NNOS and p-ERK involvement in the neuroprotection exerted by remote postconditioning in rats subjected to transient middle cerebral artery occlusion

Neurobiology of Disease

Volumn 54, Issue , 2013, Pages 105-114

  Pignataro, Giuseppe ^a,b   Esposito, Elga ^a,b   Sirabella, Rossana ^a,b   Vinciguerra, Antonio ^a,b   Cuomo, Ornella ^a,b   Di Renzo, Gianfranco ^a,b   Annunziato, Lucio ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b IRCCS SDN   (Italy)

Author keywords

Brain ischemia; Focal ischemia; Ischemic postconditioning; Ischemic preconditioning; Neuroprotection; Nitric oxide; P ERK; Remote postconditioning

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CONTROLLED STUDY; FEMORAL ARTERY FLOW; GENE SILENCING; IN VIVO STUDY; ISCHEMIC POSTCONDITIONING; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; BRAIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMORAL ARTERY; GENE KNOCKDOWN TECHNIQUES; INFARCTION, MIDDLE CEREBRAL ARTERY; ISCHEMIC POSTCONDITIONING; MALE; NITRIC OXIDE SYNTHASE TYPE I; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84875586477     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.02.008     Document Type: Article

References (41)

1. Addison P.D., Neligan P.C., Ashrafpour H., Khan A., Zhong A., Moses M., Forrest C.R., Pang C.Y. Noninvasive remote ischemic preconditioning for global protection of skeletal muscle against infarction. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H1435-H1443.
2. Andreka G., Vertesaljai M., Szantho G., Font G., Piroth Z., Fontos G., Juhasz E.D., Szekely L., Szelid Z., Turner M.S., Ashrafian H., Frenneaux M.P., Andreka P. Remote ischaemic postconditioning protects the heart during acute myocardial infarction in pigs. Heart 2007, 93:749-752.
3. Ates E., Genc E., Erkasap N., Erkasap S., Akman S., Firat P., Emre S., Kiper H. Renal protection by brief liver ischemia in rats. Transplantation 2002, 74:1247-1251.
4. Birnbaum Y., Hale S.L., Kloner R.A. Ischemic preconditioning at a distance: reduction of myocardial infarct size by partial reduction of blood supply combined with rapid stimulation of the gastrocnemius muscle in the rabbit. Circulation 1997, 96:1641-1646.
5. Chen X.G., Wu B.Y., Wang J.K., Bai T. Mechanism of the protective effects of noninvasive limbs preconditioning on myocardial ischemia-reperfusion injury. Chin. Med. J. (Engl.) 2005, 118:1723-1727.
6. Dirnagl U., Meisel A. Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning?. Neuropharmacology 2008, 55:334-344.
7. Eberlin K.R., McCormack M.C., Nguyen J.T., Tatlidede H.S., Randolph M.A., Austen W.G. Sequential limb ischemia demonstrates remote postconditioning protection of murine skeletal muscle. Plast. Reconstr. Surg. 2009, 123:8S-16S.
8. Gao X., Ren C., Zhao H. Protective effects of ischemic postconditioning compared with gradual reperfusion or preconditioning. J. Neurosci. Res. 2008, 86:2505-2511.
9. Geng X., Ren C., Wang T., Fu P., Luo Y., Liu X., Yan F., Ling F., Jia J., Du H., Ji X., Ding Y. Effect of remote ischemic postconditioning on an intracerebral hemorrhage stroke model in rats. Neurol. Res. 2012, 34:143-148.
10. Gho B.C., Schoemaker R.G., van Den Doel M.A., Duncker D.J., Verdouw P.D. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 1996, 94:2193-2200.
11. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 2006, 7:437-448.
12. Gritsopoulos G., Iliodromitis E.K., Zoga A., Farmakis D., Demerouti E., Papalois A., Paraskevaidis I.A., Kremastinos D.T. Remote postconditioning is more potent than classic postconditioning in reducing the infarct size in anesthetized rabbits. Cardiovasc. Drugs Ther. 2009, 23:193-198.
13. Huang Z., Huang P.L., Panahian N., Dalkara T., Fishman M.C., Moskowitz M.A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 1994, 265:1883-1885.
14. Iadecola C., Kahles T., Gallo E.F., Anrather J. Neurovascular protection by ischaemic tolerance: role of nitric oxide. J. Physiol. 2011, 589:4137-4145.
15. Jiang X., Shi E., Nakajima Y., Sato S. Postconditioning, a series of brief interruptions of early reperfusion, prevents neurologic injury after spinal cord ischemia. Ann. Surg. 2006, 244:148-153.
16. Kanoria S., Jalan R., Davies N.A., Seifalian A.M., Williams R., Davidson B.R. Remote ischaemic preconditioning of the hind limb reduces experimental liver warm ischaemia-reperfusion injury. Br. J. Surg. 2006, 93:762-768.
17. Kawano T., Anrather J., Zhou P., Park L., Wang G., Frys K.A., Kunz A., Cho S., Orio M., Iadecola C. Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat. Med. 2006, 12:225-229.
18. Kin H., Zatta A.J., Lofye M.T., Amerson B.S., Halkos M.E., Kerendi F., Zhao Z.Q., Guyton R.A., Headrick J.P., Vinten-Johansen J. Postconditioning reduces infarct size via adenosine receptor activation by endogenous adenosine. Cardiovasc. Res. 2005, 67:124-133.
19. Konstantinov I.E., Arab S., Kharbanda R.K., Li J., Cheung M.M., Cherepanov V., Downey G.P., Liu P.P., Cukerman E., Coles J.G., Redington A.N. The remote ischemic preconditioning stimulus modifies inflammatory gene expression in humans. Physiol Genomics 2004, 19:143-150.
