Abstract
Preconditioning (PC) describes a phenomenon whereby a sub-injury-inducing stress can protect against a later injurious stress. Great strides have been made in identifying the mechanisms of PC-induced protection in animal models of brain injury. While these may help elucidate potential therapeutic targets, there are questions over the clinical utility of cerebral PC, primarily because of questions over the need to give the PC stimulus prior to the injury, narrow therapeutic windows, and safety. The object of this review is to address the question of whether there may indeed be a clinical use for cerebral PC and to discuss the deficiencies in our knowledge of PC that may hamper such clinical translation.
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References
Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74(5):1124–1136
Yoshizumi T, Yanaga K, Soejima Y, Maeda T, Uchiyama H, Sugimachi K (1998) Amelioration of liver injury by ischaemic preconditioning. Br J Surg 85(12):1636–1640
Bonventre JV (2002) Kidney ischemic preconditioning. Curr Opin Nephrol Hypertens 11(1):43–48
Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M et al (1990) ‘Ischemic tolerance’ phenomenon found in the brain. Brain Res 528(1):21–24
Kirino T, Nakagomi T, Kanemitsu H, Tamura A (1996) Ischemic tolerance. Adv Neurol 71:505–511
Gidday JM (2006) Cerebral preconditioning and ischaemic tolerance. Nat Rev, Neurosci 7(6):437–448
Obrenovitch TP (2008) Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol Rev 88(1):211–247
Dirnagl U, Becker K, Meisel A (2009) Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 8(4):398–412
Steiger HJ, Hanggi D (2007) Ischaemic preconditioning of the brain, mechanisms and applications. Acta Neurochir 149(1):1–10
Hausenloy DJ, Yellon DM (2009) Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis 204(2):334–341
Zhao H (2009) Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J Cereb Blood Flow Metab 29(5):873–885
Mack WJ, Kellner CP, Sahlein DH, Ducruet AF, Kim GH, Mocco J et al (2009) Intraoperative magnesium infusion during carotid endarterectomy: a double-blind placebo-controlled trial. J Neurosurg 110(5):961–967
Sacco RL, Adams R, Albers G, Alberts MJ, Benavente O, Furie K et al (2006) Guidelines for prevention of stroke in patients with ischemic stroke or transient ischemic attack: a statement for healthcare professionals from the American Heart Association/American Stroke Association Council on Stroke: co-sponsored by the Council on Cardiovascular Radiology and Intervention: the American Academy of Neurology affirms the value of this guideline.[see comment]. Stroke 37(2):577–617
Amarenco P, Bogousslavsky J, Callahan A 3rd, Goldstein LB, Hennerici M, Rudolph AE et al (2006) High-dose atorvastatin after stroke or transient ischemic attack [see comment]. N Engl J Med 355(6):549–559
Weih M, Kallenberg K, Bergk A, Dirnagl U, Harms L, Wernecke KD et al (1999) Attenuated stroke severity after prodromal TIA: a role for ischemic tolerance in the brain? [see comment]. Stroke 30(9):1851–1854
Moncayo J, de Freitas GR, Bogousslavsky J, Altieri M, van Melle G (2000) Do transient ischemic attacks have a neuroprotective effect? [see comment]. Neurology 54(11):2089–2094
Wegener S, Gottschalk B, Jovanovic V, Knab R, Fiebach JB, Schellinger PD et al (2004) Transient ischemic attacks before ischemic stroke: preconditioning the human brain? A multicenter magnetic resonance imaging study. Stroke 35(3):616–621
