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Journal of Oncology
Volume 2011 (2011), Article ID 693424, 10 pages
http://dx.doi.org/10.1155/2011/693424
Review Article

From Smoking to Cancers: Novel Targets to Neuronal Nicotinic Acetylcholine Receptors

1Graduate Institute of Medical Sciences, Taipei Medical University, Taipei 110, Taiwan
2Department of Surgery, School of Medicine, Taipei Medical University, Shuang Ho Hospital, Taipei 235, Taiwan
3Department of Laboratory Medicine, Taipei Medical University Hospital, Taipei 110, Taiwan
4Center of Excellence for Cancer Research, Taipei Medical University, Taipei 110, Taiwan

Received 14 December 2010; Revised 18 February 2011; Accepted 17 March 2011

Academic Editor: Sushant Kachhap

Copyright © 2011 Chia-Hwa Lee et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. H. M. Schuller, “Is cancer triggered by altered signalling of nicotinic acetylcholine receptors?” Nature Reviews Cancer, vol. 9, no. 3, pp. 195–205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. S. S. Hecht and D. Hoffmann, “Tobacco-specific nitrosamines, an important group of carcinogens in tobacco and tobacco smoke,” Carcinogenesis, vol. 9, no. 6, pp. 875–884, 1988. View at Scopus
  3. P. Song, H. S. Sekhon, X. W. Fu, et al., “Activated cholinergic signaling provides a target in squamous cell lung carcinoma,” Cancer Research, vol. 68, no. 12, pp. 4693–4700, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Song, H. S. Sekhon, Y. Jia et al., “Acetylcholine is synthesized by and acts as an autocrine growth factor for small cell lung carcinoma,” Cancer Research, vol. 63, no. 1, pp. 214–221, 2003. View at Scopus
  5. C. H. Lee, Y. C. Chang, C. S. Chen, et al., “Crosstalk between nicotine and estrogen-induced estrogen receptor activation induces alpha9-nicotinic acetylcholine receptor expression in human breast cancer cells,” Breast Cancer Research and Treatment. In press.
  6. H. A. N. Al-Wadei, M. H. Al-Wadei, T. Masi, and H. M. Schuller, “Chronic exposure to estrogen and the tobacco carcinogen NNK cooperatively modulates nicotinic receptors in small airway epithelial cells,” Lung Cancer, vol. 69, no. 1, pp. 33–39, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. R. J. Hung, J. D. McKay, V. Gaborieau et al., “A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25,” Nature, vol. 452, no. 7187, pp. 633–637, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Liu, H. G. Vikis, D. Wang et al., “Familial aggregation of common sequence variants on 15q24-25.1 in lung cancer,” Journal of the National Cancer Institute, vol. 100, no. 18, pp. 1326–1330, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. J. Arredondo, A. I. Chernyavsky, D. L. Jolkovsky, K. E. Pinkerton, and S. A. Grando, “Receptor-mediated tobacco toxicity: acceleration of sequential expression of α5 and α7 nicotinic receptor subunits in oral keratinocytes exposed to cigarette smoke,” FASEB Journal, vol. 22, no. 5, pp. 1356–1368, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. C. I. Amos, X. Wu, P. Broderick et al., “Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1,” Nature Genetics, vol. 40, no. 5, pp. 616–622, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. I. R. Schlaepfer, N. R. Hoft, A. C. Collins et al., “The CHRNA5/A3/B4 gene cluster variability as an important determinant of early alcohol and tobacco initiation in young adults,” Biological Psychiatry, vol. 63, no. 11, pp. 1039–1046, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. H. M. Schuller, “Nitrosamines