An animal model for the rapid induction of tongue neoplasms in human c-Ha-ras proto-oncogene transgenic rats by 4-nitroquinoline 1-oxide: Its potential use for preclinical chemoprevention studies

Carcinogenesis

Volumn 27, Issue 3, 2006, Pages 619-630

  Suzuki, Rikako ^a,b   Kohno, Hiroyuki ^a   Suzui, Masumi ^c   Yoshimi, Naoki ^c   Tsuda, Hiroyuki ^d   Wakabayashi, Keiji ^e   Tanaka, Takuji ^a  

^a KANAZAWA MEDICAL UNIVERSITY   (Japan)

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

^c UNIVERSITY OF THE RYUKYUS   (Japan)

^d NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^e NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; 4 NITROQUINOLINE 1 OXIDE; BETA CATENIN; BIOLOGICAL MARKER; CYCLIN D1; CYCLOOXYGENASE 2; DNA; DRINKING WATER; FERULIC ACID; GLUTATHIONE TRANSFERASE; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOENZYME; NIMESULIDE; PIOGLITAZONE; RAS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INVASION; CARCINOGENESIS; CHEMOPROPHYLAXIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG EXPOSURE; DRUG SCREENING; DYSPLASIA; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INCIDENCE; MALE; MOUTH CANCER; NONHUMAN; ONCOGENE H RAS; PAPILLOMA; PLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIMULATION; SQUAMOUS CELL; SQUAMOUS CELL CARCINOMA; TONGUE CARCINOMA; TONGUE TUMOR; TRANSGENIC ANIMAL; TUMOR GROWTH;

4-NITROQUINOLINE-1-OXIDE; ADMINISTRATION, ORAL; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BETA CATENIN; CARCINOGENS; CELL TRANSFORMATION, NEOPLASTIC; CHEMOPREVENTION; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; NITRIC OXIDE SYNTHASE TYPE II; PLOIDIES; RATS; TONGUE NEOPLASMS;

EID: 33644849048     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgi241     Document Type: Article

References (65)

