Exercise preconditioning and brain ischemic tolerance

Neuroscience

Volumn 177, Issue , 2011, Pages 170-176

  Zhang, F ^a,b   Wu, Y ^a,b   Jia, J ^a,b  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

Blood brain barrier; Brain ischemic tolerance; Cerebral vasculature; Exercise preconditioning; Inflammatory response; Neuron apoptosis

Indexed keywords

GLUTAMIC ACID; MESSENGER RNA; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN EDEMA; BRAIN INFARCTION; BRAIN ISCHEMIA; CYTOKINE RELEASE; DAILY LIFE ACTIVITY; HUMAN; INFLAMMATION; ISCHEMIC PRECONDITIONING; KINESIOTHERAPY; MANUAL LABOR; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PHYSICAL TOLERANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; THERAPY EFFECT; TREADMILL EXERCISE;

ANIMALS; BRAIN INFARCTION; BRAIN ISCHEMIA; EXERCISE THERAPY; HUMANS; ISCHEMIC PRECONDITIONING; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL FITNESS;

EID: 79952003196     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.01.018     Document Type: Review

References (95)

1. Aberg M.A.I., Aberg N.D., Hedbacker H., Oscarsson J., Eriksson P.S. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 2000, 20:2896-2903.
2. Alevizos A., Lentzas J., Kokkoris S., Mariolis A., Korantzopoulos P. Physical activity and stroke risk. Int J Clin Pract 2005, 59:922-930.
3. Ang E.T., Wong P.T.H., Moochhala S., Ng Y.K. Neuroprotection associated with running: is it a result of increased endogenous neurotrophic factors?. Neuroscience 2003, 118:335-345.
4. Asahi M., Wang X.Y., Mori T., Sumii T., Jung J.C., Moskowitz M.A., Fini M.E., Lo E.H. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 2001, 21:7724-7732.
5. Berti R., Williams A.J., Moffett J.R., Hale S.L., Velarde L.C., Elliott P.J., Yao C.P., Dave J.R., Tortella F.C. Quantitative real-time RT-PCR analysis of inflammatory gene expression associated with ischemia-reperfusion brain injury. J Cereb Blood Flow Metab 2002, 22:1068-1079.
6. Bigdeli M.R., Hajizadeh S., Froozandeh M., Rasulian B., Heidarianpour A., Khoshbaten A. Prolonged and intermittent normobaric hyperoxia induce different degrees of ischemic tolerance in rat brain tissue. Brain Res 2007, 1152:228-233.
7. Blondeau N., Widmann C., Lazdunski M., Heurteaux C. Activation of the nuclear factor-kappaB is a key event in brain tolerance. J Neurosci 2001, 21:4668-4677.
8. Brandt M.D., Maass A., Kempermann G., Storch A. Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. Eur J Neurosci 2010, 32:1256-1264.
9. Brown J., Cooper-Kuhn C.M., Kempermann G., Van Praag H., Winkler J., Gage F.H., Kuhn H.G. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003, 17:2042-2046.
10. Bullitt E., Rahman F.N., Smith J.K., Kim E., Zeng D., Katz L.M., Marks B.L. The effect of exercise on the cerebral vasculature of healthy aged subjects as visualized by MR angiography. AJNR Am J Neuroradiol 2009, 30:1857-1863.
11. Cao L., Jiao X.Y., Zuzga D.S., Liu Y.H., Fong D.M., Young D., During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 2004, 36:827-835.
12. Cardenas A., Moro M.A., Leza J.C., O'Shea E., Davalos A., Castillo J., Lorenzo P., Lizasoain I. Upregulation of TACE/ADAM17 after ischemic preconditioning is involved in brain tolerance. J Cereb Blood Flow Metab 2002, 22:1297-1302.
13. Carro E., Nunez A., Busiguina S., Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 2000, 20:2926-2933.
14. Chaudhry K., Rogers R., Guo M., Lai Q., Goel G., Liebelt B., Ji X.M., Curry A., Carranza A., Jimenez D.F., Ding Y.C. Matrix metalloproteinase-9 (MMP-9) expression and extracellular signal-regulated kinase 1 and 2 (ERK1/2) activation in exercise-reduced neuronal apoptosis after stroke. Neurosci Lett 2010, 474:109-114.
