Cogprints

Delayed treatment with nimesulide reduces measures of oxidative stress following global ischemic brain injury in gerbils

Candelario-Jalil, Eduardo and Alvarez, Dalia and Merino, Nelson and Leon, Olga S. (2003) Delayed treatment with nimesulide reduces measures of oxidative stress following global ischemic brain injury in gerbils. [Journal (Paginated)]

Full text available as:

[img]
Preview
PDF
117Kb

Abstract

Metabolism of arachidonic acid by cyclooxygenase is one of the primary sources of reactive oxygen species in the ischemic brain. Neuronal overexpression of cyclooxygenase-2 has recently been shown to contribute to neurodegeneration following ischemic injury. In the present study, we examined the possibility that the neuroprotective effects of the cyclooxygenase-2 inhibitor nimesulide would depend upon reduction of oxidative stress following cerebral ischemia. Gerbils were subjected to 5 min of transient global cerebral ischemia followed by 48 h of reperfusion and markers of oxidative stress were measured in hippocampus of gerbils receiving vehicle or nimesulide treatment at three different clinically relevant doses (3, 6 or 12 mg/kg). Compared with vehicle, nimesulide significantly (P<0.05) reduced hippocampal glutathione depletion and lipid peroxidation, as assessed by the levels of malondialdehyde (MDA), 4-hydroxy-alkenals (4-HDA) and lipid hydroperoxides levels, even when the treatment was delayed until 6 h after ischemia. Biochemical evidences of nimesulide neuroprotection were supported by histofluorescence findings using the novel marker of neuronal degeneration Fluoro-Jade B. Few Fluoro-Jade B positive cells were seen in CA1 region of hippocampus in ischemic animals treated with nimesulide compared with vehicle. These results suggest that nimesulide may protect neurons by attenuating oxidative stress and reperfusion injury following the ischemic insult with a wide therapeutic window of protection.

Item Type:Journal (Paginated)
Keywords:oxidative stress; cerebral ischemia; glutathione; lipid peroxidation; nimesulide; cyclooxygenase-2; Fluoro-Jade B; neurodegeneration; prostaglandin E2; stroke
Subjects:Neuroscience > Neurochemistry
ID Code:5642
Deposited By:Candelario-Jalil, Dr Eduardo
Deposited On:20 Aug 2007
Last Modified:11 Mar 2011 08:56

References in Article

Select the SEEK icon to attempt to find the referenced article. If it does not appear to be in cogprints you will be forwarded to the paracite service. Poorly formated references will probably not work.

1. Anderson, M.E., 1985. Determination of glutathione and glutathione disulfide in biological samples. Meth. Enzymol. 113, 548-555.

2. Bezzi, P., Carmignoto, G., Pasti, L., Vesce, S., Rossi, D., Rizzini, B.L., Pozzan, T., Volterra A., 1998. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391, 281-285.

3. Busija, D.W., Bari, F., Degi, R., Domoki, F., Veltkamp, R., Louis, T.M., Thrikawala, N., Robins, G., 1998. Pathophysiology of COX-2 and NOS-derived metabolites and free radicals during brain ischemia. In: Krieglstein J. (Ed.), Pharmacology of Cerebral Ischemia, Wissenschaftliche Verlagsgesellschaft GmbH., Stuttgart, pp. 237-241.

4. Candelario-Jalil, E., Ajamieh, H.H., Sam, S., Martínez, G., León, O.S., 2000. Nimesulide limits kainate-induced oxidative damage in the rat hippocampus. Eur. J. Pharmacol. 390, 295-298.

5. Candelario-Jalil, E., Alvarez, D., Castañeda, J.M., Al-Dalain, S.M., Martínez, G., Merino, N., León, O.S., 2002a. The highly selective cyclooxygenase-2 inhibitor DFU is neuroprotective when given several hours after transient cerebral ischemia in gerbils. Brain Res. 927, 212-215.

6. Candelario-Jalil, E., Alvarez, D., González-Falcón, A., García-Cabrera, M., Martínez-Sánchez, G., Merino, N., Giuliani, A., León, O.S., 2002b. Neuroprotective efficacy of nimesulide against hippocampal neuronal damage following transient forebrain ischemia. Eur. J. Pharmacol. 453, 189-195.

7. Candelario-Jalil, E., González, A., García, M., León, O.S., Springer J.E., 2002c. Involvement of cyclooxygenase-2 in blood-brain barrier damage and leukocyte infiltration following transient focal cerebral ischemia in rats. Soc. Neurosci. Abstr. 28, 580.10.

