Startseite Redox-sensitive GFP to monitor oxidative stress in neurodegenerative diseases
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Redox-sensitive GFP to monitor oxidative stress in neurodegenerative diseases

  • Sonia Esposito , Alessandra Masala , Simona Sanna , Mauro Rassu , Viengsavanh Pimxayvong , Ciro Iaccarino und Claudia Crosio EMAIL logo
Veröffentlicht/Copyright: 28. Dezember 2016
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Abstract

Redox processes are key events in the degenerative cascade of many adult-onset neurodegenerative diseases (NDs), but the biological relevance of a single redox change is often dependent on the redox couple involved and on its subcellular origin. The biosensors based on engineered fluorescent proteins (redox-sensitive GFP [roGFP]) offer a unique opportunity to monitor redox changes in both physiological and pathological contexts in living animals and plants. Here, we review the use of roGFPs to monitor oxidative stress in different three adult-onset NDs: Alzheimer’s disease (AD), Parkinson’s disease (PD), and amyotrophic lateral sclerosis (ALS). Despite the many differences spanning from incidence to onset, the hypotheses on biological processes underlying both sporadic and familiar ND forms in humans outline a model in which noncompeting mechanisms are likely to converge in various unsuccessful patterns to mediate the selective degeneration of a specific neuronal population. roGFPs, targeted to different cell compartments, are successfully used as specific markers of cell toxicity, induced by expression of causative genes linked to a determined ND. We also report the use of roGFP to monitor oxidative stress induced by the expression of the ALS-causative gene SOD1.

Acknowledgments

This study was supported by AriSLA (pilot grant project ALSHDAC1), Regione Sardegna (grant CRP17171), and PRIN 2015 (grant 2015LFPNMN_005). We would like to acknowledge all the people from the laboratory that critically read the manuscript. Thanks are due to Manuela Galioto for technical assistance and to Giustina Casu for proofreading the manuscript for English language.

References

Albrecht, S.C., Barata, A.G., Grosshans, J., Teleman, A.A., and Dick, T.P. (2011). In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell Metab. 14, 819–829.10.1016/j.cmet.2011.10.010Suche in Google Scholar PubMed

Aller, I., Rouhier, N., and Meyer, A.J. (2013). Development of roGFP2-derived redox probes for measurement of the glutathione redox potential in the cytosol of severely glutathione-deficient rml1 seedlings. Front. Plant Sci. 4, 506.10.3389/fpls.2013.00506Suche in Google Scholar PubMed PubMed Central

Anandhan, A., Rodriguez-Rocha, H., Bohovych, I., Griggs, A.M., Zavala-Flores, L., Reyes-Reyes, E.M., Seravalli, J., Stanciu, L.A., Lee, J., Rochet, J.C., et al. (2015). Overexpression of alpha-synuclein at non-toxic levels increases dopaminergic cell death induced by copper exposure via modulation of protein degradation pathways. Neurobiol. Dis. 81, 76–92.10.1016/j.nbd.2014.11.018Suche in Google Scholar PubMed PubMed Central

Andersen, J.K. (2004). Oxidative stress in neurodegeneration: cause or consequence? Nat. Med. 10, S18–S25.10.1038/nrn1434Suche in Google Scholar PubMed

Apolloni, S., Parisi, C., Pesaresi, M.G., Rossi, S., Carri, M.T., Cozzolino, M., Volonte, C., and D’Ambrosi, N. (2013). The NADPH oxidase pathway is dysregulated by the P2X7 receptor in the SOD1-G93A microglia model of amyotrophic lateral sclerosis. J. Immunol. 190, 5187–5195.10.4049/jimmunol.1203262Suche in Google Scholar PubMed

Arnoult, D., Soares, F., Tattoli, I., Castanier, C., Philpott, D.J., and Girardin, S.E. (2009). An N-terminal addressing sequence targets NLRX1 to the mitochondrial matrix. J. Cell. Sci. 122, 3161–3168.10.1242/jcs.051193Suche in Google Scholar PubMed PubMed Central

Barlow, C.A., Kitiphongspattana, K., Siddiqui, N., Roe, M.W., Mossman, B.T., and Lounsbury, K.M. (2008). Protein kinase A-mediated CREB phosphorylation is an oxidant-induced survival pathway in alveolar type II cells. Apoptosis 13, 681–692.10.1007/s10495-008-0203-zSuche in Google Scholar PubMed PubMed Central

