Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer

Clinical Cancer Research

Volumn 16, Issue 2, 2010, Pages 509-520

  Du, Juan ^a   Martin, Sean M ^a   Levine, Mark ^d   Wagner, Brett A ^a   Buettner, Garry R ^a,b   Wang, Sih Han ^a   Taghiyev, Agshin F ^a   Du, Changbin ^a   Knudson, Charles M ^a   Cullen, Joseph J ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

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

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ASCORBIC ACID; CATALASE; HYDROGEN PEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CANCER INHIBITION; CANCER SURVIVAL; CELL DEATH; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL;

ADENOCARCINOMA; ANIMALS; ASCORBIC ACID; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; CYTOTOXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; HYDROGEN PEROXIDE; MICE; MICE, NUDE; OXIDATIVE STRESS; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 74549157124     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-09-1713     Document Type: Article

References (46)

1. Jemal A, Siegel R, Ward E, et al. Cancer Statistics, 2008. CA Cancer J Clin 2008;58:71-96.
2. Bramhall SR, Allum WH, Jones AG, et al. Treatment and survival in 13,560 patients with pancreatic cancer, and incidence of the disease, in the epidemiological study. Br J Surg 1995;82:111-5.
3. Yeo CJ, Cameron JL. Pancreatic cancer. Curr Probl Surg 1999;36: 59-152.
4. White R, Lee C, Anscher M, et al. Preoperative chemoradiation for patients with locally advanced Adenocarcinoma of the pancreas. Ann Surg Oncol 1999;6:38-45.
5. Chen Q, Espey MG, Krishna MC, et al. Pharmacologic ascorbic acid concentrations selectively kill cancer cells: action as a pro-drug to deliver hydrogen peroxide to tissues. Proc Natl Acad Sci U S A 2005;102:13604-9.
6. Chen Q, Espey MG, Sun Y, et al. Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo. Proc Natl Acad Sci U S A 2007;104:8749-54.
7. Lee YJ, Schacter EJ. Oxidative stress inhibits apoptosis in human lymphoma cells. J Biol Chem 1999;274:19792-8.
8. Shraufshtatter IU, Hinshaw DB, Hyslop PA, Spragg RG, Cochrane CG. Glutathione cycle activity and pyridine nucleotide levels in oxidant-induced injury of cells. J Clin Invest 1985;76:1131-9.
9. Lee YJ, Galoforo SS, Berns CM, et al. Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J Biol Chem 1998;273:5294-9.
10. Hyslop PA, Hinshaw DB, Halsey WA, et al. Mechanisms of oxidant-mediated cell injury. The glycolytic and mitochondrial pathways of ADP phosphorylation are major intracellular targets inactivated by hydrogen peroxide. J Biol Chem 1988;263:1665-75.
11. Comelli M, Di Pancrazio F, Mavelli I. Apoptosis is induced by decline of mitochondrial ATP synthesis in erythroleukemia cells. Free Radic Biol Med 2003;34:1190-9.
12. 2 mediates glucose deprivation-induced cytotoxicity and oxidative stress in human cancer cells. J Biol Chem 2005;280: 4254-63.
13. 2 in vitro and in vivo and reduce menadione-induced DNA injury and cytotoxicity. Am J Physiol 1995;268: C227-36.
14. Ohtani S, Iwamaru A, Deng W, et al. Tumor suppressor 101F6 and ascorbate synergistically and selectively inhibit non-small cell lung cancer growth by caspase-independent apoptosis and autophagy. Cancer Res 2007;67:6293-303.
15. Daido S, Yamamoto A, Fujiwara K, et al. Inhibition of the DNAdependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing autophagy. Cancer Res 2005;65:4368-75.
16. Takeuchi H, Kondo Y, Fujiwara K, et al. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylionistol 3-kinase/protein kinase B inhibition. Cancer Res 2005;65:3336-46.
17. Shao Y, Gao Z, Marks PA, et al. Apoptotic and autophagic cell death induced by histone deacetylase inhibition. Proc Natl Acad Sci U S A 2004;52:18030-65.
18. Qian J, Niu J, Li M, Chiao PJ, Tsao MS. In vitro modeling of human pancreatic duct epithelial cell transformation defines gene expression changes induced by K-ras oncogenic activation in pancreatic carcinogenesis. Cancer Res 2005:5045-53.
19. Lewis A, Ough M, Du J, Tsao MS, Oberley LW, Cullen JJ. Targeting NAD(P)H:quinone oxidoreductase (NQO1) in pancreatic cancer. Mol Carcinog 2005;43:215-24.
20. Du J, Daniels DH, Asbury CA, et al. Mitochondrial production of reactive oxygen species mediate dicumarol-induced cytotoxicity in cancer cells. J Biol Chem 2006;281:37416-26.