8. Candelario-Jalil, E., Mhadu, N.H., Al-Dalain, S.M., Martínez, G., León, O.S., 2001. Time course of oxidative damage in different brain regions following transient cerebral ischemia in gerbils. Neurosci. Res. 41, 233-241.

9. Cernak, I., O´Connor, C., Vink, R., 2001. Activation of cyclo-oxygenase-2 contributes to motor and cognitive dysfunction following diffuse traumatic brain injury in rats. Clin. Exp. Pharmacol. Physiol. 28, 922-925.

10. Cernak, I., O'Connor, C., Vink, R., 2002. Inhibition of cyclooxygenase 2 by nimesulide improves cognitive outcome more than motor outcome following diffuse traumatic brain injury in rats. Exp. Brain Res. 147, 193-199.

11. Chabrier, P.E., Auguet, M., Spinnewyn, B., Auvin, S., Cornet, S., Demerle-Pallardy, C., Guilmard-Favre, C., Marin, J.G., Pignol, B., Guillard-Roubert, V., Roussillot-Charnet, C., Schulz, J., Viossat, I., Bigg, D., Moncada, S., 1999. BN 80933, a dual inhibitor of neuronal nitric oxide synthase and lipid peroxidation: a promising neuroprotective strategy. Proc. Natl. Acad. Sci. USA 96, 10824-10829.

12. Chan P.H., 2001. Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metab. 21, 2-14.

13. Coyle, J.T., Puttfarcken, P., 1993. Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695.

14. Cullen, L., Kelly, L., Connor, S.O., Fitzgerald, D.J., 1998. Selective cyclooxygenase-2 inhibition by nimesulide in man. J. Pharmacol. Exp. Ther. 287, 578-582.

15. Domoki, F., Perciaccante, J.V., Puskar, M., Bari, F., Busija, D.W., 2001. Cyclooxygenase-2 inhibitor NS398 preserves neuronal function after hypoxia/ischemia in piglets. Neuroreport 12, 4065-4068.

16. Dugan, L.L., Sensi, S.L., Canzoniero, L.M., 1995. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15, 6377-6388.

17. Facchinetti, F., Dawson, V.L., Dawson, T.M., 1998. Free radicals as mediators of neuronal injury. Cell Mol. Neurobiol. 18, 667-682.

18. Floreani, M., Skaper, S.D., Facci, L., Lipartiti, M., Giusti, P., 1997. Melatonin maintains glutathione homeostasis in kainic acid-exposed rat brain tissues. FASEB J. 11, 1309-1315.

19. Gay, C., Collins, J., Gebicki, J.M., 1999. Hydroperoxide assay with the ferric-xylenol orange complex. Anal. Biochem. 273, 149-155.

20. Hall, E.D., Andrus, P.K., Althaus, J.S., VonVoigtlander, P.F., 1993. Hydroxyl radical production and lipid peroxidation parallels selective post-ischemic vulnerability in gerbil brain. J. Neurosci. Res. 34, 107-112.

21. Hall, E.D., Oostveen, J.A., Andrus, P.K., Anderson, D.K., Thomas, C.E., 1997. Immunocytochemical method for investigating in vivo neuronal oxygen radical-induced lipid peroxidation. J. Neurosci. Meth. 76, 115-122.

22. Halliwell, B., Gutteridge, J.M.C., 1985. Oxygen radicals and the nervous system. Trends Neurosci. 8, 22-29.

23. Hewett, S.J., Uliasz, T.F., Vidwans, A.S., Hewett, J.A., 2000. Cyclooxygenase-2 contributes to N-methyl-D-aspartate-mediated neuronal cell death in primary cortical cell culture. J. Pharmacol. Exp. Ther. 293, 417-425.

24. Iadecola, C., Alexander, M., 2001. Cerebral ischemia and inflammation. Curr. Opin. Neurol. 14, 89-94.

25. Iadecola, C., Forster, C., Nogawa, S., Clark, H.B., Ross, M.E., 1999. Cyclooxygenase-2 immunoreactivity in the human brain following cerebral ischemia. Acta Neuropathol. (Berl.) 98, 9-14.

26. Iadecola, C., Niwa, K., Nogawa, S., Zhao, X., Nagayama, M., Araki, E., Morham, S., Ross, M., 2001. Reduced susceptibility to ischemic brain injury and NMDA-mediated neurotoxicity in cyclooxygenase-2-deficient mice. Proc. Natl. Acad. Sci. USA 98, 1294-1299.