Barnham, K.J., Masters, C.L., and Bush, A.I. (2004). Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 3, 205–214.10.1038/nrd1330Suche in Google Scholar PubMed

Berkelhamer, S.K., Kim, G.A., Radder, J.E., Wedgwood, S., Czech, L., Steinhorn, R.H., and Schumacker, P.T. (2013). Developmental differences in hyperoxia-induced oxidative stress and cellular responses in the murine lung. Free Radic. Biol. Med. 61, 51–60.10.1016/j.freeradbiomed.2013.03.003Suche in Google Scholar PubMed PubMed Central

Bhaskar, A., Munshi, M., Khan, S.Z., Fatima, S., Arya, R., Jameel, S., and Singh, A. (2015). Measuring glutathione redox potential of HIV-1-infected macrophages. J. Biol. Chem. 290, 1020–1038.10.1074/jbc.M114.588913Suche in Google Scholar PubMed PubMed Central

Birk, J., Meyer, M., Aller, I., Hansen, H.G., Odermatt, A., Dick, T.P., Meyer, A.J., and Appenzeller-Herzog, C. (2013). Endoplasmic reticulum: reduced and oxidized glutathione revisited. J. Cell. Sci. 126, 1604–1617.10.1242/jcs.117218Suche in Google Scholar PubMed

Brach, T., Soyk, S., Muller, C., Hinz, G., Hell, R., Brandizzi, F., and Meyer, A.J. (2009). Non-invasive topology analysis of membrane proteins in the secretory pathway. Plant J. 57, 534–541.10.1111/j.1365-313X.2008.03704.xSuche in Google Scholar PubMed

Breckwoldt, M.O., Pfister, F.M., Bradley, P.M., Marinkovic, P., Williams, P.R., Brill, M.S., Plomer, B., Schmalz, A., St Clair, D.K., Naumann, R., et al. (2014). Multiparametric optical analysis of mitochondrial redox signals during neuronal physiology and pathology in vivo. Nat. Med. 20, 555–560.10.1038/nm.3520Suche in Google Scholar PubMed

Calabrese, V., Cornelius, C., Mancuso, C., Lentile, R., Stella, A.M.G., and Butterfield, D.A. (2010). Redox homeostasis and cellular stress response in aging and neurodegeneration. Methods Mol. Biol. 610, 14.10.1007/978-1-60327-029-8_17Suche in Google Scholar PubMed

Carri, M.T., Valle, C., Bozzo, F., and Cozzolino, M. (2015). Oxidative stress and mitochondrial damage: importance in non-SOD1 ALS. Front. Cell. Neurosci. 9, 41.10.3389/fncel.2015.00041Suche in Google Scholar PubMed PubMed Central

Chi, A.Y., Waypa, G.B., Mungai, P.T., and Schumacker, P.T. (2010). Prolonged hypoxia increases ROS signaling and RhoA activation in pulmonary artery smooth muscle and endothelial cells. Antioxid. Redox. Signal 12, 603–610.10.1089/ars.2009.2861Suche in Google Scholar PubMed PubMed Central

Chiurchiu, V., Orlacchio, A., and Maccarrone, M. (2016). Is modulation of oxidative stress an answer? the state of the art of redox therapeutic actions in neurodegenerative diseases. Oxid. Med. Cell. Longev. 2016, 7909380.10.1155/2016/7909380Suche in Google Scholar PubMed PubMed Central

Cossu, A., Posadino, A.M., Giordo, R., Emanueli, C., Sanguinetti, A.M., Piscopo, A., Poiana, M., Capobianco, G., Piga, A., and Pintus, G. (2012). Apricot melanoidins prevent oxidative endothelial cell death by counteracting mitochondrial oxidation and membrane depolarization. PLoS One 7, e48817.10.1371/journal.pone.0048817Suche in Google Scholar PubMed PubMed Central

Cunniff, B., Benson, K., Stumpff, J., Newick, K., Held, P., Taatjes, D., Joseph, J., Kalyanaraman, B., and Heintz, N.H. (2013). Mitochondrial-targeted nitroxides disrupt mitochondrial architecture and inhibit expression of peroxiredoxin 3 and FOXM1 in malignant mesothelioma cells. J. Cell. Physiol. 228, 835–845.10.1002/jcp.24232Suche in Google Scholar PubMed PubMed Central

