Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion

Ang ET, Wong PT, Moochhala S, Ng YK (2003) Neuroprotection associated with running: is it a result of increased endogenous neurotrophic factors? Neuroscience 118:335–345 Ay I, Sugimori H, Finklestein SP (2001) Intravenous basic fibroblast growth factor (bFGF) decreases DNA fragmentation and prevents downregulation of Bcl-2 expression in the ischemic brain following middle cerebral artery occlusion in rats. Brain Res Mol Brain Res 87:71–80 Barone FC, Feuerstein GZ (1999) Inflammatory mediators and stroke: new opportunities for novel therapeutics. J Cereb Blood Flow Metab 19:819–834 Barone FC, Hillegass LM, Price WJ, White RF, Lee EV, Feuerstein GZ, Sarau HM, Clark RK, Griswold DE (1991) Polymorphonuclear leukocyte infiltration into cerebral focal ischemic tissue: myeloperoxidase activity assay and histologic verification. J Neurosci Res 29:336–345 Belayev L, Alonso OF, Busto R, Zhao W, Ginsberg MD (1996) Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke 27:1616–1622 Berti R, Williams AJ, Moffett JR, Hale SL, Velarde LC, Elliott PJ, Yao C, Dave JR, Tortella FC (2002) Quantitative real-time RT-PCR analysis of inflammatory gene expression associated with ischemia-reperfusion brain injury. J Cereb Blood Flow Metab 22:1068–1079 Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT (1990) Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA 87:5568–5572 Black JE, Zelazny AM, Greenough WT (1991) Capillary and mitochondrial support of neural plasticity in adult rat visual cortex. Exp Neurol 111:204–209 Boero JA, Ascher J, Arregui A, Rovainen C, Woolsey TA (1999) Increased brain capillaries in chronic hypoxia. J Appl Physiol 86:1211–1219 Botchkina GI, Meistrell ME, Botchkina IL, Tracey KJ (1997) Expression of TNF and TNF receptors (p55 and p75) in the rat brain after focal cerebral ischemia. Mol Med 3:765–781 Bruce AJ, Boling W, Kindy MS, Peschon J, Kraemer PJ, Carpenter MK, Holtsberg FW, Mattson MP (1996) Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat Med 2:788–794 Carroll JE, Hess DC, Howard EF, Hill WD (2000) Is nuclear factor-kappaB a good treatment target in brain ischemia/reperfusion injury? NeuroReport 11:R1–R4 Chandrasekar B, Streitman JE, Colston JT, Freeman GL (1998) Inhibition of nuclear factor kappa B attenuates proinflammatory cytokine and inducible nitric oxide synthase expression in postischemic myocardium. Biochim Biophys Acta 1406:91–106 Chatzipanteli K, Alonso OF, Kraydieh S, Dietrich WD (2000) Importance of posttraumatic hypothermia and hyperthermia on the inflammatory response after fluid percussion brain injury: biochemical and immunocytochemical studies. J Cereb Blood Flow Metab 20:531–542 Cotman CW, Engesser C (2002) Exercise enhances and protects brain function. Exerc Sport Sci Rev 30:75–79 Del Zoppo GJ, Becker KJ, Hallenbeck JM (2001) Inflammation after stroke: is it harmful? Arch Neurol 58:669–672 Ding Y, Li J, Rafols JA, Phillis JW, Diaz FG (2002) Pre-reperfusion flushing of ischemic territory reduces inflammatory injury following transient middle cerebral artery occlusion in rats. Stroke 33:2492–2498 Ding Y, Li J, Rafols JA, Clark J, Phillis JW, Diaz FG (2003) Pre-ischemic motor exercise reduces ischemia/reperfusion injury in rats that correlateds with regional angiogenesis and cellular expression of neurotrophin. Stroke 34:240–241 Ding Y, Young C, Li C, Luan X, McAllister JP, II, Clark J, Diaz FG (2003) Reduced inflammatory mediator expression by pre-reperfusion infusion into ischemic territory: a real-time polymerase chain reaction analysis. Neurosci Lett 353:173–176 Ding Y, Li J, Luan X, Ding YH, Lai Q, Rafols JA, Phillis JW, Clark J, Diaz FG (2004) Exercise pre-conditioning reduces brain damage in ischemic rats via regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 124:583–591 Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391–397 Domenech RJ, Macho P, Velez D, Sanchez G, Liu X, Dhalla N (1998) Tachycardia preconditions infarct size in dogs: role of adenosine and protein kinase C. Circulation 97:786–794 Feuerstein GZ, Wang X (2001) Inflammation and stroke: benefits without harm? Arch Neurol 58:672–674 Fisher M, Meadows ME, Do T, Weise J, Trubetskoy V, Charette M, Finklestein SP (1995) Delayed treatment with intravenous basic fibroblast growth factor reduces infarct size following permanent focal cerebral ischemia in rats. J Cereb