Insights in pathogenesis of multiple sclerosis: nitric oxide may induce mitochondrial dysfunction of oligodendrocytes

References

Abeti, R., Uzun, E., Renganathan, I., Honda, T., Pook, M.A., and Giunti, P. (2015). Targeting lipid peroxidation and mitochondrial imbalance in Friedreich’s ataxia. Pharmacol. Res. 99, 344–350.10.1016/j.phrs.2015.05.015Suche in Google Scholar PubMed

al-Ali, M.K. and Howarth, P.H. (1998). Nitric oxide and the respiratory system in health and disease. Respir. Med. 92, 701–715.10.1016/S0954-6111(98)90000-2Suche in Google Scholar PubMed

Al-Shobaili, H.A. and Rasheed, Z. (2013). Physicochemical and immunological studies on mitochondrial DNA modified by peroxynitrite: implications of neo-epitopes of mitochondrial DNA in the etiopathogenesis of systemic lupus erythematosus. Lupus 22, 1024–1037.10.1177/0961203313498803Suche in Google Scholar PubMed

Al-Shobaili, H.A. and Rasheed, Z. (2014). Mitochondrial DNA acquires immunogenicity on exposure to nitrosative stress in patients with vitiligo. Hum. Immunol. 75, 1053–1061.10.1016/j.humimm.2014.09.003Suche in Google Scholar PubMed

Aliev, G., Obrenovich, M.E., Tabrez, S., Jabir, N.R., Reddy, V.P., Li, Y., Burnstock, G., Cacabelos, R., and Kamal, M.A. (2013). Link between cancer and Alzheimer disease via oxidative stress induced by nitric oxide-dependent mitochondrial DNA overproliferation and deletion. Oxid. Med. Cell Longev. 2013, 962984.10.1155/2013/962984Suche in Google Scholar PubMed PubMed Central

Alizadeh, A., Dyck, S.M., and Karimi-Abdolrezaee, S. (2015). Myelin damage and repair in pathologic CNS: challenges and prospects. Front Mol. Neurosci. 8, 35.10.3389/fnmol.2015.00035Suche in Google Scholar PubMed PubMed Central

Amaral, A.I., Meisingset, T.W., Kotter, M.R., and Sonnewald, U. (2013). Metabolic aspects of neuron-oligodendrocyte-astrocyte interactions. Front Endocrinol. (Lausanne) 4, 54.10.3389/fendo.2013.00054Suche in Google Scholar PubMed PubMed Central

Aqil, M., Elseth, K.M., Vesper, B.J., Deliu, Z., Aydogan, B., Xue, J., and Radosevich, J.A. (2014). Part I-mechanism of adaptation: high nitric oxide adapted A549 cells show enhanced DNA damage response and activation of antiapoptotic pathways. Tumour Biol. 35, 2403–2415.10.1007/s13277-013-1318-6Suche in Google Scholar PubMed

Atochin, D.N., Demchenko, I.T., Astern, J., Boso, A.E., Piantadosi, C.A., and Huang, P.L. (2003). Contributions of endothelial and neuronal nitric oxide synthases to cerebrovascular responses to hyperoxia. J. Cereb. Blood Flow Metab. 23, 1219–1226.10.1097/01.WCB.0000089601.87125.E4Suche in Google Scholar PubMed

Awasaki, T. and Ito, K. (2016). Neurodevelopment: regeneration switch is a gas. Nature 531, 182–183.10.1038/nature17308Suche in Google Scholar PubMed

Banerjee, R., Gladkova, C., Mapa, K., Witte, G., and Mokranjac, D. (2015). Protein translocation channel of mitochondrial inner membrane and matrix-exposed import motor communicate via two-domain coupling protein. eLife 4, e11897.10.7554/eLife.11897Suche in Google Scholar PubMed PubMed Central

Basso, A.S., Frenkel, D., Quintana, F.J., Costa-Pinto, F.A., Petrovic-Stojkovic, S., Puckett, L., Monsonego, A., Bar-Shir, A., Engel, Y., Gozin, M., et al. (2008). Reversal of axonal loss and disability in a mouse model of progressive multiple sclerosis. J. Clin. Invest. 118, 1532–1543.10.1172/JCI33464Suche in Google Scholar PubMed PubMed Central

Baydoun, H.H., Cherian, M.A., Green, P., and Ratner, L. (2015). Inducible nitric oxide synthase mediates DNA double strand breaks in human T-cell leukemia virus type 1-induced leukemia/lymphoma. Retrovirology 12, 71.10.1186/s12977-015-0196-ySuche in Google Scholar PubMed PubMed Central

Bechtold, D.A., Yue, X., Evans, R.M., Davies, M., Gregson, N.A., and Smith, K.J. (2005). Axonal protection in experimental autoimmune neuritis by the sodium channel blocking agent flecainide. Brain 128, 18–28.10.1093/brain/awh328Suche in Google Scholar PubMed

Beckman, J.S. and Koppenol, W.H. (1996). Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol. 271, C1424–C1437.10.1152/ajpcell.1996.271.5.C1424Suche in Google Scholar PubMed

Beda, N.V. and Nedospasov, A.A. (2007). NO-dependent modifications of nucleic acids. Bioorg. Khim. 33, 195–228.10.1134/S106816200702001XSuche in Google Scholar PubMed

Bian, K., Doursout, M.F., and Murad, F. (2008). Vascular system: role of nitric oxide in cardiovascular diseases. J. Clin. Hypertens. (Greenwich) 10, 304–310.10.1111/j.1751-7176.2008.06632.xSuche in Google Scholar PubMed PubMed Central

Bicker, G. (2001). Nitric oxide: an unconventional messenger in the nervous system of an orthopteroid insect. Arch. Insect. Biochem. Physiol. 48, 100–110.10.1002/arch.1062Suche in Google Scholar PubMed

Black, J.A., Liu, S., Hains, B.C., Saab, C.Y., and Waxman, S.G. (2006). Long-term protection of central axons with phenytoin in monophasic and chronic-relapsing EAE. Brain 129, 3196–3208.10.1093/brain/awl216Suche in Google Scholar PubMed

Boczkowski, J., Lisdero, C.L., Lanone, S., Carreras, M.C., Aubier, M., and Poderoso, J.J. (2001). Peroxynitrite-mediated mitochondrial dysfunction. Biol. Signals Recept. 10, 66–80.10.1159/000046876Suche in Google Scholar PubMed

Bolanos, J.P., Heales, S.J., Land, J.M., and Clark, J.B. (1995). Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurones and astrocytes in primary culture. J. Neurochem. 64, 1965–1972.10.1046/j.1471-4159.1995.64051965.xSuche in Google Scholar PubMed

Bolton, C. and Paul, C. (2006). Glutamate receptors in neuroinflammatory demyelinating disease. Mediat. Inflamm. 2006, 93684.10.1155/MI/2006/93684Suche in Google Scholar

Bouafia, A., Golmard, J.L., Thuries, V., Sazdovitch, V., Hauw, J.J., Fontaine, B., and Seilhean, D. (2014). Axonal expression of sodium channels and neuropathology of the plaques in multiple sclerosis. Neuropathol. Appl. Neurobiol. 40, 579–590.10.1111/nan.12059Suche in Google Scholar PubMed

