Tumor cells have decreased ability to metabolize H2O2: Implications for pharmacological ascorbate in cancer therapy

Redox Biology

Volumn 10, Issue , 2016, Pages 274-284

  Doskey, Claire M ^a   Buranasudja, Visarut ^a   Wagner, Brett A ^b   Wilkes, Justin G ^a   Du, Juan ^a   Cullen, Joseph J ^a,b,c   Buettner, Garry R ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; CATALASE; HYDROGEN PEROXIDE; ANTIOXIDANT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER THERAPY; CELL LINE; CELL METABOLISM; CELL SURVIVAL; CLONOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG RESPONSE; ED50; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; A-549 CELL LINE; ANIMAL; DRUG EFFECTS; DRUG SCREENING; HEP-G2 CELL LINE; METABOLISM; OXIDATIVE STRESS; PANCREAS TUMOR; TUMOR CELL LINE;

A549 CELLS; ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; CATALASE; CELL LINE, TUMOR; HEP G2 CELLS; HUMANS; HYDROGEN PEROXIDE; MICE; OXIDATIVE STRESS; PANCREATIC NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84994762982     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2016.10.010     Document Type: Article

References (69)

1. [1] Chen, Q., Espey, M.G., Krishna, M.C., Mitchell, J.B., Corpe, C.P., Buettner, G.R., Shacter, E., Levine, M., Ascorbic acid at pharmacologic concentrations selectively kills cancer cells: ascorbic acid as a pro-drug for hydrogen peroxide delivery to tissues. Proc. Natl. Acad. Sci. USA 102 (2005), 13604–13609 (PMID: 16157892).
2. [2] 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., Levine, M., Ascorbic acid in pharmacologic concentrations: a pro-drug for selective delivery of ascorbate radical and hydrogen peroxide to extracellular fluid in vivo. Proc. Natl. Acad. Sci. USA 104 (2007), 8749–8754 (PMID: 17502596).
3. [3] Du, J., Martin, S.M., Levine, M., Wagner, B.A., Buettner, G.R., Wang, S.H., Taghiyev, A.F., Du, C., Knudson, C.M., Cullen, J.J., Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer. Clin. Cancer Res. 16:2 (2010), 509–520 (PMID: 20068072).
4. 2 generation. Cancer Res. 73:16 (2013), 5232–5241 (PMID: 23764544).
5. [5] Sestili, P., Brandi, G., Brambilla, L., Cattabeni, F., Cantoni, O., Hydrogen peroxide mediates the killing of U937 tumor cells elicited by pharmacologically attainable concentrations of ascorbic acid: cell death prevention by extracellular catalase or catalase from cocultured erythrocytes or fibroblasts. J. Pharm. Exp. Ther. 277:3 (1996), 1719–1725 (PMID: 8667243).
6. [6] 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 32:105 (2008), 11105–11109 (PMID: 18678913).
7. [7] Tian, J., Peehl, D.M., Knox, S.J., Metalloporphyrin synergizes with ascorbic acid to inhibit cancer cell growth through fenton chemistry. Cancer Biother. Radiopharm. 25:4 (2010), 439–448 (PMID: 20735206).
8. [8] Espey, M.G., Chen, P., Chalmers, B., Drisko, J., Sun, A.Y., Levine, M., Chen, Q., Pharmacologic ascorbate synergizes with gemcitabine in preclinical models of pancreatic cancer. Free Radic. Biol. Med. 50:11 (2011), 1610–1619 (PMID: 21402145).
9. [9] Ranzato, E., Biffo, S., Burlando, B., Selective ascorbate toxicity in malignant mesothelioma: a redox Trojan mechanism. Am. J. Respir. Cell Mol. Biol. 44:1 (2011), 108–117 (PMID: 20203294).
10. [10] Chen, P., Yu, J., Chalmers, B., Drisko, J., Yang, J., Li, B., Chen, Q., Pharmacological ascorbate induces cytotoxicity in prostate cancer cells through ATP depletion and induction of autophagy. Anticancer Drugs 23:4 (2012), 437–444 (PMID: 22205155).
11. [11] Klingelhoeffer, C., Kämmerer, U., Koospal, M., Mühling, B., Schneider, M., Kapp, M., Kübler, A., Germer, C.T., Otto, C., Natural resistance to ascorbic acid induced oxidative stress is mainly mediated by catalase activity in human cancer cells and catalase-silencing sensitizes to oxidative stress. BMC Complement. Alter. Med., 12(61), 2012 (PMID: 22551313).