D’Amico, E., Factor-Litvak, P., Santella, R.M., and Mitsumoto, H. (2013). Clinical perspective on oxidative stress in sporadic amyotrophic lateral sclerosis. Free Radic. Biol. Med. 65, 509–527.10.1016/j.freeradbiomed.2013.06.029Suche in Google Scholar PubMed PubMed Central

de Souza, A.H., Santos, L.R., Roma, L.P., Bensellam, M., Carpinelli, A.R., and Jonas, J.C. (2017). NADPH oxidase-2 does not contribute to b-cell glucotoxicity in cultured pancreatic islets from C57BL/6J mice. Mol. Cell. Endocrinol. 439, 354–362.10.1016/j.mce.2016.09.022Suche in Google Scholar PubMed

Delic, M., Mattanovich, D., and Gasser, B. (2010). Monitoring intracellular redox conditions in the endoplasmic reticulum of living yeasts. FEMS Microbiol. Lett. 306, 61–66.10.1111/j.1574-6968.2010.01935.xSuche in Google Scholar PubMed

Delic, M., Rebnegger, C., Wanka, F., Puxbaum, V., Haberhauer-Troyer, C., Hann, S., Kollensperger, G., Mattanovich, D., and Gasser, B. (2012). Oxidative protein folding and unfolded protein response elicit differing redox regulation in endoplasmic reticulum and cytosol of yeast. Free Radic. Biol. Med. 52, 2000–2012.10.1016/j.freeradbiomed.2012.02.048Suche in Google Scholar PubMed

Desireddi, J.R., Farrow, K.N., Marks, J.D., Waypa, G.B., and Schumacker, P.T. (2010). Hypoxia increases ROS signaling and cytosolic Ca2+ in pulmonary artery smooth muscle cells of mouse lungs slices. Antioxid. Redox. Signal 12, 595–602.10.1089/ars.2009.2862Suche in Google Scholar PubMed PubMed Central

Dlaskova, A., Spacek, T., Santorova, J., Plecita-Hlavata, L., Berkova, Z., Saudek, F., Lessard, M., Bewersdorf, J., and Jezek, P. (2010). 4Pi microscopy reveals an impaired three-dimensional mitochondrial network of pancreatic islet β-cells, an experimental model of type-2 diabetes. Biochim. Biophys. Acta. 1797, 1327–1341.10.1016/j.bbabio.2010.02.003Suche in Google Scholar PubMed

Dooley, C.T., Dore, T.M., Hanson, G.T., Jackson, W.C., Remington, S.J., and Tsien, R.Y. (2004). Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279, 22284–22293.10.1074/jbc.M312847200Suche in Google Scholar PubMed

Dryanovski, D.I., Guzman, J.N., Xie, Z., Galteri, D.J., Volpicelli-Daley, L.A., Lee, V.M., Miller, R.J., Schumacker, P.T., and Surmeier, D.J. (2013). Calcium entry and a-synuclein inclusions elevate dendritic mitochondrial oxidant stress in dopaminergic neurons. J. Neurosci. 33, 10154–10164.10.1523/JNEUROSCI.5311-12.2013Suche in Google Scholar PubMed PubMed Central

Duprez, J., Roma, L.P., Close, A.F., and Jonas, J.C. (2012). Protective antioxidant and antiapoptotic effects of ZnCl2 in rat pancreatic islets cultured in low and high glucose concentrations. PLoS One 7, e46831.10.1371/journal.pone.0046831Suche in Google Scholar PubMed PubMed Central

Freeman, D., Cedillos, R., Choyke, S., Lukic, Z., McGuire, K., Marvin, S., Burrage, A.M., Sudholt, S., Rana, A., O’Connor, C., et al. (2013). Alpha-synuclein induces lysosomal rupture and cathepsin dependent reactive oxygen species following endocytosis. PLoS One 8, e62143.10.1371/journal.pone.0062143Suche in Google Scholar PubMed PubMed Central

Gao, H.M., Zhou, H., and Hong, J.S. (2012). NADPH oxidases: novel therapeutic targets for neurodegenerative diseases. Trends Pharmacol. Sci. 33, 295–303.10.1016/j.tips.2012.03.008Suche in Google Scholar PubMed PubMed Central

