Obligatory role of inducible nitric oxide synthase in ischemic preconditioning

Journal of Cerebral Blood Flow and Metabolism

Volumn 25, Issue 4, 2005, Pages 493-501

  Cho, Sunghee ^a   Park, Eun Mi ^a   Zhou, Ping ^a   Frys, Kelly ^a   Ross, M Elizabeth ^a   Iadecola, Costantino ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Division of Neurobiology   (United States)

Author keywords

Aminoguanidine; iNOS null mice; Ischemic preconditioning; Mitochondria

Indexed keywords

AMINOGUANIDINE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; THIONINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN INFARCTION; BRAIN INFARCTION PREVENTION; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN MITOCHONDRION; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; DEPOLARIZATION; DRUG EFFECT; HEART MUSCLE; IMMUNOCYTOCHEMISTRY; LASER DOPPLER FLOWMETRY; MALE; MEMBRANE POTENTIAL; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; MOUSE STRAIN; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION; SIGNAL TRANSDUCTION; STAINING; STATISTICAL SIGNIFICANCE; TISSUE SECTION;

ANIMALS; BRAIN ISCHEMIA; CALCIUM; CAROTID STENOSIS; GUANIDINES; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; ISCHEMIC PRECONDITIONING; LIPOPOLYSACCHARIDES; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II;

EID: 17044374680     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600058     Document Type: Article

References (46)