Jiang X, Zhu D, Okagaki P, Lipsky R, Wu X, Banaudha K et al (2003) N-methyl-D-aspartate and TrkB receptor activation in cerebellar granule cells: an in vitro model of preconditioning to stimulate intrinsic survival pathways in neurons. Ann N Y Acad Sci 993:134–145, discussion 59–60
Lin JH, Lou N, Kang N, Takano T, Hu F, Han X et al (2008) A central role of connexin 43 in hypoxic preconditioning. J Neurosci 28(3):681–695
Andjelkovic AV, Stamatovic SM, Keep RF (2003) The protective effects of preconditioning on cerebral endothelial cells in vitro. J Cereb Blood Flow Metab 23(11):1348–1355
Kapinya KJ, Lowl D, Futterer C, Maurer M, Waschke KF, Isaev NK et al (2002) Tolerance against ischemic neuronal injury can be induced by volatile anesthetics and is inducible NO synthase dependent. Stroke 33(7):1889–1898
Mayanagi K, Gaspar T, Katakam PV, Busija DW (2007) Systemic administration of diazoxide induces delayed preconditioning against transient focal cerebral ischemia in rats. Brain Res 1168:106–111
Bickler PE, Zhan X, Fahlman CS (2005) Isoflurane preconditions hippocampal neurons against oxygen-glucose deprivation: role of intracellular Ca2+ and mitogen-activated protein kinase signaling. Anesthesiology 103(3):532–539
Kis B, Rajapakse NC, Snipes JA, Nagy K, Horiguchi T, Busija DW (2003) Diazoxide induces delayed pre-conditioning in cultured rat cortical neurons. J Neurochem 87(4):969–980
Matchett GA, Martin RD, Zhang JH (2009) Hyperbaric oxygen therapy and cerebral ischemia: neuroprotective mechanisms. Neurol Res 31(2):114–121
Bigdeli MR, Khoshbaten A (2008) In vivo preconditioning with normobaric hyperoxia induces ischemic tolerance partly by triggering tumor necrosis factor-alpha converting enzyme/tumor necrosis factor-alpha/nuclear factor-kappaB. Neuroscience 153(3):671–678
Nishio S, Yunoki M, Chen ZF, Anzivino MJ, Lee KS (2000) Ischemic tolerance in the rat neocortex following hypothermic preconditioning. J Neurosurg 93(5):845–851
Xu H, Aibiki M, Nagoya J (2002) Neuroprotective effects of hyperthermic preconditioning on infarcted volume after middle cerebral artery occlusion in rats: role of adenosine receptors. Crit Care Med 30(5):1126–1130
Muramatsu H, Kariko K, Welsh FA (2004) Induction of tolerance to focal ischemia in rat brain: dissociation between cortical lesioning and spreading depression. J Cereb Blood Flow Metab 24(10):1167–1171
Horiguchi T, Snipes JA, Kis B, Shimizu K, Busija DW (2006) Cyclooxygenase-2 mediates the development of cortical spreading depression-induced tolerance to transient focal cerebral ischemia in rats. Neuroscience 140(2):723–730
Wang Q, Xiong L, Chen S, Liu Y, Zhu X (2005) Rapid tolerance to focal cerebral ischemia in rats is induced by preconditioning with electroacupuncture: window of protection and the role of adenosine. Neurosci Lett 381(1–2):158–162
Xiong LZ, Yang J, Wang Q, Lu ZH (2007) Involvement of delta-and mu-opioid receptors in the delayed cerebral ischemic tolerance induced by repeated electroacupuncture preconditioning in rats. Chin Med J 120(5):394–399
Ding YH, Young CN, Luan X, Li J, Rafols JA, Clark JC et al (2005) Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol 109(3):237–246
Blanck TJ, Haile M, Xu F, Zhang J, Heerdt P, Veselis RA et al (2000) Isoflurane pretreatment ameliorates postischemic neurologic dysfunction and preserves hippocampal Ca2+/calmodulin-dependent protein kinase in a canine cardiac arrest model. Anesthesiology 93(5):1285–1293
