Chemical conditioning as an approach to ischemic stroke tolerance: Mitochondria as the target

International Journal of Molecular Sciences

Volumn 17, Issue 3, 2016, Pages

  Jin, Zhen ^a   Wu, Jinzi ^a   Yan, Liang Jun ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Chemical conditioning; Hypoxic conditioning; Ischemic conditioning; Mitochondria; Neuroprotection; Stroke injury

Indexed keywords

3 NITROPROPIONIC ACID; ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM ION; CARBON DIOXIDE; CARBON MONOXIDE; CYANIDE; CYCLOPHILIN D; CYTOCHROME C OXIDASE; DIAZOXIDE; ISOFLURANE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NICOTINAMIDE ADENINE DINUCLEOTIDE; SUCCINATE DEHYDROGENASE; MITOCHONDRIAL PROTEIN; NEUROPROTECTIVE AGENT;

BRAIN HYPOXIA; BRAIN ISCHEMIA; CELL DEATH; CROSS TOLERANCE; HUMAN; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NEUROPROTECTION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; REPERFUSION INJURY; REVIEW; TISSUE INJURY; ANIMAL; BRAIN; COMPLICATION; DRUG EFFECTS; METABOLISM; STROKE; VASCULARIZATION;

ANIMALS; BRAIN; BRAIN ISCHEMIA; HUMANS; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEUROPROTECTIVE AGENTS; STROKE;

EID: 84960096545     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17030351     Document Type: Review

References (107)

1. Kitagawa, K.; Matsumoto, M.; Tagaya, M.; Hata, R.; Ueda, H.; Niinobe, M.; Handa, N.; Fukunaga, R.; Kimura, K.; Mikoshiba, K.; et al. “Ischemic tolerance” phenomenon found in the brain. Brain Res. 1990, 528, 21–24.
2. Della-Morte, D.; Guadagni, F.; Palmirotta, R.; Ferroni, P.; Testa, G.; Cacciatore, F.; Abete, P.; Rengo, F.; Perez-Pinzon, M.A.; Sacco, R.L.; et al. Genetics and genomics of ischemic tolerance: Focus on cardiac and cerebral ischemic preconditioning. Pharmacogenomics 2012, 13, 1741–1757.
3. Prass, K.; Scharff, A.; Ruscher, K.; Lowl, D.; Muselmann, C.; Victorov, I.; Kapinya, K.; Dirnagl, U.; Meisel, A. Hypoxia-induced stroke tolerance in the mouse is mediated by erythropoietin. Stroke 2003, 34, 1981–1986.
4. Obrenovitch, T.P. Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol. Rev. 2008, 88, 211–247.
5. Wang, Y.; Reis, C.; Applegate, R., 2nd; Stier, G.; Martin, R.; Zhang, J.H. Ischemic conditioning-induced endogenous brain protection: Applications pre-, per- or post-stroke. Exp. Neurol. 2015, 272, 26–40.
6. Cuomo, O.; Vinciguerra, A.; Cerullo, P.; Anzilotti, S.; Brancaccio, P.; Bilo, L.; Scorziello, A.; Molinaro, P.; di Renzo, G.; Pignataro, G. Ionic homeostasis in brain conditioning. Front. Neurosci. 2015, 9.
7. Pan, J.; Li, X.; Peng, Y. Remote ischemic conditioning for acute ischemic stroke: Dawn in the darkness. Rev. Neurosci. 2016.
8. Yamashita, T.; Abe, K. Recent progress in therapeutic strategy for ischemic stroke. Cell Transplant. 2016.
9. Fairbanks, S.L.; Brambrink, A.M. Preconditioning and postconditioning for neuroprotection: The most recent evidence. Best Pract. Res. Clin. Anaesthesiol. 2010, 24, 521–534.
10. Pignataro, G.; Cuomo, O.; Vinciguerra, A.; Sirabella, R.; Esposito, E.; Boscia, F.; di Renzo, G.; Annunziato, L. Ncx as a key player in the neuroprotection exerted by ischemic preconditioning and postconditioning. Adv. Exp. Med. Biol. 2013, 961, 223–240.
