Pharmacological concentrations of ascorbate radiosensitize glioblastoma multiforme primary cells by increasing oxidative DNA damage and inhibiting G2/M arrest

Free Radical Biology and Medicine

Volumn 52, Issue 8, 2012, Pages 1486-1493

  Herst, Patries M ^a,b   Broadley, Kate W R ^a   Harper, Jacquie L ^a   McConnell, Melanie J ^a  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

breaks, cell cycle arrest, apoptosis autophagy; Free radicals; Glioblastoma multiforme; Pharmacological ascorbate; Radiosensitization, double stranded DNA

Indexed keywords

3 METHYLADENINE; ASCORBIC ACID; CESIUM 137; HISTONE H2AX; HYDROGEN PEROXIDE; LIPOCORTIN 5; PROPIDIUM IODIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; ASTROCYTOMA CELL; AUTOPHAGY; CANCER CELL; CELL CYCLE PROGRESSION; CELL DEATH; CELL ISOLATION; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; FLUORESCENCE ACTIVATED CELL SORTING; G2 PHASE CELL CYCLE CHECKPOINT; GAMMA IRRADIATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; RADIOSENSITIZATION;

ANIMALS; ASCORBIC ACID; BRAIN NEOPLASMS; CELL DIVISION; CELL LINE, TUMOR; DNA DAMAGE; FLOW CYTOMETRY; G2 PHASE; GLIOBLASTOMA; MICE; OXIDATIVE STRESS; RADIATION-SENSITIZING AGENTS;

EID: 84859002998     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.01.021     Document Type: Article

References (53)

