Nitric oxide synthase isoforms undertake unique roles during excitotoxicity

Stroke

Volumn 38, Issue 6, 2007, Pages 1938-1945

  Parathath, Susana R ^a   Gravanis, Iordanis ^a   Tsirka, Stella E ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Animal models of human disease; Blood brain barrier; Endothelium vascular type nitric oxide; Excitotoxicity; Neurodegeneration

Indexed keywords

ARGININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOENZYME; KAINIC ACID; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; EXCITOTOXICITY; IMMUNOFLUORESCENCE; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BLOOD-BRAIN BARRIER; EXCITATORY AMINO ACID AGONISTS; ISOENZYMES; KAINIC ACID; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE DEGENERATION; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III;

EID: 34249784535     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/STROKEAHA.106.478826     Document Type: Article

References (45)

1. Naito S, Ueda T. Adenosine triphosphate-dependent uptake of glutamate into protein I-associated synaptic vesicles. J Biol Chem. 1983;258:696-699.
2. Dienel G, Hertz L. Astrocytic contributions to bioenergetics of cerebral ischemia. Glia. 2005;50:362-388.
3. Kimelberg H, Goderie S, Higman S, Pang S, Waniewski R. Swellinginduced release of glutamate, aspartate and taurine from astrocyte cultures. J Neurosci. 1990;10:1583-1591.
4. Dawson T, Bredt D, Fotuhi M, Hwang P, Snyder S. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. PNAS. 1991;88:7797-7801.
5. Stuehr D, Gross S, Sakuma I, Levi R, Nathan C. Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium-derived relaxing factor and the chemical reactivity of nitric oxide. J Exp Med. 1989;169:1011-1020.
6. Lamas S, Marsden P, Li G, Tempst P, Michel T. Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform. PNAS. 1992;89:6348-6352.
7. Parathath S, Parathath S, Tsirka S. Nitric oxide mediates neurodegeneration and breakdown of the blood brain barrier in tPA-dependent excitotoxic injury in mice. J Cell Sci. 2006;119:339-349.
8. Samadani A, Dawson T, Dawson V. Nitric oxide synthase in a model of focal ischemia. Stroke. 1997;28:1283-1288.
9. Wong D, Dorovini-Zis K, Vincent S. Cytokines, nitric oxide, and CGMP modulate the permeability of an in vitro model of the human blood- brain barrier. Exp Neurol. 2004;190:446-455.
10. Dawson V, Kizushi V, Huang P, Snyder S, Dawson T. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthasedeficient mice. J Neurosci. 1996;16:2479-2487.
11. Bal-Price A, Brown GC. Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. J Neurosci. 2001;21:6480-6491.
12. Rogove A, Tsirka S. Neurotoxic responses by microglia elicited by excitotoxic injury in the mouse hippocampus. Curr Biol. 1998;8:19-25.
13. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. PNAS. 1998;95:15769-15774.
14. Carson M. Microglia as liaisons between the immune and central nervous systems. Glia. 2002;40:218-231.
15. Chao CC, Hu S, Molitor TW, Shaskan EG, Petersen PK. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J Immunol. 1992;149:2736-2741.
16. Pou S, Pou WS, Bredt DS, Snyder SH, Rosen GM. Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem. 1992;267:24173-24176.
17. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, Pritchard KA Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. PNAS. 1998;95:9220-9225.
18. 2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. J Biol Chem. 1998;273:25804- 25808.
19. Alderton W, Cooper C, Knowles R. Nitric oxide synthases: structure, function and inhibition. Biochem J. 2001;357:593-615.
20. Pignitter M, Gorren A, Nedeianu S, Schmidt K, Mayer B. Inefficient spin trapping of superoxide in the presence of nitric-oxide: implications for studies on nitric-oxide synthase uncoupling. Free Radic Biol Med. 2006;41:455-463.
21. Xie Z, Wei M, Morgan TE, Fabrizio P, Han D, Finch CE, Longo VD. Peroxynitrite mediates neurotoxicity of amyloid beta-peptide1-42- and lipopolysaccharide-activated microglia. J Neurosci. 2002;22:3484-3492.
