Inhibition of oxidative stress by coenzyme Q10 increases mitochondrial mass and improves bioenergetic function in optic nerve head astrocytes

Cell Death and Disease

Volumn 4, Issue 10, 2013, Pages

  Noh, Y H ^a   Kim, K Y ^b   Shim, M S ^a   Choi, S H ^c   Choi, S ^b   Ellisman, M H ^b   Weinreb, R N ^a   Perkins, G A ^b   Ju, W K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Coenzyme Q10; Glaucoma; Mitochondrial dysfunction; Optic nerve head astrocytes; Oxidative stress; OXPHOS complex

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEME OXYGENASE 1; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; OXIDATIVE PHOSPHORYLATION COMPLEX PROTEIN; OXIDOREDUCTASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1; REACTIVE OXYGEN METABOLITE; UBIDECARENONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BIOENERGY; BIOGENESIS; CELL COUNT; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME INHIBITION; IN VITRO STUDY; MASS; MEDIATOR; MITOCHONDRIAL VOLUME DENSITY; MITOCHONDRION; NONHUMAN; OPTIC NERVE; OPTIC NERVE HEAD; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; RECEPTOR UPREGULATION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; ENERGY METABOLISM; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL TURNOVER; MULTIPROTEIN COMPLEXES; OPTIC DISK; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION FACTORS; UBIQUINONE;

EID: 84887445214     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.341     Document Type: Article

References (58)

1. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000; 29: 222-230
2. Chrysostomou V, Rezania F, Trounce IA, Crowston JG. Oxidative stress and mitochondrial dysfunction in glaucoma. Curr Opin Pharmacol 2013; 13: 12-15
3. McElnea EM, Quill B, Docherty NG, Irnaten M, Siah WF, Clark AF et al. Oxidative stress, mitochondrial dysfunction and calcium overload in human lamina cribrosa cells from glaucoma donors. Mol Vis 2011; 17: 1182-1191
4. Abu-Amero KK, Morales J, Bosley TM. Mitochondrial abnormalities in patients with primary open-Angle glaucoma. Invest Ophthalmol Vis Sci 2006; 47: 2533-2541
5. Lee D, Kim KY, Noh YH, Chai S, Lindsey JD, Ellisman MH et al. Brimonidine blocks glutamate excitotoxicity-induced oxidative stress and preserves mitochondrial transcription factor a in ischemic retinal injury. PLoS One 2012; 7: E47098
6. Hernandez MR, Agapova OA, Yang P, Salvador-Silva M, Ricard CS, Aoi S. Differential gene expression in astrocytes from human normal and glaucomatous optic nerve head analyzed by cDNA microarray. Glia 2002; 38: 45-64
7. Weinreb RN, Khaw PT. Primary open-Angle glaucoma. Lancet 2004; 363: 1711-1720
8. Hernandez MR. The optic nerve head in glaucoma: Role of astrocytes in tissue remodeling. Prog Retin Eye Res 2000; 19: 297-321
9. Tezel G. Oxidative stress in glaucomatous neurodegeneration: Mechanisms and consequences. Prog Retin Eye Res 2006; 25: 490-513
10. Dai C, Khaw PT, Yin ZQ, Li D, Raisman G, Li Y. Structural basis of glaucoma: The fortified astrocytes of the optic nerve head are the target of raised intraocular pressure. Glia 2012; 60: 13-28
11. Ju WK, Kim KY, Lindsey JD, Angert M, Duong-Polk KX, Scott RT et al. Intraocular pressure elevation induces mitochondrial fission and triggers OPA1 release in glaucomatous optic nerve. Invest Ophthalmol Vis Sci 2008; 49: 4903-4911
12. Ju WK, Kim KY, Angert M, Duong-Polk KX, Lindsey JD, Ellisman MH et al. Memantine blocks mitochondrial OPA1 and cytochrome c release and subsequent apoptotic cell death in glaucomatous retina. Invest Ophthalmol Vis Sci 2009; 50: 707-716
13. Ju WK, Kim KY, Duong-Polk KX, Lindsey JD, Ellisman MH, Weinreb RN. Increased optic atrophy type 1 expression protects retinal ganglion cells in a mouse model of glaucoma. Mol Vis 2010; 16: 1331-1342
14. Son JL, Soto I, Oglesby E, Lopez-Roca T, Pease ME, Quigley HA et al. Glaucomatous optic nerve injury involves early astrocyte reactivity and late oligodendrocyte loss. Glia 2010; 58: 780-789
15. Beal MF, Shults CW. Effects of Coenzyme Q10 in Huntington's disease and early Parkinson's disease. Biofactors 2003; 18: 153-161
16. McCarthy S, Somayajulu M, Sikorska M, Borowy-Borowski H, Pandey S. Paraquat induces oxidative stress and neuronal cell death; neuroprotection by water-soluble coenzyme Q10. Toxicol Appl Pharmacol 2004; 201: 21-31
17. Bessero AC, Clarke PG. Neuroprotection for optic nerve disorders. Curr Opin Neurol 2010; 23: 10-15
18. Qu J, Kaufman Y, Washington I. Coenzyme Q10 in the human retina. Invest Ophthalmol Vis Sci 2009; 50: 1814-1818
19. Nucci C, Tartaglione R, Cerulli A, Mancino R, Spano A, Cavaliere F et al. Retinal damage caused by high intraocular pressure-induced transient ischemia is prevented by coenzyme Q10 in rat. Int Rev Neurobiol 2007; 82: 397-406
20. Russo R, Cavaliere F, Rombola L, Gliozzi M, Cerulli A, Nucci C et al. Rational basis for the development of coenzyme Q10 as a neurotherapeutic agent for retinal protection. Prog Brain Res 2008; 173: 575-582
21. Nakajima Y, Inokuchi Y, Nishi M, Shimazawa M, Otsubo K, Hara H. Coenzyme Q10 protects retinal cells against oxidative stress in vitro and in vivo. Brain Res 2008; 1226: 226-233
22. Lulli M, Witort E, Papucci L, Torre E, Schipani C, Bergamini C et al. Coenzyme Q10 instilled as eye drops on the cornea reaches the retina and protects retinal layers from apoptosis in a mouse model of kainate-induced retinal damage. Invest Ophthalmol Vis Sci 2012; 53: 8295-8302
23. Hernandez MR, Igoe F, Neufeld AH. Cell culture of the human lamina cribrosa. Invest Ophthalmol Vis Sci 1988; 29: 78-89
24. Yu AL, Fuchshofer R, Birke M, Kampik A, Bloemendal H, Welge-Lussen U. Oxidative stress and TGF-beta2 increase heat shock protein 27 expression in human optic nerve head astrocytes. Invest Ophthalmol Vis Sci 2008; 49: 5403-5411
25. Hernandez MR, Miao H, Lukas T. Astrocytes in glaucomatous optic neuropathy. Prog Brain Res 2008; 173: 353-373
26. John GB, Shang Y, Li L, Renken C, Mannella CA, Selker JM et al. The mitochondrial inner membrane protein mitofilin controls cristae morphology. Mol Biol Cell 2005; 16: 1543-1554
27. Van Laar VS, Dukes AA, Cascio M, Hastings TG. Proteomic analysis of rat brain mitochondria following exposure to dopamine quinone: Implications for Parkinson disease. Neurobiol Dis 2008; 29: 477-489
28. Marriage BJ, Clandinin MT, Macdonald IM, Glerum DM. Cofactor treatment improves ATP synthetic capacity in patients with oxidative phosphorylation disorders. Mol Genet Metab 2004; 81: 263-272
29. Haas RH. The evidence basis for coenzyme Q therapy in oxidative phosphorylation disease. Mitochondrion 2007; 7(Suppl): S136-S145