27. Katsuki, H., Okuda S., 1995. Arachidonic acid as a neurotoxic and neurotrophic substance. Prog. Neurobiol. 46, 607–636.

28. Keller, J., Mark, R., Bruce, A., Blanc, E., Rothstein, J., Uchida, K., Mattson, M., 1997. 4-hydroxynonenal, an aldehydic product of membrane lipid peroxidation, impairs glutamate transport and mitochondrial function in synaptosomes. Neuroscience 80, 685-696.

29. Kelley, K.A., Ho, L., Winger, D., Freire-Moar, J., Borelli, C.B., Aisen, P.S., Pasinetti, G.M., 1999. Potentiation of excitotoxicity in transgenic mice overexpressing neuronal cyclooxygenase-2. Am. J. Pathol. 155, 995-1004.

30. Kirino, T., 1982. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239, 57-69.

31. Kitagawa, K., Matsumoto, M., Oda, T., Niinobe, M., Hata, R., Handa, N., Fukunaga, R., Isaka, Y., Kimura, K., Maeda, H., 1990. Free radical generation during brief period of cerebral ischemia may trigger delayed neuronal death. Neuroscience 35, 551-558.

32. Koistinaho, J., Koponen, S., Chan, P.H., 1999. Expression of cyclooxygenase-2 mRNA after global ischemia is regulated by AMPA receptors and glucocorticoids. Stroke 30, 1900-1906.

33. Liu, P.K., 2003. Ischemia-reperfusion-related repair deficit after oxidative stress: implications of faulty transcripts in neuronal sensitivity after brain injury. J. Biomed. Sci. 10, 4-13.

34. Lyeth, B.G., Gong, Q.Z., Shields, S., Muizelaar, J.P., Berman R.F., 2001. Group I Metabotropic Glutamate Antagonist Reduces Acute Neuronal Degeneration and Behavioral Deficits after Traumatic Brain Injury in Rats. Exp. Neurol. 169, 191-199.

35. Marnett, L., Rowlinson, S., Goodwin, D., Kalgutkar, A., Lanzo, C., 1999. Arachidonic acid oxygenation by COX-1 and COX-2. Mechanisms of catalysis and inhibition. J. Biol. Chem. 274, 22903-22906.

36. Martínez, G., Candelario-Jalil, E., Giuliani, A., León, O.S., Sam, S., Delgado, R., Núñez-Sellés, A.J., 2001. Mangifera indica L. extract (QF808) reduces ischemia -induced neuronal loss and oxidative damage in the gerbil brain. Free Radic. Res. 35, 465-473.

37. Mattson, M.P., 1998. Modification of ion homeostasis by lipid peroxidation: roles in neuronal degeneration and adaptive plasticity. Trends Neurosci. 20, 53-57.

38. Miettinen, S., Fusco, F.R., Yrjanheikki, J., Keinanen, R., Hirvonen, T., Roivainen, R., Narhi, M., Hokfelt, T., Koistinaho, J., 1997. Spreading depression and focal brain ischemia induce cyclooxygenase-2 in cortical neurons through N-methyl-D-aspartic acid-receptors and phospholipase A2. Proc. Natl. Acad. Sci. USA 94, 6500–6505.

39. Mirjany, M., Ho, L., Pasinetti, G.M., 2002. Role of cyclooxygenase-2 in neuronal cell cycle activity and glutamate-mediated excitotoxicity. J. Pharmacol. Exp. Ther. 301, 494-500.

40. Miyamoto, O., Tamae, K., Kasai, H., Hirakawa, H., Hayashida, Y., Konishi, R., Itano, T., 2003. Suppression of hyperemia and DNA oxidation by indomethacin in cerebral ischemia. Eur. J. Pharmacol. 459, 179-186.

41. Nakamura, T., Minamisawa, H., Katayama, Y., Ueda, M., Terashi, A., Nakamura, K., Kudo, Y., 1999. Increased intracellular Ca2+ concentration in the hippocampal CA1 area during global ischemia and reperfusion in the rat: a possible cause of delayed neuronal death. Neuroscience 88, 57-67.

42. Nakayama, M., Uchimura, K., Zhu, R.L., Nagayama, T., Rose, M.E., Stetler, R.A., Isakson, P.C., Chen, J., Graham, S.H., 1998. Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc. Natl. Acad. Sci. USA 95, 10954-10959.

