Loss of C/EBPδ enhances IR-induced cell death by promoting oxidative stress and mitochondrial dysfunction

Free Radical Biology and Medicine

Volumn 99, Issue , 2016, Pages 296-307

  Banerjee, Sudip ^a   Aykin Burns, Nukhet ^a   Krager, Kimberly J ^a   Shah, Sumit K ^a   Melnyk, Stepan B ^b   Hauer Jensen, Martin ^a,c   Pawar, Snehalata A ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b ARKANSAS CHILDREN S HOSPITAL RESEARCH INSTITUTE   (United States)

^c CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

Author keywords

CCAAT enhancer binding protein delta; Glutathione; Ionizing radiation; Mitochondrial dysfunction; Oxidative stress; Reactive oxygen species

Indexed keywords

4 HYDROXYNONENAL; ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; BUTHIONINE SULFOXIMINE; CATALASE; CCAAT ENHANCER BINDING PROTEIN DELTA; COPPER ZINC SUPEROXIDE DISMUTASE; CYSTEINE; GLUTATHIONE; GLUTATHIONE DISULFIDE; MACROGOL; METHIONINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; 4-HYDROXY-2-NONENAL; ALDEHYDE; CATALASE-POLYETHYLENE GLYCOL; CEBPD PROTEIN, MOUSE; DNA; MACROGOL DERIVATIVE; POLYETHYLENE GLYCOL-SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BIOENERGY; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CLONOGENESIS; CLONOGENIC ASSAY; CONTROLLED STUDY; EMBRYO; FLOW CYTOMETRY; GAMMA RADIATION; IMMUNOBLOTTING; IONIZING RADIATION; KNOCKOUT MOUSE; LIPID PEROXIDATION; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TOXICITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RADIATION EXPOSURE; RADIATION INJURY; RADIATION PROTECTION; RADIATION RESPONSE; RADIOSENSITIVITY; WILD TYPE; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CYTOLOGY; DEFICIENCY; DOUBLE STRANDED DNA BREAK; DRUG EFFECTS; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; MAMMALIAN EMBRYO; METABOLISM; MITOCHONDRION; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION;

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; ALDEHYDES; ANIMALS; APOPTOSIS; BUTHIONINE SULFOXIMINE; CATALASE; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; DNA; DNA BREAKS, DOUBLE-STRANDED; DOSE-RESPONSE RELATIONSHIP, RADIATION; EMBRYO, MAMMALIAN; FIBROBLASTS; GAMMA RAYS; GENE EXPRESSION REGULATION; GLUTATHIONE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; OXIDATIVE STRESS; POLYETHYLENE GLYCOLS; PRIMARY CELL CULTURE; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84983786179     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.08.022     Document Type: Article

References (61)

