About this Journal Submit a Manuscript Table of Contents
Journal of Oncology
Volume 2011 (2011), Article ID 456743, 11 pages
http://dx.doi.org/10.1155/2011/456743
Review Article

Nicotinic Acetylcholine Receptor Signaling in Tumor Growth and Metastasis

Department of Tumor Biology, H. Lee Moffitt Cancer Center and Research Institute, 12902 Magnolia Drive, Tampa, FL 33612, USA

Received 19 December 2010; Accepted 28 January 2011

Academic Editor: Venkateshwar Keshamouni

Copyright © 2011 Sandeep Singh 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. D. M. Burns, “Tobacco-related diseases,” Seminars in Oncology Nursing, vol. 19, no. 4, pp. 244–249, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Vineis, M. Alavanja, P. Buffler et al., “Tobacco and cancer: recent epidemiological evidence,” Journal of the National Cancer Institute, vol. 96, no. 2, pp. 99–106, 2004. View at Scopus
  3. “Smoking-attributable mortality, years of potential life lost, and productivity losses—United States, 2000–2004,” Morbidity and Mortality Weekly Report, vol. 57, no. 45, pp. 1226–1228, 2008.
  4. Tobacco Smoking, vol. 38 of IARC Monogr Eval Carcinog Risk Chem Hum, IARC, Lyon, France, 1986.
  5. K. D. Brunnemann and D. Hoffmann, “Analytical studies on tobacco-specific N-nitrosamines in tobacco and tobacco smoke,” Critical Reviews in Toxicology, vol. 21, no. 4, pp. 235–240, 1991. View at Scopus
  6. 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
  7. S. S. Hecht, “Cigarette smoking and lung cancer: chemical mechanisms and approaches to prevention,” The Lancet Oncology, vol. 3, no. 8, pp. 461–469, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. S. S. Hecht, A. Abbaspour, and D. Hoffman, “A study of tobacco carcinogenesis XLII. Bioassay in A/J mice of some structural analogues of tobacco-specific nitrosamines,” Cancer Letters, vol. 42, no. 1-2, pp. 141–145, 1988. View at Scopus
  9. Y. Sekido, K. M. Fong, and J. D. Minna, “Molecular genetics of lung cancer,” Annual Review of Medicine, vol. 54, pp. 73–87, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. J. Lindstrom, “Neuronal nicotinic acetylcholine receptors,” Ion Channels, vol. 4, pp. 377–450, 1996. View at Scopus
  11. J. Lindstrom, “Nicotinic acetylcholine receptors in health and disease,” Molecular Neurobiology, vol. 15, no. 2, pp. 193–222, 1997. View at Scopus
  12. N. L. Benowitz, “Neurobiology of nicotine addiction: implications for smoking cessation treatment,” American Journal of Medicine, vol. 121, no. 4, supplement 1, pp. S3–S10, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. 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
  14. 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
  15. H. M. Schuller, H. K. Plummer, and B. A. Jull, “Receptor-mediated effects of nicotine and its nitrosated derivative NNK on pulmonary neuroendocrine cells,” Anatomical Record Part A, vol. 270, no. 1, pp. 51–58, 2003. View at Scopus
  16. J. L. Galzi, F. Revah, A. Bessis, and J. P. Changeux, “Functional architecture of the nicotinic acetylcholine receptor: from electric organ to brain,” Annual Review of Pharmacology and Toxicology, vol. 31, pp. 37–72, 1991. View at Scopus
  17. A. Sobel, M. Weber, and J. P. Changeux, “Large-scale purification of the acetylcholine-receptor protein in its membrane-bound and detergent-extracted forms from Torpedo marmorata electric organ,” European Journal of Biochemistry, vol. 80, no. 1, pp. 215–224, 1977. View at Scopus
  18. G. S. Portugal and T. J. Gould, “Genetic variability in nicotinic acetylcholine receptors and nicotine addiction: converging evidence from human and animal research,” Behavioural Brain Research, vol. 193, no. 1, pp. 1–16, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. 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 PubMed · View at Scopus
  20. C. Gotti, D. Fornasari, and F. Clementi, “Human neuronal nicotinic receptors,” Progress in Neurobiology, vol. 53, no. 2, pp. 199–237, 1997. View at Publisher · View at Google Scholar · View at Scopus
  21. 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
  22. 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
  23. 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 PubMed · View at Scopus
  24. A. C. Villablanca, “Nicotine stimulates DNA synthesis and proliferation in vascular endothelial cells in vitro,” Journal of Applied Physiology, vol. 84, no. 6, pp. 2089–2098, 1998. View at Scopus
  25. 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
