Differential requirement of signal pathways for benzo[a]pyrene (B[a]P)-induced nitric oxide synthase (iNOS) in rat esophageal epithelial cells

Carcinogenesis

Volumn 26, Issue 6, 2005, Pages 1035-1043

  Chen, Jingyuan ^a,b   Yan, Yan ^a,b   Li, Jingxia ^a   Ma, Qian ^a   Stoner, Gary D ^c   Ye, Jianping ^d   Huang, Chuanshu ^a  

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

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c OHIO STATE UNIVERSITY   (United States)

^d PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; BENZO[A]PYRENE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE SYNTHASE; CARCINOGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; MAMMALIAN TARGET OF RAPAMYCIN; NOS2 PROTEIN, RAT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; S6 KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME INDUCTION; EPITHELIUM CELL; ESOPHAGUS; ESOPHAGUS CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CELL LINE; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; TIME;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BENZO(A)PYRENE; CARCINOGENS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INDUCTION; EPITHELIAL CELLS; ESOPHAGUS; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PROTEIN KINASES; RATS; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 22344453630     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/bgi052     Document Type: Article

References (77)

1. Jemal, A., Murray, T., Samuels, A., Ghafoor, A., Ward, E. and Thun, M.J. (2003) Cancer statistics for Hispanics. CA Cancer J. Clin., 53, 5-26.
2. Hecht, S.S. (2003) Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat. Rev. Cancer, 3, 733-734.
3. Pfeifer, G.P., Denissenko, M.F., Olivier, M., Tretyakova, N., Hecht, S.S. and Hainaut, P. (2002) Tobacco smoke carcinogens, DNA damage and p53 mutations in smoking-associated cancers. Oncogens, 21, 7435-7451.
4. Roth, M.J., Strickland, K.L., Wang, G.Q., Rothman, N., Greenberg, A. and Dawsey, S.M. (1998) High levels of carcinogenic polycyclic aromatic hydrocarbons present within food from Linxian, China may contribute to that region's high incidence of oesophageal cancer. Eur. J. Cancer, 34, 757-758.
5. Roth, M.J., Qiao, Y.-L., Rothman, N., Tangrea, J.A., Dawsey, S.M., Wang, G.-Q., Cho, S.-H., Kang, D., Taylor, P.R. and Strickland, P.T. (2001) High urine 1-hydroxypyrene glucuronide concentrations in Linxian, China, an area of high risk for squamous oesophageal cancer. Biomarkers, 6, 381-386.
6. van Gijssel, H.E., Divi, R.L., Olivero, O.A. et al. (2002) Semiquantitation of polycyclic aromatic hydrocarbon-DNA adducts in human esophagus by immunohistochemistry and the automated cellular imaging system. Cancer Epidemiol. Biomarkers Prev., 11, 1622-1629.
7. Toth, B. (1980) Tumorigenesis by benzo(a)pyrene administered intracolonically. Oncology, 37, 77-82.
8. Dunham, L.J., Sheets, R.H. and Morton, J.F. (1974) Proliferative lesions in cheek pouch and esophagus of hamsters treated with plants from Curacao, Netherlands Antilles. J. Natl Cancer Inst., 53, 1259-1269.
9. Culp, S.J., Gaylor, D.W., Sheldon, W.G., Goldstein, L.S. and Beland, F.A. (1998) A comparison of the tumors induced by coal tar and benzo[a] pyrene in a 2-year bioassay. Carcinogenesis, 19, 117-124.
10. Culp, S.J., Warbritton, A.R., Smith, B.A., Li, E.E. and Beland, F.A. (2000) DNA adduct measurements, cell proliferation and tumor mutation induction in relation to tumor formation in B6C3F1 mice fed coal tar or benzo[a]pyrene. Carcinogenesis, 21, 1433-1440.
11. Bostrom, C.E., Gerde, P., Hanberg, A., Jernstrom, B., Johansson, C., Kyrklund, T., Rannug, A., Tornqvist, M., Victorin, K. and Westerholm, R. (2002) Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ. Health Perspect., 110, 451-488.
12. Xu, W., Liu, L.Z., Loizidou, M., Ahmed, M. and Charles, I.G. (2002) The role of nitric oxide in cancer. Cell Res., 12, 311-320.