Blood Flow Metab 15:953–959 Garcia JH, Liu KF, Yoshida Y, Lian J, Chen S, Zoppo GJ del (1994) Influx of leukocytes and platelets in an evolving brain infarct (Wistar rat). Am J Pathol 144:188–199 Gibson UE, Heid CA, Williams PM (1996) A novel method for real time quantitative RT-PCR. Genome Res 6:995–1001 Ginis I, Schweizer U, Brenner M, Liu J, Azzam N, Spatz M, Hallenbeck JM (1999) TNF-alpha pretreatment prevents subsequent activation of cultured brain cells with TNF-alpha and hypoxia via ceramide. Am J Physiol 276:C1171–C1183 Ginis I, Hallenbeck JM, Liu J, Spatz M, Jaiswal R, Shohami E (2000) Tumor necrosis factor and reactive oxygen species cooperative cytotoxicity is mediated via inhibition of NF-kappaB. Mol Med 6:1028–1041 Ginis I, Jaiswal R, Klimanis D, Liu J, Greenspon J, Hallenbeck JM (2002) 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 22:142–152 Gomez M, Bequet F, Berthelot M, Chennaoui M, Guezennec CY (2001) Site-dependent effects of an acute intensive exercise on extracellular 5-HT and 5-HIAA levels in rat brain. Neurosci Lett 301:143–146 Gomez P, Dao L, So V (1997) Physical exercise induces FGF-2 and its mRNA in the hippocampus. Brain Res 764:1–8 Hess DC, Howard E, Cheng C, Carroll J, Hill WD, Hsu CY (2000) Hypertonic mannitol loading of NF-kappaB transcription factor decoys in human brain microvascular endothelial cells blocks upregulation of ICAM-1. Stroke 31:1179–1186 Hiratsuka M, Agatsuma Y, Mizugaki M (1999) Rapid detection of CYP2C9*3 alleles by real-time fluorescence PCR based on SYBR Green. Mol Genet Metab 68:357–362 Howard EF, Chen Q, Cheng C, Carroll JE, Hess D (1998) NF-kappa B is activated and ICAM-1 gene expression is upregulated during reoxygenation of human brain endothelial cells. Neurosci Lett 248:199–203 Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, Granholm AC (2000) Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164:45–52 Isaacs KR, Anderson BJ, Alcantara AA, Black JE, Greenough WT (1992) Exercise and the brain: angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J Cereb Blood Flow Metab 12:110–119 Jean WC, Spellman SR, Nussbaum ES, Low WC (1998) Reperfusion injury after focal cerebral ischemia: the role of inflammation and the therapeutic horizon. Neurosurgery 43:1382–1396 Jiang N, Finklestein SP, Do T, Caday CG, Charette M, Chopp M (1996) Delayed intravenous administration of basic fibroblast growth factor (bFGF) reduces infarct volume in a model of focal cerebral ischemia/reperfusion in the rat. J Neurol Sci 139:173–179 Kleim JA, Cooper NR, VandenBerg PM (2002) Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 934:1–6 Kleim JA, Jones TA, Schallert T (2003) Motor enrichment and the induction of plasticity before or after brain injury. Neurochem Res 28:1757–1769 Koketsu N, Berlove DJ, Moskowitz MA, Kowall NW, Caday CG, Finklestein SP (1994) Pretreatment with intraventricular basic fibroblast growth factor decreases infarct size following focal cerebral ischemia in rats. Ann Neurol 35:451–457 LaManna JC, Vendel LM, Farrell RM (1992) Brain adaptation to chronic hypobaric hypoxia in rats. J Appl Physiol 72:2238–2243 Ledebur HC, Parks TP (1995) Transcriptional regulation of the intercellular adhesion molecule-1 gene by inflammatory cytokines in human endothelial cells. Essential roles of a variant NF-kappa B site and p65 homodimers. J Biol Chem 270:933–943 Li J, Luan X, Clark J, Rafols JA, Ding Y (2004) Neuroprotection against transient cerebral ischemia by exercise pre-conditioning in rats. Neurol Res 26:404–408 Maybaum S, Ilan M, Mogilevsky J, Tzivoni D (1996) Improvement in ischemic parameters during repeated exercise testing: a possible model for myocardial preconditioning. Am J Cardiol 78:1087–1091 Neeper SA, Gomez P, Choi J, Cotman C (1995) Exercise and brain neurotrophins. Nature 373:109 Neeper SA, Gomez P, Choi J, Cotman CW (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726:49–56 Ohtsuki T, Ruetzler CA, Tasaki K, Hallenbeck JM (1996) Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. J Cereb Blood Flow Metab 16:1137–1142 Okada Y, Copeland BR, Mori E, Tung MM, Thomas WS, Zoppo GJ del (1994) P-selectin and intercellular adhesion molecule-1 expression after focal brain ischemia and reperfusion. Stroke 25:202–211 Pagliari R, Peyrin L (1995) Norepinephrine release in the rat frontal cortex under treadmill exercise: a study with microdialysis. J Appl Physiol 