Pharmacologic concentrations of ascorbate are achieved by parenteral administration and exhibit antitumoral effects

Free Radical Biology and Medicine

Volumn 47, Issue 1, 2009, Pages 32-40

  Verrax, Julien ^a   Calderon, Pedro Buc ^a  

^a Louvain Drug Research Institute   (Belgium)

Author keywords

Ascorbate; Cancer; Chemotherapy; Free radicals; Oxidative stress; Vitamin C

Indexed keywords

ASCORBIC ACID; HYDROGEN PEROXIDE; TRANSITION ELEMENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CONTROLLED STUDY; CYTOTOXICITY; DRUG BLOOD LEVEL; DRUG INHIBITION; DRUG MECHANISM; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACETYLCYSTEINE; ADMINISTRATION, ORAL; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; ASCORBIC ACID; CATALASE; CELL DEATH; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DRUG DOSAGE CALCULATIONS; DRUG SYNERGISM; FEMALE; FREE RADICAL SCAVENGERS; HUMANS; INFUSIONS, PARENTERAL; LIVER NEOPLASMS, EXPERIMENTAL; MICE;

MURINAE;

EID: 67349235547     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.02.016     Document Type: Article

References (59)

1. Cameron E., and Pauling L. Supplemental ascorbate in the supportive treatment of cancer: prolongation of survival times in terminal human cancer. Proc. Natl. Acad. Sci. USA 73 (1976) 3685-3689
2. Cameron E., and Pauling L. Supplemental ascorbate in the supportive treatment of cancer: reevaluation of prolongation of survival times in terminal human cancer. Proc. Natl. Acad. Sci. USA 75 (1978) 4538-4542
3. Cameron E., Pauling L., and Leibovitz B. Ascorbic acid and cancer: a review. Cancer Res 39 (1979) 663-681
4. Bodansky O., Wroblewski F., and Markardt B. Concentrations of ascorbic acid in plasma and white blood cells of patients with cancer and noncancerous chronic disease. Cancer 5 (1952) 678-684
5. Gonçalves T., Erthal F., Corte C., Müller L., Piovezan C., Nogueira C., and Rocha J. Involvement of oxidative stress in the pre-malignant and malignant states of cervical cancer in women. Clin. Biochem 38 (2005) 1071-1075
6. Mayland C., Bennett M., and Allan K. Vitamin C deficiency in cancer patients. Palliat. Med 19 (2005) 17-20
7. Georgiannos S., Weston P., and Goode A. Micronutrients in gastrointestinal cancer. Br. J. Cancer 68 (1993) 1195-1198
8. Weijl N., Elsendoorn T., Lentjes E., Hopman G., Wipkink-Bakker A., Zwinderman A., Cleton F., and Osanto S. Supplementation with antioxidant micronutrients and chemotherapy-induced toxicity in cancer patients treated with cisplatin-based chemotherapy: a randomised, double-blind, placebo-controlled study. Eur. J. Cancer 40 (2004) 1713-1723
9. Creagan E., Moertel C., O'Fallon J., Schutt A., O'Connell M., Rubin J., and Frytak S. Failure of high-dose vitamin C (ascorbic acid) therapy to benefit patients with advanced cancer: a controlled trial. N. Engl. J. Med 301 (1979) 687-690
10. Moertel C., Fleming T., Creagan E., Rubin J., O'Connell M., and Ames 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 (1985) 137-141
11. Padayatty S., and Levine M. Reevaluation of ascorbate in cancer treatment: emerging evidence, open minds and serendipity. J. Am. Coll. Nutr 19 (2000) 423-425
12. Padayatty S., Sun H., Wang Y., Riordan H., Hewitt S., Katz A., Wesley R., and Levine M. Vitamin C pharmacokinetics: implications for oral and intravenous use. Ann. Intern. Med 140 (2004) 533-537
