Signaling pathways modulating dependence of lung cancer on mutant epidermal growth factor receptor and mechanisms of intrinsic and acquired resistance to tyrosine Kinase inhibitors

Current Pharmaceutical Design

Volumn 20, Issue 24, 2014, Pages 3883-3893

  Wannesson, Luciano ^a   Viteri, Santiago ^b   Costa, Carlota ^b   Karachaliou, Niki ^b   Molina Vila, Miguel Angel ^b   Rosell, Rafael ^b,c  

^a ONCOLOGY INSTITUTE OF SOUTHERN SWITZERLAND   (Switzerland)

^b INSTITUT UNIVERSITARI DEXEUS   (Spain)

^c HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

Author keywords

Afatinib; Erlotinib; Gefitinib; Primary resistance; Refractory; Secondary resistance; Sensitivity

Indexed keywords

B RAF KINASE; DACTOLISIB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; FAS ANTIGEN; GEFITINIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; SCATTER FACTOR; ANTINEOPLASTIC AGENT; PROTEIN KINASE INHIBITOR;

APOPTOSIS; ASTROCYTE; CANCER REGRESSION; CANCER RESISTANCE; DNA REPAIR; DRUG EFFICACY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE MUTATION; HUMAN; LUNG ADENOCARCINOMA; LUNG CANCER CELL LINE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; REVIEW; TREATMENT DURATION; TREATMENT RESPONSE; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; LUNG NEOPLASMS; METABOLISM; MUTATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; HUMANS; LUNG NEOPLASMS; MUTATION; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84903954155     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113196660758     Document Type: Review

References (81)

