Repetitive nicotine exposure leads to a more malignant and metastasis-prone phenotype of SCLC: A molecular insight into the importance of quitting smoking during treatment

Toxicological Sciences

Volumn 116, Issue 2, 2010, Pages 467-476

  Martínez García, Eva ^a,b   Irigoyen, Marta ^a,b   González Moreno, Óscar ^a   Corrales, Leticia ^a   Teijeira, Álvaro ^a   Salvo, Elizabeth ^a   Rouzaut, Ana ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b UNIVERSITY OF NAVARRA   (Spain)

Author keywords

CXCR4; Malignancy; Nicotine; SCLC

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; COLLAGEN; NICOTINE; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; NICOTINIC RECEPTOR; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CELL ADHESION; CELL DIFFERENTIATION; CELL STRUCTURE; CHEMICAL CARCINOGENESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; IN VITRO STUDY; LUNG SMALL CELL CANCER; LYMPH VESSEL ENDOTHELIUM; MOUSE; N417 CELL; NONHUMAN; PHENOTYPE; RETROSPECTIVE STUDY; SMOKING CESSATION; TOBACCO; TUMOR VASCULARIZATION; ANIMAL; CARCINOMA, SMALL CELL; CHEMICALLY INDUCED; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; HUMAN; LUNG NEOPLASMS; METASTASIS; PATHOLOGY; PHYSIOLOGY; TOXICITY;

ANIMALS; CARCINOMA, SMALL CELL; CELL ADHESION; CHEMOKINE CXCL12; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; LUNG NEOPLASMS; MICE; NEOPLASM METASTASIS; NICOTINE; PHENOTYPE; RECEPTORS, CXCR4; RECEPTORS, NICOTINIC; SMOKING CESSATION;

EID: 77955069034     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq138     Document Type: Article

References (45)

