Chapter 9 Ischemic tolerance as an active and intrinsic neuroprotective mechanism

Handbook of Clinical Neurology

Volumn 92, Issue , 2008, Pages 171-195

  Stetler, R Anne ^a   Zhang, Feng ^a   Liu, Collin ^a   Chen, Jun ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 66049142543     PISSN: 00729752     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0072-9752(08)01909-X     Document Type: Review

References (219)

1. Abe H., and Nowak Jr. T.S. Postischemic temperature as a modulator of the stress response in brain: dissociation of heat shock protein 72 induction from ischemic tolerance after bilateral carotid artery occlusion in the gerbil. Neurosci Lett 295 (2000) 54-58
2. Abe H., and Nowak Jr. T.S. Induced hippocampal neuron protection in an optimized gerbil ischemia model: insult thresholds for tolerance induction and altered gene expression defined by ischemic depolarization. J Cereb Blood Flow Metab 24 (2004) 84-97
3. Alkayed N.J., Goyagi T., Joh H.D., et al. Neuroprotection and P450 2C11 upregulation after experimental transient ischemic attack. Stroke 33 (2002) 1677-1684
4. Amaravadi R., and Thompson C.B. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest 115 (2005) 2618-2624
5. Arthur P.G., Lim S.C., Meloni B.P., et al. The protective effect of hypoxic preconditioning on cortical neuronal cultures is associated with increases in the activity of several antioxidant enzymes. Brain Res 1017 (2004) 146-154
6. Atochin D.N., Clark J., Demchenko I.T., et al. Rapid cerebral ischemic preconditioning in mice deficient in endothelial and neuronal nitric oxide synthases. Stroke 34 (2003) 1299-1303
7. Badaut J., Hirt L., Price M., et al. Hypoxia/hypoglycemia preconditioning prevents the loss of functional electrical activity in organotypic slice cultures. Brain Res 1051 (2005) 117
8. Barone F.C., and Feuerstein G.Z. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19 (1999) 819-834
9. Barone F.C., White R.F., Spera P.A., et al. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29 (1998) 1937-1950
10. Barzilai A., and Yamamoto K. DNA damage responses to oxidative stress. DNA Repair (Amst) 3 (2004) 1109-1115
11. Bergeron M., Gidday J.M., Yu A.Y., et al. Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol 48 (2000) 285-296
12. Bernaudin M., Tang Y., Reilly M., et al. Brain genomic response following hypoxia and re-oxygenation in the neonatal rat. Identification of genes that might contribute to hypoxia-induced ischemic tolerance. J Biol Chem 277 (2002) 39728-39738
13. Bernaudin M., Nedelec A.S., Divoux D., et al. Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes, erythropoietin and VEGF, in the adult mouse brain. J Cereb Blood Flow Metab 22 (2002) 393-403
14. Blondeau N., Widmann C., Lazdunski M., et al. Activation of the nuclear factor-κB is a key event in brain tolerance. J Neurosci 21 (2001) 4668-4677
15. Bordet R., Deplanque D., Maboudou P., et al. Increase in endogenous brain superoxide dismutase as a potential mechanism of lipopolysaccharide-induced brain ischemic tolerance. J Cereb Blood Flow Metab 20 (2000) 1190-1196
16. Bruer U., Weih M.K., Isaev N.K., et al. Induction of tolerance in rat cortical neurons: hypoxic preconditioning. FEBS Lett 414 (1997) 117-121
17. Chen D., Minami M., Henshall D.C., et al. Upregulation of mitochondrial base-excision repair capability within rat brain after brief ischemia. J Cereb Blood Flow Metab 23 (2003) 88-98
18. Chen J., and Simon R. Ischemic tolerance in the brain. Neurology 48 (1997) 306-311
19. Chen J., Graham S.H., Zhu R.L., et al. Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 16 (1996) 566-577
20. Chen J., Jin K., Chen M., et al. Early detection of DNA strand breaks in the brain after transient focal ischemia: implications for the role of DNA damage in apoptosis and neuronal cell death. J Neurochem 69 (1997) 232-245
21. Chen J., Nagayama T., Jin K., et al. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 18 (1998) 4914-4928
22. Chiarugi A. Poly(ADP-ribosyl)ation and stroke. Pharmacol Res 52 (2005) 15-24
23. Chiarugi P. PTPs versus PTKs: the redox side of the coin. Free Radic Res 39 (2005) 353-364
24. Cho S., Park E.M., Zhou P., et al. Obligatory role of inducible nitric oxide synthase in ischemic preconditioning. J Cereb Blood Flow Metab 25 (2005) 493-501
25. Choi Y.B., Tenneti L., Le D.A., et al. Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nat Neurosci 3 (2000) 15-21
26. Chopp M., Chen H., Ho K.L., et al. Transient hyperthermia protects against subsequent forebrain ischemic cell damage in the rat. Neurology 39 (1989) 1396-1398
27. Chow A.K., Thompson C.S., Hogan M.J., et al. Cortical spreading depression transiently activates MAP kinases. Brain Res Mol Brain Res 99 (2002) 75-81