1. D'Addario G, Fruh M, Reck M, et al. Metastatic non-small-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010; 21 Suppl 5: v116-v119.
2. Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006; 355: 2542-2550.
3. Scagliotti GV, De Marinis F, Rinaldi M, et al. Phase III randomized trial comparing three platinum-based doublets in advanced non-small-cell lung cancer. J Clin Oncol 2002; 20: 4285-4291.
4. Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 2008; 26: 3543-3551.
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: 2129-2139.
6. Paez JG, Janne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304: 1497-1500.
7. Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatinpaclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009; 361: 947-957.
8. Azzoli CG, Temin S, Aliff T, et al. 2011 Focused Update of 2009 American Society of Clinical Oncology Clinical Practice Guideline Update on Chemotherapy for Stage IV Non-Small-Cell Lung Cancer. J Clin Oncol 2011; 29: 3825-3831.
9. Maemondo M, Inoue A, Kobayashi K, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 2010; 362: 2380-2388.
10. 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, randomised phase 3 trial. Lancet Oncol 2010; 11: 121-128.
11. Rosell R, Carcereny E, Gervais R, et al. 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.
12. Zhou C, Wu YL, Chen G, et al. 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.
13. Sharma SV, Settleman J. Exploiting the balance between life and death: targeted cancer therapy and oncogenic shock. Biochem Pharmacol 2010; 80: 666-673.
14. Weinstein IB. Cancer. Addiction to oncogenes--the Achilles heal of cancer. Science 2002; 297: 63-64.
15. Felsher DW, Bishop JM. Reversible tumorigenesis by MYC in hematopoietic lineages. Mol Cell 1999; 4: 199-207.
16. Chin L, Tam A, Pomerantz J, et al. Essential role for oncogenic Ras in tumour maintenance. Nature 1999; 400: 468-472.
17. Workman P. Cancer genome targets: RAF-ing up tumor cells to overcome oncogene addiction. Expert Rev Anticancer Ther 2002; 2: 611-614.
18. Sharma SV, Gajowniczek P, Way IP, et al. A common signaling cascade may underlie addiction to the Src, BCR-ABL, and EGF receptor oncogenes. Cancer Cell 2006; 10: 425-435.
19. Solimini NL, Luo J, Elledge SJ. Non-oncogene addiction and the stress phenotype of cancer cells. Cell 2007; 130: 986-988.
20. Luo J, Solimini NL, Elledge SJ. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 2009; 136: 823-837.
21. Gazdar AF. Activating and resistance mutations of EGFR in non-small-cell lung cancer: role in clinical response to EGFR tyrosine kinase inhibitors. Oncogene 2009; 28 Suppl 1: S24-S31.
22. Kumar A, Petri ET, Halmos B, Boggon TJ. Structure and clinical relevance of the epidermal growth factor receptor in human cancer. J Clin Oncol 2008; 26: 1742-1751.
23. Pao W, Iafrate AJ, Su Z. Genetically informed lung cancer medicine. J Pathol 2011; 223: 230-240.
24. Ciardiello F, Tortora G. EGFR antagonists in cancer treatment. N Engl J Med 2008; 358: 1160-1174.
25. De Luca A, Normanno N. Predictive biomarkers to tyrosine kinase inhibitors for the epidermal growth factor receptor in non-small-cell lung cancer. Curr Drug Targets 2010; 11: 851-864.
26. Gazdar AF, Minna JD. Deregulated EGFR signaling during lung cancer progression: mutations, amplicons, and autocrine loops. Cancer Prev Res (Phila) 2008; 1: 156-160.
27. Ekstrand AJ, Sugawa N, James CD, Collins VP. Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proc Natl Acad Sci USA 1992; 89: 4309-4313.
28. Ji H, Li D, Chen L, et al. 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.
29. Xin H, Herrmann A, Reckamp K, et al. Antiangiogenic and antimetastatic activity of JAK inhibitor AZD1480. Cancer Res 2011; 71: 6601-6610.
30. Rosell R, Viteri S, Molina MA, et al. Epidermal growth factor receptor tyrosine kinase inhibitors as first-line treatment in advanced nonsmall-cell lung cancer. Curr Opin Oncol 2010; 22: 112-120.
31. Faber AC, Li D, Song Y, et al. Differential induction of apoptosis in HER2 and EGFR addicted cancers following PI3K inhibition. Proc Natl Acad Sci USA 2009; 106: 19503-19508.
32. Willis SN, Fletcher JI, Kaufmann T, et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 2007; 315: 856-859.
33. Gavathiotis E, Suzuki M, Davis ML, et al. BAX activation is initiated at a novel interaction site. Nature 2008; 455: 1076-1081.
34. Faber AC, Corcoran RB, Ebi H, et al. BIM expression in treatment-naive cancers predicts responsiveness to kinase inhibitors. Cancer Discov 2011; 1: 352-355.
35. Richter-Larrea JA, Robles EF, Fresquet V, et al. Reversion of epigenetically mediated BIM silencing overcomes chemoresistance in Burkitt lymphoma. Blood 2010; 116: 2531-2542.
36. Bachmann PS, Piazza RG, Janes ME, et al. Epigenetic silencing of BIM in glucocorticoid poor-responsive pediatric acute lymphoblastic leukemia, and its reversal by histone deacetylase inhibition. Blood 2010; 116: 3013-3022.
37. San Jose-Eneriz E, Agirre X, Jimenez-Velasco A, et al. Epigenetic down-regulation of BIM expression is associated with reduced optimal responses to imatinib treatment in chronic myeloid leukaemia. Eur J Cancer 2009; 45: 1877-1889.
38. Ng KP, Hillmer AM, Chuah CT, et al. A common BIM deletion polymorphism mediates intrinsic resistance and inferior responses to tyrosine kinase inhibitors in cancer. Nat Med 2012; 18: 521-528.
39. Rosell R, Molina MA, Costa C, et al. Pretreatment EGFR T790M mutation and BRCA1 mRNA expression in erlotinib-treated advanced non-small-cell lung cancer patients with EGFR mutations. Clin Cancer Res 2011; 17: 1160-1168.
40. Rosell R, Taron M, Benlloch S, et al. Nanostring Multiple Target Profiling Identifies Aeg-1 as an Essential Predictor of Erlotinib Outcome in Egfr-Mutant Non-Small-Cell Lung Cancer (NSCLC). Lung Cancer 2011; 71: S31-S32.
41. Mayo C, Bertran-Alamillo J, Molina-Vila MA, et al. Pharmacogenetics of EGFR in lung cancer: perspectives and clinical applications. Pharmacogenomics 2012; 13: 789-802.
