Nicotine and gastrointestinal disorders: Its role in ulceration and cancer development

Current Pharmaceutical Design

Volumn 19, Issue 1, 2013, Pages 5-10

  Chu, Kent Man ^a   Cho, Chi H ^b   Shin, Vivian Y ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

Adrenergic receptors; Angiogenesis; Cigarette smoke; Colon cancer; Crohn's disease; EMT; Gastric cancer; Gastric ulceration; miRNA; nAChRs; Nicotine; NNK; Ulcerative colitis

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ADRENERGIC RECEPTOR; ALPHA BUNGAROTOXIN; ATENOLOL; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CBO P 11; CHOLINERGIC RECEPTOR BLOCKING AGENT; CIGARETTE SMOKE; CYCLOOXYGENASE 2; ICI 118 511; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MECAMYLAMINE; MICRORNA; NICOTINE; NICOTINIC RECEPTOR; NITROSAMINE; PROPRANOLOL; STILONIUM IODIDE; TAR; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; CARCINOGENESIS; DIGESTIVE SYSTEM CANCER; DIGESTIVE SYSTEM INFLAMMATION; DIGESTIVE SYSTEM ULCER; EPITHELIAL MESENCHYMAL TRANSITION; GASTROINTESTINAL DISEASE; HUMAN; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; SMOKING; SMOKING CESSATION; TUMOR GROWTH; TUMOR VASCULARIZATION; ULCEROGENESIS;

EID: 84873952954     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811306010005     Document Type: Review

References (81)

1. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process-First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992; 52: 6735-40.
2. Shin VY, Wu WK, Ye YN, So WH, Koo MW, Liu ES, et al. Nicotine promotes gastric tumor growth and neovascularization by activating extracellular signal-regulated kinase and cyclooxygenase-2. Carcinogenesis 2004; 25: 2487-95.
3. Nishioka T, Kim HS, Luo LY, Huang Y, Guo J, Yan Chen C. Sensitization of epithelial growth factor receptors by nicotine exposure to promote breast cancer cell growth. Breast Cancer Res 2011; 13: R113.
4. Wong HP, Yu L, Lam EK, Tai EK, Wu WK, Cho CH. Nicotine promotes cell proliferation via alpha7-nicotinic acetylcholine receptor and catecholamine-synthesizing enzymes-mediated pathway in human colon adenocarcinoma HT-29 cells. Toxicol Appl Pharmacol 2007; 221: 261-7.
5. Dasgupta P, Rastogi S, Pillai S, Ordonez-Ercan D, Morris M, Haura E, et al. Nicotine induces cell proliferation by beta-arrestinmediated activation of Src and Rb-Raf-1 pathways. The Journal of clinical investigation 2006; 116: 2208-17.
6. Schuller HM, Cekanova M. NNK-induced hamster lung adenocarcinomas over-express beta2-adrenergic and EGFR signaling pathways. Lung Cancer 2005; 49: 35-45.
7. Fujimoto J, Kadara H, Men T, van Pelt C, Lotan D, Lotan R. Comparative functional genomics analysis of NNK tobaccocarcinogen induced lung adenocarcinoma development in Gprc5aknockout mice. PLoS One 2010; 5: e11847.
8. Sachs G, Scott DR, Wen Y. Gastric Infection by Helicobacter pylori. Current gastroenterology reports 2011; 13: 540-6.
9. Maity P, Biswas K, Roy S, Banerjee RK, Bandyopadhyay U. Smoking and the pathogenesis of gastroduodenal ulcer-recent mechanistic update. Mol Cell Biochem 2003; 253: 329-38.
10. Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn't the stomach digest itself? Physiological reviews 2008; 88: 1547-65.
11. Gyires K. Gastric mucosal protection: from prostaglandins to genetherapy. Current medicinal chemistry 2005; 12: 203-15.
12. Cover TL, Vaughn SG, Cao P, Blaser MJ. Potentiation of Helicobacter pylori vacuolating toxin activity by nicotine and other weak bases. J Infect Dis 1992; 166: 1073-8.