1. [1] Hall E. J. a. G., A.J., Radiobiology for the Radiologist,. 6th edn, 2006.
2. [2] Andreassen, C.N., lsner, J., Genetic variants and normal tissue toxicity after radiotherapy: a systematic review. Radiat. Oncol. 92 (2009), 299–309.
3. [3] Prasanna, P., Stone, H., Wong, R., Capala, J., V., B, Coleman, C., Normal tissue protection for improving radiotherapy: where are the Gaps?. Transl. Cancer Res 1 (2012), 35–48.
4. [4] Robbins, M.E., Zhao, W., Chronic oxidative stress and radiation-induced late normal tissue injury: a review. Int. J. Radiat. Biol. 80 (2004), 251–259.
5. [5] Zhao, W., Diz, D.I., Robbins, M.E., Oxidative damage pathways in relation to normal tissue injury. Br. J. Radiol. 80 (2007), S23–S31.
6. [6] Ryter, S.W., Kim, H.P., Hoetzel, A., Park, J.W., Nakahira, K., Wang, X., Choi, A.M., Mechanisms of cell death in oxidative stress. Antioxid. Redox Signal. 9 (2007), 49–89.
7. [7] Spitz, D.R., Hauer-Jensen, M., Ionizing radiation-induced responses: where free radical chemistry meets redox biology and medicine. Antioxid. Redox Signal. 20 (2014), 1407–1409.
8. [8] Okunieff, P., Swarts, S., Keng, P., Sun, W., Wang, W., Kim, J., Yang, S., Zhang, H., Liu, C., Williams, J.P., Huser, A.K., Zhang, L., Antioxidants reduce consequences of radiation exposure. Adv. Exp. Med. Biol. 614 (2008), 165–178.
9. [9] Santivasi, W.L., Xia, F., Ionizing radiation-induced DNA damage, response, and repair. Antioxid. Redox Signal. 21 (2014), 251–259.
10. [10] Azzam, E.I., Jay-Gerin, J.P., Pain, D., Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 327 (2012), 48–60.
11. [11] Auten, R.,L., Davis, J.,M., Oxygen toxicity and reactive oxygen species: the devil is in the details. Pediatr. Res. 66 (2009), 121–127.
12. [12] Sun, J., Chen, Y., Li, M., Ge, Z., Role of antioxidant enzymes on ionizing radiation resistance. Free Radic. Biol. Med. 24 (1998), 586–593.
13. [13] Leonarduzzi, G., Sottero, B., Poli, G., Targeting tissue oxidative damage by means of cell signaling modulators: the antioxidant concept revisited. Pharmacol. Ther. 128 (2010), 336–374.
14. [14] Spitz, D., Azzam, E., Jian Li, J., Gius, D., Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer and Metastasis Reviews, 2004, Kluwer Academic Publishers, Dordrecht, The Netherlands.
15. [15] Green, D.R., Reed, J.C., Mitochondria and apoptosis. Science 281 (1998), 1309–1312.
16. [16] Turrens, J.F., Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (2003), 335–344.
17. [17] Simon, H.U., Haj-Yehia, A., Levi-Schaffer, F., Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5 (2000), 415–418.
18. [18] Kobashigawa, S., Kashino, G., Suzuki, K., Yamashita, S., Mori, H., Ionizing radiation-induced cell death is partly caused by increase of mitochondrial reactive oxygen species in normal human fibroblast cells. Radiat. Res. 183 (2015), 455–464.
19. [19] Wang, C.H., Wu, S.B., Wu, Y.T., Wei, Y.H., Oxidative stress response elicited by mitochondrial dysfunction: implication in the pathophysiology of aging. Exp. Biol. Med. 238 (2013), 450–460.
20. [20] Hwang, J.J., Lin, G.L., Sheu, S.C., Lin, F.J., Effect of ionizing radiation on liver mitochondrial respiratory functions in mice. Chin. Med. J. 112 (1999), 340–344.
21. [21] Dayal, D., Martin, S.M., Owens, K.M., Aykin-Burns, N., Zhu, Y., Boominathan, A., Pain, D., Limoli, C.L., Goswami, P.C., Domann, F.E., Spitz, D.R., Mitochondrial complex II dysfunction can contribute significantly to genomic instability after exposure to ionizing radiation. Radiat. Res. 172 (2009), 737–745.
22. [22] Kulkarni, R., Marples, B., Balasubramaniam, M., Thomas, R.A., Tucker, J.D., Mitochondrial gene expression changes in normal and mitochondrial mutant cells after exposure to ionizing radiation. Radiat. Res. 173 (2010), 635–644.
23. [23] Yeung, Y.T., McDonald, K.L., Grewal, T., Munoz, L., Interleukins in glioblastoma pathophysiology: implications for therapy. Br. J. Pharmacol. 168 (2013), 591–606 [Review].
24. [24] Dickinson, D.A., Forman, H.J., Glutathione in defense and signaling: lessons from a small thiol. Ann. N. Y. Acad. Sci. 973 (2002), 488–504.