11. Pignataro, G.; Scorziello, A.; di Renzo, G.; Annunziato, L. Post-ischemic brain damage: Effect of ischemic preconditioning and postconditioning and identification of potential candidates for stroke therapy. Febs J. 2009, 276, 46–57.
12. Zhao, H. Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J. Cereb. Blood Flow Metab. 2009, 29, 873–885.
13. Yamashita, T.; Deguchi, K.; Sehara, Y.; Lukic-Panin, V.; Zhang, H.; Kamiya, T.; Abe, K. Therapeutic strategy for ischemic stroke. Neurochem. Res. 2009, 34, 707–710.
14. Dezfulian, C.; Garrett, M.; Gonzalez, N.R. Clinical application of preconditioning and postconditioning to achieve neuroprotection. Transl. Stroke Res. 2013, 4, 19–24.
15. Rybnikova, E.; Samoilov, M. Current insights into the molecular mechanisms of hypoxic pre- and postconditioning using hypobaric hypoxia. Front. Neurosci. 2015, 9.
16. Esposito, E.; Desai, R.; Ji, X.; Lo, E.H. Pharmacologic pre- and postconditioning for stroke: Basic mechanisms and translational opportunity. Brain Circ. 2015, 1, 104–113.
17. Sharma, A.; Goyal, R. Experimental brain ischemic preconditioning: A concept to putative targets. CNS Neurol. Disord. Drug Targets 2015. in press.
18. Hassell, K.J.; Ezzati, M.; Alonso-Alconada, D.; Hausenloy, D.J.; Robertson, N.J. New horizons for newborn brain protection: Enhancing endogenous neuroprotection. Arch. Dis. Child. Fetal Neonatal. Ed. 2015, 100, F541–F552.
19. Dirnagl, U.; Becker, K.; Meisel, A. Preconditioning and tolerance against cerebral ischaemia: From experimental strategies to clinical use. Lancet Neurol. 2009, 8, 398–412.
20. Dirnagl, U.; Meisel, A. Endogenous neuroprotection: Mitochondria as gateways to cerebral preconditioning? Neuropharmacology 2008, 55, 334–344.
21. Davis, D.P.; Patel, P.M. Ischemic preconditioning in the brain. Curr. Opin. Anaesthesiol. 2003, 16, 447–452.
22. Moro, M.A.; Almeida, A.; Bolanos, J.P.; Lizasoain, I. Mitochondrial respiratory chain and free radical generation in stroke. Free Radic. Biol. Med. 2005, 39, 1291–1304.
23. Sims, N.R.; Anderson, M.F. Mitochondrial contributions to tissue damage in stroke. Neurochem. Int. 2002, 40, 511–526.
24. Zhan, R.Z.; Fujihara, H.; Baba, H.; Yamakura, T.; Shimoji, K. Ischemic preconditioning is capable of inducing mitochondrial tolerance in the rat brain. Anesthesiology 2002, 97, 896–901.
25. Jackson, M.J.; Papa, S.; Bolanos, J.; Bruckdorfer, R.; Carlsen, H.; Elliott, R.M.; Flier, J.; Griffiths, H.R.; Heales, S.; Holst, B.; et al. Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function. Mol. Asp. Med. 2002, 23, 209–285.
26. Warner, D.S.; Sheng, H.; Batinic-Haberle, I. Oxidants, antioxidants and the ischemic brain. J. Exp. Biol. 2004, 207, 3221–3231.
27. Lenaz, G. Mitochondria and reactive oxygen species. Which role in physiology and pathology? Adv. Exp. Med. Biol. 2012, 942, 93–136.
28. Brookes, P.S.; Yoon, Y.; Robotham, J.L.; Anders, M.W.; Sheu, S.S. Calcium, atp, and ROS: A mitochondrial love-hate triangle. Am. J. Physiol. Cell Physiol. 2004, 287, C817–C833.
29. 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 ischemia-reperfusion injury. Cell Metab. 2016, 23, 254–263.
