Effects of edaravone on N-methyl-d-aspartate (NMDA)-mediated cytochrome c release and apoptosis in neonatal rat cerebrocortical slices

International Journal of Developmental Neuroscience

Volumn 24, Issue 6, 2006, Pages 349-356

  Nakano Okuda, Yumi ^a   Hasegawa, Koh ^a   Hirai, Kiyoshi ^a   Kanai Ochiai, Rika ^a   Morimoto, Masafumi ^a   Sugimoto, Toru ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Brain slice; Cytochrome c; Edaravone; N Methyl d aspartate; Reactive oxygen species; TUNEL

Indexed keywords

CYTOCHROME C; N METHYL DEXTRO ASPARTIC ACID; NITRIC OXIDE; NORPHENAZONE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BRAIN SLICE; CEREBROSPINAL FLUID; CONTROLLED STUDY; ENZYME RELEASE; EXCITOTOXICITY; IMMUNOREACTIVITY; NEUROTOXICITY; NEWBORN; NICK END LABELING; NONHUMAN; PARIETAL LOBE; PRIORITY JOURNAL; RAT; RAT STRAIN;

ANIMALS; ANIMALS, NEWBORN; ANTIPYRINE; APOPTOSIS; CEREBRAL CORTEX; CYTOCHROMES C; FREE RADICAL SCAVENGERS; HUMANS; IN SITU NICK-END LABELING; N-METHYLASPARTATE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33748300950     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2006.08.001     Document Type: Article

References (50)

