Connections of nicotine to cancer

Nature Reviews Cancer

Volumn 14, Issue 6, 2014, Pages 419-429

  Grando, Sergei A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; NICOTINE; NICOTINIC RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; BLADDER CANCER; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER PREVENTION; CANCER THERAPY; CARCINOGENESIS; CELL PROLIFERATION; CELL SPREADING; CELL SURVIVAL; COLON CANCER; GALLBLADDER CANCER; GENE EXPRESSION; HEAD AND NECK CANCER; HEAD AND NECK CARCINOMA; HUMAN; IMMUNOSURVEILLANCE; KIDNEY; KIDNEY CANCER; LIVER CANCER; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; METASTASIS; MUTAGENIC ACTIVITY; NEOPLASM; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STOMACH CANCER; TRANSFORMED CELL; TUMOR GENE; UTERINE CERVIX CANCER;

ANIMALS; HUMANS; LUNG NEOPLASMS; NICOTINE; SIGNAL TRANSDUCTION;

EID: 84901604202     PISSN: 1474175X     EISSN: 14741768     Source Type: Journal    
DOI: 10.1038/nrc3725     Document Type: Review

References (192)

1. Hoffmann, D., Hoffmann, I. & El-Bayoumy, K. The less harmful cigarette: a controversial issue. a tribute to Ernst, L. Wynder. Chem. Res. Toxicol. 14, 767-790 (2001).
2. Talhout, R. et al. Hazardous compounds in tobacco smoke. Int. J. Environ. Res. Publ. Health 8, 613-628 (2011).
3. Hecht, S. S. & Hoffmann, D. Tobacco-specific nitrosamines, an important group of carcinogens in tobacco and tobacco smoke. Carcinogenesis 9, 875-884 (1988).
4. Hecht, S. S. et al. Quantification of urinary metabolites of a tobacco-specific lung carcinogen after smoking cessation. Cancer Res. 59, 590-596 (1999).
5. Carmella, S. G., Borukhova, A., Desai, D. & Hecht, S. S. Evidence for endogenous formation of tobacco-specific nitrosamines in rats treated with tobacco alkaloids and sodium nitrite. Carcinogenesis 18, 587-592 (1997).
6. Caponnetto, P., Campagna, D., Papale, G., Russo, C. & Polosa, R. The emerging phenomenon of electronic cigarettes. Expert Rev. Respir. Med. 6, 63-74 (2012).
7. Bullen, C. et al. Electronic cigarettes for smoking cessation: a randomised controlled trial. Lancet 382, 1629-1637 (2013).
8. Frost-Pineda, K., Zedler, B. K., Liang, Q. & Roethig, H. J. Environmental tobacco smoke (ETS) evaluation of a third-generation electrically heated cigarette smoking system (EHCSS). Regul. Toxicol. Pharmacol. 52, 118-121 (2008).
9. Kim, H. J. & Shin, H. S. Determination of tobacco-specific nitrosamines in replacement liquids of electronic cigarettes by liquid chromatography-tandem mass spectrometry. J. Chromatogr. A 1291, 48-55 (2013).
10. Wessler, I. & Kirkpatrick, C. J. Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans. Br. J. Pharmacol. 154, 1558-1571 (2008).
11. Grando, S. A., Pittelkow, M. R. & Schallreuter, K. U. Adrenergic and cholinergic control in the biology of epidermis: physiological and clinical significance. J. Invest. Dermatol. 126, 1948-1965 (2006).
12. Improgo, M. R., Tapper, A. R. & Gardner, P. D. Nicotinic acetylcholine receptor-mediated mechanisms in lung cancer. Biochem. Pharmacol. 82, 1015-1021 (2011).
13. Singh, S., Pillai, S. & Chellappan, S. Nicotinic acetylcholine receptor signalling in tumour growth and metastasis. J. Oncol. 2011, 456743 (2011).
14. Basu, S. et al. Role of nicotine in gallbladder carcinoma: a preliminary report. J. Dig. Dis. 13, 536-540 (2012).
15. Wu, C. H., Lee, C. H. & Ho, Y. S. Nicotinic acetylcholine receptor-based blockade: Applications of molecular target for cancer therapy. Clin. Cancer Res. 17, 3533-3541 (2011).
16. Calleja-Macias, I. et al. Association of single nucleotide polymorphisms of nicotinic acetylcholine receptor subunits with cervical neoplasia. Life Sci. 91, 1099-1102 (2012).
17. Jensen, K., Afroze, S., Munshi, M. K., Guerrier, M. & Glaser, S. S. Mechanisms for nicotine in the development and progression of gastrointestinal cancers. Transl. Gastrointest. Cancer 1, 81-87 (2012).
18. Russo, P., Cardinale, A., Margaritora, S. & Cesario, A. Nicotinic receptor and tobacco-related cancer. Life Sci. 91, 1087-1092 (2012).
19. Koukourakis, G. & Zacharias, G. Nicotine has implications in different tumours types. Expert's eye making a literature analysis. J. BUON 16, 210-214 (2011).
20. Wang, Y. et al. Association of CHRNA5-A3-B4 variation with esophageal squamous cell carcinoma risk and smoking behaviours in a Chinese population. PLoS ONE 8, e67664 (2013).