30. Genova, M.L.; Pich, M.M.; Bernacchia, A.; Bianchi, C.; Biondi, A.; Bovina, C.; Falasca, A.I.; Formiggini, G.; Castelli, G.P.; Lenaz, G. The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann. N. Y. Acad. Sci. 2004, 1011, 86–100.
31. Griffiths, E.J.; Halestrap, A.P. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem. J. 1995, 307, 93–98.
32. Li, P.; Nijhawan, D.; Budihardjo, I.; Srinivasula, S.M.; Ahmad, M.; Alnemri, E.S.; Wang, X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91, 479–489.
33. Budihardjo, I.; Oliver, H.; Lutter, M.; Luo, X.; Wang, X. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 1999, 15, 269–290.
34. Wu, J.; Luo, X.; Yan, L.J. Two dimensional blue native/SDS-PAGE to identify mitochondrial complex I subunits modified by 4-hydroxynonenal (HNE). Front. Physiol. 2015, 6, 98.
35. Yan, L.J. Analysis of oxidative modification of proteins. Curr. Protoc. Protein Sci. 2009.
36. Anderson, E.J.; Katunga, L.A.; Willis, M.S. Mitochondria as a source and target of lipid peroxidation products in healthy and diseased heart. Clin. Exp. Pharmacol. Physiol. 2012, 39, 179–193.
37. Ames, B.N.; Shigenaga, M.K. Oxidants are a major contributor to aging. Ann. N. Y. Acad. Sci. 1992, 663, 85–96.
38. Shacter, E. Protein oxidative damage. Methods Enzymol. 2000, 319, 428–436.
39. Chen, H.; Yoshioka, H.; Kim, G.S.; Jung, J.E.; Okami, N.; Sakata, H.; Maier, C.M.; Narasimhan, P.; Goeders, C.E.; Chan, P.H. Oxidative stress in ischemic brain damage: Mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid. Redox Signal. 2011, 14, 1505–1517.
40. Brookes, P.S.; Hoffman, D.L. Aging and cardiac ischemia-mitochondria and free radical consideration. In Oxidative Stress in Aging: From Model Systems to Human Diseases; Miwa, S., Bechkman, K.B., Muller, F.L., Eds.; Humana Press: Totowa, NJ, USA, 2008; pp. 253–268.
41. Lebuffe, G.; Schumacker, P.T.; Shao, Z.H.; Anderson, T.; Iwase, H.; Vanden Hoek, T.L. ROS and NO trigger early preconditioning: Relationship to mitochondrial KATP channel. Am. J. Physiol. Heart Circ. Physiol. 2003, 284, H299–H308.
42. Wang, X.; Wang, H.; Xu, L.; Rozanski, D.J.; Sugawara, T.; Chan, P.H.; Trzaskos, J.M.; Feuerstein, G.Z. Significant neuroprotection against ischemic brain injury by inhibition of the MEK1 protein kinase in mice: Exploration of potential mechanism associated with apoptosis. J. Pharmacol. Exp. Ther. 2003, 304, 172–178.
43. Liang, H.W.; Xia, Q.; Bruce, I.C. Reactive oxygen species mediate the neuroprotection conferred by a mitochondrial ATP-sensitive potassium channel opener during ischemia in the rat hippocampal slice. Brain Res. 2005, 1042, 169–175.
44. Pong, K. Ischaemic preconditioning: Therapeutic implications for stroke? Expert Opin. Ther. Targets 2004, 8, 125–139.
45. Blanco, M.; Lizasoain, I.; Sobrino, T.; Vivancos, J.; Castillo, J. Ischemic preconditioning: A novel target for neuroprotective therapy. Cerebrovasc. Dis. 2006, 21, 38–47.
46. Kirino, T. Ischemic tolerance. J. Cereb. Blood Flow Metab. 2002, 22, 1283–1296.
47. Zhao, H. The protective effect of ischemic postconditioning against ischemic injury: From the heart to the brain. J. Neuroimmune Pharmacol. 2007, 2, 313–318.
48. Thompson, J.W.; Dave, K.R.; Young, J.I.; Perez-Pinzon, M.A. Ischemic preconditioning alters the epigenetic profile of the brain from ischemic intolerance to ischemic tolerance. Neurotherapeutics 2013, 10, 789–797.
