Dicumarol inhibition of NADPH:quinone oxidoreductase induces growth inhibition of pancreatic cancer via a superoxide-mediated mechanism

Cancer Research

Volumn 63, Issue 17, 2003, Pages 5513-5520

  Cullen, Joseph J ^a,b,d   Hinkhouse, Marilyn M ^d   Grady, Matthew ^c   Gaut, Andrew W ^a   Liu, Jingru ^a   Zhang, Yu Ping ^a   Weydert, Christine J Darby ^a   Domann, Frederick E ^a,b   Oberley, Larry W ^a,b  

^a Department of Surgery ^*  (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; COMPLEMENTARY DNA; CYTOCHROME P450 REDUCTASE; DICOUMAROL; FLAVOPROTEIN; HYDROQUINONE DERIVATIVE; MANGANESE SUPEROXIDE DISMUTASE; OXIDOREDUCTASE; QUINONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SUPEROXIDE;

ARTICLE; CANCER CELL; CANCER GROWTH; CATALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTRON; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPOTHESIS; IN VITRO STUDY; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REDUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOCARCINOMA; BLOTTING, WESTERN; CELL DIVISION; DICUMAROL; ENZYME INHIBITORS; HUMANS; NAD(P)H DEHYDROGENASE (QUINONE); PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SUPEROXIDE DISMUTASE; SUPEROXIDES; UP-REGULATION;

EID: 0141592795     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (40)