1. Amemiya S., Kamiya T., Nito C., Inaba T., Kato K., Ueda M., Shimazaki K., and Katayama Y. Anti-apoptotic and neuroprotective effects of edaravone following transient focal ischemia in rats. Eur. J. Pharmacol. 516 2 (2005) 125-130
2. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., and Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 1620-1624
3. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., and Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-asparate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 7162-7166
4. Brookes P.S., and Darley-Usmar V.M. Role of calcium and superoxide dismutase in sensitizing mitochondria to peroxynitrite-induced permeability transition. Am. J. Physiol. 286 (2004) H39-H46
5. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S. Calcium, ATP and ROS: a mitochondrial love-hate triangle. Am. J. Physiol. 287 (2004) C817-C833
6. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., Frisch S., and Reed J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science 282 (1998) 1318-1321
7. Chan P.H. Mitochondrial and neuronal death/survival signaling pathways in cerebral ischemia. Neurochem. Res. 29 11 (2004) 1943-1949
8. Dawson V.L., and Dawson T.M. Deadly conversation: nuclear-mitochondrial cross-talk. J. Bioenerg. Biomembr. 36 4 (2004) 287-293
9. Dawson V.L., Dawson T.M., London E.D., Bredt D.S., and Snyder S.H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 6368-6371
10. de Murcia G., Schreiber V., Molinite M., Saulier B., Poch O., Masson M., Niedergang C., and Menissier de Murcia J. Structure and function of poly(ADP-ribose)polymerase. Mol. Cell Biochem. 138 (1994) 15-24
11. Dobsak P., Courderot-Masuyer C., Zeller M., Vergely C., Laubriet A., Assem M., Eicher J.C., Teyssier J.R., Wolf J.E., and Rochette L. Antioxidative properties of pyruvate and protection of the ischemic rat heart during cardioplegia. J. Cardiovas. Pharmacol. 34 5 (1999) 651-659
12. Duchen M.R. Role of mitochondria in health and disease. Diabetes 53 (2004) S96-S102
13. 1H NMR study. J. Neurochem. 59 (1992) 1820-1828
14. Espanol M.T., Litt L., Chang L.H., James T.L., Weinstein P.R., and Chan P.H. Adult rat brain-slice preparation for nuclear magnetic resonance spectroscopy studies of hypoxia. Anesthesiology 84 (1996) 201-210
15. Frenzel J., Richter J., and Eschrich K. Pyruvate protects glucose-deprived Muller cells from nitric oxide-induced oxidative stress by radical scavenging. GLIA 52 4 (2005) 276-288
16. Fujimura M., Fujimura-Morita Y., Murakami K., Kawase M., and Chan P.H. Cytosolic redistribution of cytochrome c after transient focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 18 (1998) 1239-1247
17. Fujimura M., Morita-Fujimura Y., Kawase M., Copin J.C., Calagui B., Epstein C.J., and Chan P.H. Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome c and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J. Neurosci. 19 (1999) 3414-3422
18. Gross A., McDonnell J.M., and Korsmeyer S.J. Bcl-2 family members and the mitochondria in apoptosis. Genes Develop. 13 (1999) 1899-1911
19. Haberny K.A., Paule M.G., Scallet A.C., Sistare F.D., Lester D.S., Hanig J.P., and Slikker Jr. W. Ontogeny of the N-methyl-d-aspartate (NMDA) receptor system and susceptibility to neurotoxicity. Toxicol. Sci. 68 (2002) 9-17
20. Hagberg H., Bona E., Gilland E., and Puka-Sundvall M. Hypoxia-ischemia model in the 7-day-old rat: possibilities and shortcomings. Acta Pediatr. Suppl. 442 (1997) 85-88
21. Hagberg H., Ichord R., Palmer C., Yager J.Y., and Vannucci J. Animal models of developmental brain injury: relevance to human disease. Develop. Neurosci. 24 (2002) 364-366
22. Hasegawa K., Litt L., Espanol M.T., Gregory G.A., Sharp F.R., and Chan P.H. Effects of neuroprotective dose of fructose-1,6-bisphosphate on hypoxia-induced expression of c-fos and hsp70 mRNA in neonatal rat cerebrocortical slices. Brain Res. 750 (1997) 1-10
23. Hasegawa K., Litt L., Espanol M.T., Sharp F.R., and Chan P.H. Expression of c-fos and hsp70 mRNA in neonatal rat cerebrocortical slices during NMDA-induced necrosis and apoptosis. Brain Res. 785 (1998) 262-278
24. Hirai K., Sugawara T., Chan P.H., Basus V.J., James T.L., and Litt L. Cytochrome c associated apoptosis during ATP recovery after hypoxia in neonatal rat cerebrocortical slices. J. Neurochem. 83 (2002) 309-319
25. Hirai K., Hayashi T., Chan P.H., Zeng J., Yang G.-Y., Basus V.J., James T.L., and Litt L. PI3K inhibition in neonatal rat brain slices during and after hypoxia reduces phospho-Akt and increases cytosolic cytochrome c and apoptosis. Mol. Brain Res. 124 (2004) 51-61
26. Iverson S.L., and Orrenius S. The cardiolipin-cytochrome c interaction and the mitochondrial regulation of apoptosis. Arch. Biochem. Biophys. 423 (2004) 37-46
