Oxygen deprivation produces delayed inhibition of long-term potentiation by activation of NMDA receptors and nitric oxide synthase

Journal of Cerebral Blood Flow and Metabolism

Volumn 18, Issue 1, 1998, Pages 97-108

  Izumi, Yukitoshi ^a   Katsuki, Hiroshi ^a   Benz, Ann M ^a   Zorumski, Charles F ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anoxia; Hippocampal slices; Hypoxia; Longterm potentiation; N methyl D aspartate (NMDA) receptors; Nitric oxide

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HYPOXIA; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; HISTOPATHOLOGY; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REOXYGENATION; SYNAPTIC TRANSMISSION;

EID: 0031975111     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004647-199801000-00010     Document Type: Article

References (56)

1. Akira T, Henry D, Baldwin RA, Wasterlain CG (1994) Nitric oxide participates in excitotoxic mechanisms induced by chemical hypoxia. Brain Res 645:285-290
2. Ando S, Kametani H, Osada H, Iwamoto M, Kimura N (1987) Delayed memory dysfunction by transient hypoxia and its prevention with forskolin. Brain Res 405:371-374
3. Arai A, Larson J, Lynch G (1990) Anoxia reveals a vulnerable period in the development of long-term potentiation. Brain Res 511:353-357
4. Babbedge RC, Bland-Ward PA, Hart SL, Moore PK (1992) Inhibition of rat cerebellar nitric oxide synthase by 7-nitro indazole and related substituted indazoles. Br J Pharmacol 110:225-228
5. Bannerman DM, Chapman PF, Kelly PAT, Butcher SP, Morris RGM (1994) Inhibition of nitric oxide synthase does not prevent the induction of long-term potentiation in vivo. J Neurosci 14:7415-7425
6. Boissard CG, Lindner MD, Gribkoff VK (1992) Hypoxia produces cell death in the rat hippocampus in the presence of an A1 adenosine receptor antagonist: an anatomical and behavioral study. Neuroscience 48:807-812
7. Canhao P, de Mendonça A, Ribeiro JA (1994) 1,3-Dipropyl-8-cyclopentylxanthine attenuates the NMDA response to hypoxia in the rat hippocampus. Brain Res 661:265-273
8. Chen Z-F, Schottler F, Arlinghaus L, Kassell NF, Lee KS (1996) Hypoxic neuronal damage in the absence of hypoxic depolarization in rat hippocampal slices: the role of glutamate receptors. Brain Res 708:82-92
9. Clark GD, Rothman SM (1987) Blockade of excitatory amino acid receptors protects anoxic hippocampal slices. Neuroscience 21: 665-671
10. Coan EJ, Irving AJ, Collingridge GL (1989) Low-frequency activation of the NMDA receptor system can prevent the induction of LTP. Neurosci Lett 105:205-210
11. Collingridge GL, Kehl SL, McLennan H (1983) Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 334:33-46
12. Dawson VL, Dawson TM, London ED, Bredt DS, Snyder SH (1991) Nitric oxide mediates glutamate neurotoxicity in primary cultures. Proc Natl Acad Sci USA 88:6368-6371
13. Deckel AW (1994) Carbon monoxide poisoning and frontal lobe pathology: two case reports and a discussion of the literature. Brain Inj 8:345-356
14. Dezsi L, Greenberg JH, Sladky J, Araki N, Hamar J, Reivich M (1994) Prolonged effects of MK-801 in the cat during focal cerebral ischemia and recovery: survival, EEG activity and histopathology. J Neurol Sci 121:110-120
15. Fairchild MD, Parsons JE, Wasterlain CG, Rinaldi PC, Wallis RA (1988) A hypoxic injury potential in the hippocampal slices. Neurosci Lett 453:357-361
16. Gozlan H, Diabira D, Chinestra P, Ben-Ari Y (1994) Anoxic LTP is mediated by the redox modulatory site of the NMDA receptor. J Neurophysiol 72:3017-3022
17. Grinker RR (1926) Parkinsonism following carbon monoxide poisoning. J Nerv Ment Dis 64:18-29
18. Hamada Y, Hayakawa T, Hattori H, Mikawa H (1994) Inhibitor of nitric oxide synthesis reduces hypoxic-ischemic brain damage in the neonatal rat. Pediatr Res 35:10-14
19. Hardy KR, Thom SR (1994) Pathophysiology and treatment of carbon monoxide poisoning. J Toxicol Clin Toxicol 32:613-629
20. Hegstad E, Berg-Johnsen J, Haugstad TS, Hauglie-Hanssen E, Langmoen IA (1996) Amino acid release from human cerebral cortex during simulated ischaemia in vitro. Acta Neurochir 138:234-241
21. Hershkowitz N, Katchman AN, Veregge S (1993) Site of synaptic depression during hypoxia: a patch-clamp analysis. J Neurophysiol 69:432-441
22. Huang Y-Y, Colino A, Selig DK, Malenka RC (1992) The influence of prior synaptic activity of the induction of long-term potentiation. Science 255:730-733
23. Ischiropoulos H, Beers MF, Ohnishi ST, Fisher D, Garner SE, Thom SR (1996) Nitric oxide production and perivascular nitration in brain after carbon monoxide poisoning in the rat. J Clin Invest 97:2260-2267