1. Stewart,B.W. and Kleihues,P. (eds) (2003) World Cancer Report. IARC, Lyon.
2. Patel,V., Leethanakul,C. and Gutkind,J.S. (2001) New approaches to the understanding of the molecular basis of oral cancer. Crit. Rev. Oral Biol. Med., 12, 55-63.
3. Davis,S. and Severson,R.K. (1987) Increasing incidence of cancer of the tongue in the United States among young adults. Lancet, 2, 910-911.
4. Macfarlane,G.J., Boyle,P., Evstifeeva,T.V., Robertson,C. and Scully,C. (1994) Rising trends of oral cancer mortality among males worldwide: The return of an old public health problem. Cancer Causes Control, 5, 259-265.
5. Mackenzie,J., Ah-See,K., Thakker,N., Sloan,P., Maran,A.G., Birch,J. and Macfarlane,G.J. (2000) Increasing incidence of oral cancer amongst young persons: What is the aetiology? Oral Oncol., 36, 387-389.
6. Day,G.L. and Blot,W.J. (1992) Second primary tumors inpatients with oral cancer. Cancer, 70, 14-19.
7. Slaughter,D.P., Southwick,H.W. and Smejkal,W. (1953) 'Field cancrization' in oral stratified squanrous epithelium: Clinical implications of multicentric origin. Cancer, 6, 963-968.
8. Tanaka,T. (1995) Chemoprevention of oral carcinogenesis. Eur. J. Cancer B Oral Oncol., 31B, 3-15.
9. Lippman,S.M. and Hong,W.K. (2002) Cancer prevention science and practice. Cancer Res., 62, 5119-5125.
10. Kim,E.S., Hong,W.K. and Khuri,F.R. (2002) Chemoprevention of aerodigestive tract cancers. Annu. Rev. Med., 53, 223-243.
11. Gimenez-Conti,I.B. and Slaga,T.J. (1992) The hamster cheek pouch model of carcinogenesis and chemoprevention. Adv. Exp. Med. Biol., 320, 63-67.
12. Gimenez-Conti,I.B. and Slaga,T.J. (1993) The hamster cheek pouch carcinogenesis model. J. Cell. Biochem. Suppl., 17F, 83-90.
13. Tanaka,T., Kojima,T., Okumura,A., Yoshimi,N. and Mori,H. (1991) Alterations of the nucleolar organizer regions during 4-nitroquinoline 1-oxide-induced tongue carcinogenesis in rats. Carcinogenesis, 12, 329-333.
14. Tang,X.H., Knudsen,B., Bemis,D., Tickoo,S. and Gudas,L.J. (2004) Oral cavity and esophageal carcinogenesis modeled in carcinogen-treated mice. Clin. Cancer Res., 10, 301-313.
15. Paterson,I.C., Eveson,J.W. and Prime,S.S. (1996) Molecular changes in oral cancer may reflect aetiology and ethnic origin. Eur. J. Cancer B Oral Oncol., 32B, 150-153.
16. Harris,C.C. (1996) p53 tumor suppressor gene: At the crossroads of molecular carcinogenesis, molecular epidemiology, and cancer risk assessment. Environ. Health Perspect., 104(suppl.), 435-439.
17. Frijhoff,A.F., Conti,C.J. and Senderowicz,A.M. (2004) Advances in molecular carcinogenesis: Current and future use of mouse models to screen and validate molecularly targeted anticancer drugs. Mol. Carcinog., 39, 183-194.
18. Bos,J.L. (1989) Ras oncogenes in human cancer: A review. Cancer Res., 49, 4682-4689.
19. Das,N., Majumder,J. and DasGupta,U.B. (2000) Ras gene mutations in oral cancer in eastern India. Oral Oncol., 36, 76-80.
20. Yuan,B., Heniford,B.M., Ackermann,D.M., Hawkins,B.L. and Hendler,F.J. (1994) Harvey ras (H-ras) point mutations are induced by 4-nitroquinoline-1-oxide in murine oral squamous epithelia, while squamous cell carcinomas and loss of heterozygosity occur without additional exposure. Cancer Res., 54, 5310-5317.
21. Caulin,C., Nguyen,T., Longley,M.A., Zhou,Z., Wang,X.J. and Roop,D.R. (2004) Inducible activation of oncogenic K-ras results in tumor formation in the oral cavity. Cancer Res., 64, 5054-5058.
22. Suzui,M., Yoshimi,N., Tanaka,T. and Mori,H. (1995) Infrequent Ha-ras mutations and absence of Ki-ras, N-ras, and p53 mutations in 4-nitroquinoline 1-oxide-induced rat oral lesions. Mol. Carcinog., 14, 294-298.
23. Resor,L., Bowen,T.J. and Wynshaw-Boris,A. (2001) Unraveling human cancer in the mouse: Recent refinements to modeling and analysis. Hum. Mol. Genet., 10, 669-675.
24. Klatt,P. and Serrano,M. (2003) Engineering cancer resistance in mice. Carcinogenesis, 24, 817-826.
25. Herzig,M. and Christofori,G. (2002) Recent advances in cancer research: mouse models of tumorigenesis. Biochim. Biophys. Acta, 1602, 97-113.