12. [12] Shatzer, A.N., Espey, M.G., Chavez, M., Tu, H., Levine, M., Cohen, J.I., Ascorbic acid kills Epstein-Barr virus positive Burkitt lymphoma cells and Epstein-Barr virus transformed B-cells in vitro, but not in vivo. Leuk. Lymphoma 54:5 (2013), 1069–1078 (PMID: 23067008).
13. [13] 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(222), 2014 222ra18 (PMID: 24500406).
14. 2 in red blood cells. Antioxid. Redox Signal. 12:11 (2010), 1235–1246 (PMID: 2007018).
15. [15] Du, J., Cullen, J.J., Buettner, G.R., Ascorbic acid: chemistry, biology and the treatment of cancer. Biochim. Biophys. Acta: Rev. Cancer 1826 (2012), 443–457 (PMID: 22728050).
16. [16] Johnson, R.M., HoY-S, Yu.D.-Y., Kuypers, F.A., Ravindranath, Y., Goyette, G.W., The effects of disruption of genes for peroxiredoxin-2, glutathione peroxidase-1, and catalase on erythrocyte oxidative metabolism. Free Radic. Biol. Med. 48 (2010), 519–525 (PMID: 19969073).
17. [17] Benfeitas, R., Selvaggio, G., Antunes, F., Coelho, P.M., Salvador, A., Hydrogen peroxide metabolism and sensing in human erythrocytes: a validated kinetic model and reappraisal of the role of peroxiredoxin II. Free Radic. Biol. Med. 74 (2014), 35–49 (PMID: 24952139).
18. [18] Nicholls, P., Activity of catalase in the red cell. Biochim Biophys. Acta 99 (1965), 286–297 (PMID: 14336065).
19. [19] Cohen, G., Hochstein, P., Glutathione peroxidase: the primary agent for the elimination of hydrogen peroxide in erythrocytes. Biochemistry 2 (1963), 1420–1428 (PMID: 14093920).
20. 2. Arch. Biochem. Biophys. 210:2 (1981), 505–516 (PMID: 7305340).
21. [21] Makino, N., Mochizuki, Y., Bannai, S., Sugita, Y., Kinetic studies on the removal of extracellular hydrogen peroxide by cultured fibroblasts. J. Biol. Chem. 269:2 (1994), 1020–1025 (PMID: 8288557).
22. [22] Sasaki, K., Bannai, S., Makino, N., Kinetics of hydrogen peroxide elimination by human umbilical vein endothelial cells in culture. Biochim. Biophys. Acta 1380:2 (1998), 275–288 (PMID: 9565698).
23. [23] Winterbourn, C.C., Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4:5 (2008), 278–286 (PMID: 18421291).
24. 2 permeation through cytoplasmic and peroxisomal membranes: comparisons with experimental data. Biochim. Biophys. Acta 1673 (2004), 149–159 (PMID: 15279886).
25. [25] Mitozo, P.A., de Souza, L.F., Loch-Neckel, G., Flesch, S., Maris, A.F., Figueiredo, C.P., Dos Santos, A.R., Farina, M., Dafre, A.L., A study of the relative importance of the peroxiredoxin-, catalase-, and glutathione-dependent systems in neural peroxide metabolism. Free Radic. Biol. Med. 51:1 (2011), 69–77 (PMID: 21440059).
26. 2 levels in erythrocytes. Free Radic. Biol. Med. 39:11 (2005), 1407–1417 (PMID: 16274876).
27. [27] De Duve, C., Baudhuin, P., Peroxisomes (microbodies and related particles). Physiol. Rev. 46:2 (1966), 323–357 (PMID: 5325972).
28. [28] Marklund, S.L., Westman, N.G., Lundgreen, E., Roos, G., Copper- and zinc-containing superoxide dismutase, catalase, and glutathione peroxidase in normal and neoplastic cell lines and normal human tissues. Cancer Res. 42 (1982), 1955–1961 (PMID: 7066906).
29. [29] Oberley, T.D., Oberley, L.W., Antioxidant enzyme levels in cancer. Histol. Histopathol. 12 (1997), 525–535 (PMID: 9151141).
30. [30] Oberley, L.W., Buettner, G.R., The role of superoxide dismutase in cancer: a review. Cancer Res. 39 (1979), 1141–1149 (PMID: 217531).
31. [31] Roy, I., Zimmerman, N.P., Mackinnon, A.C., Tsai, S., Evans, D.B., Dwinell, M.B., CXCL12 chemokine expression suppresses human pancreatic cancer growth and metastasis. PLoS One, 9(3), 2014, e90400 (PMID: 24594697).