Boullerne, A.I. and Benjamins, J.A. (2006). Nitric oxide synthase expression and nitric oxide toxicity in oligodendrocytes. Antioxid. Redox Signal. 8, 967–980.10.1089/ars.2006.8.967Suche in Google Scholar PubMed

Boullerne, A.I., Nedelkoska, L., and Benjamins, J.A. (1999). Synergism of nitric oxide and iron in killing the transformed murine oligodendrocyte cell line N20.1. J. Neurochem. 72, 1050–1060.10.1046/j.1471-4159.1999.0721050.xSuche in Google Scholar PubMed

Bradl, M. and Lassmann, H. (2010). Oligodendrocytes: biology and pathology. Acta Neuropathol. 119, 37–53.10.1007/s00401-009-0601-5Suche in Google Scholar PubMed

Broadwater, L., Pandit, A., Clements, R., Azzam, S., Vadnal, J., Sulak, M., Yong, V.W., Freeman, E.J., Gregory, R.B., and McDonough, J. (2011). Analysis of the mitochondrial proteome in multiple sclerosis cortex. Biochim. Biophys. Acta 1812, 630–641.10.1016/j.bbadis.2011.01.012Suche in Google Scholar PubMed

Broholm, H., Braendstrup, O., and Lauritzen, M. (2001). Nitric oxide synthase expression of oligodendrogliomas. Clin. Neuropathol. 20, 233–238.Suche in Google Scholar PubMed

Brookes, P.S., Land, J.M., Clark, J.B., and Heales, S.J. (1998). Peroxynitrite and brain mitochondria: evidence for increased proton leak. J. Neurochem. 70, 2195–2202.10.1046/j.1471-4159.1998.70052195.xSuche in Google Scholar PubMed

Brown, G.C. (1999). Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta 1411, 351–369.10.1016/S0005-2728(99)00025-0Suche in Google Scholar PubMed

Brown, A.M., Tekkok, S.B., and Ransom, B.R. (2003). Glycogen regulation and functional role in mouse white matter. J. Physiol. 549, 501–512.10.1113/jphysiol.2003.042416Suche in Google Scholar PubMed PubMed Central

Browne, L., Lidster, K., Al-Izki, S., Clutterbuck, L., Posada, C., Chan, A.W., Riddall, D., Garthwaite, J., Baker, D., and Selwood, D.L. (2014). Imidazol-1-ylethylindazole voltage-gated sodium channel ligands are neuroprotective during optic neuritis in a mouse model of multiple sclerosis. J. Med. Chem. 57, 2942–2952.10.1021/jm401881qSuche in Google Scholar

Burney, S., Caulfield, J.L., Niles, J.C., Wishnok, J.S., and Tannenbaum, S.R. (1999). The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutat Res. 424, 37–49.10.1016/S0027-5107(99)00006-8Suche in Google Scholar PubMed

Calcerrada, P., Peluffo, G., and Radi, R. (2011). Nitric oxide-derived oxidants with a focus on peroxynitrite: molecular targets, cellular responses and therapeutic implications. Curr. Pharm. Des. 17, 3905–3932.10.2174/138161211798357719Suche in Google Scholar PubMed

Cambron, M., D‘Haeseleer, M., Laureys, G., Clinckers, R., Debruyne, J., and De Keyser, J. (2012). White-matter astrocytes, axonal energy metabolism, and axonal degeneration in multiple sclerosis. J. Cereb. Blood Flow Metab. 32, 413–424.10.1038/jcbfm.2011.193Suche in Google Scholar PubMed

Carreras, M.C., Melani, M., Riobo, N., Converso, D.P., Gatto, E.M., and Poderoso, J.J. (2002). Neuronal nitric oxide synthases in brain and extraneural tissues. Methods Enzymol. 359, 413–423.10.1016/S0076-6879(02)59203-XSuche in Google Scholar PubMed

Cassano, T., Pace, L., Bedse, G., Lavecchia, A.M., De Marco, F., Gaetani, S., and Serviddio, G. (2016). Glutamate and mitochondria: two prominent players in the oxidative stress-induced neurodegeneration. Curr. Alzheimer Res. 13, 185–197.10.2174/1567205013666151218132725Suche in Google Scholar PubMed

Centonze, D., Muzio, L., Rossi, S., Furlan, R., Bernardi, G., and Martino, G. (2010). The link between inflammation, synaptic transmission and neurodegeneration in multiple sclerosis. Cell Death Differ. 17, 1083–1091.10.1038/cdd.2009.179Suche in Google Scholar PubMed

Chakraborti, T., Das, S., Mondal, M., Roychoudhury, S., and Chakraborti, S. (1999). Oxidant, mitochondria and calcium: an overview. Cell Signal. 11, 77–85.10.1016/S0898-6568(98)00025-4Suche in Google Scholar PubMed

Chamberlain, K.A., Nanescu, S.E., Psachoulia, K., and Huang, J.K. (2016). Oligodendrocyte regeneration: its significance in myelin replacement and neuroprotection in multiple sclerosis. Neuropharmacology 110(Pt B), 633–643.10.1016/j.neuropharm.2015.10.010Suche in Google Scholar PubMed PubMed Central

Chambers, T.W., Daly, T.P., Hockley, A., and Brown, A.M. (2014). Contribution of glycogen in supporting axon conduction in the peripheral and central nervous systems: the role of lactate. Front Neurosci. 8, 378.10.3389/fnins.2014.00378Suche in Google Scholar PubMed PubMed Central

Chipuk, J.E., Bouchier-Hayes, L., and Green, D.R. (2006). Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 13, 1396–1402.10.1038/sj.cdd.4401963Suche in Google Scholar PubMed

Correale, J. and Farez, M.F. (2015). The role of astrocytes in multiple sclerosis progression. Front Neurol. 6, 180.10.3389/fneur.2015.00180Suche in Google Scholar PubMed

Cossenza, M., Socodato, R., Portugal, C.C., Domith, I.C., Gladulich, L.F., Encarnacao, T.G., Calaza, K.C., Mendonca, H.R., Campello-Costa, P., and Paes-de-Carvalho, R. (2014). Nitric oxide in the nervous system: biochemical, developmental, and neurobiological aspects. Vitam. Horm. 96, 79–125.10.1016/B978-0-12-800254-4.00005-2Suche in Google Scholar PubMed

Craner, M.J., Hains, B.C., Lo, A.C., Black, J.A., and Waxman, S.G. (2004). Co-localization of sodium channel Nav1.6 and the sodium-calcium exchanger at sites of axonal injury in the spinal cord in EAE. Brain 127, 294–303.10.1093/brain/awh032Suche in Google Scholar PubMed

Czerniczyniec, A., La Padula, P., Bustamante, J., Karadayian, A.G., Lores-Arnaiz, S., and Costa, L.E. (2015). Mitochondrial function in rat cerebral cortex and hippocampus after short- and long-term hypobaric hypoxia. Brain Res. 1598, 66–75.10.1016/j.brainres.2014.12.018Suche in Google Scholar

D’Souza, C.A., Zhao, F.L., Li, X., Xu, Y., Dunn, S.E., and Zhang, L. (2016). OGR1/GPR68 modulates the severity of experimental autoimmune encephalomyelitis and regulates nitric oxide production by macrophages. PLoS One 11, e0148439.10.1371/journal.pone.0148439Suche in Google Scholar PubMed