Kanoria S, Jalan R, Seifalian AM, Williams R, Davidson BR (2007) Protocols and mechanisms for remote ischemic preconditioning: a novel method for reducing ischemia reperfusion injury. Transplantation 84(4):445–458
Walsh SR, Tang T, Sadat U, Dutka DP, Gaunt ME (2007) Cardioprotection by remote ischaemic preconditioning [see comment]. Br J Anaesth 99(5):611–616
Hausenloy DJ, Yellon DM (2008) Remote ischaemic preconditioning: underlying mechanisms and clinical application. Cardiovasc Res 79(3):377–386
Ren C, Gao X, Steinberg GK, Zhao H (2008) Limb remote-preconditioning protects against focal ischemia in rats and contradicts the dogma of therapeutic time windows for preconditioning. Neuroscience 151(4):1099–1103
He Z, Crook JE, Meschia JF, Brott TG, Dickson DW, McKinney M (2005) Aging blunts ischemic-preconditioning-induced neuroprotection following transient global ischemia in rats. Current Neurovascular Research 2(5):365–374
Purcell JE, Lenhard SC, White RF, Schaeffer T, Barone FC, Chandra S (2003) Strain-dependent response to cerebral ischemic preconditioning: differences between spontaneously hypertensive and stroke prone spontaneously hypertensive rats. Neurosci Lett 339(2):151–155
Wang WZ, Jones S, Stepheson LL, Khiabani KT, Zamboni WA (2002) Microvascular protection induced by late preconditioning was abolished in STZ-induced acute diabetic rats. J Reconstr Microsurg 18(8):689–696
Kim SH, Kim EH, Lee BI, Heo JH (2008) Chronic cerebral hypoperfusion protects against focal ischemia, improves motor function, and results in vascular remodeling. Current Neurovascular Research 5:28–56
Petcu EB, Kocher T, Kuhr A, Buga AM, Kloting I, Herndon JG et al (2008) Mild systemic inflammation has a neuroprotective effect after stroke in rats. Current Neurovascular Research 5(4):214–223
Kitano H, Young JM, Cheng J, Wang L, Hurn PD, Murphy SJ (2007) Gender-specific response to isoflurane preconditioning in focal cerebral ischemia. J Cereb Blood Flow Metab 27(7):1377–1386
Kasischke K, Huber R, Li H, Timmler M, Riepe MW (1999) Primary hypoxic tolerance and chemical preconditioning during estrus cycle in mice. Stroke 30(6):1256–1262
Chan MT, Boet R, Ng SC, Poon WS, Gin T (2005) Effect of ischemic preconditioning on brain tissue gases and pH during temporary cerebral artery occlusion. Acta Neurochir Suppl 95:93–96
Johnston SC (2004) Ischemic preconditioning from transient ischemic attacks? Data from the Northern California TIA Study. Stroke 35(11 Suppl 1):2680–2682
Della Morte D, Abete P, Gallucci F, Scaglione A, D'Ambrosio D, Gargiulo G et al (2008) Transient ischemic attack before nonlacunar ischemic stroke in the elderly. J Stroke Cerebrovasc Dis 17(5):257–262
Yellon DM, Alkhulaifi AM, Pugsley WB (1993) Preconditioning the human myocardium. Lancet 342(8866):276–277
Walsh SR, Tang TY, Kullar P, Jenkins DP, Dutka DP, Gaunt ME (2008) Ischaemic preconditioning during cardiac surgery: systematic review and meta-analysis of perioperative outcomes in randomised clinical trials. Eur J Cardiothorac Surg 34(5):985–994
Yu CH, Beattie WS (2006) The effects of volatile anesthetics on cardiac ischemic complications and mortality in CABG: a meta-analysis [see comment]. Can J Anaesth 53(9):906–918
Symons JA, Myles PS (2006) Myocardial protection with volatile anaesthetic agents during coronary artery bypass surgery: a meta-analysis [see comment]. Br J Anaesth 97(2):127–136