  26. R. Davis, W. Rizwani, S. Banerjee et al., “Nicotine promotes tumor growth and metastasis in mouse models of lung cancer,” PLoS One, vol. 4, no. 10, Article ID e7524, 2009. View at Publisher · View at Google Scholar · View at PubMed
  27. 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 PubMed · View at Scopus
  28. H. Sartelet, K. Maouche, J. L. Totobenazara et al., “Expression of nicotinic receptors in normal and tumoral pulmonary neuroendocrine cells (PNEC),” Pathology Research and Practice, vol. 204, no. 12, pp. 891–898, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. 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
  30. 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 PubMed · View at Scopus
  31. S. Trombino, A. Bisio, A. Catassi, A. Cesario, C. Falugi, and P. Russo, “Role of the non-neuronal human cholinergic system in lung cancer and mesothelioma: possibility of new therapeutic strategies,” Current Medicinal Chemistry—Anti-Cancer Agents, vol. 4, no. 6, pp. 535–542, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. 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
  33. A. Grozio, A. Catassi, Z. Cavalieri, L. Paleari, A. Cesario, and P. Russo, “Nicotine, lung and cancer,” Anti-Cancer Agents in Medicinal Chemistry, vol. 7, no. 4, pp. 461–466, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Jull, H. K. Plummer III, and H. Schuller, “Nicotinic receptor-mediated activation by the tobacco-specific nitrosamine NNK of a Raf-1/MAP kinase pathway, resulting in phosphorylation of c-myc in human small cell lung carcinoma cells and pulmonary neuroendocrine cells,” Journal of Cancer Research and Clinical Oncology, vol. 127, no. 12, pp. 707–717, 2001. View at Scopus
  35. 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
  36. A. Codignola, “Serotonin release and cell proliferation are under the control of α-bungarotoxin-sensitive nicotinic receptors in small-cell lung carcinoma cell lines,” FEBS Letters, vol. 342, no. 3, pp. 286–290, 1994. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Martínez-García, M. Irigoyen, Ó. González-Moreno et al., “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, vol. 116, no. 2, pp. 467–476, 2010. View at Publisher · View at Google Scholar · View at PubMed
  38. 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 PubMed · View at Scopus
  39. 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
  40. D. C. Blake, O. R. Mikse, W. M. Freeman, and C. R. Herzog, “FOXO3a elicits a pro-apoptotic transcription program and cellular response to human lung carcinogen nicotine-derived nitrosaminoketone (NNK),” Lung Cancer, vol. 67, no. 1, pp. 37–47, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. 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 PubMed · View at Scopus
  42. 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 PubMed · View at Scopus
  43. J. Arredondo, A. I. Chernyavsky, and S. A. Grando, “SLURP-1 and -2 in normal, immortalized and malignant oral keratinocytes,” Life Sciences, vol. 80, no. 24-25, pp. 2243–2247, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  44. A. Pettersson, G. Nylund, A. Khorram-Manesh, S. Nordgren, and D. S. Delbro, “Nicotine induced modulation of SLURP-1 expression in human colon cancer cells,” Autonomic Neuroscience, vol. 148, no. 1-2, pp. 97–100, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. 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 ID e4849, 2009. View at Publisher · View at Google Scholar · View at PubMed
  46. 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 PubMed · View at Scopus
  47. 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, vol. 125, no. 1, pp. 73–87, 2011. View at Publisher · View at Google Scholar · View at PubMed
  48. N. Hirata, Y. Sekino, and Y. Kanda, “Nicotine increases cancer stem cell population in MCF-7 cells,” Biochemical and Biophysical Research Communications, vol. 403, no. 1, pp. 138–143, 2010. View at Publisher · View at Google Scholar · View at PubMed
  49. B. J. Sheppard, M. Williams, H. K. Plummer III, 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. H. M. Schuller, P. K. Tithof, M. Williams, and H. K. Plummer III, “The tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1- butanone is a β-adrenergic agonist and stimulates DNA synthesis in lung adenocarcinoma via β-adrenergic receptor-mediated release of arachidonic acid,” Cancer Research, vol. 59, no. 18, pp. 4510–4515, 1999. View at Scopus
