Potential carcinogenic effects of cigarette smoke and Swedish moist snuff on pancreas: A study using a transgenic mouse model of chronic pancreatitis

Laboratory Investigation

Volumn 90, Issue 3, 2010, Pages 426-435

  Song, Zhigang ^a   Bhagat, Govind ^a   Quante, Michael ^a   Baik, Gwang Ho ^b   Marrache, Frederic ^a   Tu, Shui Ping ^a   Zhao, Chun Mei ^c   Chen, Duan ^c   Dannenberg, Andrew J ^d   Wang, Timothy C ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Chuncheon Sacred Heart Hospital   (South Korea)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Carcinogenic; Chronic pancreatitis; Cigarette smoke; Snus; Transgenic mouse model

Indexed keywords

CIGARETTE SMOKE; ELASTASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DAMAGE; CHRONIC PANCREATITIS; CONTROLLED STUDY; FEMALE; MALE; MOUSE; NONHUMAN; PANCREAS DUCT; PANCREAS ISLET CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; EPITHELIUM; FEMALE; FIBROSIS; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PANCREATIC ELASTASE; PANCREATIC NEOPLASMS; PANCREATITIS; SMOKING; TOBACCO, SMOKELESS;

EID: 77649175499     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.145     Document Type: Article

References (49)