13. Puhakka, A., Kinnula, V., Napankangas, U., Saily, M., Koistinen, P., Paakko, P. and Soini, Y. (2003) High expression of nitric oxide synthases is a favorable prognostic sign in non-small cell lung carcinoma. APMIS, 111, 1137-1146.
14. Bing, R.J., Miyataka, M., Rich, K.A., Hanson, N., Wang, X., Slosser, H.D. and Shi, S.R. (2001) Nitric oxide, prostanoids, cyclooxygenase, and angiogenesis in colon and breast cancer. Clin. Cancer Res., 7, 3385-3392.
15. Kong, G., Kim, E.K., Kim, W.S., Lee, K.T., Lee, Y.W., Lee, J.K., Paik, S.W. and Rhee, J.C. (2002) Role of cyclooxygenase-2 and inducible nitric oxide synthase in pancreatic cancer. J. Gastroenterol. Hepatol., 17, 914-921.
16. Park, S.W., Lee, S.G., Song, S.H., Heo, D.S., Park, B.J., Lee, D.W., Kim, K.H. and Sung, M.W. (2003) The effect of nitric oxide on cyclooxygenase-2 (COX-2) overexpression in head and neck cancer cell lines. Int. J. Cancer, 107, 729-738.
17. Tanaka, H., Kijima, H., Tokunaga, T. et al. (1999) Frequent expression of inducible nitric oxide synthase in esophageal squamous cell carcinomas. Int. J. Oncol., 14, 1069-1073.
18. Wilson, K.T. (2002) Angiogenic markers, neovascularization and malignant deformation of Barrett's esophagus. Dis. Esophagus, 15, 16-21.
19. Wilson, K.T., Fu, S., Ramanujam, K.S. and Meltzer, S.J. (1998) Increased expression of inducible nitric oxide synthase and cyclooxygenase-2 in Barrett's esophagus and associated adenocarcinomas. Cancer Res., 58, 2929-2934.
20. Stoner, G.D., Babcock, M.S., McCorquodale, M.M, Gunning, W.T. III, Jamasbi, R., Budd, N. and Hukku, B. (1989) Comparative properties of untreated and N-nitrosobenzylmethylamine-transformed rat esophageal epithelial cells. In Vitro Cell. Dev. Biol., 25, 899-908.
21. Harvey, R.G. (1991) Polycyclic Aromatic Hydrocarbons: Chemistry and Carcinogenicity. Cambridge University Press, Cambridge, UK.
22. Pataki, J., Lee, H. and Harvey, R.G. (1983) Carcinogenic metabolites of 5-methylchrysene. Carcinogenesis, 4, 399-402.
23. Amin, S., Huie, K., Melikian, A.A., Leszczynska, J.M. and Hecht, S.S. (1985) Comparative metabolic activation in mouse skin of the weak carcinogen 6-methylchrysene and the strong carcinogen 5-methylchrysene. Cancer Res., 45, 6406-6442.
24. Verma, I.M. and Stevenson, J. (1997) IkappaB kinase: beginning, not the end. Proc. Natl Acad. Sci. USA, 94, 11758-11760.
25. Cheshire, J.L. and Baldwin, A.S. Jr (1997) Synergistic activation of NF-kappaB by tumor necrosis factor alpha and gamma interferon via enhanced I kappaB alpha degradation and de novo I kappaBbeta degradation. Mol. Cell. Biol., 17, 6746-6754.
26. Nakano, H., Shindo, M., Sakon, S., Nishinaka, S., Mihara, M., Yagita, H. and Okumura, K. (1998) Differential regulation of IkappaB kinase alpha and beta by two upstream kinases, NF-kappaB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1. Proc. Natl Acad. Sci. USA, 95, 3537-3542.
27. Huang, Y., Davidson, G., Li, J., Yan, Y., Chen, F., Costa, M., Chen, L.C. and Huang, C. (2002) Activation of NFκB and not AP-1 in cellular response to nickel compounds. Environ. Health Perspect., 110(Suppl. 5), 835-839.
28. Robbins, D.J., Zhen, E., Owaki, H., Vanderbilt, C.A., Ebert, D., Geppert, T.D. and Cobb, M.H. (1993) Regulation and properties of extracellular signal-regulated protein kinases 1 and 2 in vitro. J. Biol. Chem., 268, 5097-5106.
29. Huang, C., Ma, W.-Y. and Dong, Z. (1999) The extracellular-signal- regulated protein kinases (Erks) are required for UV-induced AP-1 activation. Oncogene, 18, 2828-2835.