Takagi H, Manabe H, Kawai N, Goto SN, Umemoto T (2008) Review and meta-analysis of randomized controlled clinical trials of remote ischemic preconditioning in cardiovascular surgery. Am J Cardiol 102(11):1487–1488
Plamondon H, Blondeau N, Heurteaux C, Lazdunski M (1999) Mutually protective actions of kainic acid epileptic preconditioning and sublethal global ischemia on hippocampal neuronal death: involvement of adenosine A1 receptors and K(ATP) channels. J Cereb Blood Flow Metab 19(12):1296–1308
Simon R, Henshall D, Stoehr S, Meller R (2007) Endogenous mechanisms of neuroprotection [erratum appears in Epilepsia. 2007 Dec;48(12):2384]. Epilepsia 48(Suppl 8):72–73
Dirnagl U, Simon RP, Hallenbeck JM (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26(5):248–254
Perez-Pinzon MA, Alonso O, Kraydieh S, Dietrich WD (1999) Induction of tolerance against traumatic brain injury by ischemic preconditioning. NeuroReport 10(14):2951–2954
Shein NA, Horowitz M, Shohami E (2007) Heat acclimation: a unique model of physiologically mediated global preconditioning against traumatic brain injury. Prog Brain Res 161:353–363
Yellon DM, Downey JM (2003) Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83(4):1113–1151
Kleindorfer D, Panagos P, Pancioli A, Khoury J, Kissela B, Woo D et al (2005) Incidence and short-term prognosis of transient ischemic attack in a population-based study. Stroke 36(4):720–723
Johnston SC, Gress DR, Browner WS, Sidney S (2000) Short-term prognosis after emergency department diagnosis of TIA. JAMA 284(22):2901–2906
Lovett JK, Dennis MS, Sandercock PA, Bamford J, Warlow CP, Rothwell PM (2003) Very early risk of stroke after a first transient ischemic attack. Stroke 34(8):e138–e140
Coull AJ, Lovett JK, Rothwell PM (2004) Population based study of early risk of stroke after transient ischaemic attack or minor stroke: implications for public education and organisation of services. BMJ 328(7435):326
Lisabeth LD, Ireland JK, Risser JM, Brown DL, Smith MA, Garcia NM et al (2004) Stroke risk after transient ischemic attack in a population-based setting. Stroke 35(8):1842–1846
Chandratheva A, Mehta Z, Geraghty OC, Marquardt L, Rothwell PM (2009) Population-based study of risk and predictors of stroke in the first few hours after a TIA. Neurology 72(22):1941–1947
LaManna JC, Chavez JC, Pichiule P (2004) Structural and functional adaptation to hypoxia in the rat brain. J Exp Biol 207(Pt 18):3163–3169
Raval AP, Lin HW, Dave KR, Defazio RA, Della Morte D, Kim EJ et al (2008) Resveratrol and ischemic preconditioning in the brain. Curr Med Chem 15(15):1545–1551
Zhao J, Moore AN, Redell JB, Dash PK (2007) Enhancing expression of Nrf2-driven genes protects the blood brain barrier after brain injury. J Neurosci 27(38):10240–10248
Haljan G, Maitland A, Buchan A, Arora RC, King M, Haigh J et al (2009) The erythropoietin neuroprotective effect: assessment in CABG surgery (TENPEAKS): a randomized, double-blind, placebo controlled, proof-of-concept clinical trial. Stroke 40(8):2769–2775
Dawson TM (2002) Preconditioning-mediated neuroprotection through erythropoietin? [erratum appears in Lancet 2002 May 18;359(9319):1782]. Lancet 359(9301):96–97
Malhotra S, Savitz SI, Ocava L, Rosenbaum DM (2006) Ischemic preconditioning is mediated by erythropoietin through PI-3 kinase signaling in an animal model of transient ischemic attack. J Neurosci Res 83(1):19–27