21. Wu, H. et al. Is susceptibility locus for lung cancer in the 15q25 nicotinic acetylcholine receptor gene cluster CHRNA5-A3-B4 associated with risk of gastric cancer? Med. Oncol. 30, 576 (2013).
22. Lee, P. N. & Hamling, J. Systematic review of the relation between smokeless tobacco and cancer in Europe and North America. BMC Med. 7, 36 (2009).
23. Wickholm, S., Lahtinen, A., Ainamo, A. & Rautalahti, M. Adverse effects of Swedish smokeless tobacco "snus". Duodecim 128, 1089-1096 (2012).
24. Jacob, T., Clouden, N., Hingorani, A. & Ascher, E. The effect of cotinine on telomerase activity in human vascular smooth muscle cells. J. Cardiovasc. Surg. 50, 345-349 (2009).
25. Nakada, T. et al. Lung tumorigenesis promoted by anti-apoptotic effects of cotinine, a nicotine metabolite through activation of PI3K/Akt pathway. J. Toxicol. Sci. 37, 555-563 (2012).
26. Hukkanen, J., Jacob, P. 3rd & Benowitz, N. L. Metabolism and disposition kinetics of nicotine. Pharmacol. Rev. 57, 79-115 (2005).
27. Hecht, S. S. Biochemistry, biology, and carcinogenicity of tobacco-specific N-nitrosamines. Chem. Res. Toxicol. 11, 559-603 (1998).
28. Arredondo, J., Chernyavsky, A. I. & Grando, S. A. Nicotinic receptors mediate tumorigenic action of tobacco-derived nitrosamines on immortalized oral epithelial cells. Cancer Biol. Ther. 5, 511-517 (2006).
29. Arredondo, J., Chernyavsky, A. I. & Grando, S. A. The nicotinic receptor antagonists abolish pathobiologic effects of tobacco-derived nitrosamines on BEP2D cells. J. Cancer Res. Clin. Oncol. 132, 653-663 (2006).
30. Grando, S. A. Basic and clinical aspects of non-neuronal acetylcholine: biological and clinical significance of non-canonical ligands of epithelial nicotinic acetylcholine receptors. J. Pharmacol. Sci. 106, 174-179 (2008).
31. Catassi, A., Servent, D., Paleari, L., Cesario, A. & Russo, P. Multiple roles of nicotine on cell proliferation and inhibition of apoptosis: implications on lung carcinogenesis. Mutat. Res. 659, 221-231 (2008).
32. Ginzkey, C. et al. Nicotine induces DNA damage in human salivary glands. Toxicol. Lett. 184, 1-4 (2009).
33. Ginzkey, C. et al. Assessment of nicotine-induced DNA damage in a genotoxicological test battery. Mutat. Res. 751, 34-39 (2013).
34. Ginzkey, C. et al. Analysis of nicotine-induced DNA damage in cells of the human respiratory tract. Toxicol. Lett. 208, 23-29 (2012).
35. Galitovskiy, V., Chernyavsky, A. I., Edwards, R. A. & Grando, S. A. Muscle sarcomas and alopecia in A/J mice chronically treated with nicotine. Life Sci. 91, 1109-1112 (2012).
36. Nair, M. K., Chetty, D. J., Ho, H. & Chien, Y. W. Biomembrane permeation of nicotine: mechanistic studies with porcine mucosae and skin. J. Pharm. Sci. 86, 257-262 (1997).
37. Chen, L. L., Chetty, D. J. & Chien, Y. W. A mechanistic analysis to characterize oramucosal permeation properties. Int. J. Pharm. 184, 63-72 (1999).
38. Nielsen, H. M. & Rassing, M. R. Nicotine permeability across the buccal TR146 cell culture model and porcine buccal mucosa in vitro: effect of pH and concentration. Eur. J. Pharm. Sci. 16, 151-157 (2002).
39. Takami, K., Saito, H., Okuda, M., Takano, M. & Inui, K. I. Distinct characteristics of transcellular transport between nicotine and tetraethylammonium in LLC-PK1 cells. J. Pharmacol. Exp. Ther. 286, 676-680 (1998).
40. Fukada, A., Saito, H. & Inui, K. Transport mechanisms of nicotine across the human intestinal epithelial cell line Caco-2. J. Pharmacol. Exp. Ther. 302, 532-538 (2002).
41. Yildiz, D., Liu, Y. S., Ercal, N. & Armstrong, D. W. Comparison of pure nicotine-and smokeless tobacco extract-induced toxicities and oxidative stress. Arch. Environ. Contam. Toxicol. 37, 434-439 (1999).
42. Argentin, G. & Cicchetti, R. Genotoxic and antiapoptotic effect of nicotine on human gingival fibroblasts. Toxicol. Sci. 79, 75-81 (2004).
43. Oreffo, V. I., Lin, H. W., Padmanabhan, R. & Witschi, H. K-ras and p53 point mutations in 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone-induced hamster lung tumours. Carcinogenesis 14, 451-455 (1993).
44. Mayer, B. How much nicotine kills a human? Tracing back the generally accepted lethal dose to dubious self-experiments in the nineteenth century. Arch. Toxicol. 88, 5-7 (2014).