49. N, T.V.; Sangwan, A.; Sharma, B.; Majid, A.; Gk, R. Cerebral ischemic preconditioning: The road so far. Mol. Neurobiol. 2015.
50. Zhao, H.; Ren, C.; Chen, X.; Shen, J. From rapid to delayed and remote postconditioning: The evolving concept of ischemic postconditioning in brain ischemia. Curr. Drug Targets 2012, 13, 173–187.
51. Stowe, A.M.; Wacker, B.K.; Cravens, P.D.; Perfater, J.L.; Li, M.K.; Hu, R.; Freie, A.B.; Stuve, O.; Gidday, J.M. CCL2 upregulation triggers hypoxic preconditioning-induced protection from stroke. J. Neuroinflamm. 2012, 9.
52. Galle, A.A.; Jones, N.M. The neuroprotective actions of hypoxic preconditioning and postconditioning in a neonatal rat model of hypoxic-ischemic brain injury. Brain Res. 2013, 1498, 1–8.
53. Stowe, A.M.; Altay, T.; Freie, A.B.; Gidday, J.M. Repetitive hypoxia extends endogenous neurovascular protection for stroke. Ann. Neurol. 2011, 69, 975–985.
54. Riepe, M.W.; Ludolph, A.C. Chemical preconditioning: A cytoprotective strategy. Mol. Cell. Biochem. 1997, 174, 249–254.
55. Hoshi, A.; Nakahara, T.; Kayama, H.; Yamamoto, T. Ischemic tolerance in chemical preconditioning: Possible role of astrocytic glutamine synthetase buffering glutamate-mediated neurotoxicity. J. Neurosci. Res. 2006, 84, 130–141.
56. Riepe, M.W.; Esclaire, F.; Kasischke, K.; Schreiber, S.; Nakase, H.; Kempski, O.; Ludolph, A.C.; Dirnagl, U.; Hugon, J. Increased hypoxic tolerance by chemical inhibition of oxidative phosphorylation: “Chemical preconditioning”. J. Cereb. Blood Flow Metab. 1997, 17, 257–264.
57. Stetler, R.A.; Leak, R.K.; Gan, Y.; Li, P.; Zhang, F.; Hu, X.; Jing, Z.; Chen, J.; Zigmond, M.J.; Gao, Y. Preconditioning provides neuroprotection in models of CNS disease: Paradigms and clinical significance. Prog. Neurobiol. 2014, 114, 58–83.
58. Jeong, J.I.; Lee, Y.W.; Kim, Y.K. Chemical hypoxia-induced cell death in human glioma cells: Role of reactive oxygen species, ATP depletion, mitochondrial damage and Ca2+. Neurochem. Res. 2003, 28, 1201–1211.
59. Roemgens, A.; Singh, S.; Beyer, C.; Arnold, S. Inducers of chemical hypoxia act in a gender- and brain region-specific manner on primary astrocyte viability and cytochrome c oxidase. Neurotox. Res. 2011, 20, 1–14.
60. Danielisova, V.; Gottlieb, M.; Nemethova, M.; Kravcukova, P.; Domorakova, I.; Mechirova, E.; Burda, J. Bradykinin postconditioning protects pyramidal Ca1 neurons against delayed neuronal death in rat hippocampus. Cell. Mol. Neurobiol. 2009, 29, 871–878.
61. Luo, X.; Li, R.; Yan, L.J. Roles of pyruvate, nadh, and mitochondrial complex I in redox balance and imbalance in ß cell function and dysfunction. J. Diabetes Res. 2015, 2015.
62. Luo, X.; Wu, J.; Jing, S.; Yan, L.J. Hyperglycemic stress and carbon stress in diabetic glucotoxicity. Aging Dis. 2016, 7, 90–110.
63. Lieberman, M.; Marks, A.D. Marks’ Basic Medical Biochemistry: A Clinical Approach, 4th ed.; Wolters Kluwer/Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2013.
64. Sun, X.; Sun, J.; Liu, L.; Ding, Z. Isoflurane preconditioning and postconditioning in multiple organ protection. J. Biochem. Pharmacol. Res. 2013, 1, 6–14.
