Nicotine induces tumor growth and chemoresistance through activation of the PI3K/Akt/mTOR pathway in bladder cancer

Molecular Cancer Therapeutics

Volumn 14, Issue 9, 2015, Pages 2112-2120

  Yuge, Kazuyuki ^a   Kikuchi, Eiji ^a   Hagiwara, Masayuki ^a   Yasumizu, Yota ^a   Tanaka, Nobuyuki ^a   Kosaka, Takeo ^a   Miyajima, Akira ^a   Oya, Mototsugu ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; DACTOLISIB; MAMMALIAN TARGET OF RAPAMYCIN; NICOTINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; S6 KINASE; PROTEIN KINASE INHIBITOR; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSAY; BLADDER CANCER; BLADDER CANCER CELL LINE; CANCER INHIBITION; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DRUG RESISTANCE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSITIONAL CELL CARCINOMA; TUMOR GROWTH; UPREGULATION; WESTERN BLOTTING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; DRUG POTENTIATION; DRUG SCREENING; METABOLISM; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE; TUMOR VOLUME; URINARY BLADDER NEOPLASMS;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HUMANS; MICE; NICOTINE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR BURDEN; URINARY BLADDER NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942155439     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-15-0140     Document Type: Article

References (40)

1. Levin ML, Lilienfeld AM, Moore GE. The association of smoking with cancer of the urinary bladder in humans. AMA Arch Intern Med 1956;98:129-35.
2. Freedman ND, Silverman DT, Hollenbeck AR, Schatzkin A, Abnet CC. Association between smoking and risk of bladder cancer among men and women. JAMA 2011;306:737-45.
3. Chen CH, Shun CT, Huang KH, Huang CY, Tsai YC, Yu HJ, et al. Stopping smoking might reduce tumour recurrence in nonmuscle-invasive bladder cancer. BJU Int 2007;100:281-6.
4. Fleshner N, Garland J, Moadel A, Herr H, Ostroff J, Trambert R, et al. Influence of smoking status on the disease-related outcomes of patients with tobacco-associated superficial transitional cell carcinoma of the bladder. Cancer 1999;86:2337-45.
5. Oya M, Kikuchi E. Evidenced-based clinical practice guideline for upper tract urothelial carcinoma (summary - Japanese Urological Association, 2014 edition). Int J Urol 2015;22:3-13.
6. Zeegers MP, Tan FE, Dorant E, van Den Brandt PA. The impact of characteristics of cigarette smoking on urinary tract cancer risk: a meta-analysis of epidemiologic studies. Cancer 2000;89:630-9.
7. Lammers RJ, Witjes WP, Hendricksen K, Caris CT, Janzing-Pastors MH, Witjes JA. Smoking status is a risk factor for recurrence after transurethral resection of non-muscle-invasive bladder cancer. Eur Urol 2011;60:713-20.
8. Hagiwara M, Kikuchi E, Tanaka N, Matsumoto K, Ide H, Miyajima A, et al. Impact of smoking status on bladder tumor recurrence after radical nephroureterectomy for upper tract urothelial carcinoma. J Urol 2013;189:2062-8.
9. Browman GP, Wong G, Hodson I, Sathya J, Russell R, McAlpine L, et al. Influence of cigarette smoking on the efficacy of radiation therapy in head and neck cancer. N Engl J Med 1993;328:159-63.
10. Videtic GM, Stitt LW, Dar AR, Kocha WI, Tomiak AT, Truong PT, et al. Continued cigarette smoking by patients receiving concurrent chemoradiotherapy for limited-stage small-cell lung cancer is associated with decreased survival. J Clin Oncol 2003;21:1544-9.
11. Arredondo J, Chernyavsky AI, Grando SA. Nicotinic receptors mediate tumorigenic action of tobacco-derived nitrosamines on immortalized oral epithelial cells. Cancer Biol Ther 2006;5:511-7.
12. Laag E, Majidi M, Cekanova M, Masi T, Takahashi T, Schuller HM. NNK activates ERK1/2 and CREB/ATF-1 via beta-1-AR and EGFR signaling in human lung adenocarcinoma and small airway epithelial cells. Int J Cancer 2006;119:1547-52.
13. Schuller HM, Plummer HK 3rd, Jull BA. Receptor-mediated effects of nicotine and its nitrosated derivative NNK on pulmonary neuroendocrine cells. Anat Rec A Discov Mol Cell Evol Biol 2003;270:51-8.
14. Minna JD. Nicotine exposure and bronchial epithelial cell nicotinic acetylcholine receptor expression in the pathogenesis of lung cancer. J Clin Invest 2003;111:31-3.
15. Shin VY, Wu WK, Chu KM, Wong HP, Lam EK, Tai EK, et al. Nicotine induces cyclooxygenase-2 and vascular endothelial growth factor receptor-2 in association with tumor-associated invasion and angiogenesis in gastric cancer. Mol Cancer Res 2005;3:607-15.
16. Jin Z, Gao F, Flagg T, Deng X. Nicotine induces multi-site phosphorylation of Bad in association with suppression of apoptosis. J Biol Chem 2004;279:23837-44.