15. Chen J., Graham S.H., Zhu R.L., Simon R.P. Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 1996, 16:566-577.
16. Chen J., Zhu R.L., Nakayama M., Kawaguchi K., Jin K.L., Stetler R.A., Simon R.P., Graham S.H. Expression of the apoptosis-effector gene, Bax, is up-regulated in vulnerable hippocampal CA1 neurons following global ischemia. J Neurochem 1996, 67:64-71.
17. Chrysohoou C., Pitsavos C., Kokkinos P., Panagiotakos D.B., Singh S.N., Stefanadis C. The role of physical activity in the prevention of stroke. Cent Eur J Public Health 2005, 13:132-136.
18. Correale J., Villa A. The neuroprotective role of inflammation in nervous system injuries. J Neurol 2004, 251:1304-1316.
19. Cotman C.W., Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002, 25:295-301.
20. Cotman C.W., Berchtold N.C., Christie L.A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007, 30:464-472.
21. Ding Y., Li J., Luan X., Ding Y.H., Lai Q., Rafols J.A., Phillis J.W., Clark J.C., Diaz F.G. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 2004, 124:583-591.
22. Ding Y.H., Ding Y.C., Li J., Bessert D.A., Rafols J.A. Exercise pre-conditioning strengthens brain microvascular integrity in a rat stroke model. Neurol Res 2006, 28:184-189.
23. Ding Y.H., Li J., Yao W.X., Rafols J.A., Clark J.C., Ding Y. Exercise preconditioning upregulates cerebral integrins and enhances cerebrovascular integrity in ischemic rats. Acta Neuropathol 2006, 112:74-84.
24. Ding Y.H., Young C.N., Luan X.D., Li J., Rafols J.A., Clark J.C., McAllister J.P., Ding Y.C. Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol 2005, 109:237-246.
25. Dirnagl U., Becker K., Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 2009, 8:398-412.
26. Dirnagl U., Simon R.P., Hallenbeck J.M. Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 2003, 26:248-254.
27. Emsley H.C., Hopkins S.J. Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol 2008, 7:341-353.
28. Endres M., Gertz K., Lindauer U., Katchanov J., Schultze J., Schrock H., Nickenig G., Kuschinsky W., Dirnagl U., Laufs U. Mechanisms of stroke protection by physical activity. Ann Neurol 2003, 54:582-590.
29. Evenson K.R., Rosamond W.D., Cai J.W., Toole J.F., Hutchinson R.G., Shahar E., Folsom A.R., Investigators A.S. Physical activity and ischemic stroke risk-the atherosclerosis risk in communities study. Stroke 1999, 30:1333-1339.
30. Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., Kuo C.J., Palmer T.D. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 2003, 18:2803-2812.
31. Ferrer I., Friguls B., Dalfo E., Justicia C., Planas A.M. Caspase-dependent and caspase-independent signalling of apoptosis in the penumbra following middle cerebral artery occlusion in the adult rat. Neuropathol Appl Neurobiol 2003, 29:472-481.
32. Gidday J.M., Fitzgibbons J.C., Shah A.R., Park T.S. Neuroprotection from ishcemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci Lett 1994, 168:221-224.
33. Giffard R.G., Yenari M.A. Many mechanisms for Hsp70 protection from cerebral ischemia. J Neurosurg Anesthesiol 2004, 16:53-61.
34. Guo M., Cox B., Mahale S., Davis W., Carranza A., Hayes K., Sprague S., Jimenez D., Ding Y. Pre-ischemic exercise reduces matrix metalloproteinase-9 expression and ameliorates blood-brain barrier dysfunction in stroke. Neuroscience 2008, 151:340-351.
35. Guo M., Lin V., Davis W., Huang T., Carranza A., Sprague S., Reyes R., Jimenez D., Ding Y.C. Pre-ischemic induction of TNF-alpha by physical exercise reduces blood-brain barrier dysfunction in stroke. J Cereb Blood Flow Metab 2008, 28:1422-1430.
36. Hallenbeck J.M. Inflammatory reactions at the blood-endothelial interface in acute stroke. Adv Neurol 1996, 71:281-300.
