Reduction of zinc accumulation in mitochondria contributes to decreased cerebral ischemic injury by normobaric hyperoxia treatment in an experimental stroke model

Experimental Neurology

Volumn 272, Issue , 2015, Pages 181-189

  Dong, Wen ^a   Qi, Zhifeng ^a   Liang, Jia ^a   Shi, Wenjuan ^a   Zhao, Yongmei ^a   Luo, Yumin ^a   Ji, Xunming ^a   Liu, Ke Jian ^a,b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Brain; Ischemia; Mitochondria; Oxygen; Penumbra; Zinc

Indexed keywords

CYTOCHROME C; ZINC; CHOLINESTERASE INHIBITOR; ENOLASE; ETHYLENEDIAMINE DERIVATIVE; N,N,N',N'-TETRAKIS(2-PYRIDYLMETHYL)ETHYLENEDIAMINE; OXYGEN; RHODZIN-3; XANTHENE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; CELL DAMAGE; CELL LEVEL; CELL MEMBRANE DEPOLARIZATION; CELL SURVIVAL; CONTROLLED STUDY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; NORMOBARIC HYPEROXIA; OXYGEN THERAPY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; TRANSIENT ISCHEMIC ATTACK; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; HEMISPHERIC DOMINANCE; INFARCTION, MIDDLE CEREBRAL ARTERY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CHOLINESTERASE INHIBITORS; CYTOCHROMES C; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHYLENEDIAMINES; FUNCTIONAL LATERALITY; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXYGEN; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, SPRAGUE-DAWLEY; XANTHENES; ZINC;

EID: 84945469885     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.04.005     Document Type: Article

References (40)

