Epigallocatechin-3-gallate induces oxidative phosphorylation by activating cytochrome c oxidase in human cultured neurons and astrocytes

Oncotarget

Volumn 7, Issue 7, 2016, Pages 7426-7440

  Castellano González, Gloria ^a   Pichaud, Nicolas ^b   Ballard, J William O ^c   Bessede, Alban ^d   Marcal, Helder ^c   Guillemin, Gilles J ^a  

^a MACQUARIE UNIVERSITY   (Australia)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d Immusmol Pty Ltd   (France)

Author keywords

ATP; Cytochrome c oxidase; Epigallocatechin 3 gallate; Gerotarget; Mitochondria; Neurodegeneration

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; EPIGALLOCATECHIN GALLATE; OLIGOMYCIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; SODIUM AZIDE; CATECHIN; MESSENGER RNA; NEUROPROTECTIVE AGENT;

APOPTOSIS; ARTICLE; ASTROCYTE CULTURE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FETUS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KINETIC PARAMETERS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MODULATION; NERVE CELL CULTURE; OXIDATIVE PHOSPHORYLATION; REGULATORY MECHANISM; ANALOGS AND DERIVATIVES; ASTROCYTE; BRAIN; CELL CULTURE; CELL PROLIFERATION; CELL RESPIRATION; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; MITOCHONDRION; NERVE CELL; OXIDATION REDUCTION REACTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ASTROCYTES; BLOTTING, WESTERN; BRAIN; CATECHIN; CELL PROLIFERATION; CELL RESPIRATION; CELLS, CULTURED; ELECTRON TRANSPORT COMPLEX IV; FETUS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84958817456     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6863     Document Type: Article

References (62)

