGFR kinase inhibitors against EGFR T790M. Nature 2009; 462: 1070-4.
27. Ellison G, Donald E, McWalter G, et al. A comparison of ARMS and DNA sequencing for mutation analysis in clinical biopsy samples. J Exp Clin Cancer Res 2010; 29: 132-9.
28. Inukai M, Toyooka S, Ito S, et al. Presence of epidermal growth factor receptor gene T790M mutation as a minor clone in non-small-cell lung cancer. Cancer Res 2006; 66: 7854-8. (Pubitemid 44299146)
29. Wu JY, Wu SG, Yang CH, et al. Lung cancer with epidermal growth factor receptor eon 20 mutations is associated with poor gefitinib treatment response. Clin Cancer Res 2008; 14: 4877-82.
30. Yun CH, Mengwasser KE, Toms AV, et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci U S A 2008; 105: 2070-5. (Pubitemid 351439466)
31. Ma C, Wei S, Song Y. T790M and acquired resistance of EGFR TKI: a literature review of clinical reports. J Thorac Dis 2011; 3: 10-8.
32. Bean J, Riely GJ, Balak MN, et al. Acquired resistance to epidermal growth factor receptor kinase inhibitors associated with a novel T854A mutation in a patient with EGFR-mutant lung adenocarcinoma. Clin Cancer Res 2008; 14: 7519-25.
33. Asahina H, Yamazaki K, Kinoshita I, Yokouchi H, Dosaka-Akita H, Nishimura M. Non-responsiveness to gefitinib in a patient with lung adenocarcinoma having rare EGFR mutations S768I and V769L. Lung Cancer 2006; 54: 419-22. (Pubitemid 44634147)
34. Balak MN, Gong Y, Riely GJ, et al. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinoma with acquired resistance to kinase inhibitors. Clin Cancer Res 2006; 12: 6494-501. (Pubitemid 44799723)
35. asuda H, Kobayashi S, Costa DB. EGFR exon 20 insertion mutations in non-small-cell lung cancer: preclinical data and clinical implications. Lancet Oncol 2012; 13: e23-31.
36. Harada T, Lopez-Chavez A, Xi L, Raffeld M, Wang Y, Giaccone G. Characterization of epidermal growth factor receptor mutations in non-small-cell lung cancer patients of African-American ancestry. Oncogene 2011; 30: 1744-52.
37. Schneider C, Schott-von Römer K, Gütz S i wsp. Biomarker analysis from TRUST, a trial of erlotinib in non-small cell lung cancer (NSCLC) J Clin Oncol 2007; 25 (suppl.): abstr. 7674.
38. Linardou H, Dahabreh IJ, Kanaloupiti D, Siannis F, Bafaloukos D, Kosmidis P, Papadimitriou CA, Murray S. Assessment of somatic k-RAS mutations as a mechanism associated with resistance to EGFR-targeted agents: a systematic review and meta-analysis of studies in advanced non-small-cell lung cancer and metastatic colorectal cancer. Lancet Oncol 2008; 9: 962-72.
39. Pao W, Wang TY, Riely GJ, et al. KRAS mutations and primary resistance of lung adenocarcinomas to gefitinib or erlotinib. PLoS Med 2005; 2: 57-61.
40. Gumerlock PH, Holland WS, Chen H, et al. Mutational analysis of K-RAS and EGFR implicates K-RAS as a resistance marker in the Southwest Oncology Group (SWOG) trial S0126 of bronchioalveolar carcinoma (BAC) patients (pts) treated with gefitinib. J Clin Oncol 2005; 23 (suppl.): abstr. 7008.
41. Zhang X, Chang A. Molecular predictors of EGFR-TKI sensitivity in advanced non-small cell lung cancer. Int J Med Sci 2008; 5: 209-17.
42. Toschi L, Cappuzzo F. Understanding the new genetics of responsiveness to epidermal growth factor receptor tyrosine kinase inhibitors. Oncologist 2007; 12: 211-20.
43. Mitsudomi T, Yatabe Y. Mutations of the epidermal growth factor receptor gene and related genes as determinants of epidermal growth factor receptor tyrosine kinase inhibitors sensitivity in lung cancer. Cancer Sci 2007; 98: 1817-24. (Pubitemid 350002184)
44. Kubo T, Yamamoto H, Lockwood WW, et al. MET gene amplification or EGFR mutation activate MET in lung cancers untreated with EGFR tyrosine kinase inhibitors. Int J Cancer 2009; 124: 1778-84.
45. Turke AB, Zejnullahu K, Wu YL, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010; 17: 77-88.
46. Bean J, Brennan C, Shih JY, et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc Natl Acad Sci U S A 2007; 104: 20932-7.
47. Yano S, Wang W, Li QI, et al. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res 2008; 68: 9479-87.
48. Sequist LV, von Pawel J, Garmey EG, et al. Randomized phase II study of erlotinib plus tivantinib versus erlotinib plus placebo in previously treated non-small-cell lung cancer. J Clin Oncol 2011; 29: 3307-15.
49. Gridelli C, Rossi A, Bareschino MA, Schettino C, Sacco PC, Maione P. The potential role of insulin-like growth factor receptor inhibitors in the treatment of advanced non-small cell lung cancer. Expert Opin Investig Drugs 2010; 19: 631-9.
50. Guix M, Faber AC, Wang SE i wsp. Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J Clin Invest 2008; 118: 2609-19.
51. Gridelli C, Rossi A, Bareschino MA, Schettino C, Sacco PC, Maione P. The potential role of insulin-like growth factor receptor inhibitors in the treatment of advanced non-small cell lung cancer. Expert Opin Investig Drugs 2010; 19: 631-9.
52. Hirsch FR, Varella-Garcia M, Cappuzzo F. Predictive value of EGFR and HER2 overexpression in advanced non-small-cell lung cancer. Oncogene 2009; 28 (suppl.): 32-7.
53. Shigematsu H, Takahashi T, Nomura M, et al. Somatic Mutations of the HER2 Kinase Domain in Lung Adenocarcinomas. Cancer Res 2005; 65: 1642-6. (Pubitemid 40478587)
54. Perera SA, Danan L, Shimamura T, et al. HER2YVMA drives rapid development of adenosquamous lung tumor in mice that are sensitive to BIBW2992 and rapamycin combination therapy. PNAS 2009; 2: 474-9.
55. Hirsh V. Afatinib (BIBW 2992) development in non-small-cell lung cancer. Future Oncol 2011; 7: 817-25.
56. Giaccone G, Wang Y. Strategies for overcoming resistance to EGFR family tyrosine kinase inhibitors. Cancer Treat Rev 2011; 37: 456-64.
57. Bonanno L, Jirillo A, Favaretto A. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors and new therapeutic perspectives in non small cell lung cancer. Curr Drug Targets 2011; 12: 922-33.