A specific inducible nitric oxide synthase inhibitor, ONO-1714 attenuates inflammation-related large bowel carcinogenesis in male ApcMin/+ mice

International Journal of Cancer

Volumn 121, Issue 3, 2007, Pages 506-513

  Kohno, Hiroyuki ^a   Takahashi, Mami ^b   Yasui, Yumiko ^a   Suzuki, Rikako ^a   Miyamoto, Shingo ^a   Kamanaka, Yoshihisa ^c   Naka, Masao ^c   Maruyama, Takayuki ^c   Wakabayashi, Keiji ^b   Tanaka, Takuji ^a  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c ONO PHARMACEUTICAL CO   (Japan)

Author keywords

Apcmin + mice; Chemoprevention; Colitis related carcinogenesis; Dextran sodium sulfate; iNOS

Indexed keywords

7 CHLORO 3 IMINO 5 METHYL 2 AZABICYCLO[4.1.0]HEPTANE; CYCLOOXYGENASE 2; DEXTRAN; DRINKING WATER; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; LIPID; MESSENGER RNA; NITRIC OXIDE SYNTHASE INHIBITOR; SODIUM SULFATE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; COLITIS; COLON ADENOCARCINOMA; COLON CARCINOGENESIS; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG SCREENING; LIPID BLOOD LEVEL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL;

ADENOCARCINOMA; ADENOMATOUS POLYPOSIS COLI; AMIDINES; ANIMALS; COLITIS; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; DEXTRAN SULFATE; DOSE-RESPONSE RELATIONSHIP, DRUG; HETEROCYCLIC COMPOUNDS, 2-RING; INTERLEUKIN-1BETA; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE II; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRIGLYCERIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34250886851     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22736     Document Type: Article

References (50)

