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Carcinogenesis Advance Access published online on June 5, 2003
Carcinogenesis, doi:10.1093/carcin/bgg094
© 2003 by Oxford University Press
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© 2003 Oxford University Press

CARCINOGENESIS

Cigarette smoke exposure increases ulcerative colitis-associated colonic adenoma formation in mice

Edgar S. L. Liu 1, Yi-Ni Ye 2, Vivian Y. Shin 1, Siu-Tsan Yuen 3, Suet-Yi Leung 3, Benjamin C. Y. Wong 4, and Chi-Hin Cho 1*

1 Department of Pharmacology, Faculty of Medicine, The University of Hong Kong, Hong Kong, China
2 Department of Pharmacology, Faculty of Medicine, The University of Hong Kong, Hong Kong, China; Department of Pharmacology, Faculty of Medicine, Zhejiang University, Hangzhou, China
3 Department of Pathology, Faculty of Medicine, The University of Hong Kong, Hong Kong, China
4 Department of Medicine, Faculty of Medicine, The University of Hong Kong, Hong Kong, China

* Corresponding author. E-mail: chcho{at}hkusua.hku.hk.

Received 18 November 2002 ; revised 17 April 2003 ; accepted 20 May 2003

Abstract

Both chronic ulcerative colitis and smoking are associated with colorectal cancer in humans. In the present study, we investigated the effects of cigarette smoke (CS) exposure on inflammation-associated tumorigenesis in the mouse colon. Male balb/c mice were allocated into 6 groups: Control, CS(2%), CS(4%), Colitis, Colitis + CS(2%), and Colitis + CS(4%). They were given water or 3% dextran sulfate sodium (DSS) in drinking water for 7 days to induce colitis, with or without 1-hour daily exposure to 2% or 4% CS. They were then allowed to drink water for 14 days. The cycle of 7-day DSS ± CS /14-day H2O treatments were repeated twice. Mice were sacrificed immediately or 1 month after the three cycles of treatments. Results indicated colonic adenoma was only found in the Colitis group (1 out of 11), Colitis + CS(2%) group (7 out of 12) and Colitis + CS(4%) group (4 out of 5) 1 month after 3 cycles of DSS and/or CS treatment. CS exposure dose-dependently increased adenoma formation in mice with inflamed mucosa. CS exposure plus colitis was strongly associated with a high incidence of dysplasia (p<0.01) and adenocarcinoma formation (p<0.01) compared to induction of colitis alone. Colitis induced cell proliferation and apoptosis in colonic tissues. Cigarette smoking significantly attenuated the apoptotic effect by DSS probably via the induction of anti-apoptotic protein bcl-2. The ratio of apoptosis over proliferation was also significantly lower in the Colitis + CS groups. Vascular endothelial growth factor and angiogenesis in the colon were also increased by cigarette smoking in animals with colitis. In conclusion, cigarette smoke promotes inflammation-associated adenoma/adenocarcinoma formation in the mouse colon in a dose-dependent manner. This tumor development is associated with the inhibition of cellular apoptosis and supported by increased angiogenesis.


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