Nitric oxide production and perivascular tyrosine nitration following focal ischemia in neonatal rat

Journal of Neurochemistry

Volumn 70, Issue 6, 1998, Pages 2516-2525

  Coeroli, L ^a   Renolleau, S ^a   Arnaud, S ^a   Plotkine, D ^a   Cachin, N ^a   Plotkine, M ^b   Ben Ari, Y ^a   Charriaut Marlangue, C ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b FACULTÉ DES SCIENCES PHARMACEUTIQUES ET BIOLOGIQUES   (France)

Author keywords

Neonatal ischemia; Nitric oxide; Nitrotyrosine; Peroxynitrite; Reperfusion

Indexed keywords

NITRIC OXIDE; OXYGEN RADICAL; PEROXYNITRITE; TYROSINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; NEWBORN; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RAT; VASCULAR ENDOTHELIUM;

ANIMALIA; ARACHNOIDEA;

EID: 0031745288     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70062516.x     Document Type: Article

References (71)

1. Ashwal S., Cole D., Osborne S., Osborne T., and Pearce W. (1995a) L-NAME reduces infarct volume in a filament model of transient middle cerebral artery occlusion in the rat pup. Pediatr. Res. 38, 652-656.
2. Ashwal S., Cole D., Osborne S., Osborne T., and Pearce W. (1995b) A new model of neonatal stroke: reversible middle cerebral artery occlusion in the rat pup. Pediatr. Neurol. 12, 191-196.
3. Barone F., Hilegass L., Price W., White R., Lee E., Feuerstein G., Sarau H., Clark R., and Griswold D. (1991) Polymorphonuclear leukocyte infiltration into cerebral focal ischemic tissue: myeloperoxidase activity assay and histologic verification. J. Neurol. Res. 29, 336-345.
4. Beckman J. S., Beckman T. W., Chen J., and Marshall P. A. (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87, 1620-1624.
5. Beckman J., Chen J., Ischiropoulos H., and Crow J. (1994) Oxidative chemistry of peroxynitrite. Methods Enzymol. 233, 229-240.
6. Beckman J., Ye Y., Chen J., and Conger K. (1996) The interactions of nitric oxide with oxygen radicals and scavengers in cerebral ischemic injury, in Advances in Neurology, Vol. 71: Cellular and Molecular Mechanisms of Ischemic Brain Damage (Siesjö B. K. and Wieloch T., eds), pp. 339-354. Lippincott-Raven, Philadelphia.
7. Betz A. L. (1985) Identification of hypoxanthine transport and xanthine oxidase activity in brain capillaries. J. Neurochem. 44, 574-579.
8. Bidmon H., Wu J., Buchkremer-Ratzmann I., Mayer B., Witte O., and Zilles K. (1997) Transient changes in the presence of nitric-oxide synthases and nitrotyrosine immunoreactivity after focal cortical lesions. Neuroscience 82, 377-395.
9. Bolaños J. P., Almeida A., Stewart V., Peuchen S., Land J., Clark J. B., and Heales S. J. R. (1997) Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases. J. Neurochem. 68, 2227-2240.
10. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and Lipton S. (1995) Apoptosis and necrosis: two distinct events induced by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92, 7162-7166.
11. Chan P. (1994) Oxygen radicals in focal cerebral ischemia. Brain Pathol. 4, 59-65.
12. Charriaut-Marlangue C., Renolleau S., Plotkine M., and Ben-Ari Y. (1997) Neuronal apoptosis in a new model of transient unilateral focal ischemia in rat pups. (Abstr.) J. Cereb. Blood Flow Metab. 17 (Suppl.), S729.
13. Chopp M., Zhang R., and Jiang N. (1996) The role of adhesion molecules in reducing cerebral ischemic cell damage, Advances in Neurology, Vol. 71: Cellular and Molecular Mechanisms of Ischemic Brain Damage (Siesjö B. K. and Wieloch T., eds), pp. 315-327. Lippincott-Raven, Philadelphia.