1. Dragicevic N, Smith A, Lin X, Yuan F, Copes N, Delic V, Tan J, Cao C, Shytle RD and Bradshaw PC. Green tea epigallocatechin-3-gallate (EGCG) and other flavonoids reduce Alzheimer's amyloid-induced mitochondrial dysfunction. Journal of Alzheimer's disease: JAD. 2011; 26:507-521.
2. Schroeder EK, Kelsey NA, Doyle J, Breed E, Bouchard RJ, Loucks FA, Harbison RA and Linseman DA. Green tea epigallocatechin 3-gallate accumulates in mitochondria and displays a selective antiapoptotic effect against inducers of mitochondrial oxidative stress in neurons. Antioxidants & redox signaling. 2009; 11:469-480.
3. Valenti D, De Rasmo D, Signorile A, Rossi L, de Bari L, Scala I, Granese B, Papa S and Vacca RA. Epigallocatechin-3-gallate prevents oxidative phosphorylation deficit and promotes mitochondrial biogenesis in human cells from subjects with Down's syndrome. Biochimica et biophysica acta. 2013; 1832:542-552.
4. Prochazkova D, Bousova I and Wilhelmova N. Antioxidant and prooxidant properties of flavonoids. Fitoterapia. 2011; 82:513-523.
5. Murakami A and Ohnishi K. Target molecules of food phytochemicals: food science bound for the next dimension. Food & function. 2012; 3:462-476.
6. Cusi MG, Del Vecchio MT, Terrosi C, Savellini GG, Di Genova G, La Placa M, Fallarino F, Moser C, Cardone C, Giorgi G, Francini G and Correale P. Immune-reconstituted influenza virosome containing CD40L gene enhances the immunological and protective activity of a carcinoembryonic antigen anticancer vaccine. Journal of Immunology. 2005; 174:7210-7216.
7. Takahashi A, Watanabe T, Mondal A, Suzuki K, Kurusu-Kanno M, Li Z, Yamazaki T, Fujiki H and Suganuma M. Mechanism-based inhibition of cancer metastasis with (-)-epigallocatechin gallate. Biochem Biophys Res Commun. 2014; 443:1-6.
8. Katiyar S, Elmets CA and Katiyar SK. Green tea and skin cancer: photoimmunology, angiogenesis and DNA repair. The Journal of nutritional biochemistry. 2007; 18:287-296.
9. Singh T and Katiyar SK. Green tea catechins reduce invasive potential of human melanoma cells by targeting COX-2, PGE2 receptors and epithelial-to-mesenchymal transition. PLoS One. 2011; 6:e25224.
10. Singh BN, Shankar S and Srivastava RK. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem Pharmacol. 2011; 82:1807-1821.
11. Fu Z, Zhen W, Yuskavage J and Liu D. Epigallocatechin gallate delays the onset of type 1 diabetes in spontaneous non-obese diabetic mice. The British journal of nutrition. 2011; 105:1218-1225.
12. Mandel SA, Avramovich-Tirosh Y, Reznichenko L, Zheng H, Weinreb O, Amit T and Youdim MB. Multifunctional activities of green tea catechins in neuroprotection. Modulation of cell survival genes, iron-dependent oxidative stress and PKC signaling pathway. Neurosignals. 2005; 14:46-60.
13. Zhang HS, Wu TC, Sang WW and Ruan Z. EGCG inhibits Tat-induced LTR transactivation: role of Nrf2, AKT, AMPK signaling pathway. Life Sci. 2012; 90:747-754.
14. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, Banayo E, Mihaylova MM, Nelson MC, Zou Y, Juguilon H, Kang H, Shaw RJ and Evans RM. AMPK and PPARdelta agonists are exercise mimetics. Cell. 2008; 134:405-415.
15. Rietveld A and Wiseman S. Antioxidant effects of tea: evidence from human clinical trials. The Journal of nutrition. 2003; 133:3285S-3292S.
16. Lin LC, Wang MN, Tseng TY, Sung JS and Tsai TH. Pharmacokinetics of (-)-epigallocatechin-3-gallate in conscious and freely moving rats and its brain regional distribution. J Agric Food Chem. 2007; 55:1517-1524.
17. Lee JH, Moon JH, Kim SW, Jeong JK, Nazim UM, Lee YJ, Seol JW and Park SY. EGCG-mediated autophagy flux has a neuroprotection effect via a class III histone deacetylase in primary neuron cells. Oncotarget. 2015; 6: 9701-17. doi: 10.18632/oncotarget.3832.
18. Srinivasan S and Avadhani NG. Cytochrome c oxidase dysfunction in oxidative stress. Free Radical Biology and Medicine. 2012; 53:1252-1263.
19. Arnold S. The power of life. Cytochrome c oxidase takes center stage in metabolic control, cell signalling and survival. Mitochondrion. 2012; 12:46-56.
20. Perry SW, Norman JP, Barbieri J, Brown EB and Gelbard HA. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. BioTechniques. 2011; 50:98-115.
21. Fernandez-Fernandez S, Almeida A and Bolaños JP. Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochemical Journal. 2012; 443:3-11.
22. Pendergrass W, Wolf N and Poot M. Efficacy of MitoTracker Green™ and CMXrosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry Part A. 2004; 61A:162-169.
23. Nicholls DG and Budd SL. Mitochondria and Neuronal Survival. Physiol Rev. 2000; 80:315-60.
24. Hutter E, Unterluggauer H, Garedew A, Jansen-Durr P and Gnaiger E. High-resolution respirometry--a modern tool in aging research. Experimental gerontology. 2006; 41:103-109.
25. Pesta D and Gnaiger E. High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods in molecular biology. 2012; 810:25-58.
26. Kelly DP and Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes & development. 2004; 18:357-368.
27. Dasgupta B and Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A. 2007; 104:7217-7222.
28. Sugioka K, Nakano M, Totsune-Nakano H, Minakami H, Tero-Kubota S and Ikegami Y. Mechanism of O2-generation in reduction and oxidation cycle of ubiquinones in a model of mitochondrial electron transport systems. Biochimica et biophysica acta. 1988; 936:377-385.
29. Jellinger KA. Basic mechanisms of neurodegeneration: a critical update. Journal of cellular and molecular medicine. 2010; 14:457-487.
30. Zhang Z, Ding Y, Dai X, Wang J and Li Y. Epigallocatechin-3-gallate protects pro-inflammatory cytokine induced injuries in insulin-producing cells through the mitochondrial pathway. Eur J Pharmacol. 2011; 670:311-316.
31. Collins QF, Liu HY, Pi J, Liu Z, Quon MJ and Cao W. Epigallocatechin-3-gallate (EGCG), a green tea polyphenol, suppresses hepatic gluconeogenesis through 5'-AMP-activated protein kinase. The Journal of biological chemistry. 2007; 282:30143-30149.
