Mechanisms of oral carcinogenesis induced by dibenzo[a,l]pyrene: An environmental pollutant and a tobacco smoke constituent

International Journal of Cancer

Volumn 133, Issue 6, 2013, Pages 1300-1309

  Chen, Kun Ming ^a   Guttenplan, Joseph B ^b   Zhang, Shang Min ^a   Aliaga, Cesar ^a   Cooper, Timothy K ^a   Sun, Yuan Wan ^a   Deltondo, Joseph ^a   Kosinska, Wieslawa ^b   Sharma, Arun K ^a   Jiang, Kun ^a   Bruggeman, Richard ^a   Ahn, Kwangmi ^a   Amin, Shantu ^a   El Bayoumy, Karam ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

carcinogenesis; COX 2; mutagenesis; oral cancer; p53

Indexed keywords

11,12 DIHYDROXY 13,14 EPOXY 11,12,13,14 TETRAHYDRODIBENZO[A,L]PYRENE; CYCLOOXYGENASE 2; DIBENZO[A,L]PYRENE; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN P53; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CARCINOGENICITY; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CII GENE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE MUTATION; GENETIC ANALYSIS; GENETIC REGULATION; LACI GENE; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; MUTAGENICITY; NONHUMAN; ONCOGENE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPORTER GENE; TONGUE CARCINOMA;

CARCINOGENESIS; COX-2; MUTAGENESIS; ORAL CANCER; P53;

ANIMALS; BENZOPYRENES; CARCINOGENS, ENVIRONMENTAL; FEMALE; GENES, P53; IMMUNOHISTOCHEMISTRY; MICE; MOUTH NEOPLASMS; MUTATION; SMOKE; TOBACCO;

EID: 84879992235     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28152     Document Type: Article

References (50)