Gibbs-Flournoy, E.A., Simmons, S.O., Bromberg, P.A., Dick, T.P., and Samet, J.M. (2013). Monitoring intracellular redox changes in ozone-exposed airway epithelial cells. Environ. Health Perspect. 121, 312–317.10.1289/ehp.1206039Suche in Google Scholar PubMed PubMed Central

Goldberg, J.A., Guzman, J.N., Estep, C.M., Ilijic, E., Kondapalli, J., Sanchez-Padilla, J., and Surmeier, D.J. (2012). Calcium entry induces mitochondrial oxidant stress in vagal neurons at risk in Parkinson’s disease. Nat. Neurosci. 15, 1414–1421.10.1038/nn.3209Suche in Google Scholar PubMed PubMed Central

Gutscher, M., Pauleau, A.L., Marty, L., Brach, T., Wabnitz, G.H., Samstag, Y., Meyer, A.J., and Dick, T.P. (2008). Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553–559.10.1038/nmeth.1212Suche in Google Scholar PubMed

Gutscher, M., Sobotta, M.C., Wabnitz, G.H., Ballikaya, S., Meyer, A.J., Samstag, Y., and Dick, T.P. (2009). Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases. J. Biol. Chem. 284, 31532–31540.10.1074/jbc.M109.059246Suche in Google Scholar PubMed PubMed Central

Guzman, J.N., Sanchez-Padilla, J., Wokosin, D., Kondapalli, J., Ilijic, E., Schumacker, P.T., and Surmeier, D.J. (2010). Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468, 696–700.10.1038/nature09536Suche in Google Scholar PubMed PubMed Central

Hanson, G.T., Aggeler, R., Oglesbee, D., Cannon, M., Capaldi, R.A., Tsien, R.Y., and Remington, S.J. (2004). Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J. Biol. Chem. 279, 13044–13053.10.1074/jbc.M312846200Suche in Google Scholar PubMed

Heller, J., Meyer, A.J., and Tudzynski, P. (2012). Redox-sensitive GFP2: use of the genetically encoded biosensor of the redox status in the filamentous fungus Botrytis cinerea. Mol. Plant. Pathol. 13, 935–947.10.1111/j.1364-3703.2012.00802.xSuche in Google Scholar PubMed PubMed Central

Hernandez, D.G., Reed, X., and Singleton, A.B. (2016). Genetics in Parkinson disease: Mendelian versus non-Mendelian inheritance. J. Neurochem. 139(Suppl 1), 59–7410.1111/jnc.13593Suche in Google Scholar PubMed PubMed Central

Hwang, O. (2013). Role of oxidative stress in Parkinson’s disease. Exp. Neurobiol. 22, 11–17.10.5607/en.2013.22.1.11Suche in Google Scholar PubMed PubMed Central

Iaccarino, C., Mura, M.E., Esposito, S., Carta, F., Sanna, G., Turrini, F., Carri, M.T. and Crosio, C. (2011). Bcl2-A1 interacts with pro-caspase-3: implications for amyotrophic lateral sclerosis. Neurobiol. Dis. 43, 642–650.10.1016/j.nbd.2011.05.013Suche in Google Scholar PubMed

Jenner, P. (2003). Oxidative stress in Parkinson’s disease. Ann. Neurol. 53, S26–S36; discussion S36–S28.10.1016/S0072-9752(07)83024-7Suche in Google Scholar

Jiang, K., Schwarzer, C., Lally, E., Zhang, S., Ruzin, S., Machen, T., Remington, S.J., and Feldman, L. (2006). Expression and characterization of a redox-sensing green fluorescent protein (reduction-oxidation-sensitive green fluorescent protein) in Arabidopsis. Plant Physiol. 141, 397–403.10.1104/pp.106.078246Suche in Google Scholar PubMed PubMed Central

Lohman, J.R. and Remington, S.J. (2008). Development of a family of redox-sensitive green fluorescent protein indicators for use in relatively oxidizing subcellular environments. Biochemistry 47, 8678–8688.10.1021/bi800498gSuche in Google Scholar PubMed

Loor, G., Kondapalli, J., Schriewer, J.M., Chandel, N.S., Vanden Hoek, T.L., and Schumacker, P.T. (2010). Menadione triggers cell death through ROS-dependent mechanisms involving PARP activation without requiring apoptosis. Free Radic. Biol. Med. 49, 1925–1936.10.1016/j.freeradbiomed.2010.09.021Suche in Google Scholar PubMed PubMed Central

