A DNA methyltransferase inhibitor and All-trans retinoic acid reduce oral cavity carcinogenesis induced by the carcinogen 4-nitroquinoline 1-oxide

Cancer Prevention Research

Volumn 2, Issue 12, 2009, Pages 1100-1110

  Tang, Xiao Han ^a   Albert, Martin ^a   Scognamiglio, Theresa ^a   Gudas, Lorraine J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 NITROQUINOLINE 1 OXIDE; 5 AZA 2' DEOXYCYTIDINE; CELL NUCLEUS ANTIGEN; CYCLINE; DNA METHYLTRANSFERASE INHIBITOR; PROTEIN P16; RETINOIC ACID; ANTINEOPLASTIC AGENT; AZACITIDINE; CARCINOGEN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLOOXYGENASE 2; DNA METHYLTRANSFERASE; DRUG DERIVATIVE; MESSENGER RNA; PROTEIN C MYB; PTGS2 PROTEIN, MOUSE; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR BETA; RETINOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER PREVENTION; CARCINOGENESIS; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE SEVERITY; DNA METHYLATION; DRUG EFFICACY; DRUG MEGADOSE; EPITHELIUM CELL; FEMALE; HISTOPATHOLOGY; LOW DRUG DOSE; MOUSE; MOUTH CANCER; MOUTH CAVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TONGUE TUMOR; ANIMAL; BLOOD; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DRUG ANTAGONISM; DRUG EFFECT; ENZYME IMMUNOASSAY; GENETICS; METABOLISM; MOUTH MUCOSA; MOUTH TUMOR; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SQUAMOUS CELL CARCINOMA;

4-NITROQUINOLINE-1-OXIDE; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; AZACITIDINE; CARCINOGENS; CARCINOMA, SQUAMOUS CELL; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLOOXYGENASE 2; DNA MODIFICATION METHYLASES; FEMALE; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED C57BL; MOUTH MUCOSA; MOUTH NEOPLASMS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTO-ONCOGENE PROTEINS C-MYB; RECEPTORS, RETINOIC ACID; RETINOIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRETINOIN;

EID: 76549130531     PISSN: 19406207     EISSN: None     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-09-0136     Document Type: Article