  51. E. Laag, M. Majidi, M. Cekanova, T. Masi, T. Takahashi, and H. M. Schuller, “NNK activates ERK1/2 and CREB/ATF-1 via β-1-AR and EGFR signaling in human lung adenocarcinoma and small airway epithelial cells,” International Journal of Cancer, vol. 119, no. 7, pp. 1547–1552, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. H. A. N. Al-Wadei, H. K. Plummer III, and H. M. Schuller, “Nicotine stimulates pancreatic cancer xenografts by systemic increase in stress neurotransmitters and suppression of the inhibitory neurotransmitter γ-aminobutyric acid,” Carcinogenesis, vol. 30, no. 3, pp. 506–511, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. V. Y. Shin, W. K. K. Wu, K. M. Chu et al., “Functional role of β-adrenergic receptors in the mitogenic action of nicotine on gastric cancer cells,” Toxicological Sciences, vol. 96, no. 1, pp. 21–29, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. V. Y. Shin, W. K. K. Wu, YI. N. Ye et al., “Nicotine promotes gastric tumor growth and neovascularization by activating extracellular signal-regulated kinase and cyclooxygenase-2,” Carcinogenesis, vol. 25, no. 12, pp. 2487–2495, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. H. P. S. Wong, LE. Yu, E. K. Y. Lam, E. K. K. Tai, W. K. K. Wu, and C. H. Cho, “Nicotine promotes colon tumor growth and angiogenesis through β-adrenergic activation,” Toxicological Sciences, vol. 97, no. 2, pp. 279–287, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. 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 PubMed · View at Scopus
  57. H. M. Schuller, B. Porter, and A. Riechert, “Beta-adrenergic modulation of NNK-induced lung carcinogenesis in hamsters,” Journal of Cancer Research and Clinical Oncology, vol. 126, no. 11, pp. 624–630, 2000. View at Scopus
  58. 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 PubMed · View at Scopus
  59. M. J. Jarzynka, P. Guo, I. Bar-Joseph, B. Hu, and S. Y. Cheng, “Estradiol and nicotine exposure enhances A549 bronchioloalveolar carcinoma xenograft growth in mice through the stimulation of angiogenesis,” International Journal of Oncology, vol. 28, no. 2, pp. 337–344, 2006. View at Scopus
  60. 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 PubMed · View at Scopus
  61. Z. Jin, F. Gao, T. Flagg, and X. Deng, “Tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone promotes functional cooperation of Bcl2 and c-Myc through phosphorylation in regulating cell survival and proliferation,” Journal of Biological Chemistry, vol. 279, no. 38, pp. 40209–40219, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. L. Xu and X. Deng, “Tobacco-specific nitrosamine 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone induces phosphorylation of μ- and m-calpain in association with increased secretion, cell migration, and invasion,” Journal of Biological Chemistry, vol. 279, no. 51, pp. 53683–53690, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. J. Brognard, A. S. Clark, Y. Ni, and P. A. Dennis, “Akt/pbotein kinace B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation,” Cancer Research, vol. 61, no. 10, pp. 3986–3997, 2001. View at Scopus
  64. M. Xin and X. Deng, “Nicotine inactivation of the proapoptotic function of Bax through phosphorylation,” Journal of Biological Chemistry, vol. 280, no. 11, pp. 10781–10789, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. 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 PubMed · View at Scopus
  66. H. C. Dan, M. Sun, S. Kaneko et al., “Akt phosphorylation and stabilization of X-linked inhibitor of apoptosis protein (XIAP),” Journal of Biological Chemistry, vol. 279, no. 7, pp. 5405–5412, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  67. 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 PubMed · View at Scopus
  68. J. Zhao, M. Xin, T. Wang, Y. Zhang, and X. Deng, “Nicotine enhances the antiapoptotic function of mcl-1 through phosphorylation,” Molecular Cancer Research, vol. 7, no. 12, pp. 1954–1961, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. 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 PubMed · View at Scopus
  70. O. Boutherin-Falson and N. Blaes, “Nicotine increases basal prostacyclin production and DNA synthesis of human endothelial cells in primary cultures,” Nouvelle Revue Francaise d'Hematologie, vol. 32, no. 4, pp. 253–258, 1990. View at Scopus
  71. R. M. Pittilo, H. A. Bull, S. Gulati et al., “Nicotine and cigarette smoking: effects on the ultrastructure of aortic endothelium,” International Journal of Experimental Pathology, vol. 71, no. 4, pp. 573–586, 1990. View at Scopus
  72. C. S. Carty, P. D. Soloway, S. Kayastha et al., “Nicotine and cotinine stimulate secretion of basic fibroblast growth factor and affect expression of matrix metalloproteinases in cultured human smooth muscle cells,” Journal of Vascular Surgery, vol. 24, no. 6, pp. 927–935, 1996. View at Publisher · View at Google Scholar · View at Scopus
