Coenzyme Q10 ameliorates oxidative stress and prevents mitochondrial alteration in ischemic retinal injury
详细信息    查看全文
  • 作者:Dongwook Lee (1) (2)
    Keun-Young Kim (3)
    Myoung Sup Shim (1)
    Sang Yeop Kim (1)
    Mark H. Ellisman (3)
    Robert N. Weinreb (1)
    Won-Kyu Ju (1)
  • 关键词:Coenzyme Q10 ; Retinal ischemia ; Retinal ganglion cell ; Oxidative stress ; Mitochondrial transcription factor A ; Mitochondrial DNA
  • 刊名:Apoptosis
  • 出版年:2014
  • 出版时间:April 2014
  • 年:2014
  • 卷:19
  • 期:4
  • 页码:603-614
  • 全文大小:1,514 KB
  • 参考文献:1. Weinreb RN, Khaw PT (2004) Primary open-angle glaucoma. Lancet 363:1711-720 CrossRef
    2. Ju WK, Lindsey JD, Angert M, Patel A, Weinreb RN (2008) Glutamate receptor activation triggers OPA1 release and induces apoptotic cell death in ischemic rat retina. Mol Vis 14:2629-638
    3. Park SW, Kim KY, Lindsey JD, Heo H, Nguyen DH, Ellisman MH et al (2011) A selective inhibitor of drp1, mdivi-1, increases retinal ganglion cell survival in acute ischemic mouse retina. Invest Ophthalmol Vis Sci 52:2837-843 CrossRef
    4. Chan AS, Saraswathy S, Rehak M, Ueki M, Rao NA (2012) Neuroglobin protection in retinal ischemia. Invest Ophthalmol Vis Sci 53:704-11 CrossRef
    5. Lee D, Kim KY, Noh YH, Chai S, Lindsey JD, Ellisman MH et al (2012) Brimonidine blocks glutamate excitotoxicity-induced oxidative stress and preserves mitochondrial transcription factor a in ischemic retinal injury. PLoS One 7:e47098 CrossRef
    6. Liu Q, Ju WK, Crowston JG, Xie F, Perry G, Smith MA et al (2007) Oxidative stress is an early event in hydrostatic pressure induced retinal ganglion cell damage. Invest Ophthalmol Vis Sci 48:4580-589 CrossRef
    7. Kong YX, Van Bergen N, Trounce IA, Bui BV, Chrysostomou V, Waugh H et al (2011) Increase in mitochondrial DNA mutations impairs retinal function and renders the retina vulnerable to injury. Aging Cell 10:572-83 CrossRef
    8. Oguni M, Tanaka O, Tamura H, Shinohara H, Kato K, Setogawa T (1995) Ontogeny of copper-zinc and manganese superoxide dismutase in the developing rat retina: immunohistochemical and immunochemical study. Ophthalmic Res 27:227-33 CrossRef
    9. Fukui M, Zhu BT (2010) Mitochondrial superoxide dismutase SOD2, but not cytosolic SOD1, plays a critical role in protection against glutamate-induced oxidative stress and cell death in HT22 neuronal cells. Free Radic Biol Med 48:821-30 CrossRef
    10. Jarrett SG, Lin H, Godley BF, Boulton ME (2008) Mitochondrial DNA damage and its potential role in retinal degeneration. Prog Retin Eye Res 27:596-07 CrossRef
    11. Lee S, Van Bergen NJ, Kong GY, Kong GY, Chrysostomou V, Waugh HS et al (2011) Mitochondrial dysfunction in glaucoma and emerging bioenergetic therapies. Exp Eye Res 93:204-12 CrossRef
    12. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M et al (1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18:231-36 CrossRef
    13. Bonawitz ND, Clayton DA, Shadel GS (2006) Initiation and beyond: multiple functions of the human mitochondrial transcription machinery. Mol Cell 24:813-25 CrossRef
    14. Falkenberg M, Larsson NG, Gustafsson CM (2007) DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 76:679-99 CrossRef
    15. Ngo HB, Kaiser JT, Chan DC (2011) The mitochondrial transcription and packaging factor Tfam imposes a U-turn on mitochondrial DNA. Nat Struct Mol Biol 18:1290-296 CrossRef
    16. Xu S, Zhong M, Zhang L, Wang Y, Zhou Z, Hao Y et al (2009) Overexpression of Tfam protects mitochondria against beta-amyloid-induced oxidative damage in SH-SY5Y cells. FEBS J 276:3800-809 CrossRef
    17. Hokari M, Kuroda S, Kinugawa S, Ide T, Tsutsui H, Iwasaki Y (2010) Overexpression of mitochondrial transcription factor A (TFAM) ameliorates delayed neuronal death due to transient forebrain ischemia in mice. Neuropathology 30:401-07 CrossRef
    18. Piao Y, Kim HG, Oh MS, Pak YK (2012) Overexpression of TFAM, NRF-1 and myr-AKT protects the MPP(+)-induced mitochondrial dysfunctions in neuronal cells. Biochim Biophys Acta 1820:577-85 CrossRef
    19. Yin W, Signore AP, Iwai M, Cao G, Gao Y, Chen J (2008) Rapidly increased neuronal mitochondrial biogenesis after hypoxic-ischemic brain injury. Stroke 39:3057-063 CrossRef