as nicotinic receptor ligands,” Life Sciences, vol. 80, no. 24-25, pp. 2274–2280, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. P. Russo, A. Catassi, A. Cesario, and D. Servent, “Development of novel therapeutic strategies for lung cancer: targeting the cholinergic system,” Current Medicinal Chemistry, vol. 13, no. 29, pp. 3493–3512, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Lindstrom, “Nicotinic acetylcholine receptors in health and disease,” Molecular Neurobiology, vol. 15, no. 2, pp. 193–222, 1997. View at Scopus
  15. C. Gotti and F. Clementi, “Neuronal nicotinic receptors: from structure to pathology,” Progress in Neurobiology, vol. 74, no. 6, pp. 363–396, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. C. M. Flores, R. M. DeCamp, S. Kilo, S. W. Rogers, and K. M. Hargreaves, “Neuronal nicotinic receptor expression in sensory neurons of the rat trigeminal ganglion: demonstration of α3β4, a novel subtype in the mammalian nervous system,” Journal of Neuroscience, vol. 16, no. 24, pp. 7892–7901, 1996. View at Scopus
  17. S. E. McCallum, A. C. Collins, R. Paylor, and M. J. Marks, “Deletion of the beta 2 nicotinic acetylcholine receptor subunit alters development of tolerance to nicotine and eliminates receptor upregulation,” Psychopharmacology, vol. 184, no. 3-4, pp. 314–327, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Klink, A. De Kerchove D'Exaerde, M. Zoli, and J. P. Changeux, “Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei,” Journal of Neuroscience, vol. 21, no. 5, pp. 1452–1463, 2001. View at Scopus
  19. L. C. Gahring, E. L. Days, T. Kaasch et al., “Pro-inflammatory cytokines modify neuronal nicotinic acetylcholine receptor assembly,” Journal of Neuroimmunology, vol. 166, no. 1-2, pp. 88–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. E. X. Albuquerque, E. F. R. Pereira, N. G. Castro et al., “Nicotinic receptor function in the mammalian central nervous system,” Annals of the New York Academy of Sciences, vol. 757, pp. 48–72, 1995. View at Publisher · View at Google Scholar · View at Scopus
  21. R. S. Broide and F. M. Leslie, “The α7 nicotinic acetylcholine receptor in neuronal plasticity,” Molecular Neurobiology, vol. 20, no. 1, pp. 1–16, 1999. View at Scopus
  22. M. Quik, J. Philie, and J. Choremis, “Modulation of α7 nicotinic receptor-mediated calcium influx by nicotinic agonists,” Molecular Pharmacology, vol. 51, no. 3, pp. 499–506, 1997. View at Scopus
  23. Y. S. Ho, C. H. Chen, Y. J. Wang et al., “Tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) induces cell proliferation in normal human bronchial epithelial cells through NFκB activation and cyclin D1 up-regulation,” Toxicology and Applied Pharmacology, vol. 205, no. 2, pp. 133–148, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. R. J. Chen, Y. S. Ho, H. R. Guo, and Y. J. Wang, “Rapid activation of Stat3 and ERK1/2 by nicotine modulates cell proliferation in human bladder cancer cells,” Toxicological Sciences, vol. 104, no. 2, pp. 283–293, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. P. L. Wei, Y. J. Chang, Y. S. Ho, et al., “Tobacco-specific carcinogen enhances colon cancer cell migration through alpha7-nicotinic acetylcholine receptor,” Annals of Surgery, vol. 249, pp. 978–985, 2009.
  26. C. H. Lee, C. S. Huang, C. S. Chen, et al., “Overexpression and activation of the {alpha}9-nicotinic receptor during tumorigenesis in human breast epithelial cells,” Journal of the National Cancer Institute, vol. 102, pp. 1322–1335, 2010.
