Chronic nicotine exposure mediates resistance to EGFR-TKI in EGFR-mutated lung cancer via an EGFR signal

Lung Cancer

Volumn 88, Issue 1, 2015, Pages 16-23

  Togashi, Yosuke ^a   Hayashi, Hidetoshi ^a,b   Okamoto, Kunio ^a,b   Fumita, Soichi ^a,b   Terashima, Masato ^a   de Velasco, Marco A ^a   Sakai, Kazuko ^a   Fujita, Yoshihiko ^a   Tomida, Shuta ^a   Nakagawa, Kazuhiko ^a   Nishio, Kazuto ^a  

^a KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KISHIWADA CITY HOSPITAL   (Japan)

Author keywords

Cigarette smoking; Epidermal growth factor receptor mutation; Epidermal growth factor receptor tyrosine kinase inhibitor; Nicotine; Non small cell lung cancer

Indexed keywords

GEFITINIB; HEXAMETHONIUM; NICOTINE; ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; NICOTINIC RECEPTOR; QUINAZOLINE DERIVATIVE;

11.18 CELL LINE; ADULT; AGED; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CANCER SURVIVAL; CONTROLLED STUDY; EPIDERMAL GROWTH FACTOR RECEPTOR GENE; FEMALE; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INDEPENDENT VARIABLE; LONG TERM EXPOSURE; LUNG CANCER CELL LINE; MAJOR CLINICAL STUDY; MALE; MEDICAL HISTORY; MONOTHERAPY; MUTATOR GENE; NON SMALL CELL LUNG CANCER; PC 9 CELL LINE; PREDICTOR VARIABLE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMOKING; TREATMENT OUTCOME; TREATMENT RESPONSE; ADVERSE EFFECTS; ANTAGONISTS AND INHIBITORS; CARCINOMA, NON-SMALL-CELL LUNG; DISEASE FREE SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; KAPLAN MEIER METHOD; LUNG NEOPLASMS; METABOLISM; MIDDLE AGED; MORTALITY; MUTATION; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; NICOTINE; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION; SMOKING;

EID: 84924590379     PISSN: 01695002     EISSN: 18728332     Source Type: Journal    
DOI: 10.1016/j.lungcan.2015.01.027     Document Type: Article

References (39)

1. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013, 63(1):11-30. (PubMed PMID: 23335087). 10.3322/caac.21166.
2. Siegel R., DeSantis C., Virgo K., Stein K., Mariotto A., Smith T., et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 2012, 62(4):220-241. (Epub 2012/06/16, PubMed PMID: 22700443). 10.3322/caac.21149.
3. Pao W., Chmielecki J. Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nat Rev Cancer 2010, 10(11):760-774. (PubMed PMID: 20966921; PubMed Central PMCID: PMCPMC3072803). 10.1038/nrc2947.
4. Pao W., Girard N. New driver mutations in non-small-cell lung cancer. Lancet Oncol 2011, 12(2):175-180. (PubMed PMID: 21277552). 10.1016/S1470-2045(10)70087-5.
5. Mok T.S., Wu Y.L., Thongprasert S., Yang C.H., Chu D.T., Saijo N., et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009, 361(10):947-957. (Epub 2009/08/21, PubMed PMID: 19692680). 10.1056/NEJMoa0810699.
6. Mitsudomi T., Morita S., Yatabe Y., Negoro S., Okamoto I., Tsurutani J., 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(2):121-128. (Epub 2009/12/22, PubMed PMID: 20022809). 10.1016/s1470-2045(09)70364-x.
7. Maemondo M., Inoue A., Kobayashi K., Sugawara S., Oizumi S., Isobe H., et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 2010, 362(25):2380-2388. (Epub 2010/06/25, PubMed PMID: 20573926). 10.1056/NEJMoa0909530.
8. Zhou C., Wu Y.L., Chen G., Feng J., Liu X.Q., Wang C., 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(8):735-742. (PubMed PMID: 21783417). 10.1016/S1470-2045(11)70184-X.
9. Rosell R., Carcereny E., Gervais R., Vergnenegre A., Massuti B., Felip E., 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(3):239-246. (PubMed PMID: 22285168). 10.1016/S1470-2045(11)70393-X.
10. Sequist L.V., Yang J.C., Yamamoto N., O'Byrne K., Hirsh V., Mok T., et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol 2013, 31(27):3327-3334. (PubMed PMID: 23816960). 10.1200/JCO.2012.44.2806.
11. Jackman D., Pao W., Riely G.J., Engelman J.A., Kris M.G., Jänne P.A., et al. Clinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. J Clin Oncol 2010, 28(2):357-360. (PubMed PMID: 19949011). 10.1200/JCO.2009.24.7049.
12. Kobayashi S., Boggon T.J., Dayaram T., Jänne P.A., Kocher O., Meyerson M., et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005, 352(8):786-792. (PubMed PMID: 15728811). 10.1056/NEJMoa044238.
13. Suda K., Mizuuchi H., Maehara Y., Mitsudomi T. Acquired resistance mechanisms to tyrosine kinase inhibitors in lung cancer with activating epidermal growth factor receptor mutation-diversity, ductility, and destiny. Cancer Metastasis Rev 2012, 31(3-4):807-814. (PubMed PMID: 22736441). 10.1007/s10555-012-9391-7.
14. Remon J., Morán T., Majem M., Reguart N., Dalmau E., Márquez-Medina D., et al. Acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in EGFR-mutant non-small cell lung cancer: a new era begins. Cancer Treat Rev 2014, 40(1):93-101. (PubMed PMID: 23829935). 10.1016/j.ctrv.2013.06.002.
15. Hecht S.S., Abbaspour A., Hoffman D. A study of tobacco carcinogenesis. XLII. Bioassay in A/J mice of some structural analogues of tobacco-specific nitrosamines. Cancer Lett 1988, 42(1-2):141-145. (PubMed PMID: 3180033).
16. Hecht S.S. Cigarette smoking and lung cancer: chemical mechanisms and approaches to prevention. Lancet Oncol 2002, 3(8):461-469. (PubMed PMID: 12147432).
17. Dasgupta P., Rastogi S., Pillai S., Ordonez-Ercan D., Morris M., Haura E., et al. Nicotine induces cell proliferation by beta-arrestin-mediated activation of Src and Rb-Raf-1 pathways. J Clin Invest 2006, 116(8):2208-2217. (PubMed PMID: 16862215; PubMed Central PMCID: PMCPMC1513051). 10.1172/JCI28164.
18. Dasgupta P., Rizwani W., Pillai S., Kinkade R., Kovacs M., Rastogi S., et al. Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int J Cancer 2009, 124(1):36-45. (PubMed PMID: 18844224; PubMed Central PMCID: PMCPMC2826200). 10.1002/ijc.23894.
19. Heeschen C., Jang J.J., Weis M., Pathak A., Kaji S., Hu R.S., et al. Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis. Nat Med 2001, 7(7):833-839. (PubMed PMID: 11433349). 10.1038/89961.
20. Filosto S., Baston D.S., Chung S., Becker C.R., Goldkorn T. Src mediates cigarette smoke-induced resistance to tyrosine kinase inhibitors in NSCLC cells. Mol Cancer Ther 2013, 12(8):1579-1590. (PubMed PMID: 23686837). 10.1158/1535-7163.MCT-12-1029.
21. Filosto S., Becker C.R., Goldkorn T. Cigarette smoke induces aberrant EGF receptor activation that mediates lung cancer development and resistance to tyrosine kinase inhibitors. Mol Cancer Ther 2012, 11(4):795-804. (PubMed PMID: 22302097). 10.1158/1535-7163.MCT-11-0698.