    20. Beal MF, Shults CW (2003) Effects of Coenzyme Q10 in Huntington’s disease and early Parkinson’s disease. Biofactors 18:153-61 CrossRef
    21. McCarthy S, Somayajulu M, Sikorska M, Borowy-Borowski H, Pandey S (2004) Paraquat induces oxidative stress and neuronal cell death; neuroprotection by water-soluble Coenzyme Q10. Toxicol Appl Pharmacol 201:21-1 CrossRef
    22. Bessero AC, Clarke PG (2010) Neuroprotection for optic nerve disorders. Curr Opin Neurol 23:10-5 CrossRef
    23. Nakajima Y, Inokuchi Y, Nishi M, Shimazawa M, Otsubo K, Hara H (2008) Coenzyme Q10 protects retinal cells against oxidative stress in vitro and in vivo. Brain Res 1226:226-33 CrossRef
    24. Russo R, Cavaliere F, Rombola L, Gliozzi M, Cerulli A, Nucci C et al (2008) Rational basis for the development of coenzyme Q10 as a neurotherapeutic agent for retinal protection. Prog Brain Res 173:575-82 CrossRef
    25. Nucci C, Tartaglione R, Cerulli A, Mancino R, Spano A, Cavaliere F et al (2007) Retinal damage caused by high intraocular pressure-induced transient ischemia is prevented by coenzyme Q10 in rat. Int Rev Neurobiol 82:397-06 CrossRef
    26. Yang L, Calingasan NY, Wille EJ, Cormier K, Smith K, Ferrante RJ et al (2009) Combination therapy with coenzyme Q10 and creatine produces additive neuroprotective effects in models of Parkinson’s and Huntington’s diseases. J Neurochem 109:1427-439 CrossRef
    27. Ju WK, Misaka T, Kushnareva Y, Nakagomi S, Agarwal N, Kubo Y et al (2005) OPA1 expression in the normal rat retina and optic nerve. J Comp Neurol 488:1-0 CrossRef
    28. Galindo-Romero C, Aviles-Trigueros M, Jimenez-Lopez M, Vallente-Soriano FJ, Sallinas-Navarro M, Nadal-Nicolas F et al (2011) Axotomy-induced retinal ganglion cell death in adult mice: quantitative and topographic time course analyses. Exp Eye Res 92:377-87 CrossRef
    29. Galindo-Romero C, Valiente-Soriano FJ, Jimenez-Lopez M, Valiente-Soriano FJ, Salinas-Navarro M, Nadal-Nicolas F et al (2013) Effect of brain-derived neurotrophic factor on mouse axotomized retinal ganglion cells and phagocytic microglia. Invest Ophthalmol Vis Sci 54:974-85 CrossRef
    30. Nadal-Nicolas FM, Jimenez-Lopez M, Sobrado-Calvo P, Nieto-Lopex L, Canovas-Martinez I, Salinas-Navarro M et al (2009) Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci 50:3860-868 CrossRef
    31. Alavi MV, Bette S, Schimpf S, Schuettauf F, Schraermeyer U, Wehrl HF et al (2007) A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. Brain 130:1029-042 CrossRef
    32. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-108 CrossRef
    33. Zhi Z, Cepurna W, Johnson E, Shen T, Morrison J, Wang RK (2011) Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography. Biomed Opt Express 2:579-91 CrossRef
    34. Ju WK, Kim KY (2011) Measuring glutamate receptor activation-induced apoptotic cell death in ischemic rat retina using the TUNEL assay. Methods Mol Biol 740:149-56 CrossRef
    35. Lulli M, Witort E, Papucci L, Torre E, Schipani C, Bergamini C et al (2012) 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 53:8295-302 CrossRef
    36. Lulli M, Witort E, Papucci L, Torre E, Schiavone N, Dal Monte M et al (2012) Coenzyme Q10 protects retinal cells from apoptosis induced by radiation in vitro and in vivo. J Radiat Res 53:695-03 CrossRef
    37. Tezel G, Chauhan BC, LeBlanc RP, Wax MB (2003) Immunohistochemical assessment of the glial mitogen-activated protein kinase activation in glaucoma. Invest Ophthalmol Vis Sci 44:3025-033
    38. Schuettauf F, Rejdak R, Walski M, Frontczak-Baniewicz M, Voelker M, Blastsios G et al (2004) Retinal neurodegeneration in the DBA/2?J mouse-a model for ocular hypertension. Acta Neuropathol 107:352-58 CrossRef
    39. Bosco A, Inman DM, Steele MR, Wu G, Soto I, Marsh-Armstrong N et al (2008) Reduced retina microglial activation and improved optic nerve integrity with minocycline treatment in the DBA/2?J mouse model of glaucoma. Invest Ophthalmol Vis Sci 49:1437-446 CrossRef
