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REVIEW ARTICLE

Do glial cells play an anti-oxidative role in Huntington's disease?

, , , , , , & show all
Pages 1135-1144 | Received 13 May 2014, Accepted 16 Jun 2014, Published online: 14 Aug 2014

References

  • Aiken CT, Kaake RM, Wang X, Huang L. Oxidative Stress-Mediated Regulation of Proteasome Complexes. Mol Cell Proteomics 2011;10:R110.006924.
  • Velaga MK, Basuri CK, Robinson Taylor KS, Yallapragada PR, Rajanna S, Rajanna B. Ameliorative effects of Bacopa monniera on lead-induced oxidative stress in different regions of rat brain. Drug Chem Toxicol 2013;37:357–364.
  • Koopman WJ, Nijtmans LG, Dieteren CE, Roestenberg P, Valsecchi F, Smeitink JA, Willems PH. Mammalian mitochondrial complex i: biogenesis, regulation, and reactive oxygen species generation. Antioxid Redox Signal 2010;12:1431–1470.
  • Fulda S, Gorman AM, Hori O, Samali A. Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010;2010:214074.
  • Chan DC. Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006;125:1241–1252.
  • Besson MT, Dupont P, Fridell YWC, Lievens JC. Increased energy metabolism rescues glia-induced pathology in a Drosophila model of Huntington’s disease. Hum Mol Gen 2010;19:3372–3382.
  • Zhang M, An C, Gao Y, Leak RK, Chen J, Zhang F. Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Prog Neurobiol 2013;100:30–47.
  • Ruiz C, Casarejos MJ, Gomez A, Solano R, de Yebenes JG, Mena MA. Protection by glia-conditioned medium in a cell model of Huntington disease. PLoS Curr 2012;4:e4fbca54a2028b.
  • Sorolla MA, Reverter-Branchat G, Tamarit J, Ferrer I, Ros J, Cabiscol E. Proteomic and oxidative stress analysis in human brain samples of Huntington disease. Free Radic Biol Med 2008;45:667–678.
  • Sieradzan KA, Mann DMA. The selective vulnerability of nerve cells in Huntington’s disease. Neuropath Appl Neurobiol 2001;27:1–21.
  • Kumar P, Kalonia H, Kumar A. Huntington's disease: pathogenesis to animal models. Pharmacological Reports 2010;62:1–14.
  • Tunez I, Tasset I, Perez-De La Cruz V, Santamaria A. 3-Nitropropionic acid as a tool to study the mechanisms involved in Huntington’s disease: past, present and future. Molecules 2010;15:878–916.
  • Chandra A, Johri A, Beal MF. Prospects for neuroprotective therapies in prodromal Huntington’s disease. Mov Disord 2014;29:285–293.
  • Cabezas R, El-Bacha RS, Gonzalez J, Barreto GE. Mitochondrial functions in astrocytes: neuroprotective implications from oxidative damage by rotenone. Neurosci Res 2012;74:80–90.
  • Gil JM, Rego AC. Mechanisms of neurodegeneration in Huntington’s disease. Eur J Neurosci 2008;27:2803–2820.
  • Butterfield DA, Kanski J. Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech Ageing Dev. 2001;122:945–962.
  • Choo YS, Mao Z, Johnson GV, Lesort M. Increased glutathione levels in cortical and striatal mitochondria of the R6/2 Huntington’s disease mouse model. Neurosci Lett 2005;386:63–68.
  • Xueping C, Chunyan G, Kong J. Oxidative stress in neurodegenerative diseases. Neural Regener Res 2012;7:376–385.
  • de Vries HE, Witte M, Hondius D, Rozemuller AJ, Drukarch B, Hoozemans J, van Horssen J. Nrf2-induced antioxidant protection: a promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med 2008;45:1375–1383.
  • Browne SE, Beal MF. Oxidative Damage in Huntington's Disease Pathogenesis. Antioxid Redox Signal 2006;8:2061–2073.
  • Trushina E, McMurray CT. Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience 2007;145:1233–1248.
  • Melkani GC, Trujillo AS, Ramos R, Bodmer R, Bernstein SI, Ocorr K. Huntington’s disease induced cardiac amyloidosis is reversed by modulating protein folding and oxidative stress pathways in the Drosophila heart. PLoS Genet 2013;9:e1004024.