  73. W. O. Lee and S. M. Wright, “Production of endothelin by cultured human endothelial cells following exposure to nicotine or caffeine,” Metabolism, vol. 48, no. 7, pp. 845–848, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Cucina, P. Sapienza, V. Corvino et al., “Nicotine-induced smooth muscle cell proliferation is mediated through bFGF and TGF-β,” Surgery, vol. 127, no. 3, pp. 316–322, 2000. View at Scopus
  75. A. Sugimoto, H. Masuda, M. Eguchi, H. Iwaguro, T. Tanabe, and T. Asahara, “Nicotine enlivenment of blood flow recovery following endothelial progenitor cell transplantation into ischemic hindlimb,” Stem Cells and Development, vol. 16, no. 4, pp. 649–656, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  76. 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 PubMed · View at Scopus
  77. B. Q. Zhu, C. Heeschen, R. E. Sievers et al., “Second hand smoke stimulates tumor angiogenesis and growth,” Cancer Cell, vol. 4, no. 3, pp. 191–196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. T. Natori, M. Sata, M. Washida, Y. Hirata, R. Nagai, and M. Makuuchi, “Nicotine enhances neovascularization and promotes tumor growth,” Molecules and Cells, vol. 16, no. 2, pp. 143–146, 2003. View at Scopus
  79. C. Heeschen, E. Chang, A. Aicher, and J. P. Cooke, “Endothelial progenitor cells participate in nicotine-mediated angiogenesis,” Journal of the American College of Cardiology, vol. 48, no. 12, pp. 2553–2560, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  80. X. Wang, J. Zhu, J. Chen, and Y. Shang, “Effects of nicotine on the number and activity of circulating endothelial progenitor cells,” Journal of Clinical Pharmacology, vol. 44, no. 8, pp. 881–889, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. 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 PubMed · View at Scopus
  82. 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 PubMed · View at Scopus
  83. 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
  84. 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
  85. Q. Zhang, X. Tang, Z. F. Zhang, R. Velikina, S. Shi, and A. D. Le, “Nicotine induces hypoxia-inducible factor-1α expression in human lung cancer cells via nicotinic acetylcholine receptor-mediated signaling pathways,” Clinical Cancer Research, vol. 13, no. 16, pp. 4686–4694, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. 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 PubMed · View at Scopus
  87. S. A. Mani, W. Guo, M. J. Liao et al., “The epithelial-mesenchymal transition generates cells with properties of stem cells,” Cell, vol. 133, no. 4, pp. 704–715, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. R. Kalluri and R. A. Weinberg, “The basics of epithelial-mesenchymal transition,” Journal of Clinical Investigation, vol. 119, no. 6, pp. 1420–1428, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  89. K. Polyak and R. A. Weinberg, “Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits,” Nature Reviews Cancer, vol. 9, no. 4, pp. 265–273, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. 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 PubMed · View at Scopus
  91. A. Gautam, Z. R. Li, and G. Bepler, “RRM1-induced metastasis suppression through PTEN-regulated pathways,” Oncogene, vol. 22, no. 14, pp. 2135–2142, 2003. View at Publisher · View at Google Scholar · View at PubMed
  92. Y. I. Garces, P. Yang, J. Parkinson et al., “The relationship between cigarette smoking and quality of life after lung cancer diagnosis,” Chest, vol. 126, no. 6, pp. 1733–1741, 2004. View at Publisher · View at Google Scholar · View at PubMed
  93. A. Johnston-Early, M. H. Cohen, and J. D. Minna, “Smoking abstinence and small cell lung cancer survival. An association,” Journal of the American Medical Association, vol. 244, no. 19, pp. 2175–2179, 1980. View at Publisher · View at Google Scholar
  94. S. Murin and J. Inciardi, “Cigarette smoking and the risk of pulmonary metastasis from breast cancer,” Chest, vol. 119, no. 6, pp. 1635–1640, 2001. View at Publisher · View at Google Scholar
  95. S. Murin, K. E. Pinkerton, N. E. Hubbard, and K. Erickson, “The effect of cigarette smoke exposure on pulmonary metastatic disease in a murine model of metastatic breast cancer,” Chest, vol. 125, no. 4, pp. 1467–1471, 2004. View at Publisher · View at Google Scholar
  96. H. W. Daniell, “Increased lymph node metastases at mastectomy for breast cancer associated with host obesity, cigarette smoking, age, and large tumor size,” Cancer, vol. 62, no. 2, pp. 429–435, 1988.