  27. C. S. Chen, C. H. Lee, C. D. Hsieh et al., “Nicotine-induced human breast cancer cell proliferation attenuated by garcinol through down-regulation of the nicotinic receptor and cyclin D3 proteins,” Breast Cancer Research and Treatment, pp. 1–15, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. L. Shih, H. C. Liu, C. S. Chen et al., “Combination treatment with luteolin and quercetin enhances antiproliferative effects in nicotine-treated MDA-MB-231 cells by down-regulating nicotinic acetylcholine receptors,” Journal of Agricultural and Food Chemistry, vol. 58, no. 1, pp. 235–241, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Abreu-Villaça, F. J. Seidler, D. Qiao et al., “Short-term adolescent nicotine exposure has immediate and persistent effects on cholinergic systems: critical periods, patterns of exposure, dose thresholds,” Neuropsychopharmacology, vol. 28, no. 11, pp. 1935–1949, 2003. View at Scopus
  30. R. G. Taylor, G. Woodman, and S. W. Clarke, “Plasma nicotine concentration and the white blood cell count in smokers,” Thorax, vol. 41, no. 5, pp. 407–408, 1986. View at Scopus
  31. B. V. R. Sastry, M. B. Chance, G. Singh, J. L. Horn, and V. E. Janson, “Distribution and retention of nicotine and its metabolite, cotinine, in the rat as a function of time,” Pharmacology, vol. 50, no. 2, pp. 128–136, 1995. View at Scopus
  32. C. T. C. Okoli, T. Kelly, and E. J. Hahn, “Secondhand smoke and nicotine exposure: a brief review,” Addictive Behaviors, vol. 32, no. 10, pp. 1977–1988, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Arredondo, A. I. Chernyavsky, and S. A. Grando, “The nicotinic receptor antagonists abolish pathobiologic effects of tobacco-derived nitrosamines on BEP2D cells,” Journal of Cancer Research and Clinical Oncology, vol. 132, no. 10, pp. 653–663, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Arredondo, A. I. Chernyavsky, and S. A. Grando, “Nicotinic receptors mediate tumorigenic action of tobacco-derived nitrosamines on immortalized oral epithelial cells,” Cancer Biology and Therapy, vol. 5, no. 5, pp. 511–517, 2006. View at Scopus
  35. D. Kishino, K. Kiura, N. Takigawa et al., “Effect of gefitinib on N-nitrosamine-4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone induced lung tumorigenesis in A/J mice,” Lung Cancer, vol. 65, no. 3, pp. 284–289, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Nishioka, J. Guo, D. Yamamoto, L. Chen, P. Huppi, and C. Y. Chen, “Nicotine, through upregulating pro-survival signaling, cooperates with NNK to promote transformation,” Journal of Cellular Biochemistry, vol. 109, no. 1, pp. 152–161, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Mei, H. Hu, M. McEntee, H. Plummer, P. Song, and H. C. R. Wang, “Transformation of non-cancerous human breast epithelial cell line MCF10A by the tobacco-specific carcinogen NNK,” Breast Cancer Research and Treatment, vol. 79, no. 1, pp. 95–105, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. H. M. Schuller, “Neurotransmitter receptor-mediated signaling pathways as modulators of carcinogenesis,” Progress in Experimental Tumor Research, vol. 39, pp. 45–63, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Girod, G. Crabtree, G. Ernstrom et al., “Heteromeric complexes of α5 and/or α7 subunits. Effects of calcium and potential role in nicotine-induced presynaptic facilitation,” Annals of the New York Academy of Sciences, vol. 868, pp. 578–590, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Fucile, “Ca2+ permeability of nicotinic acetylcholine receptors,” Cell Calcium, vol. 35, no. 1, pp. 1–8, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. V. Itier and D. Bertrand, “Neuronal nicotinic receptors: from protein structure to function,” FEBS Letters, vol. 504, no. 3, pp. 118–125, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. J. M. Lindstrom, “Nicotinic acetylcholine receptors of muscles and nerves: comparison of their structures, functional roles, and vulnerability to pathology,” Annals of the New York Academy of Sciences, vol. 998, pp. 41–52, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. J. M. Cunningham, V. A. Lennon, E. H. Lambert, and B. Scheithauer, “Acetylcholine receptors in small cell carcinomas,” Journal of Neurochemistry, vol. 45, no. 1, pp. 159–167, 1985. View at Scopus