Dendorfer A, Heidbreder M, Hellwig-Burgel T, Johren O, Qadri F, Dominiak P (2005) Deferoxamine induces prolonged cardiac preconditioning via accumulation of oxygen radicals. Free Radic Biol Med 38(1):117–124
Zhu Y, Zhang L, Gidday JM (2008) Deferroxamine preconditioning promotes long-lasting retinal ischemic tolerance. J Ocular Pharmacol Ther 24(6):527–535
Jones NM, Kardashyan L, Callaway JK, Lee EM, Beart PM (2008) Long-term functional and protective actions of preconditioning with hypoxia, cobalt chloride, and desferrioxamine against hypoxic-ischemic injury in neonatal rats. Pediatr Res 63(6):620–624
Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2004) Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J Neurosurg 100(4):672–678
Gu Y, Hua Y, Keep RF, Morgenstern LB, Xi G (2009) Deferoxamine reduces intracerebral hematoma-induced iron accumulation and neuronal death in piglets. Stroke 40(6):2241–2243
Freret T, Valable S, Chazalviel L, Saulnier R, Mackenzie ET, Petit E et al (2006) Delayed administration of deferoxamine reduces brain damage and promotes functional recovery after transient focal cerebral ischemia in the rat. Eur J NeuroSci 23(7):1757–1765
Hoshi A, Nakahara T, Ogata M, Yamamoto T (2005) The critical threshold of 3-nitropropionic acid-induced ischemic tolerance in the rat. Brain Res 1050(1–2):33–39
Coyle P, Jokelainen PT (1983) Differential outcome to middle cerebral artery occlusion in spontaneously hypertensive stroke-prone rats (SHRSP) and Wistar Kyoto (WKY) rats. Stroke 14:605–611
Hua Y, Wu J, Pecina S, Yang S, Schallert T, Keep RF et al (2005) Ischemic preconditioning procedure induces behavioral deficits in the absence of brain injury? Neurol Res 27(3):261–267
Komotar RJ, Zacharia BE, Mocco J, Connolly ES Jr (2008) Controversies in the surgical treatment of ruptured intracranial aneurysms: the First Annual J. Lawrence Pool Memorial Research Symposium—controversies in the management of cerebral aneurysms. Neurosurgery 62(2):396–407, discussion 5-7
Woertgen C, Rothoerl RD, Albert R, Schebesch KM, Ullrich OW (2008) Effects of temporary clipping during aneurysm surgery. Neurol Res 30(5):542–546
Newman MF, Kirchner JL, Phillips-Bute B, Gaver V, Grocott H, Jones RH et al (2001) Longitudinal assessment of neurocognitive function after coronary-artery bypass surgery [see comment][erratum appears in N Engl J Med 2001 Jun 14;344(24):1876]. N Engl J Med 344(6):395–402
van Dijk D, Keizer AM, Diephuis JC, Durand C, Vos LJ, Hijman R (2000) Neurocognitive dysfunction after coronary artery bypass surgery: a systematic review [see comment]. J Thorac Cardiovasc Surg 120(4):632–639
Keizer AM, Hijman R, Kalkman CJ, Kahn RS, van Dijk D (2005) Octopus Study G. The incidence of cognitive decline after (not) undergoing coronary artery bypass grafting: the impact of a controlled definition. Acta Anaesthesiol Scand 49(9):1232–1235
Heyer EJ, Adams DC, Solomon RA, Todd GJ, Quest DO, McMahon DJ et al (1998) Neuropsychometric changes in patients after carotid endarterectomy. Stroke 29(6):1110–1115
Heyer EJ, Sharma R, Rampersad A, Winfree CJ, Mack WJ, Solomon RA et al (2002) A controlled prospective study of neuropsychological dysfunction following carotid endarterectomy. Arch Neurol 59(2):217–222
Mayberg MR, Batjer HH, Dacey R, Diringer M, Haley EC, Heros RC et al (1994) Guidelines for the management of aneurysmal subarachnoid hemorrhage. A statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 25(11):2315–2328