1. Hussain SP, Hofseth LJ, Harris CC. Radical causes of cancer. Nat Rev Cancer 2003;3:276-85.
2. Lashner BA, Provencher KS, Bozdech JM, Brzezinski A. Worsening risk for the development of dysplasia or cancer in patients with chronic ulcerative colitis. Am J Gastroenterol 1995;90:377-80.
3. Tanaka T, Kohno H, Suzuki R, Yamada Y, Sugie S, Mori H. A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci 2003;94:965-73.
4. Kohno H, Suzuki R, Sugie S, Tanaka T. β-Catenin mutations in a mouse model of inflammation-related colon carcinogenesis induced by 1,2-dimethylhydrazine and dextran sodium sulfate. Cancer Sci 2005;96:69-76.
5. Tanaka T, Suzuki R, Kohno H, Sugie S, Takahashi M, Wakabayashi K, Colonic adenocarcinomas rapidly induced by the combined treatment with 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine and dextran sodium sulfate in male ICR mice possess β-catenin gene mutations and increases immunoreactivity for β-catenin, cyclooxygenase-2 and inducible nitric oxide synthase. Carcinogenesis 2005;26: 229-38.
6. Seril DN, Liao J, Ho KL, Warsi A, Yang CS, Yang GY. Dietary iron supplementation enhances DSS-induced colitis and associated colorectal carcinoma development in mice. Dig Dis Sci 2002;47:1266-78.
7. 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, B-catenin and p53 expression and the role of inflammation. Carcinogenesis 2000;21:757-68.
8. Min/+ mice: inflammatory stimuli by dextran sodium sulfate results in development of multiple colonic neoplasms. Int J Cancer 2006;118:25-34.
9. Kolios G, Valatas V, Ward SG. Nitric oxide in inflammatory bowel disease: a universal messenger in an unsolved puzzle. Immunology 2004;113:427-37.
10. Hofseth LJ, Hussain SP, Wogan GN, Harris CC. Nitric oxide in cancer and chemoprevention. Free Radic Biol Med 2003;34:955-68.
11. Singer II, Kawka DW, Scott S, Weidner JR, Mumford RA, Riehl TE, Stenson WF. Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology 1996;111:871-85.
12. Takahashi M, Wakabayashi K. Gene mutations and altered gene expression in azoxymethane-induced colon carcinogenesis in rodents. Cancer Sci 2004;95:475-80.
13. Suzuki R, Kohno H, Sugie S, Tanaka T. Dose-dependent promoting effect of dextran sodium sulfate on mouse colon carcinogenesis initiated with azoxymethane. Histol Histopathol 2005;20:483-92.
14. Naka M, Nanbu T, Kobayashi K, Kamanaka Y, Komeno M, Yanase R, Fukutomi T, Fujimura S, Seo HG, Fujiwara N, Ohuchida S, Suzuki K, et al. A potent inhibitor of inducible nitric oxide synthase, ONO-1714, a cyclic amidine derivative. Biochem Biophys Res Commun 2000;270:663-7.
15. Hayashi Y, Abe M, Murai A, Shimizu N, Okamoto I, Katsuragi T, Tanaka K. Comparison of effects of nitric oxide synthase (NOS) inhibitors on plasma nitrite/nitrate levels and tissue NOS activity in septic organs. Microbiol Immunol 2005;49:139-47.
16. Asp12 cDNA markedly elevates IL-1β- and lipopolysaccharide-mediated inducible nitric oxide synthase expression in rat intestinal epithelial cells. Oncogene 2003;22:7667-76.
17. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 1992;256:668-70.
18. Takahashi M, Mutoh M, Shoji Y, Sato H, Kamanaka Y, Naka M, Maruyama T, Sugimura T, Wakabayashi K. Suppressive effect of an inducible nitric oxide inhibitor, ONO-1714, on AOM-induced rat colon carcinogenesis. Nitric Oxide 2006;14:130-6.
19. Watanabe K, Kawamori T, Nakatsugi S, Ohta T, Ohuchida S, Yamamoto H, Maruyama T, Kondo K, Ushikubi F, Narumiya S, Sugimura T, Wakabayashi K. Role of the prostaglandin E receptor subtype EP, in colon carcinogenesis. Cancer Res 1999;59:5093-6.
20. Ward JM. Morphogenesis of chemically induced neoplasms of the colon and small intestine in rats. Lab Invest 1974;30:505-13.
21. Cooper HS, Murthy SN, Shah RS, Sedergran DJ. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 1993;69:238-49.
22. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004;287:G7-G17.
23. Naito Y, Takagi T, Ishikawa T, Handa O, Matsumoto N, Yagi N, Matsuyama K, Yoshida N, Yoshikawa T. The inducible nitric oxide synthase inhibitor ONO-1714 blunts dextran sulfate sodium colitis in mice. Eur J Pharmacol 2001;412:91-9.
24. Kohno H, Suzuki R, Curini M, Epifano F, Maltese F, Gonzales SP, Tanaka T. Dietary administration with prenyloxycoumarins, auraptene and collinin, inhibits colitis-related colon carcinogenesis in mice. Int J Cancer 2006;118:2936-42.
25. Takamatsu Y, Shimada K, Yamaguchi K, Kuroki S, Chijiiwa K, Tanaka M. Inhibition of inducible nitric oxide synthase prevents hepatic, but not pulmonary, injury following ischemia-reperfusion of rat liver, Dig Dis Sci 2006;51:571-9.