1. An H., Liu Q., Chen Y., Vo K.D., Ford A.L., Lee J.M., Lin W. Oxygen metabolism in ischemic stroke using magnetic resonance imaging. Transl. Stroke Res. 2012, 3:65-75.
2. Astrup J., Siesjo B.K., Symon L. Thresholds in cerebral ischemia-the ischemic penumbra. Stroke 1981, 12:723-725.
3. Bonanni L., Chachar M., Jover-Mengual T., et al. Zinc-dependent multi-conductance channel activity in mitochondria isolated from ischemic brain. J. Neurosci. 2006, 26:6851-6862.
4. Calderone A., Jover T., Mashiko T., Noh K.M., Tanaka H., Bennett M.V., Zukin R.S. Late calcium EDTA rescues hippocampal CA1 neurons from global ischemia-induced death. J. Neurosci. 2004, 24:9903-9913.
5. Chen F., Qi Z., Luo Y., Hinchliffe T., Ding G., Xia Y., Ji X. Non-pharmaceutical therapies for stroke: mechanisms and clinical implications. Prog. Neurobiol. 2014, 115:246-269.
6. Chiu E.H., Liu C.S., Tan T.Y., Chang K.C. Venturi mask adjuvant oxygen therapy in severe acute ischemic stroke. Arch. Neurol. 2006, 63:741-744.
7. Cuajungco M.P., Lees G.J. Diverse effects of metal chelating agents on the neuronal cytotoxicity of zinc in the hippocampus. Brain Res. 1998, 799:97-107.
8. Deng J., Lei C., Chen Y., et al. Neuroprotective gases-fantasy or reality for clinical use?. Prog. Neurobiol. 2014, 115:210-245.
9. Dineley K.E., Richards L.L., Votyakova T.V., Reynolds I.J. Zinc causes loss of membrane potential and elevates reactive oxygen species in rat brain mitochondria. Mitochondrion 2005, 5:55-65.
10. Foley L.M., Hitchens T.K., Barbe B., Zhang F., Ho C., Rao G.R., Nemoto E.M. Quantitative temporal profiles of penumbra and infarction during permanent middle cerebral artery occlusion in rats. Transl. Stroke Res. 2010, 1:220-229.
11. Ford A.L., An H., Vo K.D., Lin W., Lee J.M. Defining the ischemic penumbra using hyperacute neuroimaging: deriving quantitative ischemic thresholds. Transl. Stroke Res. 2012, 3:198-204.
12. Galasso S.L., Dyck R.H. The role of zinc in cerebral ischemia. Mol. Med. 2007, 13:380-387.
13. Gazaryan I.G., Krasinskaya I.P., Kristal B.S., Brown A.M. Zinc irreversibly damages major enzymes of energy production and antioxidant defense prior to mitochondrial permeability transition. J. Biol. Chem. 2007, 282:24373-24380.
14. Henninger N., Fisher M. Normobaric hyperoxia-a promising approach to expand the time window for acute stroke treatment. Cerebrovasc. Dis. 2006, 21:134-136.
15. Henninger N., Bouley J., Nelligan J.M., Sicard K.M., Fisher M. Normobaric hyperoxia delays perfusion/diffusion mismatch evolution, reduces infarct volume, and differentially affects neuronal cell death pathways after suture middle cerebral artery occlusion in rats. J. Cereb. Blood Flow Metab. 2007, 27:1632-1642.
16. Jiang D., Sullivan P.G., Sensi S.L., Steward O., Weiss J.H. Zn(2+) induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. J. Biol. Chem. 2001, 276:47524-47529.
17. Lai T.W., Zhang S., Wang Y.T. Excitotoxicity and stroke: identifying novel targets for neuroprotection. Prog. Neurobiol. 2014, 115:157-188.
18. Leng T., Shi Y., Xiong Z.G., Sun D. Proton-sensitive cation channels and ion exchangers in ischemic brain injury: new therapeutic targets for stroke?. Prog. Neurobiol. 2014, 115:189-209.
19. 2 in ischemic penumbra and core are differentially affected following transient focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 2004, 24:343-349.
20. Liu S., Liu W., Ding W., Miyake M., Rosenberg G.A., Liu K.J. Electron paramagnetic resonance-guided normobaric hyperoxia treatment protects the brain by maintaining penumbral oxygenation in a rat model of transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2006, 26:1274-1284.
21. Liu W., Hendren J., Qin X.J., Shen J., Liu K.J. Normobaric hyperoxia attenuates early blood-brain barrier disruption by inhibiting MMP-9-mediated occludin degradation in focal cerebral ischemia. J. Neurochem. 2009, 108:811-820.
22. Liu J., Wang Y., Akamatsu Y., Lee C.C., Stetler R.A., Lawton M.T., Yang G.Y. Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials. Prog. Neurobiol. 2014, 115:138-156.
23. Medvedeva Y.V., Weiss J.H. Intramitochondrial Zn2+ accumulation via the Ca2+ uniporter contributes to acute ischemic neurodegeneration. Neurobiol. Dis. 2014, 68:137-144.
24. Medvedeva Y.V., Lin B., Shuttleworth C.W., Weiss J.H. Intracellular Zn2+ accumulation contributes to synaptic failure, mitochondrial depolarization, and cell death in an acute slice oxygen-glucose deprivation model of ischemia. J. Neurosci. 2009, 29:1105-1114.
25. Pan R., Chen C., Liu W.-L., Liu K.-J. Zinc promotes the death of hypoxic astrocytes by upregulating hypoxia-induced hypoxia-inducible factor-1alpha expression via poly(ADP-ribose) polymerase-1. CNS Neurosci. Ther. 2013, 19:511-520.
26. Qi Z., Yan F., Shi W., et al. AKT-related autophagy contributes to the neuroprotective efficacy of hydroxysafflor yellow A against ischemic stroke in rats. Transl. Stroke Res. 2014, 5:501-509.
27. Sensi S.L., Yin H.Z., Weiss J.H. AMPA/kainate receptor-triggered Zn2+ entry into cortical neurons induces mitochondrial Zn2+ uptake and persistent mitochondrial dysfunction. Eur. J. Neurosci. 2000, 12:3813-3818.
28. Sensi S.L., Ton-That D., Sullivan P.G., Jonas E.A., Gee K.R., Kaczmarek L.K., Weiss J.H. Modulation of mitochondrial function by endogenous Zn2+ pools. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6157-6162.
29. Sensi S.L., Paoletti P., Bush A.I., Sekler I. Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci. 2009, 10:780-791.
30. Shin H.K., Dunn A.K., Jones P.B., Boas D.A., Lo E.H., Moskowitz M.A., Ayata C. Normobaric hyperoxia improves cerebral blood flow and oxygenation, and inhibits peri-infarct depolarizations in experimental focal ischaemia. Brain 2007, 130:1631-1642.
31. Shuttleworth C.W., Weiss J.H. Zinc: new clues to diverse roles in brain ischemia. Trends Pharmacol. Sci. 2011, 32:480-486.
32. Singhal A.B., Dijkhuizen R.M., Rosen B.R., Lo E.H. Normobaric hyperoxia reduces MRI diffusion abnormalities and infarct size in experimental stroke. Neurology 2002, 58:945-952.
33. Singhal A.B., Benner T., Roccatagliata L., Koroshetz W.J., Schaefer P.W., Lo E.H., Buonanno F.S., Gonzalez R.G., Sorensen A.G. A pilot study of normobaric oxygen therapy in acute ischemic stroke. Stroke 2005, 36:797-802.
34. Song M., Yu S.P. Ionic regulation of cell volume changes and cell death after ischemic stroke. Transl. Stroke Res. 2014, 5:17-27.
35. Swanson R.A., Morton M.T., Tsao-Wu G., Savalos R.A., Davidson C., Sharp F.R. A semiautomated method for measuring brain infarct volume. J. Cereb. Blood Flow Metab. 1990, 10:290-293.
36. Tajiri N., Dailey T., Metcalf C., et al. In vivo animal stroke models: a rationale for rodent and non-human primate models. Transl. Stroke Res. 2013, 4:308-321.
37. Yin H.Z., Sensi S.L., Ogoshi F., Weiss J.H. Blockade of Ca2+-permeable AMPA/kainate channels decreases oxygen-glucose deprivation-induced Zn2+ accumulation and neuronal loss in hippocampal pyramidal neurons. J. Neurosci. 2002, 22:1273-1279.
38. Zhao Y., Pan R., Li S., et al. Chelating intracellularly accumulated zinc decreased ischemic brain injury through reducing neuronal apoptotic death. Stroke 2014, 45:1139-1147.
39. Zhou J., van Zijl P.C. Defining an acidosis-based ischemic penumbra from pH-weighted MRI. Transl. Stroke Res. 2011, 3:76-83.
40. Zhu G., Michel P., Zhang W., Wintermark M. Standardization of stroke perfusion CT for reperfusion therapy. Transl. Stroke Res. 2012, 3:221-227.