Hua Y, Wu J, Keep RF, Hoff JT, Xi G (2003) Thrombin exacerbates brain edema in focal cerebral ischemia. Acta Neurochir Suppl 86:163–166
Weststrate W, Hijdra A, de Gans J (1996) Brain infarcts in adults with bacterial meningitis. Lancet 347(8998):399
Kastenbauer S, Pfister HW (2003) Pneumococcal meningitis in adults: spectrum of complications and prognostic factors in a series of 87 cases. Brain 126(Pt 5):1015–1025
Levi M, van der Poll T (2005) Two-way interactions between inflammation and coagulation. Trends Cardiovasc Med 15(7):254–259
de Souza AL, Seguro AC (2008) Two centuries of meningococcal infection: from Vieusseux to the cellular and molecular basis of disease. J Med Microbiol 57(Pt 11):1313–1321
Bowen KK, Naylor M, Vemuganti R (2006) Prevention of inflammation is a mechanism of preconditioning-induced neuroprotection against focal cerebral ischemia. Neurochem Int 49(2):127–135
Jacobson DL, Gange SJ, Rose NR, Graham NM (1997) Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol 84(3):223–243
Keegan BM, Noseworthy JH (2002) Multiple sclerosis. Annu Rev Med 53:285–302
Panitch HS (1994) Influence of infection on exacerbations of multiple sclerosis. Ann Neurol 36(Suppl):S25–S28
de Borst GJ, Moll FL, van de Pavoordt HD, Mauser HW, Kelder JC, Ackerstaf RG (2001) Stroke from carotid endarterectomy: when and how to reduce perioperative stroke rate? Eur J Vasc Endovasc Surg 21(6):484–489
Pinkerton JA Jr (2002) EEG as a criterion for shunt need in carotid endarterectomy. Ann Vasc Surg 16(6):756–761
Pera J, Zawadzka M, Kaminska B, Szczudlik A (2004) Influence of chemical and ischemic preconditioning on cytokine expression after focal brain ischemia. J Neurosci Res 78(1):132–140
Puisieux F, Deplanque D, Pu Q, Souil E, Bastide M, Bordet R (2000) Differential role of nitric oxide pathway and heat shock protein in preconditioning and lipopolysaccharide-induced brain ischemic tolerance. Eur J Pharmacol 389(1):71–78
Zimmermann C, Ginis I, Furuya K, Klimanis D, Ruetzler C, Spatz M et al (2001) Lipopolysaccharide-induced ischemic tolerance is associated with increased levels of ceramide in brain and in plasma. Brain Res 895(1–2):59–65
Furuya K, Ginis I, Takeda H, Chen Y, Hallenbeck JM (2001) 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(3):226–232
Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI et al (2009) Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 40(6):2244–2250
Wang L, Traystman RJ, Murphy SJ (2008) Inhalational anesthetics as preconditioning agents in ischemic brain. Curr Opin Pharmacol 8(1):104–110
Xi G, Keep RF, Hua Y, Xiang J, Hoff JT (1999) Attenuation of thrombin-induced brain edema by cerebral thrombin preconditioning. Stroke 30(6):1247–1255
Masada T, Xi G, Hua Y, Keep RF (2000) The effects of thrombin preconditioning on focal cerebral ischemia in rats. Brain Res 867(1–2):173–179
Hua Y, Keep RF, Hoff JT, Xi G (2003) Thrombin preconditioning attenuates brain edema induced by erythrocytes and iron. J Cereb Blood Flow Metab 23(12):1448–1454
Saleh MC, Connell BJ, Saleh TM (2009) Ischemic tolerance following low dose NMDA involves modulation of cellular stress proteins. Brain Res 1247:212–220
Samson D, Batjer HH, Bowman G, Mootz L, Krippner WJ Jr, Meyer YJ et al (1994) A clinical study of the parameters and effects of temporary arterial occlusion in the management of intracranial aneurysms. Neurosurgery 34(1):22–28, discussion 8-9