  44. S. A. Grando, “Receptor-mediated action of nicotine in human skin,” International Journal of Dermatology, vol. 40, no. 11, pp. 691–693, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. J. D. Minna, “Nicotine exposure and bronchial epithelial cell nicotinic acetylcholine receptor expression in the pathogenesis of lung cancer,” Journal of Clinical Investigation, vol. 111, no. 1, pp. 31–33, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Zeidler, K. Albermann, and S. Lang, “Nicotine and apoptosis,” Apoptosis, vol. 12, no. 11, pp. 1927–1943, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. E. Sher, A. Codignola, M. Passafaro et al., “Nicotinic receptors and calcium channels in small cell lung carcinoma: functional role, modulation, and autoimmunity,” Annals of the New York Academy of Sciences, vol. 841, pp. 606–624, 1998. View at Scopus
  48. B. M. Conti-Fine, D. Navaneetham, S. Lei, and A. D. J. Maus, “Neuronal nicotinic receptors in non-neuronal cells: new mediators of tobacco toxicity?” European Journal of Pharmacology, vol. 393, no. 1–3, pp. 279–294, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. B. J. Sheppard, M. Williams, H. K. Plummer, and H. M. Schuller, “Activation of voltage-operated Ca2+-channels in human small cell lung carcinoma by the tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone,” International Journal of Oncology, vol. 16, no. 3, pp. 513–518, 2000. View at Scopus
  50. C. Heeschen, J. J. Jang, M. Weis et al., “Nicotine stimulates angiogenesis and promotes tumor growth and atherosclerosis,” Nature Medicine, vol. 7, no. 7, pp. 833–839, 2001. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Heeschen, M. Weis, and J. P. Cooke, “Nicotine promotes arteriogenesis,” Journal of the American College of Cardiology, vol. 41, no. 3, pp. 489–496, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Heeschen, M. Weis, A. Aicher, S. Dimmeler, and J. P. Cooke, “A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors,” Journal of Clinical Investigation, vol. 110, no. 4, pp. 527–536, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. J. P. Cooke and H. Bitterman, “Nicotine and angiogenesis: a new paradigm for tobacco-related diseases,” Annals of Medicine, vol. 36, no. 1, pp. 33–40, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. P. Dasgupta and S. P. Chellappan, “Nicotine-mediated cell proliferation and angiogenesis: new twists to an old story,” Cell Cycle, vol. 5, no. 20, pp. 2324–2328, 2006. View at Scopus
  55. P. Dasgupta, R. Kinkade, B. Joshi, C. DeCook, E. Haura, and S. Chellappan, “Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and survivin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 16, pp. 6332–6337, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. R. D. Egleton, K. C. Brown, and P. Dasgupta, “Angiogenic activity of nicotinic acetylcholine receptors: implications in tobacco-related vascular diseases,” Pharmacology and Therapeutics, vol. 121, no. 2, pp. 205–223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Avogaro and G. P. Fadini, “The janus face of nicotinic angiogenesis,” Journal of the American College of Cardiology, vol. 48, no. 12, pp. 2561–2563, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. J. P. Cooke, “Angiogenesis and the role of the endothelial nicotinic acetylcholine receptor,” Life Sciences, vol. 80, no. 24-25, pp. 2347–2351, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. D. Adamopoulos, P. Van De Borne, and J. F. Argacha, “New insights into the sympathetic, endothelial and coronary effects of nicotine,” Clinical and Experimental Pharmacology and Physiology, vol. 35, no. 4, pp. 458–463, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Chu, J. Guo, and C. Y. Chen, “Long-term exposure to nicotine, via Ras pathway, induces cyclin D1 to stimulate G cell cycle transition,” Journal of Biological Chemistry, vol. 280, no. 8, pp. 6369–6379, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. B. S. Conklin, W. Zhao, D. S. Zhong, and C. Chen, “Nicotine and cotinine up-regulate vascular endothelial growth factor expression in endothelial cells,” American Journal of Pathology, vol. 160, no. 2, pp. 413–418, 2002. View at Scopus
  62. L. Xu and X. Deng, “Protein kinase Ciota promotes nicotine-induced migration and invasion of cancer cells via phosphorylation of micro- and m-calpains,” The Journal of Biological Chemistry, vol. 281, pp. 4457–4466, 2006.
