Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Research Article

Naked Mole-Rat Cortex Maintains Reactive Oxygen Species Homeostasis During In Vitro Hypoxia or Ischemia and Reperfusion

Author(s): Liam Eaton, Tina Wang, Maria Roy and Matthew E. Pamenter*

Volume 21, Issue 6, 2023

Published on: 08 June, 2022

Page: [1450 - 1461] Pages: 12

DOI: 10.2174/1570159X20666220327220929

Price: $65

Abstract

Neuronal injury during acute hypoxia, ischemia, and following reperfusion are partially attributable to oxidative damage caused by deleterious fluctuations of reactive oxygen species (ROS). In particular, mitochondrial superoxide (O2•-) production is believed to upsurge during lowoxygen conditions and also following reperfusion, before being dismutated to H2O2 and released into the cell. However, disruptions of redox homeostasis may be beneficially attenuated in the brain of hypoxia-tolerant species, such as the naked mole-rat (NMR, Heterocephalus glaber). As such, we hypothesized that ROS homeostasis is better maintained in the brain of NMRs during severe hypoxic/ ischemic insults and following reperfusion. We predicted that NMR brain would not exhibit substantial fluctuations in ROS during hypoxia or reoxygenation, unlike previous reports from hypoxiaintolerant mouse brain. To test this hypothesis, we measured cortical ROS flux using corrected total cell fluorescence measurements from live brain slices loaded with the MitoSOX red superoxide (O2•-) indicator or chloromethyl 2’,7’-dichlorodihydrofluorescein diacetate (CM-H2-DCFDA; which fluoresces with whole-cell hydrogen peroxide (H2O2) production) during various low-oxygen treatments, exogenous oxidative stress, and reperfusion. We found that NMR cortex maintained ROS homeostasis during low-oxygen conditions, while mouse cortex exhibited a ~40% increase and a ~30% decrease in mitochondrial O2•- and cellular H2O2 production, respectively. Mitochondrial ROS homeostasis in NMRs was only disrupted following sodium cyanide application, which was similarly observed in mice. Our results suggest that NMRs have evolved strategies to maintain ROS homeostasis during acute bouts of hypoxia and reoxygenation, potentially as an adaptation to life in an intermittently hypoxic environment.

Keywords: Anoxia, sodium cyanide, H2O2, superoxide, mitochondria, electron transport system.