13. Blum H, Mutschler E, van Zwieten PA. [On the influence of cholinergic drugs on ulcer development and gastric juice secretion on the Shay rat]. Naunyn-Schmiedebergs Archiv fur experimentelle Pathologie und Pharmakologie 1967; 256: 99-111.
14. Ogle CW, Cho CH, Wong SH. The effect of nicotine on ethanolinduced gastric ulcers in rats. Experientia 1985; 41: 1140-1.
15. Wong D, Koo MW, Shin VY, Liu ES, Cho CH. Pathogenesis of nicotine treatment and its withdrawal on stress-induced gastric ulceration in rats. Eur J Pharmacol 2002; 434: 81-6.
16. Chow JY, Ma L, Zhu M, Cho CH. The potentiating actions of cigarette smoking on ethanol-induced gastric mucosal damage in rats. Gastroenterology 1997; 113: 1188-97.
17. Zhang Z, Zou YY, Zhou Y, Zhou H, Li YJ. The aggravatory effect of nicotine on Helicobacter pylori-induced gastric mucosa injury: role of asymmetric dimethylarginine. J Clin Gastroenterol 2009; 43: 261-6.
18. Shin VY, Liu ES, Koo MW, Wang JY, Matsui H, Cho CH. Cigarette smoke extracts delay wound healing in the stomach: involvement of polyamine synthesis. Exp Biol Med (Maywood) 2002; 227: 114-24.
19. Thomas GA, Rhodes J, Ingram JR. Mechanisms of disease: nicotine-a review of its actions in the context of gastrointestinal disease. Nature clinical practice Gastroenterology & hepatology 2005; 2: 536-44.
20. Mahid SS, Minor KS, Soto RE, Hornung CA, Galandiuk S. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clinic proceedings Mayo Clinic 2006; 81: 1462-71.
21. Pullan RD, Rhodes J, Ganesh S, Mani V, Morris JS, Williams GT, et al. Transdermal nicotine for active ulcerative colitis. The New England journal of medicine 1994; 330: 811-5.
22. Bustamante M, Nos P, Hoyos M, Hinojosa J, Moles JR, Garcia-Herola A, et al. Relationship between smoking and colonic involvement in inflammatory bowel disease. Revista espanola de enfermedades digestivas: organo oficial de la Sociedad Espanola de Patologia Digestiva 1998; 90: 833-40.
23. Helio T, Halme L, Lappalainen M, Fodstad H, Paavola-Sakki P, Turunen U, et al. CARD15/NOD2 gene variants are associated with familially occurring and complicated forms of Crohn's disease. Gut 2003; 52: 558-62.
24. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001; 411: 599-603.
25. Karban A, Eliakim R. Effect of smoking on inflammatory bowel disease: Is it disease or organ specific? World J Gastroenterol 2007; 13: 2150-2.
26. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003; 421: 384-8.
27. van Westerloo DJ, Giebelen IA, Florquin S, Bruno MJ, Larosa GJ, Ulloa L, et al. The vagus nerve and nicotinic receptors modulate experimental pancreatitis severity in mice. Gastroenterology 2006; 130: 1822-30.
28. Alexandre M, Pandol SJ, Gorelick FS, Thrower EC. The emerging role of smoking in the development of pancreatitis. Pancreatology 2011; 11: 469-74.
29. Wittel UA, Pandey KK, Andrianifahanana M, Johansson SL, Cullen DM, Akhter MP, et al. Chronic pancreatic inflammation induced by environmental tobacco smoke inhalation in rats. The American journal of gastroenterology 2006; 101: 148-59.
30. Chipitsyna G, Gong Q, Anandanadesan R, Alnajar A, Batra SK, Wittel UA, et al. Induction of osteopontin expression by nicotine and cigarette smoke in the pancreas and pancreatic ductal adenocarcinoma cells. Int J Cancer 2009; 125: 276-85.
31. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer? Annals of internal medicine 2009; 151: 121-8.
32. Lijinsky W. Nitrosamines and nitrosamides in the etiology of gastrointestinal cancer. Cancer 1977; 40: 2446-9.
33. Gurkalo VK, Volfson NI. Nicotine influence upon the development of experimental stomach tumors. Archiv fur Geschwulstforschung 1982; 52: 259-65.