  63. V. Y. Shin, W. K. K. Wu, K. M. Chu et al., “Nicotine induces cyclooxygenase-2 and vascular endothelial growth factor receptor-2 in association with tumor-associated invasion and angiogenesis in gastric cancer,” Molecular Cancer Research, vol. 3, no. 11, pp. 607–615, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. M. K. C. Ng, J. Wu, E. Chang et al., “A central role for nicotinic cholinergic regulation of growth factor-induced endothelial cell migration,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 1, pp. 106–112, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Yu, N. F. Huang, K. D. Wilson et al., “NAChRs mediate human embryonic stem cell-derived endothelial cells: proliferation, apoptosis, and angiogenesis,” PLoS ONE, vol. 4, no. 9, article e7040, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. K. A. West, J. Brognard, A. S. Clark et al., “Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells,” Journal of Clinical Investigation, vol. 111, no. 1, pp. 81–90, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Tsurutani, S. S. Castillo, J. Brognard et al., “Tobacco components stimulate Akt-dependent proliferation and NFκB-dependent survival in lung cancer cells,” Carcinogenesis, vol. 26, no. 7, pp. 1182–1195, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. E. Gemenetzidis, A. Bose, A. M. Riaz et al., “FOXM1 upregulation is an early event in human squamous cell carcinoma and it is enhanced by nicotine during malignant transformation,” PLoS ONE, vol. 4, no. 3, article e4849, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. S. S. Hecht, “Cigarette smoking and lung cancer: chemical mechanisms and approaches to prevention,” Lancet Oncology, vol. 3, no. 8, pp. 461–469, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. R. B. Everson, E. Randerath, R. M. Santella, T. A. Avitts, I. B. Weinstein, and K. Randerath, “Quantitative associations between DNA damage in human placenta and maternal smoking and birth weight,” Journal of the National Cancer Institute, vol. 80, no. 8, pp. 567–576, 1988. View at Scopus
  71. R. K. Lin, Y. S. Hsieh, P. Lin et al., “The tobacco-specific carcinogen NNK induces DNA methyltransferase 1 accumulation and tumor suppressor gene hypermethylation in mice and lung cancer patients,” Journal of Clinical Investigation, vol. 120, no. 2, pp. 521–532, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. E. R. Spindel, “Is nicotine the estrogen of lung cancer?” American Journal of Respiratory and Critical Care Medicine, vol. 179, no. 12, pp. 1081–1082, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. J. Zuo, J. Treadaway, T. W. Buckner, and B. Fritzsch, “Visualization of α9 acetylcholine receptor expression in hair cells of transgenic mice containing a modified bacterial artificial chromosome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 24, pp. 14100–14105, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. I. Wessler, C. J. Kirkpatrick, and K. Racké, “Non-neuronal acetylcholine, a locally acting molecule, widely distributed in biological systems: expression and function in humans,” Pharmacology and Therapeutics, vol. 77, no. 1, pp. 59–79, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. H. S. Sekhon, J. Yibing, R. Raab et al., “Prenatal nicotine increases pulmonary α7 nicotinic receptor expression and alters fetal lung development in monkeys,” Journal of Clinical Investigation, vol. 103, no. 5, pp. 637–647, 1999. View at Scopus
  76. I. Wessler and C. J. Kirkpatrick, “Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans,” British Journal of Pharmacology, vol. 154, no. 8, pp. 1558–1571, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. Y. Z. Fan, H. Chang, YE. Yu, J. Liu, and R. Wang, “Thymosin α suppresses proliferation and induces apoptosis in human leukemia cell lines,” Peptides, vol. 27, no. 9, pp. 2165–2173, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. J. Gould, H. L. Reeve, P. F. T. Vaughan, and C. Peers, “Nicotinic acetylcholine receptors in human neuroblastoma (SH-SY5Y) cells,” Neuroscience Letters, vol. 145, no. 2, pp. 201–204, 1992. View at Publisher · View at Google Scholar · View at Scopus
  79. R. M. Yan, Y. M. Chiung, C. Y. Pan, J. H. Liu, and P. S. Liu, “Effects of dichlorobenzene on acetylcholine receptors in human neuroblastoma SH-SY5Y cells,” Toxicology, vol. 253, no. 1–3, pp. 28–35, 2008. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Zhang, S. Togo, K. Minakata et al., “Distinct roles of cholinergic receptors in small cell lung cancer cells,” Anticancer Research, vol. 30, no. 1, pp. 97–106, 2010. View at Scopus
  81. H. M. Schuller, “Cell type specific, receptor-mediated modulation of growth kinetics in human lung cancer cell lines by nicotine and tobacco-related nitrosamines,” Biochemical Pharmacology, vol. 38, no. 20, pp. 3439–3442, 1989. View at Publisher · View at Google Scholar · View at Scopus