32. [32] Du, J., Cieslak, J.A. 3rd, Welsh, J.L., Sibenaller, Z.A., Allen, B.G., Wagner, B.A., Kalen, A.L., Doskey, C.M., Strother, R.K., Button, A.M., Mott, S.L., Smith, B., Tsai, S., Mezhir, J., Goswami, P.C., Spitz, D.R., Buettner, G.R., Cullen, J.J., Pharmacological ascorbate radiosensitizes pancreatic cancer. Cancer Res. 75:16 (2015), 3314–3326 (PMID: 26081808).
33. [33] Wagner, B.A., Witmer, J.R., van ‘t Erve, T.J., Buettner, G.R., An assay for the rate of removal of extracellular hydrogen peroxide by cells. Redox Biol. 1 (2013), 210–217 (PMID: 23936757).
34. [34] Aebi, H., Catalase in vitro. Methods Enzym. 105 (1984), 121–126 (PMID: 6727660).
35. [35] Bonnichsen, R., Blood catalase. Methods Enzym. 2 (1955), 781–784.
36. [36] Higashi, T., Peters, T. Jr., Studies of rat liver catalase. I. Combined immunochemical and enzymatic determination of catalase in liver cell fractions. J. Biol. Chem. 238 (1963), 3945–3951 (PMID: 14086728).
37. [37] Sies, H., Bücher, T., Oshino, N., Chance, B., Heme occupancy of catalase in hemoglobin-free perfused rat liver and of isolated rat liver catalase. Arch. Biochem. Biophys. 154:1 (1973), 106–116 (PMID: 4689773).
38. [38] Chance, B., Sies, H., Boveris, A., Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:3 (1979), 527–605 (PMID: 37532).
39. [39] Furda, A., Santos, J.H., Meyer, J.N., Van Houten, B., Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells. Methods Mol. Biol. 1105 (2014), 419–437 (PMID: 24623245).
40. [40] Van Houten, B., Cheng, S., Chen, Y., Measuring gene-specific nucleotide excision repair in human cells using quantitative amplification of long targets from nanogram quantities of DNA. Mutat. Res. 460:2 (2000), 81–94 (PMID: 10882849).
41. [41] Salazar, J.J., Van Houten, B., Preferential mitochondrial DNA injury caused by glucose oxidase as a steady generator of hydrogen peroxide in human fibroblasts. Mutat. Res. 385:2 (1997), 139–149 (PMID: 9447235).
42. [42] Euhus, D.M., Hudd, C., LaRegina, M.C., Johnson, F.E., Tumor measurement in the nude mouse. J. Surg. Oncol. 31:4 (1986), 229–234 (PMID: 3724177).
43. [43] Wagner, B.A., Venkataraman, S., Buettner, G.R., The rate of oxygen utilization by cells. Free Radic. Biol. Med 51 (2011), 700–712 (PMID: 21664270).
44. [44] Murphy, M.P., How mitochondria produce reactive oxygen species. Biochem J. 417:1 (2009), 1–13 (PMID: 19061483).
45. [45] 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 47:3 (2013), 154–163 (PMID: 23205739).
46. 2 in cells and thereby their biological state. Free Radic. Biol. Med. 41 (2006), 1338–1350 (PMID: 17015180).
47. [47] De Duve, C., The separation and characterization of subcellular particles. Harvey Lect. 59 (1965), 49–87 (PMID: 5337823).
48. [48] 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(7), 2015, e0132572 (PMID: 26172833).
49. 2-resistant Chinese hamster fibroblast cell lines. Arch. Biochem Biophys. 279 (1990), 249–260 (PMID:2350176).
50. 2 in cell cultures: impact of cell concentration and exposure time. Free Radic. Biol. Med 49 (2010), 1298–1305 (PMID: 20673847).
51. 2: a quantitative comparison between continuous low-dose and one-time high-dose treatments. Free Radic. Biol. Med. 60 (2013), 325–335 (PMID: 23485584).
52. [52] Du, J., Cieslak, J.A. 3rd, Welsh, J.L., Sibenaller, Z.A., Allen, B.G., Wagner, B.A., Kalen, A.L., Doskey, C.M., Strother, R.K., Button, A.M., Mott, S.L., Smith, B., Tsai, S., Mezhir, J., Goswami, P.C., Spitz, D.R., Buettner, G.R., Cullen, J.J., Pharmacological ascorbate radiosensitizes pancreatic cancer. Cancer Res. 75:16 (2015), 3314–3326 (PMID: 26081808).