Loor, G., Kondapalli, J., Iwase, H., Chandel, N.S., Waypa, G.B., Guzy, R.D., Vanden Hoek, T.L., and Schumacker, P.T. (2011). Mitochondrial oxidant stress triggers cell death in simulated ischemia-reperfusion. Biochim. Biophys. Acta. 1813, 1382–1394.10.1016/j.bbamcr.2010.12.008Suche in Google Scholar PubMed PubMed Central

Lushchak, V.I. (2014). Free radicals, reactive oxygen species, oxidative stress and its classification. Chem. Biol. Interact. 224C, 164–175.10.1016/j.cbi.2014.10.016Suche in Google Scholar PubMed

Meyer, A.J. (2008). The integration of glutathione homeostasis and redox signaling. J. Plant Physiol. 165, 1390–1403.10.1016/j.jplph.2007.10.015Suche in Google Scholar PubMed

Meyer, A.J. and Dick, T.P. (2010). Fluorescent protein-based redox probes. Antioxid. Redox. Signal 13, 621–650.10.1089/ars.2009.2948Suche in Google Scholar PubMed

Meyer, A.J., Brach, T., Marty, L., Kreye, S., Rouhier, N., Jacquot, J.P., and Hell, R. (2007). Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J. 52, 973–986.10.1111/j.1365-313X.2007.03280.xSuche in Google Scholar PubMed

Morgan, B., Sobotta, M.C., and Dick, T.P. (2011). Measuring E(GSH) and H2O2 with roGFP2-based redox probes. Free Radic. Biol. Med. 51, 1943–1951.10.1016/j.freeradbiomed.2011.08.035Suche in Google Scholar PubMed

Mungai, P.T., Waypa, G.B., Jairaman, A., Prakriya, M., Dokic, D., Ball, M.K., and Schumacker, P.T. (2011). Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels. Mol. Cell. Biol. 31, 3531–3545.10.1128/MCB.05124-11Suche in Google Scholar PubMed PubMed Central

Nayernia, Z., Jaquet, V., and Krause, K.H. (2014). New insights on NOX enzymes in the central nervous system. Antioxid. Redox. Signal 20, 2815–2837.10.1089/ars.2013.5703Suche in Google Scholar PubMed PubMed Central

Ostergaard, H., Henriksen, A., Hansen, F.G., and Winther, J.R. (2001). Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J. 20, 5853–5862.10.1093/emboj/20.21.5853Suche in Google Scholar PubMed PubMed Central

Pal, R., Basu Thakur, P., Li, S., Minard, C., and Rodney, G.G. (2013). Real-time imaging of NADPH oxidase activity in living cells using a novel fluorescent protein reporter. PLoS One 8, e63989.10.1371/journal.pone.0063989Suche in Google Scholar PubMed PubMed Central

Pal, R., Bajaj, L., Sharma, J., Palmieri, M., Di Ronza, A., Lotfi, P., Chaudhury, A., Neilson, J., Sardiello, M., and Rodney, G.G. (2016). NADPH oxidase promotes Parkinsonian phenotypes by impairing autophagic flux in an mTORC1-independent fashion in a cellular model of Parkinson’s disease. Sci. Rep. 6, 22866.10.1038/srep22866Suche in Google Scholar PubMed PubMed Central

Pesaresi, M.G., Amori, I., Giorgi, C., Ferri, A., Fiorenzo, P., Gabanella, F., Salvatore, A.M., Giorgio, M., Pelicci, P.G., Pinton, P., et al. (2011). Mitochondrial redox signalling by p66Shc mediates ALS-like disease through Rac1 inactivation. Hum. Mol. Genet. 20, 4196–4208.10.1093/hmg/ddr347Suche in Google Scholar PubMed

Posadino, A.M., Cossu, A., Piga, A., Madrau, M.A., Del Caro, A., Colombino, M., Paglietti, B., Rubino, S., Iaccarino, C., Crosio, C., et al. (2011). Prune melanoidins protect against oxidative stress and endothelial cell death. Front. Biosci. (Elite Ed) 3, 1034–1041.10.2741/309Suche in Google Scholar