1. Karacetin, D.; Okten, B.; Yalcin, B.; Incekara, O. Concomitant temozolomide and radiotherapy versus radiotherapy alone for treatment of newly diagnosed glioblastoma multiforme. J. BUON 16:133-137; 2011.
2. Stupp, R.; Hegi, M. E.; Mason, W. P., et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10:459-466; 2009.
3. Facchino, S.; Abdouh, M.; Chatoo, W.; Bernier, G. BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J. Neurosci. 30:10096-10111; 2010.
4. Li, Z.; Xia, L.; Lee, L. M., et al. Effector genes altered in MCF-7 human breast cancer cells after exposure to fractionated ionizing radiation. Radiat. Res. 155:543-553; 2001.
5. Guo, G.; Yan-Sanders, Y.; Lyn-Cook, B. D., et al. Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses. Mol. Cell. Biol. 23:2362-2378; 2003.
6. 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. 73:3685-3689; 1976.
7. 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. 75:4538-4542; 1978.
8. Cameron, E.; Campbell, A. The orthomolecular treatment of cancer. II. Clinical trial of high-dose ascorbic acid supplements in advanced human cancer. Chem. Biol. Interact. 9:285-315; 1974.
9. Padayatty, S. J.; Riordan, H. D.; Hewitt, S. M.; Katz, A.; Hoffer, L. J.; Levine, M. Intravenously administered vitamin C as cancer therapy: three cases. Can. Med. Assoc. J. 174:937-943; 2006.
10. Moertel, C. G.; Fleming, T. R.; Creagan, E. T.; Rubin, J.; O'Connell, M. J.; Ames, M. M. 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. 312:137-141; 1985.
11. Creagan, E. T.; Moertel, C. G.; O'Fallon, J. R., et al. Failure of high-dose vitamin C (ascorbic acid) therapy to benefit patients with advanced cancer: a controlled trial. N. Engl. J. Med. 301:687-690; 1979.
12. Hoffer, L. J.; Levine, M.; Assouline, S., et al. Phase I clinical trial of i.v. ascorbic acid in advanced malignancy. Ann. Oncol. 19:1969-1974; 2008.
13. Riordan, H. D.; Casciari, J. J.; González, M. J., et al. A pilot clinical study of continuous intravenous ascorbate in terminal cancer patients. P. R. Health Sci. J. 24: 269-276; 2005.
14. Padayatty, S. J.; Sun, A. Y.; Chen, Q.; Espey, M. G.; Drisko, J.; Levine, M. Vitamin C: intravenous use by complementary and alternative medicine practitioners and adverse effects. PLoS One 5 (e1 1414); 2010.
15. Chen, Q.; Espey, M. G.; Krishna, M. C., 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. 102:13604-13609; 2005.
16. Chen, Q.; Espey, M. G.; Sun, A. 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. 104:8749-8754; 2007.
17. Chen, Q.; Espey, M. G.; Sun, A. Y., et al. Pharmacologic doses of ascorbate act as a prooxidant and decrease growth of aggressive tumor xenografts in mice. Proc. Natl. Acad. Sci. U. S. A. 105:11105-11109; 2008.
18. Du, J.; Sean, M.; Martin, S. M.; Levine, M., et al. Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer. Clin. Cancer Res. 16:509-520; 2010.
19. Chen, P.; Stone, J.; Sullivan, G.; Drisko, J. A.; Chen, Q. Anti-cancer effect of pharmacologic ascorbate and its interaction with supplementary parenteral glutathione in preclinical cancer models. Free Radic. Biol. Med. 51:681-687; 2011.
20. Cuddihy, S. L.; Parker, A.; Harwood, D. T.; Vissers, M. C.; Winterbourn, C. C. Ascorbate interacts with reduced glutathione to scavenge phenoxyl radicals in HL60 cells. Free Radic. Biol. Med. 44:1637-1644; 2008.
21. Padayatty, S. J.; Sun, H.; Wang, Y., et al. Vitamin C pharmacokinetics: implications for oral and intravenous use. Ann. Intern. Med. 140:533-537; 2004.
22. Goodman, M.; Bostick, R. M.; Kucuk, O.; Jones, D. P. Clinical trials of antioxidants as cancer prevention agents: past, present, and future. Free Radic. Biol. Med. 51: 1068-1084; 2011.
23. 2 on iron-dependent DNA strand breaks and related processes in the neuroblastoma cell line SK-N-SH. Cancer Res. 51:6066-6072; 1991.
24. 2-mediated cytotoxicity of pharmacologic ascorbate concentrations to neuroblastoma cells: potential role of lactate and ferritin. Cell. Physiol. Biochem. 25:767-774; 2010.
25. 2 and transition metal ions in the genotoxic action of ascorbic acid in cell culture models. Toxicol. Lett. 170:57-65; 2007.
26. Steinkühler, C.; Mavelli, I.; Melino, G., et al. Antioxygenic enzyme activities in differentiating human neuroblastoma cells. Ann. N. Y. Acad. Sci. 551:137-140; 1988.
27. Espey, M. G.; Chen, P.; Chalmers, B., et al. Pharmacologic ascorbate synergizes with gemcitabine in preclinical models of pancreatic cancer. Free Radic. Biol. Med. 50:1610-1619; 2011.
28. Gokhalé, P.; Patel, T.; Morrison, M. J.; Vissers, M. C. The effect of intracellular ascorbate on the susceptibility of HL60 and Jurkat cells to chemotherapy agents. Apoptosis 11:1737-1746; 2006.