28. Cui J., Holmes E.H., and Liu P.K. Oxidative damage to the c-fos gene and reduction of its transcription after focal cerebral ischemia. J Neurochem 73 (1999) 1164-1174
29. Currie R.W., Ellison J.A., White R.F., et al. Benign focal ischemic preconditioning induces neuronal Hsp70 and prolonged astrogliosis with expression of Hsp27. Brain Res 863 (2000) 169-181
30. D'Amours D., Desnoyers S., D'Silva I., et al. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J 342 (1999) 249-268
31. Danielisova V., Nemethova M., Gottlieb M., et al. Changes of endogenous antioxidant enzymes during ischemic tolerance acquisition. Neurochem Res 30 (2005) 559-565
32. Dave K.R., Saul I., Busto R., et al. Ischemic preconditioning preserves mitochondrial function after global cerebral ischemia in rat hippocampus. J Cereb Blood Flow Metab 21 (2001) 1401-1410
33. Dawson D.A., Furuya K., Gotoh J., et al. Cerebrovascular hemodynamics and ischemic tolerance: lipopolysaccharide-induced resistance to focal cerebral ischemia is not due to changes in severity of the initial ischemic insult, but is associated with preservation of microvascular perfusion. J Cereb Blood Flow Metab 19 (1999) 616-623
34. DeGracia D.J., and Montie H.L. Cerebral ischemia and the unfolded protein response. J Neurochem 91 (2004) 1-8
35. Deutsch E., Berger M., Kussmaul W.G., et al. Adaptation to ischemia during percutaneous transluminal coronary angioplasty. Clinical, hemodynamic, and metabolic features. Circulation 82 (1990) 2044-2051
36. Dhodda V.K., Sailor K.A., Bowen K.K., et al. Putative endogenous mediators of preconditioning-induced ischemic tolerance in rat brain identified by genomic and proteomic analysis. J Neurochem 89 (2004) 73-89
37. Dirnagl U., Simon R.P., and Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26 (2003) 248-254
38. Drew K.L., Rice M.E., Kuhn T.B., et al. Neuroprotective adaptations in hibernation: therapeutic implications for ischemia-reperfusion, traumatic brain injury and neurodegenerative diseases. Free Radic Biol Med 31 (2001) 563-573
39. Drew K.L., Toien O., Rivera P.M., et al. Role of the antioxidant ascorbate in hibernation and warming from hibernation. Comp Biochem Physiol C Toxicol Pharmacol 133 (2002) 483-492
40. Dringen R., and Hirrlinger J. Glutathione pathways in the brain. Biol Chem 384 (2003) 505-516
41. Dringen R., Pfeiffer B., and Hamprecht B. Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J Neurosci 19 (1999) 562-569
42. Du C., Fang M., Li Y., et al. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102 (2000) 33-42
43. Freiberger J.J., Suliman H.B., Sheng H., et al. A comparison of hyperbaric oxygen versus hypoxic cerebral preconditioning in neonatal rats. Brain Res 1075 (2006) 213-222
44. Frerichs K.U., and Hallenbeck J.M. Hibernation in ground squirrels induces state and species-specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices. J Cereb Blood Flow Metab 18 (1998) 168-175
45. Fujiwara N., Higashi H., Shimoji K., et al. Effects of hypoxia on rat hippocampal neurones in vitro. J Physiol 384 (1987) 131-151
46. Furuta S., Ohta S., Hatakeyama T., et al. Recovery of protein synthesis in tolerance-induced hippocampal CA1 neurons after transient forebrain ischemia. Acta Neuropathol (Berl) 86 (1993) 329-336
47. Furuya K., Ginis I., Takeda H., et al. Cell permeable exogenous ceramide reduces infarct size in spontaneously hypertensive rats supporting in vitro studies that have implicated ceramide in induction of tolerance to ischemia. J Cereb Blood Flow Metab 21 (2001) 226-232
48. Furuya K., Zhu L., Kawahara N., et al. Differences in infarct evolution between lipopolysaccharide-induced tolerant and nontolerant conditions to focal cerebral ischemia. J Neurosurg 103 (2005) 715-723
49. Gao Y., Signore A.P., Yin W., et al. Neuroprotection against focal ischemic brain injury by inhibition of c-Jun N-terminal kinase and attenuation of the mitochondrial apoptosis-signaling pathway. J Cereb Blood Flow Metab 25 (2005) 694-712
50. Garcia L., Burda J., Hrehorovska M., et al. Ischaemic preconditioning in the rat brain: effect on the activity of several initiation factors, Akt and extracellular signal-regulated protein kinase phosphorylation, and GRP78 and GADD34 expression. J Neurochem 88 (2004) 136-147
51. Garnier P., Ying W., and Swanson R.A. Ischemic preconditioning by caspase cleavage of poly(ADP-ribose) polymerase-1. J Neurosci 23 (2003) 7967-7973
52. Gehrmann J., Mies G., Bonnekoh P., et al. Microglial reaction in the rat cerebral cortex induced by cortical spreading depression. Brain Pathol 3 (1993) 11-17
53. Gidday J.M., Shah A.R., Maceren R.G., et al. Nitric oxide mediates cerebral ischemic tolerance in a neonatal rat model of hypoxic preconditioning. J Cereb Blood Flow Metab 19 (1999) 331-340