Lavine SD, Masri LS, Levy ML, Giannotta SL (1997) Temporary occlusion of the middle cerebral artery in intracranial aneurysm surgery: time limitation and advantage of brain protection. J Neurosurg 87(6):817–824
Tapuria N, Kumar Y, Habib MM, Abu Amara M, Seifalian AM, Davidson BR (2008) Remote ischemic preconditioning: a novel protective method from ischemia reperfusion injury—a review. J Surg Res 150(2):304–330
Qin Z, Song S, Xi G, Silbergleit R, Keep RF, Hoff JT et al (2007) Preconditioning with hyperbaric oxygen attenuates brain edema after experimental intracerebral hemorrhage. Neurosurg Focus 22(5):E13
Alex J, Laden G, Cale AR, Bennett S, Flowers K, Madden L et al (2005) Pretreatment with hyperbaric oxygen and its effect on neuropsychometric dysfunction and systemic inflammatory response after cardiopulmonary bypass: a prospective randomized double-blind trial. J Thorac Cardiovasc Surg 130(6):1623–1630
Horiguchi T, Kis B, Rajapakse N, Shimizu K, Busija DW (2003) Opening of mitochondrial ATP-sensitive potassium channels is a trigger of 3-nitropropionic acid-induced tolerance to transient focal cerebral ischemia in rats. Stroke 34(4):1015–1020
Hoshi A, Nakahara T, Kayama H, Yamamoto T (2006) Ischemic tolerance in chemical preconditioning: possible role of astrocytic glutamine synthetase buffering glutamate-mediated neurotoxicity. J Neurosci Res 84(1):130–141
Zhu H, Sun S, Li H, Xu Y (2006) Cerebral ischemic tolerance induced by 3-nitropropionic acid is associated with increased expression of erythropoietin in rats. Journal of Huazhong University of Science and Technology Medical Sciences 26(4):440–443
Wiegand F, Liao W, Busch C, Castell S, Knapp F, Lindauer U et al (1999) Respiratory chain inhibition induces tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 19(11):1229–1237
Yu ZF, Mattson MP (1999) Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J Neurosci Res 57(6):830–839
Li W, Luo Y, Zhang F, Signore AP, Gobbel GT, Simon RP et al (2006) 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(2):181–198
Li L, Peng L, Zuo Z (2008) Isoflurane preconditioning increases B-cell lymphoma-2 expression and reduces cytochrome c release from the mitochondria in the ischemic penumbra of rat brain. Eur J Pharmacol 586(1–3):106–113
Codaccioni JL, Velly LJ, Moubarik C, Bruder NJ, Pisano PS, Guillet BA (2009) Sevoflurane preconditioning against focal cerebral ischemia: inhibition of apoptosis in the face of transient improvement of neurological outcome. Anesthesiology 110(6):1271–1278
Mayanagi K, Gaspar T, Katakam PV, Kis B, Busija DW (2007) The mitochondrial K(ATP) channel opener BMS-191095 reduces neuronal damage after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 27(2):348–355
Chimon GN, Wong PT (1998) Ischemic tolerance and lipid peroxidation in the brain. NeuroReport 9(10):2269–2272
Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X et al (1998) Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29(9):1937–1950, discussion 50-1
Masada T, Hua Y, Xi G, Ennis SR, Keep RF (2001) Attenuation of ischemic brain edema and cerebrovascular injury after ischemic preconditioning in the rat. J Cereb Blood Flow Metab 21(1):22–33
Cardenas A, Moro MA, Leza JC, O'Shea E, Davalos A, Castillo J et al (2002) Upregulation of TACE/ADAM17 after ischemic preconditioning is involved in brain tolerance. J Cereb Blood Flow Metab 22(11):1297–1302