14. Crow J. and Beckman J. (1995) The role of peroxynitrite in nitric oxide-mediated toxicity. Curr. Top. Microbiol. Immunol. 196, 57-73.
15. Culcasi M., Lafon-Cazal M., Pietri S., and Bockaert J. (1994) Glutamate receptors induce a burst of superoxide via activation of nitric oxide synthase in arginine-depleted neurons. J. Biol. Chem. 269, 12589-12593.
16. Daugherty A., Dunn J., Rateri D., and Heinecke J. (1994) Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J. Clin. Invest. 94, 437-444.
17. Dawson V. (1991) Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88, 6368-6371.
18. Dawson V. (1994) Nitric oxide and focal cerebral ischemia: multiplicity of actions and diverse outcome. Cerebrovasc. Brain Metab. Rev. 6, 299-324.
19. Dawson V., Dawson T., Uhl G., and Snyder S. (1993) Human immunodeficiency virus type 1 coat protein neurotoxicity mediated by nitric oxide in primary cortical cultures. Proc. Natl. Acad. Sci. USA 90, 3256-3259.
20. Dijkstra C., Döpp E., Joling P., and Kraal G. (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54, 589-599.
21. Floy R. and Carney J. (1992) Free radical damage to protein and DNA: mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann. Neurol. 32 (Suppl.), S22-S27.
22. Garcia J., Yoshida Y., Chen H., Li Y., Zhang Z., Lian J., Chen S., and Chopp M. (1993) Progression from ischemic injury to infarct following middle cerebral artery occlusion in the rat. Am. J. Pathol. 142, 623-635.
23. Garthwaite J., Garthwaite G., Palmer R., and Moncada S. (1989) NMDA receptor activation induces nitric oxide synthesis from arginine in rat brain slices. Eur. J. Pharmacol. 172, 413-416.
24. Haddad I., Pataki G., Hu P., Galliani C., and Beckman J. (1994) Quantification of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. J. Clin. Invest. 94, 2407-2413.
25. Hall N., Carney J., Cheng M., and Butterfield D. (1995) Prevention of ischemia-reperfusion-induced alterations in synaptosomal membrane-associated proteins and lipids by N-tert-butyl-alpha-phenylnitrone and difluoromethylornithine. Neuroscience 69, 591-600.
26. Heiss W., Huber M., Fink G., Pietrzyk U., Wagner R., and Weinhard K. (1992) Progressive derangement of periinfarct viable tissue in ischemic stroke. J. Cereb. Blood Flow Metab. 12, 193-203.
27. Hogg N., Darley-Usmar V., Wilson M., and Moncada S. (1992) Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem. J. 281, 419-424.
28. Huang Z., Huang P., Panahian N., Dalkara T., Fishman M., and Moskowitz M. (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265, 1883-1885.
29. Hudome S., Palmer C., Roberts R., Mauger D., Housman C., and Towfighi J. (1997) The role of neutrophils in the production of hypoxic-ischemic brain injury in the neonatal rat. Pediatr. Res. 41, 607-616.
30. Huie R. and Padjama S. (1993) The reaction of NO with superoxide. Free Radic. Res. Commun. 18, 195-199.
31. Iadecola C., Xu X., Zhang F., El-Fakahany E., and Ross M. (1995a) Marked induction of calcium-independent nitric oxide synthase activity after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 15, 52-59.
32. Iadecola C., Zhang F., Xu S., Casey R., and Ross M. (1995b) Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J. Cereb. Blood Flow Metab. 15, 378-384.
33. Iadecola C., Zhang F., Casey R., Clark B., and Ross E. (1996) Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke 27, 1373-1380.