« Previous
Graphical Abstract

[1]
Wang, Y.; Zang, Q.S.; Liu, Z.; Wu, Q.; Maass, D.; Dulan, G.; Shaul, P.W.; Melito, L.; Frantz, D.E.; Kilgore, J.A.; Williams, N.S.; Terada, L.S.; Nwariaku, F.E. Regulation of VEGF-induced endothelial cell migration by mitochondrial reactive oxygen species. Am. J. Physiol. Cell Physiol., 2011, 301(3), C695-C704.
[http://dx.doi.org/10.1152/ajpcell.00322.2010] [PMID: 21653897]
[2]
West, A.P.; Shadel, G.S.; Ghosh, S. Mitochondria in innate immune responses. Nat. Rev. Immunol., 2011, 11(6), 389-402.
[http://dx.doi.org/10.1038/nri2975] [PMID: 21597473]
[3]
Finkel, T. Signal transduction by mitochondrial oxidants. J. Biol. Chem., 2012, 287(7), 4434-4440.
[http://dx.doi.org/10.1074/jbc.R111.271999] [PMID: 21832045]
[4]
Kiselyov, K.; Muallem, S. ROS and intracellular ion channels. Cell Calcium, 2016, 60(2), 108-114.
[http://dx.doi.org/10.1016/j.ceca.2016.03.004] [PMID: 26995054]
[5]
Scherz-Shouval, R.; Shvets, E.; Fass, E.; Shorer, H.; Gil, L.; Elazar, Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J., 2007, 26(7), 1749-1760.
[http://dx.doi.org/10.1038/sj.emboj.7601623] [PMID: 17347651]
[6]
Starkov, A.A.; Andreyev, A.Y.; Zhang, S.F.; Starkova, N.N.; Korneeva, M.; Syromyatnikov, M.; Popov, V.N. Scavenging of H2O2 by mouse brain mitochondria. J. Bioenerg. Biomembr., 2014, 46(6), 471-477.
[http://dx.doi.org/10.1007/s10863-014-9581-9] [PMID: 25248416]
[7]
Munro, D.; Banh, S.; Sotiri, E.; Tamanna, N.; Treberg, J.R. The thioredoxin and glutathione-dependent H2O2 consumption pathways in muscle mitochondria: Involvement in H2O2 metabolism and consequence to H2O2 efflux assays. Free Radic. Biol. Med., 2016, 96, 334-346.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.04.014] [PMID: 27101737]
[8]
Drechsel, D.A.; Patel, M. Respiration-dependent H2O2 removal in brain mitochondria via the thioredoxin/peroxiredoxin system. J. Biol. Chem., 2010, 285(36), 27850-27858.
[http://dx.doi.org/10.1074/jbc.M110.101196] [PMID: 20558743]
[9]
Martínez, M.C.; Andriantsitohaina, R. Reactive nitrogen species: Molecular mechanisms and potential significance in health and disease. Antioxid. Redox Signal., 2009, 11(3), 669-702.
[http://dx.doi.org/10.1089/ars.2007.1993] [PMID: 19014277]
[10]
Apel, K.; Hirt, H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol., 2004, 55(1), 373-399.
[http://dx.doi.org/10.1146/annurev.arplant.55.031903.141701] [PMID: 15377225]
[11]
Levraut, J.; Iwase, H.; Shao, Z.H.; Vanden Hoek, T.L.; Schumacker, P.T. Cell death during ischemia: Relationship to mitochondrial depolarization and ROS generation. Am. J. Physiol. -Hear. Circ. Physiol., 2003, 284(253-2), 549-558.
[http://dx.doi.org/10.1152/ajpheart.00708.2002]
[12]
Marchi, S.; Giorgi, C.; Suski, J.M.; Agnoletto, C.; Bononi, A.; Bonora, M.; De Marchi, E.; Missiroli, S.; Patergnani, S.; Poletti, F.; Rimessi, A.; Duszynski, J.; Wieckowski, M.R.; Pinton, P. Mitochondria-ros crosstalk in the control of cell death and aging. J. Signal Transduct., 2012, 2012, 329635.
[http://dx.doi.org/10.1155/2012/329635] [PMID: 22175013]
[13]
Adam-Vizi, V. Production of reactive oxygen species in brain mitochondria: Contribution by electron transport chain and non-electron transport chain sources. Antioxid. Redox Signal., 2005, 7(9-10), 1140-1149.
[http://dx.doi.org/10.1089/ars.2005.7.1140] [PMID: 16115017]