    40. Ferrante RJ, Andreassen OA, Dedeoglu A, Ferrante KL, Jenkins BG, Hersch SM et al (2002) Therapeutic effects of coenzyme Q10 and remacemide in transgenic mouse models of Huntington’s disease. J Neurosci 22:1592-599
    41. Guo L, Cordeiro MF (2008) Assessment of neuroprotection in the retina with DARC. Prog Brain Res 173:437-50 CrossRef
    42. Li G, Zou L, Jack CR Jr, Yang Y, Yang ES (2007) Neuroprotective effect of Coenzyme Q10 on ischemic hemisphere in aged mice with mutations in the amyloid precursor protein. Neurobiol Aging 28:877-82 CrossRef
    43. Bhagavan HN, Chopra RK (2006) Coenzyme Q10: absorption, tissue uptake, metabolism and pharmacokinetics. Free Radic Res 40:445-53 CrossRef
    44. Ho YS, Crapo JD (1988) Isolation and characterization of complementary DNAs encoding human manganese-containing superoxide dismutase. FEBS Lett 229:256-60 CrossRef
    45. Kasahara E, Lin LR, Ho YS, Reddy VN (2005) SOD2 protects against oxidation-induced apoptosis in mouse retinal pigment epithelium: implications for age-related macular degeneration. Invest Ophthalmol Vis Sci 46:3426-434 CrossRef
    46. Hu Y, Rosen DG, Zhou Y, Feng L, Yang G, Liu J et al (2005) Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: role in cell proliferation and response to oxidative stress. J Biol Chem 280:39485-9492 CrossRef
    47. Yokoyama K, Nakamura K, Kimura M, Nomoto K, Itoman M (1999) Effect of coenzyme Q10 on superoxide production in rats with reperfusion injuries. Scand J Plast Reconstr Surg Hand Surg 33:1- CrossRef
    48. Liu Y, Tang L, Chen B (2012) Effects of antioxidant gene therapy on retinal neurons and oxidative stress in a model of retinal ischemia/reperfusion. Free Radic Biol Med 52:909-15 CrossRef
    49. Chen B, Caballero S, Seo S, Grant MB, Lewin AS (2009) Delivery of antioxidant enzyme genes to protect against ischemia/reperfusion-induced injury to retinal microvasculature. Invest Ophthalmol Vis Sci 50:5587-595 CrossRef
    50. Rohl C, Armbrust E, Kolbe K, Lucius R, Maser E, Venz S et al (2008) Activated microglia modulate astroglial enzymes involved in oxidative and inflammatory stress and increase the resistance of astrocytes to oxidative stress in vitro. Glia 56:1114-126 CrossRef
    51. Bruce-Keller AJ, Geddes JW, Knapp PE, McFall RQ, Keller JN, Holtsberg FW et al (1999) Anti-death properties of TNF against metabolic poisoning: mitochondrial stabilization by MnSOD. J Neuroimmunol 93:53-1 CrossRef
    52. Malone PE, Hernandez MR (2007) 4-Hydroxynonenal, a product of oxidative stress, leads to an antioxidant response in optic nerve head astrocytes. Exp Eye Res 84:444-54 CrossRef
    53. Hernandez MR, Miao H, Lukas T (2008) Astrocytes in glaucomatous optic neuropathy. Prog Brain Res 173:353-73 CrossRef
    54. Lee I, Lee H, Kim JM, Chae EH, Kim SJ, Chang N (2007) Short-term hyperhomocysteinemia-induced oxidative stress activates retinal glial cells and increases vascular endothelial growth factor expression in rat retina. Biosci Biotechnol Biochem 71:1203-210 CrossRef
    55. Luo C, Yang X, Kain AD, Powell DW, Kuehn MH, Tezel G (2010) Glaucomatous tissue stress and the regulation of immune response through glial Toll-like receptor signaling. Invest Ophthalmol Vis Sci 51:5697-707 CrossRef
    56. McElnea EM, Quill B, Docherty NG, Irnaten M, Siah WF, Clark AF et al (2011) Oxidative stress, mitochondrial dysfunction and calcium overload in human lamina cribrosa cells from glaucoma donors. Mol Vis 17:1182-191
    57. Ramirez AI, Salazar JJ, de Hoz R, Rojas B, Gallego BI, Sallinas-Navarro M et al (2010) Quantification of the effect of different levels of IOP in the astroglia of the rat retina ipsilateral and contralateral to experimental glaucoma. Invest Ophthalmol Vis Sci 51:5690-696 CrossRef
    58. Gallego BI, Salazar JJ, de Hoz R, Rojas B, Ramirez AI, Salinas-Navarro M et al (2012) IOP induces upregulation of GFAP and MHC-II and microglia reactivity in mice retina contralateral to experimental glaucoma. J Neuroinflammation 9:92 CrossRef
    59. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ et al (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727-30 CrossRef
    60. Wasiak S, Zunino R, McBride HM (2007) Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J Cell Biol 177:439-50 CrossRef
