Nitric-oxide-induced inhibition of mitochondrial complexes following aglycaemic hypoxia in neonatal cortical rat brain slices

Developmental Neuroscience

Volumn 22, Issue 5-6, 2000, Pages 359-365

  Brooks, Keith J ^a,d   Hargreaves, Iain P ^b   Bates, Timothy E ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Brain; Complexes; Ischaemia; Mitochondria; Neonate

Indexed keywords

CALCIUM ION; CITRATE SYNTHASE; GLUCOSE; MITOCHONDRIAL ENZYME; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; OXYGEN;

ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN HYPOXIA; BRAIN MITOCHONDRION; BRAIN TISSUE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GLUCOSE BRAIN LEVEL; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RESPIRATORY CHAIN;

ANIMALS; ANIMALS, NEWBORN; CEREBRAL CORTEX; CITRATE (SI)-SYNTHASE; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; ELECTRON TRANSPORT COMPLEX III; ELECTRON TRANSPORT COMPLEX IV; FEMALE; GLUCOSE; HYPOXIA, BRAIN; MALE; MITOCHONDRIA; MULTIENZYME COMPLEXES; NADH, NADPH OXIDOREDUCTASES; NITRIC OXIDE; OXIDOREDUCTASES; RATS; RATS, WISTAR; SUCCINATE DEHYDROGENASE;

EID: 0033667523     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000017461     Document Type: Article

References (43)

