Remote ischemic postconditioning protects the brain from global cerebral ischemia/reperfusion injury by up-regulating endothelial nitric oxide synthase through the PI3K/Akt pathway

Brain Research

Volumn 1445, Issue , 2012, Pages 92-102

  Peng, Bei ^a   Guo, Qu Lian ^a   He, Zhi Jing ^a   Ye, Zhi ^a   Yuan, Ya Jing ^a   Wang, Na ^a   Zhou, Jun ^b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Delayed neuronal death; Endothelial nitric oxide synthase; Global cerebral ischemia; Phosphatidylinositol 3 kinase Akt; Remote ischemic postconditioning

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BAG 1 PROTEIN; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; DNA NUCLEOTIDYLEXOTRANSFERASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL OCCLUSION; BRAIN ISCHEMIA; CONTROLLED STUDY; HIPPOCAMPUS; ISCHEMIC POSTCONDITIONING; LEARNING; MALE; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BRAIN; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL DEATH; CHROMONES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; IN SITU NICK-END LABELING; ISCHEMIC POSTCONDITIONING; MALE; MAZE LEARNING; MORPHOLINES; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE III; NITROARGININE; ONCOGENE PROTEIN V-AKT; PHOSPHATIDYLINOSITOL 3-KINASE; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; REPERFUSION INJURY;

RATTUS;

EID: 84862813296     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.01.033     Document Type: Article

References (50)