  82. D. C. L. Lam, L. Girard, R. Ramirez et al., “Expression of nicotinic acetylcholine receptor subunit genes in non-small-cell lung cancer reveals differences between smokers and nonsmokers,” Cancer Research, vol. 67, no. 10, pp. 4638–4647, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. X. Sun, J. D. Ritzenthaler, X. Zhong, Y. Zheng, J. Roman, and S. Han, “Nicotine stimulates PPARβ/δ expression in human lung carcinoma cells through activation of P13K/mTOR and suppression of AP-2α,” Cancer Research, vol. 69, no. 16, pp. 6445–6453, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. S. A. Grando, “Basic and clinical aspects of non-neuronal acetylcholine: biological and clinical significance of non-canonical ligands of epithelial nicotinic acetylcholine receptors,” Journal of Pharmacological Sciences, vol. 106, no. 2, pp. 174–179, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. L. Paleari, A. Cesario, M. Fini, and P. Russo, “α7-Nicotinic receptor antagonists at the beginning of a clinical era for NSCLC and Mesothelioma?” Drug Discovery Today, vol. 14, no. 17-18, pp. 822–836, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. A. Paliwal, T. Vaissière, A. Krais et al., “Aberrant DNA methylation links cancer susceptibility locus 15q25.1 to apoptotic regulation and lung cancer,” Cancer Research, vol. 70, no. 7, pp. 2779–2788, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. H. M. Schuller and M. Orloff, “Tobacco-specific carcinogenic nitrosamines: ligands for nicotinic acetylcholine receptors in human lung cancer cells,” Biochemical Pharmacology, vol. 55, no. 9, pp. 1377–1384, 1998. View at Publisher · View at Google Scholar · View at Scopus
  88. S. S. Hecht, “Tobacco smoke carcinogens and lung cancer,” Journal of the National Cancer Institute, vol. 91, no. 14, pp. 1194–1210, 1999. View at Scopus
  89. H. K. Plummer, M. Dhar, and H. M. Schuller, “Expression of the α7 nicotinic acetylcholine receptor in human lung cells,” Respiratory Research, vol. 6, p. 29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. S. F. Saccone, A. L. Hinrichs, N. L. Saccone et al., “Cholinergic nicotinic receptor genes implicated in a nicotine dependence association study targeting 348 candidate genes with 3713 SNPs,” Human Molecular Genetics, vol. 16, no. 1, pp. 36–49, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. R. Maneckjee and J. D. Minna, “Opioid and nicotine receptors affect growth regulation of human lung cancer cell lines,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 9, pp. 3294–3298, 1990. View at Publisher · View at Google Scholar · View at Scopus
  92. R. Maneckjee and J. D. Minna, “Opioids induce while nicotine suppresses apoptosis in human lung cancer cells,” Cell Growth and Differentiation, vol. 5, no. 10, pp. 1033–1040, 1994. View at Scopus
  93. M. G. Cattaneo, A. Codignola, L. M. Vicentini, F. Clementi, and E. Sher, “Nicotine stimulates a serotonergic autocrine loop in human small-cell lung carcinoma,” Cancer Research, vol. 53, no. 22, pp. 5566–5568, 1993. View at Scopus
  94. H. M. Schuller, “Neurotransmission and cancer: implications for prevention and therapy,” Anti-Cancer Drugs, vol. 19, no. 7, pp. 655–671, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. L. Paleari, A. Catassi, M. Ciarlo et al., “Role of α7-nicotinic acetylcholine receptor in human non-small cell lung cancer proliferation,” Cell Proliferation, vol. 41, no. 6, pp. 936–959, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Zheng, J. D. Ritzenthaler, J. Roman, and S. Han, “Nicotine stimulates human lung cancer cell growth by inducing fibronectin expression,” American Journal of Respiratory Cell and Molecular Biology, vol. 37, no. 6, pp. 681–690, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. P. Dasgupta, S. Rastogi, S. Pillai et al., “Nicotine induces cell proliferation by β-arrestin-mediated activation of Src and Rb-Raf-1 pathways,” Journal of Clinical Investigation, vol. 116, no. 8, pp. 2208–2217, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Trombino, A. Cesario, S. Margaritora et al., “α7-nicotinic acetylcholine receptors affect growth regulation of human mesothelioma cells: role of mitogen-activated protein kinase pathway,” Cancer Research, vol. 64, no. 1, pp. 135–145, 2004. View at Publisher · View at Google Scholar · View at Scopus
  99. L. Paleari, A. Grozio, A. Cesario, and P. Russo, “The cholinergic system and cancer,” Seminars in Cancer Biology, vol. 18, no. 3, pp. 211–217, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. L. Paleari, F. Sessa, A. Catassi, et al., “Inhibition of non-neuronal alpha7-nicotinic receptor reduces tumorigenicity in A549 NSCLC xenografts,” International Journal of Cancer, vol. 125, pp. 199–211, 2009.