1. Jemal, A., Thomas, A., Murray, T., Thun, M. Cancer statistics, 2002. CA Cancer J. Clin., 52: 23-47, 2002.
2. Bramhall, S. R., Allum, W. H., Jones, A. G., Allwood, A., Cummins, C., Neoptolemos, J. P. Treatment and survival in 13,560 patients with pancreatic cancer, and incidence of the disease, in the epidemiological study. Br. J. Surg., 82: 111-115, 1995.
3. Yeo, C. J., Cameron, J. L. Pancreatic cancer. Cur. Probl. Surg., 36: 59-152, 1999.
4. Burris, H. A., Moore, M. J., Andersen, J., Greem, M. R., Rothenber, M. I., Modiano, M. R., Cripps, M. C., Portenoy, R. K., Storniolo, A. M., Tarassoff, P., Nelson, R., Dorr, F. A., Stephens, C. D., and von Hoff, D. D. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreatic cancer: a randomized trial. J. Clin. Oncol., 15: 2403-2413, 1997.
5. Jessup, J. M., Steele, G., Mayer, R. J., et al. Neoadjuvant therapy for unresectable pancreatic adenocarcinoma. Arch. Surg., 128: 559-564, 1993.
6. White, R., Lee, C., Anscher, M., et al. Preoperative chemoradiation for patients with locally advanced sdenocarcinoma of the pancreas. Ann. Surg. Oncol., 6: 38-45, 1999.
7. Ernster L. DT-diaphorase. Methods Enzymol., 10: 309-317, 1967.
8. Sun, I. L., Sun, E. E., Crane, F. L., Morre, D. J., Lindgren, A., and Low, H. Requirement for coenzyme Q in plasma membrane electron transport. Proc. Natl. Acad. Sci. USA, 89: 11126-11130, 1992.
9. Beyer, R. E., Segura-Aguilar, J., DiBernardo, S., Cavazzoni, M., Fato, R., Fiorentini, D., Galli, M., Setti, M., Landi, L., and Lenaz, G. The role of DT-diaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems. Proc. Natl. Acad. Sci. USA, 93: 2528-2532, 1996.
10. Siegel, D., Bolton, E. M., Burr, J. A., Liebler, D. C., and Ross, D. The reduction of α-tocopherolquinone by human NAD(P)H:quinone oxidoreductase: the role of α-tocopherol hydroquinone as a cellular antioxidant. Mol. Pharmacol., 52: 300-305, 1997.
11. Benson, A. M., Hunkler, M. G., and Talalay, P. Increase of NAD(P)H:quinone reductase by dietary antioxidants: possible role in protection against carcinogenesis and toxicity. Proc. Nat. Acad. Sci. USA., 77: 5216-5220, 1980.
12. Talalay, P., DeLong, M. G., and Prochaska, H. J. Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis. Proc. Natl. Acad. Sci. USA, 85: 8261-8265, 1988.
13. Trush, M. A., Twerdok, L. E., Rembish, S. J., Zhu, H., and Li, Y. B. Analysis of target cell susceptibility as a basis for the development of a chemoprotective strategy against benzene-induced hematotoxicities. Environ. Health Perspect., 104(Suppl. 6): 1227-1234, 1996.
14. Chesis, P. L., Levin, D. E., Smith, M. T., Ernster, L., and Ames, B. N. Mutagenicity of quinines: pathways of metabolic activation and detoxification. Proc. Nat. Acad. Sci. USA., 81: 1696-1700, 1984.
15. Lind, C., Hochstein, P., and Ernster, L. DT-Diaphorase as a quinone reductase: a cellular control device against semiquinone and superoxide radical formation. Arch. Biochem. Biophys., 216: 178-185, 1982.
16. Thor, H., Smith, M. T., Hartzell, P., Bellomo, G., Jewell, S. A., and Orrenius, S. The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes. A study of the implication of oxidative stress in intact cells. J. Biol. Chem., 257: 12419-12425, 1982.
17. Siegel, D., and Ross, D. Immunodetection of NAD(P)H:quinone oxidoreductase 1 (NQOI) in human tissues. Free Rad. Biol. Med., 29: 246-253, 2000.
18. Malkinson, A. M., Siegel, D., Forrest, G. L., Gazdar, A. F., Oie, H. K., Chan, D. C., Bunn, P. A., Mabry, M., Dykes, D. J., Harrsion, S. D., and Ross, D. Elevated DT-diaphorase activity and messenger RNA content in human non-small cell lung carcinoma: relationship to the response of lung tumor xenografts to mitomycin C. Cancer Res., 52: 4752-4757, 1992.
19. Logsdon, C. D., Simeone, D. M., Binkley, C., Arumugam, T., Greenson, J. K., Giordano, T. J., Misek, D. E., and Hanash, S. Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer. Cancer Res., 63: 2649-2657, 2003.
20. O'Donnell, V. B., Smith, G. C. M., and Jones, O. T. G. Involvement of phenyl radicals in iodonium compound inhibition of flavoenzymes. Mol. Pharmacol., 46: 778-786, 1994.
21. Edwards, Y. H., Potter, J., and Hopkinson, D. A. Human FAD-dependent NADPH diaphorase. Biochem. J., 187: 429-436, 1980.
22. 1 (DT-diaphorase) expression in normal and tumor tissues. Cancer Metastasis Rev., 12: 103-117, 1993.
23. Li, J. J., Oberley, L. W., St. Clair, D. K., Ridnour, L. A., and Oberley, T. D. Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene, 10: 1989-2000, 1995.
24. 1 (DT-diaphorase) messenger RNA lacking the putative quinone substrate binding site is present in human normal and tumor tissues. Cancer Res., 55: 2542-2547, 1995.
25. Fitzsimmons, S. A., Workman, P., Grever, M., Paull, K., Camalier, R., and Lewis, A. D. Reductase enzyme expression across the National Cancer Institute tumor cell line panel: correlation with sensitivity to mitomycin C and EO9. J. Natl. Cancer Inst., 88: 259-269, 1996.
26. Cullen, J. J., Weydert, C. J., Hinkhouse, M. M., Domann, F. E., Spitz, D. R., and Oberley, L. W. The role of manganese superoxide dismutase in the growth of pancreatic adenocarcinoma. Cancer Res., 63: 1297-1303, 2003.
27. Cullen, J. J., Mitros, F. A., and Oberley, L. W. Expression of antioxidant enzymes in diseases of the human pancreas: another link between chronic pancreatitis and pancreatic cancer. Pancreas, 26: 23-27, 2003.
28. Oberley, T. D., Oberley, L. W., Slattery, A. F., Lauchner. L. J., and Elwell, J. H. Immunohistochemical localization of antioxidant enzymes in adult Syrian hamster tissues and during kidney development. Am. J. Pathol., 137: 199-214, 1990.
29. Misra, V., Klamut, H. J., and Rauth, A. M. Expression of the prodrug-activiting enzyme DT-diaphorase via Ad5 delivery to human colon carcinoma cells in vitro. Cancer Gene Ther., 9: 209-217, 2002.
30. o cells. J. Biol. Chem., 269: 30097-30100, 1994.
31. Brar, S. S., Kennedy, T. P., Whorton, A. R., Sturrock, A. B., Huecksteadt, T. P., Ghio, A. J., and Hoidal, J. R. Reactive oxygen species from NAD(P)H: quinone oxidoreductase constitutively activate NF-κ B in malignant melanoma cells. Am. J. Physiol., 280: C659-C676, 2001.
32. Brar, D. D., Kennedy, T. P., Whorton, A. R., Murphy, T. M., Chitano, P., and Hoidal, J. R. Requirement for reactive oxygen species in serum-induced and platelet-derived growth factor-induced growth of airway smooth muscle. J. Bio. Chem., 274: 20017-20026, 1999.
33. Hollander, P., and Ernster, L. Studies on the reaction mechanism of DT diaphorase. Action of dead-end inhibitors and effects of phospholipids. Arch. Biochem. Biophys., 169: 560-567, 1975.
34. Josoda, S., Nakamura, W., and Hayashi, K. Properties and reaction mechanisms of DT diaphorase from rat liver. J. Biol. Chem., 249: 6416-6423, 1974.
35. Ross, D., Siegel, D., Beall, H., Prakash, A. S., Mulcahy, R. T., and Gibson, N. W. DT-diaphorase in activation and detoxification of quinones. Bioreductive activation of mitomycin C. Cancer Metastasis Rev., 12: 83-101, 1993.
36. Hulse, M., Feldman, S., and Bruckner, J. V. Effect of blood sampling schedules on protein drug binding in the rat. J. Pharmacol. Exp. Ther., 218: 416-420, 1981.
37. Preusch, P. C., Siegel, D., Givson, N. W., and Ross, D. A note on the inhibition of DT-diaphorase by dicoumarol. Free Radic. Biol. Med., 11: 77-80, 1991.
38. Li, N., Ragheb, K., Lawler, G., Sturgis, J., Rajwa, B., Melendez, J. A., and Robinson, J. P. DPI induces mitochondrial superoxide-mediated apoptosis Free Radic. Biol. Med. 34: 465-477, 2003.
39. Edlund, C., Elhammer, A., and Dallncr, G. Distribution of newly synthesized DT-diaphorase in rat liver. Biosci. Rep., 2: 861-865, 1982.
40. Winski, S. L., Koutalos, Y., Bentley, D. L., and Ross. D. Subcellular localization of NAD(P)H:quinone oxidoreductase 1 in human cancer cells. Cancer Res., 62: 1420-1424, 2002.