  97. 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 PubMed
  98. J. Mei, H. Hu, M. McEntee, H. K. Plummer III, 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
  99. N. Siriwardhana, S. Choudhary, and H. C. R. Wang, “Precancerous model of human breast epithelial cells induced by NNK for prevention,” Breast Cancer Research and Treatment, vol. 109, no. 3, pp. 427–441, 2008. View at Publisher · View at Google Scholar · View at PubMed
  100. C.-H. Lee, C.-S. Huang, C.-S. Chen et al., “Overexpression and activation of the α9-nicotinic receptor during tumorigenesis in human breast epithelial cells,” Journal of the National Cancer Institute, vol. 102, no. 17, pp. 1322–1335, 2010. View at Publisher · View at Google Scholar · View at PubMed
  101. R. Ladeiras-Lopes, A. K. Pereira, A. Nogueira et al., “Smoking and gastric cancer: systematic review and meta-analysis of cohort studies,” Cancer Causes and Control, vol. 19, no. 7, pp. 689–701, 2008. View at Publisher · View at Google Scholar · View at PubMed
  102. V. Y. Shin, H. C. Jin, E. K. O. Ng, J. J. Y. Sung, K. M. Chu, and C. H. Cho, “Activation of 5-lipoxygenase is required for nicotine mediated epithelial-mesenchymal transition and tumor cell growth,” Cancer Letters, vol. 292, no. 2, pp. 237–245, 2010. View at Publisher · View at Google Scholar · View at PubMed
  103. T. M. Mack, M. C. Yu, R. Hanisch, and B. E. Henderson, “Pancreas cancer and smoking, beverage consumption, and past medical history,” Journal of the National Cancer Institute, vol. 76, no. 1, pp. 49–60, 1986.
  104. D. C. Farrow and S. Davis, “Risk of pancreatic cancer in relation to medical history and the use of tobacco, alcohol and coffee,” International Journal of Cancer, vol. 45, no. 5, pp. 816–820, 1990. View at Publisher · View at Google Scholar
  105. D. T. Silverman, J. A. Dunn, R. N. Hoover et al., “Cigarette smoking and pancreas cancer: a case-control study based on direct interviews,” Journal of the National Cancer Institute, vol. 86, no. 20, pp. 1510–1516, 1994.
  106. G. Chipitsyna, Q. Gong, R. Anandanadesan et al., “Induction of osteopontin expression by nicotine and cigarette smoke in the pancreas and pancreatic ductal adenocarcinoma cells,” International Journal of Cancer, vol. 125, no. 2, pp. 276–285, 2009. View at Publisher · View at Google Scholar · View at PubMed
  107. M. Lazar, J. Sullivan, G. Chipitsyna et al., “Involvement of osteopontin in the matrix-degrading and proangiogenic changes mediated by nicotine in pancreatic cancer cells,” Journal of Gastrointestinal Surgery, vol. 14, no. 10, pp. 1566–1577, 2010. View at Publisher · View at Google Scholar · View at PubMed
  108. M. Lazar, J. Sullivan, G. Chipitsyna et al., “Induction of monocyte chemoattractant protein-1 by nicotine in pancreatic ductal adenocarcinoma cells: role of osteopontin,” Surgery, vol. 148, no. 2, pp. 298–309, 2010. View at Publisher · View at Google Scholar · View at PubMed
  109. L. Paleari, E. Negri, A. Catassi et al., “Inhibition of nonneuronal α7-nicotinic receptor for lung cancer treatment,” American Journal of Respiratory and Critical Care Medicine, vol. 179, no. 12, pp. 1141–1150, 2009. View at Publisher · View at Google Scholar · View at PubMed
  110. A. Catassi, L. Paleari, D. Servent et al., “Targeting α7-nicotinic receptor for the treatment of pleural mesothelioma,” European Journal of Cancer, vol. 44, no. 15, pp. 2296–2311, 2008. View at Publisher · View at Google Scholar · View at PubMed