21. Buettner GR. In the absence of catalytic metals, ascorbate does not autoxidize at pH 7: ascorbate as a test for catalytic metals. J Biochem Biophys Methods 1988;16:27-40.
22. Coleman MC, Asbury C, Daniels DH, et al. Inhibition of glucose metabolism in pancreatic cancer induces cytotoxicity via metabolic oxidative stress. Free Radic Biol Med 2008;44:322-32.
23. Clement MV, Ramalingam R, Long LH, Halliwell B. The in vitro cytotoxicity of ascorbate depends on the culture medium used to perform the assay and involves hydrogen peroxide. Antioxid Redox Signal 2001;3:157-63.
24. Zwacka RM, Dudus L, Epperly MW, Greenburger JS, Engelhardt JF. Redox gene therapy protects human IB-3 lung epithelial cells against ionizing radiation-induced apoptosis. Hum Gene Ther 1998;9:1381-6.
25. Bai J, Rodriguez AM, Melendez JA, Cederbaum AI. Overexpression of catalase in cytosolic or mitochondrial compartment protects HepG2 cells against oxidative injury. J Biol Chem 1999;274:26217-24.
26. Budanov AV, Sablina AA, Feinstein E, Koonin EV, Chumakov PM. Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 2004;304:596-600.
27. Padayatty SJ, Sun H, Wang Y, et al. Vitamin C pharmacokinetics: implications for oral and intravenous use. Ann Intern Med 2004; 140:533-7.
28. Hoffer LJ, Levine M, Assouline S, et al. Phase 1 clinical trial of i.v. ascorbic acid in advanced malignancy. Ann Oncol 2008;19:1969-74.
29. Cloos C, Daniels DH, Kalen A, et al. Mitochondrial DNA depletion induces radioresistance by suppressing G2-checkpoint activation in human pancreatic cancer cells. Radiat Res 2009;171:581-7.
30. Jagtap P, Szabo C. Poly(ADP-ribose) polymerase and the therapeutic effects of it inhibitors. Nat Rev Drug Discov 2005;4:421-40.
31. Du J, Tsao MS, Oberley LW, Cullen JJ. K-ras oncogene increases reactive oxygen species (ROS): Mechanisms involved in regulating pancreatic cancer cell growth. Free Radic Biol Med 2007;43:S53.
32. Huang Q, Wu YT, Tan HL, Ong CN, Shen HM. A novel function of poly(ADP-ribose) polymerase-1 in modulation of autophagy and necrosis under oxidative stress. Cell Death Differ 2008;16:264-77.
33. McCormick WJ. Cancer: the preconditioning factor in pathogenesis. Arch Pediatr 1954;71:313-22.
34. McCormick WJ. Cancer: a collagen disease, secondary to a nutritional deficiency? Arch Pediatr 1959;76:166-71.
35. Cameron E, Rotman D. Ascorbic acid, cell proliferation, and cancer. Lancet 1972;299:542.
36. Cameron E, Pauling L. Ascorbic acid and the glycosaminoglycans. An orthomolecular approach to cancer and other diseases. Oncology 1973;27:181-92.
37. Cameron E, Pauling L. Supplemental ascorbate in the supportive treatment of cancer: prolongation of survival times in terminal human cancer. Proc Natl Acad Sci U S A 1976;73:3685-9.
38. Cameron E, Campbell A. The orthomolecular treatment of cancer. II Clinical trial of high-does ascorbic acid supplements in advanced human cancer. Chem Biol Interact 1974;9:285-315.
39. Cameron E, Pauling L. Supplemental ascorbate in the supportive treatment of cancer: reevaluation of prolongation of survival times in terminal human cancer. Proc Natl Acad Sci U S A 1978;75: 4538-42.
40. Creagan ET, Moertel CG, O'Fallon JR, et al. Failure of high-dose vitamin C (ascorbic acid) therapy to benefit patients with advanced cancer. A controlled trial. N Engl J Med 1979;301:687-90.
41. Moertel CG, Flemin TR, Creagan ET, Rubin J, O'Connell MJ, Ames MM. High-dose vitamin C versus placebo in the treatment of patients with advanced cancer who have had no prior chemotherapy. A randomized double-blind comparison. N Engl J Med 1985;312: 137-41.
42. Levine M, Conry-Cantilena C, Wang Y, et al. Vitamin C Pharmacokinetics in healthy volunteers: evidence for a recommended dietary allowance. Proc Natl Acad Sci U S A 1996;93:3704-9.
43. Graumlich JF, Ludden TM, Conry-Cantilena C, Cantilena LR, Jr., Wang Y, Levine M. Phamacokinetic model for ascorbic acid in healthy male volunteers during depletion and repletion. Pharm Res 1997;14:1133-9.
44. Verrax J, Calderon PB. Pharmacologic concentrations of ascorbate are achieved by parenteral administration and exhibit antitumoral effects. Free Radic Biol Med 2009;47:32-40.
45. Chen Y, McMillan-Ward E, Kong J, Israels SJ, Gibson SB. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008;15:171-82.
46. Wu YT, Tan HL, Huang Q, et al. Autophagy plays a protective role during zVAD-induced necrotic cell death. Autophagy 2008;4: 457-66.