78:2121–2130 Radak Z, Sasvari M, Nyakas C, Pucsok J, Nakamoto H, Goto S (2000) Exercise preconditioning against hydrogen peroxide-induced oxidative damage in proteins of rat myocardium. Arch Biochem Biophys 376:248–251 Radak Z, Sasvari M, Nyakas C, Taylor AW, Ohno H, Nakamoto H, Goto S (2000) Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Arch Biochem Biophys 383:114–118 Rahman A, Anwar KN, True AL, Malik AB (1999) Thrombin-induced p65 homodimer binding to downstream NF-kappa B site of the promoter mediates endothelial ICAM-1 expression and neutrophil adhesion. J Immunol 162:5466–5476 Read MA, Whitley MZ, Williams AJ, Collins T (1994) NF-kappa B and I kappa B alpha: an inducible regulatory system in endothelial activation. J Exp Med 179:503–512 Ren JM, Finklestein SP (1997) Time window of infarct reduction by intravenous basic fibroblast growth factor in focal cerebral ischemia. Eur J Pharmacol 327:11–16 Ritter LS, Orozco JA, Coull BM, McDonagh PF, Rosenblum WI (2000) Leukocyte accumulation and hemodynamic changes in the cerebral microcirculation during early reperfusion after stroke. Stroke 31:1153–1161 Schabitz WR, Schwab S, Spranger M, Hacke W (1997) Intraventricular brain-derived neurotrophic factor reduces infarct size after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 17:500–506 Stanimirovic D, Satoh K (2000) Inflammatory mediators of cerebral endothelium: a role in ischemic brain inflammation. Brain Pathol 10:113–126 Stummer W, Weber K, Tranmer B, Baethmann A, Kempski O (1994) Reduced mortality and brain damage after locomotor activity in gerbil forebrain ischemia. Stroke 25:1862–1869 Swain RA, Harris AB, Wiener EC, Dutka MV, Morris HD, Theien BE, Konda S, Engberg K, Lauterbur PC, Greenough WT (2003) Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117:1037–1046 Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR (1990) A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 10:290–293 Tasaki K, Ruetzler CA, Ohtsuki T, Martin D, Nawashiro H, Hallenbeck JM (1997) Lipopolysaccharide pre-treatment induces resistance against subsequent focal cerebral ischemic damage in spontaneously hypertensive rats. Brain Res 748:267–270 Tomai F, Crea F, Chiariello L, Gioffre PA (1999) Ischemic preconditioning in humans: models, mediators, and clinical relevance. Circulation 100:559–563 Tracey KJ, Vlassara H, Cerami A (1989) Cachectin/tumour necrosis factor. Lancet 1:1122–1126 Vissing J, Andersen M, Diemer NH (1996) Exercise-induced changes in local cerebral glucose utilization in the rat. J Cereb Blood Flow Metab 16:729–736 Wang RY, Yang YR, Yu SM (2001) Protective effects of treadmill training on infarction in rats. Brain Res 922:140–143 Wang X, Li X, Currie RW, Willette RN, Barone FC, Feuerstein GZ (2000) Application of real-time polymerase chain reaction to quantitate induced expression of interleukin-1beta mRNA in ischemic brain tolerance. J Neurosci Res 59:238–246 Wang X, Li X, Erhardt JA, Barone FC, Feuerstein GZ (2000) Detection of tumor necrosis factor-alpha mRNA induction in ischemic brain tolerance by means of real-time polymerase chain reaction. J Cereb Blood Flow Metab 20:15–20 Yamashita K, Wiessner C, Lindholm D, Thoenen H, Hossmann KA (1997) Post-occlusion treatment with BDNF reduces infarct size in a model of permanent occlusion of the middle cerebral artery in rat. Metab Brain Dis 12:271–280 Yamashita N, Hoshida S, Otsu K, Taniguchi N, Kuzuya T, Hori M (1999) Monophosphoryl lipid A provides biphasic cardioprotection against ischaemia-reperfusion injury in rat hearts. Br J Pharmacol 128:412–418 Yanamoto H, Hashimoto N, Nagata I, Kikuchi H (1998) Infarct tolerance against temporary focal ischemia following spreading depression in rat brain. Brain Res 784:239–249 Yanamoto H, Nagata I, Sakata M, Zhang Z, Tohnai N, Sakai H, Kikuchi H (2000) Infarct tolerance induced by intra-cerebral infusion of recombinant brain-derived neurotrophic factor. Brain Res 859:240–248 Zea Longa Z, Weinstein PR, Carlson S, Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84–91 Zhang RL, Chopp M, Chen H, Garcia JH (1994) Temporal profile of ischemic tissue damage, neutrophil response, and vascular plugging following permanent and transient (2H) middle cerebral artery occlusion in the rat. J Neurol Sci 125:3–10 Zhang Z, Chopp M (2002) Vascular endothelial growth factor and angiopoietins in focal cerebral ischemia. Trends Cardiovasc Med 12:62–66