  • Bogdanov MB, Ferrante RJ, Kuemmerle S, Peter K, FlintBeal M. Increased vulnerability to 3-Nitropropionic acid in an animal model of Huntington’s disease. J Neurochem 1998;71:2642–2644.
  • Klivenyi P, Ferrante RJ, Gardian G, Browne S, Chabrier P-E, Beal MF. Increased survival and neuroprotective effects of BN82451 in a transgenic mouse model of Huntington’s disease. J Neurochem 2003;87:272–272.
  • Ferrante RJ, Andreassen OA, Dedeoglu A, Ferrante LK, Jenkins BG, Hersch SM, Beal MF. Therapeutic Effects of Coenzyme Q10 and Remacemide inTransgenic Mouse Models of Huntington's Disease. J Neurosci 2002;22: 1592–1599.
  • Ramaswamy S, McBride JL, Kordower JH. Animal models of Huntington's disease. ILAR Journal 2007;48:356–373.
  • Joshi G, Johnson JA. The Nrf2-ARE pathway: a valuable therapeutic target for the treatment of neurodegenerative diseases. Recent Pat CNS Drug Discov. 2012:218–229.
  • Calkins MJ, Jakel RJ, Johnson DA, Chan K, Kan YW, Johnson JA. Protection from mitochondrial complex II inhibition in vitro and in vivo by Nrf2-mediated transcription. Proc Natl Acad Sci U S A 2005;102:244–249.
  • Kim GW, Chan PH. Oxidative stress and neuronal DNA fragmentation mediate age-dependent vulnerability to the mitochondrial toxin, 3-nitropropionic acid, in the mouse striatum. Neurobiol Dis 2001;8:114–126.
  • Kim GW, Chan PH. Involvement of superoxide in excitotoxicity and dna fragmentation in striatal vulnerability in mice after treatment with the mitochondrial toxin, 3-Nitropropionic acid. J Cereb Blood Flow Metab 2002;22:798–809.
  • Kim GW, Copin J-C, Kawase M, Chen SF, Sato S, Gobbel GT, Chan PH. Excitotoxicity is required for induction of oxidative stress and apoptosis in mouse striatum by the mitochondrial toxin, 3-Nitropropionic acid. J Cereb Blood Flow Metab 2000;20:119–129.
  • Schulz JB, Matthews RT, Henshaw DR, Beal MF. Neuroprotective strategies for treatment of lesions produced by mitochondrial toxins: implications for neurodegenerative diseases. Neuroscience 1996;71:1043–1048.
  • McCracken E, Dewar D, Hunter AJ. White matter damage following systemic injection of the mitochondrial inhibitor 3-nitropropionic acid in rat. Brain Research 2001;892: 329–335.
  • Alston TA, Mela L, Bright HJ. 3-Nitropropionate, the toxic substance of Indigofera, is a suicide inactivator of succinate dehydrogenase. Proc Natl Acad Sci. 1977;74:3767–3771.
  • Andreassen OA, Ferrante RJ, Dedeoglu A, Albers DW, Klivenyi P, Carlson EJ, et al. Mice with a partial deficiency of manganese superoxide dismutase show increased vulnerability to the mitochondrial toxins malonate, 3-nitropropionic acid, and MPTP. Exp Neurol 2001;167:189–195.
  • Li XJ, Li S. Large animal models of Huntington's disease. Curr Top Behav Neurosci 2013.
  • Pouladi MA, Morton AJ, Hayden MR. Choosing an animal model for the study of Huntington’s disease. Nat Rev Neurosci 2013;14:708–721.
  • Carreira JC, Jahanshahi A, Zeef D, Kocabicak E, Vlamings R, von Horsten S, Temel Y. Transgenic Rat Models of Huntington’s Disease. Curr Top Behav Neurosci 2013.
  • Perluigi M, Poon HF, Maragos W, Pierce WM, Klein JB, Calabrese V, Cini C, Marco CD, Butterfield DA. Proteomic analysis of protein expression and oxidative modification in R6/2 transgenic mice. Mol Cell Proteomics 2005;4: 1849–1861.
  • Liu W, Tang Y, Feng J. Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci 2011;89:141–146.
  • Aldskogius HK, Kozlova EN. Central neuron-gial and gial-gial interactions following axon injury. Prog Neurobiol 1998;55:1–26.
  • Colangelo AM, Cirillo G, Lavitrano ML, Alberghina L, Papa M. Targeting reactive astrogliosis by novel biotechnological strategies. Biotechnol Adv 2012;30:261–271.