1. G. Andreka, M. Vertesaljai, G. Szantho, G. Font, Z. Piroth, G. Fontos, E.D. Juhasz, L. Szekely, Z. Szelid, M.S. Turner, H. Ashrafian, M.P. Frenneaux, and P. Andreka Remote ischaemic postconditioning protects the heart during acute myocardial infarction in pigs Heart 93 2007 749 752 (Pubitemid 46808282)
2. G.C. Brown Nitric oxide and neuronal death Nitric Oxide 23 2010 153 165
3. X. Chao, J. Zhou, T. Chen, W. Liu, W. Dong, Y. Qu, X. Jiang, X. Ji, H. Zhen, and Z. Fei Neuroprotective effect of osthole against acute ischemic stroke on middle cerebral ischemia occlusion in rats Brain Res. 1363 2010 206 211
4. L.L. Chen, H. Yin, and J. Huang Inhibition of TGF-beta1 signaling by eNOS gene transfer improves ventricular remodeling after myocardial infarction through angiogenesis and reduction of apoptosis Cardiovasc. Pathol. 16 2007 221 230 (Pubitemid 47048752)
5. C.A. Chen, T.Y. Wang, S. Varadharaj, L.A. Reyes, C. Hemann, M.A. Talukder, Y.R. Chen, L.J. Druhan, and J.L. Zweier S-glutathionylation uncouples eNOS and regulates its cellular and vascular function Nature 468 2010 1115 1118
6. L.L. Chen, T.B. Zhu, H. Yin, J. Huang, L.S. Wang, K.J. Cao, and Z.J. Yang Inhibition of MAPK signaling by eNOS gene transfer improves ventricular remodeling after myocardial infarction through reduction of inflammation Mol. Biol. Rep. 37 2010 3067 3072
7. B.J. Connell, M. Saleh, B.V. Khan, and T.M. Saleh Lipoic acid protects against reperfusion injury in the early stages of cerebral ischemia Brain Res. 1375 2011 128 136
8. C. De Palma, S. Falcone, C. Panzeri, S. Radice, M.T. Bassi, and E. Clementi Endothelial nitric oxide synthase overexpression by neuronal cells in neurodegeneration: a link between inflammation and neuroprotection J. Neurochem. 106 2008 193 204 (Pubitemid 351840202)
9. S. Dimmeler, I. Fleming, B. Fisslthaler, C. Hermann, R. Busse, and A.M. Zeiher Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation Nature 399 1999 601 605
10. M. Endres, U. Laufs, J.K. Liao, and M.A. Moskowitz Targeting eNOS for stroke protection Trends Neurosci. 27 2004 283 289 (Pubitemid 38529957)
11. M.V. Frantseva, P.L. Carlen, and V.J. Perez Dynamics of intracellular calcium and free radical production during ischemia in pyramidal neurons Free Radic. Biol. Med. 31 2001 1216 1227 (Pubitemid 33052497)
12. X. Gao, H. Zhang, T. Takahashi, J. Hsieh, J. Liao, G.K. Steinberg, and H. Zhao The Akt signaling pathway contributes to postconditioning's protection against stroke; the protection is associated with the MAPK and PKC pathways J. Neurochem. 105 2008 943 955 (Pubitemid 351562746)
13. G. Gritsopoulos, E.K. Iliodromitis, A. Zoga, D. Farmakis, E. Demerouti, A. Papalois, I.A. Paraskevaidis, and D.T. Kremastinos Remote postconditioning is more potent than classic postconditioning in reducing the infarct size in anesthetized rabbits Cardiovasc. Drugs Ther. 23 2009 193 198
14. J.Y. Guo, T. Yang, X.G. Sun, N.Y. Zhou, F.S. Li, D. Long, T. Lin, P.Y. Li, and L. Feng Ischemic postconditioning attenuates liver warm ischemia-reperfusion injury through Akt-eNOS-NO-HIF pathway J. Biomed. Sci. 18 2011 79
15. A. Hashiguchi, S. Yano, M. Morioka, J. Hamada, Y. Ushio, Y. Takeuchi, and K. Fukunaga Up-regulation of endothelial nitric oxide synthase via phosphatidylinositol 3-kinase pathway contributes to ischemic tolerance in the CA1 subfield of gerbil hippocampus J. Cereb. Blood Flow Metab. 24 2004 271 279 (Pubitemid 38314583)
16. L. Hui, D.S. Pei, Q.G. Zhang, Q.H. Guan, and G.Y. Zhang The neuroprotection of insulin on ischemic brain injury in rat hippocampus through negative regulation of JNK signaling pathway by PI3K/Akt activation Brain Res. 1052 2005 1 9 (Pubitemid 41116281)