54. Ginis I., Jaiswal R., Klimanis D., et al. TNF-alpha-induced tolerance to ischemic injury involves differential control of NF-kappaB transactivation: the role of NF-kappaB association with p300 adaptor. J Cereb Blood Flow Metab 22 (2002) 142-152
55. Glantz L., Avramovich A., Trembovler V., et al. Ischemic preconditioning increases antioxidants in the brain and peripheral organs after cerebral ischemia. Exp Neurol 192 (2005) 117-124
56. Glazier S.S., O'Rourke D.M., Graham D.I., et al. Induction of ischemic tolerance following brief focal ischemia in rat brain. J Cereb Blood Flow Metab 14 (1994) 545-553
57. Gonzalez-Zulueta M., Feldman A.B., Klesse L.J., et al. Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc Natl Acad Sci USA 97 (2000) 436-441
58. Grabb M.C., and Choi D.W. Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J Neurosci 19 (1999) 1657-1662
59. Graham S.H., and Chen J. Programmed cell death in cerebral ischemia. J Cereb Blood Flow Metab 21 (2001) 99-109
60. Gu Z., Jiang Q., and Zhang G. Extracellular signal-regulated kinase and c-Jun N-terminal protein kinase in ischemic tolerance. Neuroreport 12 (2001) 3487-3491
61. Halaby I.A., Takeda Y., Yufu K., et al. Depolarization thresholds for hippocampal damage, ischemic preconditioning, and changes in gene expression after global ischemia in the rat. Neurosci Lett 372 (2004) 12-16
62. Han H.S., and Yenari M.A. Cellular targets of brain inflammation in stroke. Curr Opin Investig Drugs 4 (2003) 522-529
63. Hara T., Hamada J., Yano S., et al. CREB is required for acquisition of ischemic tolerance in gerbil hippocampal CA1 region. J Neurochem 86 (2003) 805-814
64. Hayashi T., Saito A., Okuno S., et al. Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stress and prevents delayed neuronal cell death. J Cereb Blood Flow Metab 23 (2003) 949-961
65. Hayashi T., Saito A., Okuno S., et al. Oxidative damage to the endoplasmic reticulum is implicated in ischemic neuronal cell death. J Cereb Blood Flow Metab 23 (2003) 1117-1128
66. Hess D.T., Matsumoto A., Kim S.O., et al. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6 (2005) 150-166
67. + channels in cerebral ischemic preconditioning. Proc Natl Acad Sci USA 92 (1995) 4666-4670
68. Hiraide T., Katsura K., Muramatsu H., et al. Adenosine receptor antagonists cancelled the ischemic tolerance phenomenon in gerbil. Brain Res 910 (2001) 94-98
69. Horiguchi T., Snipes J.A., Kis B., et al. The role of nitric oxide in the development of cortical spreading depression-induced tolerance to transient focal cerebral ischemia in rats. Brain Res 1039 (2005) 84-89
70. Hu B.R., Martone M.E., Jones Y.Z., et al. Protein aggregation after transient cerebral ischemia. J Neurosci 20 (2000) 3191-3199
71. Huang P.L. Nitric oxide and cerebral ischemic preconditioning. Cell Calcium 36 (2004) 323-329
72. Ikeda Y., Hokamura K., Kawai T., et al. Neuroprotective effects of KCL-440, a new poly(ADP-ribose) polymerase inhibitor, in the rat middle cerebral artery occlusion model. Brain Res 1060 (2005) 73-80
73. Ito D., Tanaka K., Suzuki S., et al. Up-regulation of the Ire1-mediated signaling molecule, Bip, in ischemic rat brain. Neuroreport 12 (2001) 4023-4028
74. Jander S., Schroeter M., Peters O., et al. Cortical spreading depression induces proinflammatory cytokine gene expression in the rat brain. J Cereb Blood Flow Metab 21 (2001) 218-225
75. Janssen Y.M., Van Houten B., Borm P.J., et al. Cell and tissue responses to oxidative damage. Lab Invest 69 (1993) 261-274
76. Johnston S.C. Ischemic preconditioning from transient ischemic attacks. Data from the Northern California TIA Study. Stroke 35 (2004) 2680-2682
77. Jones N.M., and Bergeron M. Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J Cereb Blood Flow Metab 21 (2001) 1105-1114
78. Kapinya K., Penzel R., Sommer C., et al. Temporary changes of the AP-1 transcription factor binding activity in the gerbil hippocampus after transient global ischemia, and ischemic tolerance induction. Brain Res 872 (2000) 282-293
79. Kariko K., Weissman D., and Welsh F.A. Inhibition of toll-like receptor and cytokine signaling-a unifying theme in ischemic tolerance. J Cereb Blood Flow Metab 24 (2004) 1288-1304
80. Kato H., Liu Y., Araki T., et al. Temporal profile of the effects of pretreatment with brief cerebral ischemia on the neuronal damage following secondary ischemic insult in the gerbil: cumulative damage and protective effects. Brain Res 553 (1991) 238-242
81. Kato H., Kogure K., Araki T., et al. Graded expression of immunomolecules on activated microglia in the hippocampus following ischemia in a rat model of ischemic tolerance. Brain Res 694 (1995) 85-93
82. Kato H., Kogure K., Araki T., et al. Immunohistochemical localization of superoxide dismutase in the hippocampus following ischemia in a gerbil model of ischemic tolerance. J Cereb Blood Flow Metab 15 (1995) 60-70