45. Sher, R. B., Cox, G. A., Mills, K. D. & Sundberg, J. P. Rhabdomyosarcomas in ageing A/J mice. PLoS ONE 6, e23498 (2011).
46. Sundberg, J. P. & Ichiki, T. in Handbook on genetically engineered mice (eds Sundberg, J. P. & Ichiki, T.) 223-229 (CRC Press, 2005).
47. 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. 42, 141-145 (1988).
48. Fu, X. W., Lindstrom, J. & Spindel, E. R. Nicotine activates and upregulates nicotinic acetylcholine receptors in bronchial epithelial cells. Am. J. Respir. Cell. Mol. Biol. 41, 93-99 (2009).
49. Song, P. & Spindel, E. R. Basic and clinical aspects of non-neuronal acetylcholine: expression of non-neuronal acetylcholine in lung cancer provides a new target for cancer therapy. J. Pharmacol. Sci. 106, 180-185 (2008).
50. Conti-Tronconi, B. M., McLane, K. E., Raftery, M. A., Grando, S. A. & Protti, M. P. The nicotinic acetylcholine receptor: structure and autoimmune pathology. Crit. Rev. Biochem. Mol. Biol. 29, 69-123 (1994).
51. Gerzanich, V. Wang, F., Kuryatov, A. & Lindstrom, J. α5 subunit alters desensitization, pharmacology, Ca2+ permeability and Ca2+ modulation of human neuronal α3 nicotinic receptors. J. Pharmacol. Exp. Ther. 286, 311-320 (1998).
52. Vainio, P. J. & Tuominen, R. K. Cotinine binding to nicotinic acetylcholine receptors in bovine chromaffin cell and rat brain membranes. Nicotine Tob. Res. 3, 177-182 (2001).
53. O'Leary, K., Parameswaran, N., McIntosh, J. M. & Quik, M. Cotinine selectively activates a subpopulation of α3/α6β2 nicotinic receptors in monkey striatum. J. Pharmacol. Exp. Ther. 325, 646-654 (2008).
54. Zia, S., Ndoye, A., Nguyen, V. T. & Grando, S. A. Nicotine enhances expression of the α3, α4, α5, and α7 nicotinic receptors modulating calcium metabolism and regulating adhesion and motility of respiratory epithelial cells. Res. Commun. Mol. Pathol. Pharmacol. 97, 243-262 (1997).
55. Lam, D. C. et al. Expression of nicotinic acetylcholine receptor subunit genes in non-small-cell lung cancer reveals differences between smokers and nonsmokers. Cancer Res. 67, 4638-4647 (2007).
56. West, K. A. et al. Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J. Clin. Invest. 111, 81-90 (2003).
57. Carlisle, D. L. et al. Nicotine activates cell-signalling pathways through muscle-type and neuronal nicotinic acetylcholine receptors in non-small cell lung cancer cells. Pulm. Pharmacol. Ther. 20, 629-641 (2007).
58. Arredondo, J. et al. Receptor-mediated tobacco toxicity: Regulation of gene expression through α3β2 nicotinic receptor in oral epithelial cells. Am. J. Pathol. 166, 597-613 (2005).
59. Arredondo, J., Chernyavsky, A. I., Jolkovsky, D. L., Pinkerton, K. E. & Grando, S. A. Receptor-mediated tobacco toxicity: cooperation of the Ras/Raf-1/MEK1/ERK and JAK-2/STAT-3 pathways downstream of α7 nicotinic receptor in oral keratinocytes. FASEB J. 20, 2093-2101 (2006).
60. Arredondo, J., Chernyavsky, A. I., Jolkovsky, D. L., Pinkerton, K. E. & Grando, S. A. Receptor-mediated tobacco toxicity: acceleration of sequential expression of α5 and α7 nicotinic receptor subunits in oral keratinocytes exposed to cigarette smoke. FASEB J. 22, 1356-1368 (2008).
61. Davis, R. et al. Nicotine promotes tumour growth and metastasis in mouse models of lung cancer. PLoS ONE 4, e7524 (2009).
62. Schuller, H. M. Regulatory Role of the α7nAChR in Cancer. Curr. Drug Targets 13, 680-687 (2012).
63. Denda, M., Fujiwara, S. & Hibino, T. Expression of voltage-gated calcium channel subunit α1C in epidermal keratinocytes and effects of agonist and antagonists of the channel on skin barrier homeostasis. Exp. Dermatol. 15, 455-460 (2006).
64. Fucile, S. Ca2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 35, 1-8 (2004).
65. Fucile, S., Sucapane, A. & Eusebi, F. Ca2+ permeability through rat cloned α9-containing nicotinic acetylcholine receptors. Cell Calcium 39, 349-355 (2006).
66. Zia, S., Ndoye, A., Lee, T. X., Webber, R. J. & Grando, S. A. Receptor-mediated inhibition of keratinocyte migration by nicotine involves modulations of calcium influx and intracellular concentration. J. Pharmacol. Exp. Ther. 293, 973-981 (2000).
67. Singh, G. S. Modification of acetylcholine action by bivalent cations on the perfused heart of the frog. Recent Adv. Stud Cardiac Struct. Metab. 7, 401-404 (1975).