[14]
Chandel, N.S.; Maltepe, E.; Goldwasser, E.; Mathieu, C.E.; Simon, M.C.; Schumacker, P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA, 1998, 95(20), 11715-11720.
[http://dx.doi.org/10.1073/pnas.95.20.11715] [PMID: 9751731]
[15]
Berry, C.E.; Hare, J.M. Xanthine oxidoreductase and cardiovascular disease: Molecular mechanisms and pathophysiological implications. J. Physiol., 2004, 555(Pt 3), 589-606.
[http://dx.doi.org/10.1113/jphysiol.2003.055913] [PMID: 14694147]
[16]
Guzy, R.D.; Hoyos, B.; Robin, E.; Chen, H.; Liu, L.; Mansfield, K.D.; Simon, M.C.; Hammerling, U.; Schumacker, P.T. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab., 2005, 1(6), 401-408.
[http://dx.doi.org/10.1016/j.cmet.2005.05.001] [PMID: 16054089]
[17]
MacGregor, D.G.; Avshalumov, M.V.; Rice, M.E. Brain edema induced by in vitro ischemia: Causal factors and neuroprotection. J. Neurochem., 2003, 85(6), 1402-1411.
[http://dx.doi.org/10.1046/j.1471-4159.2003.01772.x] [PMID: 12787060]
[18]
Abramov, A.Y.; Scorziello, A.; Duchen, M.R. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J. Neurosci., 2007, 27(5), 1129-1138.
[http://dx.doi.org/10.1523/JNEUROSCI.4468-06.2007] [PMID: 17267568]
[19]
Fekete, A.; Vizi, E.S.; Kovács, K.J.; Lendvai, B.; Zelles, T. Layer-specific differences in reactive oxygen species levels after oxygen-glucose deprivation in acute hippocampal slices. Free Radic. Biol. Med., 2008, 44(6), 1010-1022.
[http://dx.doi.org/10.1016/j.freeradbiomed.2007.11.022] [PMID: 18206124]
[20]
Wilson, D.F.; Rumsey, W.L.; Green, T.J.; Vanderkooi, J.M. The oxygen dependence of mitochondrial oxidative phosphorylation measured by a new optical method for measuring oxygen concentration. J. Biol. Chem., 1988, 263(6), 2712-2718.
[http://dx.doi.org/10.1016/S0021-9258(18)69126-4] [PMID: 2830260]
[21]
Scialò, F.; Fernández-Ayala, D.J.; Sanz, A. Role of mitochondrial reverse electron transport in ROS signaling: Potential roles in health and disease. Front. Physiol., 2017, 8, 428.
[http://dx.doi.org/10.3389/fphys.2017.00428] [PMID: 28701960]
[22]
Orr, A.L.; Ashok, D.; Sarantos, M.R.; Shi, T.; Hughes, R.E.; Brand, M.D. Inhibitors of ROS production by the ubiquinone-binding site of mitochondrial complex I identified by chemical screening. Free Radic. Biol. Med., 2013, 65, 1047-1059.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.08.170] [PMID: 23994103]
[23]
Quinlan, C.L.; Orr, A.L.; Perevoshchikova, I.V.; Treberg, J.R.; Ackrell, B.A.; Brand, M.D. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J. Biol. Chem., 2012, 287(32), 27255-27264.
[http://dx.doi.org/10.1074/jbc.M112.374629] [PMID: 22689576]
[24]
Paddenberg, R.; Ishaq, B.; Goldenberg, A.; Faulhammer, P.; Rose, F.; Weissmann, N.; Braun-Dullaeus, R. C.; Kummer, W. Essential role of complex II of the respiratory chain in hypoxia-induced ROS generation in the pulmonary vasculature. Am. J. Physiol. - Lung Cell. Mol. Physiol., 2003, 284(5 28-5), 710-719.
[http://dx.doi.org/10.1152/ajplung.00149.2002]
[25]
Du, G.; Mouithys-Mickalad, A.; Sluse, F.E. Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radic. Biol. Med., 1998, 25(9), 1066-1074.
[http://dx.doi.org/10.1016/S0891-5849(98)00148-8] [PMID: 9870560]
[26]
