A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate

Cancer Science

Volumn 94, Issue 11, 2003, Pages 965-973

  Tanaka, Takuji ^a   Kohno, Hiroyuki ^a   Suzuki, Rikako ^a,b   Yamada, Yasuhiro ^c   Sugie, Shigeyuki ^d   Mori, Hideki ^d  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d GIFU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; BETA CATENIN; CARCINOGEN; CYCLOOXYGENASE 2; DEXTRAN DERIVATIVE; NITRIC OXIDE SYNTHASE; PROTEIN P53; XENOBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INCIDENCE; COLITIS; COLON ADENOCARCINOMA; COLON ADENOMA; COLON CARCINOGENESIS; COLON TUMOR; CONTROLLED STUDY; DYSPLASIA; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; MALE; MAST CELL; NONHUMAN; PRIORITY JOURNAL; TUMOR PROMOTION;

ADENOCARCINOMA; ADENOMA; ANIMALS; ANTICOAGULANTS; AZOXYMETHANE; BETA CATENIN; CARCINOGENS; COLITIS; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; CYTOSKELETAL PROTEINS; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; INFLAMMATION; INJECTIONS, INTRAPERITONEAL; ISOENZYMES; MALE; MAST CELLS; MICE; MICE, INBRED ICR; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0344237231     PISSN: 13479032     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2003.tb01386.x     Document Type: Article

References (55)