34. Shin VY, Liu ES, Ye YN, Koo MW, Chu KM, Cho CH. A mechanistic study of cigarette smoke and cyclooxygenase-2 on proliferation of gastric cancer cells. Toxicol Appl Pharmacol 2004; 195: 103-12.
35. Shin VY, Jin HC, Ng EK, Yu J, Leung WK, Cho CH, et al. Nicotine and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone induce cyclooxygenase-2 activity in human gastric cancer cells: Involvement of nicotinic acetylcholine receptor (nAChR) and betaadrenergic receptor signaling pathways. Toxicol Appl Pharmacol 2008; 233: 254-61.
36. Crowley-Weber CL, Dvorakova K, Crowley C, Bernstein H, Bernstein C, Garewal H, et al. Nicotine increases oxidative stress, activates NF-kappaB and GRP78, induces apoptosis and sensitizes cells to genotoxic/xenobiotic stresses by a multiple stress inducer, deoxycholate: relevance to colon carcinogenesis. Chem Biol Interact 2003; 145: 53-66.
37. Liu ES, Ye YN, Shin VY, Yuen ST, Leung SY, Wong BC, et al. Cigarette smoke exposure increases ulcerative colitis-associated colonic adenoma formation in mice. Carcinogenesis 2003; 24: 1407-13.
38. Ye YN, Wu WK, Shin VY, Cho CH. A mechanistic study of colon cancer growth promoted by cigarette smoke extract. Eur J Pharmacol 2005; 519: 52-7.
39. Wong HP, Yu L, Lam EK, Tai EK, Wu WK, Cho CH. Nicotine promotes colon tumor growth and angiogenesis through betaadrenergic activation. Toxicol Sci 2007; 97: 279-87.
40. Wu WK, Wong HP, Luo SW, Chan K, Huang FY, Hui MK, et al. 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone from cigarette smoke stimulates colon cancer growth via beta-adrenoceptors. Cancer Res 2005; 65: 5272-7.
41. Dasgupta P, Rizwani W, Pillai S, Kinkade R, Kovacs M, Rastogi S, et al. Nicotine induces cell proliferation, invasion and epithelialmesenchymal transition in a variety of human cancer cell lines. Int J Cancer 2009; 124: 36-45.
42. Lam DC, Girard L, Ramirez R, Chau WS, Suen WS, Sheridan S, et al. Expression of nicotinic acetylcholine receptor subunit genes in non-small-cell lung cancer reveals differences between smokers and nonsmokers. Cancer Res 2007; 67: 4638-47.
43. Shin VY, Liu ES, Koo MW, Luo JC, So WH, Cho CH. Nicotine suppresses gastric wound repair via the inhibition of polyamine and K(+) channel expression. Eur J Pharmacol 2002; 444: 115-21.
44. Wang W, Chin-Sheng H, Kuo LJ, Wei PL, Lien YC, Lin FY, et al. NNK Enhances Cell Migration through alpha7-nicotinic Acetylcholine Receptor Accompanied by Increased of Fibronectin Expression in Gastric Cancer. Ann Surg Oncol 2011
45. Lien YC, Wang W, Kuo LJ, Liu JJ, Wei PL, Ho YS, et al. Nicotine promotes cell migration through alpha7 nicotinic acetylcholine receptor in gastric cancer cells. Ann Surg Oncol 2011; 18: 2671-9.
46. Brown KC, Lau JK, Dom AM, Witte TR, Luo H, Crabtree CM, et al. MG624, an alpha7-nAChR antagonist, inhibits angiogenesis via the Egr-1/FGF2 pathway. Angiogenesis 2011
47. Al-Wadei MH, Al-Wadei HA, Schuller HM. Pancreatic cancer cells and normal pancreatic duct epithelial cells express an autocrine catecholamine loop that is activated by nicotinic acetylcholine receptors alpha3, alpha5, and alpha7. Mol Cancer Res 2012; 10: 239-49.