Milton, S.L.; Nayak, G.; Kesaraju, S.; Kara, L.; Prentice, H.M. Suppression of reactive oxygen species production enhances neuronal survival in vitro and in vivo in the anoxia-tolerant turtle Trachemys scripta. J. Neurochem., 2007, 101(4), 993-1001.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04466.x] [PMID: 17326763]
[27]
Pamenter, M.E.; Richards, M.D.; Buck, L.T. Anoxia-induced changes in reactive oxygen species and cyclic nucleotides in the painted turtle. J. Comp. Physiol. B, 2007, 177(4), 473-481.
[http://dx.doi.org/10.1007/s00360-007-0145-8] [PMID: 17347830]
[28]
Hogg, D.W.; Pamenter, M.E.; Dukoff, D.J.; Buck, L.T. Decreases in mitochondrial reactive oxygen species initiate GABA(A) receptor-mediated electrical suppression in anoxia-tolerant turtle neurons. J. Physiol., 2015, 593(10), 2311-2326.
[http://dx.doi.org/10.1113/JP270474] [PMID: 25781154]
[29]
Larson, J.; Park, T.J. Extreme hypoxia tolerance of naked mole-rat brain. Neuroreport, 2009, 20(18), 1634-1637.
[http://dx.doi.org/10.1097/WNR.0b013e32833370cf] [PMID: 19907351]
[30]
Braude, S.; Holtze, S.; Begall, S.; Brenmoehl, J.; Burda, H.; Dammann, P.; Del Marmol, D.; Gorshkova, E.; Henning, Y.; Hoeflich, A.; Höhn, A.; Jung, T.; Hamo, D.; Sahm, A.; Shebzukhov, Y.; Šumbera, R.; Miwa, S.; Vyssokikh, M.Y.; von Zglinicki, T.; Averina, O.; Hildebrandt, T.B. Surprisingly long survival of premature conclusions about naked mole-rat biology. Biol. Rev. Camb. Philos. Soc., 2021, 96(2), 376-393.
[http://dx.doi.org/10.1111/brv.12660] [PMID: 33128331]
[31]
Buffenstein, R.; Amoroso, V.; Andziak, B.; Avdieiev, S.; Azpurua, J.; Barker, A.J.; Bennett, N.C.; Brieño Enríquez, M.A.; Bronner, G.N.; Coen, C.; Delaney, M.A.; Dengler Crish, C.M.; Edrey, Y.H.; Faulkes, C.G.; Frankel, D.; Friedlander, G.; Gibney, P.A.; Gorbunova, V.; Hine, C.; Holmes, M.M.; Jarvis, J.U.M.; Kawamura, Y.; Kutsukake, N.; Kenyon, C.; Khaled, W.T.; Kikusui, T.; Kissil, J.; Lagestee, S.; Larson, J.; Lauer, A.; Lavrenchenko, L.A.; Lee, A.; Levitt, J.B.; Lewin, G.R.; Lewis, H.K.N.; Lin, T.D.; Mason, M.J.; McCloskey, D.; McMahon, M.; Miura, K.; Mogi, K.; Narayan, V.; O’Connor, T.P.; Okanoya, K.; O’Riain, M.J.; Park, T.J.; Place, N.J.; Podshivalova, K.; Pamenter, M.E.; Pyott, S.J.; Reznick, J.; Ruby, J.G.; Salmon, A.B.; Santos Sacchi, J.; Sarko, D.K.; Seluanov, A.; Shepard, A.; Smith, M.; Storey, K.B.; Tian, X.; Vice, E.N.; Viltard, M.; Watarai, A.; Wywial, E.; Yamakawa, M.; Zemlemerova, E.D.; Zions, M.; Smith, E.S.J. The naked truth: A comprehensive clarification and classification of current ‘Myths’ in naked mole rat biology. Biol. Rev. Camb. Philos. Soc., 2002, 97(1), 115-140.
[http://dx.doi.org/10.1111/brv.12791] [PMID: 34476892]
[32]
Ilacqua, A.N.; Kirby, A.M.; Pamenter, M.E. Behavioural responses of naked mole rats to acute hypoxia and anoxia. Biol. Lett., 2017, 13(12), 1-4.
[http://dx.doi.org/10.1098/rsbl.2017.0545] [PMID: 29263131]
[33]
Kirby, A.M.; Fairman, G.D.; Pamenter, M.E. Atypical behavioural, metabolic and thermoregulatory responses to hypoxia in the naked mole rat (heterocephalus glaber). J. Zool. (Lond.), 2018, 305(2), 106-115.
[http://dx.doi.org/10.1111/jzo.12542]
[34]