  • Singh S, Swarnkar S, Goswami P, Nath C. Astrocytes and microglia: responses to neuropathological conditions. Int J Neurosci 2011;121:589–597.
  • Calkins MJ, Vargas MR, Johnson DA, Johnson JA. Astrocyte-specific overexpression of Nrf2 protects striatal neurons from mitochondrial complex II inhibition. Toxicological Sciences 2010;115:557–568.
  • Colangelo AM, Alberghina L, Papa M. Astrogliosis as a therapeutic target for neurodegenerative diseases. Neurosci Lett 2014.
  • Falcao AS, Silva RF, Vaz AR, Silva SL, Fernandes A, Brites D. Cross-talk between neurons and astrocytes in response to bilirubin: early beneficial effects. Neurochem Res 2013;38:644–659.
  • Barreto GE, Gonzalez J, Torres Y, Morales L. Astrocytic-neuronal crosstalk: implications for neuroprotection from brain injury. Neurosci Res 2011;71:107–113.
  • Singh S, Misiak M, Beyer C, Arnold S. Cytochrome c oxidase isoform IV-2 is involved in 3-nitropropionic acid-induced toxicity in striatal astrocytes. Glia 2009;57:1480–1491.
  • Maragakis NJ, Rothstein JD. Mechanisms of Disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol 2006;2:679–689.
  • Kipp M, Karakaya S, Pawlak J, Araujo-Wright G, Arnold S, Beyer C. Estrogen and the development and protection of nigrostriatal dopaminergic neurons: concerted action of a multitude of signals, protective molecules, and growth factors. Front Neuroendocrinol 2006;27:376–390.
  • Dugan LL, Bruno VMG, Amagasu SM, Giffard RG. Glia modulate the response of murine cortical neurons to excitotoxicity: glia exacerbate AMPA neurotoxicity. J Neurosci 1995;15:4545–4555.
  • Barreto GE, Gonzalez J, Capani F, Morales L. Neuroprotective agents in brain injury: a partial failure? Int J Neurosci 2012;122:223–226.
  • Fernandez-Fernandez S, Almeida A, Bolanos JP. Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochem J 2012;443:3–11.
  • Bolaños JP, Almeida A, Stewart V, Peuchen S, Land JM, Clark JB, Heales SJR. Nitric Oxide-Mediated Mitochondrial Damage in the Brain: Mechanisms and Implications for Neurodegenerative Diseases. J Neurochem 1997:2227–2240.
  • Allaman I, Belanger M, Magistretti PJ. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 2011;34:76–87.
  • Shih AY, Erb H, Sun X, Toda S, Kalivas PW, Murphy TH. Cystine/glutamate exchange modulates glutathione supply for neuroprotection from oxidative stress and cell proliferation. J Neurosci 2006;26:10514–10523.
  • Vargas MR, Johnson JA. The Nrf2–ARE cytoprotective pathway in astrocytes. Expert Rev Mol Med 2009;11:e17.
  • Chen PC, Vargas MR, Pani AK, Smeyne RJ, Johnson DA, Kan YW, Johnson JA. Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson’s disease: Critical role for the astrocyte. Proc Natl Acad Sci U S A 2009;106: 2933–2938.
  • Fu R, Shen Q, Xu P, Luo JJ, Tang Y. Phagocytosis of Microglia in the Central Nervous System Diseases. Mol Neurobiol 2014;49:1422–1434.
  • Soulet D, Rivest S. Microglia. Curr Biol 2008;18: R506–R508.
  • Stollg G, Jander S. The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol 1999;58:233–247.
  • Nimmerjahn A, Kirchhoff F, Helmchen F. Resting Microglial Cells Are Highly Dynamic Surveillants if Brain Parenchymia in vivo. Science 2005;308:1314.
  • Gehrmann J, Matsumoto Y, Kreutzberg GW. Microgla: intrinsic immuneffector cell of the brain. Brain Res Rev 1995;20:269–287.
  • Kim SU, de Vellis J. Microglia in health and disease. J Neurosci Res 2005;81:302–313.
  • Tseng G-F, Wang Y-J, Lai Q-C. Perineuronal microglial reactivity following proximal and distal axotomy of rat rubrospinal neurons. Brain Res 1996;715:32–43.
  • Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. GLIA 1996;19:312–318.