25. [25] Dickinson, D.A., Forman, H.J., Cellular glutathione and thiols metabolism. Biochem. Pharm. 64 (2002), 1019–1026.
26. [26] Franco, R., Cidlowski, J.A., Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ. 16 (2009), 1303–1314.
27. [27] Lushchak, V.I., Glutathione homeostasis and functions: potential targets for medical interventions. J. Amino Acids, 2012, 2012, 26.
28. [28] Chatterjee, A., Reduced glutathione: a radioprotector or a modulator of DNA-repair activity?. Nutrients 5 (2013), 525–542.
29. [29] Awasthi, Y.C., Chaudhary, P., Vatsyayan, R., Sharma, A., Awasthi, S., Sharma, R., Physiological and pharmacological significance of glutathione-conjugate transport. J. Toxicol. Environ. Health Part B Crit. Rev. 12 (2009), 540–551.
30. [30] Sekhar, R.V., Patel, S.G., Guthikonda, A.P., Reid, M., Balasubramanyam, A., Taffet, G.E., Jahoor, F., Deficient synthesis of glutathione underlies oxidative stress in aging and can be corrected by dietary cysteine and glycine supplementation. Am. J. Clin. Nutr. 94 (2011), 847–853.
31. [31] Diaz-Vivancos, P., de Simone, A., Kiddle, G., Foyer, C.H., Glutathione linking cell proliferation to oxidative stress. Free Radic. Biol. Med. 89 (2015), 1154–1164.
32. [32] Ramji, D.P., Foka, P., CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem. J. 365 (2002), 561–575.
33. [33] Yu, X., Si, J., Zhang, Y., DeWille, J., CCAAT/Enhancer Binding Protein-delta (C/EBP-delta) regulates cell growth, migration and differentiation. Cancer Cell Int., 10, 2010, 48.
34. [34] O'Rourke, J.P., Newbound, G.C., Hutt, J.A., Dewille, J., CCAAT/enhancer-binding protein delta regulates mammary epithelial cell G0 growth arrest and apoptosis. J. Biol. Chem. 274 (1999), 16582–16589.
35. [35] Choi, A.M., Sylvester, S., Otterbein, L., Holbrook, N.J., Molecular responses to hyperoxia in vivo: relationship to increased tolerance in aged rats. Am. J. Respir. Cell Mol. Biol., 1995.
36. [36] Huang, A.M., Montagna, C., Sharan, S., Ni, Y., Ried, T., Sterneck, E., Loss of CCAAT/enhancer binding protein delta promotes chromosomal instability. Oncogene 23 (2004), 1549–1557.
37. [37] Sarkar, T.R., Sharan, S., WANG, J., Pawar, S.A., Cantwell, C.A., Johnson, P.F., Morrison, D.K., Wang, J.M., Sterneck, E., Identification of a Src tyrosine kinase/SIAH2 E3 ubiquitin ligase pathway that regulates C/EBPdelta expression and contributes to transformation of breast tumor cells. Mol. Cell Biol. 32 (2012), 320–332.
38. [38] Barbaro, V., Testa, A., Di, I.E., Mavilio, F., Pellegrini, G., De, L.M., C/EBPdelta regulates cell cycle and self-renewal of human limbal stem cells. J. Cell Biol. 177 (2007), 1037–1049.
39. [39] Hour, T.C., Lai, Y.L., Kuan, C.I., Chou, C.K., Wang, J.M., Tu, H.Y., Hu, H.T., Lin, C.S., Wu, W.J., Pu, Y.S., Sterneck, E., Huang, A.M., Transcriptional up-regulation of SOD1 by CEBPD: a potential target for cisplatin resistant human urothelial carcinoma cells. Biochem. Pharmacol. 80 (2010), 325–334.
40. [40] Pawar, S.A., Sarkar, T.R., Balamurugan, K., Sharan, S., WANG, J., Zhang, Y., Dowdy, S.F., Huang, A.M., Sterneck, E., C/EBP delta targets cyclin D1 for proteasome-mediated degradation via induction of CDC27/APC3 expression. Proc. Natl. Acad. Sci. USA 107 (2010), 9210–9215.
41. [41] Wang, J., Sarkar, T.R., Zhou, M., Sharan, S., Ritt, D.A., Veenstra, T.D., Morrison, D.K., Huang, A.M., Sterneck, E., CCAAT/enhancer binding protein delta (C/EBPdelta, CEBPD)-mediated nuclear import of FANCD2 by IPO4 augments cellular response to DNA Damage. Proc. Natl. Acad. Sci. USA 107 (2010), 16131–16136.
42. [42] Balamurugan, K., Sterneck, E., The many faces of C/EBPdelta and their relevance for inflammation and cancer. Int. J. Biol. Sci. 9 (2013), 917–933.
43. [43] Pawar, S.A., Shao, L., Chang, J., Wang, W., Pathak, R., Zhu, X., Wang, J., Hendrickson, H., Boerma, M., Sterneck, E., Zhou, D., Hauer-Jensen, M., C/EBP delta deficiency sensitizes mice to ionizing radiation-induced hematopoietic and intestinal injury. PLoS One, 9, 2014, e94967.
