Spatio-temporal changes in glutathione and thioredoxin redox couples during ionizing radiation-induced oxidative stress regulate tumor radio-resistance

Free Radical Research

Volumn 49, Issue 10, 2015, Pages 1218-1232

  Patwardhan, R S ^a   Sharma, D ^a   Checker, R ^a   Thoh, M ^a   Sandur, S K ^a  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

Author keywords

antioxidant; ionizing radiation; oxidative stress; radio sensitivity; redox homeostasis

Indexed keywords

GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; THIOREDOXIN REDUCTASE; TRANSCRIPTION FACTOR NRF2; DNA; NFE2L2 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; THIOL DERIVATIVE; TUMOR PROTEIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IONIZING RADIATION; METABOLISM; OXIDATIVE STRESS; RADIATION EXPOSURE; RADIOSENSITIVITY; RESPIRATORY BURST; SPATIOTEMPORAL ANALYSIS; T CELL LYMPHOMA; TUMOR CELL; ACTIVE TRANSPORT; ADVERSE EFFECTS; ANTAGONISTS AND INHIBITORS; APOPTOSIS; DNA DAMAGE; GAMMA RADIATION; GENETIC TRANSFECTION; GENETICS; HOMEOSTASIS; JURKAT CELL LINE; MITOCHONDRION; MONONUCLEAR CELL; OXIDATION REDUCTION REACTION; PHYSIOLOGY; RADIATION RESPONSE; RADIATION TOLERANCE; RNA INTERFERENCE; TIME FACTOR;

ACTIVE TRANSPORT, CELL NUCLEUS; APOPTOSIS; DNA DAMAGE; DNA, NEOPLASM; GAMMA RAYS; GLUTATHIONE; HOMEOSTASIS; HUMANS; JURKAT CELLS; LEUKOCYTES, MONONUCLEAR; MITOCHONDRIA; NADPH OXIDASE; NEOPLASM PROTEINS; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; RADIATION TOLERANCE; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SULFHYDRYL COMPOUNDS; THIOREDOXINS; TIME FACTORS; TRANSFECTION;

EID: 84940036765     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2015.1056180     Document Type: Article

References (73)