Park, T.J.; Reznick, J.; Peterson, B.L.; Blass, G.; Omerbašić, D.; Bennett, N.C.; Kuich, P.H.J.L.; Zasada, C.; Browe, B.M.; Hamann, W.; Applegate, D.T.; Radke, M.H.; Kosten, T.; Lutermann, H.; Gavaghan, V.; Eigenbrod, O.; Bégay, V.; Amoroso, V.G.; Govind, V; Minshall, R.D.; Smith, E.S.J.; Larson, J.; Gotthardt, M.; Kempa, S.; Lewin, G.R. Fructose-driven glycolysis supports anoxia resistance in the naked mole-rat. Science (80-.), 2017, 356(6335), 307-311.
[http://dx.doi.org/10.1126/science.aab3896]
[35]
Peterson, B.L.; Larson, J.; Buffenstein, R.; Park, T.J.; Fall, C.P. Blunted neuronal calcium response to hypoxia in naked mole-rat hippocampus. PLoS One, 2012, 7(2), e31568.
[http://dx.doi.org/10.1371/journal.pone.0031568] [PMID: 22363676]
[36]
Pamenter, M.E.; Lau, G.Y.; Richards, J.G.; Milsom, W.K. Naked mole rat brain mitochondria electron transport system flux and H+ leak are reduced during acute hypoxia. J. Exp. Biol., 2018, 221(Pt 4), jeb171397.
[http://dx.doi.org/10.1242/jeb.171397] [PMID: 29361591]
[37]
Farhat, E.; Devereaux, M.E.M.; Cheng, H.; Weber, J.M.; Pamenter, M.E. Na+/K+-ATPase activity is regionally regulated by acute hypoxia in naked mole-rat brain. Neurosci. Lett., 2021, 764, 136244.
[http://dx.doi.org/10.1016/j.neulet.2021.136244] [PMID: 34530116]
[38]
Cheng, H.; Qin, Y.A.; Dhillon, R.; Dowell, J.; Denu, J.M.; Pamenter, M.E. Metabolomic analysis of carbohydrate and amino acid changes induced by hypoxia in naked mole-rat brain and liver. Metabolites, 2022, 12(1), 56.
[http://dx.doi.org/10.3390/metabo12010056] [PMID: 35050178]
[39]
Pamenter, M.E.; Dzal, Y.A.; Thompson, W.A.; Milsom, W.K. Do naked mole rats accumulate a metabolic acidosis or an oxygen debt in severe hypoxia? J. Exp. Biol., 2019, 222(Pt 3), jeb191197.
[http://dx.doi.org/10.1242/jeb.191197] [PMID: 30573665]
[40]
Cheng, H.; Munro, D.; Huynh, K.; Pamenter, M.E. Naked mole-rat skeletal muscle mitochondria exhibit minimal functional plasticity in acute or chronic hypoxia. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2021, 255(255), 110596.
[http://dx.doi.org/10.1016/j.cbpb.2021.110596] [PMID: 33757832]
[41]
Wang, T.H.; Eaton, L.; Pamenter, M.E. Nitric oxide homeostasis is maintained during acute in vitro hypoxia and following reoxygenation in naked mole-rat but not mouse cortical neurons. Comp. Biochem. Physiol. A Mol. Integr. Physiol., 2020, 250, 110792.
[http://dx.doi.org/10.1016/j.cbpa.2020.110792] [PMID: 32805413]
[42]
Cheng, H.; Pamenter, M.E. Naked mole-rat brain mitochondria tolerate in vitro ischaemia. J. Physiol., 2021, 599(20), 4671-4685.
[http://dx.doi.org/10.1113/JP281942] [PMID: 34472099]
[43]
Munro, D.; Baldy, C.; Pamenter, M.E.; Treberg, J.R. The exceptional longevity of the naked mole-rat may be explained by mitochondrial antioxidant defenses. Aging Cell, 2019, 18(3), e12916.
[http://dx.doi.org/10.1111/acel.12916] [PMID: 30768748]
[44]
Munro, D.; Pamenter, M.E. Comparative studies of mitochondrial reactive oxygen species in animal longevity: Technical pitfalls and possibilities. Aging Cell, 2019, 18(5), e13009.
[http://dx.doi.org/10.1111/acel.13009] [PMID: 31322803]
[45]
Lesuisse, C.; Martin, L.J. Long-term culture of mouse cortical neurons as a model for neuronal development, aging, and death. J. Neurobiol., 2002, 51(1), 9-23.
[http://dx.doi.org/10.1002/neu.10037] [PMID: 11920724]
[46]
Du, S.N.N.; Mahalingam, S.; Borowiec, B.G.; Scott, G.R. Mitochondrial physiology and reactive oxygen species production are altered by hypoxia acclimation in killifish (Fundulus heteroclitus). J. Exp. Biol., 2016, 219(Pt 8), 1130-1138.