43. Nelson, C.W., Wei, E.P., Povlishock, J.T., Kontos, K.A., Moskowitz, M.A., 1992. Oxygen radicals in cerebral ischemia. Am. J. Physiol. 263, H1356-H1362.

44. Nogawa, S., Zhang, F., Ross, M.E., Iadecola, C., 1997. Cyclo-oxygenase-2 gene expression in neurons contributes to ischemic brain damage. J. Neurosci. 17, 2746-2755.

45. Oostveen, J.A., Dunn, E., Carter, D.B., Hall, E.D., 1998. Neuroprotective efficacy and mechanisms of novel pyrrolopyrimidine lipid peroxidation inhibitors in the gerbil forebrain ischemia model. J. Cereb. Blood Flow Metab. 18, 539-547.

46. Scali, C., Prosperi, C., Vannucchi, M.G., Pepeu, G., Casamenti, F., 2000. Brain inflammatory reaction in an animal model of neuronal degeneration and its modulation by an anti-inflammatory drug: implication in Alzheimer's disease. Eur. J. Neurosci. 12, 1900-1912.

47. Schmidt-Kastner, R., Freund, T.F., 1991. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40, 599-636.

48. Schmued, L.C., Hopkins, K.J., 2000. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 874, 123-130.

49. Schulz, J.B., Lindenau, J., Seyfried, J., Dichgans, J., 2000. Glutathione, oxidative stress and neurodegeneration. Eur. J. Biochem. 267, 4904-4911.

50. Seibert, K., Zhang, Y., Leahy, K., Hauser, S., Masferrer, J., Isakson, P., 1997. Distribution of COX-1 and COX-2 in normal and inflamed tissues. Adv. Exp. Med. Biol. 400A, 167–170.

51. Song, J.H., Shin, S.H., Ross, G.M., 1999. Prooxidant effects of ascorbate in rat brain slices. J. Neurosci. Res. 58, 328-336.

52. Spielman, L., Winger, D., Ho, L., Aisen, P.S., Shohami, E., Pasinetti, G.M., 2002. Induction of the complement component C1qB in brain of transgenic mice with neuronal overexpression of human cyclooxygenase-2. Acta Neuropathol. (Berl.) 103, 157-62.

53. Springer, J.E., Azbill, R.D., Mark, R.J., Begley, J.G., Waeg, G., Mattson, M.P., 1997. 4-hydroxynonenal, a lipid peroxidation product, rapidly accumulates following traumatic spinal cord injury and inhibits glutamate uptake. J. Neurochem. 68, 2469-2476.

54. Taniguchi, Y., Yokoyama, K., Noda, K., 1997. Inhibition of brain cyclooxygenase-2 activity and the antipyretic action of nimesulide. Eur. J. Pharmacol. 330, 221-229.

55. Tietze, F., 1969. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27, 502-522.

56. Tyurin, V.A., Tyurina, Y.Y., Borisenko, G.G., Sokolova, T.V., Ritov, V.B., Quinn, P.J., Rose, M., Kochanek, P., Graham, S.H., Kagan, V.E., 2000. Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates. J. Neurochem. 75, 2178-2189.

57. Urabe, T., Yamasaki, Y., Hattori, N., Yoshikawa, M., Uchida, K., Mizuno, Y., 2000. Accumulation of 4-hydroxynonenal-modified proteins in hippocampal CA1 pyramidal neurons precedes delayed neuronal damage in the gerbil brain. Neuroscience 100, 241-250.

58. Vane, J.R., Bakhle, Y.S., Botting, R.M., 1998. Cyclooxygenases 1 and 2. Annu. Rev. Pharmacol. Toxicol. 38, 97-120.

59. Volterra, A., Trotti, D., Tromba, C., Floridi, S., Racagni, G., 1994. Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. J. Neurosci. 14, 2924-2932.

60. Wakita, H., Tomimoto, H., Akiguchi, I., Lin, J.X., Miyamoto, K., Oka, N., 1999. A cyclooxygenase-2 inhibitor attenuates white matter damage in chronic cerebral ischemia. Neuroreport 10, 1461-1465.

61. Yamaguchi, S., Ogata, H., Hamaguchi, S., Kitajima, T., 1998. Superoxide radical generation and histopathological changes in hippocampal CA1 after ischemia/reperfusion in gerbils. Can. J. Anaesth. 45, 226-232.

Metadata

Repository Staff Only: item control page