83. Kato K., Shimazaki K., Kamiya T., et al. Differential effects of sublethal ischemia and chemical preconditioning with 3-nitropropionic acid on protein expression in gerbil hippocampus. Life Sci 77 (2005) 2867-2878
84. Kawahara N., Ide T., Saito N., et al. Propentofylline potentiates induced ischemic tolerance in gerbil hippocampal neurons via adenosine receptor. J Cereb Blood Flow Metab 18 (1998) 472-475
85. Kawahara N., Wang Y., Mukasa A., et al. Genome-wide gene expression analysis for induced ischemic tolerance and delayed neuronal death following transient global ischemia in rats. J Cereb Blood Flow Metab 24 (2004) 212-223
86. Khaspekov L., Shamloo M., Victorov I., et al. Sublethal in vitro glucose-oxygen deprivation protects cultured hippocampal neurons against a subsequent severe insult. Neuroreport 9 (1998) 1273-1276
87. Kim W.K., Choi Y.B., Rayudu P.V., et al. Attenuation of NMDA receptor activity and neurotoxicity by nitroxyl anion, NO. Neuron 24 (1999) 461-469
88. Kirino T. Ischemic tolerance. J Cereb Blood Flow Metab 22 (2002) 1283-1296
89. Kirino T., Tsujita Y., and Tamura A. Induced tolerance to ischemia in gerbil hippocampal neurons. J Cereb Blood Flow Metab 11 (1991) 299-307
90. Kis B., Rajapakse N.C., Snipes J.A., et al. Diazoxide induces delayed pre-conditioning in cultured rat cortical neurons. J Neurochem 87 (2003) 969-980
91. Kitagawa K., Matsumoto M., Tagaya M., et al. 'Ischemic tolerance' phenomenon found in the brain. Brain Res 528 (1990) 21-24
92. Kitagawa K., Matsumoto M., Kuwabara K., et al. 'Ischemic tolerance' phenomenon detected in various brain regions. Brain Res 561 (1991) 203-211
93. Kitagawa K., Matsumoto M., Matsushita K., et al. Ischemic tolerance in moderately symptomatic gerbils after unilateral carotid occlusion. Brain Res 716 (1996) 39-46
94. Kitano T., Nisimaru N., Shibata E., et al. Lactate utilization as an energy substrate in ischemic preconditioned rat brain slices. Life Sci 72 (2002) 557-564
95. Kobayashi S., Harris V.A., and Welsh F.A. Spreading depression induces tolerance of cortical neurons to ischemia in rat brain. J Cereb Blood Flow Metab 15 (1995) 721-727
96. Komjati K., Mabley J.G., Virag L., et al. Poly(ADP-ribose) polymerase inhibition protect neurons and the white matter and regulates the translocation of apoptosis-inducing factor in stroke. Int J Mol Med 13 (2004) 373-382
97. Krokan H.E., Nilsen H., Skorpen F., et al. Base excision repair of DNA in mammalian cells. FEBS Lett 476 (2000) 73-77
98. Kumar R., Krause G.S., Yoshida H., et al. Dysfunction of the unfolded protein response during global brain ischemia and reperfusion. J Cereb Blood Flow Metab 23 (2003) 462-471
99. Kurkinen K., Keinanen R., Li W., et al. Preconditioning with spreading depression activates specifically protein kinase Cδ. Neuroreport 12 (2001) 269-273
100. Kurkinen K., Busto R., Goldsteins G., et al. Isoform-specific membrane translocation of protein kinase C after ischemic preconditioning. Neurochem Res 26 (2001) 1139-1144
101. Lan J., Li W., Zhang F., et al. Inducible repair of oxidative DNA lesions in the rat brain after transient focal ischemia and reperfusion. J Cereb Blood Flow Metab 23 (2003) 1324-1339
102. Lange-Asschenfeldt C., Raval A.P., Dave K.R., et al. Epsilon protein kinase C mediated ischemic tolerance requires activation of the extracellular regulated kinase pathway in the organotypic hippocampal slice. J Cereb Blood Flow Metab 24 (2004) 636-645
103. Lee H.T., Chang Y.C., Wang L.Y., et al. cAMP response element-binding protein activation in ligation preconditioning in neonatal brain. Ann Neurol 56 (2004) 611-623
104. Li W., Luo Y., Zhang F., et al. Ischemic preconditioning in the rat brain enhances the repair of endogenous oxidative DNA damage by activating the base-excision repair pathway. J Cereb Blood Flow Metab 26 (2006) 181-198
105. Lin Y.F., Raab-Graham K., Jan Y.N., et al. NO stimulation of ATP-sensitive potassium channels: involvement of Ras/mitogen-activated protein kinase pathway and contribution to neuroprotection. Proc Natl Acad Sci USA 101 (2004) 7799-7804
106. Liou A.K., Clark R.S., Henshall D.C., et al. To die or not to die for neurons in ischemia, traumatic brain injury and epilepsy: a review on the stress-activated signaling pathways and apoptotic pathways. Prog Neurobiol 69 (2003) 103-142
107. Lipton S.A. Neuronal protection and destruction by NO. Cell Death Differ 6 (1999) 943-951
108. Liu C., Chen S., Kamme F., et al. Ischemic preconditioning prevents protein aggregation after transient cerebral ischemia. Neuroscience 134 (2005) 69-80
109. Liu J., Ginis I., Spatz M., et al. Hypoxic preconditioning protects cultured neurons against hypoxic stress via TNF-alpha and ceramide. Am J Physiol Cell Physiol 278 (2000) C144-C153