1. Eaden JA, Abrams KR, Mayberry JF. The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 2001; 48: 526-35.
2. van Hogezand RA, Eichhorn RF, Choudry A, Veenendaal RA, Lamers BHW. Malignancies in inflammatory bowel disease: fact or fiction? Scand J Gastroenterol Suppl 2002; 235: 48-53.
3. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R. Novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990; 98: 694-702.
4. Seril DN, Liao J, Ho K-LK, Warsi A, Yang CY, Yang G-Y. Dietary iron supplementation enhances DSS-induced colitis and associated colorectal carcinoma development in mice. Dig Dis Sci 2002; 47: 1266-78.
5. Seril DN, Liao J, Ho K-LK, Yang CS, Yang G-Y. Inhibition of chronic ulcerative colitis-associated colorectal adenocarcinoma development in a murine model by N-acetylcysteine. Carcinogenesis 2002; 23: 993-1001.
6. Okayasu I, Yamada M, Mikami T, Yoshida T, Kanno J, Ohkusa T. Dysplasia and carcinoma development in a repeated dextran sulfate sodium-induced colitis model. J Gastroenterol Hepatol 2002; 17: 1078-83.
7. Tanaka T, Kohno H, Murakami M, Shimada. R, Kagami S. Colitis-related rat colon carcinogenesis induced by 1-hydroxyanthraquinone and methylazoxymethanol acetate (Review). Oncol Rep 2000; 7: 501-8.
8. Seril DN, Liao J, Yang G-Y, Yang CS. Oxidative stress and ulcerative colitis-associated carcinogenesis: stuides in human and animal models. Carcinogenesis 2003; 24: 353-62.
9. Su CG, Wen X, Bailey ST, Jiang W, Rangwala SM, Keilbaugh SA, Flanigan A, Murthy S, Lazar MA, Wu GD. A novel therapy for colitis utilizing PPAR-γ ligands to inhibit the epithelial inflammation response. J Clin Invest 1999; 104: 383-9.
10. Kohno H, Yoshitani S, Takashima S, Okumura A, Hosokawa M, Yamaguchi N, Tanaka T. Troglitazone, a ligand for peroxisome proliferator-activated receptor γ, inhibits chemically-induced aberrant crypt foci in rats. Jpn J Cancer Res 2001; 92: 396-403.
11. Tanaka T, Kohno H, Yoshitani S, Takashima S, Okumura A, Murakami A, Hosokawa M. Ligands for peroxisome proliferator-activated receptors α and γ inhibit chemically induced colitis and formation of aberrant crypt foci in rats. Cancer Res 2001; 61: 2424-8.
12. Osawa E, Nakajima A, Wada K, Ishimine S, Fujisawa N, Kawamori T, Matsuhashi N, Kadowaki T, Ochiai M, Sekihara H, Nakagama H. Peroxisome proliferator-activated receptor γ ligands suppress colon carcinogenesis induced by azoxymethane in mice. Gastroenterology 2003; 124: 361-7.
13. Malaviya R, Ikeda T, Ross EA, Jakschik BA, Abraham SN. Bacteria-mast cell interactions in inflammatory disease. Am J Ther 1995; 2: 787-92.
14. Maeda H, Akaike T. Review: nitric oxide and oxygen radicals in infection, inflammation, and cancer. Biochemistry (Mosc) 1998; 63: 854-65.
15. Anton PM, Theodorou V, Bertrand V, Eutamene H, Aussenac T, Feyt N, Fioramonti J, Bueno L. Chronic ingestion of a potential food contaminant induces gastrointestinal inflammation in rats: role of nitric oxide and mast cells. Dig Dis Sci 2000; 45: 1842-9.
16. Alican I, Kubes P. A critical role for nitric oxide in intestinal barrier function and dysfunction. Am J Physiol 1996; 270: G225-37.
17. Okamoto M, Ohtsu H, Miyaki M, Yonekawa H. No alleic loss at the p53 locus in 1,2-dimethylhydrazine-induced mouse colon tumours: PCR-SSCP analysis with sequence-tagged microsatellite site primers. Carcinogenesis 1993; 14: 1483-6.
18. Moen CJ, Groo PC, Har AA, Snoek M, Demant P. Fine mapping of colon tumor susceptibility (Scc) genes in the mouse, different from the genes known to be somatically mutated in colon cancer. Proc Natl Acad Sci USA 1996; 93: 1082-6.
19. Sugimura T, Nagao M, Wakabayashi K. How we should deal with unavoidable exposure of man to environmental mutagens: cooked food mutagen discovery, facts and lessons for cancer prevention. Mutat Res 2000; 447: 15-25.
20. Riddell RH, Goldman H, Ransohof DF, Appleman HD, Fenoglio CM, Haggitt RC, Ahren C, Correa P, Hamilton SR, Morson BC, Sommers SC, Yardley JH. Dysplasia in inflammatory bowel disease: standardized classification with provisional clinical application. Hum Pathol 1983; 14: 931-68.
21. Pascal RR. Dysplasia and early carcinoma in inflammatory bowel disease and colorectal carcinomas. Hum Pathol 1994; 25: 1160-71.
22. Ward JM. Morphogenesis of chemically induced neoplasms of the colon and small intestine in rats. Lab Invest 1974; 30: 505-13.
23. Okayasu I, Ohkusa T, Kajiura K, Kanno J, Sakamoto S. Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut 1996; 39: 87-92.
24. Sohn OS, Fiala ES, Requeijo SP, Weisburger JH, Gonzalez FJ. Differential effects of CYP2E1 status on the metabolic activation of the colon carcinogens azoxymethane and methylazoxymethanol. Cancer Res 2001; 61: 8435-40.
25. Hirono I, Kuhara K, Yamaji T, Hosaka S, Golberg L. Induction of colorectal squamous cell carcinomas in rats by dextran sulfate sodium. Carcinogenesis 1992; 3: 353-5.
26. Mori Y, Yoshimi N, Iwata H, Tanaka T, Mori H. The synergistic effect of 1-hydroxyanthraquinone on methylazoxymethanol acetate-induced carcinogenesis in rats. Carcinogenesis 1991; 12: 335-8.
27. Sugie S, Mori Y, Okumura A, Yoshimi N, Okamoto K, Sato S, Tanaka T, Mori H. Promoting and synergistic effects of chrysazin on 1,2-dimethylhydrazine-induced carcinogenesis in male ICR/CD-1 mice. Carcinogenesis 1994; 15: 1175-9.
28. Miller JR, Moon RT. Signal transduction through β-catenin and specification of cell fate during embryogenesis. Genes Dev 1996; 10: 2527-39.
29. Brabletz T, Jung A, Kirchner T. β-Catenin and the morphogenesis of colorectal cancer. Virchows Arch 2002; 441: 1-11.