68. Sorimachi, M., Nishimura, S. & Yamagami, K. Inability of Ca2+ influx through nicotinic ACh receptor channels to stimulate catecholamine secretion in bovine adrenal chromaffin cells: studies with fura-2 and SBFI microfluorometry. Jpn J. Physiol. 44, 343-356 (1994).
69. Chernyavsky, A. I., Arredondo, J., Karlsson, E., Wessler, I. & Grando, S. A. The Ras/Raf-1/MEK1/ERK signalling pathway coupled to integrin expression mediates cholinergic regulation of keratinocyte directional migration. J. Biol. Chem. 280, 39220-39228 (2005).
70. Chernyavsky, A. I., Arredondo, J., Marubio, L. M. & Grando, S. A. Differential regulation of keratinocyte chemokinesis and chemotaxis through distinct nicotinic receptor subtypes. J. Cell Sci. 117, 5665-5679 (2004).
71. Chernyavsky, A. I., Arredondo, J., Vetter, D. E. & Grando, S. A. Central role of α9 acetylcholine receptor in coordinating keratinocyte adhesion and motility at the initiation of epithelialization. Exp. Cell Res. 313, 3542-3555 (2007).
72. Tsurutani, J. et al. Tobacco components stimulate Akt-dependent proliferation and NF{κ}B-dependent survival in lung cancer cells. Carcinogenesis 26 1182-95 (2005).
73. Tsai, J. R. et al. Mitogen-activated protein kinase pathway was significantly activated in human bronchial epithelial cells by nicotine. DNA Cell Biol. 25, 312-322 (2006).
74. Shi, D. et al. Nicotine promotes proliferation of human nasopharyngeal carcinoma cells by regulating α7AChR, ERK, HIF-1α and VEGF/PEDF signalling. PLoS ONE 7, e43898 (2012).
75. Nishioka, T. et al. Sensitization of epithelial growth factor receptors by nicotine exposure to promote breast cancer cell growth. Breast Cancer Res. 13, R113 (2011).
76. Arredondo, J., Chernyavsky, A. I., Jolkovsky, D. L., Pinkerton, K. E. & Grando, S. A. Receptor-mediated tobacco toxicity: alterations of the NF-κB expression and activity downstream of α7 nicotinic receptor in oral keratinocytes. Life Sci. 80, 2191-2194 (2007).
77. Chernyavsky, A. I., Arredondo, J., Qian, J., Galitovskiy, V. & Grando, S. A. Coupling of ionic events to protein kinase signalling cascades upon activation of α7 nicotinic receptor: Cooperative regulation of α2-integrin expression and Rho-kinase activity. J. Biol. Chem. 284, 22140-22148 (2009).
78. van Hoek, M. L., Allen, C. S. & Parsons, S. J. Phosphotyrosine phosphatase activity associated with c-Src in large multimeric complexes isolated from adrenal medullary chromaffin cells. Biochem. J. 326, 271-277 (1997).
79. de Jonge, W. J. et al. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signalling pathway. Nature Immunol. 6, 844-851 (2005).
80. Kihara, T. et al. α7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A β-amyloid-induced neurotoxicity. J. Biol. Chem. 276, 13541-13546 (2001).
81. Wang, K. et al. Regulation of the neuronal nicotinic acetylcholine receptor by SRC family tyrosine kinases. J. Biol. Chem. 279, 8779-8786 (2004).
82. Fischer, H., Liu, D. M., Lee, A., Harries, J. C. & Adams, D. J. Selective modulation of neuronal nicotinic acetylcholine receptor channel subunits by Go-protein subunits. J. Neurosci. 25, 3571-3577 (2005).
83. Dasgupta, P. et al. Nicotine induces cell proliferation by β-arrestin-mediated activation of Src and Rb-Raf-1 pathways. J. Clin. Invest. 116, 2208-2217 (2006).
84. Chernyavsky, A. I., Arredondo, J., Piser, T., Karlsson, E. & Grando, S. A. Differential coupling of M1 muscarinic and α7 nicotinic receptors to inhibition of pemphigus acantholysis. J. Biol. Chem. 283, 3401-3408 (2008).
85. Wen, J., Fu, J. H., Zhang, W. & Guo, M. Lung carcinoma signalling pathways activated by smoking. Chin. J. Cancer 30, 551-558 (2011).
86. Dajas-Bailador, F. & Wonnacott, S. Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol. Sci. 25, 317-324 (2004).
87. Schaal, C. & Chellappan, S. P. Nicotine-mediated cell proliferation and tumour progression in smoking-related cancers. Mol. Cancer Res. 12, 14-23 (2014).
88. Dunckley, T. & Lukas, R. J. Nicotine modulates the expression of a diverse set of genes in the neuronal SH-SY5Y cell line. J. Biol. Chem. 278, 15633-15640 (2003).
89. Koshi, R., Sugano, N., Orii, H., Fukuda, T. & Ito, K. Microarray analysis of nicotine-induced changes in gene expression in a macrophage-like human cell line. J. Periodontal Res. 42, 518-526 (2007).
90. Grando, S. A. Cholinergic control of epidermal cohesion in norm and pathology. Exp. Dermatol. 15, 265-282 (2006).
91. Arredondo, J. et al. A receptor-mediated mechanism of nicotine toxicity in oral keratinocytes. Lab Invest. 81, 1653-1668 (2001).