48. Al-Wadei MH, Al-Wadei HA, Schuller HM. Pancreatic Cancer Cells and Normal Pancreatic Duct Epithelial Cells Express an Autocrine Catecholamine Loop that Is Activated by Nicotinic Acetylcholine Receptors alpha3, alpha5, and alpha7. Mol Cancer Res 2012
49. Wei PL, Kuo LJ, Huang MT, Ting WC, Ho YS, Wang W, et al. Nicotine enhances colon cancer cell migration by induction of fibronectin. Ann Surg Oncol 2011; 18: 1782-90.
50. Sakurai R, Cerny LM, Torday JS, Rehan VK. Mechanism for nicotine-induced up-regulation of Wnt signaling in human alveolar interstitial fibroblasts. Experimental lung research 2011; 37: 144-54.
51. Shin VY, Wu WK, Chu KM, Koo MW, Wong HP, Lam EK, et al. Functional role of beta-adrenergic receptors in the mitogenic action of nicotine on gastric cancer cells. Toxicol Sci 2007; 96: 21-9.
52. Powe DG, Entschladen F. Targeted therapies: Using beta-blockers to inhibit breast cancer progression. Nature reviews Clinical oncology 2011; 8: 511-2.
53. Park SY, Kang JH, Jeong KJ, Lee J, Han JW, Choi WS, et al. Norepinephrine induces VEGF expression and angiogenesis by a hypoxia-inducible factor-1alpha protein-dependent mechanism. Int J Cancer 2011; 128: 2306-16.
54. Al-Wadei HA, Al-Wadei MH, Schuller HM. Cooperative regulation of non-small cell lung carcinoma by nicotinic and Betaadrenergic receptors: a novel target for intervention. PLoS One 2012; 7: e29915.
55. Perez-Sayans M, Somoza-Martin JM, Barros-Angueira F, Diz PG, Gandara Rey JM, Garcia-Garcia A. Beta-adrenergic receptors in cancer: therapeutic implications. Oncol Res 2010; 19: 45-54.
56. Zhang D, Ma QY, Hu HT, Zhang M. beta2-adrenergic antagonists suppress pancreatic cancer cell invasion by inhibiting CREB, NFkappaB and AP-1. Cancer Biol Ther 2010; 10: 19-29.
57. Majidi M, Al-Wadei HA, Takahashi T, Schuller HM. Nongenomic beta estrogen receptors enhance beta1 adrenergic signaling induced by the nicotine-derived carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in human small airway epithelial cells. Cancer Res 2007; 67: 6863-71.
58. Liao X, Che X, Zhao W, Zhang D, Bi T, Wang G. The betaadrenoceptor antagonist, propranolol, induces human gastric cancer cell apoptosis and cell cycle arrest via inhibiting nuclear factor kappaB signaling. Oncol Rep 2010; 24: 1669-76.
59. Perrone MG, Notarnicola M, Caruso MG, Tutino V, Scilimati A. Upregulation of beta3-adrenergic receptor mRNA in human colon cancer: a preliminary study. Oncology 2008; 75: 224-9.
60. Shin VY, Wu WK, Chu KM, Wong HP, Lam EK, Tai EK, et al. Nicotine induces cyclooxygenase-2 and vascular endothelial growth factor receptor-2 in association with tumor-associated invasion and angiogenesis in gastric cancer. Mol Cancer Res 2005; 3: 607-15.
61. Shin VY, Jin HC, Ng EK, Cho CH, Leung WK, Sung JJ, et al. 4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone promoted gastric cancer growth through prostaglandin E receptor (EP2 and EP4) in vivo and in vitro. Cancer Sci 2011; 102: 926-33.
62. Kosaka T, Kikuchi E, Mikami S, Miyajima A, Shirotake S, Ishida M, et al. Expression of snail in upper urinary tract urothelial carcinoma: prognostic significance and implications for tumor invasion. Clin Cancer Res 2010; 16: 5814-23.
63. Shin VY, Jin HC, Ng EK, Sung JJ, Chu KM, Cho CH. Activation of 5-lipoxygenase is required for nicotine mediated epithelialmesenchymal transition and tumor cell growth. Cancer Lett 2010; 292: 237-45.