34. Iadecola C., Zhang F., Casey R., Nagamaya M., and Ross M. (1997) Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J. Neurosci. 17, 9157-9164.
35. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J., Smith C., and Beckman J. (1992) Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298, 431-437.
36. Kajiwara K., Ito H., and Fukumoto T. (1990) Lymphocyte infiltration into normal rat brain following hyperosmotic blood-brain barrier opening. J. Neuroimmunol. 27, 133-140.
37. Kinouchi H., Epstein C., Mizui T., Carlson E., Chen S., and Chan P. (1991) Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc. Natl. Acad. Sci. USA 88, 11158-11162.
38. Kinuta Y., Kimura M., Itokawa Y., Ishikawa M., and Kikuchi H. (1989a) Changes in xanthine oxidase in ischemic rat brain. J. Neurosurg. 71, 417-420.
39. Kinuta Y., Kikuchi H., Ishikawa M., Kimura M., and Itokawa Y. (1989b) Lipid peroxidation in focal cerebral ischemia. J. Neurosurg. 71, 421-429.
40. Kinuta Y., Kikuchi H., and Ishikawa M. (1990) Ischaemic brain oedema and xanthine-xanthine oxidase system. Acta Neurochir. (Wien) 51, 192-194.
41. Kochanek P. and Hallenbeck J. (1992) Polymorphonuclear leukocytes and monocytes/macrophages in the pathogenesis of cerebral ischemia and stroke. Stroke 23, 1367-1379.
42. Kondo T., Reaume A., Huang T., Carlson E., Murakami K., Chen S., Hoffman E., Scott R., Epstein C., and Chan P. (1997) Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema after transient focal cerebral ischemia. J. Neurosci. 17, 4180-4189.
43. Kumura E., Yoshimine T., Iwatsuki K., Yamanaka K., Tanaka S., Hayakawa T., Shiga T., and Kosaka H. (1996) Generation of nitric oxide and superoxide during reperfusion after focal ischemia in rats. Am. J. Physiol. 270, C748-C752.
44. Lin K., Xue J.-Y., Nomen M., Spur B., and Wong P.-K. (1995) Peroxynitrite-induced apoptosis in HL-60. J. Biol. Chem. 270, 16487-16490.
45. Liu T., Beckman J., Freeman B., Hogan E., and Hsu C. (1989) Polyethylene glycol-conjugated superoxide dismutase and catalase reduce ischemic brain injury. Am. J. Physiol. 256, H589-H593.
46. Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-272.
47. Margaill I., Allix M., Boulu R., and Plotkine M. (1997) Dose- and time-dependent L-NAME neuroprotection in transient focal cerebral ischaemia in rats. Br. J. Pharmacol. 120, 160-163.
48. Morioka T., Kalehua A., and Streit W. (1992) Progressive expression of immunomolecules on microglial cells in rat dorsal hippocampus following transient forebrain ischemia. Acta Neuropathol. (Berl.) 83, 149-157.
49. Morris S. and Billiar T. (1994) New insights into the regulation of inducible nitric oxide synthesis. Am. J. Physiol. 266, E829-E839.
50. Pellegrini-Giampietro D., Cozzi A., and Moroni F. (1994) The glycine antagonist and free radical scavenger 7-Cl-thio-kynurenate reduces CA1 ischemic damage in the gerbil. Neuroscience 63, 701-709.
51. Radi R., Beckman J., Bush K., and Freeman B. (1991) Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J. Biol. Chem. 266, 4244-4250.
52. Renolleau S., Benjelloun N., Ben-Ari Y., and Charriaut-Marlangue C. (1997) Regulation of apoptosis-associated proteins in cell death following transient focal ischemia in rat pup. Apoptosis 2, 368-376.
53. Rodenas J., Mitjavila M., and Carbonell T. (1995) Simultaneous generation of nitric oxide and superoxide by inflammatory cells in rats. Free Radic. Biol. Med. 18, 869-875.