13. Levine M., Conry-Cantilena C., Wang Y., Welch R., Washko P., Dhariwal K., Park J., Lazarev A., Graumlich J., King J., and Cantilena L. Vitamin C pharmacokinetics in healthy volunteers: evidence for a recommended dietary allowance. Proc. Natl. Acad. Sci. USA 93 (1996) 3704-3709
14. Levine M., Wang Y., Padayatty S., and Morrow J. A new recommended dietary allowance of vitamin C for healthy young women. Proc. Natl. Acad. Sci. USA 98 (2001) 9842-9846
15. Prasad K. Modulation of the effects of tumor therapeutic agents by vitamin C. Life Sci 27 (1980) 275-280
16. De Laurenzi V., Melino G., Savini I., Annicchiarico-Petruzzelli M., Finazzi-Agrò A., and Avigliano L. Cell death by oxidative stress and ascorbic acid regeneration in human neuroectodermal cell lines. Eur. J. Cancer 31A (1995) 463-466
17. Kang J., Cho D., Kim Y., Hahm E., Yang Y., Kim D., Hur D., Park H., Bang S., Hwang Y., and Lee W. l-Ascorbic acid (vitamin C) induces the apoptosis of B16 murine melanoma cells via a caspase-8-independent pathway. Cancer Immunol. Immunother 52 (2003) 693-698
18. Chen Q., Espey M., Krishna M., Mitchell J., Corpe C., Buettner G., Shacter E., and Levine M. Pharmacologic ascorbic acid concentrations selectively kill cancer cells: action as a pro-drug to deliver hydrogen peroxide to tissues. Proc. Natl. Acad. Sci. USA 102 (2005) 13604-13609
19. Verrax J., Stockis J., Tison A., Taper H., and Calderon P. Oxidative stress by ascorbate/menadione association kills K562 human chronic myelogenous leukaemia cells and inhibits its tumour growth in nude mice. Biochem. Pharmacol 72 (2006) 671-680
20. Verrax J., Vanbever S., Stockis J., Taper H., and Calderon P. Role of glycolysis inhibition and poly(ADP-ribose) polymerase activation in necrotic-like cell death caused by ascorbate/menadione-induced oxidative stress in K562 human chronic myelogenous leukemic cells. Int. J. Cancer 120 (2007) 1192-1197
21. Chen Q., Espey M., Sun A., Pooput C., Kirk K., Krishna M., Khosh D., Drisko J., and Levine M. Pharmacologic doses of ascorbate act as a prooxidant and decrease growth of aggressive tumor xenografts in mice. Proc. Natl. Acad. Sci. USA 105 (2008) 11105-11109
22. Wroblewski F., and Ladue J. Lactic dehydrogenase activity in blood. Proc. Soc. Exp. Biol. Med 90 (1955) 210-213
23. Emadi-Konjin P., Verjee Z., Levin A., and Adeli K. Measurement of intracellular vitamin C levels in human lymphocytes by reverse phase high performance liquid chromatography (HPLC). Clin. Biochem 38 (2005) 450-456
24. Casciari J., Riordan N., Schmidt T., Meng X., Jackson J., and Riordan H. Cytotoxicity of ascorbate, lipoic acid, and other antioxidants in hollow fibre in vitro tumours. Br. J. Cancer 84 (2001) 1544-1550
25. Hoffer L., Levine M., Assouline S., Melnychuk D., Paddayatty S., Rosadiuk K., Rousseau C., Robitaille L., and Miller W.J. Phase I clinical trial of i.v. ascorbic acid in advanced malignancy. Ann. Oncol 19 (2008) 1969-1974
26. Murphy J., Ravi N., Byrne P., McDonald G., and Reynolds J. Neither antioxidants nor COX-2 inhibition protect against esophageal inflammation in an experimental model of severe reflux. J. Surg. Res 142 (2007) 20-27
27. Pincemail J., Siquet J., Chapelle J., Cheramy-Bien J., Paulissen G., Chantillon A., Christiaens G., Gielen J., Limet R., and Defraigne J. Determination of plasma concentrations of antioxidants, antibodies against oxidized LDL, and homocysteine in a population sample from Liège. Ann. Biol. Clin. (Paris) 58 (2000) 177-185