110. Liu J., Bartels M., Lu A., et al. Microglia/macrophages proliferate in striatum and neocortex but not in hippocampus after brief global ischemia that produces ischemic tolerance in gerbil brain. J Cereb Blood Flow Metab 21 (2001) 361-373
111. Liu P.K., Hsu C.Y., Dizdaroglu M., et al. Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia-reperfusion. J Neurosci 16 (1996) 6795-6806
112. Liu Y., Kato H., Nakata N., et al. Temporal profile of heat shock protein 70 synthesis in ischemic tolerance induced by preconditioning ischemia in rat hippocampus. Neuroscience 56 (1993) 921-927
113. Mabuchi T., Kitagawa K., Kuwabara K., et al. Phosphorylation of cAMP response element-binding protein in hippocampal neurons as a protective response after exposure to glutamate in vitro and ischemia in vivo. J Neurosci 21 (2001) 9204-9213
114. McLaughlin B., Hartnett K.A., Erhardt J.A., et al. Caspase 3 activation is essential for neuroprotection in preconditioning. Proc Natl Acad Sci USA 100 (2003) 715-720
115. Matsushima K., and Hakim A.M. Transient forebrain ischemia protects against subsequent focal cerebral ischemia without changing cerebral perfusion. Stroke 26 (1995) 1047-1052
116. Matsushima K., Hogan M.J., and Hakim A.M. Cortical spreading depression protects against subsequent focal cerebral ischemia in rats. J Cereb Blood Flow Metab 16 (1996) 221-226
117. Mattson M.P., and Meffert M.K. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 13 (2006) 852-860
118. Meller R., Minami M., Cameron J.A., et al. CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J Cereb Blood Flow Metab 25 (2005) 234-246
119. Meller R., Anastasia Cameron J., John Torrey D., et al. Rapid degradation of bim by the ubiquitin-proteasome pathway mediates short-term ischemic tolerance in cultured neurons. J Biol Chem 281 (2006) 7429-7436
120. Miao B., Yin X.H., Pei D.S., et al. Neuroprotective effects of preconditioning ischemia on ischemic brain injury through down-regulating activation of JNK1/2 via N-methyl-D-aspartate receptor-mediated Akt1 activation. J Biol Chem 280 (2005) 21693-21699
121. Mihara M., Erster S., Zaika A., et al. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11 (2003) 577-590
122. Miyashita K., Abe H., Nakajima T., et al. Induction of ischaemic tolerance in gerbil hippocampus by pretreatment with focal ischaemia. Neuroreport 6 (1994) 46-48
123. Mocanu M.M., and Yellon D.M. p53 down-regulation: a new molecular mechanism involved in ischaemic preconditioning. FEBS Lett 555 (2003) 302-306
124. Moncayo J., de Freitas G.R., Bogousslavsky J., et al. Do transient ischemic attacks have a neuroprotective effect?. Neurology 54 (2000) 2089-2094
125. Muramatsu H., Kariko K., and Welsh F.A. Induction of tolerance to focal ischemia in rat brain: dissociation between cortical lesioning and spreading depression. J Cereb Blood Flow Metab 24 (2004) 1167-1171
126. Nakagomi T., Kirino T., Kanemitsu H., et al. Early recovery of protein synthesis following ischemia in hippocampal neurons with induced tolerance in the gerbil. Acta Neuropathol (Berl) 86 (1993) 10-15
127. Nakajima T., Iwabuchi S., Miyazaki H., et al. Relationship between the activation of cyclic AMP responsive element binding protein and ischemic tolerance in the penumbra region of rat cerebral cortex. Neurosci Lett 331 (2002) 13-16
128. Nakajima T., Iwabuchi S., Miyazaki H., et al. Preconditioning prevents ischemia-induced neuronal death through persistent Akt activation in the penumbra region of the rat brain. J Vet Med Sci 66 (2004) 521-527
129. Nakamura M., Nakakimura K., Matsumoto M., et al. Rapid tolerance to focal cerebral ischemia in rats is attenuated by adenosine A1 receptor antagonist. J Cereb Blood Flow Metab 22 (2002) 161-170
130. Nakamura H., Katsumata T., Nishiyama Y., et al. Effect of ischemic preconditioning on cerebral blood flow after subsequent lethal ischemia in gerbils. Life Sci 78 (2005) 1713-1719
131. Nakano K., and Vousden K.H. PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7 (2001) 683-694
132. Nakata N., Kato H., and Kogure K. Inhibition of ischaemic tolerance in the gerbil hippocampus by quercetin and anti-heat shock protein-70 antibody. Neuroreport 4 (1993) 695-698
133. Nakatsuka H., Ohta S., Tanaka J., et al. Cytochrome c release from mitochondria to the cytosol was suppressed in the ischemia-tolerance-induced hippocampal CA1 region after 5-min forebrain ischemia in gerbils. Neurosci Lett 278 (2000) 53-56
134. Namura S., Zhu J., Fink K., et al. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 18 (1998) 3659-3668
135. Namura S., Nagata I., Kikuchi H., et al. Serine-threonine protein kinase Akt does not mediate ischemic tolerance after global ischemia in the gerbil. J Cereb Blood Flow Metab 20 (2000) 1301-1305
136. Nandagopal K., Dawson T.M., and Dawson V.L. Critical role for nitric oxide signaling in cardiac and neuronal ischemic preconditioning and tolerance. J Pharmacol Exp Ther 297 (2001) 474-478