Davis, K.L., Martin, E., Turko, I.V., and Murad, F. (2001). Novel effects of nitric oxide. Annu. Rev. Pharmacol. Toxicol. 41, 203–236.10.1146/annurev.pharmtox.41.1.203Suche in Google Scholar PubMed

Dawson, V.L. and Dawson, T.M. (1996). Nitric oxide neurotoxicity. J. Chem. Neuroanat. 10, 179–190.10.1016/0891-0618(96)00148-2Suche in Google Scholar PubMed

Desai, R.A., Davies, A.L., Tachrount, M., Kasti, M., Laulund, F., Golay, X., and Smith, K.J. (2016). Cause and prevention of demyelination in a model multiple sclerosis lesion. Ann. Neurol. 79, 591–604.10.1002/ana.24607Suche in Google Scholar PubMed PubMed Central

Diers, A.R., Broniowska, K.A., Chang, C.F., Hill, R.B., and Hogg, N. (2014). S-Nitrosation of monocarboxylate transporter 1: inhibition of pyruvate-fueled respiration and proliferation of breast cancer cells. Free Radic. Biol. Med. 69, 229–238.10.1016/j.freeradbiomed.2014.01.031Suche in Google Scholar PubMed PubMed Central

Ding, S., Riddoch-Contreras, J., Abramov, A.Y., Qi, Z., and Duchen, M.R. (2012). Mild stress of caffeine increased mtDNA content in skeletal muscle cells: the interplay between Ca²⁺ transients and nitric oxide. J. Muscle Res. Cell Motil. 33, 327–337.10.1007/s10974-012-9318-5Suche in Google Scholar PubMed

Druzhyna, N.M., Musiyenko, S.I., Wilson, G.L., and LeDoux, S.P. (2005). Cytokines induce nitric oxide-mediated mtDNA damage and apoptosis in oligodendrocytes. Protective role of targeting 8-oxoguanine glycosylase to mitochondria. J. Biol. Chem. 280, 21673–21679.10.1074/jbc.M411531200Suche in Google Scholar PubMed

Dugas, N., Delfraissy, J.F., and Tardieu, M. (1995). Immune regulatory role of nitric oxide within the central nervous system. Res. Immunol. 146, 707–710.10.1016/0923-2494(96)84923-6Suche in Google Scholar PubMed

Dulamea, A.O. (2017). Role of oligodendrocyte dysfunction in demyelination, remyelination and neurodegeneration in multiple sclerosis. Adv. Exp. Med. Biol. 958, 91–127.10.1007/978-3-319-47861-6_7Suche in Google Scholar PubMed

Dutta, R. and Trapp, B.D. (2011). Mechanisms of neuronal dysfunction and degeneration in multiple sclerosis. Prog. Neurobiol. 93, 1–12.10.1016/j.pneurobio.2010.09.005Suche in Google Scholar PubMed

El-Mas, M.M. and Abdel-Rahman, A.A. (2014). Endothelial and neuronal nitric oxide synthases variably modulate the oestrogen-mediated control of blood pressure and cardiovascular autonomic control. Clin. Exp. Pharmacol. Physiol. 41, 246–254.10.1111/1440-1681.12207Suche in Google Scholar PubMed

Fagian, M.M., Pereira-da-Silva, L., Martins, I.S., and Vercesi, A.E. (1990). Membrane protein thiol cross-linking associated with the permeabilization of the inner mitochondrial membrane by Ca²⁺ plus prooxidants. J. Biol. Chem. 265, 19955–19960.10.1016/S0021-9258(17)45467-6Suche in Google Scholar PubMed

Franca, R.F., Costa, R.S., Silva, J.R., Peres, R.S., Mendonca, L.R., Colon, D.F., Alves-Filho, J.C. and Cunha, F.Q. (2016). IL-33 signaling is essential to attenuate viral-induced encephalitis development by downregulating iNOS expression in the central nervous system. J. Neuroinflamm. 13, 159.10.1186/s12974-016-0628-1Suche in Google Scholar PubMed PubMed Central

Furchgott, R.F. and Zawadzki, J.V. (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373–376.10.1038/288373a0Suche in Google Scholar PubMed

Garthwaite, J. (2016). From synaptically localized to volume transmission by nitric oxide. J. Physiol. 594, 9–18.10.1113/JP270297Suche in Google Scholar PubMed PubMed Central

Gellerich, F.N., Trumbeckaite, S., Opalka, J.R., Seppet, E., Rasmussen, H.N., Neuhoff, C., and Zierz, S. (2000). Function of the mitochondrial outer membrane as a diffusion barrier in health and diseases. Biochem. Soc. Trans. 28, 164–169.10.1042/bst0280164Suche in Google Scholar PubMed

Ghafourifar, P., Mousavizadeh, K., Parihar, M.S., Nazarewicz, R.R., Parihar, A., and Zenebe, W.J. (2008). Mitochondria in multiple sclerosis. Front Biosci. 13, 3116–3126.10.2741/2913Suche in Google Scholar PubMed

Grigoriadis, N., Ben-Hur, T., Karussis, D., and Milonas, I. (2004). Axonal damage in multiple sclerosis: a complex issue in a complex disease. Clin. Neurol. Neurosurg. 106, 211–217.10.1016/j.clineuro.2004.02.017Suche in Google Scholar

Grishko, V.I., Druzhyna, N., LeDoux, S.P., and Wilson, G.L. (1999). Nitric oxide-induced damage to mtDNA and its subsequent repair. Nucleic Acids Res. 27, 4510–4516.10.1093/nar/27.22.4510Suche in Google Scholar PubMed

Gupta, S., Goswami, P., Biswas, J., Joshi, N., Sharma, S., Nath, C., and Singh, S. (2015). 6-Hydroxydopamine and lipopolysaccharides induced DNA damage in astrocytes: involvement of nitric oxide and mitochondria. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 778, 22–36.10.1016/j.mrgentox.2014.12.007Suche in Google Scholar PubMed

Haj-Mirzaian, A., Amiri, S., Kordjazy, N., Momeny, M., Razmi, A., Rahimi-Balaei, M., Amini-Khoei, H., Haj-Mirzaian, A., Marzban, H., Mehr, S.E., et al. (2016). Lithium attenuated the depressant and anxiogenic effect of juvenile social stress through mitigating the negative impact of interlukin-1beta and nitric oxide on hypothalamic-pituitary-adrenal axis function. Neuroscience 315, 271–285.10.1016/j.neuroscience.2015.12.024Suche in Google Scholar PubMed

Halestrap, A.P. and Richardson, A.P. (2015). The mitochondrial permeability transition: a current perspective on its identity and role in ischaemia/reperfusion injury. J. Mol. Cell Cardiol. 78, 129–141.10.1016/j.yjmcc.2014.08.018Suche in Google Scholar PubMed

Haorah, J., Floreani, N.A., Knipe, B., and Persidsky, Y. (2011). Stabilization of superoxide dismutase by acetyl-l-carnitine in human brain endothelium during alcohol exposure: novel protective approach. Free Radic. Biol. Med. 51, 1601–1609.10.1016/j.freeradbiomed.2011.06.020Suche in Google Scholar PubMed