28. Myint P., Luben R., Welch A., Bingham S., Wareham N., and Khaw K. Plasma vitamin C concentrations predict risk of incident stroke over 10 y in 20 649 participants of the European Prospective Investigation into Cancer Norfolk prospective population study. Am. J. Clin. Nutr 87 (2008) 64-69
29. Chen Q., Espey M., Sun A., Lee J., Krishna M., Shacter E., Choyke P., Pooput C., Kirk K., Buettner G., and Levine M. Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo. Proc. Natl. Acad. Sci. USA 104 (2007) 8749-8754
30. Taper H., Woolley G., Teller M., and Lardis M. A new transplantable mouse liver tumor of spontaneous origin. Cancer Res 26 (1966) 143-148
31. Ansiaux R., Baudelet C., Cron G., Segers J., Dessy C., Martinive P., De Wever J., Verrax J., Wauthier V., Beghein N., Grégoire V., Buc Calderon P., Feron O., and Gallez B. Botulinum toxin potentiates cancer radiotherapy and chemotherapy. Clin. Cancer Res 12 (2006) 1276-1283
32. Crokart N., Jordan B., Baudelet C., Cron G., Hotton J., Radermacher K., Grégoire V., Beghein N., Martinive P., Bouzin C., Feron O., and Gallez B. Glucocorticoids modulate tumor radiation response through a decrease in tumor oxygen consumption. Clin. Cancer Res 13 (2007) 630-635
33. Frérart F., Sonveaux P., Rath G., Smoos A., Meqor A., Charlier N., Jordan B., Saliez J., Noël A., Dessy C., Gallez B., and Feron O. The acidic tumor microenvironment promotes the reconversion of nitrite into nitric oxide: towards a new and safe radiosensitizing strategy. Clin. Cancer Res 14 (2008) 2768-2774
34. Jordan B., Grégoire V., Demeure R., Sonveaux P., Feron O., O'Hara J., Vanhulle V., Delzenne N., and Gallez B. Insulin increases the sensitivity of tumors to irradiation: involvement of an increase in tumor oxygenation mediated by a nitric oxide-dependent decrease of the tumor cells oxygen consumption. Cancer Res 62 (2002) 3555-3561
35. Vickers A., Kuo J., and Cassileth B. Unconventional anticancer agents: a systematic review of clinical trials. J. Clin. Oncol 24 (2006) 136-140
36. 2 and transition metal ions in the genotoxic action of ascorbic acid in cell culture models. Toxicol. Lett 170 (2007) 57-65
37. Hanahan D., and Weinberg R. The hallmarks of cancer. Cell 100 (2000) 57-70
38. Carr A., and Frei B. Does vitamin C act as a pro-oxidant under physiological conditions?. FASEB J 13 (1999) 1007-1024
39. Buettner G., and Jurkiewicz B. Catalytic metals, ascorbate and free radicals: combinations to avoid. Radiat. Res 145 (1996) 532-541
40. Frei B., and Lawson S. Vitamin C and cancer revisited. Proc. Natl. Acad. Sci. USA 105 (2008) 11037-11038
41. Vafa O., Wade M., Kern S., Beeche M., Pandita T., Hampton G., and Wahl G. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol. Cell 9 (2002) 1031-1044
42. Sattler M., Verma S., Shrikhande G., Byrne C., Pride Y., Winkler T., Greenfield E., Salgia R., and Griffin J. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J. Biol. Chem 275 (2000) 24273-24278
43. Laurent A., Nicco C., Chéreau C., Goulvestre C., Alexandre J., Alves A., Lévy E., Goldwasser F., Panis Y., Soubrane O., Weill B., and Batteux F. Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer Res 65 (2005) 948-956
44. Trachootham D., Zhou Y., Zhang H., Demizu Y., Chen Z., Pelicano H., Chiao P., Achanta G., Arlinghaus R., Liu J., and Huang P. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10 (2006) 241-252