30. Hao XP, Pretlow TG, Rao JS, Pretlow TP. β-catenin expression is altered in human colonic aberrant crypt foci. Cancer Res 2001; 61: 8085-8.
31. Yamada Y, Yoshimi N, Hirose Y, Kawabata K, Matsunaga K, Shimizu M, Hara A, Mori H. Frequent β-catenin gene mutations and accumulations of the protein in the putative preneoplastic lesions lacking macroscopic aberrant crypt foci appearance, in rat colon carcinogenesis. Cancer Res 2000; 60: 3323-7.
32. Yamada Y, Yoshimi N, Hirose Y, Matsunaga K, Katayama M, Sakata K, Shimizu M, Kuno T, Mori H. Sequential analysis of morphological and biological properties of β-catenin-accumulated crypts, provable premalignant lesions independent of aberrant crypt foci in rat colon carcinogenesis. Cancer Res 2001; 61: 1874-8.
33. Min/+ mice. Cancer Res 2002; 62: 6367-70.
34. Cooper HS, Murthy S, Kido K, Yoshitake H, Flanigan A. Dysplasia and cancer in the dextran sulfate sodium mouse colitis model. Relevance to colitis-associated neoplasia in the human: a study of histopathology, β-catenin and p53 expression and the role of inflammation. Carcinogenesis 2000; 21: 757-68.
35. Walsh SV, Loda M, Torres CM, Antonioli D, Odze R. P53 and β catenin expression in chronic ulcerative colitis-associated polypoid dysplasia and sporadic adenomas: an immunohistochemical study. Am J Surg Pathol 1999; 23: 963-9.
36. Mikami T, Mitomi H, Hara A, Yanagisawa N, Yoshida T, Tsuruta O, Okayasu I. Decreased expression of CD44, α-catenin, and deleted colon carcinoma and altered expression of β-catenin in ulcerative colitis-associated dysplasia and carcinoma, as compared with sporadic colon neoplasms. Cancer 2000; 89: 733-40.
37. Suzui M, Ushijima T, Dashwood RH, Yoshimi N, Sugimura T, Mori H, Nagao M. Frequent mutations of the rat β-catenin gene in colon cancers induced by methylazoxymethanol acetate plus 1-hydroxyanthraquinone. Mol Carcinog 1999; 24: 232-7.
38. Takesue F, Korenaga D, Yao T, Kabashima A, Sugimachi K. Development of colonic neoplasms and expressions of p53 and p21 proteins of experimental colitis of mice induced by dextran sulfate sodium. J Exp Clin Cancer Res 2001; 20: 413-8.
39. Ishitsuka T, Kashiwagi H, Konishi F. Microsatellite instability in inflamed and neoplastic epithelium in ulcerative colitis. J Clin Invest 2001; 54: 526-32.
40. Suzui M, Yoshimi N, Ushijima T, Hirose Y, Makita H, Wang A, Kawamori T, Tanaka T, Mori H, Nagao M. No involvement of Ki-ras or p53 gene mutations in colitis-associated rat colon tumors induced by 1-hydroxyanthraquinone and methylazoxymethanol acetate. Mol Carcinog 1995; 12: 193-7.
41. Vane JR, Mitchell JA, Appleton I, Tomlinson A, Bishop-Bailey D, Croxtall J, Willoughby DA. Inducible isoforms of cyclooxygenase and nitric-oxide synthase in inflammation. Proc Natl Acad Sci USA 1994; 91: 2046-50.
42. Takahashi M, Mutoh M, Kawamori T, Sugimura T, Wakabayashi K. Altered expression of β-catenin, inducible nitric oxide synthase and cyclooxygenase-2 in azoxymethane-induced rat colon carcinogenesis. Carcinogenesis 2000; 21: 1319-27.
43. Takahashi M, Fukuda K, Ohata T, Sugimura T, Wakabayashi K. Increased expression of inducible and endothelial constitutive nitric oxide synthases in rat colon tumors induced by azoxymethane. Cancer Res 1997; 57: 1233-7.
44. Bradding P, Holgate ST. Immunopathology and human mast cell cytokines. Crit Rev Oncol/Hematol 1999; 31: 119-33.
45. Minocha A, Thomas C, Omar R. Lack of crucial role of mast cells in pathogenesis of experimental colitis in mice. Dig Dis Sci 1995; 40: 1757-62.
46. Araki Y, Andoh A, Fujiyama Y, Bamba T. Development of dextran sulphate sodium-induced experimental colitis is suppressed in genetically mast cell-deficient Ws/Ws rats. Clin Exp Immunol 2000; 119: 264-9.
47. Sasaki Y, Tanaka M, Kudo H. Differentiation between ulcerative colitis and Crohn's disease by a quantitative immunohistochemical evaluation of T lymphocytes, neutrophils, histiocytes and mast cells. Pathol Int 2002; 52: 277-85.
48. Flynn EA, Schwartz JL, Shklar G. Sequential mast cell infiltration and degranulation during experimental carcinogenesis. J Cancer Res Clin Oncol 1991; 117: 115-22.
49. Lachter J, Stein M, Lichtig C, Eidelman S, Munichor M. Mast cells in colorectal neoplasias and premalignant disorders. Dis Colon Rectum 1995; 38: 290-3.
50. Kawai N, Tsuji S, Tsujii M, Ito T, Yasumaru M, Kakiuchi Y, Kimura A, Komori M, Sasaki Y, Hayashi N, Kawano S, Dubois R, Hori M. Tumor necrosis factor alpha stimulates invasion of Src-activated intestinal cells. Gastroenterology 2002; 122: 331-9.
51. Bischoff SC, Lorentz A, Schwengberg S, Weier G, Raab R, Manus MP. Mast cells are an important cellular source of tumour necrosis factor α in human intestinal tissue. Gut 1999; 44: 643-52.
52. Korenaga D, Takesue F, Kido K, Yasuda M, Inutsuka S, Honda M, Nagahama S. Impaired antioxidant defense system of colonic tissue and cancer development in dextran sulfate sodium-induced colitis in mice. J Surg Res 2002; 102: 144-9.
53. Yoshimi N, Sato S, Makita H, Wang A, Hirose Y, Tanaka T, Mori H. Expression of cytokines, TNF-α and IL-1α, in MAM acetate and 1-hydroxyanthraquinone-induced colon carcinogenesis in rats. Carcinogenesis 1994; 15: 783-5.
54. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, Werb Z, Caughey GH, Hanahan D. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 1999; 13: 1382-97.
55. Mirvish SS, Haorah J, Zhou L, Clapper ML, Harrison KL, Povey AC. Total N-nitroso compounds and their precursors in hot dogs and in the gastrointestinal tract and feces of rats and mice: possible etiologic agents for colon cancer. J Nutr 2002; 132: 3526S-9S.