Inducible nitric oxide synthase does not mediate brain damage after transient focal cerebral ischemia in mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 28, Issue 3, 2008, Pages 526-539

  Prüss, Harald ^a   Prass, Konstantin ^a,b   Ghaeni, Leyli ^a   Milosevic, Milan ^a   Muselmann, Claudia ^a   Freyer, Dorette ^a   Royl, Georg ^a   Reuter, Uwe ^a   Baeva, Nevena ^a   Dirnagl, Ulrich ^a   Meisel, Andreas ^a   Priller, Josef ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Landesklinikum Waldviertel ^*  (Austria)

Author keywords

Bone marrow transplantation; Gene expression; Inflammation; INOS; Knockout mouse; Middle cerebral artery occlusion

Indexed keywords

GREEN FLUORESCENT PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; BRAIN DAMAGE; BRAIN ISCHEMIA; BRAIN SIZE; CELL STIMULATION; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MEASUREMENT; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ALTERNATIVE SPLICING; ANIMALS; BRAIN CHEMISTRY; BRAIN ISCHEMIA; EXONS; ISCHEMIC ATTACK, TRANSIENT; LUNG; MICE; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE II; RNA, MESSENGER; UP-REGULATION;

EID: 39749136078     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.jcbfm.9600550     Document Type: Article

References (37)

1. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593-615
2. Beray-Berthat V, Palmier B, Plotkine M, Margaill I (2003) Neutrophils do not contribute to infarction, oxidative stress, and NO synthase activity in severe brain ischemia. Exp Neurol 182:446-54
3. Cash D, Beech JS, Rayne RC, Bath PMW, Meldrum BS, Williams SCR (2001) Neuroprotective effect of aminoguanidine on transient focal ischaemia in the rat brain. Brain Res 905:91-103
4. Cohen J (1988) Statistical power analysis for the behavioral sciences (2nd ed), New York: Academic Press
5. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischemic stroke: an integrated view. Trends Neurosci 22:391-7
6. Dirnagl U, Simon RP, Hallenbeck JM (2003) Ischemic tolerance and endogenous neuroprotection. Trends Neurosci 26:248-54
7. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I, Kindy MS, Wise PM (2001) Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci USA 98:1952-7
8. Eissa NT, Strauss AJ, Haggerty CM, Choo EK, Chu SC, Moss J (1996) Alternative splicing of human inducible nitric-oxide synthase mRNA. J Biol Chem 271:27184-7
9. Eissa NT, Yuan JW, Haggerty CM, Choo EK, Palmer CD, Moss J (1998) Cloning and characterization of human inducible nitric oxide synthase splice variants: a domain, encoded by exons 8 and 9, is critical for dimerization. Proc Natl Acad Sci USA 95:7625-30
10. Emerich DF, Dean RL, III, Bartus RT (2002) The role of leukocytes following cerebral ischemia: pathogenic variable or bystander reaction to emerging infarct? Exp Neurol 173:168-81
11. Freyer D, Manz R, Ziegenhorn A, Weih M, Angstwurm K, Döcke WD, Meisel A, Schumann RR, Schönfelder G, Dirnagl U, Weber JR (1999) Cerebral endothelial cells release TNF-alpha after stimulation with cell walls of Streptococcus pneumoniae and regulate inducible nitric oxide synthase and ICAM-1 expression via autocrine loops. J Immunol 163:4308-14
12. Fujii M, Hara H, Meng W, Vonsattel JP, Huang Z, Moskowitz MA (1997) Strain-related differences in susceptibility to transient forebrain ischemia in SV-129 and C57black/6 mice. Stroke 28:1805-11
13. Galea E, Golanov EV, Feinstein DL, Kobylarz KA, Glickstein SB, Reis DJ (1998) Cerebellar stimulation reduces inducible nitric oxide synthase expression and protects brain from ischemia. Am J Physiol 274: H2035-45
14. Gibson CL, Coughlan TC, Murphy SP (2005) Glial nitric oxide and ischemia. Glia 50:417-26
15. Huang CY, Fujimura M, Noshita N, Chang YY, Chan PH (2001) SOD1 down-regulates NF-kappaB and c-Myc expression in mice after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21:163-73
16. Iadecola C, Xu X, Zhang F, el-Fakahany EE, Ross ME (1995) Marked induction of calcium-independent nitric oxide synthase activity after focal cerebral ischemia. J Cereb Blood Flow Metab 15:52-9
17. 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
18. Iadecola C, Zhang F, Casey R, Nagayama M, Ross ME (1997) Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 17:9157-64
19. Ivey NS, Martin EN, Jr, Scheld WM, Nathan BR (2005) A new method for measuring blood-brain barrier permeability demonstrated with Europium-bound albumin during experimental lipopolysaccharide (LPS) induced meningitis in the rat. J Neurosci Methods 142:91-5
20. Keynes RG, Garthwaite J (2004) Nitric oxide and its role in ischemic brain injury. Curr Mol Med 4:179-91
21. Laubach VE, Shesely EG, Smithies O, Sherman PA (1995) Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc Natl Acad Sci USA 92:10688-92
22. Lee CM, Robinson LJ, Michel T (1995) Oligomerization of endothelial nitric oxide synthase. J Biol Chem 270:27403-6
23. Lerouet D, Jafarian-Tehrani M, Louin G, Palmier B, Bonnefont-Rousselot D, Plotkine M, Margaill I (2005) Lack of iNOS induction in a severe model of transient focal cerebral ischemia in rats. Exp Neurol 195:218-28
24. Loihl AK, Asensio V, Campbell IL, Murphy J (1999) Expression of nitric oxide synthase (NOS)-2 following permanent focal ischemia and the role of nitric oxide in infarct generation in male, female and NOS-2 gene-deficient mice. Brain Res 830:155-64
25. MacMicking JD, Nathan C, Hom G, Chartrain N, Fletcher DS, Trumbauer M, Stevens K, Xie QW, Sokol K, Hutchinson N, Chen H, Mudgett JS (1995) Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81:641-50
26. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902
27. Moro MA, Cárdenas A, Hurtado O, Leza JC, Lizasoain I (2004) Role of nitric oxide after brain ischaemia. Cell Calcium 36:265-75
28. Ou P, Wolff SP (1993) Aminoguanidine: a drug proposed for prophylaxis in diabetes inhibits catalase and generates hydrogen peroxide in vitro. Biochem Pharmacol 46:1139-44
29. Prass K, Meisel C, Hoflich C, Braun J, Halle E, Wolf T, Ruscher K, Victorov IV, Priller J, Dirnagl U, Volk HD, Meisel A (2003) Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by post-stroke T helper cell type 1-like immunostimulation. J Exp Med 198:725-36
30. Prass K, Royl G, Lindauer U, Freyer D, Megow D, Dirnagl U, Stockler-Ipsiroglu G, Wallimann T, Priller J (2007) Improved reperfusion and neuroprotection by creatine in a mouse model of stroke. J Cereb Blood Flow Metab 27:452-9
31. Priller J, Flügel A, Wehner T, Boentert M, Haas CA, Prinz M, Fernández-Klett F, Prass K, Bechmann I, de Boer BA, Frotscher M, Kreutzberg GW, Persons DA, Dirnagl U (2001) Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat Med 7:1356-61
32. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, Sawitzki B, Priller J, Dirnagl U, Meisel A (2002) Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22:10291-301
33. Schroeter M, Küry P, Jander S (2003) Inflammatory gene expression in focal cortical brain ischemia: differences between rats and mice. Mol Brain Res 117:1-7
34. Storini C, Rossi E, Marrella V, Distaso M, Veerhuis R, Vergani C, Bergamaschini L, De Simoni MG (2005) C1-inhibitor protects against brain ischemia-reperfusion injury via inhibition of cell recruitment and inflammation. Neurobiol Dis 19:10-7
35. Tiscornia AC, Cayota A, Bandoni AI, Brito C, Oppezzo P, Vuillier P, Robello C, Dighiero G, Gabùs R, Pritsch O (2004) Post-transcriptional regulation of inducible nitric oxide synthase in chronic lymphocytic leukemia B cells in pro- and antiapoptotic culture conditions. Leukemia 18:48-56
36. Yoshida T, Waeber C, Huang Z, Moskowitz MA (1995) Induction of nitric oxide synthase activity in rodent brain following middle cerebral artery occlusion. Neurosci Let 194:214-8
37. Zhu DY, Liu SH, Sun HS, Lu YM (2003) Expression of inducible nitric oxide synthase after focal cerebral ischemia stimulates neurogenesis in the adult rodent dentate gyrus. J Neurosci 23:223-9