Evaluation of mitochondrial redox status and energy metabolism of X-irradiated HeLa cells by LC/UV, LC/MS/MS and ESR

References

• Warburg O. On the origin of cancer cells. Science. 1956;123(3191):309–314.
   PubMed Web of Science ®Google Scholar
• Zong WX, Rabinowitz JD, White E. Mitochondria and cancer. Mol Cell. 2016;61(5):667–676.
   PubMed Web of Science ®Google Scholar
• Chen Y, McMillan-Ward E, Kong J, et al. Mitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen species. J Cell Sci. 2007;120(Pt 23):4155–4166.
   PubMed Web of Science ®Google Scholar
• Lu CL, Qin L, Liu HC, et al. Tumour cells switch to mitochondrial oxidative phosphorylation under radiation via mTOR-mediated hexokinase II inhibition--a Warburg-reversing effect. PLoS One. 2015;10(3):e0121046.
   PubMed Web of Science ®Google Scholar
• Yamamori T, Ike S, Bo T, et al. Inhibition of the mitochondrial fission protein dynamin-related protein 1 (Drp1) impairs mitochondrial fission and mitotic catastrophe after x-irradiation. Mol Biol Cell. 2015;26(25):4607–4617.
   PubMed Web of Science ®Google Scholar
• Yamamori T, Sasagawa T, Ichii O, et al. Analysis of the mechanism of radiation-induced upregulation of mitochondrial abundance in mouse fibroblasts. J Radiat Res. 2017;58(3):292–301.
   PubMed Web of Science ®Google Scholar
• Yasui H, Yamamoto K, Suzuki M, et al. Lipophilic triphenylphosphonium derivatives enhance radiation-induced cell killing via inhibition of mitochondrial energy metabolism in tumour cells. Cancer Lett. 2017;390:160–167.
   PubMed Web of Science ®Google Scholar
• Marrache S, Pathak RK, Dhar S. Detouring of cisplatin to access mitochondrial genome for overcoming resistance. Proc Natl Acad Sci. 2014;111(29):10444–10449.
   PubMed Web of Science ®Google Scholar
• Nishida N, Yasui H, Nagane M, et al. 3-methyl pyruvate enhances radiosensitivity through increasing mitochondria-derived reactive oxygen species in tumour cell lines. J Radiat Res. 2014;55(3):455–463.
   PubMed Web of Science ®Google Scholar
• Indo HP, Inanami O, Koumura T, et al. Roles of mitochondria-generated reactive oxygen species on X-ray-induced apoptosis in a human hepatocellular carcinoma cell line, HLE. Free Radic Res. 2012;46(8):1029–1043.
   PubMed Web of Science ®Google Scholar
• Motoori S, Majima HJ, Ebara M, et al. Overexpression of mitochondrial manganese superoxide dismutase protects against radiation-induced cell death in the human hepatocellular carcinoma cell line HLE. Cancer Res. 2001;61(14):5382–5388.
   PubMed Web of Science ®Google Scholar
• Chen Z, Wang B, Yu F, et al. The roles of mitochondria in radiation-induced autophagic cell death in cervical cancer cells. Tumour Biol. 2016;37(3):4083–4091.
   PubMedGoogle Scholar
• Hosoki A, Yonekura S, Zhao QL, et al. Mitochondria-targeted superoxide dismutase (SOD2) regulates radiation resistance and radiation stress response in HeLa cells. J Radiat Res. 2012;53(1):58–71.
   PubMed Web of Science ®Google Scholar
• Hu S, Gao Y, Zhou H, et al. New insight into mitochondrial changes in vascular endothelial cells irradiated by gamma ray. Int J Radiat Biol. 2017;93(5):470–476.
   PubMed Web of Science ®Google Scholar
• Fetisova EK, Antoschina MM, Cherepanynets VD, et al. Radioprotective effects of mitochondria-targeted antioxidant SkQR1. Radiat Res. 2015;183(1):64–71.
   PubMed Web of Science ®Google Scholar
• Saenko Y, Cieslar-Pobuda A, Skonieczna M, et al. Changes of reactive oxygen and nitrogen species and mitochondrial functioning in human K562 and HL60 cells exposed to ionizing radiation. Radiat Res. 2013;180(4):360–366.
   PubMed Web of Science ®Google Scholar
• Kobashigawa S, Kashino G, Suzuki K, et al. Ionizing radiation-induced cell death is partly caused by increase of mitochondrial reactive oxygen species in normal human fibroblast cells. Radiat Res. 2015;183(4):455–464.
   PubMed Web of Science ®Google Scholar
• Kashino G, Tamari Y, Kumagai J, et al. Suppressive effect of ascorbic acid on the mutagenesis induced by the bystander effect through mitochondrial function. Free Radic Res. 2013;47(6–7):474–479.
   PubMed Web of Science ®Google Scholar
• Choi YM, Kim HK, Shim W, et al. Mechanism of cisplatin-induced cytotoxicity is correlated to impaired metabolism due to mitochondrial ROS Generation. PLoS One 2015;10(8):e0135083.