1. Boyle P, Maisonneuve P, Bueno de Mesquita B, et al. Cigarette smoking and pancreas cancer: a case control study of the search programme of the IARC. Int J Cancer 1996;67:63-71.
2. Silverman DT. Risk factors for pancreatic cancer: a case-control study based on direct interviews. Teratog Carcinog Mutagen 2001;21:7-25.
3. Duell EJ, Holly EA, Bracci PM, et al. A population-based, case-control study of polymorphisms in carcinogen-metabolizing genes, smoking, and pancreatic adenocarcinoma risk. J Natl Cancer Inst 2002;94: 297-306.
4. Michaud DS. Epidemiology of pancreatic cancer. Minerva Chir 2004;59:99-111.
5. Iodice S, Gandini S, Maisonneuve P, et al. Tobacco and the risk of pancreatic cancer: a review and meta-analysis. Langenbecks Arch Surg 2008;393:535-545.
6. Boffetta P, Aagnes B, Weiderpass E, et al. Smokeless tobacco use and risk of cancer of the pancreas and other organs. Int J Cancer 2005;114:992-995.
7. Luo J, Ye W, Zendehdel K, et al. Oral use of Swedish moist snuff (snus) and risk for cancer of the mouth, lung, and pancreas in male construction workers: a retrospective cohort study. Lancet 2007;369:2015-2020.
8. Alguacil J, Silverman DT. Smokeless and other noncigarette tobacco use and pancreatic cancer: a case-control study based on direct interviews. Cancer Epidemiol Biomarkers Prev 2004;13:55-58.
9. Hassan MM, Abbruzzese JL, Bondy ML, et al. Passive smoking and the use of noncigarette tobacco products in association with risk for pancreatic cancer: a case-control study. Cancer 2007;109:2547-2556.
10. Prokopczyk B, Hoffmann D, Bologna M, et al. Identification of tobacco-derived compounds in human pancreatic juice. Chem Res Toxicol 2002;15:677-685.
11. Benowitz NL, Jacob III P, Yu L. Daily use of smokeless tobacco: systemic effects. Ann Intern Med 1989;111:112-116.
12. Hecht SS, Carmella SG, Murphy SE, et al. Similar exposure to a tobacco-specific carcinogen in smokeless tobacco users and cigarette smokers. Cancer Epidemiol Biomarkers Prev 2007;16:1567-1572.
13. Belinsky SA, Devereux TR, Maronpot RR, et al. Relationship between the formation of promutagenic adducts and the activation of the K-ras protooncogene in lung tumors from A/J mice treated with nitrosamines. Cancer Res 1989;49:5305-5311.
14. Belinsky SA, Devereux TR, Anderson MW. Role of DNA methylation in the activation of proto-oncogenes and the induction of pulmonary neoplasia by nitrosamines. Mutat Res 1990;233:105-116.
15. Belinsky SA, Foley JF, White CM, et al. Dose-response relationship between O6-methylguanine formation in Clara cells and induction of pulmonary neoplasia in the rat by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Cancer Res 1990;50:3772-3780.
16. Schuller HM. Mechanisms of smoking-related lung and pancreatic adenocarcinoma development. Nat Rev Cancer 2002;2:455-463.
17. Rivenson A, Hoffmann D, Prokopczyk B, et al. Induction of lung and exocrine pancreas tumors in F344 rats by tobacco-specific and Areca-derived N-nitrosamines. Cancer Res 1988;48:6912-6917.
18. Hoffmann D, Rivenson A, Abbi R, et al. A study of tobacco carcinogenesis: effect of the fat content of the diet on the carcinogenic activity of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in F344 rats. Cancer Res 1993;53:2758-2761.
19. Stenstrom B, Zhao CM, Rogers AB, et al. Swedish moist snuff accelerates gastric cancer development in Helicobacter pylori-infected wild-type and gastrin transgenic mice. Carcinogenesis 2007;28: 2041-2046.
20. Yen S, Hsieh CC, MacMahon B. Consumption of alcohol and tobacco and other risk factors for pancreatitis. Am J Epidemiol 1982;116:407-414.
21. Lowenfels AB, Zwemer FL, Jhangiani S, et al. Pancreatitis in a native American Indian population. Pancreas 1987;2:694-697.
22. Bourliere M, Barthet M, Berthezene P, et al. Is tobacco a risk factor for chronic pancreatitis and alcoholic cirrhosis? Gut 1991;32:1392-1395.
23. Talamini G, Bassi C, Falconi M, et al. Cigarette smoking: an independent risk factor in alcoholic pancreatitis. Pancreas 1996;12:131-137.
24. Talamini G, Bassi C, Falconi M, et al. Alcohol and smoking as risk factors in chronic pancreatitis and pancreatic cancer. Dig Dis Sci 1999;44:1303-1311. (Pubitemid 29404289)
25. Lin Y, Tamakoshi A, Hayakawa T, et al. Cigarette smoking as a risk factor for chronic pancreatitis: a case-control study in Japan. Research Committee on Intractable Pancreatic Diseases. Pancreas 2000;21: 109-114.
26. Morton C, Klatsky AL, Udaltsova N. Smoking, coffee, and pancreatitis. Am J Gastroenterol 2004;99:731-738.
27. Lindkvist B, Appelros S, Manjer J, et al. A prospective cohort study of smoking in acute pancreatitis. Pancreatology 2008;8:63-70.
28. Tolstrup JS, Kristiansen L, Becker U, et al. Smoking and risk of acute and chronic pancreatitis among women and men: a population-based cohort study. Arch Intern Med 2009;169:603-609.
29. Chowdhury P, Rayford PL, Chang LW. Induction of pancreatic acinar pathology via inhalation of nicotine. Proc Soc Exp Biol Med 1992;201:159-164.
30. Chowdhury P, Doi R, Tangoku A, et al. Structural and functional changes of rat exocrine pancreas exposed to nicotine. Int J Pancreatol 1995;18:257-264.
31. Wittel UA, Pandey KK, Andrianifahanana M, et al. Chronic pancreatic inflammation induced by environmental tobacco smoke inhalation in rats. Am J Gastroenterol 2006;101:148-159.
32. Lowenfels AB, Maisonneuve P, Whitcomb DC, et al. Cigarette smoking as a risk factor for pancreatic cancer in patients with hereditary pancreatitis. JAMA 2001;286:169-170.
33. Marrache F, Tu SP, Bhagat G, et al. Overexpression of interleukin-1beta in the murine pancreas results in chronic pancreatitis. Gastroenterology 2008;135:1277-1287.
34. Bernert Jr JT, Turner WE, Pirkle JL, et al. Development and validation of sensitive method for determination of serum cotinine in smokers and nonsmokers by liquid chromatography/atmospheric pressure ionization tandem mass spectrometry. Clin Chem 1997;43:2281-2291.
35. Demols A, Van Laethem JL, Quertinmont E, et al. Endogenous interleukin-10 modulates fibrosis and regeneration in experimental chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 2002;282:G1105-G1112.
36. Hatsukami DK, Lemmonds C, Zhang Y, et al. Evaluation of carcinogen exposure in people who used 'reduced exposure' tobacco products. J Natl Cancer Inst 2004;96:844-852.
37. Boffetta P, Hecht S, Gray N, et al. Smokeless tobacco and cancer. Lancet Oncol 2008;9:667-675.
38. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Tobacco smoke and involuntary smoking. IARC Monogr Eval Carcinog Risks Hum 2004;83:1-1438.
39. Feneley MR, Young MP, Chinyama C, et al. Ki-67 expression in early prostate cancer and associated pathological lesions. J Clin Pathol 1996;49:741-748.
40. Ruska KM, Sauvageot J, Epstein JI. Histology and cellular kinetics of prostatic atrophy. Am J Surg Pathol 1998;22:1073-1077.
41. De Marzo AM, Marchi VL, Epstein JI, et al. Proliferative inflammatory atrophy of the prostate: implications for prostatic carcinogenesis. Am J Pathol 1999;155:1985-1992.
42. De Marzo AM, Platz EA, Sutcliffe S, et al. Inflammation in prostate carcinogenesis. Nat Rev Cancer 2007;7:256-269.
43. Chowdhury P, Hosotani R, Chang L, et al. Metabolic and pathologic effects of nicotine on gastrointestinal tract and pancreas of rats. Pancreas 1990;5:222-229.
44. Chowdhury P, MacLeod S, Udupa KB, et al. Pathophysiological effects of nicotine on the pancreas: an update. Exp Biol Med (Maywood) 2002;227:445-454.
45. Dissin J, Mills LR, Mains DL, et al. Experimental induction of pancreatic adenocarcinoma in rats. J Natl Cancer Inst 1975;55:857-864.
46. Osvaldt AB, Wendt LR, Bersch VP, et al. Pancreatic intraepithelial neoplasia and ductal adenocarcinoma induced by DMBA in mice. Surgery 2006;140:803-809.
47. Bersch VP, Osvaldt AB, Edelweiss MI, et al. Effect of nicotine and cigarette smoke on an experimental model of intraepithelial lesions and pancreatic adenocarcinoma induced by 7,12-dimethyl-benzanthracene in mice. Pancreas 2009;38:65-70.
48. Rodu B, Jansson C. Smokeless tobacco and oral cancer: a review of the risks and determinants. Crit Rev Oral Biol Med 2004;15:252-263.
49. Nilsson R. De minimus non curat lex-virtual thresholds for cancer initiation by tobacco specific nitrosamines-prospects for harm reduction by smokeless tobacco. Int J Occup Med Environ Health 2006;19:6-35.