27. Kops G.J., and Burgering B.M. Forkhead transcription factors: new insights into protein kinase B (c-Akt) signaling. J. Mol. Med. 77 (1999) 656-665
28. Lafon-Cazal M., Pietri S., Culcasi M., and Bockaert J. NMDA-dependent superoxide production and neurotoxicity. Nature 364 (1993) 535-537
29. Lewen A., Matz P., and Chan P.H. Free radical pathways in CNS injury. J. Neurotrauma 17 (2000) 871-890
30. Lipton S.A., and Rosenberg P.A. Mechanisms of disease: excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330 (1994) 613-622
31. Liu X., Kim C.N., Yang J., Jemmerson R., and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86 (1996) 147-157
32. Marla S.S., Lee J., and Groves J.T. Peroxynitrite rapidly permeates phospholipid membranes. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14243-14248
33. McDonald J.W., Silverstein F.S., and Johnston M.V. Neurotoxicity of N-methyl-d-aspartate is markedly enhanced in developing rat central nervous system. Brain Res. 459 (1988) 200-203
34. Miyamoto K., Nakanishi H., Moriguchi S., Fukuyama N., Eto K., Wakamiya J., Murao K., Arimura K., and Osame M. Involvement of enhanced sensitivity of N-methyl-d-aspartate receptors in vulnerability of developing cortical neurons to methylmercury neurotoxicity. Brain Res. 901 (2001) 252-258
35. Noshita N., Sugawara T., Lewen A., Hayashi T., and Chan P.H. Copper-zinc superoxide dismutase affects Akt activation after transient focal cerebral ischemia in mice. Stroke 34 (2003) 1513-1518
36. Ochiai-Kanai R., Hasegawa K., Takeuchi Y., Yoshioka H., and Sawada T. Immunohistochemical nitrotyrosine distribution in neonatal rat cerebrocortical slices during and after hypoxia. Brain Res. 847 (1999) 59-70
37. Ott M., Robertoson J.D., Gogvadze V., Zhivotovsky B., and Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 1259-1263
38. Panov A.V., Andreeva L., and Greenamyre J.T. Quantitative evaluation of the effects of mitochondrial permeability transition pore modifiers on accumulation of calcium phosphate: comparison of rat liver and brain mitochondria. Arch. Biochem. Biophys. 424 (2004) 44-52
39. Park J.Y., Kim E.J., Kwon K.J., Jung Y.S., Moon C.H., Lee S.H., and Baik E.J. Neuroprotection by fructose-1,6-bisphosphate involves ROS alterations via p38 MAPK/ERK. Brain Res. 1026 (2004) 295-301
40. Rajesh K.G., Sasaguri S., Suzuki R., and Maeda H. Antioxidant MCI-186 inhibits mitochondrial permeability transition pore and upregulates Bcl-2 expression. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H2171-H2178
41. Saito A., Narasimhan P., Hayashi T., Okuno S., Drake M.F., and Chan P.H. Neuroprotective role of a proline-rich Akt substrate in apoptotic neuronal cell death after stroke: relationships with nerve growth factor. J. Neurosci. 24 7 (2004) 1584-1593
42. Shichinohe H., Kuroda S., Yasuda H., Ishikawa T., Iwai M., Horiuchi M., and Iwasaki Y. Neuroprotective effects of the free radical scavenger Edaravone (MCI-186) in mice permanent focal brain ischemia. Brain Res. 1029 (2004) 200-206
43. Shidoji Y., Hayashi K., Komura S., Ohishi N., and Yagi K. Loss of molecular interaction between cytochrome c and cardiolipin due to lipid peroxidation. Biochem. Biophys. Res. Commun. 264 (1999) 343-347
44. Wang H., Yu S.W., Koh D.W., Lew J., Coombs C., Bowers W., Federoff H.J., Poirier G.G., Dawson T.M., and Dawson V.L. Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J. Neurosci. 24 48 (2004) 10963-10973
45. Watanabe T., Tanaka M., Watanabe K., Takamatsu Y., and Tobe A. Research and development of free radical scavenger edaravone as a neuroprotectant. Yakugaku Zasshi: J. Pharm. Soc. Jpn. 124 3 (2004) 99-111 (in Japanese)
46. Watanabe T., Yuki S., Egawa M., and Nishi H. Protective effects of MCI-186 on cerebral ischemia: possible involvement of free radical scavenging and antioxidant actions. J. Pharmacol. Exp. Ther. 268 3 (1994) 1597-1604
47. Waters K.A., and Machaalani R. NMDA receptors in the developing brain and effects of noxious insults. Neurosignals 13 (2004) 162-174
48. Wen J., Watanabe K., Ma M., Yamaguchi K., Tachikawa H., Kodama M., and Aizawa Y. Edaravone inhibits JNK-c-Jun pathway and restores antioxidative defense after ischemia-reperfusion injury in aged rats. Biol. Pharm. Bull. 29 4 (2006) 713-718
49. Yasuoka N., Nakajima W., Ishida A., and Takada G. Neuroprotection of edaravone on hypoxic-ischemic brain injury in neonatal rats. Develop. Brain Res. 151 (2004) 129-139
50. Yu Y.M., Kim J.B., Lee K.W., Kim S.Y., Han P.L., and Lee J.K. Inhibition of cerebral ischemic injury by ethyl pyruvate with a wide therapeutic window. Stroke 36 10 (2005) 2238-2243