37. Hornebeck W., Lambert E., Petitfrere E., Bernard P. Beneficial and detrimental influences of tissue inhibitor of metalloproteinase-1 (TIMP-1) in tumor progression. Biochimie 2005, 87:377-383.
38. Hu X.Q., Zheng H.Q., Yan T.B., Pan S.Q., Fang J., Jiang R.S., Ma S.F. Physical exercise induces expression of CD31 and facilitates neural function recovery in rats with focal cerebral infarction. Neurol Res 2010, 32:397-402.
39. Isaacs K.R., Anderson B.J., Alcantara A.A., Black J.E., Greenough W.T. Exercise and the brain: -angiogenesis in the adult-rat cerebellum after vigorous physical-activity and motor skill learning. J Cereb Blood Flow Metab 1992, 12:110-119.
40. Jack K., McLean S.M., Moffett J.K., Gardiner E. Barriers to treatment adherence in physiotherapy outpatient clinics: a systematic review. Man Ther 2010, 15:220-228.
41. Jia J., Hu Y.S., Wu Y., Liu G., Yu H.X., Zheng Q.P., Zhu D.N., Xia C.M., Cao Z.J. Pre-ischemic treadmill training affects glutamate and gamma aminobutyric acid levels in the striatal dialysate of a rat model of cerebral ischemia. Life Sci 2009, 84:505-511.
42. Jiang X.Y., Tian F., Mearow K., Okagaki P., Lipsky R.H., Marini A.M. The excitoprotective effect of N-methyl-d-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons. J Neurochem 2005, 94:713-722.
43. Kim S.E., Ko I.G., Kim B.K., Shin M.S., Cho S., Kim C.J., Kim S.H., Baek S.S., Lee E.K., Jee Y.S. Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 2010, 45:357-365.
44. Kitagawa K., Matsumoto M., Tagaya M., Hata R., Ueda H., Niinobe M., Handa N., Fukunaga R., Kimura K., Mikoshiba K., Kamada T. Ischemic tolerance phenomenon in the brain. Brain Res 1990, 528:21-24.
45. Kleffner I., Bungeroth M., Schiffbauer H., Schabitz W.R., Ringelstein E.B., Kuhlenbaumer G. The role of aquaporin-4 polymorphisms in the development of brain edema after middle cerebral artery occlusion. Stroke 2008, 39:1333-1335.
46. Lau L.T., Yu A.C.H. Astrocytes produce and release interleukin-1, interleukin-6, tumor necrosis factor alpha and interferon-gamma following traumatic and metabolic injury. J Neurotrauma 2001, 18:351-359.
47. Lee C.D., Folsom A.R., Blair S.N. Physical activity and stroke risk: a meta-analysis. Stroke 2003, 34:2475-2481.
48. Lee J.E., Yenari M.A., Sun G.H., Xu L.J., Emond M.R., Cheng D.Y., Steinberg G.K., Giffard R.G. Differential neuroprotection from human heat shock protein 70 overexpression in in vitro and in vivo models of ischemia and ischemia-like conditions. Exp Neurol 2001, 170:129-139.
49. Lennon S.L., Quindry J., Hamilton K.L., French J., Staib J., Mehta J.L., Powers S.K. Loss of exercise-induced cardioprotection after cessation of exercise. J Appl Physiol 2004, 96:1299-1305.
50. Li D.Y., Tao L., Liu H., Christopher T.A., Lopez B.L., Ma X.L. Role of ERK1/2 in the anti-apoptotic and cardioprotective effects of nitric oxide after myocardial ischemia and reperfusion. Apoptosis 2006, 11:923-930.
51. Li J., Luan X.D., Clark J.C., Rafols J.A., Ding Y.C. Neuroprotection against transient cerebral ischemia by exercise pre-conditioning in rats. Neurol Res 2004, 26:404-408.
52. Li Y., Powers C., Jiang N., Chopp M. Intact, injured, necrotic and apoptotic cells after focal cerebral ischemia in the rat. J Neurol Sci 1998, 156:119-132.
53. Liebelt B., Papapetrou P., Ali A., Guo M., Ji X., Peng C., Rogers R., Curry A., Jimenez D., Ding Y. Exercise preconditioning reduces neuronal apoptosis in stroke by up-regulation heat shock protein-70 (heat shock protein-72) and extracellular-signal-regulated-kinase1/2. Neuroscience 2010, 166:1091-1100.
54. Liu J., Ginis T., Spatz M., Hallenbeck J.M. Hypoxic preconditioning protects cultured neurons against hypoxic stress via TNF-alpha and ceramide. Am J Physiol Cell Physiol 2000, 278:C144-C153.