17. F. Kerendi, H. Kin, M.E. Halkos, R. Jiang, A.J. Zatta, Z.Q. Zhao, R.A. Guyton, and J. Vinten-Johansen Remote postconditioning. Brief renal ischemia and reperfusion applied before coronary artery reperfusion reduces myocardial infarct size via endogenous activation of adenosine receptors Basic Res. Cardiol. 100 2005 404 412 (Pubitemid 41300495)
18. T. Kirino, A. Tamura, and K. Sano A reversible type of neuronal injury following ischemia in the gerbil hippocampus Stroke 17 1986 455 459 (Pubitemid 16085688)
19. J.M. Lee, M.C. Grabb, G.J. Zipfel, and D.W. Choi Brain tissue responses to ischemia J. Clin. Invest. 106 2000 723 731
20. C.M. Li, X.H. Zhang, X.J. Ma, and M. Luo Limb ischemic postconditioning protects myocardium from ischemia-reperfusion injury Scand. Cardiovasc. J. 40 2006 312 317 (Pubitemid 44501941)
21. J. Li, W. Liu, S. Ding, W. Xu, Y. Guan, J.H. Zhang, and X. Sun Hyperbaric oxygen preconditioning induces tolerance against brain ischemia-reperfusion injury by upregulation of antioxidant enzymes in rats Brain Res. 1210 2008 223 229
22. H.W. Liang, S.F. Qiu, J. Shen, L.N. Sun, J.Y. Wang, I.C. Bruce, and Q. Xia Genistein attenuates oxidative stress and neuronal damage following transient global cerebral ischemia in rat hippocampus Neurosci. Lett. 438 2008 116 120
23. H.Y. Lin, C.L. Wu, and C.C. Huang The Akt-endothelial nitric oxide synthase pathway in lipopolysaccharide preconditioning-induced hypoxic-ischemic tolerance in the neonatal rat brain Stroke 41 2010 1543 1551
24. H.Q. Liu, W.B. Li, Q.J. Li, M. Zhang, X.C. Sun, R.F. Feng, X.H. Xian, S.Q. Li, J. Qi, and H.G. Zhao Nitric oxide participates in the induction of brain ischemic tolerance via activating ERK1/2 signaling pathways Neurochem. Res. 31 2006 967 974 (Pubitemid 44134251)
25. X. Liu, H. Chen, B. Zhan, B. Xing, J. Zhou, H. Zhu, and Z. Chen Attenuation of reperfusion injury by renal ischemic postconditioning: the role of NO Biochem. Biophys. Res. Commun. 359 2007 628 634 (Pubitemid 46898997)
26. K. Liu, Q. Li, L. Zhang, and X. Zheng The dynamic detection of NO during stroke and reperfusion in vivo Brain Inj. 23 2009 450 458
27. C. Liu, T. Su, F. Li, L. Li, X. Qin, W. Pan, F. Feng, F. Chen, D. Liao, and L. Chen PI3K/Akt signaling transduction pathway is involved in rat vascular smooth muscle cell proliferation induced by apelin-13 Acta Biochim. Biophys. Sin. (Shanghai) 42 2010 396 402
28. Y.P. Lu, S.Y. Liu, H. Sun, X.M. Wu, J.J. Li, and L. Zhu Neuroprotective effect of astaxanthin on H(2)O(2)-induced neurotoxicity in vitro and on focal cerebral ischemia in vivo Brain Res. 1360 2010 40 48
29. R. Morris Developments of a water-maze procedure for studying spatial learning in the rat J. Neurosci. Methods 11 1984 47 60 (Pubitemid 14088970)
30. H. Pruss, K. Prass, L. Ghaeni, M. Milosevic, C. Muselmann, D. Freyer, G. Royl, U. Reuter, N. Baeva, U. Dirnagl, A. Meisel, and J. Priller Inducible nitric oxide synthase does not mediate brain damage after transient focal cerebral ischemia in mice J. Cereb. Blood Flow Metab. 28 2008 526 539 (Pubitemid 351304264)
31. W.A. Pulsinelli, and J.B. Brierley A new model of bilateral hemispheric ischemia in the unanesthetized rat Stroke 10 1979 267 272 (Pubitemid 9141527)
32. W.A. Pulsinelli, J.B. Brierley, and F. Plum Temporal profile of neuronal damage in a model of transient forebrain ischemia Ann. Neurol. 11 1982 491 498 (Pubitemid 12158810)
33. R. Rastaldo, P. Pagliaro, S. Cappello, C. Penna, D. Mancardi, N. Westerhof, and G. Losano Nitric oxide and cardiac function Life Sci. 81 2007 779 793 (Pubitemid 47332516)