54. Rubbo H., Radi R., Trujillo M., Telleri R., Kalyanaraman B., Barnes S., Kirk M., and Freeman B. (1994) Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. J. Biol. Chem. 269, 26066-26075.
55. Sampei K., Asano Y., Mandir A., Wong P., Traystman R., Dawson V., Dawson T., and Hum P. (1997) Stroke outcome in antioxidant transgenics: nNOS, Cu-Zn superoxide dismutase and combined mutants. (Abstr.) J. Cereb. Blood Flow Metab. 17 (Suppl.), S454.
56. Slater A., Nobel C., and Orrenius S. (1995) The role of intracellular oxidants in apoptosis. Biochim. Biophys. Acta 1271, 59-62.
57. Stamler J. (1994) Redox signalling: nitrotyrosylation and related target interactions of nitric oxide. Cell 78, 931-936.
58. Taylor G., Trescher W., Johnston M., and Traystman R. (1995) Experimental neuronal injury in the newborn lamb: a comparison of N-methyl-D-aspartic acid receptor blockade and nitric oxide synthesis inhibition on lesion size and cerebral hyperemia. Pediatr. Res. 38, 644-651.
59. Terada L., Willingham I., Rosandich M., Leff J., Kindt G., and Repine J. (1991) Generation of superoxide anion by brain endothelial cell xanthine oxidase. J. Cell. Physiol. 148, 191-196.
60. Thordstein M., Bågenholm R., Thiringer K., and Kjellmer I. (1993) Scavengers of free oxygen radicals in combination with magnesium ameliorate perinatal hypoxic-ischemic brain damage in the rat. Pediatr. Res. 34, 23-26.
61. Thorn S. (1993) Leukocytes in carbon monoxide-mediated brain oxidative injury. Toxicol. Appl. Pharmacol. 123, 234-247.
62. Tuor U., Bigio M., and Chumas P. (1996) Brain damage due to cerebral hypoxia/ischemia in the neonate: pathology and pharmacological modification. Cerebrovasc. Brain Metab. Rev. 8, 159-193.
63. van der Vliet A., O'Neil C., Halliwell B., Cross C., and Kaur H. (1994) Aromatic hydroxylation and nitration of phenylalanine and tyrosine by peroxynitrite. Evidence for hydroxyl radical production from peroxynitrite. FEBS Lett. 339, 89-92.
64. van der Vliet A., Eiserich J., Kaur H., Cross C. and Halliwell B. (1996) Nitrotyrosine as biomarker for reactive nitrogen species. Methods Enzymol. 269, 175-184.
65. van der Vliet A., Eiserich J., Halliwell B., and Cross C. (1997) Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272, 7617-7625.
66. Verrechia C., Boulu R., and Plotkine M. (1995) Neuroprotective and deleterious effects of nitric oxide on focal cerebral ischemia-induced neurone death. Adv. Neuroimmunol. 5, 359-378.
67. Williams L., Oostveen J., Hall E., Jolly R., Satoh P., and Petry T. (1996) Cyclophosphamide is neuroprotective in a gerbil model of transient severe focal cerebral ischemia: correlation with effects of tirilazad mesylate (U-74006F). J. Neurotrauma 13, 103-113.
68. Yang G., Chan P., Chen J., Carlson E., Chen S., Weinstein P., Epstein C., and Kamii H. (1994) Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke 25, 165-170.
69. Ye Y., Strong M., Huang Z., and Beckman J. (1996) Antibodies that recognize nitrotyrosine. Methods Enzymol. 269, 201-209.
70. Yoshida T., Waeber C., Huang Z., and Moskowitz M. (1995) Induction of nitric oxide synthase activity in rodent brain following middle cerebral artery occlusion. Neurosci. Lett. 194, 214-218.
71. Zhang J., Dawson V., Dawson T., and Snyder S. (1994) Nitric oxide activation of poly(ADP-ribose) synthase in neurotoxicity. Science 263, 687-689.