1. Fuller CD, Wang SJ, Thomas CR, Jr, et al. Conditional survival in head and neck squamous cell carcinoma: results from the SEER dataset 1973-1998. Cancer 2007; 109: 1331-43.
2. Siegel R, Naishadham D, Jemal A,. Cancer statistics, 2012. CA: A Cancer J Clinicians 2012; 62: 10-29.
3. Parkin DM, Bray F, Ferlay J, et al. Global cancer statistics, 2002. CA: Cancer J Clinicians 2005; 55: 74-108.
4. Boone CW, Kelloff GJ, Steel V,. Histopathology of the premalignant process. Cancer Bull 1991; 43: 481-4.
5. Kramer IR, Lucas RB, Pindborg JJ, et al. Definition of leukoplakia and related lesions: an aid to studies on oral precancer. Oral Surg Oral Med Oral Pathol 1978; 46: 518-39.
6. Franco EL, Kowalski LP, Kanda JL,. Risk factors for second cancers of the upper respiratory and digestive systems: a case-control study. J Clin Epidemiol 1991; 44: 615-25.
7. Licciardello JT, Spitz MR, Hong WK,. Multiple primary cancer in patients with cancer of the head and neck: second cancer of the head and neck, esophagus, and lung. Int J Radiat Oncol Biol Phys 1989; 17: 467-76.
8. Lippman SM, Hong WK,. Second malignant tumors in head and neck squamous cell carcinoma: the overshadowing threat for patients with early-stage disease. Int J Radiat Oncol Biol Phys 1989; 17: 691-4.
9. Day GL, Blot WJ,. Second primary tumors in patients with oral cancer. Cancer 1992; 70: 14-9.
10. Jovanovic A, van der Tol IG, Schulten EA, et al. Risk of multiple primary tumors following oral squamous-cell carcinoma. Int J Cancer 1994; 56: 320-3.
11. Forastiere A, Koch W, Trotti A, et al. Head and neck cancer. N Engl J Med 2001; 345: 1890-900.
12. Wong KK,. Oral-specific chemical carcinogenesis in mice: an exciting model for cancer prevention and therapy. Cancer Prev Res (Phila Pa) 2009; 2: 10-3.
13. Vitale-Cross L, Czerninski R, Amornphimoltham P, et al. Chemical carcinogenesis models for evaluating molecular-targeted prevention and treatment of oral cancer. Cancer Prev Res (Phila Pa) 2009; 2: 419-22.
14. Raimondi AR, Molinolo A, Gutkind JS,. Rapamycin prevents early onset of tumorigenesis in an oral-specific K-ras and p53 two-hit carcinogenesis model. Cancer Res 2009; 69: 4159-66.
15. Hoffmann D, Hoffmann I, El-Bayoumy K,. The less harmful cigarette: a controversial issue: a tribute to Ernst L. Wynder. Chem Res Toxicol 2001; 14: 767-90.
16. Luch A,. On the impact of the molecule structure in chemical carcinogenesis. Exs 2009; 99: 151-79.
17. Leavitt SA, George MH, Moore T, et al. Mutations induced by benzo[a]pyrene and dibenzo[a,l]pyrene in lacI transgenic B6C3F1 mouse lung result from stable DNA adducts. Mutagenesis 2008; 23: 445-50.
18. Guttenplan JB, Kosinska W, Zhao ZL, et al. Mutagenesis and carcinogenesis induced by dibenzo[a,l]pyrene in the mouse oral cavity: a potential new model for oral cancer. Int J Cancer 2012; 130: 2783-90.
19. Krzeminski J, Lin JM, Amin S, et al. Synthesis of Fjord region diol epoxides as potential ultimate carcinogens of dibenzo[a,l]pyrene. Chem Res Toxicol 1994; 7: 125-9.
20. Leininger JR, Jokinen MP, et al. Oral cavity, esophagus, and stomach. St. Louis, MO: Cache River Press, 1999.
21. Boyiri T, Guttenplan J, Khmelnitsky M, et al. Mammary carcinogenesis and molecular analysis of in vivo cII gene mutations in the mammary tissue of female transgenic rats treated with the environmental pollutant 6-nitrochrysene. Carcinogen 2004; 25: 637-43.
22. Chen KM, Zhang SM, Aliaga C, et al. Induction of ovarian cancer and DNA adducts by Dibenzo[a,l]pyrene in the mouse. Chem Res Toxicol 2012; 25: 374-80.
23. Zhang SM, Chen KM, Aliaga C, et al. Identification and quantification of DNA adducts in the oral tissues of mice treated with the environmental carcinogen dibenzo[a,l]pyrene by HPLC-MS/MS. Chem Res Toxicol 2011; 24: 1297-303.
24. Tam AS, Foley JF, Devereux TR, et al. High frequency and heterogeneous distribution of p53 mutations in aflatoxin B1-induced mouse lung tumors. Cancer Res 1999; 59: 3634-40.
25. Trukhanova LS, Hong HH, Sills RC, et al. Predominant p53 G->A transition mutation and enhanced cell proliferation in uterine sarcomas of CBA mice treated with 1,2-dimethylhydrazine. Toxicol Pathol 1998; 26: 367-74.