65. Hanley, P.J.; Ray, J.; Brandt, U.; Daut, J. Halothane, isoflurane and sevoflurane inhibit NADH: Ubiquinone oxidoreductase (complex I) of cardiac mitochondria. J. Physiol. 2002, 544, 687–693.
66. Kayser, E.B.; Suthammarak, W.; Morgan, P.G.; Sedensky, M.M. Isoflurane selectively inhibits distal mitochondrial complex I in Caenorhabditis elegans. Anesth. Analg. 2011, 112, 1321–1329.
67. Pravdic, D.; Hirata, N.; Barber, L.; Sedlic, F.; Bosnjak, Z.J.; Bienengraeber, M. Complex I and ATP synthase mediate membrane depolarization and matrix acidification by isoflurane in mitochondria. Eur. J. Pharmacol. 2012, 690, 149–157.
68. Agarwal, B.; Dash, R.K.; Stowe, D.F.; Bosnjak, Z.J.; Camara, A.K. Isoflurane modulates cardiac mitochondrial bioenergetics by selectively attenuating respiratory complexes. Biochim. Biophys. Acta 2014, 1837, 354–365.
69. Sosunov, S.A.; Ameer, X.; Niatsetskaya, Z.V.; Utkina-Sosunova, I.; Ratner, V.I.; Ten, V.S. Isoflurane anesthesia initiated at the onset of reperfusion attenuates oxidative and hypoxic-ischemic brain injury. PLoS ONE 2015, 10, e0120456.
70. Schapira, A.H. Human complex I defects in neurodegenerative diseases. Biochim. Biophys. Acta 1998, 1364, 261–270.
71. Lefort, N.; Glancy, B.; Bowen, B.; Willis, W.T.; Bailowitz, Z.; de Filippis, E.A.; Brophy, C.; Meyer, C.; Hojlund, K.; Yi, Z.; et al. Increased reactive oxygen species production and lower abundance of complex I subunits and carnitine palmitoyltransferase 1B protein despite normal mitochondrial respiration in insulin-resistant human skeletal muscle. Diabetes 2010, 59, 2444–2452.
72. St-Pierre, J.; Buckingham, J.A.; Roebuck, S.J.; Brand, M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 2002, 277, 44784–44790.
73. Hirst, J.; King, M.S.; Pryde, K.R. The production of reactive oxygen species by complex i. Biochem. Soc. Trans. 2008, 36, 976–980.
74. Ludwig, L.M.; Tanaka, K.; Eells, J.T.; Weihrauch, D.; Pagel, P.S.; Kersten, J.R.; Warltier, D.C. Preconditioning by isoflurane is mediated by reactive oxygen species generated from mitochondrial electron transport chain complex III. Anesth. Analg. 2004, 99, 1308–1315.
75. Teixeira, G.; Chiari, P.; Fauconnier, J.; Abrial, M.; Couture-Lepetit, E.; Harisseh, R.; Pillot, B.; Lacampagne, A.; Tourneur, Y.; Gharib, A.; et al. Involvement of cyclophilin D and calcium in isoflurane-induced preconditioning. Anesthesiology 2015, 123, 1374–1384.
76. Zhao, P.; Ji, G.; Xue, H.; Yu, W.; Zhao, X.; Ding, M.; Yang, Y.; Zuo, Z. Isoflurane postconditioning improved long-term neurological outcome possibly via inhibiting the mitochondrial permeability transition pore in neonatal rats after brain hypoxia-ischemia. Neuroscience 2014, 280, 193–203.
77. Perier, C.; Bove, J.; Vila, M.; Przedborski, S. The rotenone model of parkinson’s disease. Trends Neurosci. 2003, 26, 345–346.
78. Schonfeld, P.; Reiser, G. Rotenone-like action of the branched-chain phytanic acid induces oxidative stress in mitochondria. J. Biol. Chem. 2006, 281, 7136–7142.
79. Marella, M.; Seo, B.B.; Nakamaru-Ogiso, E.; Greenamyre, J.T.; Matsuno-Yagi, A.; Yagi, T. Protection by the NDI1 gene against neurodegeneration in a rotenone rat model of parkinson’s disease. PLoS ONE 2008, 3, e1433.