Pouvreau, S. (2014). Genetically encoded reactive oxygen species (ROS) and redox indicators. Biotechnol. J. 9, 282–293.10.1002/biot.201300199Suche in Google Scholar PubMed

Pujol-Carrion, N., Belli, G., Herrero, E., Nogues, A., and de la Torre-Ruiz, M.A. (2006). Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J. Cell Sci. 119, 4554–4564.10.1242/jcs.03229Suche in Google Scholar PubMed

Renton, A.E., Chio, A., and Traynor, B.J. (2014). State of play in amyotrophic lateral sclerosis genetics. Nat. Neurosci. 17, 17–23.10.1038/nn.3584Suche in Google Scholar PubMed PubMed Central

Rodriguez-Rocha, H., Garcia-Garcia, A., Pickett, C., Li, S., Jones, J., Chen, H., Webb, B., Choi, J., Zhou, Y., Zimmerman, M.C., et al. (2013). Compartmentalized oxidative stress in dopaminergic cell death induced by pesticides and complex I inhibitors: distinct roles of superoxide anion and superoxide dismutases. Free Radic. Biol. Med. 61, 370–383.10.1016/j.freeradbiomed.2013.04.021Suche in Google Scholar

Rosenwasser, S., Rot, I., Sollner, E., Meyer, A.J., Smith, Y., Leviatan, N., Fluhr, R., and Friedman, H. (2011). Organelles contribute differentially to reactive oxygen species-related events during extended darkness. Plant Physiol. 156, 185–201.10.1104/pp.110.169797Suche in Google Scholar

Scheltens, P., Blennow, K., Breteler, M.M.B., de Strooper, B., Frisoni, G.B., Salloway, S., and Van der Flier, W.M. (2016). Alzheimer’s disease. The Lancet. 388, 505–51710.1016/S0140-6736(15)01124-1Suche in Google Scholar

Schwarzlander, M., Fricker, M.D., Muller, C., Marty, L., Brach, T., Novak, J., Sweetlove, L.J., Hell, R., and Meyer, A.J. (2008). Confocal imaging of glutathione redox potential in living plant cells. J. Microsc. 231, 299–316.10.1111/j.1365-2818.2008.02030.xSuche in Google Scholar PubMed

Selkoe, D.J. and Hardy, J. (2016). The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol. Med. 8, 595–60810.15252/emmm.201606210Suche in Google Scholar PubMed PubMed Central

Sies, H. (2015). Oxidative stress: a concept in redox biology and medicine. Redox. Biol. 4, 180–183.10.1016/j.redox.2015.01.002Suche in Google Scholar PubMed PubMed Central

Surmeier, D.J., Guzman, J.N., Sanchez-Padilla, J., and Schumacker, P.T. (2011). The role of calcium and mitochondrial oxidant stress in the loss of substantia nigra pars compacta dopaminergic neurons in Parkinson’s disease. Neuroscience 198, 221–231.10.1016/j.neuroscience.2011.08.045Suche in Google Scholar PubMed PubMed Central

Uttara, B., Singh, A.V., Zamboni, P., and Mahajan, R.T. (2009). Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr. Neuropharmacol. 7, 65–74.10.2174/157015909787602823Suche in Google Scholar PubMed PubMed Central

Van Cauwenberghe, C., Van Broeckhoven, C., and Sleegers, K. (2015). The genetic landscape of Alzheimer disease: clinical implications and perspectives. Genet. Med. 18, 421–43010.1038/gim.2015.117Suche in Google Scholar PubMed PubMed Central

van Lith, M., Tiwari, S., Pediani, J., Milligan, G., and Bulleid, N.J. (2011). Real-time monitoring of redox changes in the mammalian endoplasmic reticulum. J. Cell Sci. 124, 2349–2356.10.1242/jcs.085530Suche in Google Scholar PubMed PubMed Central

Wagener, K.C., Kolbrink, B., Dietrich, K., Kizina, K.M., Terwitte, L.S., Kempkes, B., Bao, G., and Muller, M. (2016). Redox indicator mice stably expressing genetically encoded neuronal roGFP: versatile tools to decipher subcellular redox dynamics in neuropathophysiology. Antioxid. Redox. Signal. 25, 41–5810.1089/ars.2015.6587Suche in Google Scholar PubMed PubMed Central