64. Liu Y, Liu BA. Enhanced proliferation, invasion, and epithelialmesenchymal transition of nicotine-promoted gastric cancer by periostin. World J Gastroenterol 2011; 17: 2674-80.
65. Huang RY, Li MY, Hsin MK, Underwood MJ, Ma LT, Mok TS, et al. 4-Methylnitrosamino-1-3-pyridyl-1-butanone (NNK) promotes lung cancer cell survival by stimulating thromboxane A2 and its receptor. Oncogene 2011; 30: 106-16.
66. Davis R, Rizwani W, Banerjee S, Kovacs M, Haura E, Coppola D, et al. Nicotine promotes tumor growth and metastasis in mouse models of lung cancer. PLoS One 2009; 4: e7524.
67. Caldas C, Brenton JD. Sizing up miRNAs as cancer genes. Nat Med 2005; 11: 712-4.
68. Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, et al. Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 2005; 37: 766-70.
69. Berezikov E, Guryev V, van de Belt J, Wienholds E, Plasterk RH, Cuppen E. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 2005; 120: 21-4.
70. Izzotti A, Calin GA, Arrigo P, Steele VE, Croce CM, De Flora S. Downregulation of microRNA expression in the lungs of rats exposed to cigarette smoke. FASEB J 2009; 23: 806-12.
71. Schembri F, Sridhar S, Perdomo C, Gustafson AM, Zhang X, Ergun A, et al. MicroRNAs as modulators of smoking-induced gene expression changes in human airway epithelium. Proc Natl Acad Sci U S A 2009; 106: 2319-24.
72. Xi S, Yang M, Tao Y, Xu H, Shan J, Inchauste S, et al. Cigarette smoke induces C/EBP-beta-mediated activation of miR-31 in normal human respiratory epithelia and lung cancer cells. PLoS One 2010; 5: e13764.
73. Kalscheuer S, Zhang X, Zeng Y, Upadhyaya P. Differential expression of microRNAs in early-stage neoplastic transformation in the lungs of F344 rats chronically treated with the tobacco carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Carcinogenesis 2008; 29: 2394-9.
74. Izzotti A, Larghero P, Longobardi M, Cartiglia C, Camoirano A, Steele VE, et al. Dose-responsiveness and persistence of microRNA expression alterations induced by cigarette smoke in mouse lung. Mutat Res 2011; 717: 9-16.
75. Ma X, Kumar M, Choudhury SN, Becker Buscaglia LE, Barker JR, Kanakamedala K, et al. Loss of the miR-21 allele elevates the expression of its target genes and reduces tumorigenesis. Proc Natl Acad Sci U S A 2011; 108: 10144-9.
76. Sempere LF, Preis M, Yezefski T, Ouyang H, Suriawinata AA, Silahtaroglu A, et al. Fluorescence-based codetection with protein markers reveals distinct cellular compartments for altered MicroRNA expression in solid tumors. Clin Cancer Res 2010; 16: 4246-55.
77. Tsujiura M, Ichikawa D, Komatsu S, Shiozaki A, Takeshita H, Kosuga T, et al. Circulating microRNAs in plasma of patients with gastric cancers. Br J Cancer 2010; 102: 1174-9.
78. Zhang Z, Li Z, Gao C, Chen P, Chen J, Liu W, et al. miR-21 plays a pivotal role in gastric cancer pathogenesis and progression. Lab Invest 2008; 88: 1358-66.
79. Gao C, Zhang Z, Liu W, Xiao S, Gu W, Lu H. Reduced microRNA-218 expression is associated with high nuclear factor kappa B activation in gastric cancer. Cancer 2010; 116: 41-9.
80. Loffler D, Brocke-Heidrich K, Pfeifer G, Stocsits C, Hackermuller J, Kretzschmar AK, et al. Interleukin-6 dependent survival of multiple myeloma cells involves the Stat3-mediated induction of microRNA-21 through a highly conserved enhancer. Blood 2007; 110: 1330-3.
81. Shin VY, Jin H, Ng EK, Cheng AS, Chong WW, Wong CY, et al. NF-kappaB targets miR-16 and miR-21 in gastric cancer: involvement of prostaglandin E receptors. Carcinogenesis 2011; 32: 240-5.