80. Zhou, Q.; Liu, C.; Liu, W.; Zhang, H.; Zhang, R.; Liu, J.; Zhang, J.; Xu, C.; Liu, L.; Huang, S.; et al. Rotenone induction of hydrogen peroxide inhibits mTOR-mediated S6K1 and 4E-BP1/eIF4E pathways, leading to neuronal apoptosis. Toxicol. Sci. 2015, 143, 81–96.
81. Yan, L.J.; Sumien, N.; Thangthaeng, N.; Forster, M.J. Reversible inactivation of dihydrolipoamide dehydrogenase by mitochondrial hydrogen peroxide. Free Radic. Res. 2013, 47, 123–133.
82. Turrens, J.F.; Alexandre, A.; Lehninger, A.L. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 1985, 237, 408–414.
83. Sun, F.; Huo, X.; Zhai, Y.; Wang, A.; Xu, J.; Su, D.; Bartlam, M.; Rao, Z. Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 2005, 121, 1043–1057.
84. Hirata, T.; Fukuse, T.; Ishikawa, S.; Hanaoka, S.; Chen, Q.; Shoji, T.; Wada, H. “Chemical preconditioning” by 3-nitropropionate reduces ischemia-reperfusion injury in cardiac-arrested rat lungs. Transplantation 2001, 71, 352–359.
85. Brambrink, A.M.; Schneider, A.; Noga, H.; Astheimer, A.; Gotz, B.; Korner, I.; Heimann, A.; Welschof, M.; Kempski, O. Tolerance-inducing dose of 3-nitropropionic acid modulates bcl-2 and bax balance in the rat brain: A potential mechanism of chemical preconditioning. J. Cereb. Blood Flow Metab. 2000, 20, 1425–1436.
86. Hoshi, A.; Nakahara, T.; Ogata, M.; Yamamoto, T. The critical threshold of 3-nitropropionic acid-induced ischemic tolerance in the rat. Brain Res. 2005, 1050, 33–39.
87. Wiegand, F.; Liao, W.; Busch, C.; Castell, S.; Knapp, F.; Lindauer, U.; Megow, D.; Meisel, A.; Redetzky, A.; Ruscher, K.; et al. Respiratory chain inhibition induces tolerance to focal cerebral ischemia. J. Cereb. Blood Flow Metab. 1999, 19, 1229–1237.
88. Cooper, C.E.; Brown, G.C. The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: Chemical mechanism and physiological significance. J. Bioenerg. Biomembr. 2008, 40, 533–539.
89. Correia, S.C.; Santos, R.X.; Cardoso, S.M.; Santos, M.S.; Oliveira, C.R.; Moreira, P.I. Cyanide preconditioning protects brain endothelial and NT2 neuron-like cells against glucotoxicity: Role of mitochondrial reactive oxygen species and HIF-1. Neurobiol. Dis. 2012, 45, 206–218.
90. 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, 285–293.
91. Queiroga, C.S.; Almeida, A.S.; Martel, C.; Brenner, C.; Alves, P.M.; Vieira, H.L. Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis. J. Biol. Chem. 2010, 285, 17077–17088.
92. Hochgrafe, F.; Mostertz, J.; Albrecht, D.; Hecker, M. Fluorescence thiol modification assay: Oxidatively modified proteins in Bacillus subtilis. Mol. Microbiol. 2005, 58, 409–425.
93. Lim, S.Y.; Davidson, S.M.; Hausenloy, D.J.; Yellon, D.M. Preconditioning and postconditioning: The essential role of the mitochondrial permeability transition pore. Cardiovasc. Res. 2007, 75, 530–535.
94. Yan, L.J.; Christians, E.S.; Liu, L.; Xiao, X.; Sohal, R.S.; Benjamin, I.J. Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J. 2002, 21, 5164–5172.
95. Fan, Y.Y.; Shen, Z.; He, P.; Jiang, L.; Hou, W.W.; Shen, Y.; Zhang, X.N.; Hu, W.W.; Chen, Z. A novel neuroprotective strategy for ischemic stroke: Transient mild acidosis treatment by CO2 inhalation at reperfusion. J. Cereb. Blood Flow Metab. 2014, 34, 275–283.