92. Bavarva, J. H., Tae, H., Settlage, R. E. & Garner, H. R. Characterizing the genetic basis for nicotine induced cancer development: a transcriptome sequencing study. PLoS ONE 8, e67252 (2013).
93. Liu, D. et al. Intervention of nicotine on MNU-induced bladder cancer in rats. J. Huazhong Univ. Sci. Technolog. Med. Sci. 31, 103-106 (2011).
94. Cucina, A. et al. Nicotine stimulates proliferation and inhibits apoptosis in colon cancer cell lines through activation of survival pathways. J. Surg. Res. 178, 233-241 (2012).
95. Iskandar, A. R. et al. β-cryptoxanthin restores nicotine-reduced lung SIRT1 to normal levels and inhibits nicotine-promoted lung tumorigenesis and emphysema in A/J mice. Cancer Prev. Res. 6, 309-320 (2013).
96. Song, P. et al. Acetylcholine is synthesized by and acts as an autocrine growth factor for small cell lung carcinoma. Cancer Res. 63, 214-221 (2003).
97. Lau, J. K. et al. Inhibition of cholinergic signalling causes apoptosis in human bronchioalveolar carcinoma. Cancer Res. 73, 1328-1339 (2013).
98. Brown, K. C. et al. Nicotine induces the upregulation of the α7-nicotinic receptor (α7-nAChR) in human squamous cell lung cancer cells via the Sp1/GATA pathway. J. Biol. Chem. 288, 33049-33059 (2013).
99. Wang, F. et al. Chronic nicotine treatment upregulates human α3β2 but not α3β4 acetylcholine receptors stably transfected in human embryonic kidney cells. J. Biol. Chem. 273, 28721-28732 (1998).
100. Morimoto, N., Takemoto, S., Kawazoe, T. & Suzuki, S. Nicotine at a low concentration promotes wound healing. J. Surg. Res. 145, 199-204 (2008).
101. Liem, P. H., Morimoto, N., Ito, R., Kawai, K. & Suzuki, S. Treating a collagen scaffold with a low concentration of nicotine promoted angiogenesis and wound healing. J. Surg. Res. 182, 353-361 (2013).
102. Jacobi, J. et al. Nicotine accelerates angiogenesis and wound healing in genetically diabetic mice. Am. J. Pathol. 161, 97-104 (2002).
103. Narla, S. T. et al. Activation of developmental nuclear fibroblast growth factor receptor 1 signalling and neurogenesis in adult brain by α7 nicotinic receptor agonist. Stem Cells Transl. Med. 2, 776-788 (2013).
104. Mousa, S. & Mousa, S. A. Cellular and molecular mechanisms of nicotine's pro-angiogenesis activity and its potential impact on cancer. J. Cell. Biochem. 97, 1370-1378 (2006).
105. Mudo, G., Belluardo, N., Mauro, A. & Fuxe, K. Acute intermittent nicotine treatment induces fibroblast growth factor-2 in the subventricular zone of the adult rat brain and enhances neuronal precursor cell proliferation. Neuroscience 145, 470-483 (2007).
106. Belluardo, N. et al. Nicotine-induced fibroblast growth factor-2 restores the age-related decline of precursor cell proliferation in the subventricular zone of rat brain. Brain Res. 1193, 12-24 (2008).
107. Salimi, M. et al. Change in nicotine-induced VEGF, PGE2 and COX-2 expression following COX inhibition in human oral squamous cancer. J. Environ. Pathol. Toxicol. Oncol. 31, 349-356 (2012).
108. Moffett, J., Kratz, E. & Stachowiak, M. K. Increased tyrosine phosphorylation and novel cis-acting element mediate activation of the fibroblast growth factor-2 (FGF-2) gene by nicotinic acetylcholine receptor. New mechanism for trans-synaptic regulation of cellular development and plasticity. Brain Res. Mol. Brain Res. 55, 293-305 (1998).
109. Brown, K. C. et al. MG624, an α7-nAChR antagonist, inhibits angiogenesis via the Egr-1/FGF2 pathway. Angiogenesis 15, 99-114 (2012).
110. Baker, L. P. & Peng, H. B. Induction of acetylcholine receptor cluster formation by local application of growth factors in cultured Xenopus muscle cells. Neurosci. Lett. 185, 135-138 (1995).
111. Dai, Z. & Peng, H. B. The influence of basic fibroblast growth factor on acetylcholine receptors in cultured muscle cells. Neurosci. Lett. 144, 14-18 (1992).
112. Cucina, A. et al. Nicotine regulates basic fibroblastic growth factor and transforming growth factor β1 production in endothelial cells. Biochem. Biophys. Res. Commun. 257, 306-312 (1999).
113. Cucina, A. et al. Nicotine-induced smooth muscle cell proliferation is mediated through bFGF and TGF-β 1. Surgery 127, 316-322 (2000).
114. de Caestecker, M. P., Piek, E. & Roberts, A. B. Role of transforming growth factor-β signalling in cancer. J. Natl Cancer Inst. 92, 1388-1402 (2000).