Heales, S.J., Bolanos, J.P., Stewart, V.C., Brookes, P.S., Land, J.M., and Clark, J.B. (1999). Nitric oxide, mitochondria and neurological disease. Biochim. Biophys. Acta 1410, 215–228.10.1016/S0005-2728(98)00168-6Suche in Google Scholar PubMed

Heck, D.E., Kagan, V.E., Shvedova, A.A., and Laskin, J.D. (2005). An epigrammatic (abridged) recounting of the myriad tales of astonishing deeds and dire consequences pertaining to nitric oxide and reactive oxygen species in mitochondria with an ancillary missive concerning the origins of apoptosis. Toxicology 208, 259–271.10.1016/j.tox.2004.11.027Suche in Google Scholar PubMed

Hegardt, P., Widegren, B., Li, L., Sjogren, B., Kjellman, C., Sur, I., and Sjogren, H.O. (2001). Nitric oxide synthase inhibitor and IL-18 enhance the anti-tumor immune response of rats carrying an intrahepatic colon carcinoma. Cancer Immunol. Immunother. 50, 491–501.10.1007/s002620100230Suche in Google Scholar PubMed

Hemnani, T. and Parihar, M.S. (1998). Reactive oxygen species and oxidative DNA damage. Ind. J. Physiol. Pharmacol. 42, 440–452.Suche in Google Scholar

Holan, V., Krulova, M., Zajicova, A., and Pindjakova, J. (2002). Nitric oxide as a regulatory and effector molecule in the immune system. Mol. Immunol. 38, 989–995.10.1016/S0161-5890(02)00027-5Suche in Google Scholar PubMed

Hoos, M.D., Richardson, B.M., Foster, M.W., Everhart, A., Thompson, J.W., Moseley, M.A., and Colton, C.A. (2013). Longitudinal study of differential protein expression in an Alzheimer’s mouse model lacking inducible nitric oxide synthase. J. Proteome Res. 12, 4462–4477.10.1021/pr4005103Suche in Google Scholar PubMed PubMed Central

Huang, S.Q., Tang, C.L., Sun, S.Q., Yang, C., Xu, J., Wang, K.J., Lu, W.T., Huang, J., Zhuo, F., Qiu, G.P., et al. (2014). Demyelination initiated by oligodendrocyte apoptosis through enhancing endoplasmic reticulum-mitochondria interactions and Id2 expression after compressed spinal cord injury in rats. CNS Neurosci. Ther. 20, 20–31.10.1111/cns.12155Suche in Google Scholar PubMed PubMed Central

Huie, R.E. and Padmaja, S. (1993). The reaction of no with superoxide. Free Radic. Res. Commun. 18, 195–199.10.3109/10715769309145868Suche in Google Scholar PubMed

Hung, A.C. and Porter, A.G. (2009). p53 mediates nitric oxide-induced apoptosis in murine neural progenitor cells. Neurosci. Lett. 467, 241–246.10.1016/j.neulet.2009.10.050Suche in Google Scholar PubMed

Ignarro, L.J. (1996). Physiology and pathophysiology of nitric oxide. Kidney Int. 55(Suppl), S2–S5.Suche in Google Scholar

Ignarro, L.J. (2002). Wei Lun visiting professorial lecture: nitric oxide in the regulation of vascular function: an historical overview. J. Card. Surg. 17, 301–306.10.1111/j.1540-8191.2001.tb01148.xSuche in Google Scholar PubMed

Imaizumi, N. and Aniya, Y. (2011). The role of a membrane-bound glutathione transferase in the peroxynitrite-induced mitochondrial permeability transition pore: formation of a disulfide-linked protein complex. Arch. Biochem. Biophys. 516, 160–172.10.1016/j.abb.2011.10.012Suche in Google Scholar PubMed

Ito, H., Ando, T., Ogiso, H., Arioka, Y., and Seishima, M. (2015). Inhibition of induced nitric oxide synthase enhances the anti-tumor effects on cancer immunotherapy using TLR7 agonist in mice. Cancer Immunol. Immunother. 64, 429–436.10.1007/s00262-014-1644-6Suche in Google Scholar PubMed

Jack, C., Antel, J., Bruck, W., and Kuhlmann, T. (2007). Contrasting potential of nitric oxide and peroxynitrite to mediate oligodendrocyte injury in multiple sclerosis. Glia 55, 926–934.10.1002/glia.20514Suche in Google Scholar PubMed

Jackson, V.N., Price, N.T., Carpenter, L., and Halestrap, A.P. (1997). Cloning of the monocarboxylate transporter isoform MCT2 from rat testis provides evidence that expression in tissues is species-specific and may involve post-transcriptional regulation. Biochem. J. 324, 447–453.10.1042/bj3240447Suche in Google Scholar PubMed

Jana, M. and Pahan, K. (2013). Down-regulation of myelin gene expression in human oligodendrocytes by nitric oxide: implications for demyelination in multiple sclerosis. J. Clin. Cell Immunol. 4. doi: 10.4172/2155-9899.1000157.10.4172/2155-9899.1000157Suche in Google Scholar PubMed

Jiang, F., Ryan, M.T., Schlame, M., Zhao, M., Gu, Z., Klingenberg, M., Pfanner, N., and Greenberg, M.L. (2000). Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J. Biol. Chem. 275, 22387–22394.10.1074/jbc.M909868199Suche in Google Scholar PubMed

Jourd’heuil, D., Kang, D., and Grisham, M.B. (1997). Interactions between superoxide and nitric oxide: implications in DNA damage and mutagenesis. Front Biosci. 2, d189–196.10.2741/A182Suche in Google Scholar PubMed

Kakizawa, S. and Yamazawa, T. (2016). Nitric-oxide induced calcium release: regulatory mechanism and physiological function. Nihon Yakurigaku Zasshi 147, 194–199.10.1254/fpj.147.194Suche in Google Scholar PubMed

Kalman, B. and Leist, T.P. (2003). A mitochondrial component of neurodegeneration in multiple sclerosis. Neuromol. Med. 3, 147–158.10.1385/NMM:3:3:147Suche in Google Scholar

Kapoor, R. (2008). Sodium channel blockers and neuroprotection in multiple sclerosis using lamotrigine. J. Neurol. Sci. 274, 54–56.10.1016/j.jns.2008.03.019Suche in Google Scholar PubMed

Koriyama, Y., Yasuda, R., Homma, K., Mawatari, K., Nagashima, M., Sugitani, K., Matsukawa, T. and Kato, S. (2009). Nitric oxide-cGMP signaling regulates axonal elongation during optic nerve regeneration in the goldfish in vitro and in vivo. J. Neurochem. 110, 890–901.10.1111/j.1471-4159.2009.06182.xSuche in Google Scholar PubMed

Kowaltowski, A.J., Castilho, R.F., and Vercesi, A.E. (2001). Mitochondrial permeability transition and oxidative stress. FEBS Lett. 495, 12–15.10.1016/S0014-5793(01)02316-XSuche in Google Scholar PubMed

Lee, C.S., Han, E.S., Park, E.S., and Bang, H. (2005). Inhibition of MG132-induced mitochondrial dysfunction and cell death in PC12 cells by 3-morpholinosydnonimine. Brain Res. 1036, 18–26.10.1016/j.brainres.2004.12.036Suche in Google Scholar PubMed

