Pharmacological doses of daily ascorbate protect tumours from radiation damage after a single dose of radiation in an intracranial mouse glioma model

Frontiers in Oncology

Volumn 4, Issue NOV, 2014, Pages

  Grasso, Carole ^a   Fabre, Marie Sophie ^b   Collis, Sarah V ^b   Letitia Castro, M ^b   Field, Cameron S ^a   Schleich, Nanette ^c,d   McConnell, Melanie J ^a,b   Herst, Patries M ^a,c  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

^b VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d WELLINGTON HOSPITAL   (New Zealand)

Author keywords

GL261; Intracranial mouse glioma model; Pharmacological ascorbate; Radiation; Radioprotection; Radiosensitisation

Indexed keywords

ASCORBIC ACID; BUPRENORPHINE; CARPROFEN; CESIUM 137; MENADIONE; SODIUM ASCORBIC ACID COTRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN RADIATION; CANCER TRANSPLANTATION; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL VIABILITY; CFU COUNTING; CLONOGENESIS; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GLIOBLASTOMA; GLIOMA; HISTOLOGY; IMMUNOCOMPETENT CELL; MALE; MOUSE; NONHUMAN; POSTOPERATIVE PAIN; RADIATION DOSE; RADIATION INJURY; RADIOSENSITIZATION; SENSITIVITY ANALYSIS; THERMOLUMINESCENCE DOSIMETER; THERMOLUMINESCENCE DOSIMETRY; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR NECROSIS; X IRRADIATION;

EID: 84915760604     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00356     Document Type: Article

References (58)