32. Hwang JT, Ha J, Park IJ, Lee SK, Baik HW, Kim YM and Park OJ. Apoptotic effect of EGCG in HT-29 colon cancer cells via AMPK signal pathway. Cancer letters. 2007; 247:115-121.
33. Huang CH, Tsai SJ, Wang YJ, Pan MH, Kao JY and Way TD. EGCG inhibits protein synthesis, lipogenesis, and cell cycle progression through activation of AMPK in p53 positive and negative human hepatoma cells. Molecular nutrition & food research. 2009; 53:1156-1165.
34. Park SY, Jung CH, Song B, Park OJ and Kim YM. Pro-apoptotic and migration-suppressing potential of EGCG, and the involvement of AMPK in the p53-mediated modulation of VEGF and MMP-9 expression. Oncology letters. 2013; 6:1346-1350.
35. Chen C, Shen G, Hebbar V, Hu R, Owuor ED and Kong AN. Epigallocatechin-3-gallate-induced stress signals in HT-29 human colon adenocarcinoma cells. Carcinogenesis. 2003; 24:1369-1378.
36. Hardie DG, Ross FA and Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 2012; 13:251-262.
37. Mihaylova MM and Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nature cell biology. 2011; 13:1016-1023.
38. Spasic MR, Callaerts P and Norga KK. AMP-activated protein kinase (AMPK) molecular crossroad for metabolic control and survival of neurons. The Neuroscientist: a review journal bringing neurobiology, neurology and psychiatry. 2009; 15:309-316.
39. Wagner AE, Piegholdt S, Rabe D, Baenas N, Schloesser A, Eggersdorfer M, Stocker A and Rimbach G. Epigallocatechin gallate affects glucose metabolism and increases fitness and lifespan in Drosophila melanogaster. Oncotarget. 2015; 6:30568-78. doi: 10.18632/oncotarget.5215.
40. Dinuzzo M, Mangia S, Maraviglia B and Giove F. The role of astrocytic glycogen in supporting the energetics of neuronal activity. Neurochem Res. 2012; 37:2432-2438.
41. Ludwig B, Bender E, Arnold S, Huttemann M, Lee I and Kadenbach B. Cytochrome C oxidase and the regulation of oxidative phosphorylation. Chembiochem: a European journal of chemical biology. 2001; 2:392-403.
42. Arnold S and Kadenbach B. The intramitochondrial ATP/ADP-ratio controls cytochrome c oxidase activity allosterically. FEBS Lett. 1999; 443:105-108.
43. Huttemann M, Kadenbach B and Grossman LI. Mammalian subunit IV isoforms of cytochrome c oxidase. Gene. 2001; 267:111-123.
44. Misiak M, Singh S, Drewlo S, Beyer C and Arnold S. Brain region-specific vulnerability of astrocytes in response to 3-nitropropionic acid is mediated by cytochrome c oxidase isoform expression. Cell and tissue research. 2010; 341:83-93.
45. Horvat S, Beyer C and Arnold S. Effect of hypoxia on the transcription pattern of subunit isoforms and the kinetics of cytochrome c oxidase in cortical astrocytes and cerebellar neurons. J Neurochem. 2006; 99:937-951.
46. Collman JP, Dey A, Barile CJ, Ghosh S and Decreau RA. Inhibition of electrocatalytic O(2) reduction of functional CcO models by competitive, non-competitive, and mixed inhibitors. Inorganic chemistry. 2009; 48:10528-10534.
47. Arnold S, Goglia F and Kadenbach B. 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. European journal of biochemistry/FEBS. 1998; 252:325-330.
48. Fukuda R, Zhang H, Kim JW, Shimoda L, Dang CV and Semenza GL. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell. 2007; 129:111-122.
49. Pope S, Land JM and Heales SJ. Oxidative stress and mitochondrial dysfunction in neurodegeneration; cardiolipin a critical target? Biochimica et biophysica acta. 2008; 1777:794-799.
50. Helling S, Huttemann M, Ramzan R, Kim SH, Lee I, Muller T, Langenfeld E, Meyer HE, Kadenbach B, Vogt S and Marcus K. Multiple phosphorylations of cytochrome c oxidase and their functions. Proteomics. 2012; 12:950-959.
51. Piccoli C, Scrima R, Boffoli D and Capitanio N. Control by cytochrome c oxidase of the cellular oxidative phosphorylation system depends on the mitochondrial energy state. The Biochemical journal. 2006; 396:573-583.
52. Lu LY, Ou N and Lu QB. Antioxidant induces DNA damage, cell death and mutagenicity in human lung and skin normal cells. Scientific reports. 2013; 3:3169.
53. Guillemin GJ, Smythe G, Takikawa O and Brew BJ. Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia. 2005; 49:15-23.
54. Guillemin GJ, Cullen KM, Lim CK, Smythe GA, Garner B, Kapoor V, Takikawa O and Brew BJ. Characterization of the Kynurenine Pathway in Human Neurons. The Journal of Neuroscience. 2007; 27:12884-12892.
55. Braidy N, Grant R, Adams S and Guillemin GJ. Neuroprotective effects of naturally occurring polyphenols on quinolinic acid-induced excitotoxicity in human neurons. FEBS Journal. 2010; 277:368-382.
56. Ting KK, Brew BJ and Guillemin GJ. (2007). Effect of quinolinic acid on gene expression in human astrocytes: Implications for Alzheimer's disease. In: Takai K, ed., pp. 384-388.
57. Guillemin GJ, Croitoru-Lamoury J, Dormont D, Armati PJ and Brew BJ. Quinolinic acid upregulates chemokine production and chemokine receptor expression in astrocytes. GLIA. 2003; 41:371-381.
58. Adams S, Teo C, McDonald KL, Zinger A, Bustamante S, Lim CK, Sundaram G, Braidy N, Brew BJ and Guillemin GJ. Involvement of the kynurenine pathway in human glioma pathophysiology. PLoS One. 2014; 9:e112945.
59. Haslam G, Wyatt D and Kitos PA. Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities. Cytotechnology. 2000; 32:63-75.
60. Norman JP, Perry SW, Kasischke KA, Volsky DJ and Gelbard HA. HIV-1 Trans Activator of Transcription Protein Elicits Mitochondrial Hyperpolarization and Respiratory Deficit, with Dysregulation of Complex IV and Nicotinamide Adenine Dinucleotide Homeostasis in Cortical Neurons. The Journal of Immunology. 2007; 178:869-876.
61. Schneider CA, Rasband WS and Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature methods. 2012; 9:671-675.
62. King BA and Oh DH. Spatial control of reactive oxygen species formation in fibroblasts using two-photon excitation. Photochemistry and photobiology. 2004; 80:1-6.