  • Polazzi E, Gianni T, Contestabile A. Microglial cells protect cerebellar granule neurons from apoptosis: evidence for reciprocal signaling. Glia 2001;36:271–280.
  • Elkabes S, DiCicco-Bloom EM, Black IB. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 1996;16:2508–2521.
  • Harjes P, Wanker EE. The hunt for huntingtin function: interaction partners tell many different stories. Trends Biochem Sci 2003;28:425–433.
  • Feany MB, Spada ARL. Polyglutamines stop traffic: axonal transport as a common target in neurodegenerative diseases. Neuron 2003;40:1–2.
  • Streit WJ, Mrak RE, Griffin WS. Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 2004;1:14.
  • Ridet JL, Malhotra SK, Privat A, Gage FH. Reactive astrocytes: cellular and molecular cues to biological function. TINS 1997;20:570–577.
  • Pekny M, Nilsson M. Astrocyte activation and reactive gliosis. Glia 2005;50:427–434.
  • Herrero-Mendez A, Almeida A, Fernandez E, Maestre C, Moncada S, Bolanos JP. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat Cell Biol 2009;11:747–752.
  • Yu Z-X, Li S-H, Evans J, Pillarisetti A, Li H, Li X-J. Mutant Huntingtin Causes context-dependent neurodegeneration in mice with Huntington’s disease. J Neurosci 2003;23: 2193–2202.
  • Reddy PH, Williams M, Charles V, Garrett L, Pike-Buchanan L, Whetsell OW Jr, et al. Behavioural abnormalities and selective neuronal loss in HD transgenic mice expressing mutated full-length HD cDNA. Nature Genetics 1998;20:198–202.
  • Perucho J, Casarejos MJ, Gomez A, Ruiz C, Fernandez-Estevez MA, Munoz MP, et al. Striatal infusion of glial conditioned medium diminishes huntingtin pathology in r6/1 mice. PLoS One 2013;8:e73120.
  • Bradford J, Shin JY, Roberts M, Wang CE, Sheng G, Li S, Li XJ. Mutant Huntingtin in glial cells exacerbates neurological symptoms of Huntington disease mice. J Biol Chem 2010;285:10653–10661.
  • Bradford J, Shin JY, Roberts M, Wang CE, Li XJ, Li S. Expression of mutant huntingtin in mouse brain astrocytes causes age-dependent neurological symptoms. Proceedings of the National Academy of Sciences 2009;106: 22480–22485.
  • Shin J-Y, Fang Z-H, Yu Z-X, Wang C-E, Li S-H, Li X-J. Expression of mutant huntingtin in glial cells contributes to neuronal excitotoxicity. J Cell Biol 2005;171:1001–1012.
  • Tydlacka S, Wang CE, Wang X, Li S, Li XJ. Differential activities of the ubiquitin-proteasome system in neurons versus glia may account for the preferential accumulation of misfolded proteins in neurons. J Neurosci 2008;28: 13285–13295.
  • Brouillet E, Jacquard C, Bizat N, Blum D. 3-Nitropropionic acid: a mitochondrial toxin to uncover physiopathological mechanisms underlying striatal degeneration in Huntington’s disease. J Neurochem 2005;95:1521–1540.
  • Patten DA, Germain M, Kelly MA, Slack RS. Reactive oxygen species: stuck in the middle of neurodegeneration. J Alzheimers Dis 2010;20:S357–367.
  • Magesh S, Chen Y, Hu L. Small molecule modulators of Keap1-Nrf2-ARE pathway as potential preventive and therapeutic agents. Med Res Rev 2012;32:687–726.
  • Jung KA, Kwak MK. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 2010;15:7266–7291.
  • Zhang DD. The Nrf2-Keap1-ARE Signaling Pathway: The regulation and dual function of Nrf2 in cancer. Antioxid Redox Signal 2010;13:1623–1626.
  • Zhang DD, Lo SC, Sun Z, Habib GM, Lieberman MW, Hannink M. Ubiquitination of Keap1, a BTB-Kelch substrate adaptor protein for Cul3, targets Keap1 for degradation by a proteasome-independent pathway. J Biol Chem 2005;280:30091–30099.
  • Hong F, Sekhar KR, Freeman ML, Liebler DC. Specific patterns of electrophile adduction trigger Keap1 ubiquitination and Nrf2 activation. J Biol Chem 2005;280: 31768–31775.
  • Zhang DD, Hannink M. Distinct cysteine residues in Keap1 are required for Keap1-Dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 2003;23:8137–8151.