30. 2 promoter. Proc. Natl Acad. Sci. USA, 93, 1054-1059.
31. Surh, Y.J., Chun, K.S., Cha, H.H., Han, S.S., Keum, Y.S., Park, K.K. and Lee, S.S. (2001) Molecular mechanisms underlying chemopreventive activities of anti-inflammatory phytochemicals: down-regulation of COX-2 and iNOS through suppression of NF-κB activation. Mutat. Res., 480-481, 243-268.
32. Li, J., Chen, H., Tang, S., Shi, X., Amin, S., Desai, D., Costa, M. and Huang, C. (2004) PI-3K and Akt are mediators of AP-1 induction by 5-methylchrysene-1, 2-diol-3, 4-epoxide (5-MCDE) in mouse epidermal C141 cells. J. Cell Biol., 165, 77-86.
33. s6k-independent pathway to induce HIF transactivation and Cap43 expression in mouse epidermal C141 cells. Cancer Res., 64, 94-101.
34. Li, J., Tang, S., Liu, B., Shi, X. and Huang, C. (2004) A critical role of PI-3K/Akt/JNKs pathway in benzo(a)pyrene diol-epoxide (BPDE)-induced AP-1 transactivation in mouse epidermal C141 cells. Oncogene, 23, 3932-3944.
35. Li, J., Ding, M., Leonard, S.S., Shi, X., Costa, M., Castranova, V., Vallyathan, V. and Huang, C. (2002) Differential role of hydrogen peroxide in UV-induced signal transduction. Mol. Cell. Biochem., 234-235, 81-90.
36. Xie, Q.W., Kashiwabara, Y. and Nathan, C. (1994) Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem., 269, 4705-4708.
37. Lee, J.K., Choi, S.S., Won, J.S. and Suh, H.W. (2003) The regulation of inducible nitric oxide synthase gene expression induced by lipopolysaccharide and tumor necrosis factor-α in C6 cells: involvement of AP-1 and NF-κB. Life Sci., 73, 595-609.
38. IARC (1983) WHO polynuclear aromatic compounds, part 1, chemicals, environmental and experimental data. In Evaluation of the Carcinogenic Risk of Chemicals to Humans. IARC Monographs, Vol. 32, Lyon, pp. 1-477.
39. IARC (1984) WHO polynuclear aromatic compounds, part 3, chemicals, environmental and experimental data. In: Evaluation of the Carcinogenic Risk of Chemicals to Humans. IARC Monographs, Vol. 34, Lyon, pp. 37-64.
40. Juliane, H., Burkhard, K. and Wolfgang, D. (2000) Biomonitoring of environmental polycyclic aromatic hydrocarbon exposure by simultaneous measurement of urinary phenathrene, pyrene and bezo[a]pyrene hydroxides. J. Chromatogr. B, 739, 225-229.
41. Jürgen, G. and Jürgen, A. (2000) High-performance liquid chromatographic method with fluorescence detection for the determination of 3-hydroxybenzo[a]pyrene and 3-hydroxybenz[a]anthracence in the urine of polycyclic aromatic hydrocarbon-exposed workers. J. Chromatogr. B, 738, 47-55.
42. Matthias, S., Gottfried, W., Stefan, A., Antonius, K., Reinhard, N. and Dietmar, K. (2001) Mornitoring polycyclic aromatic hydrocarbon metabolites in human urine: extraction and purification with a sol-gel glass immunosorbent. Anal. Chem., 73, 5669-5676.
43. Brandt, H.C. and Watson, W.P. (2003) Monitoring human occupational and environmental exposure to polycyclic aromatic compounds. Ann. Occup. Hyg., 47, 349-378.
44. Hecht, S.S. (2002) Human urinary carcinogen metabolites: biomarkers for investigating tobacco and cancer. Carcinogenesis, 23, 907-922.
45. Panalaks, T. (1976) Determination and identification of polycyclic aromatic hydrocarbons in smoked and charcoal-broiled food products by high pressure liquid chromatography and gas chromatography. J. Environ. Sci. Health B, 11, 299-315.
46. Hattemer-Frey, H.A. and Travis, C.C. (1991) Benzo-a-pyrene: environmental partitioning and human exposure. Toxicol. Ind. Health., 7, 141-157.