    61. Antonsson B, Conti F, Ciavatta A, Montessuit S, Lewis S, Martinou I et al (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277:370-72 CrossRef
    62. Schlesinger PH, Gross A, Yin XM, Yamamoto K, Saito M, Waksman G et al (1997) Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc Natl Acad Sci USA 94:11357-1362 CrossRef
    63. Desagher S, Martinou JC (2000) Mitochondria as the central control point of apoptosis. Trends Cell Biol 10:369-77 CrossRef
    64. Oltvai ZN, Milliman CL, Korsmeyer SJ (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-19 CrossRef
    65. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80:285-91 CrossRef
    66. Tsujimoto Y, Shimizu S (2007) Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 12:835-40 CrossRef
    67. Linkermann A, Brasen JH, Darding M, Jin MK, Sanz AB, Heller JO et al (2013) Two independent pathways of regulated necrosis mediate ischemia–reperfusion injury. Proc Natl Acad Sci USA 110:12024-2029 CrossRef
    68. Chan SW, Nguyen PN, Ayele D, Chevalier S, Aprikian A, Chen JZ (2011) Mitochondrial DNA damage is sensitive to exogenous H(2)O(2) but independent of cellular ROS production in prostate cancer cells. Mutat Res 716:40-0 CrossRef
    69. Beal MF (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 38:357-66 CrossRef
    70. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K et al (2004) Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 13:935-44 CrossRef
  • 作者单位:Dongwook Lee (1) (2)
    Keun-Young Kim (3)
    Myoung Sup Shim (1)
    Sang Yeop Kim (1)
    Mark H. Ellisman (3)
    Robert N. Weinreb (1)
    Won-Kyu Ju (1)

    1. Laboratory for Optic Nerve Biology, Department of Ophthalmology, Hamilton Glaucoma Center, University of California San Diego, 9415 Campus Point Drive, La Jolla, CA, 92037, USA
    2. Research Institute of Clinical Medicine of Chonbuk National University-Biomedical Research Institute, Chonbuk National University Hospital, Chonju, Chonbuk, Republic of Korea
    3. Department of Neuroscience, Center for Research on Biological Systems, National Center for Microscopy and Imaging Research, University of California San Diego, La Jolla, CA, USA
  • ISSN:1573-675X
文摘
Coenzyme Q10 (CoQ10) acts by scavenging reactive oxygen species for protecting neuronal cells against oxidative stress in neurodegenerative diseases. We tested whether a diet supplemented with CoQ10 ameliorates oxidative stress and mitochondrial alteration, as well as promotes retinal ganglion cell (RGC) survival in ischemic retina induced by intraocular pressure elevation. A CoQ10 significantly promoted RGC survival at 2?weeks after ischemia. Superoxide dismutase 2 (SOD2) and heme oxygenase-1 (HO-1) expression were significantly increased at 12?h after ischemic injury. In contrast, the CoQ10 significantly prevented the upregulation of SOD2 and HO-1 protein expression in ischemic retina. In addition, the CoQ10 significantly blocked activation of astroglial and microglial cells in ischemic retina. Interestingly, the CoQ10 blocked apoptosis by decreasing caspase-3 protein expression in ischemic retina. Bax and phosphorylated Bad (pBad) protein expression were significantly increased in ischemic retina at 12?h. Interestingly, while CoQ10 significantly decreased Bax protein expression in ischemic retina, CoQ10 showed greater increase of pBad protein expression. Of interest, ischemic injury significantly increased mitochondrial transcription factor A (Tfam) protein expression in the retina at 12?h, however, CoQ10 significantly preserved Tfam protein expression in ischemic retina. Interestingly, there were no differences in mitochondrial DNA content among control- or CoQ10-treated groups. Our findings demonstrate that CoQ10 protects RGCs against oxidative stress by modulating the Bax/Bad-mediated mitochondrial apoptotic pathway as well as prevents mitochondrial alteration by preserving Tfam protein expression in ischemic retina. Our results suggest that CoQ10 may provide neuroprotection against oxidative stress-mediated mitochondrial alterations in ischemic retinal injury.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700