[http://dx.doi.org/10.1242/jeb.132860] [PMID: 26896545]
[47]
Ali, S.S.; Hsiao, M.; Zhao, H.W.; Dugan, L.L.; Haddad, G.G.; Zhou, D. Hypoxia-adaptation involves mitochondrial metabolic depression and decreased ROS leakage. PLoS One, 2012, 7(5), e36801.
[http://dx.doi.org/10.1371/journal.pone.0036801] [PMID: 22574227]
[48]
Xu, W.; Chi, L.; Row, B.W.; Xu, R.; Ke, Y.; Xu, B.; Luo, C.; Kheirandish, L.; Gozal, D.; Liu, R. Increased oxidative stress is associated with chronic intermittent hypoxia-mediated brain cortical neuronal cell apoptosis in a mouse model of sleep apnea. Neuroscience, 2004, 126(2), 313-323.
[http://dx.doi.org/10.1016/j.neuroscience.2004.03.055] [PMID: 15207349]
[49]
Auten, R.L.; Davis, J.M. Oxygen toxicity and reactive oxygen species: The devil is in the details. Pediatr. Res., 2009, 66(2), 121-127.
[http://dx.doi.org/10.1203/PDR.0b013e3181a9eafb] [PMID: 19390491]
[50]
Schieber, M.; Chandel, N.S. ROS function in redox signaling and oxidative stress. Curr. Biol., 2014, 24(10), R453-R462.
[http://dx.doi.org/10.1016/j.cub.2014.03.034] [PMID: 24845678]
[51]
Torres-Cuevas, I.; Corral-Debrinski, M.; Gressens, P. Brain oxidative damage in murine models of neonatal hypoxia/ischemia and reoxygenation. Free Radic. Biol. Med., 2019, 142, 3-15.
[http://dx.doi.org/10.1016/j.freeradbiomed.2019.06.011] [PMID: 31226400]
[52]
Mahalingam, S.; McClelland, G.B.; Scott, G.R. Evolved changes in the intracellular distribution and physiology of muscle mitochondria in high-altitude native deer mice. J. Physiol., 2017, 595(14), 4785-4801.
[http://dx.doi.org/10.1113/JP274130] [PMID: 28418073]
[53]
Schülke, S.; Dreidax, D.; Malik, A.; Burmester, T.; Nevo, E.; Band, M.; Avivi, A.; Hankeln, T. Living with stress: Regulation of antioxidant defense genes in the subterranean, hypoxia-tolerant mole rat, Spalax. Gene, 2012, 500(2), 199-206.
[http://dx.doi.org/10.1016/j.gene.2012.03.019] [PMID: 22441129]
[54]
Chouchani, E.T.; Pell, V.R.; Gaude, E.; Aksentijević, D.; Sundier, S.Y.; Robb, E.L.; Logan, A.; Nadtochiy, S.M.; Ord, E.N.J.; Smith, A.C.; Eyassu, F.; Shirley, R.; Hu, C.H.; Dare, A.J.; James, A.M.; Rogatti, S.; Hartley, R.C.; Eaton, S.; Costa, A.S.H.; Brookes, P.S.; Davidson, S.M.; Duchen, M.R.; Saeb-Parsy, K.; Shattock, M.J.; Robinson, A.J.; Work, L.M.; Frezza, C.; Krieg, T.; Murphy, M.P. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature, 2014, 515(7527), 431-435.
[http://dx.doi.org/10.1038/nature13909] [PMID: 25383517]
[55]
Dong, Y.; Zhang, W.; Lai, B.; Luan, W.J.; Zhu, Y.H.; Zhao, B.Q.; Zheng, P. Two free radical pathways mediate chemical hypoxia-induced glutamate release in synaptosomes from the prefrontal cortex. Biochim. Biophys. Acta, 2012, 1823(2), 493-504.
[http://dx.doi.org/10.1016/j.bbamcr.2011.10.004] [PMID: 22057390]
[56]
Jensen, M.S.; Ahlemeyer, B.; Ravati, A.; Thakur, P.; Mennel, H.D.; Krieglstein, J. Preconditioning-induced protection against cyanide-induced neurotoxicity is mediated by preserving mitochondrial function. Neurochem. Int., 2002, 40(4), 285-293.
[http://dx.doi.org/10.1016/S0197-0186(01)00096-1] [PMID: 11792457]
[57]
Choi, D.W. Excitotoxic cell death. J. Neurobiol., 1992, 23(9), 1261-1276.
[http://dx.doi.org/10.1002/neu.480230915] [PMID: 1361523]
[58]