  101. L. Paleari, E. Negri, A. Catassi, et al., “Inhibition of nonneuronal alpha7-nicotinic receptor for lung cancer treatment,” American Journal of Respiratory and Critical Care Medicine, vol. 179, pp. 1141–1150, 2009.
  102. R. M. Eglen, “Muscarinic receptor subtype pharmacology and physiology,” Progress in Medicinal Chemistry, vol. 43, pp. 105–136, 2005. View at Publisher · View at Google Scholar · View at Scopus
  103. P. Dasgupta, W. Rizwani, S. Pillai et al., “Nicotine induces cell proliferation, invasion and epithelial-mesenchymal transition in a variety of human cancer cell lines,” International Journal of Cancer, vol. 124, no. 1, pp. 36–45, 2009. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. Zhou, X. Gu, E. Ashayeri, R. Zhang, and R. Sridhar, “Nicotine decreases the cytotoxicity of doxorubicin towards MCF-7 and KB-3.1 human cancer cells in culture,” Journal of the National Medical Association, vol. 99, no. 4, pp. 319–327, 2007. View at Scopus
  105. J. Guo, S. Ibaragi, T. Zhu et al., “Nicotine promotes mammary tumor migration via a signaling cascade involving protein kinase C and cdc42,” Cancer Research, vol. 68, no. 20, pp. 8473–8481, 2008. View at Publisher · View at Google Scholar · View at Scopus
  106. K. C. Johnson and S. A. Glantz, “Evidence secondhand smoke causes breast cancer in 2005 stronger than for lung cancer in 1986,” Preventive Medicine, vol. 46, no. 6, pp. 492–496, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Jacobi, J. J. Jang, U. Sundram, H. Dayoub, L. F. Fajardo, and J. P. Cooke, “Nicotine accelerates angiogenesis and wound healing in genetically diabetic mice,” American Journal of Pathology, vol. 161, no. 1, pp. 97–104, 2002. View at Scopus
  108. N. Morimoto, S. Takemoto, T. Kawazoe, and S. Suzuki, “Nicotine at a low concentration promotes wound healing,” Journal of Surgical Research, vol. 145, no. 2, pp. 199–204, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. T. Teaktong, A. J. Graham, J. A. Court et al., “Nicotinic acetylcholine receptor immunohistochemistry in Alzheimer's disease and dementia with Lewy bodies: differential neuronal and astroglial pathology,” Journal of the Neurological Sciences, vol. 225, no. 1-2, pp. 39–49, 2004. View at Publisher · View at Google Scholar · View at Scopus
  110. W. F. Yu, Z. Z. Guan, N. Bogdanovic, and A. Nordberg, “High selective expression of alpha7 nicotinic receptors on astrocytes in the brains of patients with sporadic Alzheimer's disease and patients carrying Swedish APP 670/671 mutation: a possible association with neuritic plaques,” Experimental Neurology, vol. 192, pp. 215–225, 2005.
