Erratum: O2 ⋅− and H2O2-Mediated Disruption of Fe Metabolism Causes the Differential Susceptibility of NSCLC and GBM Cancer Cells to Pharmacological Ascorbate (Cancer Cell (2017) 32 (2)(268) (S1535610817300624) (10.1016/j.ccell.2017.02.018));O2⋅− and H2O2-Mediated Disruption of Fe Metabolism Causes the Differential Susceptibility of NSCLC and GBM Cancer Cells to Pharmacological Ascorbate

Cancer Cell

Volumn 31, Issue 4, 2017, Pages 487-500.e8

  Schoenfeld, Joshua D ^a   Sibenaller, Zita A ^a   Mapuskar, Kranti A ^a   Wagner, Brett A ^a   Cramer Morales, Kimberly L ^a   Furqan, Muhammad ^a   Sandhu, Sonia ^a   Carlisle, Thomas L ^a   Smith, Mark C ^a   Abu Hejleh, Taher ^a   Berg, Daniel J ^a   Zhang, Jun ^a   Keech, John ^b   Parekh, Kalpaj R ^b   Bhatia, Sudershan ^a   Monga, Varun ^a   Bodeker, Kellie L ^a   Ahmann, Logan ^a   Vollstedt, Sandy ^a   Brown, Heather ^a   Shanahan Kauffman, Erin P ^a   Schall, Mary E ^a   Hohl, Ray J ^a   Clamon, Gerald H ^a   Greenlee, Jeremy D ^a   Howard, Matthew A ^a   Shultz, Michael K ^a   Smith, Brian J ^b   Riley, Dennis P ^c   Domann, Frederick E ^a   Cullen, Joseph J ^b   Buettner, Garry R ^a   Buatti, John M ^a   Spitz, Douglas R ^a   Allen, Bryan G ^a   more..

^a UNIVERSITY OF IOWA   (United States)

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

^c Galera Therapeutics Inc Inc   (United States)

Author keywords

ferritin; glioblastoma multiforme; hydrogen peroxide; labile iron metabolism; non small cell lung cancer; oxidative stress; pharmacological ascorbate; superoxide; superoxide dismutase; transferrin receptor

Indexed keywords

AMMONIUM SULFATE; ASCORBIC ACID; CATALASE; DEHYDROASCORBIC ACID; GLUTATHIONE PEROXIDASE 1; HYDROGEN PEROXIDE; IRON; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; OXYGEN; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; SUPEROXIDE DISMUTASE; TEMOZOLOMIDE; ANTINEOPLASTIC AGENT; RADIOSENSITIZING AGENT;

AEROBIC METABOLISM; ARTICLE; ASTROCYTE; CELL DEATH; CELL KILLING; CELL LYSATE; CHEMORADIOTHERAPY; COMPARATIVE STUDY; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG EFFICACY; ELECTRON TRANSPORT; FATIGUE; FEMALE; GENETIC BACKGROUND; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INFECTION; IONIZING RADIATION; IRON METABOLISM; LEUKOPENIA; LOBECTOMY; METHYLATION; NAUSEA; NEUTROPENIA; NON SMALL CELL LUNG CANCER; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RESPIRATORY CHAIN; STEADY STATE; TUMOR XENOGRAFT; UPREGULATION; VOMITING; ANIMAL; BRAIN NEOPLASMS; CARCINOMA, NON-SMALL-CELL LUNG; CLINICAL TRIAL; DRUG SCREENING; LUNG NEOPLASMS; MALE; METABOLISM; MORTALITY; NUDE MOUSE; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PROCEDURES; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; ASCORBIC ACID; BRAIN NEOPLASMS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CHEMORADIOTHERAPY; FEMALE; GLIOBLASTOMA; HUMANS; HYDROGEN PEROXIDE; IRON; LUNG NEOPLASMS; MALE; MICE, NUDE; OXYGEN; RADIATION-SENSITIZING AGENTS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85016453133     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2017.07.008     Document Type: Erratum

References (73)