Ozaki, S.; Hirose, J.; Kidani, Y. Electron-transfer reaction between Fe(CN)64-/Fe(CN)63- and Copper(II)/Copper(I) ions in bovine erythrocyte superoxide dismutase: Ph dependence and inhibition by various kinds of anions. Inorg. Chem., 1988, 27(21), 3746-3751.
[http://dx.doi.org/10.1021/ic00294a015]
[59]
Zorov, D.B.; Juhaszova, M.; Sollott, S.J. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev., 2014, 94(3), 909-950.
[http://dx.doi.org/10.1152/physrev.00026.2013] [PMID: 24987008]
[60]
Maiti, P.; Singh, S.B.; Sharma, A.K.; Muthuraju, S.; Banerjee, P.K.; Ilavazhagan, G. Hypobaric hypoxia induces oxidative stress in rat brain. Neurochem. Int., 2006, 49(8), 709-716.
[http://dx.doi.org/10.1016/j.neuint.2006.06.002] [PMID: 16911847]
[61]
Pamenter, M.E.; Ali, S.S.; Tang, Q.; Finley, J.C.; Gu, X.Q.; Dugan, L.L.; Haddad, G.G. An in vitro ischemic penumbral mimic perfusate increases NADPH oxidase-mediated superoxide production in cultured hippocampal neurons. Brain Res., 2012, 1452, 165-172.
[http://dx.doi.org/10.1016/j.brainres.2012.03.004] [PMID: 22459046]
[62]
Bhowmick, S.; Moore, J.T.; Kirschner, D.L.; Drew, K.L. Arctic ground squirrel hippocampus tolerates oxygen glucose deprivation independent of hibernation season even when not hibernating and after ATP depletion, acidosis, and glutamate efflux. J. Neurochem., 2017, 142(1), 160-170.
[http://dx.doi.org/10.1111/jnc.13996] [PMID: 28222226]
[63]
Carroll, B.; Otten, E.G.; Manni, D.; Stefanatos, R.; Menzies, F.M.; Smith, G.R.; Jurk, D.; Kenneth, N.; Wilkinson, S.; Passos, J.F.; Attems, J.; Veal, E.A.; Teyssou, E.; Seilhean, D.; Millecamps, S.; Eskelinen, E.L.; Bronowska, A.K.; Rubinsztein, D.C.; Sanz, A.; Korolchuk, V.I. Oxidation of SQSTM1/p62 mediates the link between redox state and protein homeostasis. Nat. Commun., 2018, 9(1), 256.
[http://dx.doi.org/10.1038/s41467-017-02746-z] [PMID: 29343728]
[64]
Row, B.W.; Liu, R.; Xu, W.; Kheirandish, L.; Gozal, D. Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am. J. Respir. Crit. Care Med., 2003, 167(11), 1548-1553.
[http://dx.doi.org/10.1164/rccm.200209-1050OC] [PMID: 12615622]
[65]
Sbodio, J.I.; Snyder, S.H.; Paul, B.D. Redox mechanisms in neurodegeneration: From disease outcomes to therapeutic opportunities. Antioxid. Redox Signal., 2019, 30(11), 1450-1499.
[http://dx.doi.org/10.1089/ars.2017.7321] [PMID: 29634350]
[66]
Døhlen, G.; Carlsen, H.; Blomhoff, R.; Thaulow, E.; Saugstad, O.D. Reoxygenation of hypoxic mice with 100% oxygen induces brain nuclear factor-kappa B. Pediatr. Res., 2005, 58(5), 941-945.
[http://dx.doi.org/10.1203/01.PDR.0000182595.62545.EE] [PMID: 16183808]
[67]
Dhar-Mascareño, M.; Cárcamo, J.M.; Golde, D.W. Hypoxia-reoxygenation-induced mitochondrial damage and apoptosis in human endothelial cells are inhibited by vitamin C. Free Radic. Biol. Med., 2005, 38(10), 1311-1322.
[http://dx.doi.org/10.1016/j.freeradbiomed.2005.01.017] [PMID: 15855049]
[68]
Chouchani, E.T.; Pell, V.R.; James, A.M.; Work, L.M.; Saeb-Parsy, K.; Frezza, C.; Krieg, T.; Murphy, M.P. A unifying mechanism for mitochondrial superoxide production during ischemiareperfusion injury. Cell Metab., 2016, 23(2), 254-263.
[http://dx.doi.org/10.1016/j.cmet.2015.12.009] [PMID: 26777689]

Rights & Permissions Print Cite
Article Metrics
37
1
© 2024 Bentham Science Publishers | Privacy Policy