Zhang HX, Du GH, Zhang JT (2003) Ischemic pre-conditioning preserves brain mitochondrial functions during the middle cerebral artery occlusion in rat. Neurol Res 25(5):471–476
Pradillo JM, Romera C, Hurtado O, Cardenas A, Moro MA, Leza JC et al (2005) TNFR1 upregulation mediates tolerance after brain ischemic preconditioning. J Cereb Blood Flow Metab 25(2):193–203
Zhao L, Nowak TS Jr (2006) CBF changes associated with focal ischemic preconditioning in the spontaneously hypertensive rat. J Cereb Blood Flow Metab 26(9):1128–1140
Zhao J, Sun S, Chen X (2006) Protective effects of focal ischemic preconditioning and HSP70 expression on middle cerebral artery occlusion in rats. Journal of Huazhong University of Science and Technology Medical Sciences 26(4):436–439
Mori T, Muramatsu H, Matsui T, McKee A, Asano T (2000) Possible role of the superoxide anion in the development of neuronal tolerance following ischaemic preconditioning in rats. Neuropathol Appl Neurobiol 26(1):31–40
Alkayed NJ, Goyagi T, Joh HD, Klaus J, Harder DR, Traystman RJ et al (2002) Neuroprotection and P450 2C11 upregulation after experimental transient ischemic attack. Stroke 33(6):1677–1684
Yoshida M, Nakakimura K, Cui YJ, Matsumoto M, Sakabe T (2004) Adenosine A(1) receptor antagonist and mitochondrial ATP-sensitive potassium channel blocker attenuate the tolerance to focal cerebral ischemia in rats. JCereb Blood Flow Metab 24(7):771–779
Mullins PG, Reid DG, Hockings PD, Hadingham SJ, Campbell CA, Chalk JB et al (2001) Ischaemic preconditioning in the rat brain: a longitudinal magnetic resonance imaging (MRI) study. NMR Biomed 14(3):204–209
Watanabe M, Katsura K, Ohsawa I, Mizukoshi G, Takahashi K, Asoh S et al (2008) Involvement of mitoKATP channel in protective mechanisms of cerebral ischemic tolerance. Brain Res 1238:199–207
Taskapilioglu MO, Alkan T, Goren B, Tureyen K, Sahin S, Taskapilioglu O et al (2009) Neuronal protective effects of focal ischemic pre- and/or postconditioning on the model of transient focal cerebral ischemia in rats. J Clin Neurosci 16(5):693–697
Xiong L, Zhu Z, Dong H, Hu W, Hou L, Chen S (2000) Hyperbaric oxygen preconditioning induces neuroprotection against ischemia in transient not permanent middle cerebral artery occlusion rat model. Chin Med J 113(9):836–839
Prass K, Wiegand F, Schumann P, Ahrens M, Kapinya K, Harms C et al (2000) Hyperbaric oxygenation induced tolerance against focal cerebral ischemia in mice is strain dependent. Brain Res 871(1):146–150
Abe H, Nowak TS Jr (2004) 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(1):84–97
Dowden J, Corbett D (1999) Ischemic preconditioning in 18- to 20-month-old gerbils: long-term survival with functional outcome measures. Stroke 30(6):1240–1246
Sugino T, Nozaki K, Takagi Y, Hashimoto N (1999) 3-Nitropropionic acid induces ischemic tolerance in gerbil hippocampus in vivo. Neurosci Lett 259(1):9–12
Acknowledgments
This work was supported by the National Institutes of Health grants NS34709 (RFK), NS054724 (MMW), and NS039866 (GX). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.
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Keep, R.F., Wang, M.M., Xiang, J. et al. Is There a Place for Cerebral Preconditioning in the Clinic?. Transl. Stroke Res. 1, 4–18 (2010). https://doi.org/10.1007/s12975-009-0007-7
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DOI: https://doi.org/10.1007/s12975-009-0007-7