1. Borgerding, M., and Klus, H. (2005). Analysis of complex mixtures of cigarette smoke. Exp. Toxicol. Pathol. 57(Suppl. 1), 43-73.
2. Burger, M., Glodek, A., Hartmann, T., Schmitt-Gräff, A., Silberstein, L.E., Fujii, N., Kipps, T.J., and Burger, J.A. (2003). Functional expression of CXCR4 (CD184) on small-cell lung cancer cells mediates migration, integrin activation, and adhesion to stromal cells. Oncogene 22, 8093-8101.
3. Burman, A., Haworth, O., Hardie, D.L., Amft, E.N., Siewert, C., Jackson, D.G., Salmon, M., and Buckley, C.D. (2005). A chemokine dependent stromal induction mechanism for aberrant lymphocyte accumulation and compromised lymphatic return in rheumatoid arthritis. J. Immunol. 174, 1693-1700.
4. Byrne, A.M., Bouchier-Hayes, D.J., and Harmey, J.H. (2005). Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF). J. Cell Mol. Med. 9, 777-794.
5. Chen, J., Jiang, R., Garces, Y.I., Jatoi, A., Stoddard, S.M., Sun, Z., Marks, R.S., Liu, Y., and Yang, P. (2010). Prognostic factors for limited-stage small cell lung cancer: a study of 284 patients. Lung Cancer 67, 221-226.
6. Conklin, D.J., Haberzettl, P., Prough, R.A., and Bhatnagar, A. (2009). Glutathione-S-transferase P protects against endothelial dysfunction induced by exposure to tobacco smoke. Am. J. Physiol. Heart Circ. Physiol. 296, H1586-H1597.
7. Dasgupta, P., Kinkade, R., Joshi, B., Decook, C., Haura, E., and Chellappan, S. (2006). Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and surviving. Proc. Natl. Acad. Sci. U.S.A. 103, 6332-6337.
8. Dasgupta, P., Rizwani, W., Pillai, S., Kinkade, R., Kovacs, M., Rastogi, S., Banerjee, S., Carless, M., Kim, E., Coppola, D., et al. (2009). Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int. J. Cancer 124, 36-45.
9. De Stefani, E., Boffetta, P., Ronco, A.L., Brennan, P., Correa, P., Deneo-Pellegrini, H., Gutiérrez, L. P., and Mendilaharsu, M. (2005). Squamous and small cell carcinomas of the lung: similarities and differences concerning the role of tobacco smoking. Lung Cancer 47, 1-8.
10. Di Matteo, V., Pierucci, M., Di Giovanni, G., Benigno, A., and Esposito, E. (2007). The neurobiological bases for the pharmacotherapy of nicotine addiction. Curr. Pharm. Des. 13, 1269-1284.
11. Gelmini, S., Mangoni, M., Serio, M., Romagnani, P., and Lazzeri, E. (2008). The critical role of SDF-1/CXCR4 axis in cancer and cancer stem cells metastasis. J. Endocrinol. Invest. 31, 809-819.
12. Hann, C.L., and Rudin, C.M. (2008). Management of small-cell lung cancer: incremental changes but hope for the future. Oncology (Williston Park) 22, 1486-1492.
13. Hartmann, T.N., Burger, M., and Burger, J.A. (2004). The role of adhesion molecules and chemokine receptor CXCR4 (CD184) in small cell lung cancer. J. Biol. Regul. Homeost. Agents 18, 126-130.
14. Hartmann, T.N., Burger, J.A., Glodek, A., Fujii, N., and Burger, M. (2005). CXCR4 chemokine receptor and integrin signaling co-operate in mediating adhesion and chemoresistance in small cell lung cancer (SCLC) cells. Oncogene 24, 4462-4471.
15. Hecht, S.S. (2002). Cigarette smoking and lung cancer: chemical mechanisms and approaches to prevention. Lancet Oncol. 3, 461-469.
16. Hukkanen, J., Jacob, P., III., and Benowitz, N.L. (2005). Metabolism and disposition kinetics of nicotine. Pharmacol. Rev. 57, 79-115.
17. Ian Bray, F., and Weiderpass, E. (2010). Lung cancer mortality trends in 36 European countries: secular trends and birth cohort patterns by sex and region 1970-2007. Int. J. Cancer 126, 1454-1466.
18. Irigoyen, M., Ansó, E., Martínez, E., Garayoa, M., Martínez-Irujo, J.J., and Rouzaut, A. (2007). Hypoxia alters the adhesive properties of lymphatic endothelial cells. A transcriptional and functional study. Biochim. Biophys. Acta 1773, 880-890.
19. Keane, M.P., Belperio, J.A., Xue, Y.Y., Burdick, M.D., and Strieter, R.M. (2004). Depletion of CXCR2 inhibits tumor growth and angiogenesis in a murine model of lung cancer. J. Immunol. 172, 2853-2860.
20. Koletsis, E.N., Prokakis, C., Karanikolas, M., Apostolakis, E., and Dougenis, D. (2009). Current role of surgery in small cell lung carcinoma. J. Cardiothorac. Surg. 9, 4-30.
21. Lu, L.M., Zavitz, C.C., Chen, B., Kianpour, S., Wan, Y., and Stämpfli, M. R. (2007). Cigarette smoke impairs NK cell-dependent tumor immune surveillance. J. Immunol. 178, 936-943.
22. Luppi, F., Longo, A.M., de Boer, W.I., Rabe, K.F., and Hiemstra, P.S. (2007). Interleukin-8 stimulates cell proliferation in non-small cell lung cancer through epidermal growth factor receptor transactivation. Lung Cancer 56, 25-33.