44. [44] Robinson, K.M., Janes, M.S., Beckman, J.S., The selective detection of mitochondrial superoxide by live cell imaging. Nat. Protoc. 3 (2008), 941–947.
45. [45] Zielonka, J., Kalyanaraman, B., Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth. Free Radic. Biol. Med. 48 (2010), 983–1001.
46. [46] Borrelli, M.J., Thompson, L.L., Dewey, W.C., Evidence that the feeder effect in mammalian cells is mediated by a diffusible substance. Int. J. Hyperth. 5 (1989), 99–103.
47. [47] Munshi, A., Hobbs, Marvette, Meyn Raymond, E., Clonogenic cell survival assay. Methods Mol. Med., 110, 2005, 7.
48. [48] Pathak, R., Pawar, S.A., Fu, Q., Gupta, P.K., Berbee, M., Garg, S., Sridharan, V., Wang, W., Biju, P.G., Krager, K.J., Boerma, M., Ghosh, S.P., Cheema, A.K., Hendrickson, H.P., Aykin-Burns, N., Hauer-Jensen, M., Characterization of transgenic Gfrp knock-in mice: implications for tetrahydrobiopterin in modulation of normal tissue radiation responses. Antioxid. Redox Signal. 20 (2014), 1436–1446.
49. [49] Wu, M., Neilson, A., Swift, A.L., Moran, R., Tamagnine, J., Parslow, D., Armistead, S., Lemire, K., Orrell, J., Teich, J., Chomicz, S., Ferrick, D.A., Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292 (2007), C125–C136.
50. [50] Banerjee, S., Melnyk, S.B., Krager, K.J., Aykin-Burns, N., Letzig, L.G., James, L.P., Hinson, J.A., The neuronal nitric oxide synthase inhibitor NANT blocks acetaminophen toxicity and protein nitration in freshly isolated hepatocytes. Free Radic. Biol. Med. 89 (2015), 750–757.
51. [51] Stocchi, V., Cucchiarini, L., Magnani, M., Chiarantini, L., Palma, P., Crescentini, G., Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells. Anal. Biochem. 146 (1985), 118–124.
52. [52] Melnyk, S., Pogribna, M., Pogribny, I., Hine, R.J., James, S.J., A new HPLC method for the simultaneous determination of oxidized and reduced plasma aminothiols using coulometric electrochemical detection1. J. Nutr. Biochem. 10 (1999), 490–497.
53. [53] Aykin-Burns, N., Slane, B.G., Liu, A.T., Owens, K.M., O'Malley, M.S., Smith, B.J., Domann, F.E., Spitz, D.R., Sensitivity to low-dose/low-LET ionizing radiation in mammalian cells harboring mutations in succinate dehydrogenase subunit C is governed by mitochondria-derived reactive oxygen species. Radiat. Res. 175 (2011), 150–158.
54. [54] Zhong, H., Yin, H., Role of lipid peroxidation derived 4-hydroxynonenal (4-HNE) in cancer: focusing on mitochondria. Redox Biol. 4 (2015), 193–199.
55. [55] Peter, Y., Rotman, G., Lotem, J., Elson, A., Shiloh, Y., Groner, Y., Elevated Cu/Zn-SOD exacerbates radiation sensitivity and hematopoietic abnormalities of Atm-deficient mice. EMBO J. 20 (2001), 1538–1546.
56. [56] Guo, G., Yan-Sanders, Y., Lyn-Cook, B.D., Wang, T., Tamae, D., Ogi, J., Khaletskiy, A., Li, Z., Weydert, C., Longmate, J.A., Huang, T.T., Spitz, D.R., Oberley, L.W., Li, J.J., Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses. Mol. Cell. Biol. 23 (2003), 2362–2378.
57. [57] Hosoki, A., Yonekura, S.I., Zhao, Q.L., WeiZ, L., Takasaki, I., Tabuchi, Y., Wang, L.L., Hasuike, S., Nomurat, T., Tachibana, A., Hashiguchi, K., Yonei, S., Kondo, T., Zhang-Akiyama, Q.M., Mitochondria-targeted Superoxide Dismutase (SOD2) regulates radiation resistance and radiation stress response in HeLa cells. J. Radiat. Res. 53 (2012), 58–71.
58. [58] Hutt, J.A., DeWille, J.W., Oncostatin M induces growth arrest of mammary epithelium via a CCAAT/enhancer-binding protein delta-dependent pathway. Mol. Cancer Ther. 1 (2002), 601–610.
59. [59] Moore, F., Santin, I., Nogueira, T.C., Gurzov, E.N., Marselli, L., Marchetti, P., Eizirik, D.L., The transcription factor C/EBP delta has anti-apoptotic and anti-inflammatory roles in pancreatic beta cells. PLoS One, 7, 2012, e31062.
60. [60] Pfleger, J., He, M., Abdellatif, M., Mitochondrial complex II is a source of the reserve respiratory capacity that is regulated by metabolic sensors and promotes cell survival. Cell Death Dis., 6, 2015, e1835.
61. [61] Gorrini, C., Harris, I.S., Mak, T.W., Modulation of oxidative stress as an anticancer strategy. Nat. Rev. Drug Discov. 12 (2013), 931–947.