1. Davis M, Wilitely T, Turnbull DM, Mendelow AD (1997): Selective impairments of mitochondrial respiratory chain activity during aging and ischemic brain damage. Acta Neurochir Suppl 70:56-58.
2. Gillard E, Puka-Sundvall M, Hillered L, Hagberg H (1998): Mitochondrial function and energy metabolism after hypoxia-ischemia in the immature rat brain: Involvement of NMDA receptors. J Cerebr Blood Flow Metab 18:297-304.
3. Siesjo BK, Siesjo P (1996): Mechanisms of secondary brain injury. Eur J Anaesthesiol 13: 247-268.
4. Allen KL, Almeida A, Bates TE, Clark JB (1995): Changes of respiratory activity in mitochondrial and synaptosomal fractions isolated from the gerbil brain after graded ischaemia. J Neurochem 64:2222-2229.
5. Almeida A, Allen KL, Bates TE, Clark JB (1995): Effect of reperfusion following cerebral ischaemia on the activity of the mitochondrial respiratory chain in the gerbil brain. J Neurochem 65:1698-1703.
6. Feng ZC, Sick TJ, Rosenthal M ( 1998): Oxygen sensitivity of mitochondrial redox status and evoked potential recovery early during reperfusion in post-ischemic rat brain. Resuscitation 37:33-41.
7. 2+ channels. Neurochem Int 23:441-450.
8. 31P NMR. Neurochem Res 21:1089-1095.
9. Brooks KJ, Clark JB, Bates TE (1998): 3-hydroxybutyrate aids recovery of the energy state from aglycaemic hypoxia of adult but not neonatal rat brain slices. J Neurochem 70: 1986-1990.
10. Brown GC (1997): Nitric oxide inhibition of cytochrome oxidase and mitochondrial respiration: Implications for inflammatory, neurodegenerative and ischaemic pathologies. Mol Cell Biochem 174:189-192.
11. Kristian T, Siesjo BK (1998): Calcium in ischemic cell death. Stroke 29:705-718.
12. 31P nuclear magnetic resonance studies on superfused cerebral tissues. Biochem Soc Trans 13:835-839.
13. Ragan CI, Wilson MT, Darley-Usmar VM, Lowe PN (1987): Subfractionation of mitochondria, and isolation of the proteins of oxidative phosphorylation; in Darley-Usmar VM, Rickwood D, Wilson MT (eds): Mitochondria, a Practical Approach. London, IRL Press, pp 79-112.
14. 1 particle and reconstitution of succinate cytochrome c reductase. Methods Enzymol 10: 328-333.
15. Wharton DC, Tzagoloff A (1967): Cytochrome oxidase from beef heart mitochondria. Methods Enzymol 10:245-250.
16. Shepherd JA, Garland PB (1969): Citrate synthase from rat liver. Methods Enzymol 13:11-19.
17. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951): Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.
18. Blumberg RM, Cady EB, Wigglesworth JS, McKenzie JE, Edwards AD (1997): Relation between delayed impairment of cerebral energy metabolism and infarction following transient focal hypoxia-ischaemia in the developing brain. Exp Brain Res 113:130-137.
19. Vannucci RC, Towfighi J, Vannucci SJ ( 1998): Hypoxic preconditioning and hypoxic-ischemic brain damage in the immature rat: Pathologic and metabolic correlates. J Neurochem 71:1215-1220.
20. Laptook AR, Corbett RJ, Sterett R, Burns DK, Garcia D, Tollefsbol G (1997): Modest hypothermia provides partial neuroprotection when used for immediate resuscitation after brain ischemia. Pediatr Res 42:17-23.
21. Lorek A, Takei Y, Cady EB, Wyatt JS, Penrice J, Edwards AD, Peebles DM, Wylezinska M, Owen-Reece H, Kirkbride V, Cooper C, Aldridge RF, Roth SC, Brown G, Delpy DT, Reynolds EOR (1994): Delayed ('secondary') cerebral energy failure after acute hypoxia-ischaemia in the newborn piglet: Continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatric Res 36:699-706.
22. Williams CE, Gunn AJ, Mallard C, Gluckman PD (1992): Outcome after ischemia in the developing sheep brain: An electroencephalographic and histological study. Ann Neurol 131:14-21.
23. Roth SC, Baudin J, Cady E, Johal K, Townsend JP, Wyatt JS, Reynolds EOR, Stewart AL (1997): Relation of deranged neonatal cerebral oxidative metabolism with neurodevelopmental outcome and head circumference at 4 years. Dev Med Child Neurol 39:718-725.
24. Heales SJ, Davies SE, Bates TE, Clark JB (1995): Depletion of brain glutathione is accompanied by impaired mitochondrial function and decreased N-acetyl aspartate concentration. Neurochem Res 20:31-38.
25. Davey GP, Peuchen S, Clark JB (1998): Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. J Biol Chem 273:12753-12757.
26. Zaidan E, Sheu KF, Sims NR ( 1998): The pyruvate dehydrogenase complex is partially inactivated during early recirculation following short-term forebrain ischemia in rats. J Neurochem 70:233-241.
27. Cheung PV, Danial H, Jong J, Schulz R (1998): Thiols protect the inhibition of myocardial aconitase by peroxynitrite. Arch Biochem Biophys 350:104-108.
28. Wei H, Wei W, Bredesen DE, Perry DC ( 1998): Bcl-2 protects against apoptosis in neuronal cell line caused by thapsigargin-induced depletion of intracellular calcium stores. J Neurochem 70:2305-2314.
29. Budd SL, Nicholls DG (1996): Mitochondria, calcium regulation, and acute glutamate exicitotoxicity in cultured cerebellar granule cells. J Neurochem 67:2282-2291.
30. G-nitroarginine in brain in vitro and in vivo. Biochem Biophys Res Comm 176:1136-1141.
31. G-nitroarginine. Biochemistry 32:8512-8517.
32. De Alba J, Cardenas A, Moro MA, Leza JC, Lorenzo P, Bosca L, Lizasoain I (1999): Down-regulation of neuronal nitric oxide synthase by nitric oxide after oxygen-glucose deprivation in rat forebrain slices. J Neurochem 72:248-254.
33. Knowles RG, Moncada S (1994): Nitric oxide synthases in mammals. Biochem J 298:249-258.
34. Keelan J, Bates TE, Clark JB (1996): Intrasynaptosomal free calcium concentration during rat brain development. J Neurochem 66:2460-2467.
35. Matsumoto T, Pollock JS, Nakane M, Forsterman U (1993): Developmental changes of cytosolic and particulate nitric oxide synthase in rat brain. Brain Res Dev Brain Res 73:199-203.
36. Keelan J, Bates TE, Clark JB (1999): Heightened resistance of the neonatal brain to ischemia-reperfusion involves a lack of mitochondrial damage in the nerve terminal. Brain Res 821:124-133.
37. Blumberg RM, Taylor DL, Yue X, Aguan K, McKenzie J, Cady EB, Weiner CP, Mehmet H, Edwards AD (1999): Increased nitric oxide synthesis is not involved in delayed cerebral energy failure following focal hypoxic-ischemic injury to the developing brain. Pediatr Res 46: 224-231.
38. Brown GC, Cooper CE (1994): Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356: 295-298.
39. Lizasoain I, Moro MA, Knowles RG, Darley Usmar V, Moncada S (1996): Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem J 314:877-880.
40. Malinski T, Bailey F, Zhang ZG, Chopp M (1993): Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J Cerebr Blood Flow Metab 13:355-358.
41. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BH (1990): Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620-1624.
42. Bolanos JP, Peuchen S, Heales SJR, Land JM, Clark JB (1994): Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J Neurochem 63:910-916.
43. Bolanos JP, Heales SJR, Land JM, Clark JB (1995): Effect of peroxynitrite on the mitochondrial respiratory chain: Differential susceptibility of neurones and astrocytes in primary culture. J Neurochem 64:1965-1972.