115. Khalil, A. A., Jameson, M. J., Broaddus, W. C., Lin, P. S. & Chung, T. D. Nicotine enhances proliferation, migration, and radioresistance of human malignant glioma cells through EGFR activation. Brain Tumour Pathol. 30, 73-83 (2013).
116. Lee, C. H. et al. Crosstalk between nicotine and oestrogen-induced oestrogen receptor activation induces α9-nicotinic acetylcholine receptor expression in human breast cancer cells. Breast Cancer Res. Treat. 129, 331-345 (2011).
117. Schuller, H. M. Neurotransmission and cancer: implications for prevention and therapy. Anticancer Drugs 19, 655-671 (2008).
118. Nishioka, T. et al. Nicotine, through upregulating pro-survival signalling, cooperates with NNK to promote transformation. J. Cell Biochem. 109, 152-161 (2010).
119. Puliyappadamba, V. T. et al. Nicotine-induced survival signalling in lung cancer cells is dependent on their p53 status while its downregulation by curcumin is independent. Mol. Cancer 9, 220 (2010).
120. Junhui, Z. et al. Nicotine-reduced endothelial progenitor cell senescence through augmentation of telomerase activity via the PI3K/Akt pathway. Cytotherapy 11, 485-491 (2009).
121. Berger, M. R. & Zeller, W. J. Interaction of nicotine with anticancer treatment. Klin. Wochenschr. 66 (Suppl. 11), 127-133 (1988).
122. Warren, G. W. et al. Nicotinic modulation of therapeutic response in vitro and in vivo. Int. J. Cancer 131, 2519-2527 (2012).
123. Dinicola, S. et al. Nicotine increases survival in human colon cancer cells treated with chemotherapeutic drugs. Toxicol. In Vitro 27, 2256-2263 (2013).
124. Shen, T. et al. Nicotine induces resistance to chemotherapy in nasal epithelial cancer. Am. J. Rhinol. Allergy 24, e73-e77 (2010).
125. Banerjee, J., Al-Wadei, H. A. & Schuller, H. M. Chronic nicotine inhibits the therapeutic effects of gemcitabine on pancreatic cancer in vitro and in mouse xenografts. Eur. J. Cancer 49, 1152-1158 (2013).
126. Gergalova, G. et al. Mitochondria express α7 nicotinic acetylcholine receptors to regulate Ca2+ accumulation and cytochrome c release: study on isolated mitochondria. PLoS ONE 7, e31361 (2012).
127. Kalashnyk, O. M., Gergalova, G. L., Komisarenko, S. V. & Skok, M. V. Intracellular localization of nicotinic acetylcholine receptors in human cell lines. Life Sci. 91, 1033-1037 (2012).
128. Gergalova, G. Lykhmus, O., Komisarenko, S. & Skok, M. α7 Nicotinic acetylcholine receptors control cytochrome c release from isolated mitochondria through kinase-mediated pathways. Int. J. Biochem. Cell Biol. 49, 26-31 (2014).
129. Garrido, R., Mattson, M. P., Hennig, B. & Toborek, M. Nicotine protects against arachidonic-acid-induced caspase activation, cytochrome c release and apoptosis of cultured spinal cord neurons. J. Neurochem. 76, 1395-1403 (2001).
130. Yu, W. Mechawar, N., Krantic, S. & Quirion, R. α7 nicotinic receptor activation reduces β-amyloid-induced apoptosis by inhibiting caspase-independent death through phosphatidylinositol 3-kinase signalling. J. Neurochem. 119, 848-858 (2011).
131. Baldessarini, R. J. & Karobath, M. Biochemical physiology of central synapses. Annu. Rev. Physiol. 35, 273-304 (1973).
132. Dasgupta, P. et al. ARRB1-mediated regulation of E2F target genes in nicotine-induced growth of lung tumours. J. Natl Cancer Inst. 103, 317-333 (2011).
133. Lin, W., Hirata, N., Sekino, Y. & Kanda, Y. Role of α7-nicotinic acetylcholine receptor in normal and cancer stem cells. Curr. Drug Targets 13, 656-665 (2012).
134. Razani-Boroujerdi, S. & Sopori, M. L. Early manifestations of NNK-induced lung cancer: role of lung immunity in tumour susceptibility. Am. J. Respir. Cell. Mol. Biol. 36, 13-19 (2007).
135. Trevino, J. G. et al. Nicotine induces inhibitor of differentiation-1 in a Src-dependent pathway promoting metastasis and chemoresistance in pancreatic adenocarcinoma. Neoplasia 14, 1102-1114 (2012).
136. Yu, M. A. et al. Nicotine promotes acquisition of stem cell and epithelial-to-mesenchymal properties in head and neck squamous cell carcinoma. PLoS ONE 7, e51967 (2012).
137. Guo, L. et al. Mitochondrial reactive oxygen species mediates nicotine-induced hypoxia-inducible factor-1α expression in human non-small cell lung cancer cells. Biochim. Biophys. Acta 1822, 852-861 (2012).
138. Momi, N. et al. Nicotine/cigarette smoke promotes metastasis of pancreatic cancer through α7nAChR-mediated MUC4 upregulation. Oncogene 32, 1384-95 (2012).