   PubMed Web of Science ®Google Scholar
• Sorokina IV, Denisenko TV, Imreh G, et al. Reactive oxygen species regulate a balance between mitotic catastrophe and apoptosis. Int J Biochem Cell Biol. 2016;81(A):133–136.
   PubMedGoogle Scholar
• Yamamori T, Yasui H, Yamazumi M, et al. Ionizing radiation induces mitochondrial reactive oxygen species production accompanied by upregulation of mitochondrial electron transport chain function and mitochondrial content under control of the cell cycle checkpoint. Free Radic Biol Med. 2012;53(2):260–270.
   PubMed Web of Science ®Google Scholar
• Jahnke VE, Sabido O, Freyssenet D. Control of mitochondrial biogenesis, ROS level, and cytosolic Ca2+ concentration during the cell cycle and the onset of differentiation in L6E9 myoblasts. Am J Physiol Cell Physiol. 2009;296(5):C1185–C1194.
   PubMed Web of Science ®Google Scholar
• Schönfeld P, Wojtczak L. Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse electron transport but increase it at the forward transport. Biochim Biophys Acta. 2007;1767(8):1032–1040.
   PubMed Web of Science ®Google Scholar
• Lanciano P, Khalfaoui-Hassani B, Selamoglu N, et al. Molecular mechanisms of superoxide production by complex III: a bacterial versus human mitochondrial comparative case study. Biochim Biophys Acta. 2013;1827(11–12):1332–1339.
   PubMed Web of Science ®Google Scholar
• Yoshida T, Goto S, Kawakatsu M, et al. Mitochondrial dysfunction, a probable cause of persistent oxidative stress after exposure to ionizing radiation. Free Radic Res. 2012;46(2):147–153.
   PubMed Web of Science ®Google Scholar
• Ruuge EK, Ledenev AN, Lakomkin VL, et al. Free radical metabolites in myocardium during ischaemia and reperfusion. Am J Physiol. 1991;261(4 Suppl):81–86.
   PubMedGoogle Scholar
• Elas M, Bielanska J, Pustelny K, et al. Detection of mitochondrial dysfunction by EPR technique in mouse model of dilated cardiomyopathy. Free Radic Biol Med. 2008;45(3):321–328.
   PubMed Web of Science ®Google Scholar
• Svistunenko DA, Davies N, Brealey D, et al. Mitochondrial dysfunction in patients with severe sepsis: an EPR interrogation of individual respiratory chain components. Biochim Biophys Acta. 2006;1757(4):262–272.
   PubMed Web of Science ®Google Scholar
• Burlaka AP, Ganusevich II, Gafurov MR, et al. Stomach cancer: interconnection between the redox state, activity of MMP-2, MMP-9 and stage of Tumourtumour growth. Cancer Microenviron. 2016;9(1):27–32.
   PubMed Web of Science ®Google Scholar
• Ledenev AN, Ruuge EK. Generation of superoxide radicals by mitochondria of the ischemic heart. Bull Exp Biol Med. 1985;100(3):1204–1206.
   Google Scholar
• Pandian RP, Parinandi NL, Ilangovan G, et al. Novel particulate spin probe for targeted determination of oxygen in cells and tissues. Free Radic Biol Med. 2003;35(9):1138–1148.
   PubMed Web of Science ®Google Scholar
• Fujii H, Sakata K, Katsumata Y, et al. Tissue oxygenation in a murine SCC VII tumour after X-ray irradiation as determined by EPR spectroscopy. Radiother Oncol. 2008;86(3):354–360.
   PubMed Web of Science ®Google Scholar
• Labuschagne CF, van den Broek NJ, Postma P, et al. A protocol for quantifying lipid peroxidation in cellular systems by F2-isoprostane analysis. PLoS One. 2013;8(11):e80935.
   PubMed Web of Science ®Google Scholar
• Bornhorst J, Ebert F, Lohren H, et al. Effects of manganese and arsenic species on the level of energy related nucleotides in human cells. Metallomics. 2012;4(3):297–306.
   PubMed Web of Science ®Google Scholar
• Swartz HM. Cells and tissues. In: Swartz HD, Bolton JR, Borg DC, editors. Biological applications of electron spin resonance. Hoboken: John Wiley & Sons Inc; 1972. p. 155–196.
   Google Scholar
• Segre AL, Benedetto A, Eremenko T, et al. An electron paramagnetic resonance study of free radicals in cells. Biochim Biophys Acta. 1977;497(2):615–621.
   PubMedGoogle Scholar
• Jakubowska M, Sniegocka M, Podgórska E, et al. Pulmonary metastases of the A549-derived lung adenocarcinoma tumours growing in nude mice. A multiple case study. Acta Biochim Pol. 2013;60(3):323–330.
   PubMed Web of Science ®Google Scholar
• Emanuel NM. Kinetics and the free-radical mechanisms of tumour growth. Ann N Y Acad Sci. 1973;222:1010–1030.