45. Trachootham D., Zhang H., Zhang W., Feng L., Du M., Zhou Y., Chen Z., Pelicano H., Plunkett W., Wierda W., Keating M., and Huang P. Effective elimination of fludarabine-resistant CLL cells by PEITC through a redox-mediated mechanism. Blood 112 (2008) 1912-1922
46. Oberley T., and Oberley L. Antioxidant enzyme levels in cancer. Histol. Histopathol 12 (1997) 525-535
47. Sun Y., Oberley L., Elwell J., and Sierra-Rivera E. Antioxidant enzyme activities in normal and transformed mouse liver cells. Int. J. Cancer 44 (1989) 1028-1033
48. Yang J., Lam E., Hammad H., Oberley T., and Oberley L. Antioxidant enzyme levels in oral squamous cell carcinoma and normal human oral epithelium. J. Oral Pathol. Med 31 (2002) 71-77
49. Verrax J., Cadrobbi J., Marques C., Taper H., Habraken Y., Piette J., and Calderon P. Ascorbate potentiates the cytotoxicity of menadione leading to an oxidative stress that kills cancer cells by a non-apoptotic caspase-3 independent form of cell death. Apoptosis 9 (2004) 223-233
50. Taper H., de Gerlache J., Lans M., and Roberfroid M. Non-toxic potentiation of cancer chemotherapy by combined C and K3 vitamin pre-treatment. Int. J. Cancer 40 (1987) 575-579
51. Kassouf W., Highshaw R., Nelkin G., Dinney C., and Kamat A. Vitamins C and K3 sensitize human urothelial tumors to gemcitabine. J. Urol 176 (2006) 1642-1647
52. Abdel-Latif M., Raouf A., Sabra K., Kelleher D., and Reynolds J. Vitamin C enhances chemosensitization of esophageal cancer cells in vitro. J. Chemother 17 (2005) 539-549
53. Kuppusamy P., Li H., Ilangovan G., Cardounel A., Zweier J., Yamada K., Krishna M., and Mitchell J. Noninvasive imaging of tumor redox status and its modification by tissue glutathione levels. Cancer Res 62 (2002) 307-312
54. Roshchupkina G., Bobko A., Bratasz A., Reznikov V., Kuppusamy P., and Khramtsov V. In vivo EPR measurement of glutathione in tumor-bearing mice using improved disulfide biradical probe. Free Radic. Biol. Med. 45 (2008) 312-320
55. Bahlis N., McCafferty-Grad J., Jordan-McMurry I., Neil J., Reis I., Kharfan-Dabaja M., Eckman J., Goodman M., Fernandez H., Boise L., and Lee K. Feasibility and correlates of arsenic trioxide combined with ascorbic acid-mediated depletion of intracellular glutathione for the treatment of relapsed/refractory multiple myeloma. Clin. Cancer Res 8 (2002) 3658-3668
56. Dai J., Weinberg R., Waxman S., and Jing Y. Malignant cells can be sensitized to undergo growth inhibition and apoptosis by arsenic trioxide through modulation of the glutathione redox system. Blood 93 (1999) 268-277
57. Grad J., Bahlis N., Reis I., Oshiro M., Dalton W., and Boise L. Ascorbic acid enhances arsenic trioxide-induced cytotoxicity in multiple myeloma cells. Blood 98 (2001) 805-813
58. Berenson J., Boccia R., Siegel D., Bozdech M., Bessudo A., Stadtmauer E., Talisman Pomeroy J., Steis R., Flam M., Lutzky J., Jilani S., Volk J., Wong S., Moss R., Patel R., Ferretti D., Russell K., Louie R., Yeh H., and Swift R. Efficacy and safety of melphalan, arsenic trioxide and ascorbic acid combination therapy in patients with relapsed or refractory multiple myeloma: a prospective, multicentre, phase II, single-arm study. Br. J. Haematol 135 (2006) 174-183
59. Berenson J., Matous J., Swift R., Mapes R., Morrison B., and Yeh H. A phase I/II study of arsenic trioxide/bortezomib/ascorbic acid combination therapy for the treatment of relapsed or refractory multiple myeloma. Clin. Cancer Res 13 (2007) 1762-1768