Lei, J., Vodovotz, Y., Tzeng, E., and Billiar, T.R. (2013). Nitric oxide, a protective molecule in the cardiovascular system. Nitric Oxide 35, 175–185.10.1016/j.niox.2013.09.004Suche in Google Scholar PubMed

Leite, A.C., Oliveira, H.C., Utino, F.L., Garcia, R., Alberici, L.C., Fernandes, M.P., Castilho, R.F., and Vercesi, A.E. (2010). Mitochondria generated nitric oxide protects against permeability transition via formation of membrane protein S-nitrosothiols. Biochim. Biophys. Acta 1797, 1210–1216.10.1016/j.bbabio.2010.01.034Suche in Google Scholar PubMed

Li, C.Y., Xing, A.Y., Li, L., Wei, P.J., Gu, S.X., Chen, X.Y., Duan, H.F., Chen, X., Xie, L., and Ma, Y. (2003). Nitric oxide production and expression of cytokines by macrophages infected by M. tuberculosis H(37)R(v). Zhonghua Jie He He Hu Xi Za Zhi 26, 214–217.Suche in Google Scholar

Li, J., Baud, O., Vartanian, T., Volpe, J.J., and Rosenberg, P.A. (2005). Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc. Natl. Acad. Sci. USA 102, 9936–9941.10.1073/pnas.0502552102Suche in Google Scholar PubMed PubMed Central

Li, S., Lin, W., Tchantchou, F., Lai, R., Wen, J., and Zhang, Y. (2011a). Protein kinase C mediates peroxynitrite toxicity to oligodendrocytes. Mol. Cell Neurosci. 48, 62–71.10.1016/j.mcn.2011.06.006Suche in Google Scholar PubMed

Li, S., Vana, A.C., Ribeiro, R., and Zhang, Y. (2011b). Distinct role of nitric oxide and peroxynitrite in mediating oligodendrocyte toxicity in culture and in experimental autoimmune encephalomyelitis. Neuroscience 184, 107–119.10.1016/j.neuroscience.2011.04.007Suche in Google Scholar PubMed

Li, Y., Liu, K., Kang, Z.M., Sun, X.J., Liu, W.W., and Mao, Y.F. (2016). Helium preconditioning protects against neonatal hypoxia-ischemia via nitric oxide mediated up-regulation of antioxidases in a rat model. Behav. Brain Res. 300, 31–37.10.1016/j.bbr.2015.12.001Suche in Google Scholar PubMed

Liang, P. and Le, W. (2015). Role of autophagy in the pathogenesis of multiple sclerosis. Neurosci. Bull. 31, 435–444.10.1007/s12264-015-1545-5Suche in Google Scholar PubMed PubMed Central

Litvinova, L., Atochin, D.N., Fattakhov, N., Vasilenko, M., Zatolokin, P., and Kirienkova, E. (2015). Nitric oxide and mitochondria in metabolic syndrome. Front Physiol. 6, 20.10.3389/fphys.2015.00020Suche in Google Scholar PubMed PubMed Central

Liu, Z. and Martin, L.J. (2001). Motor neurons rapidly accumulate DNA single-strand breaks after in vitro exposure to nitric oxide and peroxynitrite and in vivo axotomy. J. Comp. Neurol. 432, 35–60.10.1002/cne.1087Suche in Google Scholar PubMed

Liu, Z., Song, G., Zou, C., Liu, G., Wu, W., Yuan, T., and Liu, X. (2015). Acrylamide induces mitochondrial dysfunction and apoptosis in BV-2 microglial cells. Free Radic. Biol. Med. 84, 42–53.10.1016/j.freeradbiomed.2015.03.013Suche in Google Scholar PubMed

Loscalzo, J. and Welch, G. (1995). Nitric oxide and its role in the cardiovascular system. Prog. Cardiovasc. Dis. 38, 87–104.10.1016/S0033-0620(05)80001-5Suche in Google Scholar PubMed

Mahad, D., Lassmann, H., and Turnbull, D. (2008). Review: mitochondria and disease progression in multiple sclerosis. Neuropathol. Appl. Neurobiol. 34, 577–589.10.1111/j.1365-2990.2008.00987.xSuche in Google Scholar PubMed

Mahad, D.J., Ziabreva, I., Campbell, G., Lax, N., White, K., Hanson, P.S., Lassmann, H., and Turnbull, D.M. (2009). Mitochondrial changes within axons in multiple sclerosis. Brain 132, 1161–1174.10.1093/brain/awp046Suche in Google Scholar PubMed

Maia-de-Oliveira, J.P., Kandratavicius, L., Nunes, E.A., Machado-de-Sousa, J.P., Hallak, J.E., and Dursun, S.M. (2016). Nitric oxide’s involvement in the spectrum of psychotic disorders. Curr. Med. Chem. 23, 2680–2691.10.2174/0929867323666160721144549Suche in Google Scholar PubMed

Marinelli, C., Bertalot, T., Zusso, M., Skaper, S.D., and Giusti, P. (2016). Systematic review of pharmacological properties of the oligodendrocyte lineage. Front Cell Neurosci. 10, 27.10.3389/fncel.2016.00027Suche in Google Scholar PubMed

Martinez-Palma, L., Pehar, M., Cassina, P., Peluffo, H., Castellanos, R., Anesetti, G., Beckman, J.S., and Barbeito, L. (2003). Involvement of nitric oxide on kainate-induced toxicity in oligodendrocyte precursors. Neurotox. Res. 5, 399–406.10.1007/BF03033168Suche in Google Scholar PubMed

Matute, C., Domercq, M., and Sanchez-Gomez, M.V. (2006). Glutamate-mediated glial injury: mechanisms and clinical importance. Glia 53, 212–224.10.1002/glia.20275Suche in Google Scholar PubMed

McLeod, D.S., Baba, T., Bhutto, I.A., and Lutty, G.A. (2012). Co-expression of endothelial and neuronal nitric oxide synthases in the developing vasculatures of the human fetal eye. Graefes Arch. Clin. Exp. Ophthalmol. 250, 839–848.10.1007/s00417-012-1969-9Suche in Google Scholar PubMed

Mirshafiey, A. and Mohsenzadegan, M. (2009). Antioxidant therapy in multiple sclerosis. Immunopharmacol. Immunotoxicol. 31, 13–29.10.1080/08923970802331943Suche in Google Scholar PubMed

Mitrovic, B., Ignarro, L.J., Montestruque, S., Smoll, A., and Merrill, J.E. (1994). Nitric oxide as a potential pathological mechanism in demyelination: its differential effects on primary glial cells in vitro. Neuroscience 61, 575–585.10.1016/0306-4522(94)90435-9Suche in Google Scholar PubMed

Mitrovic, B., Ignarro, L.J., Vinters, H.V., Akers, M.A., Schmid, I., Uittenbogaart, C., and Merrill, J.E. (1995). Nitric oxide induces necrotic but not apoptotic cell death in oligodendrocytes. Neuroscience 65, 531–539.10.1016/0306-4522(94)00491-MSuche in Google Scholar PubMed

Mitrovic, B., Parkinson, J., and Merrill, J.E. (1996). An in vitro model of oligodendrocyte destruction by nitric oxide and its relevance to multiple sclerosis. Methods 10, 501–513.10.1006/meth.1996.0127Suche in Google Scholar