1. Roos WP, Kaina B. DNA damage-induced cell death: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett 2013; 332: 237-248.
2. Lomax ME, Folkes LK, ONeill P. Biological consequences of radiation-induced DNA damage: relevance to radiotherapy. Clin Oncol (R Coll Radiol) 2013; 25: 578-585.
3. Vignard J, Mirey G, Salles B. Ionizing-radiation induced DNA double-strand breaks: a direct and indirect lighting up. Radiother Oncol 2013; 108: 362-369.
4. Ravanat JL, Breton J, Douki T, Gasparutto D, Grand A, Rachidi W, Sauvaigo S. Radiation-mediated formation of complex damage to DNA: a chemical aspect overview. Br J Radiol 2014; 87: 20130715.
5. Schumacker PT. Reactive oxygen species in cancer: a dance with the devil. Cancer Cell 2015; 27: 156-157.
6. Lee HC, Kim DW, Jung KY, Park IC, Park MJ, Kim MS, et al. Increased expression of antioxidant enzymes in radioresistant variant from U251 human glioblastoma cell line. Int J Mol Med 2004; 13: 883-887.
7. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009; 458: 780-783.
8. Jones DP, Liang Y. Measuring the poise of thiol/disulfide couples in vivo. Free Radic Biol Med 2009; 47: 1329-1338.
9. Lillig CH, Berndt C. Glutaredoxins in thiol/disulfide exchange. Antioxid Redox Signal 2013; 18: 1654-1665.
10. Dalle-Donne I, Rossi R, Giustarini D, Colombo R, Milzani A. S-glutathionylation in protein redox regulation. Free Radic Biol Med 2007; 43: 883-898.
11. Wouters MA, Fan SW, Haworth NL. Disulfides as redox switches: from molecular mechanisms to functional significance. Antioxid Redox Signal 2010; 12: 53-91.
12. Zhang H, Forman HJ. Glutathione synthesis and its role in redox signaling. Semin Cell Dev Biol 2012; 23: 722-728.
13. Anathy V, Roberson EC, Guala AS, Godburn KE, Budd RC, Janssen-Heininger YM. Redox-based regulation of apoptosis: S-glutathionylation as a regulatory mechanism to control cell death. Antioxid Redox Signal 2012; 16: 496-505.
14. Cheng Z, Zhang J, Ballou DP, Williams CH, Jr. Reactivity of thioredoxin as a protein thiol-disulfide oxidoreductase. Chem Rev 2011; 111: 5768-5783.
15. Rigobello MP, Folda A, Dani B, Menabo R, Scutari G, Bindoli A. Gold(I) complexes determine apoptosis with limited oxidative stress in Jurkat T cells. Eur J Pharmacol 2008; 582: 26-34.
16. Ahsan MK, Lekli I, Ray D, Yodoi J, Das DK. Redox regulation of cell survival by the thioredoxin superfamily: an implication of redox gene therapy in the heart. Antioxid Redox Signal 2009; 11: 2741-2758.
17. Holmgren A. Thioredoxin System in Cell Death Progression. Antioxid Redox Signal 2012; 17: 10.
18. Cox AG, Brown KK, Arner ES, Hampton MB. The thioredoxin reductase inhibitor auranofin triggers apoptosis through a Bax/Bak-dependent process that involves peroxiredoxin 3 oxidation. Biochem Pharmacol 2008; 76: 1097-1109.
19. Manoharan R, Seong HA, Ha H. Thioredoxin inhibits MPK38-induced ASK1, TGF-beta, and p53 function in a phosphorylation-dependent manner. Free Radic Biol Med 2013; 63: 313-324.
20. Patwardhan RS, Checker R, Sharma D, Sandur SK, Sainis KB. Involvement of ERK-Nrf-2 signaling in ionizing radiation induced cell death in normal and tumor cells. PLoS One 2013; 8: e65929.
21. Jayakumar S, Kunwar A, Sandur SK, Pandey BN, Chaubey RC. Differential response of DU145 and PC3 prostate cancer cells to ionizing radiation: role of reactive oxygen species, GSH and Nrf2 in radiosensitivity. Biochim Biophys Acta 2014; 1840: 485-494.
22. Tian H, Gao Z, Li H, Zhang B, Wang G, Zhang Q, et al. DNA damage response-a double-edged sword in cancer prevention and cancer therapy. Cancer Lett 2015; 358: 8-16.
23. Gupta A, Hunt CR, Chakraborty S, Pandita RK, Yordy J, Ramnarain DB, et al. Role of 53BP1 in the regulation of DNA double-strand break repair pathway choice. Radiat Res 2014; 181: 1-8.