29. Kassouf, W.; Highshaw, R.; Nelkin, G. M.; Dinney, C. P.; Kamat, A. M. Vitamins C and K3 sensitize human urothelial tumors to gemcitabine. J. Urol. 176 (4 Pt 1): 1642-1647; 2006.
30. Kurbacher, C. M.; Wagner, U.; Kolster, B.; Andreotti, P. E.; Krebs, D.; Bruckner, H. W. Ascorbic acid (vitamin C) improves the antineoplastic activity of doxorubicin, cisplatin, and paclitaxel in human breast carcinoma cells in vitro. Cancer Lett. 103:183-189; 1996.
31. Song, E. J.; Yang, V. C.; Chiang, C. D.; Chao, C. C. Potentiation of growth inhibition due to vincristine by ascorbic acid in a resistant human non-small cell lung cancer cell line. Eur. J. Pharmacol. 292:119-125; 1995.
32. Chu, P. M.; Chiou, S. H.; Su, T. L., et al. Enhancement of radiosensitivity in human glioblastoma cells by the DNA N-mustard alkylating agent BO-1051 through augmented and sustained damage response. Radiat. Oncol. 6; 2011.
33. Shinozaki, K.; Hosokawa, Y.; Hazawa, M., et al. Ascorbic acid enhances radiationinduced apoptosis in an HL60 human leukemia cell line. J. Radiat. Res. 52: 229-237; 2011.
34. Nagy, J. A.; Chang, S. H.; Dvorak, A. M.; Dvorak, H. F.Why are tumour blood vessels abnormal and why is it important to know? Br. J. Cancer 100:865-869; 2009.
35. Broadley, K.W. R.;Hunn,M. K.; Farrand, K. J., et al. Side population is not necessary or sufficient for a cancer stemcell phenotype in glioblastomamultiforme. StemCells 29: 452-461; 2011.
36. An, J.; Huang, Y. C.; Xu, Q. Z., et al. DNA-PKcs plays a dominant role in the regulation of H2AX phosphorylation in response to DNA damage and cell cycle progression. BMC Mol. Biol. 6:11-18; 2010.
37. Tanaka, T.; Halicka, D.; Traganos, F.; Darzynkiewicz, Z. Cytometric analysis of DNA damage: phosphorylation of histone H2AX as a marker of DNA double-strand breaks (DSBs). Methods Mol. Biol. 523:161-168; 2009.
38. Yao, K. C.; Komata, T.; Kondo, Y.; Kanzawa, T.; Kondo, S.; Germano, I. M. Molecular response of glioblastoma multiforme cells to ionizing radiation: cell cycle arrest, modulation of the expression of cyclin-dependent kinase inhibitors, and autophagy. J. Neurosurg. 98:378-384; 2003.
39. Pavlik, T.M.; Keyomarsi, K. Role of cell cycle inmediating sensitivity to radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 59:928-942; 2004.
40. Bareford, M. D.; Hamed, H. A.; Tang, Y., et al. Sorafenib enhances pemetrexed cytotoxicity through an autophagy-dependentmechanismin cancer cells. Autophagy 7:1261-1262; 2011.
41. Pattingre, S.; Levine, B. Bcl-2 inhibition of autophagy: a new route to cancer? Cancer Res. 66:2885-2888; 2006.
42. 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. 67:6293-6303; 2007.
43. Seglen, P. O.; Gordon, P. B. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 79:1889-1892; 1982.
44. Wu, Y. -T.; Tan, H. -L.; Shui, G., et al. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J. Biol. Chem. 285:10850-10861; 2010.
45. McCord, A. M.; Jamal, M.; Williams, E. S.; Camphausen, K.; Tofilon, P. J. CD133+ glioblastoma stem-like cells are radiosensitive with a defective DNA damage response compared with established cell lines. Clin. Cancer Res. 15:5145-5153; 2009.
46. Vissers, M. C.; Gunningham, S. P.; Morrison, M. J.; Dachs, G. U.; Currie, M. J. Modulation of hypoxia-inducible factor-1α in cultured primary cells by intracellular ascorbate. Free Radic. Biol. Med. 42:765-772; 2007.
47. Vissers, M. C.; Wilkie, R. P. Ascorbate deficiency results in impaired neutrophil apoptosis and clearance and is associated with up-regulation of hypoxia-inducible factor 1α. J. Leukoc. Biol. 81:1236-1244; 2007.
48. Kuiper, C.; Molenaar, I. G.; Dachs, G. U.; Currie, M. J.; Sykes, P. H.; Vissers, M. C. Low ascorbate levels are associated with increased hypoxia-inducible factor-1 activity and an aggressive tumor phenotype in endometrial cancer. Cancer Res. 70:5749-5758; 2010.
49. Han, S. S.; Kim, K.; Hahm, E. R., et al. L-Ascorbic acid represses constitutive activation of NF-κB and COX-2 expression in human acutemyeloid leukemia, HL-60. J. Cell. Biochem. 93:257-270; 2004.
50. Mao, Z.; Bozzella, M.; Seluanov, A.; Gorbunova, V. Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair 7: 1765-1771; 2008.
51. Stegh, A. H.; Chin, L.; Louis, D. N.; DePinho, R. A. What drives intense apoptosis resistance and propensity for necrosis in glioblastoma? A role for Bcl2L12 as a multifunctional cell death regulator. Cell Cycle 7:2833-2839; 2008.
52. Cullen, J. J. Ascorbate induces autophagy in pancreatic cancer. Autophagy 6: 421-422; 2010.
53. Levine, B. Cell biology: autophagy and cancer. Nature 446:745-747; 2007.