137. Nawashiro H., Tasaki K., Ruetzler C.A., et al. TNF-alpha pretreatment induces protective effects against focal cerebral ischemia in mice. J Cereb Blood Flow Metab 17 (1997) 483-490
138. Naylor M., Bowen K.K., Sailor K.A., et al. Preconditioning-induced ischemic tolerance stimulates growth factor expression and neurogenesis in adult rat hippocampus. Neurochem Int 47 (2005) 565-572
139. Nishi S., Taki W., Uemura Y., et al. Ischemic tolerance due to the induction of HSP70 in a rat ischemic recirculation model. Brain Res 615 (1993) 281-288
140. Nishino K., and Nowak Jr. T.S. Time course and cellular distribution of hsp27 and hsp72 stress protein expression in a quantitative gerbil model of ischemic injury and tolerance: thresholds for hsp72 induction and hilar lesioning in the context of ischemic preconditioning. J Cereb Blood Flow Metab 24 (2004) 167-178
141. Nishio S., Chen Z.F., Yunoki M., et al. Hypothermia-induced ischemic tolerance. Ann N Y Acad Sci 890 (1999) 26-41
142. Nishio S., Yunoki M., Chen Z.F., et al. Ischemic tolerance in the rat neocortex following hypothermic preconditioning. J Neurosurg 93 (2000) 845-851
143. Nomura M., Shimizu S., Sugiyama T., et al. 14-3-3 interacts directly with and negatively regulates pro-apoptotic Bax. J Biol Chem 278 (2003) 2058-2065
144. Nowak Jr. T.S., Bond U., and Schlesinger M.J. Heat shock RNA levels in brain and other tissues after hyperthermia and transient ischemia. J Neurochem 54 (1990) 451-458
145. Oda E., Ohki R., Murasawa H., et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288 (2000) 1053-1058
146. Ohtsuki T., Matsumoto M., Kuwabara K., et al. Influence of oxidative stress on induced tolerance to ischemia in gerbil hippocampal neurons. Brain Res 599 (1992) 246-252
147. Ohtsuki T., Matsumoto M., Kitagawa K., et al. Induced resistance and susceptibility to cerebral ischemia in gerbil hippocampal neurons by prolonged but mild hypoperfusion. Brain Res 614 (1993) 279-284
148. Ohtsuki T., Ruetzler C.A., Tasaki K., et al. Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. J Cereb Blood Flow Metab 16 (1996) 1137-1142
149. Otori T., Greenberg J.H., and Welsh F.A. Cortical spreading depression causes a long-lasting decrease in cerebral blood flow and induces tolerance to permanent focal ischemia in rat brain. J Cereb Blood Flow Metab 23 (2003) 43-50
150. Otori T., Friedland J.C., Sinson G., et al. Traumatic brain injury elevates glycogen and induces tolerance to ischemia in rat brain. J Neurotrauma 21 (2004) 707-718
151. Pearson T., Currie A.J., Etherington L.A., et al. Plasticity of purine release during cerebral ischemia: clinical implications. J Cell Mol Med 7 (2003) 362-375
152. Pera J., Zawadzka M., Kaminska B., et al. Influence of chemical and ischemic preconditioning on cytokine expression after focal brain ischemia. J Neurosci Res 78 (2004) 132-140
153. Perez-Pinzon M.A. Neuroprotective effects of ischemic preconditioning in brain mitochondria following cerebral ischemia. J Bioenerg Biomembr 36 (2004) 323-327
154. Perez-Pinzon M.A., Xu G.P., Dietrich W.D., et al. Rapid preconditioning protects rats against ischemic neuronal damage after 3 but not 7 days of reperfusion following global cerebral ischemia. J Cereb Blood Flow Metab 17 (1997) 175-182
155. Perez-Pinzon M.A., Vitro T.M., Dietrich W.D., et al. The effect of rapid preconditioning on the microglial, astrocytic and neuronal consequences of global cerebral ischemia. Acta Neuropathol (Berl) 97 (1999) 495-501
156. Perez-Pinzon M.A., Basit A., Dave K.R., et al. Effect of the first window of ischemic preconditioning on mitochondrial dysfunction following global cerebral ischemia. Mitochondrion 2 (2002) 181-189
157. Perez-Pinzon M.A., Dave K.R., and Raval A.P. Role of reactive oxygen species and protein kinase C in ischemic tolerance in the brain. Antioxid Redox Signal 7 (2005) 1150-1157
158. ATP channels. J Cereb Blood Flow Metab 19 (1999) 1296-1308
159. Plesnila N., Zinkel S., Le D.A., et al. BID mediates neuronal cell death after oxygen/glucose deprivation and focal cerebral ischemia. Proc Natl Acad Sci USA 98 (2001) 15318-15323
160. Prass K., Scharff A., Ruscher K., et al. Hypoxia-induced stroke tolerance in the mouse is mediated by erythropoietin. Stroke 34 (2003) 1981-1986
161. Pugazhenthi S., Nesterova A., Sable C., et al. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem 275 (2000) 10761-10766
162. Pugliese A.M., Latini S., Corradetti R., et al. Brief, repeated, oxygen-glucose deprivation episodes protect neurotransmission from a longer ischemic episode in the in vitro hippocampus: role of adenosine receptors. Br J Pharmacol 140 (2003) 305-314