References (50)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96.
2. Tang XH, Knudsen B, Bemis D, Tickoo S, Gudas LJ. Oral cavity and esophageal carcinogenesis modeled in carcinogen-treated mice. Clin Cancer Res 2004;10:301-13.
3. Haddad RI, Shin DM. Recent advances in head and neck cancer. N Engl J Med 2008;359:1143-54.
4. Lippman SM, Sudbo J, Hong WK. Oral cancer prevention and the evolution of molecular-targeted drug development. J Clin Oncol 2005;23:346-56.
5. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007;128:683-92.
6. Chan TL, Yuen ST, Kong CK, et al. Heritable germline epimutation of MSH2 in a family with hereditary nonpolyposis colorectal cancer. Nat Genet 2006; 38:1178-83.
7. Linhart HG, Lin H, Yamada Y, et al. Dnmt3b promotes tumorigenesis in vivo by gene-specific de novo methylation and transcriptional silencing. Genes Dev 2007;21:3110-22.
8. Lin H, Yamada Y, Nguyen S, et al. Suppression of intestinal neoplasia by deletion of Dnmt3b. Mol Cell Biol 2006;26:2976-83.
9. Yoo CB, Chuang JC, Byun HM, et al. Long-term epigenetic therapy with oral zebularine has minimal side effects and prevents intestinal tumors in mice. Cancer Prev Res 2008;1:233-40.
10. McCabe MT, Low JA, Daignault S, Imperiale MJ, Wojno KJ, Day ML. Inhibition of DNA methyltransferase activity prevents tumorigenesis in a mouse model of prostate cancer. Cancer Res 2006;66:385-92.
11. Zorn CS, Wojno KJ, McCabe MT, Kuefer R, Gschwend JE, Day ML. 5-Aza-2′-deoxycytidine delays androgen-independent disease and improves survival in the transgenic adenocarcinoma of the mouse prostate mouse model of prostate cancer. Clin Cancer Res 2007;13:2136-43.
12. Shaw R. The epigenetics of oral cancer. Int J Oral Maxillofac Surg 2006;35:101-8.
13. Issa JP. DNA methylation as a therapeutic target in cancer. Clin Cancer Res 2007;13:1634-7.
14. Issa JP. Cancer prevention: epigenetics steps up to the plate. Cancer Prev Res 2008;1:219-22.
15. Gudas LJ, Sporn MB, Roberts AB. Cell biology and biochemistry of the retinoids. In: Sporn MB, Roberts AB, Goodman DS, editors. The retinoids: biology, chemistry, and medicine. New York: Raven Press; 1994, p. 443-520.
16. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996;10:940-54.
17. Mongan NP, Gudas LJ. Diverse actions of retinoid receptors in cancer prevention and treatment. Differentiation 2007;75:853-70.
18. Clarke N, Germain P, Altucci L, Gronemeyer H. Retinoids: potential in cancer prevention and therapy. Expert Rev Mol Med 2004;6:1-23.
19. Hong WK, Itri LM. Retinoids and human cancer. In: Sporn MB, Roberts AB, Goodman DS, editors. The retinoids: biology, chemistry, and medicine. 2nd ed. New York: Raven Press; 1994, p. 597-630.
20. Schroeder CP, Kadara H, Lotan D, et al. Involvement of mitochondrial and Akt signaling pathways in augmented apoptosis induced by a combination of low doses of celecoxib and N-(4-hydroxyphenyl) retinamide in premalignant human bronchial epithelial cells. Cancer Res 2006;66:9762-70.
21. Conway AE, Lindgren A, Galic Z, et al. A self-renewal program controls the expansion of genetically unstable cancer stem cells in pluripotent stem cell-derived tumors. Stem Cells 2009;27:18-28.
22. de Thé H, Vivanco-Ruiz M, Tiollais P, Stunnenberg H, Dejean A. Identification of a retinoic acid responsive element in the retinoic acid receptor β gene. Nature 1990;343:177-80.
23. Xu XC. Tumor-suppressive activity of retinoic acid receptor-β in cancer. Cancer Lett 2007;253:14-24.
24. Youssef EM, Lotan D, Issa JP, et al. Hypermethylation of the retinoic acid receptor-β(2) gene in head and neck carcinogenesis. Clin Cancer Res 2004;10: 1733-42.
25. Gimenez-Conti IB, Slaga TJ. The hamster cheek pouch carcinogenesis model. J Cell Biochem Suppl 1993;17F:83-90.
26. Suzuki R, Kohno H, Suzui M, et al. 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 2006;27:619-30.
27. Raimondi AR, Molinolo A, Gutkind JS. Rapamycin prevents early onset of tumorigenesis in an oralspecific K-ras and p53 two-hit carcinogenesis model. Cancer Res 2009, In press.
28. Tang XH, Su D, Albert M, Scognamiglio T, Gudas LJ. Overexpression of lecithin:retinol acyltransferase in the epithelial basal layer makes mice more sensitive to oral cavity carcinogenesis induced by a carcinogen. Cancer Biol Ther 2009, In press.