Moss, D.W. and Bates, T.E. (2001). Activation of murine microglial cell lines by lipopolysaccharide and interferon-gamma causes NO-mediated decreases in mitochondrial and cellular function. Eur. J. Neurosci. 13, 529–538.10.1046/j.1460-9568.2001.01418.xSuche in Google Scholar PubMed

Muijsers, R.B., Folkerts, G., Henricks, P.A., Sadeghi-Hashjin, G., and Nijkamp, F.P. (1997). Peroxynitrite: a two-faced metabolite of nitric oxide. Life Sci. 60, 1833–1845.10.1016/S0024-3205(96)00651-0Suche in Google Scholar PubMed

Mullauer, F.B., Kessler, J.H., and Medema, J.P. (2009). Betulinic acid induces cytochrome c release and apoptosis in a Bax/Bak-independent, permeability transition pore dependent fashion. Apoptosis 14, 191–202.10.1007/s10495-008-0290-xSuche in Google Scholar PubMed

Muller, B., Kleschyov, A.L., Alencar, J.L., Vanin, A., and Stoclet, J.C. (2002). Nitric oxide transport and storage in the cardiovascular system. Ann. NY Acad. Sci. 962, 131–139.10.1111/j.1749-6632.2002.tb04063.xSuche in Google Scholar PubMed

Narita, M., Shimizu, S., Ito, T., Chittenden, T., Lutz, R.J., Matsuda, H., and Tsujimoto, Y. (1998). Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. USA 95, 14681–14686.10.1073/pnas.95.25.14681Suche in Google Scholar PubMed PubMed Central

Nguyen, T., Brunson, D., Crespi, C.L., Penman, B.W., Wishnok, J.S., and Tannenbaum, S.R. (1992). DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc. Natl. Acad. Sci. USA 89, 3030–3034.10.1073/pnas.89.7.3030Suche in Google Scholar PubMed PubMed Central

O’Malley, H.A., Shreiner, A.B., Chen, G.H., Huffnagle, G.B., and Isom, L.L. (2009). Loss of Na⁺ channel β2 subunits is neuroprotective in a mouse model of multiple sclerosis. Mol. Cell Neurosci. 40, 143–155.10.1016/j.mcn.2008.10.001Suche in Google Scholar PubMed PubMed Central

Ockelford, F., Saada, L., Gazit, E., and de Mel, A. (2016). Is nitric oxide assuming a janus-face in the central nervous system? Curr. Med. Chem. 23, 1625–1637.Suche in Google Scholar

Okada, S., Takehara, Y., Yabuki, M., Yoshioka, T., Yasuda, T., Inoue, M., and Utsumi, K. (1996). Nitric oxide, a physiological modulator of mitochondrial function. Physiol. Chem. Phys. Med. NMR 28, 69–82.Suche in Google Scholar PubMed

Olsen, J.A. and Akirav, E.M. (2015). Remyelination in multiple sclerosis: cellular mechanisms and novel therapeutic approaches. J. Neurosci. Res. 93, 687–696.10.1002/jnr.23493Suche in Google Scholar PubMed

Owens, M.W., Milligan, S.A., and Grisham, M.B. (1995). Nitric oxide-dependent N-nitrosating activity of rat pleural mesothelial cells. Free Radic. Res. 23, 371–378.10.3109/10715769509065258Suche in Google Scholar PubMed

Pacher, P., Beckman, J.S., and Liaudet, L. (2007). Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87, 315–424.10.1152/physrev.00029.2006Suche in Google Scholar PubMed

Parks, J.K., Smith, T.S., Trimmer, P.A., Bennett, J.P., Jr., and Parker, W.D., Jr. (2001). Neurotoxic Aβ peptides increase oxidative stress in vivo through NMDA-receptor and nitric-oxide-synthase mechanisms, and inhibit complex IV activity and induce a mitochondrial permeability transition in vitro. J. Neurochem. 76, 1050–1056.10.1046/j.1471-4159.2001.00112.xSuche in Google Scholar PubMed

Persson, A.K., Kim, I., Zhao, P., Estacion, M., Black, J.A., and Waxman, S.G. (2013). Sodium channels contribute to degeneration of dorsal root ganglion neurites induced by mitochondrial dysfunction in an in vitro model of axonal injury. J. Neurosci. 33, 19250–19261.10.1523/JNEUROSCI.2148-13.2013Suche in Google Scholar

Petronilli, V., Costantini, P., Scorrano, L., Colonna, R., Passamonti, S., and Bernardi, P. (1994). The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J. Biol. Chem. 269, 16638–16642.10.1016/S0021-9258(19)89437-1Suche in Google Scholar PubMed

Pinar, O., Ozden, Y.A., Omur, E., and Muhtesem, G. (2017). Heat shock proteins in multiple sclerosis. Adv. Exp. Med. Biol. 958, 29–42.10.1007/978-3-319-47861-6_3Suche in Google Scholar PubMed

Quoilin, C., Mouithys-Mickalad, A., Lecart, S., Fontaine-Aupart, M.P., and Hoebeke, M. (2014). Evidence of oxidative stress and mitochondrial respiratory chain dysfunction in an in vitro model of sepsis-induced kidney injury. Biochim. Biophys. Acta 1837, 1790–1800.10.1016/j.bbabio.2014.07.005Suche in Google Scholar

Rabinovich, D., Yaniv, S.P., Alyagor, I., and Schuldiner, O. (2016). Nitric oxide as a switching mechanism between axon degeneration and regrowth during developmental remodeling. Cell 164, 170–182.10.1016/j.cell.2015.11.047Suche in Google Scholar PubMed

Rachek, L.I., Grishko, V.I., Ledoux, S.P., and Wilson, G.L. (2006). Role of nitric oxide-induced mtDNA damage in mitochondrial dysfunction and apoptosis. Free Radic. Biol. Med. 40, 754–762.10.1016/j.freeradbiomed.2005.09.028Suche in Google Scholar PubMed

Radi, R., Beckman, J.S., Bush, K.M., and Freeman, B.A. (1991). Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288, 481–487.10.1016/0003-9861(91)90224-7Suche in Google Scholar PubMed

Radi, R., Cassina, A., and Hodara, R. (2002). Nitric oxide and peroxynitrite interactions with mitochondria. Biol. Chem. 383, 401–409.10.1515/BC.2002.044Suche in Google Scholar PubMed

Rasola, A. and Bernardi, P. (2011). Mitochondrial permeability transition in Ca²⁺-dependent apoptosis and necrosis. Cell Calcium 50, 222–233.10.1016/j.ceca.2011.04.007Suche in Google Scholar

Ricciardolo, F.L., Sterk, P.J., Gaston, B., and Folkerts, G. (2004). Nitric oxide in health and disease of the respiratory system. Physiol. Rev. 84, 731–765.10.1152/physrev.00034.2003Suche in Google Scholar PubMed

Richter, C., Gogvadze, V., Laffranchi, R., Schlapbach, R., Schweizer, M., Suter, M., Walter, P., and Yaffee, M. (1995). Oxidants in mitochondria: from physiology to diseases. Biochim. Biophys. Acta 1271, 67–74.10.1016/0925-4439(95)00012-SSuche in Google Scholar PubMed

Rinholm, J.E. and Bergersen, L.H. (2012). Neuroscience: the wrap that feeds neurons. Nature 487, 435–436.10.1038/487435aSuche in Google Scholar PubMed