22. Wang S., Takayama K., Tanaka K., Takeshita M., Nakagaki N., Ijichi K., et al. Nicotine induces resistance to epidermal growth factor receptor tyrosine kinase inhibitor by (1 nicotinic acetylcholine receptor-mediated activation in PC9 cells. J Thorac Oncol 2013, 8(6):719-725. (PubMed PMID: 23625155). 10.1097/JTO.0b013e31828b51d4.
23. Arao T., Fukumoto H., Takeda M., Tamura T., Saijo N., Nishio K. Small in-frame deletion in the epidermal growth factor receptor as a target for ZD6474. Cancer Res 2004, 64(24):9101-9104. (PubMed PMID: 15604279). 10.1158/0008-5472.CAN-04-2360.
24. Kaneda H., Arao T., Tanaka K., Tamura D., Aomatsu K., Kudo K., et al. FOXQ1 is overexpressed in colorectal cancer and enhances tumorigenicity and tumor growth. Cancer Res 2010, 70(5):2053-2063. (PubMed PMID: 20145154). 10.1158/0008-5472.CAN-09-2161.
25. Lam D.C., Girard L., Ramirez R., Chau W.S., Suen W.S., Sheridan S., et al. Expression of nicotinic acetylcholine receptor subunit genes in non-small-cell lung cancer reveals differences between smokers and nonsmokers. Cancer Res 2007, 67(10):4638-4647. (PubMed PMID: 17510389). 10.1158/0008-5472.CAN-06-4628.
26. Carlisle D.L., Liu X., Hopkins T.M., Swick M.C., Dhir R., Siegfried J.M. Nicotine activates cell-signaling pathways through muscle-type and neuronal nicotinic acetylcholine receptors in non-small cell lung cancer cells. Pulm Pharmacol Ther 2007, 20(6):629-641. (PubMed PMID: 17015027). 10.1016/j.pupt.2006.07.001.
27. Wu C.H., Lee C.H., Ho Y.S. Nicotinic acetylcholine receptor-based blockade: applications of molecular targets for cancer therapy. Clin Cancer Res 2011, 17(11):3533-3541. (PubMed PMID: 21444681). 10.1158/1078-0432.CCR-10-2434.
28. Shigematsu H., Lin L., Takahashi T., Nomura M., Suzuki M., Wistuba I.I., et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst 2005, 97(5):339-346. (PubMed PMID: 15741570). 10.1093/jnci/dji055.
29. Fukuoka M., Wu Y.L., Thongprasert S., Sunpaweravong P., Leong S.S., Sriuranpong V., et al. Biomarker analyses and final overall survival results from a phase III, randomized, open-label, first-line study of gefitinib versus carboplatin/paclitaxel in clinically selected patients with advanced non-small-cell lung cancer in Asia (IPASS). J Clin Oncol 2011, 29(21):2866-2874. (Epub 2011/06/15, PubMed PMID: 21670455). 10.1200/jco.2010.33.4235.
30. Zhang Y., Kang S., Fang W., Hong S., Liang W., Yan Y., et al. Impact of smoking status on EGFR-TKI efficacy for advanced non-small-cell lung cancer in EGFR mutants: a meta-analysis. Clin Lung Cancer 2014, (PubMed PMID: 25454007). 10.1016/j.cllc.2014.09.008.
31. 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(12):1817-1824. 10.1111/j.1349-7006.2007.00607.x. (Epub 2007/09/25, PubMed PMID: 17888036).
32. Ou S.H. Lung cancer in never-smokers. Does smoking history matter in the era of molecular diagnostics and targeted therapy?. J Clin Pathol 2013, 66(10):839-846. (PubMed PMID: 23661716). 10.1136/jclinpath-2012-201296.
33. Ferketich A.K., Niland J.C., Mamet R., Zornosa C., D'Amico T.A., Ettinger D.S., et al. Smoking status and survival in the national comprehensive cancer network non-small cell lung cancer cohort. Cancer 2013, 119(4):847-853. 10.1002/cncr.27824. (PubMed PMID: 23023590).
34. Nakagawa K., Tamura T., Negoro S., Kudoh S., Yamamoto N., Takeda K., et al. Phase I pharmacokinetic trial of the selective oral epidermal growth factor receptor tyrosine kinase inhibitor gefitinib ('Iressa', ZD1839) in Japanese patients with solid malignant tumors. Ann Oncol 2003, 14(6):922-930. (Epub 2003/06/11, PubMed PMID: 12796031).
35. Yamamoto N., Horiike A., Fujisaka Y., Murakami H., Shimoyama T., Yamada Y., et al. Phase I dose-finding and pharmacokinetic study of the oral epidermal growth factor receptor tyrosine kinase inhibitor Ro50-8231 (erlotinib) in Japanese patients with solid tumors. Cancer Chemother Pharmacol 2008, 61(3):489-496. (Epub 2007/05/08, PubMed PMID: 17483950). 10.1007/s00280-007-0494-8.
36. Benowitz N.L. Neurobiology of nicotine addiction: implications for smoking cessation treatment. Am J Med 2008, 121(4 (Suppl. 1)):S3-S10. 10.1016/j.amjmed.2008.01.015. (PubMed PMID: 18342164).
37. De Biasi M., Dani J.A., Reward addiction, withdrawal to nicotine. Annu Rev Neurosci 2011, 34:105-130. (PubMed PMID: 21438686; PubMed Central PMCID: PMCPMC3137256). 10.1146/annurev-neuro-061010-113734.
38. Egleton R.D., Brown K.C., Dasgupta P. Nicotinic acetylcholine receptors in cancer: multiple roles in proliferation and inhibition of apoptosis. Trends Pharmacol Sci 2008, 29(3):151-158. (PubMed PMID: 18262664). 10.1016/j.tips.2007.12.006.
39. Morita S., Okamoto I., Kobayashi K., Yamazaki K., Asahina H., Inoue A., et al. Combined survival analysis of prospective clinical trials of gefitinib for non-small cell lung cancer with EGFR mutations. Clin Cancer Res 2009, 15(13):4493-4498. (PubMed PMID: 19531624). 10.1158/1078-0432.CCR-09-0391.