Wang, P., Hummel, E., Osterrieder, A., Meyer, A.J., Frigerio, L., Sparkes, I., and Hawes, C. (2011). KMS1 and KMS2, two plant endoplasmic reticulum proteins involved in the early secretory pathway. Plant J. 66, 613–628.10.1111/j.1365-313X.2011.04522.xSuche in Google Scholar PubMed

Wang, X., Schwarzer, C., Hybiske, K., Machen, T.E., and Stephens, R.S. (2014). Developmental stage oxidoreductive states of Chlamydia and infected host cells. MBio 5, e01924.10.1128/mBio.01924-14Suche in Google Scholar PubMed PubMed Central

Wang, B., Liu, Q., Shan, H., Xia, C., and Liu, Z. (2015). Nrf2 inducer and cncC overexpression attenuates neurodegeneration due to a-synuclein in Drosophila. Biochem. Cell. Biol. 93, 351–358.10.1139/bcb-2015-0015Suche in Google Scholar PubMed

Waypa, G.B., Marks, J.D., Guzy, R., Mungai, P.T., Schriewer, J., Dokic, D., and Schumacker, P.T. (2010). Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ. Res. 106, 526–535.10.1161/CIRCRESAHA.109.206334Suche in Google Scholar PubMed PubMed Central

Waypa, G.B., Osborne, S.W., Marks, J.D., Berkelhamer, S.K., Kondapalli, J., and Schumacker, P.T. (2013). Sirtuin 3 deficiency does not augment hypoxia-induced pulmonary hypertension. Am. J. Respir. Cell Mol. Biol. 49, 885–891.10.1165/rcmb.2013-0191OCSuche in Google Scholar PubMed PubMed Central

Wolf, A.M., Nishimaki, K., Kamimura, N., and Ohta, S. (2014). Real-time monitoring of oxidative stress in live mouse skin. J. Invest. Dermatol. 134, 1701–1709.10.1038/jid.2013.428Suche in Google Scholar PubMed

Xie, H., Guan, J., Borrelli, L.A., Xu, J., Serrano-Pozo, A., and Bacskai, B.J. (2013a). Mitochondrial alterations near amyloid plaques in an Alzheimer’s disease mouse model. J. Neurosci. 33, 17042–17051.10.1523/JNEUROSCI.1836-13.2013Suche in Google Scholar PubMed PubMed Central

Xie, H., Hou, S., Jiang, J., Sekutowicz, M., Kelly, J., and Bacskai, B.J. (2013b). Rapid cell death is preceded by amyloid plaque-mediated oxidative stress. Proc. Natl. Acad. Sci. USA 110, 7904–7909.10.1073/pnas.1217938110Suche in Google Scholar PubMed PubMed Central

Xu, X., von Lohneysen, K., Soldau, K., Noack, D., Vu, A., and Friedman, J.S. (2011). A novel approach for in vivo measurement of mouse red cell redox status. Blood 118, 3694–3697.10.1182/blood-2011-03-342113Suche in Google Scholar PubMed PubMed Central

Zhang, H., Limphong, P., Pieper, J., Liu, Q., Rodesch, C.K., Christians, E., and Benjamin, I.J. (2012). Glutathione-dependent reductive stress triggers mitochondrial oxidation and cytotoxicity. FASEB J. 26, 1442–1451.10.1096/fj.11-199869Suche in Google Scholar PubMed PubMed Central

Zhang, J., Cao, Q., Li, S., Lu, X., Zhao, Y., Guan, J.S., Chen, J.C., Wu, Q., and Chen, G.Q. (2013). 3-Hydroxybutyrate methyl ester as a potential drug against Alzheimer’s disease via mitochondria protection mechanism. Biomaterials 34, 7552–7562.10.1016/j.biomaterials.2013.06.043Suche in Google Scholar PubMed

Zhao, Y. and Zhao, B. (2013). Oxidative stress and the pathogenesis of Alzheimer’s disease. Oxid. Med. Cell. Longev. 2013, 316523.10.1155/2013/316523Suche in Google Scholar PubMed PubMed Central

Received: 2016-7-11
Accepted: 2016-10-2
Published Online: 2016-12-28
Published in Print: 2017-2-1

©2017 Walter de Gruyter GmbH, Berlin/Boston

Heruntergeladen am 30.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/revneuro-2016-0041/html
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