Rocher, C., Taanman, J.W., Pierron, D., Faustin, B., Benard, G., Rossignol, R., Malgat, M., Pedespan, L., and Letellier, T. (2008). Influence of mitochondrial DNA level on cellular energy metabolism: implications for mitochondrial diseases. J. Bioenerg. Biomembr. 40, 59–67.10.1007/s10863-008-9130-5Suche in Google Scholar PubMed

Roger, N., Barbera, J.A., Farre, R., Cobos, A., Roca, J., and Rodriguez-Roisin, R. (1996). Effect of nitric oxide inhalation on respiratory system resistance in chronic obstructive pulmonary disease. Eur. Respir. J. 9, 190–195.10.1183/09031936.96.09020190Suche in Google Scholar PubMed

Rolo, A.P., Oliveira, P.J., Moreno, A.J., and Palmeira, C.M. (2003). Chenodeoxycholate induction of mitochondrial permeability transition pore is associated with increased membrane fluidity and cytochrome c release: protective role of carvedilol. Mitochondrion 2, 305–311.10.1016/S1567-7249(03)00007-2Suche in Google Scholar PubMed

Romero, N., Denicola, A., and Radi, R. (2006). Red blood cells in the metabolism of nitric oxide-derived peroxynitrite. IUBMB Life 58, 572–580.10.1080/15216540600936549Suche in Google Scholar PubMed

Roozbeh, M., Mohammadpour, H., Azizi, G., Ghobadzadeh, S., and Mirshafiey, A. (2014). The potential role of iNKT cells in experimental allergic encephalitis and multiple sclerosis. Immunopharmacol. Immunotoxicol. 36, 105–113.10.3109/08923973.2014.897726Suche in Google Scholar PubMed

Rose, J.W., Hill, K.E., Watt, H.E., and Carlson, N.G. (2004). Inflammatory cell expression of cyclooxygenase-2 in the multiple sclerosis lesion. J. Neuroimmunol. 149, 40–49.10.1016/j.jneuroim.2003.12.021Suche in Google Scholar PubMed

Rostami, A. and Ciric, B. (2013). Role of Th17 cells in the pathogenesis of CNS inflammatory demyelination. J. Neurol. Sci. 333, 76–87.10.1016/j.jns.2013.03.002Suche in Google Scholar PubMed

Ruiz, A., Matute, C., and Alberdi, E. (2010). Intracellular Ca²⁺ release through ryanodine receptors contributes to AMPA receptor-mediated mitochondrial dysfunction and ER stress in oligodendrocytes. Cell Death Dis. 1, e54.10.1038/cddis.2010.31Suche in Google Scholar PubMed

Sas, K., Robotka, H., Toldi, J., and Vecsei, L. (2007). Mitochondria, metabolic disturbances, oxidative stress and the kynurenine system, with focus on neurodegenerative disorders. J. Neurol. Sci. 257, 221–239.10.1016/j.jns.2007.01.033Suche in Google Scholar PubMed

Saulsbury, M.D., Heyliger, S.O., Wang, K., and Johnson, D.J. (2009). Chlorpyrifos induces oxidative stress in oligodendrocyte progenitor cells. Toxicology 259, 1–9.10.1016/j.tox.2008.12.026Suche in Google Scholar PubMed

Scarlett, J.L., Packer, M.A., Porteous, C.M., and Murphy, M.P. (1996). Alterations to glutathione and nicotinamide nucleotides during the mitochondrial permeability transition induced by peroxynitrite. Biochem. Pharmacol. 52, 1047–1055.10.1016/0006-2952(96)99426-5Suche in Google Scholar PubMed

Scheiblich, H. and Bicker, G. (2016). Nitric oxide regulates antagonistically phagocytic and neurite outgrowth inhibiting capacities of microglia. Dev. Neurobiol. 76, 566–584.10.1002/dneu.22333Suche in Google Scholar PubMed

Schurr, A. and Rigor, B.M. (1998). Brain anaerobic lactate production: a suicide note or a survival kit? Dev. Neurosci. 20, 348–357.10.1159/000017330Suche in Google Scholar PubMed

Shivane, A.G. and Chakrabarty, A. (2007). Multiple sclerosis and demyelination. Curr. Diagn. Pathol. 13, 193–202.10.1016/j.cdip.2007.04.003Suche in Google Scholar

Smith, K.J. (2006). Axonal protection in multiple sclerosis – a particular need during remyelination? Brain 129, 3147–3149.10.1093/brain/awl323Suche in Google Scholar PubMed

Stewart, V.C., Land, J.M., Clark, J.B., and Heales, S.J. (1998). Pretreatment of astrocytes with interferon-alpha/beta prevents neuronal mitochondrial respiratory chain damage. J. Neurochem. 70, 432–434.10.1046/j.1471-4159.1998.70010432.xSuche in Google Scholar PubMed

Stewart, V.C., Sharpe, M.A., Clark, J.B., and Heales, S.J. (2000). Astrocyte-derived nitric oxide causes both reversible and irreversible damage to the neuronal mitochondrial respiratory chain. J. Neurochem. 75, 694–700.10.1046/j.1471-4159.2000.0750694.xSuche in Google Scholar PubMed

Stirling, D.P. and Stys, P.K. (2010). Mechanisms of axonal injury: internodal nanocomplexes and calcium deregulation. Trends Mol. Med. 16, 160–170.10.1016/j.molmed.2010.02.002Suche in Google Scholar PubMed

Stojanovic, I.R., Kostic, M., and Ljubisavljevic, S. (2014). The role of glutamate and its receptors in multiple sclerosis. J. Neural. Transm. (Vienna) 121, 945–955.10.1007/s00702-014-1188-0Suche in Google Scholar PubMed

Su, K.G., Banker, G., Bourdette, D., and Forte, M. (2009). Axonal degeneration in multiple sclerosis: the mitochondrial hypothesis. Curr. Neurol. Neurosci. Rep. 9, 411–417.10.1007/s11910-009-0060-3Suche in Google Scholar PubMed

Tanaka, J., Markerink-van Ittersum, M., Steinbusch, H.W., and De Vente, J. (1997). Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain. Glia 19, 286–297.10.1002/(SICI)1098-1136(199704)19:4<286::AID-GLIA2>3.0.CO;2-WSuche in Google Scholar PubMed

Tang, X., Lan, M., Zhang, M., and Yao, Z. (2017). Effect of nitric oxide to axonal degeneration in multiple sclerosis via downregulating monocarboxylate transporter 1 in oligodendrocytes. Nitric Oxide. 67, 75–80.10.1016/j.niox.2017.04.004Suche in Google Scholar PubMed

Tran, A.N., Boyd, N.H., Walker, K., and Hjelmeland, A.B. (2017). NOS expression and NO function in glioma and implications for patient therapies. Antioxid. Redox Signal. 26, 986–999.10.1089/ars.2016.6820Suche in Google Scholar PubMed

Tretyakova, N.Y., Burney, S., Pamir, B., Wishnok, J.S., Dedon, P.C., Wogan, G.N., and Tannenbaum, S.R. (2000). Peroxynitrite-induced DNA damage in the supF gene: correlation with the mutational spectrum. Mutat. Res. 447, 287–303.10.1016/S0027-5107(99)00221-3Suche in Google Scholar PubMed