1. Andersen MF, Sims NR (2000) Improved recovery of highly enriched mitochondrial fractions from small brain tissue samples. Brain Res Brain Res Protoc 5:95-101
2. Argaud L, Gateau-Roesch O, Chalabreysse L, Gomez L, Loufouat J, Thivolet-Bejui F, Robert D, Ovize M (2004) Preconditioning delays Ca2+-induced mitochondrial permeability transition. Cardiovasc Res 61:115-22
3. Atochin DN, Clark J, Demchenko IT, Moskowitz MA, Huang PL (2003) Rapid cerebral ischemic preconditioning in mice deficient in endothelial and neuronal nitric oxide synthases. Stroke 34:1299-303
4. Bolli R (2001) Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: an overview of a decade of research. J Mol Cell Cardiol 33:1897-918
5. Chen J, Graham SH, Zhu RL, Simon RP (1996) Stress proteins and tolerance to focal cerebral ischemia. J Cereb Blood Flow Metab 16:566-77
6. Dave KR, Saul I, Busto R, Ginsberg MD, Sick TJ, Perez-Pinzon MA (2001) Ischemic preconditioning preserves mitochondrial function after global cerebral ischemia in rat hippocampus. J Cereb Blood Flow Metab 21:1401-10
7. Dawn B, Bolli R (2002) Role of nitric oxide in myocardial preconditioning. Ann NY Acad Sci 962:18-41
8. Dawson DA, Furuya K, Gotoh J, Nakao Y, Hallenbeck JM (1999) Cerebrovascular hemodynamics and ischemic tolerance: lipopolysaccharide-induced resistance to focal cerebral ischemia is not due to changes in severity of the initial ischemic insult, but is associated with preservation of microvascular perfusion. J Cereb Blood Flow Metab 19:616-23
9. Dawson TM (2002) Preconditioning-mediated neuroprotection through erythropoietin? Lancet 359:96-7
10. Dirnagl U, Simon RP, Hallenbeck JM (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26:248-54
11. Ehrenreich H, Hasselblatt M, Dembowski C, Cepek L, Lewczuk P, Stiefel M, Rustenbeck HH, Breiter N, Jacob S, Knerlich F, Bohn M, Poser W, Ruther E, Kochen M, Gefeller O, Gleiter C, Wessel TC, De Ryck M, Itri L, Prange H, Cerami A, Brines M, Siren AL (2002) Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 8:495-505
12. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, van der Vilet A (1998) Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391:393-7
13. Fiskum G, Kowaltowksi AJ, Andreyev AY, Kushnareva YE, Starkov AA (2000) Apoptosis-related activities measured with isolated mitochondria and digitonin-permeabilized cells. Methods Enzymol 322:222-34
14. Gidday JM, Shah AR, Maceren RG, Wang Q, Pelligrino DA, Holtzman DM, Park TS (1999) Nitric oxide mediates cerebral ischemic tolerance in a neonatal rat model of hypoxic preconditioning. J Cereb Blood Flow Metab 19:331-40
15. Gonzalez-Zulueta M, Feldman AB, Klesse LJ, Kalb RG, Dillman JF, Parada LF, Dawson TM, Dawson VL (2000) Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc Natl Acad Sci USA 97:436-41
16. Iadecola C, Zhang F, Casey R, Clark HB, Ross ME (1996) Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke 27:1373-80
17. Iadecola C, Zhang F, Casey R, Nagayama M, Ross ME (1997) Delayed reduction in ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 17:9157-64
18. Iadecola C, Zhang F, Xu X (1995a) Inhibition of inducible nitric oxide synthase ameliorates cerebral ischemic damage. Am J Physiol 268:R286-R92
19. Iadecola C, Zhang F, Xu X, Casey R, Ross ME (1995b) Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J Cereb Blood Flow Metab 15:378-84
20. Ischiropoulos H (2003) Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun 305:776-83
21. Kapinya KJ, Lowl D, Futterer C, Maurer M, Waschke KF, Isaev NK, Dirnagl U (2002) Tolerance against ischemic neuronal injury can be induced by volatile anesthetics and is inducible NO synthase dependent. Stroke 33:1889-98
22. Keynes RG, Garthwaite J (2004) Nitric oxide and its role in ischaemic brain injury. Curr Mol Med 4:179-91
23. Kirino T (2002) Ischemic tolerance. J Cereb Blood Flow Metab 22:1283-96
24. Lin T-N, He YY, Wu G, Khan M, Hsu CY (1993) Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24:117-21
25. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399-415
26. Moncayo J, de Freitas GR, Bogousslavsky J, Altieri M, van Meile G (2000) Do transient ischemic attacks have a neuroprotective effect? Neurology 54:2089-94
27. Murphy E (2004) Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection. Circ Res 94:7-16
28. Nagayama M, Niwa K, Nagayama T, Ross ME, Iadecola C (1999) The cyclooxygenase-2 inhibitor NS-398 ameliorates cerebral ischemic injury in wild-type mice but not in mice with deletion of the inducible nitric oxide synthase gene. J Cereb Blood Flow Metab 19:1213-9
29. Nandagopal K, Dawson TM, Dawson VL (2001) Critical role for nitric oxide signaling in cardiac and neuronal ischemic preconditioning and tolerance. J Pharmacol Exp Ther 297:474-8
30. Nogawa S, Zhang F, Ross ME, Iadecola C (1997) Cyclooxygenase-2 gene expression in neurons contributes to ischemic brain damage. J Neurosci 17:2746-55
31. Park E-M, Cho S, Frys K, Racchumi G, Zhou P, Anrather J, Iadecola C (2004a) Interaction between inducible nitric oxide synthase and poly(ADP-ribose) polymerase in focal ischemic brain injury. Stroke 35:2896-901
32. Park L, Anrather J, Forster C, Kazama K, Carlson GA, Iadecola C (2004b) A beta-induced vascular oxidative stress and attenuation of functional hyperemia in mouse somatosensory cortex. J Cereb Blood Flow Metab 24:334-42
33. Sitzer M, Foerch C, Neumann-Haefelin T, Steinmetz H, Misselwitz B, Kugler C, Back T (2004) Transient ischaemic attack preceding anterior circulation infarction is independently associated with favourable outcome. J Neurol Neurosurg Psychiatry 75:659-60
34. Stagliano NE, Perez-Pinzon MA, Moskowitz MA, Huang PL (1999) Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice. J Cereb Blood Flow Metab 19:757-61
35. Stenzel-Poore MP, Stevens SL, Simon RP (2004) Genomics of preconditioning. Stroke 35:2683-6
36. Sugimoto K, Iadecola C (2002) Effects of aminoguanidine on cerebral ischemia in mice: comparison between mice with and without inducible nitric oxide synthase gene. Neurosci Lett 331:25-8
37. 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 748:267-70
38. Tomai F, Crea F, Chiariello L, Gioffre PA (1999) Ischemic preconditioning in humans: models, mediators, and clinical relevance. Circulation 100:559-63
39. Wegener S, Gottschalk B, Jovanovic V, Knab R, Fiebach JB, Schellinger PD, Kucinski T, Jungehulsing GJ, Brunecker P, Muller B, Banasik A, Amberger N, Wernecke KD, Siebler M, Rother J, Villringer A, Weih M (2004) Transient ischemic attacks before ischemic stroke: preconditioning the human brain? A multicenter magnetic resonance imaging study. Stroke 35:616-21
40. Weih M, Kallenberg K, Bergk A, Dirnagl U, Harms L, Wernecke KD, Einhaupl KM (1999) Attenuated stroke severity after prodromal TIA: a role for ischemic tolerance in the brain? Stroke 30:1851-4
41. Wu C, Zhan RZ, Qi S, Fujihara H, Taga K, Shimoji K (2001) A forebrain ischemic preconditioning model established in C57Black/Crj6 mice. J Neurosci Methods 107:101-6
42. Yanamoto H, Xue JH, Miyamoto S, Nagata I, Nakano Y, Murao K, Kikuchi H (2004) Spreading depression induces long-lasting brain protection against infarcted lesion development via BDNF gene-dependent mechanism. Brain Res 1019:178-88
43. Yellon DM, Downey JM (2003) Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83:1113-51
44. Zhan RZ, Fujihara H, Baba H, Yamakura T, Shimoji K (2002) Ischemic preconditioning is capable of inducing mitochondrial tolerance in the rat brain. Anesthesiology 97:896-901
45. Zhang HX, Du GH, Zhang JT (2003) Ischemic preconditioning preserves brain mitochondrial functions during the middle cerebral artery occlusion in rat. Neurol Res 25:471-6
46. Zimmerman GA, Meistrell MI, Bloom O, Cockroft KM, Bianchi M, Risucci D, Broome J, Farmer P, Cerami A, Vlassara H, Tracey KJ (1995) Neurotoxicity of advanced glycation endproducts during focal stroke and neuroprotective effects of aminoguanidine. Proc Natl Acad Sci USA 92:3744-8