1. 2 mediate glucose deprivation-induced stress in human cancer cells. J. Biol. Chem. 280 (2005), 4254–4263.
2. Ahmad, I.M., Abdalla, M.Y., Aykin-Burns, N., Simons, A.L., Oberley, L.W., Domann, F.E., Spitz, D.R., 2-Deoxyglucose combined with wild-type p53 overexpression enhances cytotoxicity in human prostate cancer cells via oxidative stress. Free Radic. Biol. Med. 44 (2008), 826–834.
3. 2 mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem. J. 418 (2009), 29–37.
4. Birch-Machin, M.A., Briggs, H.L., Saborido, A.A., Bindoff, L.A., Turnbull, D.M., An evaluation of the measurement of the activities of complexes I-IV in the respiratory chain of human skeletal muscle mitochondria. Biochem. Med. Metab. Biol. 51 (1994), 35–42.
5. Bize, I.B., Oberley, L.W., Morris, H.P., Superoxide dismutase and superoxide radical in Morris hepatomas. Cancer Res. 40 (1980), 3686–3693.
6. Boyer, R.F., McCleary, C.J., Superoxide ion as a primary reductant in ascorbate-mediated ferritin iron release. Free Radic. Biol. Med. 3 (1987), 389–395.
7. Buettner, G.R., Ascorbate autoxidation in the presence of iron and copper chelates. Free Radic. Res. Commun. 1 (1986), 349–353.
8. Buettner, G.R., In the absence of catalytic metals ascorbate does not autoxidize at pH 7: ascorbate as a test for catalytic metals. J. Biochem. Biophys. Methods 16 (1988), 27–40.
9. Buettner, G.R., Jurkiewicz, B.A., Catalytic metals, ascorbate and free radicals: combinations to avoid. Radiat. Res. 145 (1996), 532–541.
10. 2 on the expression and function of iron-responsive element-containing mRNAs in B6 fibroblasts. J. Biol. Chem. 276 (2001), 19738–19745.
11. Cameron, E., Rotman, D., Ascorbic acid, cell proliferation, and cancer. Lancet, 299, 1972, 542.
12. Cameron, E., 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.
13. Campbell, E.J., Vissers, M.C.M., Wohlrab, C., Hicks, K.O., Strother, R.M., Bozonet, S.M., Robinson, B.A., Dachs, G.U., Pharmacokinetic and anti-cancer properties of high dose ascorbate in solid tumours of ascorbate-dependent mice. Free Radic. Biol. Med. 99 (2016), 451–462.
14. Case, A.J., McGill, J.L., Tygrett, L.T., Shirasawa, T., Spitz, D.R., Waldschmidt, T.J., Legge, K.L., Domann, F.E., Elevated mitochondrial superoxide disrupts normal T cell development, impairing adaptive immune responses to an influenza challenge. Free Radic. Biol. Med. 50 (2011), 448–458.
15. Chen, Q., Espey, M.G., Krishna, M.C., Mitchell, J.B., Corpe, C.P., Buettner, G.R., Shacter, E., 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.
16. Chen, Q., Espey, M.G., Sun, A.Y., Lee, J.-H., Krishna, M.C., Shacter, E., Choyke, P.L., Pooput, C., Kirk, K.L., Buettner, G.R., et al. 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.
17. Chen, Q., Espey, M.G., Sun, A.Y., Pooput, C., Kirk, K.L., Krishna, M.C., Khosh, D.B., Drisko, J., 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.
18. Clément, M.-V., Ramalingam, J., Long, L.H., 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. 3 (2001), 157–163.
19. Corazao-Rozas, P., Guerreschi, P., Jendoubi, M., André, F., Jonneaux, A., Scalbert, C., Garçon, G., Malet-Martino, M., Balayssac, S., Rocchi, S., et al. Mitochondrial oxidative stress is the Achilles heel of melanoma cells resistant to Braf-mutant inhibitor. Oncotarget 4 (2013), 1986–1998.
20. Cramer-Morales, K., Heer, C.D., Mapuskar, K.A., Domann, F.E., SOD2 targeted gene editing by CRISPR/Cas9 yields human cells devoid of MnSOD. Free Radic. Biol. Med. 89 (2015), 379–386.