   PubMed Web of Science ®Google Scholar
• Swartz HM. Effect of oxygen on freezing damage. II. Physical-chemical effects. Cryobiology. 1971;8(3):255–264.
   PubMed Web of Science ®Google Scholar
• De Jong AM, Albracht SP. Ubisemiquinones as obligatory intermediates in the electron transfer from NADH to ubiquinone. Eur J Biochem. 1994;222(3):975–982.
   PubMedGoogle Scholar
• Rupp H, Rao KK, Hall DO, et al. Electron spin relaxation of iron–sulphur proteins studied by microwave power saturation. Biochim Biophys Acta. 1978;537(2):255–260.
   PubMedGoogle Scholar
• Burbaev DS, Moroz IA, Kotlyar AB, et al. Ubisemiquinone in the NADH-ubiquinone reductase region of the mitochondrial respiratory chain. FEBS Lett. 1989;254(1–2):47–51.
   Web of Science ®Google Scholar
• Kotlyar AB, Sled VD, Burbaev DS, et al. Coupling site I and the rotenone-sensitive ubisemiquinone in tightly coupled submitochondrial particles. FEBS Lett. 1990;264(1):17–20.
   PubMed Web of Science ®Google Scholar
• Bartoletti-Stella A, Mariani E, Kurelac I, et al. Gamma rays induce a p53-independent mitochondrial biogenesis that is counter-regulated by HIF1alpha. Cell Death Dis. 2013;4:e663.
   PubMed Web of Science ®Google Scholar
• Derr RF, Zieve L. Adenylate energy charge: relation to guanylate energy charge and the adenylate kinase equilibrium constant. Biochem Biophys Res Commun. 1972;49(6):1385–1390.
   PubMed Web of Science ®Google Scholar
• Privalle LS, Burris RH. Adenine nucleotide levels in and nitrogen fixation by the cyanobacterium Anabaena sp. strain 7120. J Bacteriol. 1983;154(1):351–355.
   PubMed Web of Science ®Google Scholar
• Matsumoto SS, Raivio KO, Seegmiller JE. Adenine nucleotide degradation during energy depletion in human lymphoblasts. Adenosine accumulation and adenylate energy charge correlation. J Biol Chem. 1979;254(18):8956–8962.
   PubMed Web of Science ®Google Scholar
• Danielsen T, Skøyum R, Rofstad EK. Hypoxia-induced changes in radiation sensitivity in human melanoma cells: importance of oxygen-regulated proteins, adenylate energy charge and cell cycle distribution. Radiother Oncol. 1997;44(2):177–182.
   PubMed Web of Science ®Google Scholar
• Skøyum R, Eide K, Berg K, et al. Energy metabolism in human melanoma cells under hypoxic and acidic conditions in vitro. Br J Cancer. 1997;76(4):421–428.
   PubMed Web of Science ®Google Scholar
• Balestri F, Giannecchini M, Sgarrella F, et al. Purine and pyrimidine nucleosides preserve human astrocytoma cell adenylate energy charge under ischemic conditions. Neurochem Int. 2007;50(3):517–523.
   PubMed Web of Science ®Google Scholar
• Dong Y, Bey EA, Li LS, et al. Prostate cancer radiosensitization through poly(ADP-ribose) polymerase-1 hyperactivation. Cancer Res. 2010;70(20):8088–8096.
   PubMed Web of Science ®Google Scholar
• Ogura A, Oowada S, Kon Y, et al. Redox regulation in radiation-induced cytochrome c release from mitochondria of human lung carcinoma A549 cells. Cancer Lett. 2009;277(1):64–71.
   PubMed Web of Science ®Google Scholar
• Passos JF, Nelson G, Wang C, et al. Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol Syst Biol. 2010;6:347.
   PubMed Web of Science ®Google Scholar
• Fujibayashi Y, Waki A, Sakahara H, et al. Transient increase in glycolytic metabolismin cultured tumour cells immediately after exposure to ionizing radiation: from gene expressionto deoxyglucose uptake. Radiat Res. 1997;147(6):729–734.
   PubMed Web of Science ®Google Scholar
• Wang M, Keogh A, Treves S, et al. The metabolomic profile of gamma-irradiated human hepatoma and muscle cells reveals metabolic changes consistent with the Warburg effect. Peer J 2016;4:e1624.
   PubMed Web of Science ®Google Scholar
• Baker JE, Kalyanaraman B. Ischaemia-induced changes in myocardial paramagnetic metabolites: implications for intracellular oxy-radical generation. FEBS Lett. 1989;244(2):311–314.
   PubMed Web of Science ®Google Scholar
• Burlaka A, Selyuk M, Gafurov M, et al. Changes in mitochondrial functioning with electromagnetic radiation of ultra high frequency as revealed by electron paramagnetic resonance methods. Int J Radiat Biol. 2014;90(5):357–362.
   PubMed Web of Science ®Google Scholar