22. Mayhan WG, Didion SP. Glutamate-induced disruption of the blood- brain barrier in rats: role of nitric oxide. Stroke. 1996;27:965-970.
23. Mayhan WG. Role of nitric oxide in disruption of the blood-brain barrier during acute hypertension. Brain Res. 1995;686:99-103.
24. Hurst RD, Azam S, Hurst A, Clark JB. Nitric-oxide-induced inhibition of glyceraldehyde-3-phosphate dehydrogenase may mediate reduced endothelial cell monolayer integrity in an in vitro model blood-brain barrier. Brain Res. 2001;894:181-188.
25. Boje KM, Lakhman SS. Nitric oxide redox species exert differential permeability effects on the blood- brain barrier. J Pharmacol Exp Ther. 2000;293:545-550.
26. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC. Targeted disruption of the neuronal nitric oxide synthase gene. Cell. 1993;75: 1273-1286.
27. Laubach VE, Shesely EG, Smithies O, Sherman PA. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharideinduced death. PNAS. 1995;92:10688 -10692.
28. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. PNAS. 1996;93:13176 -13181.
29. Tsirka S, Rogove A, Strickland S. tPA and neuronal death. Nature. 1996;384:123-124.
30. Tsirka S, Gualandris A, Amaral D, Strickland S. Excitotoxin induced neuronal degeneration and seizure are mediated by tissue-type plasminogen activator. Nature. 1995;377:340 -344.
31. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland D, Lawrence D. Tissue-type plasminogen activator induces opening of the blood- brain barrier via the LDL receptor-related protein. J Clin Invest. 2003;112: 1533-1540.
32. Siao C-J, Fernandez SR, Tsirka SE. Cell type-specific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury. J Neurosci. 2003;23:3234 -3242.
33. Forstermann U, Boissel JP, Kleinert H. Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J. 1998;12:773-790.
34. Xia Y, Dawson VL, Dawson TM, Snyder SH, Zweier JL. Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. PNAS. 1996;93: 6770-6774.
35. Zhang Z, Chopp M, Gautam S, Zaloga C, Zhang R, Schmidt H. Upregulation of neuronal nitric oxide synthase and mRNA, and selective sparing of nitric oxide synthase containing neurons after focal cerebral ischemia in rat. Brain Res. 1994;654:85-95.
36. Dawson V, Dawson T, London E, Bredt D, Snyder S. Nitric oxide mediates glutamate neurotoxicity in primary cortical culture. PNAS. 1991;88:6368-6371.
37. Ayata C, Ayata G, Hara H, Matthews RT, Beal MF, Ferrante RJ, Endres M, Kim A, Christie RH, Waeber C, Huang PL, Hyman BT, Moskowitz MA. Mechanisms of reduced striatal NMDA excitotoxicity in type I nitric oxide synthase knock-out mice. J Neurosci. 1997;17:6908-6917.
38. Schulz JB, Mathews RT, Jenkins BG, Ferrante RJ, Siwek D, Henshaw DR, Cipolloni PB, Mecocci P, Kowall NW, Rosen BR, et al. Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. J Neurosci. 1995;15:8419-8429.
39. Endres M, Laufs U, Liao JK, Moskowitz MA. Targeting eNOS for stroke protection. TINS. 2004;27:283-289.
40. Amin-Hanjani S, Stagliano NE, Yamada M, Huang PL, Liao JK, Moskowitz MA. Mevastatin, an HMG CoA reductase inhibitor, reduces stroke damage and upregulates endothelial nitric oxide synthase in mice. Stroke. 2001;32:980 -986.
41. Huang Z, Huang PL, Ma J, Meng W, Ayata C, Fishman MC, Moskowitz MA. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J Cereb Blood Flow Metab. 1996;16: 981-987.
42. Stauss HM, Godecke A, Mrowka R, Schrader J, Persson PB. Enhanced blood pressure variability in eNOS knockout mice. Hypertension. 1999; 33:1359 -1363.
43. Iwase K, Miyanaka K, Shimizu A, Nagasaki A, Gotoh T, Mori M, Takiguchi M. Induction of endothelial nitric-oxide synthase in rat brain astrocytes by systemic lipopolysaccharide treatment. J Biol Chem. 2000; 275:11929 -11933.
44. Dinerman J, Dawson T, Schell M, Snowman A, Snyder S. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. PNAS. 1994;91:4214-4218.
45. Montecot C, Borredon J, Seylaz J, Pinard E. Nitric oxide of neuronal origin is involved in cerebral blood flow increase during seizures induced by kainate. J Cereb Blood Flow Metab. 1997;17:94 -99.