17. Nishioka T, Kim HS, Luo LY, Huang Y, Guo J, Chen CY. Sensitization of epithelial growth factor receptors by nicotine exposure to promote breast cancer cell growth. Breast Cancer Res 2011;13:R113.
18. Tsurutani J, Castillo SS, Brognard J, Granville CA, Zhang C, Gills JJ, et al. Tobacco components stimulate Akt-dependent proliferation and NFkappaB-dependent survival in lung cancer cells. Carcinogenesis 2005;26:1182-95.
19. Xu J, Huang H, Pan C, Zhang B, Liu X, Zhang L. Nicotine inhibits apoptosis induced by cisplatin in human oral cancer cells. Int J Oral Maxillofac Surg 2007;36:739-44.
20. Gaikwad SM, Ray P. Non-invasive imaging of PI3K/Akt/mTOR signalling in cancer. Am J Nucl Med Mol Imaging 2012;2:418-31.
21. Vivanco I, Sawyers CL. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501.
22. Chen RJ, Ho YS, Guo HR, Wang YJ. Long-term nicotine exposure-induced chemoresistance is mediated by activation of Stat3 and downregulation of ERK1/2 via nAChR and beta-adrenoceptors in human bladder cancer cells. Toxicol Sci 2010;115:118-30.
23. Al-Wadei MH, Al-Wadei HA, Schuller HM. Pancreatic cancer cells and normal pancreatic duct epithelial cells express an autocrine catecholamine loop that is activated by nicotinic acetylcholine receptors alpha3, alpha5, and alpha7. Mol Cancer Res 2012;10:239-49.
24. Improgo MR, Tapper AR, Gardner PD. Nicotinic acetylcholine receptor-mediated mechanisms in lung cancer. Biochem Pharmacol 2011;82:1015-21.
25. Momi N, Ponnusamy MP, Kaur S, Rachagani S, Kunigal SS, Chellappan S, et al. Nicotine/cigarette smoke promotes metastasis of pancreatic cancer through alpha7nAChR-mediated MUC4 upregulation. Oncogene 2013;32:1384-95.
26. Armitage AK, Dollery CT, George CF, Houseman TH, Lewis PJ, Turner DM. Absorption and metabolism of nicotine from cigarettes. Br Med J 1975;4:313-6.
27. Russell MA, Jarvis M, Iyer R, Feyerabend C. Relation of nicotine yield of cigarettes to blood nicotine concentrations in smokers. Br Med J 1980;280:972-6.
28. Ghamande S, Hylander BL, Oflazoglu E, Lele S, Fanslow W, Repasky EA. Recombinant CD40 ligand therapy has significant antitumor effects on CD40-positive ovarian tumor xenografts grown in SCID mice and demonstrates an augmented effect with cisplatin. Cancer Res 2001;61:7556-62.
29. Tanaka N, Miyajima A, Kosaka T, Miyazaki Y, Shirotake S, Shirakawa H, et al. Acquired platinum resistance enhances tumour angiogenesis through angiotensin II type 1 receptor in bladder cancer. Br J Cancer 2011;105:1331-7.
30. Yasumizu Y, Miyajima A, Kosaka T, Miyazaki Y, Kikuchi E, Oya M. Dual PI3K/mTOR inhibitor NVP-BEZ235 sensitizes docetaxel in castration resistant prostate cancer. J Urol 2014;191:227-34.
31. Crivelli JJ, Xylinas E, Kluth LA, Rieken M, Rink M, Shariat SF. Effect of smoking on outcomes of urothelial carcinoma: a systematic review of the literature. Eur Urol 2014;65:742-54.
32. Rink M, Zabor EC, Furberg H, Xylinas E, Ehdaie B, Novara G, et al. Impact of smoking and smoking cessation on outcomes in bladder cancer patients treated with radical cystectomy. Eur Urol 2013;64:456-64.
33. Brait M, Munari E, LeBron C, Noordhuis MG, Begum S, Michailidi C, et al. Genome-wide methylation profiling and the PI3K-AKT pathway analysis associated with smoking in urothelial cell carcinoma. Cell Cycle 2013;12:1058-70.
34. Serra V, Markman B, Scaltriti M, Eichhorn PJ, Valero V, Guzman M, et al. NVP-BEZ235, a dual PI3K/mTOR inhibitor, prevents PI3K signaling and inhibits the growth of cancer cells with activating PI3K mutations. Cancer Res 2008;68:8022-30.
35. West KA, Brognard J, Clark AS, Linnoila IR, Yang X, Swain SM, et al. Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J Clin Invest 2003;111:81-90.
36. Belyanskaya LL, Hopkins-Donaldson S, Kurtz S, Simoes-Wust AP, Yousefi S, Simon HU, et al. Cisplatin activates Akt in small cell lung cancer cells and attenuates apoptosis by survivin upregulation. Int J Cancer 2005;117:755-63.
37. Dasgupta P, Kinkade R, Joshi B, Decook C, Haura E, Chellappan S. Nicotine inhibits apoptosis induced by chemotherapeutic drugs by upregulating XIAP and survivin. Proc Natl Acad Sci U S A 2006;103:6332-7.
38. Zhang J, Kamdar O, Le W, Rosen GD, Upadhyay D. Nicotine induces resistance to chemotherapy by modulating mitochondrial signaling in lung cancer. Am J Respir Cell Mol Biol 2009;40:135-46.
39. An Y, Kiang A, Lopez JP, Kuo SZ, Yu MA, Abhold EL, et al. Cigarette smoke promotes drug resistance and expansion of cancer stem cell-like side population. PLoS One 2012;7:e47919.
40. Onoda N, Nehmi A, Weiner D, Mujumdar S, Christen R, Los G. Nicotine affects the signaling of the death pathway, reducing the response of head and neck cancer cell lines to DNA damaging agents. Head Neck 2001;23:860-70.