  111. A. Taly, P. J. Corringer, D. Guedin, P. Lestage, and J. P. Changeux, “Nicotinic receptors: allosteric transitions and therapeutic targets in the nervous system,” Nature Reviews Drug Discovery, vol. 8, no. 9, pp. 733–750, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. C. M. Martin-Ruiz, J. A. Court, E. Molnar, et al., “Alpha4 but not alpha3 and alpha7 nicotinic acetylcholine receptor subunits are lost from the temporal cortex in Alzheimer's disease,” Journal of Neurochemistry, vol. 73, pp. 1635–1640, 1999.
  113. E. D. Levin and B. B. Simon, “Nicotinic acetylcholine involvement in cognitive function in animals,” Psychopharmacology (Berl), vol. 138, pp. 217–230, 1998.
  114. P. N. Lee, “Smoking and Alzheimer's disease: a review of the epidemiological evidence,” Neuroepidemiology, vol. 13, no. 4, pp. 131–144, 1994. View at Scopus
  115. C. W. Luetje, K. Wada, S. Rogers et al., “Neurotoxins distinguish between different neuronal nicotinic acetylcholine receptor subunit combinations,” Journal of Neurochemistry, vol. 55, no. 2, pp. 632–640, 1990.
  116. M. W. Decker, D. J. Anderson, J. D. Brioni et al., “Erysodine, a competitive antagonist at neuronal nicotinic acetylcholine receptors,” European Journal of Pharmacology, vol. 280, no. 1, pp. 79–89, 1995. View at Publisher · View at Google Scholar · View at Scopus
  117. M. W. Holladay, M. J. Dart, and J. K. Lynch, “Neuronal nicotinic acetylcholine receptors as targets for drug discovery,” Journal of Medicinal Chemistry, vol. 40, no. 26, pp. 4169–4194, 1997. View at Publisher · View at Google Scholar · View at Scopus
  118. M. A. Sciamanna, G. E. Griesmann, C. L. Williams, and V. A. Lennon, “Nicotinic acetylcholine receptors of muscle and neuronal (α) types coexpressed in a small cell lung carcinoma,” Journal of Neurochemistry, vol. 69, no. 6, pp. 2302–2311, 1997. View at Scopus
  119. D. W. Sandall, N. Satkunanathan, D. A. Keays et al., “A novel α-conotoxin identified by gene sequencing is active in suppressing the vascular response to selective stimulation of sensory nerves in vivo,” Biochemistry, vol. 42, no. 22, pp. 6904–6911, 2003. View at Publisher · View at Google Scholar
  120. J. M. McIntosh, A. D. Santos, and B. M. Olivera, “Conus peptides targeted to specific nicotinic acetylcholine receptor subtypes,” Annual Review of Biochemistry, vol. 68, pp. 59–88, 1999. View at Publisher · View at Google Scholar · View at Scopus
  121. H. R. Arias and M. P. Blanton, “α-Conotoxins,” International Journal of Biochemistry and Cell Biology, vol. 32, no. 10, pp. 1017–1028, 2000. View at Publisher · View at Google Scholar · View at Scopus
  122. M. I. Damaj, W. Glassco, M. D. Aceto, and B. R. Martin, “Antinociceptive and pharmacological effects of metanicotine, a selective nicotinic agonist,” Journal of Pharmacology and Experimental Therapeutics, vol. 291, no. 1, pp. 390–398, 1999. View at Scopus
  123. S. D. Gilbert, T. M. Clark, and C. M. Flores, “Antihyperalgesic activity of epibatidine in the formalin model of facial pain,” Pain, vol. 89, no. 2-3, pp. 159–165, 2001. View at Publisher · View at Google Scholar · View at Scopus
  124. Y. Wang, D. M. Su, R. H. Wang, Y. Liu, and H. Wang, “Antinociceptive effects of choline against acute and inflammatory pain,” Neuroscience, vol. 132, no. 1, pp. 49–56, 2005. View at Publisher · View at Google Scholar · View at Scopus
  125. S. H. Tu, C. Y. Ku, C. T. Ho, et al., “Tea polyphenol (-)-epigallocatechin-3-gallate inhibits nicotine- and estrogen-induced alpha9-nicotinic acetylcholine receptor upregulation in human breast cancer cells,” Molecular Nutrition & Food Research, vol. 55, pp. 455–466, 2011.