26. Green,J.E. and Hudson,T. (2005) The promise of genetically engineered mice for cancer prevention studies. Nat. Rev. Cancer, 5, 184-198.
27. Tsuda,H., Fukamachi,K., Ohshima,Y., Ueda,S., Matsuoka,Y., Hamaguchi,T., Ohnishi,T., Takasuka,N. and Naito,A. (2005) High susceptibility of human c-Ha-ras proto-oncogene transgenic rats to carcinogenesis: A cancer-prone animal model. Cancer Sci., 96, 309-316.
28. Yoshida,K., Tanaka,T., Hirose,Y., Yamaguchi,F., Kohno,H., Toida,M., Hara,A., Sugie,S., Shibata,T. and Mori,H. (2005) Dietary garcinol inhibits 4-nitroquinoline 1-oxide-induced tongue carcinogenesis in rats. Cancer Lett., 221, 29-39.
29. Yoshida,K., Hirose,Y., Tanaka,T. et al. (2003) Inhibitory effects of troglitazone, a peroxisome proliferator-activated receptor gamma ligand, in rat tongue carcinogenesis initiated with 4-nitroquinoline 1-oxide. Cancer Sci., 94, 365-371.
30. Iida,K., Yamamoto,M., Kato,M., Yoshida,K., Kurita,K. and Tatematsu,M. (1999) Strong expression of glutathione S-transferase placental form in early preneoplastic lesions and decrease with progression in hamster buccal pouch carcinogenesis. Cancer Lett., 135, 129-136.
31. Yoshida,K., Tanaka,T., Kohno,H., Sakata,K., Kawamori,T., Mori,H. and Wakabayashi,K. (2003) 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., 18, 39-48.
32. Suzui,M., Sugie,S., Mori,H., Okuno,M., Tanaka,T. and Moriwaki,H. (2001) Different mutation status of the beta-catenin gene in carcinogen-induced colon, brain, and oral tumors in rats. Mol. Carcinog., 32, 206-212.
33. Tanaka,T., Kohno,H., Yoshitani,S., Takashima,S., Okumura,A., Murakami,A. and Hosokawa,M. (2001) Ligands for peroxisome proliferator-activated receptors alpha and gamma inhibit chemically induced colitis and formation of aberrant crypt foci in rats. Cancer Res., 61, 2424-2428.
34. Tanaka,T., Kohno,H., Nomura,E., Taniguchi,H., Tsuno,T. and Tsuda,H. (2003) A novel geranylated derivative, ethyl 3-(4′-geranyloxy-3′-methoxyphenyl)-2-propenoate, synthesized from ferulic acid suppresses carcinogenesis and inducible nitric oxide synthase in rat tongue. Oncology, 64, 166-175.
35. Asamoto,M., Toriyama-Baba,H., Ohnishi,T., Naito,A., Ota,T., Ando,A., Ochiya,T. and Tsuda,H. (2002) Transgenic rats carrying human c-Ha-ras proto-oncogene are highly susceptible to N-nitrosomethylbenzylamine induction of esophageal tumorigenesis. Jpn. J. Cancer Res., 93, 744-751.
36. Banoczy,J. and Csiba,A. (1976) Occurrence of epithelial dysplasia in oral leukoplakia. Analysis and follow-up study of 12 cases. Oral Surg. Oral Med. Oral Pathol., 42, 766-774.
37. Kramer,I.R., Lucas,R.B., Pindborg,J.J. and Sobin,L.H. (1978) Definition of leukoplakia and related lesions: An aid to studies on oral precancer. Oral Surg. Oral Med. Oral Pathol., 46, 518-539.
38. Tanaka,T. (1986) Proliferative activity in dysplasia, carcinoma in situ and microinvasive carcinoma of the uterine cervix. Pathol. Res. Pract., 181, 531-539.
39. Tanaka,T., Mori,H., Takahashi,M. and Williams,G.M. (1984) DNA content of hyperplastic and neoplastic acinar cell lesions in rat and human pancreas. J. Exp. Pathol., 1, 315-326.
40. Mori,H., Tanaka,T., Sugie,S., Takahashi,M. and Williams,G.M. (1982) DNA content of liver cell nuclei of N-2-fluorenylacetamide-induced altered foci and neoplasms in rats and human hyperplastic foci. J. Natl Cancer Inst., 69, 1277-1282.
41. Hanahan,D. and Weinberg,R.A. (2000) The hallmarks of cancer. Cell, 100, 57-70.
42. Hunter,T. and Pines,J. (1994) Cyclins and cancer. II: Cyclin D and CDK inhibitors come of age. Cell, 79, 573-582.
43. Odajima,T., Sasaki,Y., Tanaka,N., Kato-Mori,Y., Asanuma,H., Ikeda,T., Satoh,M., Hiratsuka,H., Tokino,T. and Sawada,N. (2005) Abnormal beta-catenin expression in oral cancer with no gene mutation: correlation with expression of cyclin D1 and epidermal growth factor receptor, Ki-67 labeling index, and clinicopathological features. Virchows Arch., 36, 234-241.
44. Lippman,S.M., Sudbo,J. and Hong,W.K. (2005) Oral cancer prevention and the evolution of molecular-targeted drug development. J. Clin. Oncol., 23, 346-356.