55. Llorens-Martin M., Torres-Aleman I., Trejo J.L. Exercise modulates insulin-like growth factor 1-dependent and -independent effects on adult hippocampal neurogenesis and behavior. Mol Cell Neurosci 2010, 44:109-117.
56. Masada T., Hua Y., Xi G.H., Ennis S.R., Keep R.F. Attenuation of ischemic brain edema and cerebrovascular injury after ischemic preconditioning in the rat. J Cereb Blood Flow Metab 2001, 21:22-33.
57. Maysami S., Lan J.Q., Minami M., Simon R.P. Proliferating progenitor cells: a required cellular element for induction of ischemic tolerance in the brain. J Cereb Blood Flow Metab 2008, 28:1104-1113.
58. Memezawa H., Smith M.L., Siesjo B.K. Penumbral tissues salvaged by reperfusion following middle cerebral-artery occlusion in rats. Stroke 1992, 23:552-559.
59. Mitani A., Tanaka K. Functional changes of glial glutamate transporter GLT-1 during ischemia: an in vivo study in the hippocampal CA1 of normal mice and mutant mice lacking GLT-1. J Neurosci 2003, 23:7176-7182.
60. Ohtsuka K., Suzuki T. Roles of molecular chaperones in the nervous system. Brain Res Bull 2000, 53:141-146.
61. Ohtsuki T., Matsumoto M., Kuwabara K., Kitagawa K., Suzuki K., Taniguchi N., Kamada T. Influence of oxidative stress on induced tolerance to ischemia in gerbil hippocampal neurons. Brain Res 1992, 599:246-252.
62. Ohtsuki T., Ruetzler C.A., Tasaki K., Hallenbeck J.M. Interleukin-1 mediates induction of tolerance to global ischemia in gerbil hippocampal CA1 neurons. J Cereb Blood Flow Metab 1996, 16:1137-1142.
63. Opitz T., Grooms S.Y., Bennett M.V., Zukin R.S., Optiz T. Remodeling of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit composition in hippocampal neurons after global ischemia. Proc Natl Acad Sci U S A 2000, 97:13360-13365.
64. Ostrakhovitch E.A., Cherian M.G. Inhibition of extracellular signal regulated kinase (ERK) leads to apoptosis inducing factor (AIF) mediated apoptosis in epithelial breast cancer cells: the lack of effect of ERK in p53 mediated copper induced apoptosis. J Cell Biochem 2005, 95:1120-1134.
65. PerezPinzon M.A., Mumford P.L., Rosenthal M., Sick T.J. Anoxic preconditioning in hippocampal slices: role of adenosine. Neuroscience 1996, 75:687-694.
66. Reiss J.I., Dishman R.K., Boyd H.E., Robinson J.K., Holmes P.V. Chronic activity wheel running reduces the severity of kainic acid-induced seizures in the rat: possible role of galanin. Brain Res 2009, 1266:54-63.
67. Rhodes J.S., van Praag H., Jeffrey S., Girard I., Mitchell G.S., Garland T., Gage F.H. Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav Neurosci 2003, 117:1006-1016.
68. Rhyu I.J., Bytheway J.A., Kohler S.J., Lange H., Lee K.J., Boklewski J., McCormick K., Williams N.I., Stanton G.B., Greenough W.T., Cameron J.L. Effects of aerobic exercise training on cognitive function and cortical vascularity in monkeys. Neuroscience 2010, 167:1239-1248.
69. 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.
70. Rosenberg G.A., Estrada E.Y., Dencoff J.E. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998, 29:2189-2195.
71. Sawatzky D.A., Willoughby D.A., Colville-Nash P.R., Rossi A.G. The involvement of the apoptosis-modulating proteins ERK 1/2, Bcl-xL and Bax in the resolution of acute inflammation in vivo. Am J Pathol 2006, 168:33-41.
72. Schilling M., Besselmann M., Leonhard C., Mueller M., Ringelstein E.B., Kiefer R. Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: a study in green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 2003, 183:25-33.
73. Sommer C., Roth S.U., Kuhn R., Kiessling M. Metabotropic glutamate receptor subtypes are differentially expressed after transient cerebral ischemia without, during and after tolerance induction in the gerbil hippocampus. Brain Res 2000, 872:172-180.