21. Creagan, E.T., Moertel, C.G., O'Fallon, J.R., Schutt, A.J., O'Connell, M.J., Rubin, J., 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.
22. Dickinson, B.C., Huynh, C., Chang, C.J., A palette of fluorescent probes with varying emission colors for imaging hydrogen peroxide signaling in living cells. J. Am. Chem. Soc. 132 (2010), 5906–5915.
23. Doskey, C.M., van t Erve, T.J., Wagner, B.A., Buettner, G.R., Moles of a substance per cell is a highly informative dosing metric in cell culture. PLoS One, 10, 2015, e0132572.
24. 2: implications for pharmacological ascorbate in cancer therapy. Redox Biol. 10 (2016), 274–284.
25. Du, J., Martin, S.M., Levine, M., Wagner, B.A., Buettner, G.R., Wang, S., Taghiyev, A.F., Du, C., Knudson, C.M., Cullen, J.J., Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer. Clin. Cancer Res. 16 (2010), 509–520.
26. Du, J., Wagner, B.A., Buettner, G.R., Cullen, J.J., Role of labile iron in the toxicity of pharmacological ascorbate. Free Radic. Biol. Med. 84 (2015), 289–295.
27. Du, J., Cieslak, J.A., Welsh, J.L., Sibenaller, Z.A., Allen, B.G., Wagner, B.A., Kalen, A.L., Doskey, C.M., Strother, R.K., Button, A.M., et al. Pharmacological ascorbate radiosensitizes pancreatic cancer. Cancer Res. 75 (2015), 3314–3326.
28. Eisenhauer, E.A., Therasse, P., Bogaerts, J., Schwartz, L.H., Sargent, D., Ford, R., Dancey, J., Arbuck, S., Gwyther, S., Mooney, M., et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 45 (2009), 228–247.
29. Epsztejn, S., Kakhlon, O., Glickstein, H., Breuer, W., Cabantchik, Z.I., Fluorescence analysis of the labile iron pool of mammalian cells. Anal. Biochem. 248 (1997), 31–40.
30. Halliwell, B., Gutteridge, J.M.C., Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 186 (1990), 1–85.
31. Hegi, M.E., Diserens, A.-C., Gorlia, T., Hamou, M.-F., de Tribolet, N., Weller, M., Kros, J.M., Hainfellner, J.A., Mason, W., Mariani, L., et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352 (2005), 997–1003.
32. Ibrahim, W.H., Habib, H.M., Kamal, H., St Clair, D.K., Chow, C.K., Mitochondrial superoxide mediates labile iron level: evidence from Mn-SOD-transgenic mice and heterozygous knockout mice and isolated rat liver mitochondria. Free Radic. Biol. Med. 65C (2013), 143–149.
33. Janmaat, M.L., Rodriguez, J.A., Gallegos-Ruiz, M., Kruyt, F.A.E., Giaccone, G., Enhanced cytotoxicity induced by gefitinib and specific inhibitors of the Ras or phosphatidyl inositol-3 kinase pathways in non-small cell lung cancer cells. Int. J. Cancer 118 (2006), 209–214.
34. Kuiper, C., Vissers, M.C.M., Hicks, K.O., Pharmacokinetic modeling of ascorbate diffusion through normal and tumor tissue. Free Radic. Biol. Med. 77 (2014), 340–352.
35. Kukulj, S., Jaganjac, M., Boranic, M., Krizanac, S., Santic, Z., Poljak-Blazi, M., Altered iron metabolism, inflammation, transferrin receptors, and ferritin expression in non-small-cell lung cancer. Med. Oncol. 27 (2010), 268–277.
36. Liou, G.-Y., Döppler, H., DelGiorno, K.E., Zhang, L., Leitges, M., Crawford, H.C., Murphy, M.P., Storz, P., Mutant Kras-induced mitochondrial oxidative stress in acinar cells upregulates EGFR signaling to drive formation of pancreatic precancerous lesions. Cell Rep 14 (2016), 2325–2336.
37. Liu, L., Duff, K., A technique for serial collection of cerebrospinal fluid from the cisterna magna in mouse. J. Vis. Exp., 2008, 10.3791/960.
38. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J., Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951), 265–275.
39. Ma, Y., Chapman, J., Levine, M., Polireddy, K., Drisko, J., Chen, Q., High-dose parenteral ascorbate enhanced chemosensitivity of ovarian cancer and reduced toxicity of chemotherapy. Sci. Transl. Med., 6, 2014, 222ra18.
40. Macdonald, D.R., Cascino, T.L., Schold, S.C., Cairncross, J.G., Response criteria for phase II studies of supratentorial malignant glioma. J. Clin. Oncol. 8 (1990), 1277–1280.
41. Matsubara, D., Kishaba, Y., Ishikawa, S., Sakatani, T., Oguni, S., Tamura, T., Hoshino, H., Sugiyama, Y., Endo, S., Murakami, Y., et al. Lung cancer with loss of BRG1/BRM, shows epithelial mesenchymal transition phenotype and distinct histologic and genetic features. Cancer Sci. 104 (2013), 266–273.
42. 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 (1985), 137–141.
43. Mojić, M., Bogdanović Pristov, J., Maksimović-Ivanić, D., Jones, D.R., Stanić, M., Mijatović, S., Spasojević, I., Extracellular iron diminishes anticancer effects of vitamin C: an in vitro study. Sci. Rep., 4, 2014, 5955.
44. Monti, D.A., Mitchell, E., Bazzan, A.J., Littman, S., Zabrecky, G., Yeo, C.J., Pillai, M.V., Newberg, A.B., Deshmukh, S., Levine, M., Phase I evaluation of intravenous ascorbic acid in combination with gemcitabine and erlotinib in patients with metastatic pancreatic cancer. PLoS One, 7, 2012, e29794.
45. Moser, J.C., Rawal, M., Wagner, B.A., Du, J., Cullen, J.J., Buettner, G.R., Pharmacological ascorbate and ionizing radiation (IR) increase labile iron in pancreatic cancer. Redox Biol. 2 (2014), 22–27.
46. 2 in vitro and in vivo and reduce menadione-induced DNA injury and cytotoxicity. Am. J. Physiol. 268 (1995), C227–C236.
47. Oberley, L.W., Oberley, T.D., Buettner, G.R., Cell differentiation, aging and cancer: the possible roles of superoxide and superoxide dismutases. Med. Hypotheses 6 (1980), 249–268.
48. Olney, K.E., Du, J., van t Erve, T.J., Witmer, J.R., Sibenaller, Z.A., Wagner, B.A., Buettner, G.R., Cullen, J.J., Inhibitors of hydroperoxide metabolism enhance ascorbate-induced cytotoxicity. Free Radic. Res. 47 (2013), 154–163.
49. Ornstein, L., Disc electrophoresis I. Background and theory. Ann. N. Y. Acad. Sci. 121 (1964), 321–349.
50. Packer, L., Fuehr, K., Low oxygen concentration extends the lifespan of cultured human diploid cells. Nature 267 (1977), 423–425.
51. Padayatty, S.J., Sun, H., Wang, Y., Riordan, H.D., Hewitt, S.M., Katz, A., Wesley, R.A., Levine, M., Vitamin C pharmacokinetics: implications for oral and intravenous use. Ann. Intern. Med. 140 (2004), 533–537.
52. Pantopoulos, K., Mueller, S., Atzberger, A., Ansorge, W., Stremmel, W., Hentze, M.W., Differences in the regulation of iron regulatory protein-1 (IRP-1) by extra- and intracellular oxidative stress. J. Biol. Chem. 272 (1997), 9802–9808.
53. Riordan, N.H., Riordan, H.D., Meng, X., Li, Y., Jackson, J.A., Intravenous ascorbate as a tumor cytotoxic chemotherapeutic agent. Med. Hypotheses 44 (1995), 207–213.
54. Rumsey, S.C., Kwon, O., Xu, G.W., Burant, C.F., Simpson, I., Levine, M., Glucose transporter isoforms GLUT1 and GLUT3 transport dehydroascorbic acid. J. Biol. Chem. 272 (1997), 18982–18989.
55. Sandler, A., Gray, R., Perry, M.C., Brahmer, J., Schiller, J.H., Dowlati, A., Lilenbaum, R., Johnson, D.H., Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N. Engl. J. Med. 355 (2006), 2542–2550.