  • Sykiotis GP, Habeos IG, Samuelson AV, Bohmann D. The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr Opin Clin Nutr Metab Care 2011;14:41–48.
  • Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J Biol Chem 2003;278:12029–12038.
  • Scapagnini G, Vasto S, Abraham NG, Caruso C, Zella D, Fabio G. Modulation of Nrf2/ARE pathway by food polyphenols: a nutritional neuroprotective strategy for cognitive and neurodegenerative disorders. Mol Neurobiol 2011;44: 192–201.
  • Dowell JA, Johnson JA. Mechanisms of Nrf2 Protection in astrocytes as identified by quantitative proteomics and siRNA screening. PLoS ONE 2013;8:e70163.
  • Talalay P, Dinkova-Kostova AT. Role of Nicotinamide Quinone Oxidoreductase 1 (NQO1) in Protection against Toxicity of Electrophiles and Reactive Oxygen Intermediates. Methods Enzymol 2004;382:355–364.
  • Wang XJ, Hayes JD, Henderson CJ, Wolf CR. Identification of retinoic acid as an inhibitor of transcription factor Nrf2 through activation of retinoic acid receptor alpha. Proc Natl Acad Sci U S A 2007;104:19589–19594.
  • Kraft AD, Johnson DA, Johnson JA. Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. J Neurosci 2004;24:1101–1112.
  • Shih AY, Johnson DA, Wong G, Murphy TH. Coordinate Regulation of Glutathione Biosynthesis and Release by Nrf2-Expressing Glia Potently Protects Neurons from Oxidative Stress. J Neurosci 2003;23:3394–3406.
  • Shih AY, Johnson DA, Wong G, Kraft AD, Jiang L, Erb H, et al. Coordinate Regulation of Glutathione Biosynthesis and Release by Nrf2-Expressing Glia Potently Protects Neurons from Oxidative Stress. J Neurosci 2003;23:3394–3406.
  • Tanaka J, Toku K, Zhang B, Ishihara K, Sakanaka M, Maeda N. Astrocytes prevent neuronal death induced by reactive oxygen and nitrogen species. Glia 1999:85–96.
  • Desagher S, Glowinski J, Premont J. Astrocytes Protect Neurons from Hydrogen Peroxide Toxicity. J Neurosci 1996;16:2553–2562.
  • Bronstein DM, Perez-Otano I, Sun V, Sawin SBM, Chan J, G-C W, et al. Glia-dependent neurotoxicity and neuroprotection in mesencephalic cultures. Brain Res 1995;704: 112–116.
  • Shih AY, Imbeault S, Barakauskas V, Erb H, Jiang L, Li P, Murphy TH. Induction of the Nrf2-driven antioxidant response confers neuroprotection during mitochondrial stress in vivo. J Biol Chem 2005;280:22925–22936.
  • Ma Q, Battelli L, Hubbs AF. Multiorgan autoimmune inflammation, enhanced lymphoproliferation, and impaired homeostasis of reactive oxygen species in mice lacking the antioxidant-activated transcription factor Nrf2. Am J Pathol 2006;168:1960–1974.
  • Vargas MR, Johnson DA, Sirkis DW, Messing A, Johnson JA. Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J Neurosci 2008;28:13574–13581.
  • Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007;47:89–116.
  • Lee JS, Surh YJ. Nrf2 as a novel molecular target for chemoprevention. Cancer Lett 2005;224:171–184.
  • Lee JM, Li J, Johnson DA, Stein TD, Kraft AD, Calkins MJ, et al. Nrf2, a multi-organ protector? FASEB J 2005;19: 1061–1066.
  • Lee J-M, Johnson JA. An Important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 2004;37:139–143.
  • Linseman DA. Targeting oxidative stress for neuroprotection. Antioxid Redox Signal 2009;11:421–424.
  • Zhang L, Zhu Z, Liu J, Zhu Z, Hu Z. Protective effect of N-acetylcysteine (NAC) on renal ischemia/reperfusion injury through Nrf2 signaling pathway. J Recept Signal Transduct Res 2014. Doi: 10.3109/10799893.2014.908916.
  • Blanco-Ayala T, Anderica-Romero AC, Pedraza-Chaverri J. New insights into antioxidant strategies against paraquat toxicity. Free Radic Res 2014;48:623–640.
  • Barres BA. The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 2008;60:430–440.

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