29. Vitale-Cross L, Czerninski R, Amornphimoltham P, Patel V, Molinolo AA, Gutkind JS. Chemical carcinogenesis models for evaluating moleculartargeted prevention and treatment of oral cancer. Cancer Prev Res 2009;2:419-22.
30. Liu L, Gudas LJ. Disruption of the lecithin:retinol acyltransferase gene makes mice more susceptible to vitamin a deficiency. J Biol Chem 2005;280: 40226-34.
31. Tang XH, Suh MJ, Li R, Gudas LJ. Cell proliferation inhibition and alterations in retinol esterification induced by phytanic acid and docosahexaenoic acid. J Lipid Res 2007;48:165-76.
32. Gillespie RF, Gudas LJ. Retinoic acid receptor isotype specificity in f9 teratocarcinoma stem cells results from the differential recruitment of coregulators to retinoic acid response elements. J Biol Chem 2007;282:33421-34.
33. Warnakulasuriya S, Reibel J, Bouquot J, Dabelsteen E. Oral epithelial dysplasia classification systems: predictive value, utility, weaknesses and scope for improvement. J Oral Pathol Med 2008;37:127-33.
34. Achkar CC, Bentel JM, Boylan JF, Scher HI, Gudas LJ, Miller WH, Jr. Differences in the pharmacokinetic properties of orally administered all-trans-retinoic acid and 9-cis-retinoic acid in the plasma of nude mice. Drug Metab Dispos 1994;22:451-8.
35. Hu L, Crowe DL, Rheinwald JG, Chambon P, Gudas LJ. Abnormal expression of retinoic acid receptors and keratin 19 by human oral and epidermal squamous cell carcinoma cell lines. Cancer Res 1991;51:3972-81.
36. Song S, Guan B, Men T, Hoque A, Lotan R, Xu XC. Antitumor effect of retinoic acid receptor-β2 associated with suppression of cyclooxygenase-2. Cancer Prev Res 2009;2:274-80.
37. Chan G, Boyle JO, Yang EK, et al. Cyclooxygenase-2 expression is up-regulated in squamous cell carcinoma of the head and neck. Cancer Res 1999; 59:991-4.
38. Nguyen DC, Parsa B, Close A, Magnusson B, Crowe DL, Sinha UK. Overexpression of cell cycle regulatory proteins correlates with advanced tumor stage in head and neck squamous cell carcinomas. Int J Oncol 2003;22:1285-90.
39. Moldovan GL, Pfander B, Jentsch S. PCNA, the maestro of the replication fork. Cell 2007;129: 665-79.
40. Sherr CJ. Principles of tumor suppression. Cell 2004;116:235-46.
41. Hunter KD, Thurlow JK, Fleming J, et al. Divergent routes to oral cancer. Cancer Res 2006;66: 7405-13.
42. Yakushiji T, Uzawa K, Shibahara T, Noma H, Tanzawa H. Over-expression of DNA methyltransferases and CDKN2A gene methylation status in squamous cell carcinoma of the oral cavity. Int J Oncol 2003;22:1201-7.
43. Khuri FR, Lee JJ, Lippman SM, et al. Randomized phase III trial of low-dose isotretinoin for prevention of second primary tumors in stage I and II head and neck cancer patients. J Natl Cancer Inst 2006;98: 441-50.
44. Mongan NP, Gudas LJ. Valproic acid, in combination with all-trans retinoic acid and 5-aza-2′-deoxycytidine, restores expression of silenced RARβ2 in breast cancer cells. Mol Cancer Ther 2005;4:477-86.
45. Hatoum A, El-Sabban ME, Khoury J, Yuspa SH, Darwiche N. Overexpression of retinoic acid receptors α and γ into neoplastic epidermal cells causes retinoic acid-induced growth arrest and apoptosis. Carcinogenesis 2001;22:1955-63.
46. Sirchia SM, Ferguson AT, Sironi E, et al. Evidence of epigenetic changes affecting the chromatin state of the retinoic acid receptor β2 promoter in breast cancer cells. Oncogene 2000;19:1556-63.
47. Whang YM, Choi EJ, Seo JH, Kim JS, Yoo YD, Kim YH. Hyperacetylation enhances the growthinhibitory effect of all-trans retinoic acid by the restoration of retinoic acid receptor β expression in head and neck squamous carcinoma (HNSCC) cells. Cancer Chemother Pharmacol 2005;56:543-55.
48. Chen Z, Zhang X, Li M, et al. Simultaneously targeting epidermal growth factor receptor tyrosine kinase and cyclooxygenase-2, an efficient approach to inhibition of squamous cell carcinoma of the head and neck. Clin Cancer Res 2004;10:5930-9.
49. Mestre JR, Subbaramaiah K, Sacks PG, et al. Retinoids suppress epidermal growth factor-induced transcription of cyclooxygenase-2 in human oral squamous carcinoma cells. Cancer Res 1997;57: 2890-5.
50. Khanduja KL, Kumar S, Varma N, Varma SC, Avti PK, Pathak CM. Enhancement in α-tocopherol succinate-induced apoptosis by all-trans-retinoic acid in primary leukemic cells: role of antioxidant defense, Bax and c-myc. Mol Cell Biochem 2008; 319:133-9.