139. Dasgupta, P. et al. Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines. Int. J. Cancer 124, 36-45 (2009).
140. Wei, P. L. et al. Nicotine enhances colon cancer cell migration by induction of fibronectin. Ann. Surg. Oncol. 18, 1782-1790 (2011).
141. Costa, F. & Soares, R. Nicotine: a pro-angiogenic factor. Life Sci. 84, 785-790 (2009).
142. Lee, J. & Cooke, J. P. Nicotine and pathological angiogenesis. Life Sci. 91, 1058-1064 (2012).
143. Heeschen, C. et al. Nicotine stimulates angiogenesis and promotes tumour growth and atherosclerosis. Nature Med. 7, 833-839 (2001).
144. Natori, T. et al. Nicotine enhances neovascularization and promotes tumour growth. Mol. Cells 16, 143-146 (2003).
145. Coppe, J. P. et al. A role for fibroblasts in mediating the effects of tobacco-induced epithelial cell growth and invasion. Mol. Cancer Res. 6, 1085-1098 (2008).
146. Arredondo, J. et al. Central role of fibroblast α3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine. Lab. Invest. 83, 207-225 (2003).
147. Topfer, K. et al. Tumour evasion from T cell surveillance. J. Biomed. Biotechnol. 2011, 918471 (2011).
148. Nouri-Shirazi, M. & Guinet, E. Exposure to nicotine adversely affects the dendritic cell system and compromises host response to vaccination. J. Immunol. 188, 2359-2370 (2012).
149. van Dijk, A. P. et al. Transdermal nicotine inhibits interleukin 2 synthesis by mononuclear cells derived from healthy volunteers. Eur. J. Clin. Invest. 28, 664-671 (1998).
150. Galitovskiy, V. et al. Cytokine-induced alterations of α7 nicotinic receptor in colonic CD4 T cells mediate dichotomous response to nicotine in murine models of TH1/TH17-versus TH2-mediated colitis. J. Immunol. 187, 2677-2687 (2011).
151. Qian, J., Galitovskiy, V., Chernyavsky, A. I., Marchenko, S. & Grando, S. A. Plasticity of the murine spleen T-cell cholinergic receptors and their role in in vitro differentiation of naive CD4 T cells toward the TH1, TH2 and TH17 lineages. Genes Immun. 12, 222-230 (2011).
152. Ostrand-Rosenberg, S. Immune surveillance: a balance between protumor and antitumor immunity. Curr. Opin. Genet. Dev. 18, 11-18 (2008).
153. Qiu, Y. H., Peng, Y. P., Jiang, J. L. & Wang, J. J. Effect of acetylcholine on in vitro IL-2 production and NK cell cytotoxicity of rats. Lymphology 37, 31-38 (2004).
154. Hao, J. et al. Nicotinic receptor β2 determines NK cell-dependent metastasis in a murine model of metastatic lung cancer. PLoS ONE 8, e57495 (2013).
155. Levy, E. M., Roberti, M. P. & Mordoh, J. Natural killer cells in human cancer: from biological functions to clinical applications. J. Biomed. Biotechnol. 2011, 676198 (2011).
156. Jiang, J. L., Qiu, Y. H. & Peng, Y. P. Effect of acetylcholine on the cytotoxicity of natural killer cells. Zhongguo Ying Yong Sheng Li Xue Za Zhi 21, 330-333 (in Chinese) (2005).
157. Improgo, M. R., Soll, L. G., Tapper, A. R. & Gardner, P. D. Nicotinic acetylcholine receptors mediate lung cancer growth. Front. Physiol. 4, 251 (2013).
158. Shih, Y. L. et al. Combination treatment with luteolin and quercetin enhances antiproliferative effects in nicotine-treated MDA-MB-231 cells by downregulating nicotinic acetylcholine receptors. J. Agr. Food Chem. 58, 235-241 (2010).
159. Tu, S. H. et al. Tea polyphenol (-)-epigallocatechin-3-gallate inhibits nicotine-and oestrogen-induced α9-nicotinic acetylcholine receptor upregulation in human breast cancer cells. Mol. Nutr. Food Res. 55, 455-466 (2011).
160. Catassi, A. et al. Targeting α7-nicotinic receptor for the treatment of pleural mesothelioma. Eur. J. Cancer 44, 2296-2311 (2008).
161. Grozio, A. et al. Natural agents targeting the α7-nicotinic- receptor in NSCLC: a promising prospective in anticancer drug development. Int. J. Cancer 122, 1911-1915 (2008).
162. Paleari, L. et al. Inhibition of nonneuronal α7-nicotinic receptor for lung cancer treatment. Am. J. Respir. Crit. Care Med. 179, 1141-1150 (2009).
163. Paleari, L. et al. Inhibition of non-neuronal α7-nicotinic receptor reduces tumorigenicity in A549 NSCLC xenografts. Int. J. Cancer 125, 199-211 (2009).
164. Kintz, P., Henrich, A., Cirimele, V. & Ludes, B. Nicotine monitoring in sweat with a sweat patch. J. Chromatogr. B Biomed. Sci. Appl. 705, 357-361 (1998).
165. Ortiz, A. & Grando, S. A. Smoking and the skin. Int. J. Dermatol. 51, 250-262 (2012).
166. Benoni, C. & Nilsson, A. Smoking habits in patients with inflammatory bowel disease. Scand. J. Gastroenterol. 19, 824-830 (1984).