42. Bivona TG, Hieronymus H, Parker J, et al. FAS and NF-kappaB signalling modulate dependence of lung cancers on mutant EGFR. Nature 2011; 471: 523-526.
43. Hu G, Wei Y, Kang Y. The multifaceted role of MTDH/AEG-1 in cancer progression. Clin Cancer Res 2009; 15: 5615-5620.
44. Graff JR, Konicek BW, Carter JH, Marcusson EG. Targeting the eukaryotic translation initiation factor 4E for cancer therapy. Cancer Res 2008; 68: 631-634.
45. Kono SA, Marshall ME, Ware KE, Heasley LE. The fibroblast growth factor receptor signaling pathway as a mediator of intrinsic resistance to EGFR-specific tyrosine kinase inhibitors in non-small cell lung cancer. Drug Resist Updat 2009; 12: 95-102.
46. Marek L, Ware KE, Fritzsche A, et al. Fibroblast growth factor (FGF) and FGF receptor-mediated autocrine signaling in non-small-cell lung cancer cells. Mol Pharmacol 2009; 75: 196-207.
47. Morgillo F, Kim WY, Kim ES, et al. Implication of the insulin-like growth factor-IR pathway in the resistance of non-small cell lung cancer cells to treatment with gefitinib. Clin Cancer Res 2007; 13: 2795-2803.
48. Lazzara MJ, Lane K, Chan R, et al. Impaired SHP2-mediated extracellular signal-regulated kinase activation contributes to gefitinib sensitivity of lung cancer cells with epidermal growth factor receptor-activating mutations. Cancer Res 2010; 70: 3843-3850.
49. Casas-Selves M, Kim J, Zhang Z, et al. Tankyrase and the canonical Wnt pathway protect lung cancer cells from EGFR inhibition. Cancer Res 2012.
50. Kobayashi S, Boggon TJ, Dayaram T, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005; 352: 786-792.
51. Pao W, Miller VA, Politi KA, et al. 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.
52. Pao W, Chmielecki J. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat Rev Cancer 2010; 10: 760-774.
53. 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 USA 2008; 105: 2070-2075.
54. 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: 7854-7858.
55. Maheswaran S, Sequist LV, Nagrath S, et al. Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 2008; 359: 366-377.
56. Oxnard GR, Arcila ME, Sima CS, et al. Acquired resistance to EGFR tyrosine kinase inhibitors in EGFR-mutant lung cancer: distinct natural history of patients with tumors harboring the T790M mutation. Clin Cancer Res 2011; 17: 1616-1622.
57. 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.
58. Bean J, Riely GJ, Balak M, 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: 7519-7525.
59. Brugger W, Thomas M. EGFR-TKI resistant non-small cell lung cancer (NSCLC): New developments and implications for future treatment. Lung Cancer 2012; 77: 2-8.
60. Costa DB, Halmos B, Kumar A, et al. BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS Med 2007; 4: 1669-1679; discussion 1680.
61. Engelman JA, Zejnullahu K, Mitsudomi T, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-1043.
62. Nguyen KS, Kobayashi S, Costa DB. Acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancers dependent on the epidermal growth factor receptor pathway. Clin Lung Cancer 2009; 10: 281-289.
63. Peters S, Adjei AA. MET: a promising anticancer therapeutic target. Nat Rev Clin Oncol 2012; 9: 314-326.
64. Yano S, Wang W, Li Q, et al. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res 2008; 68: 9479-9487.
65. Zhang Z, Lee JC, Lin L, et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat Genet 2012; advance online publication.
66. Yamaguchi T, Yanagisawa K, Sugiyama R, et al. NKX2-1/TITF1/ TTF-1-Induced ROR1 is required to sustain EGFR survival signaling in lung adenocarcinoma. Cancer Cell 2012; 21: 348-361.
67. Ohashi K, Sequist LV, Arcila ME, et al. Lung cancers with acquired resistance to EGFR inhibitors occasionally harbor BRAF gene mutations but lack mutations in KRAS, NRAS, or MEK1. Proc Natl Acad Sci USA 2012.
68. Harada D, Takigawa N, Ochi N, et al. A JAK2-Related Pathway Induces Acquired Erlotinib Resistance in Lung Cancer Cells Harboring an EGFR-Activating Mutation. Cancer Sci 2012.
69. Ercan D, Xu C, Yanagita M, et al. Reactivation of ERK signaling causes resistance to EGFR kinase inhibitors. Cancer Discov 2012; 2: 934-947.
70. Costa DB, Schumer ST, Tenen DG, Kobayashi S. Differential responses to erlotinib in epidermal growth factor receptor (EGFR)-mutated lung cancers with acquired resistance to gefitinib carrying the L747S or T790M secondary mutations. J Clin Oncol 2008; 26: 1182-1184; author reply 1184-6.
71. Balak MN, Gong Y, Riely GJ, et al. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors. Clin Cancer Res 2006; 12: 6494-6501.
72. 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.
73. Koizumi H, Yamada T, Takeuchi S, et al. Hsp90 Inhibition Overcomes HGF-Triggering Resistance to EGFR-TKIs in EGFR-Mutant Lung Cancer by Decreasing Client Protein Expression and Angiogenesis. J Thorac Oncol 2012; 7: 1078-1085.
74. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
75. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 2008; 14: 818-829.
76. Suda K, Tomizawa K, Fujii M, et al. Epithelial to mesenchymal transition in an epidermal growth factor receptor-mutant lung cancer cell line with acquired resistance to erlotinib. J Thorac Oncol 2011; 6: 1152-1161.
77. Sequist LV, Heist RS, Shaw AT, et al. Implementing multiplexed genotyping of non-small-cell lung cancers into routine clinical practice. Ann Oncol 2011; 22: 2616-2624.
78. Takeuchi T, Tomida S, Yatabe Y, et al. Expression profile-defined classification of lung adenocarcinoma shows close relationship with underlying major genetic changes and clinicopathologic behaviors. J Clin Oncol 2006; 24: 1679-1688.
79. Tabara K, Kanda R, Sonoda K, et al. Loss of Activating EGFR Mutant Gene Contributes to Acquired Resistance to EGFR Tyrosine Kinase Inhibitors in Lung Cancer Cells. PLoS One 2012; 7: e41017.
80. P. The epithelial-mesenchymal transition (EMT) phenomenon. Ann Oncol 2010; 21 Suppl 7: vii89-vii92.
81. Thomson S, Petti F, Sujka-Kwok I, et al. A systems view of epithelial-mesenchymal transition signaling states. Clin Exp Metastasis 2011; 28: 137-155.