26. Ambs S, Merriam WG, Bennett WP, Felley-Bosco E, Ogunfusika MO, Oser SM, Klein S, Shields PG, Billiar TR, Harris CC. Frequent nitric oxide synthase-2 expression in human colon adenomas: implication for tumor angiogenesis and colon cancer progression. Cancer Res 1998;58:334-41.
27. Kankuri E, Hamalainen M, Hukkanen M, Salmenpera P, Kivilaakso E, Vapaatalo H, Moilanen E. Suppression of pro-inflammatory cytokine release by selective inhibition of inducible nitric oxide synthase in mucosal explants from patients with ulcerative colitis. Scand J Gastroenterol 2003;38:186-92.
28. 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.
29. Kohno H, Suzuki R, Sugie S, Tanaka T. Suppression of colitis-related mouse colon carcinogenesis by a COX-2 inhibitor and PPAR ligands. BMC Cancer 2005;5:46.
30. Rao CV, Kawamori T, Hamid R, Reddy BS. Chemoprevention of colonic aberrant crypt foci by an inducible nitric oxide synthase-selective inhibitor. Carcinogenesis 1999;20:641-4.
31. Min/+ mice by inhibiting nitric oxide production. Cancer Res 2001;61:8357-60.
32. Yoshida K, Tanaka T, Kohno H, Sakata K, Kawamori T, Mori H, Wakabayashi K. A COX-2 inhibitor, nimesulide, inhibits chemically-induced rat tongue carcinogenesis through suppression of cell proliferation activity and COX-2 and iNOS expression. Histol Histopathol 2003;18:39-48.
33. Koehne CH, Dubois RN. COX-2 inhibition and colorectal cancer. Semin Oncol 2004;31:12-21.
34. Kawamori T, Rao CV, Seibert K, Reddy BS. Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res 1998;58:409-12.
35. Kim SF, Huri DA, Snyder SH. Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science 2005;310: 1966-70.
36. Cianchi F, Cortesini C, Fantappie O, Messerini L, Sardi I, Lasagna N, Perna F, Fabbroni V, Di Felice A, Perigli G, Mazzanti R, Masini E. Cyclooxygenase-2 activation mediates the proangiogenic effect of nitric oxide in colorectal cancer. Clin Cancer Res 2004;10:2697-704.
37. Lala PK, Chakraborty C. Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol 2001;2:149-56.
38. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol 2005;98:1154-62.
39. Reimund JM, Wittersheim C, Dumont S, Muller CD, Baumann R, Poindron P, Duclos B. Mucosal inflammatory cytokine production by intestinal biopsies in patients with ulcerative colitis and Crohn's disease. J Clin Immunol 1996;16:144-50.
40. Agoff SN, Brentnall TA, Crispin DA, Taylor SL, Raaka S, Haggitt RC, Reed MW, Afonina IA, Rabinovitch PS, Stevens AC, Feng Z, Bronner MP. The role of cyclooxygenase 2 in ulcerative colitis-associated neoplasia. Am J Pathol 2000;157:737-45.
41. Papadakis KA, Targan SR. Tumor necrosis factor: biology and therapeutic inhibitors. Gastroenterology 2000;119:1148-57.
42. Tsune I, Ikejima K, Hirose M, Yoshikawa M, Enomoto N, Takei Y, Sato N. Dietary glycine prevents chemical-induced experimental colitis in the rat. Gastroenterology 2003;125:775-85.
43. Kojouharoff G, Hans W, Obermeier F, Mannel DN, Andus T, Scholmerich J, Gross V, Falk W. Neutralization of tumour necrosis factor (TNF) but not of IL-1 reduces inflammation in chronic dextran sulphate sodium-induced colitis in mice. Clin Exp Immunol 1997;107: 353-8.
44. Cominelli F, Nast CC, Duchini A, Lee M. Recombinant interleukin-1 receptor antagonist blocks the proinflammatory activity of endogenous interleukin-1 in rabbit immune colitis. Gastroenterology 1992;103:65-71.
45. Naito Y, Takagi T, Handa O, Ishikawa T, Nakagawam S, Yamaguchi T, Yoshida N, Minami M, Kita M, Imanishi J, Yoshikawa T. Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-α deficient mice. J Gastroenterol Hepatol 2003;18:560-9.
46. McKeown-Eyssen GE. Epidemiology of colorectal cancer revisited: are serum triglycerides and/or plasma glucose associated with risk? Cancer Epidemiol Biomarkers Prev 1994;3:687-95.
47. Koohestani N, Chia MC, Pham NA, Tran TT, Minkin S, Wolever TM, Bruce WR. Aberrant crypt focus promotion and glucose intolerance: correlation in the rat across diets differing in fat, n-3 fatty acids and energy. Carcinogenesis 1998;19:1679-84.
48. Niho N, Takahashi M, Kitamura T, Shoji Y, Itoh M, Noda T, Sugimura T, Wakabayashi K. Concomitant suppression of hyperlipidemia and intestinal polyp formation in Apc-deficient mice by peroxisome proliferator-activated receptor ligands. Cancer Res 2003;63: 6090-5.
49. Niho N, Takahashi M, Shoji Y, Takeuchi Y, Matsubara S, Sugimura T, Wakabayashi K. Dose-dependent suppression of hyperlipidemia and intestinal polyp formation in Min mice by pioglitazone, a PPAR γ ligand. Cancer Sci 2003;94:960-4.
50. Niho N, Mutoh M, Takahashi M, Tsutsumi K, Sugimura T, Wakabayashi K. Concurrent suppression of hyperlipidemia and intestinal polyp formation by NO-1886, increasing lipoprotein lipase activity in Min mice. Proc Natl Acad Sci USA 2005;102:2970-4.