23. Marrero, M.B., and Bencherif, M. (2009). Convergence of alpha 7 nicotinic acetylcholine receptor-activated pathways for anti-apoptosis and anti-inflammation: central role for JAK2 activation of STAT3 and NF-kappaB. Brain Res. 1256, 1-7.
24. Martínez-García, E., Irigoyen, M., Ansó, E., Martínez-Irujo, J.J., and Rouzaut, A. (2008). Recurrent exposure to nicotine differentiates human bronchial epithelial cells via epidermal growth factor receptor activation. Toxicol. Appl. Pharmacol. 228, 334-342.
25. Mousa, S., and Mousa, S.A. (2006). Cellular and molecular mechanisms of nicotine's pro-angiogenesis activity and its potential impact on cancer. J. Cell Biochem. 97, 1370-1378.
26. Otsuka, S., and Bebb, G. (2008). The CXCR4/SDF-1 chemokine receptor axis: a new target therapeutic for non-small cell lung cancer. J. Thorac. Oncol. 3, 1379-1383.
27. Paleari, L., Negri, E., Catassi, A., Cilli, M., Servent, D., D'Angelillo, R., Cesario, A., Russo, P., and Fini, M. (2009). Inhibition of non-neuronal alpha7-nicotinic receptor for lung cancer treatment. Am. J. Respir. Crit. Care. Med. 179, 1141-1150.
28. Parkin, D.M., Bray, F., Ferlay, J., and Pisani, P. (2005). Global cancer statistics, 2002. CA Cancer J. Clin. 55, 1074-1082.
29. Ritzenthaler, J.D., Han, S., and Roman, J. (2008). Stimulation of lung carcinoma cell growth by fibronectin-integrin signalling. Mol. Biosyst. 4, 1160-1169.
30. Rollins, B.J. (2006). Inflammatory chemokines in cancer growth and progression. Eur. J. Cancer 42, 760-767.
31. Rubinstein, L. (1990). Cancer recurrence after resection: T1 N0 non-small cell lung cancer. Lung Cancer Stuady Group. Ann. Thorac. Surg. 49, 242-246.
32. Ruffini, P.A., Morandi, P., Cabioglu, N., Altundag, K., and Cristofanilli, M. (2007). Manipulating the chemokine-chemokine receptor network to treat cancer. Cancer 109, 2392-2404.
33. Russell, M.A., Jarvis, M., Iyer, R., and Feyerabend, C. (1980). Relation of nicotine yield of cigarettes to blood nicotine concentrations in smokers. Br. Med. J. 280, 972-976.
34. Schober, A. (2008). Chemokines in vascular dysfunction and remodeling. Arterioscler. Thromb. Vasc. Biol. 28, 1950-1959.
35. Schuller, H.M., Jull, B.A., Sheppard, B.J., and Plummer, H.K. (2000). Interaction of tobacco-specific toxicants with the neuronal alpha(7) nicotinic acetylcholine receptor and its associated mitogenic signal transduction pathway: potential role in lung carcinogenesis and pediatric lung disorders. Eur. J. Pharmacol. 393, 265-277.
36. Schuller, H.M., and Orloff, M. (1998). Tobacco-specific carcinogenic nitrosamines. Ligands for nicotinic acetylcholine receptors in human lung cancer cells. Biochem. Pharmacol. 55, 1377-1384.
37. Stacker, S.A., and Achen, M.G. (2008). From anti-angiogenesis to anti-lymphangiogenesis: emerging trends in cancer therapy. Lymphat. Res. Biol. 6, 165-172.
38. Svensson, C.K. (1987). Clinical pharmacokinetics of nicotine. Clin. Pharmacokinet. 12, 30-40.
39. Tsurutani, J., Castillo, S.S., Brognard, J., Granville, C.A., Zhang, C., Gills, J.J., Sayyah, J., and Dennis, P.A. (2005). Tobacco components stimulate Akt-dependent proliferation and NFkappaB-dependent survival in lung cancer cells. Carcinogenesis 26, 1182-1195.
40. Uchida, D., Begum, N.M., Almofti, A., Nakashiro, K., Kawamata, H., Tateishi, Y., Hamakawa, H., Yoshida, H., and Sato, M. (2003). Possible role of stromal-cell-derived factor-1/CXCR4 signaling on lymph node metastasis of oral squamous cell carcinoma. Exp. Cell Res. 290, 289-302.
41. Upadhyaya, P., and Hecht, S.S. (2008). Identification of adducts formed in the reactions of 5#-acetoxy-N#-nitrosonornicotine with deoxyadenosine, thymidine, and DNA. Chem. Res. Toxicol. 21, 2164-2171.
42. Videtic, G.M.M., Stitt, L.W., Dar, R., Kocha, W.I., Tomiak, A.T., Truong, P.T., Vincent, M.D., and Yu, E.W. (2003). Continued cigarette smoking by patients receiving concurrent chemoradiotherapy for limitedstage small-cell lung cancer is associated with decreased survival. J. Clin. Oncol. 21, 1544-1549.
43. Walser, T.C., Rifat, S., Ma, X., Kundu, N., Ward, C., Goloubeva, O., Johnson, M.G., Medina, J.C., Collins, T.L., and Fulton, A.M. (2006). Antagonism of CXCR3 inhibits lung metastasis in a murine model of metastatic breast cancer. Cancer Res. 66, 7701-7777.
44. Xin, M., Gao, F., May, W.S., Flagg, T., and Deng, X. (2007). Protein kinase Czeta abrogates the proapoptotic function of Bax through phosphorylation. J. Biol. Chem. 282, 21268-21277.
45. Zhang, J., Kamdar, O., and Le, W. (2009). Nicotine induces resistance to chemotherapy by modulating mitochondrial signaling in lung cancer. Am. J. Respir. Cell Mol. Biol. 40, 135-146.