45. Filmus,J., Robles,A.I., Shi,W., Wong,M.J., Colombo,L.L. and Conti,C.J. (1994) Induction of cyclin D1 overexpression by activated ras. Oncogene, 9, 3627-3633.
46. Aktas,H., Cai,H. and Cooper,G.M. (1997) Ras links growth factor signaling to the cell cycle machinery via regulation of cyclin D1 and the Cdk inhibitor p27KIP1. Mol. Cell Biol., 17, 3850-3857.
47. Tsuda,H., Fukushima,S., Wanibuchi,H., Morimura,K., Nakae,D., Imaida,K., Tatematsu, M., Hirose,M., Wakabayashi,K. and Moore,M.A. (2003) Value of GST-P positive preneoplastic hepatic foci in dose-response studies of hepatocarcinogenesis: Evidence for practical thresholds with both genotoxic and nongenotoxic carcinogens. A review of recent work. Toxicol. Pathol., 31, 80-86.
48. Chen,Y.K. and Lin,L.M. (1996) Sequential expression of placental glutathione S-transferase (GST-P) during DMBA-induced hamster buccal pouch squamous cell carcinogenesis. J. Oral. Pathol. Med., 25, 388-394.
49. Li,T., Hirayama,Y. and Kitano,M. (1997) Glutathione S-transferase pi-class as a tumour marker in lingual preneoplastic and neoplastic lesions of rats and humans. Virchows Arch., 431, 37-43.
50. Watanabe,K., Kawamori,T., Nakatsugi,S. and Wakabayashi,K. (2000) COX-2 and iNOS, good targets for chemoprevention of colon cancer. Biofactors, 12, 129-133.
51. Inoue,H., Yokoyama,C., Hara,S., Tone,Y. and Tanabe,T. (1995) Transcriptional regulation of human prostaglandin-endoperoxide synthase-2 gene by lipopolysaccharide and phorbol ester in vascular endothelial cells. Involvement of both nuclear factor for interleukin-6 expression site and cAMP response element. J. Biol. Chem., 270, 24965-24971.
52. Dubois,R.N., Abramson,S.B., Crofford,L., Gupta,R.A., Simon,L.S., Van De Putte,L.B. and Lipsky,P.E. (1998) Cyclooxygenase in biology and disease. FASEB J., 12, 1063-1073.
53. Chan,G., Boyle,J.O., Yang,E.K. et al. (1999) Cyclooxygenase-2 expression is up-regulated in squamous cell carcinoma of the head and neck. Cancer Res., 59, 991-994.
54. Takahashi,M. and Wakabayashi,K. (2004) Gene mutations and altered gene expression in azoxymethane-induced colon carcinogenesis in rodents. Cancer Sci., 95, 475-480.
55. Rao,C.V. (2004) Nitric oxide signaling in colon cancer chemoprevention. Mutat. Res., 555, 107-119.
56. Reddy,B.S. (2004) Studies with the azoxymethane-rat preclinical model for assessing colon tumor development and chemoprevention. Environ. Mol. Mutagen., 44, 26-35.
57. Lala,P.K. and Chakraborty,C. (2001) Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol., 2, 149-156.
58. Chen,Y.K., Hsue,S.S. and Lin,L.M. (2002) Increased expression of inducible nitric oxide synthase for human buccal squamous-cell carcinomas: Immunohistochemical, reverse transcription-polymerase chain reaction (RT-PCR) and in situ RT-PCR studies. Head Neck, 24, 925-932.
59. Tetsu,O. and McCormick,F. (1999) β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature, 398, 422-426.
60. Morin,P.J., Sparks,A.B., Korinek,V., Barker,N., Clevers,H., Vogelstein,B. and Kinzler,K.W. (1997) Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science, 275, 1787-1790.
61. Sudbo,J., Kildal,W., Risberg,B., Koppang,H.S., Danielsen,H.E. and Reith,A. (2001) DNA content as a prognostic marker in patients with oral leukoplakia. N. Engl. J. Med., 344, 1270-1278.
62. Sudbo,J., Bankfalvi,A., Bryne,M., Marcelpoil,R., Boysen,M., Piffko,J., Hemmer,J., Kraft,K. and Reith,A. (2000) Prognostic value of graph theory-based tissue architecture analysis in carcinomas of the tongue. Lab. Invest., 80, 1881-1889.
63. Sudbo,J., Ristimaki,A., Sondresen,J.E., Kildal,W., Boysen,M., Koppang,H.S., Reith,A., Risberg,B., Nesland,J.M. and Bryne,M. (2003) Cyclooxygenase-2 (COX-2) expression in high-risk premalignant oral lesions. Oral Oncol., 39, 497-505.
64. Wang,D., Mann,J.R. and DuBois,R.N. (2004) WNT and cyclooxygenase-2 cross-talk accelerates adenoma growth. Cell Cycle, 3, 1512-1515.
65. Han,S. and Roman,J. (2004) Suppression of prostaglandin E2 receptor subtype EP2 by PPARγ ligands inhibits human lung carcinoma cell growth. Biochem. Biophys. Res. Commun., 314, 1093-1099.