30. Fragaki K, Cano A, Benoist JF, Rigal O, Chaussenot A, Rouzier C et al. Fatal heart failure associated with CoQ10 and multiple OXPHOS deficiency in a child with propionic acidemia. Mitochondrion 2011; 11: 533-536
31. He Y, Leung KW, Zhang YH, Duan S, Zhong XF, Jiang RZ et al. Mitochondrial complex I defect induces ROS release and degeneration in trabecular meshwork cells of POAG patients: Protection by antioxidants. Invest Ophthalmol Vis Sci 2008; 49: 1447-1458
32. Malone PE, Hernandez MR. 4-Hydroxynonenal, a product of oxidative stress, leads to an antioxidant response in optic nerve head astrocytes. Exp Eye Res 2007; 84: 444-454
33. Mozaffarieh M, Flammer J. Is there more to glaucoma treatment than lowering IOP? Surv Ophthalmol 2007; 52(Suppl 2): S174-S179
34. Mozaffarieh M, Flammer J. A novel perspective on natural therapeutic approaches in glaucoma therapy. Expert Opin Emerg Drugs 2007; 12: 195-198
35. Mozaffarieh M, Grieshaber MC, Orgul S, Flammer J. The potential value of natural antioxidative treatment in glaucoma. Surv Ophthalmol 2008; 53: 479-505
36. Lee S, Sheck L, Crowston JG, Van Bergen NJ, O'Neill EC, O'Hare F et al. Impaired complex-I-linked respiration and ATP synthesis in primary open-Angle glaucoma patient lymphoblasts. Invest Ophthalmol Vis Sci 2012; 53: 2431-2437
37. Yu-Wai-Man P, Griffiths PG, Chinnery PF. Mitochondrial optic neuropathies-disease mechanisms and therapeutic strategies. Prog Retin Eye Res 2011; 30: 81-114
38. Yu AL, Moriniere J, Birke M, Neumann C, Fuchshofer R, Kampik A et al. Reactivation of optic nerve head astrocytes by TGF-beta2 and H2O2 is accompanied by increased Hsp32 and Hsp47 expression. Invest Ophthalmol Vis Sci 2009; 50: 1707-1717
39. Shults CW, Haas RH, Passov D, Beal MF. Coenzyme Q10 levels correlate with the activities of complexes I and II/III in mitochondria from parkinsonian and nonparkinsonian subjects. Ann Neurol 1997; 42: 261-264
40. Ferrante RJ, Andreassen OA, Dedeoglu A, Ferrante KL, Jenkins BG, Hersch SM et al. Therapeutic effects of coenzyme Q10 and remacemide in transgenic mouse models of Huntington's disease. J Neurosci 2002; 22: 1592-1599
41. Guo L, Cordeiro MF. Assessment of neuroprotection in the retina with DARC. Prog Brain Res 2008; 173: 437-450
42. Lulli M, Witort E, Papucci L, Torre E, Schiavone N, Dal Monte M et al. Coenzyme Q10 protects retinal cells from apoptosis induced by radiation in vitro and in vivo. J Radiat Res 2012; 53: 695-703
43. Rohl C, Armbrust E, Kolbe K, Lucius R, Maser E, Venz S et al. Activated microglia modulate astroglial enzymes involved in oxidative and inflammatory stress and increase the resistance of astrocytes to oxidative stress in vitro. Glia 2008; 56: 1114-1126
44. Bruce-Keller AJ, Geddes JW, Knapp PE, McFall RW, Keller JN, Holtsberg FW et al. Anti-death properties of TNF against metabolic poisoning: Mitochondrial stabilization by MnSOD. J Neuroimmunol 1999; 93: 53-71
45. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999; 98: 115-124
46. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O et al. Transcriptional co-Activator PGC-1 alpha drives the formation of slow-Twitch muscle fibres. Nature 2002; 418: 797-801
47. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 1998; 18: 231-236
48. Scarpulla RC. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 2002; 286: 81-89
49. Fosslien E. Mitochondrial medicine-molecular pathology of defective oxidative phosphorylation. Ann Clin Lab Sci 2001; 31: 25-67
50. Bargossi AM, Battino M, Gaddi A, Fiorella PL, Grossi G, Barozzi G et al. Exogenous CoQ10 preserves plasma ubiquinone levels in patients treated with 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Int J Clin Lab Res 1994; 24: 171-176
51. Fukui H, Moraes CT. The mitochondrial impairment, oxidative stress and neurodegeneration connection: Reality or just an attractive hypothesis? Trends Neurosci 2008; 31: 251-256
52. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell 2005; 120: 483-495
53. Carelli V, Rugolo M, Sgarbi G, Ghelli A, Zanna C, Baracca A et al. Bioenergetics shapes cellular death pathways in Leber's hereditary optic neuropathy: A model of mitochondrial neurodegeneration. Biochim Biophys Acta 2004; 1658: 172-179
54. Beal MF. Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 1995; 38: 357-366
55. Bergamini C, Moruzzi N, Sblendido A, Lenaz G, Fato R. A water soluble CoQ10 formulation improves intracellular distribution and promotes mitochondrial respiration in cultured cells. PLoS One 2012; 7: E33712
56. Quinzii CM, Lopez LC, Gilkerson RW, Dorado B, Coku J, Naini AB et al. Reactive oxygen species, oxidative stress, and cell death correlate with level of CoQ10 deficiency. FASEB J 2010; 24: 3733-3743
57. Fernandez-Marcos PJ, Auwerx J. Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr 2011; 93: 884S-890S.
58. Perkins GA, Renken CW, Song JY, Frey TG, Young SJ, Lamont S et al. Electron tomography of large, multicomponent biological structures. J Struct Biol 1997; 120: 219-227