167. Rubin, D. T. & Hanauer, S. B. Smoking and inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol 12, 855-862 (2000).
168. Marakoglu, K., Sezer, R. E., Toker, H. C. & Marakoglu, I. The recurrent aphthous stomatitis frequency in the smoking cessation people. Clin. Oral Investig. 11, 149-153 (2007).
169. Calabrese, E., Yanai, H., Shuster, D., Rubin, D. T. & Hanauer, S. B. Low-dose smoking resumption in ex-smokers with refractory ulcerative colitis. J. Crohns Colitis 6, 756-762 (2012).
170. Pullan, R. D. et al. Transdermal nicotine for active ulcerative colitis. New Engl. J. Med. 330, 811-815 (1994).
171. Hill, S. C., Stavrakoglou, A. & Coutts, I. R. Nicotine replacement therapy as a treatment for complex aphthosis. J. Dermatolog. Treat. 21, 317-318 (2010).
172. Rizvi, S. W. & McGrath, H. Jr. The therapeutic effect of cigarette smoking on oral/genital aphthosis and other manifestations of Behcet's disease. Clin. Exp. Rheumatol. 19, S77-78 (2001).
173. Scheid, P., Bohadana, A. & Martinet, Y. Nicotine patches for aphthous ulcers due to Behcet's syndrome. N. Engl. J. Med. 343, 1816-1817 (2000).
174. Kawabata, H. et al. Successful treatment of digital ulceration in Buerger's disease with nicotine chewing gum. Br. J. Dermatol. 140, 187-188 (1999).
175. Kanekura, T. & Kanzaki, T. Successful treatment of pyoderma gangrenosum with nicotine chewing gum. J. Dermatol. 22, 704-705 (1995).
176. Kanekura, T., Usuki, K. & Kanzaki, T. Nicotine for pyoderma gangrenosum. Lancet 345, 1058 (1995).
177. Kaklamani, V. G., Markomichelakis, N. & Kaklamanis, P. G. Could nicotine be beneficial for Behcet's disease? Clin. Rheumatol. 21, 341-342 (2002).
178. Westerman, R. A., Carr, R. W., Delaney, C. A., Morris, M. J. & Roberts, R. G. The role of skin nociceptive afferent nerves in blister healing. Clin. Exp. Neurol. 30, 39-60 (1993).
179. Kawashima, K. et al. Ubiquitous expression of acetylcholine and its biological functions in life forms without nervous systems. Life Sci. 80, 2206-2209 (2007).
180. Wessler, I., Kirkpatrick, C. J. & Racke, K. The cholinergic 'pitfall': acetylcholine, a universal cell molecule in biological systems, including humans. Clin. Exp. Pharmacol. Physiol. 26, 198-205 (1999).
181. Kaur-Knudsen, D., Bojesen, S. E., Tybjaerg-Hansen, A. & Nordestgaard, B. G. Nicotinic acetylcholine receptor polymorphism, smoking behaviour, and tobacco-related cancer and lung and cardiovascular diseases: a cohort study. J. Clin. Oncol. 29, 2875-2882 (2011).
182. Amos, C. I. et al. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nature Genet. 40, 616-622 (2008).
183. Shiraishi, K. et al. Contribution of nicotine acetylcholine receptor polymorphisms to lung cancer risk in a smoking-independent manner in the Japanese. Carcinogenesis 30, 65-70 (2009).
184. Chen, X. et al. Association of smoking with tumour size at diagnosis in non-small cell lung cancer. Lung Cancer 74, 378-383 (2011).
185. Shen, B. et al. Correlation between polymorphisms of nicotine acetylcholine acceptor subunit CHRNA3 and lung cancer susceptibility. Mol. Med. Rep. 6, 1389-1392 (2012).
186. Wei, C. et al. A case-control study of a sex-specific association between a 15q25 variant and lung cancer risk. Cancer Epidemiol. Biomarkers Prev. 20, 2603-2609 (2011).
187. Zhang, X. B. et al. Human chromosome 8p11 (CHRNB3-CHRNA6) region gene polymorphisms and susceptibility to lung cancer in Chinese Han population. Yi Chuan 33, 886-894 (2011).
188. Chikova, A. & Grando, S. A. Naturally occurring variants of human α9 nicotinic receptor differentially affect bronchial cell proliferation and transformation. PLoS ONE 6, e27978 (2011).
189. Zheng, X. et al. Functionally significant nicotine acetylcholine receptor subunit α5 promoter haplotypes are associated with susceptibility to lung cancer in Chinese. Cancer 117, 4714-4723 (2011).
190. Charpantier, E. et al. α7 neuronal nicotinic acetylcholine receptors are negatively regulated by tyrosine phosphorylation and Src-family kinases. J. Neurosci. 25, 9836-9849 (2005).
191. Warren, G. W. & Singh, A. K. Nicotine and lung cancer. J. Carcinog. 12, 1 (2013).
192. Learning about density of nicotine in e-cigarette. Electronic Cigarette Report [online], http://electroniccigarettereport.net/learning-about-density-of- nicotine-in-e-cigarette/(2012).