1. Parrow NL, Leshin JA, Levine M. Parenteral ascorbate as a cancer therapeutic: a reassessment based on pharmacokinetics. Antioxid Redox Signal. 2013;19(17):2141-56.
2. Nishikimi M, Yagi K. Molecular basis for the deficiency in humans of gulonolactone oxidase, a key enzyme for ascorbic acid biosynthesis. Am J Clin Nutr 1991. 1991;54(6):1203S-1208S.
3. Harrison FE, May JM. Vitamin C function in the brain: vital role of the ascorbate transporter SVCT2. Free Radic Biol Med. 2009;46(6):719-30.
4. Hoffer LJ, Levine M, Assouline S, Melnychuk D, Padayatty SJ, Rosadiuk K, et al. Phase I clinical trial of i.v. ascorbic acid in advanced malignancy. Ann Oncol. 2008;19(12):1969-74.
5. Stephenson CM, Levin RD, Spector T, Lis CG. Phase I clinical trial to evaluate the safety, tolerability, and pharmacokinetics of high-dose intravenous ascorbic acid in patients with advanced cancer. Cancer Chemother Pharmacol. 2013 Jul;72(1):139-46.
6. Chen Q, Espey MG, Sun AY, Lee JH, Krishna MC, Shacter E, 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(21):8749-54.
7. Herst PM, Broadley KWR, Harper JL, McConnell MJ. Pharmacological concentrations of ascorbate radiosensitize glioblastoma multiforme primary cells by increasing oxidative DNA damage and inhibiting G2/M arrest. Free Radic Biol Med. Elsevier Inc.; 2012 Apr 15;52(8):1486-93.
8. Castro ML, McConnell MJ, Herst PM. Radio-sensitisation by pharmacological ascorbate in glioblastoma multiforme cells, human glial cells and HUVECs depends on their antioxidant and DNA repair capabilities and is not cancer specific. Free Radic Biol Med. 2014;in press.
9. Du J, Martin SM, Levine M, Wagner BA, Buettner GR, Wang SH, et al. Mechanisms of Ascorbate-Induced Cytotoxicity in Pancreatic Cancer. Clin Cancer Res. 2010;16(2):509-20.
10. Chen Q, Espey MG, Sun AY, Pooput C, Kirk KL, Krishna MC, 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. 2008;105(32):11105-9.
11. Ma Y, Chapman J, Levine M, Polireddy K, Drisko J. High dose parenteral ascorbate enhanced chemosensitivity of ovarian cancer and reduced toxicity of chemotherapy. Sci Transl Med. 2014;6(222):222ra18.
12. Espey MG, Chen P, Chalmers B, Drisko J, Sun AY, Levine M, et al. Pharmacologic ascorbate synergizes with gemcitabine in preclinical models of pancreatic cancer. Free Radic Biol Med. 2011;50(11):1610-9.
13. Martinotti S, Ranzato E, Parodi M, Vitale M, Burlando B. Combination of ascorbate/epigallocatechin-3-gallate/gemcitabine synergistically induces cell cycle deregulation and apoptosis in mesothelioma cells. Toxicol Appl Pharmacol. 2014;274(1):35-41.
14. Song EJ, Yang VC, Chiang CD, Chao CC. Potentiation of growth inhibition due to vincristine by ascorbic acid in a resistant human non-small cell lung cancer cell line. Eur J Pharmacol. 1995;292(2):119-25.
15. Vuyyuri SB, Rinkinen J, Worden E, Shim H, Lee S, Davis KR. Ascorbic Acid and a cytostatic inhibitor of glycolysis synergistically induce apoptosis in non-small cell lung cancer cells. PLoS One. 2013 Jan;8(6):e67081.
16. Olney KE, Du J, van't Erve TJ, Witmer JR, Sibenaller ZA, Wagner BA, et al. Inhibitors of hydroperoxide metabolism enhance ascorbate-induced cytotoxicity. Free Radic Res. 2013;47(3):154-63.
17. Tomasetti M, Nocchi L, Neuzil J, Goodwin J, Nguyen M, Dong L, et al. Alpha tocopheryl succinate inhibits autophagic survival of prostate cancer cells induced by vitamin K3 and ascorbate to trigger cell death. PLoS One. 2012 Jan;7(12):e52263.
18. Evans MK, Tovmasyan A, Batinic-Haberle I, Devi GR. Mn porphyrin in combination with ascorbate acts as a pro-oxidant and mediates caspase-independent cancer cell death. Free Radic Biol Med. 2014;68:302-14.
19. Rawal M, Schroeder SR, Wagner BA, Cushing CM, Welsh JL, Button AM, et al. Manganoporphyrins increase ascorbate-induced cytotoxicity by enhancing H2O2 generation. Cancer Res. 2013;73(16):5232-41.
20. Felipe KB, Benites J, Glorieux C, Sid B, Valenzuela M, Kviecinski MR, et al. Antiproliferative effects of phenylaminonaphthoquinones are increased by ascorbate and associated with the appearance of a senescent phenotype in human bladder cancer cells. Biochem Biophys Res Commun. 2013;433(4):573-8.
21. Frömberg A, Gutsch D, Schulze D, Vollbracht C, Weiss G, Czubayko F, et al. Ascorbate exerts anti-proliferative effects through cell cycle inhibition and sensitizes tumor cells towards cytostatic drugs. Cancer Chemother Pharmacol. 2011;67(5):1157-66.
22. Welsh JL, Wagner BA, van't Erve TJ, Zehr PS, Berg DJ, Halfdanarson TR, et al. Pharmacological ascorbate with gemcitabine for the control of metastatic and node positive pancreatic cancer (PACMAN): results from a phase I clinical trial. Cancer Chemother Pharmacol. 2013 Mar;71(3):765-75.
23. Monti DA, Mitchell E, Bazzan AJ, Littman S, Zabrecky G, Yeo CJ, et al. Phase I evaluation of intravenous ascorbic acid in combination with gemcitabine and erlotinib in patients with metastatic pancreatic cancer. PLoS One. 2012 Jan;7(1):e29794.
24. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, 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. 2009;10(5):459-66.
25. Larson EW, Peterson HE, Lamoreaux WT, MacKay AR, Fairbanks RK, Call JA, et al. Clinical outcomes following salvage Gamma Knife radiosurgery for recurrent glioblastoma. World J Clin Oncol. 2014 May 10;5(2):142-8.
26. 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. 2010;30(30):10096-111.
27. Wondrak GT. Redox-directed cancer therapeutics: Molecular mechanisms and opportunities. Antioxidants Redox Signal. 2009;11(12):3013-69.
28. Moser JC, Rawal M, Wagner B, Du J, Cullen JJ, Buettner GR. Pharmacological ascorbate and ionizing radiation (IR) increase labile iron in pancreatic cancer. Redox Biol. Elsevier; 2013 Jan;2:22-7.