96. Garcia de Arriba, S.; Franke, H.; Pissarek, M.; Nieber, K.; Illes, P. Neuroprotection by ATP-dependent potassium channels in rat neocortical brain slices during hypoxia. Neurosci. Lett. 1999, 273, 13–16.
97. Yamauchi, T.; Kashii, S.; Yasuyoshi, H.; Zhang, S.; Honda, Y.; Akaike, A. Mitochondrial ATP-sensitive potassium channel: A novel site for neuroprotection. Investig. Ophthalmol. Vis. Sci. 2003, 44, 2750–2756.
98. Kis, B.; Rajapakse, N.C.; Snipes, J.A.; Nagy, K.; Horiguchi, T.; Busija, D.W. Diazoxide induces delayed pre-conditioning in cultured rat cortical neurons. J. Neurochem. 2003, 87, 969–980.
99. Robin, E.; Simerabet, M.; Hassoun, S.M.; Adamczyk, S.; Tavernier, B.; Vallet, B.; Bordet, R.; Lebuffe, G. Postconditioning in focal cerebral ischemia: Role of the mitochondrial ATP-dependent potassium channel. Brain Res. 2011, 1375, 137–146.
100. O’Sullivan, J.C.; Yao, X.L.; Alam, H.; McCabe, J.T. Diazoxide, as a postconditioning and delayed preconditioning trigger, increases HSP25 and HSP70 in the central nervous system following combined cerebral stroke and hemorrhagic shock. J. Neurotrauma 2007, 24, 532–546.
101. Wu, L.; Shen, F.; Lin, L.; Zhang, X.; Bruce, I.C.; Xia, Q. The neuroprotection conferred by activating the mitochondrial ATP-sensitive K+ channel is mediated by inhibiting the mitochondrial permeability transition pore. Neurosci. Lett. 2006, 402, 184–189.
102. Farkas, E.; Timmer, N.M.; Domoki, F.; Mihaly, A.; Luiten, P.G.; Bari, F. Post-ischemic administration of diazoxide attenuates long-term microglial activation in the rat brain after permanent carotid artery occlusion. Neurosci. Lett. 2005, 387, 168–172.
103. Stetler, R.A.; Leak, R.K.; Yin, W.; Zhang, L.; Wang, S.; Gao, Y.; Chen, J. Mitochondrial biogenesis contributes to ischemic neuroprotection afforded by LPS pre-conditioning. J. Neurochem. 2012, 123, 125–137.
104. Rosenzweig, H.L.; Minami, M.; Lessov, N.S.; Coste, S.C.; Stevens, S.L.; Henshall, D.C.; Meller, R.; Simon, R.P.; Stenzel-Poore, M.P. Endotoxin preconditioning protects against the cytotoxic effects of TNF after stroke: A novel role for TNF in LPS-ischemic tolerance. J. Cereb. Blood Flow Metab. 2007, 27, 1663–1674.
105. Vartanian, K.B.; Stevens, S.L.; Marsh, B.J.; Williams-Karnesky, R.; Lessov, N.S.; Stenzel-Poore, M.P. LPS preconditioning redirects TLR signaling following stroke: TRIF-IRF3 plays a seminal role in mediating tolerance to ischemic injury. J. Neuroinflamm. 2011, 8.
106. Marsh, B.; Stevens, S.L.; Packard, A.E.; Gopalan, B.; Hunter, B.; Leung, P.Y.; Harrington, C.A.; Stenzel-Poore, M.P. Systemic lipopolysaccharide protects the brain from ischemic injury by reprogramming the response of the brain to stroke: A critical role for IRF3. J. Neurosci. 2009, 29, 9839–9849.
107. Li, W.C.; Jiang, R.; Jiang, D.M.; Zhu, F.C.; Su, B.; Qiao, B.; Qi, X.T. Lipopolysaccharide preconditioning attenuates apoptotic processes and improves neuropathologic changes after spinal cord injury in rats. Int. J. Neurosci. 2013.