53. [53] Martin, D.S., Bertino, J.R., Koutcher, J.A., ATP depletion + pyrimidine depletion can markedly enhance cancer therapy: fresh insight for a new approach. Cancer Res. 60:24 (2000), 6776–6783 (PMID: 11156364).
54. [54] Zong, W.X., Ditsworth, D., Bauer, D.E., Wang, Z.Q., Thompson, C.B., Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 18:11 (2004), 1272–1282, 10.1101/gad.1199904 (PMID: 15145826).
55. [55] Herst, P.M., Broadley, K.W., Harper, J.L., McConnell, M.J., Pharmacological concentrations of ascorbate radiosensitize glioblastoma multiforme primary cells by increasing oxidative DNA damage and inhibiting G2/M arrest. Free Radic. Biol. Med. 52:8 (2012), 1486–1493 (PMID: 22342518).
56. [56] Castro, M.L., McConnell, M.J., Herst, P.M., Radiosensitisation 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. 74 (2014), 200–209 (PMID: 24992837).
57. [57] Cieslak, J.A., Strother, R.K., Rawal, M., Du, J., Doskey, C.M., Schroeder, S.R., Button, A., Wagner, B.A., Buettner, G.R., Cullen, J.J., Manganoporphyrins and ascorbate enhance gemcitabine cytotoxicity in pancreatic cancer. Free Radic. Biol. Med. 83 (2015), 227–237 (PMID: 25725418).
58. [58] Uetaki, M., Tabata, S., Nakasuka, F., Soga, T., Tomita, M., Metabolomic alterations in human cancer cells by vitamin C-induced oxidative stress. Sci. Rep., 5, 2015, 13896 (PMID: 26350063).
59. [59] Yun, J., Mullarky, E., Lu, C., Bosch, Kavalier, A., Rivera, K., Roper, J., Chio, I.I.C., Giannopoulou, E.G., Rago, C., Muley, A., Asara, J.M., Paik, J., Elemento, O., Chen, Z., Pappin, D.J., Dow, L.E., Papadopoulos, N., Gross, S.S., Cantley, L.C., Vitamin C selectively kills KRAS and BRAF mutant colorectal cancer cells by targeting GAPDH. Science 350:6266 (2015), 1391–1396 (PMID: 26541605).
60. [60] Du, J., Wagner, B.A., Buettner, G.R., Cullen, J.J., The role of labile iron in the toxicity of pharmacological ascorbate. Free Radic. Biol. Med. 84 (2015), 289–295 (PMID: 25857216).
61. [61] 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 (PMID: 25092529).
62. [62] Schafer, F.Q., Buettner, G.R., Redox state of the cell as viewed though the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30 (2001), 1191–1212 (PMID: 11368918).
63. [63] 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, Drisko, J., Levine, M., Buettner, G.R., Cullen, J.J., 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. 71:3 (2013), 765–775, 10.1007/s00280-013-2070-8 (PMID: 23381814).
64. [64] J. Cullen, D. Berg, J. Buatti, G. Buettner, M. Smith, C. Anderson, W. Sun, B. Allen, W. Rockey, D. Spitz, B. Wagner, S. Schroeder, R. Hohl, Gemcitabine, ascorbate, and radiation therapy for pancreatic cancer, Phase 1, at The University of Iowa, (Start date 01/2014) (NCT01852890) 〈http://clinicaltrials.gov/ct2/show/NCT01852890〉.
65. [65] Scheit, K., Bauer, G., Direct and indirect inactivation of tumor cell protective catalase by salicylic acid and anthocyanidins reactivated intracellular ROS signaling and allows for synergistic effects. Carcinogenesis 36:3 (2015), 400–411 (PMID: 25653236).
66. [66] Scheit, K., Bauer, G., Synergistic effects between catalase inhibitors and modulators of nitric oxide metabolism on tumor cell apoptosis. Anticancer Res. 34 (2014), 5337–5350 (PMID: 25275027).
67. [67] Yakes, F.M., Van Houten, B., Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. USA 94:2 (1997), 514–519 (PMID: 9012815).
68. [68] Cline, S.D., Mitochondrial DNA damage and its consequences for mitochondrial gene expression. Biochim. Biophys. Acta 1819:9–10 (2012), 979–991 (PMID: 22728831).
69. [69] Mini, E., Nobili, S., Caciagli, B., Landini, I., Mazzei, T., Cellular pharmacology of gemcitabine. Ann. Oncol. 17:Suppl 5 (2016), v7–v12 (PMID: 16807468).