34. C. Ren, Z. Yan, D. Wei, X. Gao, X. Chen, and H. Zhao Limb remote ischemic postconditioning protects against focal ischemia in rats Brain Res. 1288 2009 88 94
35. N. Sandu, and B. Schaller Postconditioning: a new or old option after ischemic stroke? Expert Rev. Cardiovasc. Ther. 8 2010 479 482
36. N. Sawada, and J.K. Liao Targeting eNOS and beyond: emerging heterogeneity of the role of endothelial Rho proteins in stroke protection Expert Rev. Neurother. 9 2009 1171 1186
37. R. Schmidt-Kastner, W. Paschen, B.G. Ophoff, and K.A. Hossmann A modified four-vessel occlusion model for inducing incomplete forebrain ischemia in rats Stroke 20 1989 938 946
38. A. Scorziello, M. Santillo, A. Adornetto, C. Dell'Aversano, R. Sirabella, S. Damiano, L.M. Canzoniero, G.F. Renzo, and L. Annunziato NO-induced neuroprotection in ischemic preconditioning stimulates mitochondrial Mn-SOD activity and expression via Ras/ERK1/2 pathway J. Neurochem. 103 2007 1472 1480 (Pubitemid 47631808)
39. X.C. Sun, W.B. Li, Q.J. Li, M. Zhang, X.H. Xian, J. Qi, R.L. Jin, and S.Q. Li Limb ischemic preconditioning induces brain ischemic tolerance via p38 MAPK Brain Res. 1084 2006 165 174
40. H. Tsubota, A. Marui, J. Esaki, S.C. Bir, T. Ikeda, and R. Sakata Remote postconditioning may attenuate ischaemia-reperfusion injury in the murine hindlimb through adenosine receptor activation Eur. J. Vasc. Endovasc. Surg. 40 2010 804 809
41. J.Y. Wang, J. Shen, Q. Gao, Z.G. Ye, S.Y. Yang, H.W. Liang, I.C. Bruce, B.Y. Luo, and Q. Xia Ischemic postconditioning protects against global cerebral ischemia/reperfusion-induced injury in rats Stroke 39 2008 983 990 (Pubitemid 351619573)
42. R. Xia, B. Zhao, Y. Wu, J.B. Hou, L. Zhang, J.J. Xu, and Z.Y. Xia Ginsenoside Rb1 preconditioning enhances eNOS expression and attenuates myocardial ischemia/reperfusion injury in diabetic rats J. Biomed. Biotechnol. 2011 2011 767930
43. B. Xing, H. Chen, M. Zhang, D. Zhao, R. Jiang, X. Liu, and S. Zhang Ischemic postconditioning inhibits apoptosis after focal cerebral ischemia/reperfusion injury in the rat Stroke 39 2008 2362 2369
44. T. Yamashita, S. Kawashima, Y. Ohashi, M. Ozaki, T. Ueyama, T. Ishida, N. Inoue, K. Hirata, H. Akita, and M. Yokoyama Resistance to endotoxin shock in transgenic mice overexpressing endothelial nitric oxide synthase Circulation 101 2000 931 937 (Pubitemid 30117890)
45. Y. Yang, J. Cao, W. Xiong, J. Zhang, Q. Zhou, H. Wei, C. Liang, J. Deng, T. Li, S. Yang, and L. Xu Both stress experience and age determine the impairment or enhancement effect of stress on spatial memory retrieval J. Endocrinol. 178 2003 45 54 (Pubitemid 36927008)
46. Y. Yuan, Q. Guo, Z. Ye, X. Pingping, N. Wang, and Z. Song Ischemic postconditioning protects brain from ischemia/reperfusion injury by attenuating endoplasmic reticulum stress-induced apoptosis through PI3K-Akt pathway Brain Res. 1367 2011 85 93
47. H.G. Zhao, X.C. Sun, X.H. Xian, W.B. Li, M. Zhang, and Q.J. Li The role of nitric oxide in the neuroprotection of limb ischemic preconditioning in rats Neurochem. Res. 32 2007 1919 1926 (Pubitemid 47497892)
48. H.X. Zhao, X.L. Wang, Y.H. Wang, Y. Wu, X.Y. Li, X.P. Lv, Z.Q. Zhao, R.R. Zhao, and H.R. Liu Attenuation of myocardial injury by postconditioning: role of hypoxia inducible factor-1alpha Basic Res. Cardiol. 105 2010 109 118
49. Y. Zhou, N. Fathali, T. Lekic, R.P. Ostrowski, C. Chen, R.D. Martin, J. Tang, and J.H. Zhang Remote limb ischemic postconditioning protects against neonatal hypoxic-ischemic brain injury in rat pups by the opioid receptor/Akt pathway Stroke 42 2011 439 444
50. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110 (Pubitemid 13058546)