163. Puisieux F., Deplanque D., Pu Q., et al. Differential role of nitric oxide pathway and heat shock protein in preconditioning and lipopolysaccharide-induced brain ischemic tolerance. Eur J Pharmacol 389 (2000) 71-78
164. Puisieux F., Deplanque D., Bulckaen H., et al. Brain ischemic preconditioning is abolished by antioxidant drugs but does not up-regulate superoxide dismutase and glutathione peroxidase. Brain Res 1027 (2004) 30-37
165. Romera C., Hurtado O., Botella S.H., et al. In vitro ischemic tolerance involves upregulation of glutamate transport partly mediated by the TACE/ADAM17-tumor necrosis factor-alpha pathway. J Neurosci 24 (2004) 1350-1357
166. Rosenzweig H.L., Lessov N.S., Henshall D.C., et al. Endotoxin preconditioning prevents cellular inflammatory response during ischemic neuroprotection in mice. Stroke 35 (2004) 2576-2581
167. Ruscher K., Freyer D., Karsch M., et al. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22 (2002) 10291-10301
168. Rutkowski D.T., and Kaufman R.J. A trip to the ER: coping with stress. Trends Cell Biol 14 (2004) 20-28
169. Schaller B. Ischemic preconditioning as induction of ischemic tolerance after transient ischemic attacks in human brain: its clinical relevance. Neurosci Lett 377 (2005) 206-211
170. Scheller D., Kolb J., and Tegtmeier F. Lactate and pH change in close correlation in the extracellular space of the rat brain during cortical spreading depression. Neurosci Lett 135 (1992) 83-86
171. Schurr A., Payne R.S., Tseng M.T., et al. Excitotoxic preconditioning elicited by both glutamate and hypoxia and abolished by lactate transport inhibition in rat hippocampal slices. Neurosci Lett 307 (2001) 151-154
172. Semenza G.L. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 7 (2001) 345-350
173. Shaulian E., and Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol 4 (2002) E131-E136
174. Shi Y. Caspase activation, inhibition, and reactivation: a mechanistic view. Protein Sci 13 (2004) 1979-1987
175. Shimizu S., Nagayama T., Jin K.L., et al. bcl-2 antisense treatment prevents induction of tolerance to focal ischemia in the rat brain. J Cereb Blood Flow Metab 21 (2001) 233-243
176. Simon R.P., Niiro M., and Gwinn R. Prior ischemic stress protects against experimental stroke. Neurosci Lett 163 (1993) 135-137
177. Skaper S.D. Poly(ADP-Ribose) polymerase-1 in acute neuronal death and inflammation: a strategy for neuroprotection. Ann N Y Acad Sci 993 (2003) 217-228
178. Sorimachi T., and Nowak Jr. T.S. Pharmacological manipulations of ATP-dependent potassium channels and adenosine A1 receptors do not impact hippocampal ischemic preconditioning in vivo: evidence in a highly quantitative gerbil model. J Cereb Blood Flow Metab 24 (2004) 556-563
179. Stagliano N.E., Perez-Pinzon M.A., Moskowitz M.A., et al. Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 19 (1999) 757-761
180. Stenzel-Poore M.P., Stevens S.L., Xiong Z., et al. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362 (2003) 1028-1037
181. Stenzel-Poore M.P., Stevens S.L., and Simon R.P. Genomics of preconditioning. Stroke 35 (2004) 2683-2686
182. Stroev S.A., Gluschenko T.S., Tjulkova E.I., et al. Preconditioning enhances the expression of mitochondrial antioxidant thioredoxin-2 in the forebrain of rats exposed to severe hypobaric hypoxia. J Neurosci Res 78 (2004) 563-569
183. Sugawara T., Noshita N., Lewen A., et al. Neuronal expression of the DNA repair protein Ku 70 after ischemic preconditioning corresponds to tolerance to global cerebral ischemia. Stroke 32 (2001) 2388-2393
184. Sugino T., Nozaki K., and Hashimoto N. Activation of mitogen-activated protein kinases in gerbil hippocampus with ischemic tolerance induced by 3-nitropropionic acid. Neurosci Lett 278 (2000) 101-104
185. Tajiri S., Oyadomari S., Yano S., et al. Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ 11 (2004) 403-415
186. Takahata Y., and Shimoji K. Brain injury improves survival of mice following brain ischemia. Brain Res 381 (1986) 368-371
187. Tanaka H., Yokota H., Jover T., et al. Ischemic preconditioning: neuronal survival in the face of caspase-3 activation. J Neurosci 24 (2004) 2750-2759
188. Tang Y., Pacary E., Freret T., et al. Effect of hypoxic preconditioning on brain genomic response before and following ischemia in the adult mouse: identification of potential neuroprotective candidates for stroke. Neurobiol Dis 21 (2006) 18-28
189. Tenneti L., D'Emilia D.M., and Lipton S.A. Suppression of neuronal apoptosis by S-nitrosylation of caspases. Neurosci Lett 236 (1997) 139-142
190. Tomai F., Crea F., Chiariello L., et al. Ischemic preconditioning in humans: models, mediators, and clinical relevance. Circulation 100 (1999) 559-563
191. WAF1/Cip1 and PAG608/Wig-1 in ischemic preconditioning. Brain Res Mol Brain Res 70 (1999) 304-313