24. Sasatani M, Xu Y, Kawai H, Cao L, Tateishi S, Shimura T, et al. RAD18 Activates the G2/M Checkpoint through DNA Damage Signaling to Maintain Genome Integrity after Ionizing Radiation Exposure. PLoS One 2015; 10: e0117845.
25. Desai S, Kumar A, Laskar S, Pandey BN. Differential roles of ATF-2 in survival and DNA repair contributing to radioresistance induced by autocrine soluble factors in A549 lung cancer cells. Cell Signal 2014; 26: 2424-2435.
26. Gaziev AI. [Pathways for maintenance of mitochondrial DNA integrity and mitochondrial functions in cells exposed to ionizing radiation]. Radiats Biol Radioecol 2013; 53: 117-136.
27. Alexandrou AT, Li JJ. Cell cycle regulators guide mitochondrial activity in radiation-induced adaptive response. Antioxid Redox Signal 2014; 20: 1463-1480.
28. Birch-Machin MA, Russell EV, Latimer JA. Mitochondrial DNA damage as a biomarker for ultraviolet radiation exposure and oxidative stress. Br J Dermatol 2013; 169 Suppl 2: 9-14.
29. Holley AK, Miao L, St Clair DK, St Clair WH. Redox-modulated phenomena and radiation therapy: the central role of superoxide dismutases. Antioxid Redox Signal 2014; 20: 1567-1589.
30. Patwardhan RS, Sharma D, Checker R, Sandur SK. Mitigation of radiation-induced hematopoietic injury via regulation of cellular MAPK/phosphatase levels and increasing hematopoietic stem cells. Free Radic Biol Med 2014; 68: 52-64.
31. Kalyanaraman B, Darley-Usmar V, Davies KJ, Dennery PA, Forman HJ, Grisham MB, et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 2012; 52: 1-6.
32. Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med 2007; 43: 995-1022.
33. Robinson KM, Janes MS, Beckman JS. The selective detection of mitochondrial superoxide by live cell imaging. Nat Protoc 2008; 3: 941-947.
34. Sahaf B, Heydari K, Herzenberg LA. Lymphocyte surface thiol levels. Proc Natl Acad Sci USA 2003; 100: 4001-4005.
35. Rahman I, Kode A, Biswas SK. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 2006; 1: 3159-3165.
36. Jones DP. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol 2002; 348: 93-112.
37. Aebi H, Bergmeyer HU. (Ed.), Catalase. in Methods of Enzymatic Analysis (3rd Edition), Weinheim: Verlag Chemie; 1983. pp. 273-286.
38. Lawrence RA, Burk RF. Glutathione peroxidase activity in seleniumdecient rat liver. Biochem Biophys Res Commun 1976; 71: 952-958.
39. Kumar S, Holmgren A. Induction of thioredoxin, thioredoxin reductase and glutaredoxin activity in mouse skin by TPA, a calcium ionophore and other tumor promoters. Carcinogenesis 1999; 20: 1761-1767.
40. Holmgren A, Bjornstedt M. Thioredoxin and thioredoxin reductase. Methods Enzymol 1995; 252: 199-208.
41. Kornberg A, Horecker BL. Glucose-6-Phosphate Dehydrogenase. Methods Enzymol 1955; 1: 323.
42. Sandur SK, Ichikawa H, Sethi G, Ahn KS, Aggarwal BB. Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) suppresses NF-kappaB activation and NF-kappaB-regulated gene products through modulation of p65 and IkappaBalpha kinase activation, leading to potentiation of apoptosis induced by cytokine and chemotherapeutic agents. J Biol Chem 2006; 281: 17023-17033.
43. Saenko Y, Cieslar-Pobuda A, Skonieczna M, Rzeszowska-Wolny J. Changes of reactive oxygen and nitrogen species and mitochondrial functioning in human K562 and HL60 cells exposed to ionizing radiation. Radiat Res 2013; 180: 360-366.
44. Bryan HK, Olayanju A, Goldring CE, Park BK. The Nrf2 cell defence pathway: Keap1-dependent and-independent mechanisms of regulation. Biochem Pharmacol 2013; 85: 705-717.
45. Arner ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 2000; 267: 6102-6109.
46. Nishiyama A, Masutani H, Nakamura H, Nishinaka Y, Yodoi J. Redox regulation by thioredoxin and thioredoxin-binding proteins. IUBMB Life 2001; 52: 29-33.
47. Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, Hay RT. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res 1992; 20: 3821-3830.
48. Xiong Y, Uys JD, Tew KD, Townsend DM. S-glutathionylation: from molecular mechanisms to health outcomes. Antioxid Redox Signal 2011; 15: 233-270.
49. Hayes JD, Dinkova-Kostova AT. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem Sci 2014; 39: 199-218.
50. Holmgren A, Lu J. Thioredoxin and thioredoxin reductase: current research with special reference to human disease. Biochem Biophys Res Commun 2010; 396: 120-124.
51. Lu J, Holmgren A. Thioredoxin system in cell death progression. Antioxid Redox Signal 2012; 17: 1738-1747.
52. Kavanagh JN, Redmond KM, Schettino G, Prise KM. DNA double strand break repair: a radiation perspective. Antioxid Redox Signal 2013; 18: 2458-2472.
53. Mondello C, Smirnova A, Giulotto E. Gene amplification, radiation sensitivity and DNA double-strand breaks. Mutat Res 2010; 704: 29-37.
54. Lu J, Holmgren A. The thioredoxin antioxidant system. Free Radic Biol Med 2014; 66: 75-87.
55. Aquilano K, Baldelli S, Ciriolo MR. Glutathione: new roles in redox signaling for an old antioxidant. Front Pharmacol 2014; 5: 196.
56. Bae YS, Oh H, Rhee SG, Yoo YD. Regulation of reactive oxygen species generation in cell signaling. Mol Cells 2011; 32: 491-509.
57. Go YM, Jones DP. Thiol/disulfide redox states in signaling and sensing. Crit Rev Biochem Mol Biol 2013; 48: 173-181.
58. Yin F, Sancheti H, Cadenas E. Mitochondrial thiols in the regulation of cell death pathways. Antioxid Redox Signal 2012; 17: 1714-1727.
59. Flohe L. Changing paradigms in thiology from antioxidant defense toward redox regulation. Methods Enzymol 2010; 473: 1-39.
60. Iwanaga M, Mori K, Iida T, Urata Y, Matsuo T, Yasunaga A, et al. Nuclear factor kappa B dependent induction of gamma glutamylcysteine synthetase by ionizing radiation in T98G human glioblastoma cells. Free Radic Biol Med 1998; 24: 1256-1268.
61. Toledano MB, Delaunay-Moisan A, Outten CE, Igbaria A. Functions and cellular compartmentation of the thioredoxin and glutathione pathways in yeast. Antioxid Redox Signal 2013; 18: 1699-1711.
62. Franco R, Cidlowski JA. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ 2009; 16: 1303-1314.
63. Grek CL, Zhang J, Manevich Y, Townsend DM, Tew KD. Causes and consequences of cysteine S-glutathionylation. J Biol Chem 2013; 288: 26497-26504.
64. Heiss EH, Schachner D, Zimmermann K, Dirsch VM. Glucose availability is a decisive factor for Nrf2-mediated gene expression. Redox Biol 2013; 1: 359-365.
65. Watanabe R, Nakamura H, Masutani H, Yodoi J. Anti-oxidative, anti-cancer and anti-inflammatory actions by thioredoxin 1 and thioredoxin-binding protein-2. Pharmacol Ther 2010; 127: 261-270.
66. Kodali VK, Thorpe C. Oxidative protein folding and the Quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid Redox Signal 2010; 13: 1217-1230.
67. Arner ES, Holmgren A. The thioredoxin system in cancer. Semin Cancer Biol 2006; 16: 420-426.
68. Sengupta R, Holmgren A. Thioredoxin and glutaredoxin-mediated redox regulation of ribonucleotide reductase. World J Biol Chem 2014; 5: 68-74.
69. Collet JF, Messens J. Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 2010; 13: 1205-1216.
70. Go YM, Jones DP. Redox control systems in the nucleus: mechanisms and functions. Antioxid Redox Signal 2010; 13: 489-509.
71. Hansen JM, Watson WH, Jones DP. Compartmentation of Nrf-2 redox control: regulation of cytoplasmic activation by glutathione and DNA binding by thioredoxin-1. Toxicol Sci 2004; 82: 308-317.
72. Liu Y, Li Y, Yu S, Zhao G. Recent advances in the development of thioredoxin reductase inhibitors as anticancer agents. Curr Drug Targets 2012; 13: 1432-1444.
73. Lee S, Kim SM, Lee RT. Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance. Antioxid Redox Signal 2013; 18: 1165-1207.