47. Doll, R. and Peto, R.J. (1978) Cigarette smoking and bronchial carcinoma: dose and time relationships among regular smokers and lifelong non-smokers. J. Epidemiol. Community Health, 32, 303-13.
48. Jyonouchi, H., Sun, S., Iijima, K., Wang, M. and Hecht, S.S. (1999) Effects of anti-7, 8-dihydroxy-9, 10-epoxy-7, 8, 9, 10-tetrahydrobenzo[a]pyrene on human small airway epithelial cells and the protective effects of myoinositol. Carcinogenesis, 20, 139-145.
49. Jeffy, B.D., Chirnomas, R.B., Chen, E.J., Gudas, J.M. and Romagnolo, D.F. (2002) Activation of the aromatic hydrocarbon receptor pathway is not sufficient for transcriptional repression of BRCA-1: requirements for metabolism of benzo[a]pyrene to 7r, 8t-dihydroxy-9t, 10-epoxy-7, 8, 9, 10-tetrahydrobenzo[a]pyrene. Cancer Res., 62, 113-21.
50. Yoshii, S., Tanaka, M., Otsuki, Y., Fujiyama, T., Kataoka, H., Arai, H., Hanai, H. and Sugimura, H. (2001) Involvement of alpha-PAK-interacting exchange factor in the PAK 1-c-Jun NH(2)-terminal kinase 1 activation and apoptosis induced by benzo[a]pyrene. Mol. Cell. Biol., 21, 6796-807.
51. Mendes, A.F., Caramona, M.M., Carvalho, A.P. and Lopes, M.C. (2003) Differential roles of hydrogen peroxide and Superoxide in mediating IL-1-induced NF-kappa B activation and iNOS expression in bovine articular chondrocytes. J. Cell. Biochem., 88, 783-793.
52. Yu, D., Berlin, J.A., Penning, T.M. and Field, J. (2002) Reactive oxygen species generated by PAH o-quinones cause change-in-function mutations in p53. Chem. Res. Toxicol., 15, 832-842.
53. Inoue, S. and Kawanishi, S. (1995) Oxidative DNA damage induced by simultaneous generation of nitric oxide and superoxide. FEBS Lett., 371, 86-88.
54. Zhang, J., Dawson, V.L., Dawson, T.M. and Snyder, S.H. (1994) Nitric oxide activation of poly (ADP-ribose) synthetase in neurotoxicity. Science, 263, 687-689.
55. Robertson, F.M., Long, B.W., Tober, K.L., Ross, M.S. and Oberyszyn, T.M. (1996) Gene expression and cellular sources of inducible nitric oxide synthase during tumor promotion. Carcinogenesis, 17, 2053-2059.
56. Mordan, L.J., Burnett, T.S., Zhang, L.X., Tom, J. and Cooney, R.V. (1993) Inhibitors of endogenous nitrogen oxide formation block the promotion of neoplastic transformation in C3H 10T1/2 fibroblasts. Carcinogenesis, 14, 1555-1559.
57. Konopka, T.E., Barker, J.E., Bamford, T.L., Guida, E., Anderson, R.L. and Stewart, A.G. (2001) Nitric oxide synthase II gene disruption: implications for tumor growth and vascular endothelial growth factor production. Cancer Res., 61, 3182-3187.
58. Kisley, L.R., Barrett, B.S., Bauer, A.-K., Dwyer-Nield, L.D., Barthel, B., Meyer, A.-M., Thompson, D.C. and Malkinson, A.M. (2002) Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res., 62, 6850-6856.
59. Rao, C.V., Indranie, C., Simi, B., Manning, P.T., Connor, J. and Reddy, B.S. (2002) Chemopreventive properties of a selective inducible nitric oxide synthase inhibitor in colon carcinogenesis, administered alone or in combination with celecoxib, a selective cyclooxygenase-2 inhibitor. Cancer Res., 62, 165-170.
60. Ahn, B. and Ohshima, H. (2001) Suppression of intestinal polyposis in Apc(Min/+) mice by inhibiting nitric oxide production. Cancer Res., 61, 8357-8360.
61. Wei, J., Guo, H., Gao, C. and Kuo, P.C. (2004) Peroxide-mediated chromatin remodeling of an NF-κB site in the murine iNOS promoter. Biochem. J., 377, 809-818.