29. Baader SL, Bruchelt G, Carmine TC, Lode HN, Rieth AG, Niethammer D. Ascorbic acid mediated iron release from cellular ferritin and its relation to DNA strand break formation in neuroblastoma cells. J Cancer Res Clin Oncol. 1994;120:415-21.
30. Taper HS, Keyeux A, Roberfroid M. Potentiation of radiotherapy by nontoxic pretreatment with combined vitamins C and K3 in mice bearing solid transplantable tumor. Anticancer Res. 1996;16(1):499-503.
31. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nat Protoc. 2006;1:2315-9.
32. 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. 2009;523:161-8.
33. Hunn MK, Farrand KJ, Broadley KWR, Weinkove R, Ferguson P, Miller RJ, et al. Vaccination with irradiated tumor cells pulsed with an adjuvant that stimulates NKT cells is an effective treatment for glioma. Clin Cancer Res. 2012 Dec 1;18(23):6446-59.
34. Newcomb EW, Lukyanov Y, Kawashima N, Alonso-Basanta M, Wang SC, Liu M, et al. Radiotherapy enhances antitumor effect of anti-CD137 therapy in a mouse Glioma model. Radiat Res. 2010 Apr,173(4):426-32.
35. Kron T. Thermoluminescence dosimetry and its applications in medicine-part 1: physics, materials and equipment. Australas Phys Eng Sci Med. 1994;17(4):175-99.
36. DeWerd LA, Bartol LJ, Davis SD. Thermoluminescence dosimetry. Clinical Dosimetry for Radiotherapy: AAPM Summer School. Colorado; 2009. p. 815-40.
37. Nunn AA, Davis SD, Micka JA, DeWerd LA. LiF:Mg, Ti TLD response as a function of photon energy for moderately filtered x-ray spectra in the range of 20-250 kVp relative to 60Co. Med Phys. 2008;35(5):1859.
38. Haworth A, Butler DJ, Wilfert L, Ebert MA, Todd SP, Hayton AJ, et al. Comparison of TLD calibration methods for 192Ir dosimetry. J Appl Clin Med Phys. 2013;14(1):258-72.
39. Stegh AH, Chin L, Louis DN, DePinho RA. What drives intense apoptosis resistance and propensity for necrosis in glioblastoma? A role for Bcl2L12 as a multifunctional cell death regulator. Cell Cycle. 2008;7(18):2833-9.
40. Broadley KWR, Hunn MK, Farrand KJ, Price KM, Grasso C, Miller RJ, et al. Side population is not necessary or sufficient for a cancer stem cell phenotype in gliobastoma multiforme. Stem Cells. 2011;29:452-61.
41. Kim SH, Lee JE, Yang S-H, Lee SW. Induction of cytokines and growth factors by rapamycin in the microenvironment of brain metastases of lung cancer. Oncol Lett. 2013 Mar;5(3):953-8.
42. Kim S-J, Kim J-S, Park ES, Lee J-S, Lin Q, Langley RR, et al. Astrocytes Upregulate Survival Genes in Tumor Cells and Induce Protection from Chemotherapy 1. Neoplasia. 2011;13(3):286-98.
43. Jamal M, Rath BH, Tsang PS, Camphausen K, Tofilon PJ. The brain microenvironment preferentially enhances the radioresistance of CD133(+) glioblastoma stem-like cells. Neoplasia. 2012;14(2150-158).
44. Jamal M, Rath BH, Williams ES, Camphausen K, Tofilon PJ. Microenvironmental regulation of glioblastoma radioresponse. Clin Cancer Res. 2010 Dec 15;16(24):6049-59.
45. Bürzle M, Suzuki Y, Ackermann D, Miyazaki H, Maeda N, Clémençon B, et al. The sodium-dependent ascorbic acid transporter family SLC23. Mol Asp Med. 2013;34(2-3):436-54.
46. Agus DB, Gambhir SS, Pardridge WM, Spielholz C, Baselga J, Vera JC, et al. Vitamin C crosses the blood-brain barrier in the oxidized form through the glucose transporters. J Clin Invest. 1997 Dec 1;100(11):2842-8.
47. Bürzle M, Hediger M. Functional and physiological role of vitamin C transporters. Curr Top Membr. 2012;70:357-75.
48. Vissers MC, Gunningham SP, Morrison MJ, Dachs GU, Currie MJ. Modulation of hypoxia-inducible factor-1 alpha in cultured primary cells by intracellular ascorbate. Free Radic Biol Med. 2007;42(6):765-72.
49. Pastor P, Cisternas P, Salazar K, Silva- Alvarez C, Oyarce K, Jara N, et al. SVCT2 vitamin C transporter expression in progenitor cells of the postnatal neurogenic niche. Front Cell Neurosci. 2013 Jan;7(August):119.
50. Sun L, Hui AM, Su Q, Vortmeyer A, Kotliarov Y, Pastorino S, et al. Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell. 2006;9(4):287-300.
51. Bredel M, Bredel C, Juric D, Harsh GR, Vogel H, Recht LD, et al. Functional network analysis reveals extended gliomagenesis pathway maps and three novel MYC- interacting genes in human gliomas. Cancer Res. 2005;65(19):8679-89.
52. Shai R, Shi T, Kremen TJ, Horvath S, Liau LM, Cloughesy TF, et al. Gene expression profiling identifies molecular subtypes of gliomas. Oncogene. 2003;22(31):4918-23.
53. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, Hamou MF, et al. Stem cell- related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol. 2008;26(18):3015-24.
54. Liang Y, Diehn M, Watson N, Bollen AW, Aldape KD, Nicholas MK, et al. Gene expression profiling reveals molecularly and clinically distinct subtypes of glioblastoma multiforme. Proc Natl Acad Sci U S A. 2005;102(16):5814-9.
55. Rodríguez FS, Salazar KA, Jara NA, García-Robles MA, Pérez F, Ferrada LE, et al. Superoxide-dependent uptake of vitamin C in human glioma cells. J Neurochem. 2013;127(6):793-804.
56. McCarty MF. Expression and/or activity of the SVCT2 ascorbate transporter may be decreased in many aggressive cancers, suggesting potential utility for sodium bicarbonate and dehydroascorbic acid in cancer therapy. Med Hypotheses. 2013;81(4):664-70.
57. Da Fonseca AC, Badie B. Microglia and macrophages in malignant gliomas: recent discoveries and implications for promising therapies. Clin Dev Immunol. 2013 Jan;2013:264124.
58. Badiyan S, Markovina S, Simpson J, Robinson C, DeWees T, Tran D, et al. Radiation Therapy Dose Escalation for Glioblastoma Multiforme in the Era of Temozolomide. Int J Radiat Oncol Biol Phys. 2014;Sep 23. pi:[Epub ahead of print].