Virarkar, M., Alappat, L., Bradford, P.G., and Awad, A.B. (2013). L-arginine and nitric oxide in CNS function and neurodegenerative diseases. Crit. Rev. Food Sci. Nutr. 53, 1157–1167.10.1080/10408398.2011.573885Suche in Google Scholar PubMed

Wahl, S.M., McCartney-Francis, N., Chan, J., Dionne, R., Ta, L., and Orenstein, J.M. (2003). Nitric oxide in experimental joint inflammation. Benefit or detriment? Cells Tiss. Org. 174, 26–33.10.1159/000070572Suche in Google Scholar PubMed

Wallace, D.C. (1994). Mitochondrial DNA mutations in diseases of energy metabolism. J. Bioenerg. Biomembr. 26, 241–250.10.1007/BF00763096Suche in Google Scholar PubMed

Wang, V., Chuang, T.C., Hsu, Y.D., Chou, W.Y., and Kao, M.C. (2005). Nitric oxide induces prion protein via MEK and p38 MAPK signaling. Biochem. Biophys. Res. Commun. 333, 95–100.10.1016/j.bbrc.2005.05.091Suche in Google Scholar PubMed

Wang, J.T., Medress, Z.A., and Barres, B.A. (2012). Axon degeneration: molecular mechanisms of a self-destruction pathway. J. Cell Biol. 196, 7–18.10.1083/jcb.201108111Suche in Google Scholar PubMed PubMed Central

Wang, J.Y., Lee, C.T., and Wang, J.Y. (2014). Nitric oxide plays a dual role in the oxidative injury of cultured rat microglia but not astroglia. Neuroscience 281, 164–177.10.1016/j.neuroscience.2014.09.048Suche in Google Scholar PubMed

Waxman, S.G. (2002). Sodium channels as molecular targets in multiple sclerosis. J. Rehabil. Res. Dev. 39, 233–242.Suche in Google Scholar PubMed

Welch, G. and Loscalzo, J. (1994). Nitric oxide and the cardiovascular system. J. Card. Surg. 9, 361–371.10.1111/j.1540-8191.1994.tb00857.xSuche in Google Scholar PubMed

Wilson, G.L., Patton, N.J., and LeDoux, S.P. (1997). Mitochondrial DNA in β-cells is a sensitive target for damage by nitric oxide. Diabetes 46, 1291–1295.10.2337/diab.46.8.1291Suche in Google Scholar PubMed

Wink, D.A., Kasprzak, K.S., Maragos, C.M., Elespuru, R.K., Misra, M., Dunams, T.M., Cebula, T.A., Koch, W.H., Andrews, A.W., Allen, J.S., et al. (1991). DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254, 1001–1003.10.1126/science.1948068Suche in Google Scholar PubMed

Winter, A.N., Ross, E.K., Khatter, S., Miller, K., and Linseman, D.A. (2016). Chemical basis for the disparate neuroprotective effects of the anthocyanins, callistephin and kuromanin, against nitrosative stress. Free Radic. Biol. Med. 103, 23–34.10.1016/j.freeradbiomed.2016.12.012Suche in Google Scholar PubMed

Witte, M.E., Mahad, D.J., Lassmann, H., and van Horssen, J. (2014). Mitochondrial dysfunction contributes to neurodegeneration in multiple sclerosis. Trends Mol. Med. 20, 179–187.10.1016/j.molmed.2013.11.007Suche in Google Scholar PubMed

Wynia-Smith, S.L. and Smith, B.C. (2017). Nitrosothiol formation and S-nitrosation signaling through nitric oxide synthases. Nitric Oxide 63, 52–60.10.1016/j.niox.2016.10.001Suche in Google Scholar PubMed

Xiao, B.G., Zhang, G.X., Ma, C.G., and Link, H. (1996). The cerebrospinal fluid from patients with multiple sclerosis promotes neuronal and oligodendrocyte damage by delayed production of nitric oxide in vitro. J. Neurol. Sci. 142, 114–120.10.1016/0022-510X(96)00164-5Suche in Google Scholar PubMed

Yamazawa, T. and Kakizawa, S. (2016). Nitric oxide-induced calcium release: neuronal cell death. Nihon Yakurigaku Zasshi 147, 200–205.10.1254/fpj.147.200Suche in Google Scholar PubMed

Yang, Z., Goronzy, J.J., and Weyand, C.M. (2015). Autophagy in autoimmune disease. J. Mol. Med. (Berl.) 93, 707–717.10.1007/s00109-015-1297-8Suche in Google Scholar PubMed

Yao, S.Y., Natarajan, C., and Sriram, S. (2012). nNOS mediated mitochondrial injury in LPS stimulated oligodendrocytes. Mitochondrion 12, 336–344.10.1016/j.mito.2012.01.002Suche in Google Scholar PubMed

Yermilov, V., Yoshie, Y., Rubio, J., and Ohshima, H. (1996). Effects of carbon dioxide/bicarbonate on induction of DNA single-strand breaks and formation of 8-nitroguanine, 8-oxoguanine and base-propenal mediated by peroxynitrite. FEBS Lett. 399, 67–70.10.1016/S0014-5793(96)01288-4Suche in Google Scholar PubMed

Yokota, T., Kamimura, N., Igarashi, T., Takahashi, H., Ohta, S., and Oharazawa, H. (2015). Protective effect of molecular hydrogen against oxidative stress caused by peroxynitrite derived from nitric oxide in rat retina. Clin. Exp. Ophthalmol. 43, 568–577.10.1111/ceo.12525Suche in Google Scholar PubMed

Yuste, J.E., Tarragon, E., Campuzano, C.M., and Ros-Bernal, F. (2015). Implications of glial nitric oxide in neurodegenerative diseases. Front Cell Neurosci. 9, 322.10.3389/fncel.2015.00322Suche in Google Scholar PubMed PubMed Central

Zahoor, I., Haq, E., and Asimi, R. (2017). Multiple sclerosis and EIF2B5: a paradox or a missing link. Adv. Exp. Med. Biol. 958, 57–64.10.1007/978-3-319-47861-6_5Suche in Google Scholar PubMed

Zhang, Y., Wang, H., Li, J., Dong, L., Xu, P., Chen, W., Neve, R.L., Volpe, J.J., and Rosenberg, P.A. (2006). Intracellular zinc release and ERK phosphorylation are required upstream of 12-lipoxygenase activation in peroxynitrite toxicity to mature rat oligodendrocytes. J. Biol. Chem. 281, 9460–9470.10.1074/jbc.M510650200Suche in Google Scholar PubMed

Zhang, Y., Chen, Y., Gucek, M., and Xu, H. (2016). The mitochondrial outer membrane protein MDI promotes local protein synthesis and mtDNA replication. EMBO J. 35, 1045–1057.10.15252/embj.201592994Suche in Google Scholar PubMed PubMed Central

Zindler, E. and Zipp, F. (2010). Neuronal injury in chronic CNS inflammation. Best Pract. Res. Clin. Anaesthesiol. 24, 551–562.10.1016/j.bpa.2010.11.001Suche in Google Scholar PubMed

Zou, M.H., Shi, C., and Cohen, R.A. (2002). Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. J. Clin. Invest. 109, 817–826.10.1172/JCI0214442Suche in Google Scholar PubMed