20. Leker R.R., Teichner A., Ovadia H., Keshet E., Reinherz E., Ben-Hur T. Expression of endothelial nitric oxide synthase in the ischemic penumbra: relationship to expression of neuronal nitric oxide synthase and vascular endothelial growth factor. Brain Res. 2001, 909:1-7.
21. Loukogeorgakis S.P., Williams R., Panagiotidou A.T., Kolvekar S.K., Donald A., Cole T.J., Yellon D.M., Deanfield J.E., MacAllister R.J. Transient limb ischemia induces remote preconditioning and remote postconditioning in humans by a K(ATP)-channel dependent mechanism. Circulation 2007, 116:1386-1395.
22. Lu X.M., Zhang G.X., Yu Y.Q., Kimura S., Nishiyama A., Matsuyoshi H., Shimizu J., Takaki M. The opposite roles of nNOS in cardiac ischemia-reperfusion-induced injury and in ischemia preconditioning-induced cardio protection in mice. J. Physiol. Sci. 2009, 59:253-262.
23. Moses M.A., Addison P.D., Neligan P.C., Ashrafpour H., Huang N., McAllister S.E., Lipa J.E., Forrest C.R., Pang C.Y. Inducing late phase of infarct protection in skeletal muscle by remote preconditioning: efficacy and mechanism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R1609-R1617.
24. Oxman T., Arad M., Klein R., Avazov N., Rabinowitz B. Limb ischemia preconditions the heart against reperfusion tachyarrhythmia. Am. J. Physiol. 1997, 273:H1707-H1712.
25. Peng B., Guo Q.L., He Z.J., Ye Z., Yuan Y.J., Wang N., Zhou J. 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 Res. 2012, 1445:92-102.
26. Pignataro G., Gala R., Cuomo O., Tortiglione A., Giaccio L., Castaldo P., Sirabella R., Matrone C., Canitano A., Amoroso S., Di Renzo G., Annunziato L. Two sodium/calcium exchanger gene products, NCX1 and NCX3, play a major role in the development of permanent focal cerebral ischemia. Stroke 2004, 35:2566-2570.
27. Pignataro G., Tortiglione A., Scorziello A., Giaccio L., Secondo A., Severino B., Santagada V., Caliendo G., Amoroso S., Di Renzo G., Annunziato L. Evidence for a protective role played by the Na+/Ca2+ exchanger in cerebral ischemia induced by middle cerebral artery occlusion in male rats. Neuropharmacology 2004, 46:439-448.
28. Pignataro G., Meller R., Inoue K., Ordonez A.N., Ashley M.D., Xiong Z., Gala R., Simon R.P. In vivo and in vitro characterization of a novel neuroprotective strategy for stroke: ischemic postconditioning. J. Cereb. Blood Flow Metab. 2008, 28:232-241.
29. Pignataro G., Scorziello A., Di Renzo G., Annunziato L. Post-ischemic brain damage: effect of ischemic preconditioning and postconditioning and identification of potential candidates for stroke therapy. FEBS J. 2009, 276:46-57.
30. Ren C., Gao X., Niu G., Yan Z., Chen X., Zhao H. Delayed postconditioning protects against focal ischemic brain injury in rats. PLoS One 2008, 3:e3851.
31. Ren C., Yan Z., Wei D., Gao X., Chen X., Zhao H. Limb remote ischemic postconditioning protects against focal ischemia in rats. Brain Res. 2009, 1288:88-94.
32. Singh D., Chopra K. Evidence of the role of angiotensin AT(1) receptors in remote renal preconditioning of myocardium. Methods Find. Exp. Clin. Pharmacol. 2004, 26:117-122.
33. Staat P., Rioufol G., Piot C., Cottin Y., Cung T.T., L'Huillier I., Aupetit J.F., Bonnefoy E., Finet G., Andre-Fouet X., Ovize M. Postconditioning the human heart. Circulation 2005, 112:2143-2148.
34. Takaoka A., Nakae I., Mitsunami K., Yabe T., Morikawa S., Inubushi T., Kinoshita M. Renal ischemia/reperfusion remotely improves myocardial energy metabolism during myocardial ischemia via adenosine receptors in rabbits: effects of "remote preconditioning". J. Am. Coll. Cardiol. 1999, 33:556-564.
35. Wang M.J., Huang H.M., Hsieh S.J., Jeng K.C., Kuo J.S. Resveratrol inhibits interleukin-6 production in cortical mixed glial cells under hypoxia/hypoglycemia followed by reoxygenation. J. Neuroimmunol. 2001, 112:28-34.
36. Weinbrenner C., Schulze F., Sarvary L., Strasser R.H. Remote preconditioning by infrarenal aortic occlusion is operative via delta1-opioid receptors and free radicals in vivo in the rat heart. Cardiovasc. Res. 2004, 61:591-599.
37. Zhao H. The protective effect of ischemic postconditioning against ischemic injury: from the heart to the brain. J. Neuroimmune Pharmacol. 2007, 2:313-318.
38. Zhao H. Ischemic postconditioning as a novel avenue to protect against brain injury after stroke. J. Cereb. Blood Flow Metab. 2009, 29:873-885.
39. Zhao Z.Q., Corvera J.S., Halkos M.E., Kerendi F., Wang N.P., Guyton R.A., Vinten-Johansen J. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H579-H588.
40. Zhao H., Sapolsky R.M., Steinberg G.K. Interrupting reperfusion as a stroke therapy: ischemic postconditioning reduces infarct size after focal ischemia in rats. J. Cereb. Blood Flow Metab. 2006, 26:1114-1121.
41. Zhao H., Ren C., Chen X., Shen J. From rapid to delayed and remote postconditioning: the evolving concept of ischemic postconditioning in brain ischemia. Curr. Drug Targets 2012, 13:173-187.