192. Toyoda T., and Lee K.S. Differential induction of superoxide dismutase in core and penumbra regions after transient focal ischemia in the rat neocortex. Neurosci Lett 235 (1997) 29-32
193. Toyoda T., Kassell N.F., and Lee K.S. Induction of tolerance against ischemia/reperfusion injury in the rat brain by preconditioning with the endotoxin analog diphosphoryl lipid A. J Neurosurg 92 (2000) 435-441
194. Traystman R.J. Animal models of focal and global cerebral ischemia. ILAR J 44 (2003) 85-95
195. Truettner J., Busto R., Zhao W., et al. Effect of ischemic preconditioning on the expression of putative neuroprotective genes in the rat brain. Brain Res Mol Brain Res 103 (2002) 106-115
196. Ueda M., and Nowak Jr. T.S. Protective preconditioning by transient global ischemia in the rat: components of delayed injury progression and lasting protection distinguished by comparisons of depolarization thresholds for cell loss at long survival times. J Cereb Blood Flow Metab 25 (2005) 949-958
197. Valentim L.M., Geyer A.B., Tavares A., et al. Effects of global cerebral ischemia and preconditioning on heat shock protein 27 immunocontent and phosphorylation in rat hippocampus. Neuroscience 107 (2001) 43-49
198. Valentim L.M., Rodnight R., Geyer A.B., et al. Changes in heat shock protein 27 phosphorylation and immunocontent in response to preconditioning to oxygen and glucose deprivation in organotypic hippocampal cultures. Neuroscience 118 (2003) 379-386
199. Vannucci R.C., Towfighi J., and Vannucci S.J. Hypoxic preconditioning and hypoxic-ischemic brain damage in the immature rat: pathologic and metabolic correlates. J Neurochem 71 (1998) 1215-1220
200. Von Lubitz D.K., Lin R.C., Melman N., et al. Chronic administration of selective adenosine A1 receptor agonist or antagonist in cerebral ischemia. Eur J Pharmacol 256 (1994) 161-167
201. Walton M.R., and Dragunow I. Is CREB a key to neuronal survival. Trends Neurosci 23 (2000) 8-53
202. Wang G.J., Deng H.Y., Maier C.M., et al. Mild hypothermia reduces ICAM-1 expression, neutrophil infiltration and microglia/monocyte accumulation following experimental stroke. Neuroscience 114 (2002) 1081-1090
203. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284 (1999) 339-343
204. Wang X., Deng J., Boyle D.W., et al. Potential role of IGF-I in hypoxia tolerance using a rat hypoxic-ischemic model: activation of hypoxia-inducible factor 1α. Pediatr Res 55 (2004) 385-394
205. Warner D.S., Sheng H., and Batinic-Haberle I. Oxidants, antioxidants and the ischemic brain. J Exp Biol 207 (2004) 3221-3231
206. Wegener S., Gottschalk B., Jovanovic V., et al. Transient ischemic attacks before ischemic stroke: preconditioning the human brain? A multicenter magnetic resonance imaging study. Stroke 35 (2004) 616-621
207. Weih M., Kallenberg K., Bergk A., et al. Attenuated stroke severity after prodromal TIA: a role for ischemic tolerance in the brain. Stroke 30 (1999) 1851-1854
208. Wiegand F., Liao W., Busch C., et al. Respiratory chain inhibition induces tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 19 (1999) 1229-1237
209. Wu C., Fujihara H., Yao J., et al. Different expression patterns of Bcl-2, Bcl-xl, and Bax proteins after sublethal forebrain ischemia in C57Black/Crj6 mouse striatum. Stroke 34 (2003) 1803-1808
210. Yamada K., and Inagaki N. Neuroprotection by KATP channels. J Mol Cell Cardiol 38 (2005) 945-949
211. Yellon D.M., and Dana A. The preconditioning phenomenon: a tool for the scientist or a clinical reality. Circ Res 87 (2000) 543-550
212. Yin X.M., Luo Y., Cao G., et al. Bid-mediated mitochondrial pathway is critical to ischemic neuronal apoptosis and focal cerebral ischemia. J Biol Chem 277 (2002) 42074-42081
213. 1 receptor antagonist and mitochondrial ATP-sensitive potassium channel blocker attenuate the tolerance to focal cerebral ischemia in rats. J Cereb Blood Flow Metab 24 (2004) 771-779
214. Yu S.W., Wang H., Dawson T.M., et al. Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol Dis 14 (2003) 303-317
215. Yunoki M., Nishio S., Ukita N., et al. Characteristics of hypothermic preconditioning influencing the induction of delayed ischemic tolerance. J Neurosurg 97 (2002) 650-657
216. Zhang F., Yin W., and Chen J. Apoptosis in cerebral ischemia: executional and regulatory signaling mechanisms. Neurol Res 26 (2004) 835-845
217. Zhang Y., Zhang X., Park T.S., et al. Cerebral endothelial cell apoptosis after ischemia-reperfusion: role of PARP activation and AIF translocation. J Cereb Blood Flow Metab 25 (2005) 868-877
218. Zhao L., and Nowak T.S. CBF changes associated with focal ischemic preconditioning in the spontaneously hypertensive rat. J Cereb Blood Flow Metab 26 (2006) 1128-1140
219. Zimmermann C., Ginis I., Furuya K., et al. Lipopolysaccharide-induced ischemic tolerance is associated with increased levels of ceramide in brain and in plasma. Brain Res 895 (2001) 59-65