62. Han, I.O., Kim, H.S., Kim, H.C., Joe, E.H. and Kim, W.K. (2003) Synergistic expression of inducible nitric oxide synthase by phorbol ester and interferon-γ is mediated through NF-κB and ERK in microglial cells. J. Neurosci. Res., 73, 659-669.
63. Martin, E., Nathan, C. and Xie, Q.W. (1994) Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J. Exp. Med., 180, 977-984.
64. Tedeschi, E., Menegazzi, M., Margotto, D., Suzuki, H., Forstermann, U. and Kleinert, H. (2003) Anti-inflammatory actions of St. John's wort: inhibition of human inducible nitric-oxide synthase expression by down-regulating signal transducer and activator of transcription-1α (STAT-1α) activation. J. Pharmacol. Exp. Ther., 307, 254-261.
65. Bhat, N.R., Feinstein, D.L., Shen, Q. and Bhat, A.N. (2002) p38 MAPK-mediated transcriptional activation of inducible nitric-oxide synthase in glial cells. J. Biol. Chem., 277, 29584-29592.
66. Eberhardt, W., Pluss, C., Hummel, R. and Pfeilschifter, J. (1998) Molecular mechanisms of inducible nitric oxide synthase gene expression by IL-1β and cAMP in rat mesangial cells. J. Immunol., 160, 4961-4969.
67. Asp12 cDNA markedly elevates IL-1β- and lipopolysaccharide-mediated inducible nitric oxide synthase expression in rat intestinal epithelial cells. Oncogene, 22, 7667-7676.
68. Bhat, N.R., Zhang, P., Lee, J.C. and Hogan, E.L. (1998) Extracellular signal-regulated kinase and p38 subgroups of raitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures. J. Neurosci., 18, 1633-1641.
69. Lahti, A., Jalonen, U., Kankaanranta, H. and Moilanen, E. (2003) c-Jun NH2-terminal kinase inhibitor anthra( 1, 9-cd)pyrazol-6(2H)-one reduces inducible nitric-oxide synthase expression by destabilizing mRNA in activated macrophages. Mol. Pharmacol., 64, 308-315.
70. Li, J.J., Westergaard, C., Ghosh, P. and Colburn, N.H. (1997) Inhibitors of both nuclear factor-κB and activator protein-1 activation block the neoplastic transformation response. Cancer Res., 57, 3569-3576.
71. Luque, I. and Gelinas, C. ( 1997) Rel/NF-κB and IκB factors in oncogenesis. Semin. Cancer Biol., 8, 103-111.
72. Taylor, B.S., de Vera, M.E., Ganster, R.W., Wang, Q., Shapiro, R.A., Morris, S.M. Jr, Billiar, T.R. and Geller, D.A. (1998) Multiple NF-kappaB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J. Biol. Chem., 273, 15148-15156.
73. Banerjee, R., Caruccio, L., Zhang, Y.J., McKercher, S. and Santella, R.M. (2000) Effects of carcinogen-induced transcription factors on the activation of hepatitis B virus expression in human hepatoblastoma HepG2 cells and its implication on hepatocellular carcinomas. Hepatology, 32, 367-374.
74. Jiang, B., Xu, S., Hou, X., Pimentel, D.R., Brecher, P. and Cohen, R.A. (2004) Temporal control of NF-κB activation by ERK differentially regulates interleukin-1β-induced gene expression. J. Biol. Chem., 279, 1323-1329.
75. Maiuri, M.C., De Stefano, D., Mele, G., Iovine, B., Bevilacqua, M.A., Greco, L., Auricchio, S. and Carnuccio, R. (2003) Gliadin increases iNOS gene expression in interferon-gamma-stimulated RAW 264.7 cells through a mechanism involving NF-κB. Naunyn Schmiedebergs Arch Pharmacol., 368, 63-71.
76. Huang, C., Huang, Y., Li, J., Hu, W., Aziz, R., Tang, M.S., Sun, N., Cassady, J. and Stoner, G.D. (2002) Inhibition of BPDE-induced transactivation of AP-1 and NFκB by black raspberry extracts. Cancer Res., 62, 6857-6863.
77. Li, J., Chen, H., Tang, S., Shi, X., Amin, S., Desai, D., Costa, M. and Huang, C. (2004) PI-3K and Akt are mediators of AP-1 induction by 5-methylchrysene-1, 2-diol-3, 4-epoxide (5-MCDE) in mouse epidermal C141 cells. J. Cell. Biol., 165, 77-86.