74. Soriano F.X., Papadia S., Hofmann F., Hardingham N.R., Bading H., Hardingham G.E. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J Neurosci 2006, 26:4509-4518.
75. Stames J.W., Choilawala A.M., Taylor R.P., Nelson M.J., Delp M.D. Myocardial heat shock protein 70 expression in young and old rats after identical exercise programs. J Gerontol A Biol Sci Med Sci 2005, 60:963-969.
76. Stenzel-Poore M.P., Stevens S.L., King J.S., Simon R.P. Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes-a speculative synthesis. Stroke 2007, 38:680-685.
77. Stoica B.A., Movsesyan V.A., Knoblach S.M., Faden A.I. Ceramide induces neuronal apoptosis through mitogen-activated protein kinases and causes release of multiple mitochondrial proteins. Mol Cell Neurosci 2005, 29:355-371.
78. Stoll G., Jander S., Schroeter M. Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 1998, 56:149-171.
79. Stummer W., Baethmann A., Murr R., Schurer L., Kempski O.S. Cerebral protection against ischemia by locomotor-activity in gerbils. Underlying mechanisms. Stroke 1995, 26:1423-1429.
80. Swain R.A., Harris A.B., Wiener E.C., Dutka M.V., Morris H.D., Theien B.E., Konda S., Engberg K., Lauterbur P.C., Greenough W.T. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003, 117:1037-1046.
81. Tang K.C., Xia F.C., Wagner P.D., Breen E.C. Exercise-induced VEGF transcriptional activation in brain, lung and skeletal muscle. Respir Physiol Neurobiol 2010, 170:16-22.
82. Trejo J.L., Carro E., Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 2001, 21:1628-1634.
83. van Praag H., Shubert T., Zhao C.M., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005, 25:8680-8685.
84. Vinereanu D. Risk factors for atherosclerotic disease: present and future. Herz 2006, 31:5-24.
85. Wang Q., Peng Y., Chen S.Y., Gou X.C., Hu B., Du J., Lu Y., Xiong L. Pretreatment with electroacupuncture induces rapid tolerance to focal cerebral ischemia through regulation of endocannabinoid system. Stroke 2009, 40:2157-2164.
86. Wang Q., Tang X.N., Yenari M.A. The inflammatory response in stroke. J Neuroimmunol 2007, 184:53-68.
87. Wang R.Y., Yang Y.R., Yu S.M. Protective effects of treadmill training on infarction in rats. Brain Res 2001, 922:140-143.
88. Wang X.Y., Lo E.H. Triggers and mediators of hemorrhagic transformation in cerebral ischemia. Mol Neurobiol 2003, 28:229-244.
89. Wolf P.A., Clagett G.P., Easton J.D., Goldstein L.B., Gorelick P.B., Kelly-Hayes M., Sacco R.L., Whisnant J.P. Preventing ischemic stroke in patients with prior stroke and transient ischemic attack: a statement for healthcare professionals from the Stroke Council of the American Heart Association. Stroke 1999, 30:1991-1994.
90. Yang Y.R., Wang R.Y., Wang P.S.G. Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett 2003, 339:91-94.
91. Zhang F., Jia J., Wu Y., Hu Y.S., Wang Y. The effect of treadmill training pre-exercise on glutamate receptor expression in rats after cerebral ischemia. Int J Mol Sci 2010, 11:2658-2669.
92. Zhang F., Wu Y., Jia J., Hu Y.S. Pre-ischemic treadmill training induces tolerance to brain ischemia: involvement of glutamate and ERK1/2. Molecules 2010, 15:5246-5257.
93. Zheng Z., Yenari M.A. Post-ischemic inflammation: molecular mechanisms and therapeutic implications. Neurol Res 2004, 26:884-892.
94. Zhuang S.G., Schnellmann R.G. A death-promoting role for extracellular signal-regulated kinase. J Pharmacol Exp Ther 2006, 319:991-997.
95. Zwagerman N., Sprague S., Davis M.D., Daniels B., Goel G., Ding Y.C. Pre-ischemic exercise preserves cerebral blood flow during reperfusion in stroke. Neurol Res 2010, 32:523-529.