56. Schiller, J.H., Harrington, D., Belani, C.P., Langer, C., Sandler, A., Krook, J., Zhu, J., Johnson, D.H., Eastern Cooperative Oncology Group, Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N. Engl. J. Med. 346 (2002), 92–98.
57. Simon, R., Freidlin, B., Rubinstein, L., Arbuck, S.G., Collins, J., Christian, M.C., Accelerated titration designs for phase I clinical trials in oncology. J. Natl. Cancer Inst. 89 (1997), 1138–1147.
58. Spitz, D.R., Oberley, L.W., Measurement of MnSOD and CuZnSOD activity in mammalian tissue homogenates. Curr. Protoc. Toxicol., Chapter 7, 2001 Unit 7.5.
59. Spitz, D.R., Dewey, W.C., Li, G.C., Hydrogen peroxide or heat shock induces resistance to hydrogen peroxide in Chinese hamster fibroblasts. J. Cell. Physiol 131 (1987), 364–373.
60. Spitz, D.R., Sim, J.E., Ridnour, L.A., Galoforo, S.S., Lee, Y.J., Glucose deprivation-induced oxidative stress in human tumor cells. A fundamental defect in metabolism?. Ann. N. Y. Acad. Sci. 899 (2000), 349–362.
61. Springer, E.L., Comparative study of the cytoplasmic organelles of epithelial cell lines derived from Hu man carcinomas and nonmalignant tissues. Cancer Res. 40 (1980), 803–817.
62. Storer, B.E., Design and analysis of phase I clinical trials. Biometrics 45 (1989), 925–937.
63. Stupp, R., Mason, W.P., van den Bent, M.J., Weller, M., Fisher, B., Taphoorn, M.J.B., Belanger, K., Brandes, A.A., Marosi, C., Bogdahn, U., et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352 (2005), 987–996.
64. Sunaga, N., Shames, D.S., Girard, L., Peyton, M., Larsen, J.E., Imai, H., Soh, J., Sato, M., Yanagitani, N., Kaira, K., et al. Knockdown of oncogenic KRAS in non-small cell lung cancers suppresses tumor growth and sensitizes tumor cells to targeted therapy. Mol. Cancer Ther. 10 (2011), 336–346.
65. Szatrowski, T.P., Nathan, C.F., Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 51 (1991), 794–798.
66. Torti, S.V., Torti, F.M., Iron and cancer: more ore to be mined. Nat. Rev. Cancer 13 (2013), 342–355.
67. Ueda, M., Toji, E., Nunobiki, O., Izuma, S., Okamoto, Y., Torii, K., Noda, S., Mutational analysis of the BRAF gene in human tumor cells. Hum. Cell 21 (2008), 13–17.
68. Verrax, J., Calderon, P.B., Pharmacologic concentrations of ascorbate are achieved by parenteral administration and exhibit antitumoral effects. Free Radic. Biol. Med. 47 (2009), 32–40.
69. Vislisel, J.M., Schafer, F.Q., Buettner, G.R., A simple and sensitive assay for ascorbate using a plate reader. Anal. Biochem. 365 (2007), 31–39.
70. Welsh, J.L., Wagner, B.A., van't Erve, T.J., Zehr, P.S., Berg, D.J., Halfdanarson, T.R., Yee, N.S., Bodeker, K.L., Du, J., Roberts, L.J. 2nd, 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. 71 (2013), 765–775.
71. Witmer, J.R., Wetherell, B.J., Wagner, B.A., Du, J., Cullen, J.J., Buettner, G.R., Direct spectrophotometric measurement of supra-physiological levels of ascorbate in plasma. Redox Biol. 8 (2016), 298–304.
72. Yun, J., Mullarky, E., Lu, C., Bosch, K.N., Kavalier, A., Rivera, K., Roper, J., Chio, I.I.C., Giannopoulou, E.G., Rago, C., et al. Vitamin C selectively kills KRAS and BRAF mutant colorectal cancer cells by targeting GAPDH. Science 350 (2015), 1391–1396.
73. Zwacka, R.M., Dudus, L., Epperly, M.W., Greenberger, J.S., Engelhardt, J.F., Redox gene therapy protects human IB-3 lung epithelial cells against ionizing radiation-induced apoptosis. Hum. Gene Ther. 9 (1998), 1381–1386.