26. Guttenplan JB, Spratt TE, Khmelnitsky M, et al. Effects of 3H-1,2-dithiole-3-thione, 1,4-phenylenebis(methylene)selenocyanate, and selenium-enriched yeast individually and in combination on benzo[a]pyrene- induced mutagenesis in oral tissue and esophagus in lacZ mice. Mutat Res 2004; 559: 199-210.
27. Bradley G, Irish J, MacMillan C, et al. Abnormalities of the ARF-p53 pathway in oral squamous cell carcinoma. Oncogene 2001; 20: 654-8.
28. Marsit CJ, Christensen BC, Houseman EA, et al. Epigenetic profiling reveals etiologically distinct patterns of DNA methylation in head and neck squamous cell carcinoma. Carcinogenesis 2009; 30: 416-22.
29. Hjortsberg L, Rubio-Nevado JM, Hamroun D, et al. The p53 Handbook, ed. 2, 2008. Available at: http://p53.free.fr/Database/p53-database.html.
30. Ogden GR, Kiddie RA, Lunny DP, et al. Assessment of p53 protein expression in normal, benign, and malignant oral mucosa. J Pathol 1992; 166: 389-94.
31. Field JK, Spandidos DA, Malliri A, et al. Elevated P53 expression correlates with a history of heavy smoking in squamous cell carcinoma of the head and neck. Br J Cancer 1991; 64: 573-7.
32. Gallo O, Schiavone N, Papucci L, et al. Down-regulation of nitric oxide synthase-2 and cyclooxygenase-2 pathways by p53 in squamous cell carcinoma. Am J Pathol 2003; 163: 723-32.
33. Mendes RA, Carvalho JF, Waal I,. An overview on the expression of cyclooxygenase-2 in tumors of the head and neck. Oral Oncol 2009; 45: e124-8.
34. Atula T, Hedstrom J, Ristimaki A, et al. Cyclooxygenase-2 expression in squamous cell carcinoma of the oral cavity and pharynx: association to p53 and clinical outcome. Oncol Rep 2006; 16: 485-90.
35. Olshan AF, Weissler MC, Pei H, et al. p53 mutations in head and neck cancer: new data and evaluation of mutational spectra. Cancer Epidemiol Biomarkers Prev 1997; 6: 499-504.
36. Le Page F, Margot A, Grollman AP, et al. Mutagenicity of a unique 8-oxoguanine in a human Ha-ras sequence in mammalian cells. Carcinogenesis 1995; 16: 2779-84.
37. Denissenko MF, Pao A, Tang M, et al. Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science 1996; 274: 430-2.
38. Ruggeri B, DiRado M, Zhang SY, et al. Benzo[a]pyrene-induced murine skin tumors exhibit frequent and characteristic G to T mutations in the p53 gene. Proc Natl Acad Sci USA 1993; 90: 1013-7.
39. Klingelhofer J, Senolt L, Baslund B, et al. Up-regulation of metastasis-promoting S100A4 (Mts-1) in rheumatoid arthritis: putative involvement in the pathogenesis of rheumatoid arthritis. Arthritis Rheumatism 2007; 56: 779-89.
40. Bruno T, De Nicola F, Iezzi S, et al. Che-1 phosphorylation by ATM/ATR and Chk2 kinases activates p53 transcription and the G2/M checkpoint. Cancer Cell 2006; 10: 473-86.
41. Stott FJ, Bates S, James MC, et al. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J 1998; 17: 5001-14.
42. Hong S, Pusapati RV, Powers JT, et al. Oncogenes and the DNA damage response: Myc and E2F1 engage the ATM signaling pathway to activate p53 and induce apoptosis. Cell cycle (Georgetown, Tex 2006; 5: 801-3.
43. Sperka T, Wang J, Rudolph KL,. DNA damage checkpoints in stem cells, ageing and cancer. Nat Rev Mol Cell Biol 2012; 13: 579-90.
44. Chipuk JE, Kuwana T, Bouchier-Hayes L, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004; 303: 1010-4.
45. Takimoto R, Wang W, Dicker DT, et al. The mutant p53-conformation modifying drug, CP-31398, can induce apoptosis of human cancer cells and can stabilize wild-type p53 protein. Cancer Biol Therapy 2002; 1: 47-55.
46. Shetty S, Shetty P, Idell S, et al. Regulation of plasminogen activator inhibitor-1 expression by tumor suppressor protein p53. J Biol Chem 2008; 283: 19570-80.
47. Bodvarsdottir SK, Steinarsdottir M, Hilmarsdottir H, et al. MYC amplification and TERT expression in breast tumor progression. Cancer Gene Cytogene 2007; 176: 93-9.
48. Blons H, Pallier K, Le Corre D, et al. Genome wide SNP comparative analysis between EGFR and KRAS mutated NSCLC and characterization of two models of oncogenic cooperation in non-small cell lung carcinoma. BMC Med Genomics 2008; 1: 25.
49. Wei X, Xu H, Kufe D,. Human MUC1 oncoprotein regulates p53-responsive gene transcription in the genotoxic stress response. Cancer Cell 2005; 7: 167-78.
50. Luo J, Su F, Chen D, et al. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 2000; 408: 377-81.