24. Izumi Y, Benz AM, Clifford DB, Zorumski CF (1992a) Nitric oxide inhibitors attenuate N-methyl-D-aspartate excitotoxicity in rat hippocampal slices. Neurosci Lett 135:227-230
25. Izumi Y, Benz AM, Clifford DB, Zorumski CF (1993) Neurotoxic effects of sodium nitroprusside in rat hippocampal slices. Exp Neurol 121:14-23
26. Izumi Y, Benz AM, Clifford DB, Zorumski CF (1996) Nitric oxide inhibitors attenuate ischemic degeneration in the CA1 rat hippocampal slices. Neurosci Lett 210:157-160
27. Izumi Y, Clifford DB, Zorumski CF (1992b) Low concentrations of N-methyl-D-aspartate inhibit the induction of long-term potentiation in rat hippocampal slices. Neurosci Lett 137:245-248
28. Izumi Y, Clifford DB, Zorumski CF (1992c) Inhibition of long-term potentiation by NMDA-mediated nitric oxide release. Science 257: 1273-1276
29. Izumi Y, Zorumski CF (1993) Nitric oxide and long-term synaptic depression in the rat hippocampus. Neuroreport 4:1131-1134
30. Lobner D, Lipton P (1993) Intracellular calcium levels and calcium fluxes in the CA1 region of the rat hippocampal slice during in vitro ischemia: relationship to electrophysiological cell damage. J Neurosci 13:4861-4871
31. Maiese K, Wagner J, Boccone L (1994) Nitric oxide: a downstream mediator of calcium toxicity in the ischemic cascade. Neurosci Lett 166:43-47
32. Nakane M, Klinghofer V, Kuk JE, Donnelly JL, Budzik GP, Pollock JS, Basha F, Carter GW (1995) Novel potent and selective inhibitors of inducible nitric oxide synthase. Mol Pharmacol 47:831-834
33. Nellgård B, Wieloch T (1992) Postischemic blockade of AMPA but not NMDA receptors mitigates neuronal damage in the rat brain following transient severe cerebral ischemia. J Cereb Blood Flow Metab 12:2-11
34. Ohno M, Yamamoto T, Watanabe S (1994) Intrahippocampal administration of the NO synthase inhibitor L-NAME prevents working memory deficits in rats exposed to transient cerebral ischemia. Brain Res 634:173-177
35. Opitz T, Reymann KG (1991) Blockade of metabotropic glutamate receptors protects rat CA1 neurons from hypoxic injury. Neuroreport 2:455-457
36. Patel MN, Yim GKW, Isom GE (1992) Blockade of N-methyl-D-aspartate receptors prevents cyanide-induced neuronal injury in primary hippocampal culture. Toxicol Appl Pharmacol 115:124-129
37. Penney DG, Chen K (1996) NMDA receptor-blocker ketamine protects during acute carbon monoxide poisoning, while calcium channel-blocker verapamil does not. J Appl Toxicol 16:297-304
38. Rader RK, Lanthorn TH (1989) Experimental ischemia induces a persistent depolarization blocked by decreased calcium and NMDA antagonists. Neurosci Lett 99:125-130
39. Rothman SM (1983) Synaptic activity mediates death of hypoxic neurons. Science 220:536-537
40. Rothman SM, Olney JW (1995) Excitotoxicity and the NMDA receptor: still lethal after eight years. Trends Neurosci 18:57-58
41. Rothman SM, Thurston JH, Hauhart RE, Clark GD, Solomon JS (1987) Ketamine protects hippocampal neurons from anoxia in vitro. Neuroscience 21:673-678
42. Schuman EM, Madison DV (1993) Nitric oxide as an intercellular signal in long-term potentiation. Semin Neurosci 5:207-215
43. Schurr A, Payne RS, Rigor BM (1995) Protection by MK-801 against hypoxia-, excitotoxin-, and depolarization-induced neuronal damage in vitro. Neurochem Int 26:519-525
44. Schurr A, West CA, Reid KH, Tseng MT, Reiss SJ, Rigor BM (1987) Increased glucose improves recovery of neuronal function after cerebral hypoxia in vitro. Brain Res 421:135-139
45. Somjen GG, Aitken PG, Czeh G, Jing J, Young JN (1993) Cellular physiology of hypoxia of the mammalian central system. Res Publ Assoc Res Nerv Ment Dis 71:51-65
46. Strosznajder J, Chalimoniuk M (1996) Biphasic enhancement of nitric oxide synthase activity and cGMP level following brain ischemia in gerbils. Acta Neurobiol Exp 56:71-81
47. Taylor CP, Weber ML (1993) Effect of temperature on synaptic function after reduced oxygen and glucose in hippocampal slices. Neuroscience 52:555-562
48. Wallis RA, Panizzon K, Wasterlain CG (1992) Inhibition of nitric oxide synthase protects against hypoxic neuronal injury. Neuroreport 3:645-648
49. Williams JH, Errington ML, Li Y-G, Lynch MA, Bliss TVP (1993) The search for retrograde messengers in long-term potentiation. Semin Neurosci 5:149-158
50. Yoneda K, Okada Y (1989) Effects of anoxia and recovery on the neurotransmission and level of high-energy phosphates in thin hippocampal slices from the guinea-pig. Neuroscience 28:401-407
51. Yoshida T, Limmroth V, Irikura K, Moskowitz MA (1994) The NOS inhibitor, 7-nitroindazole, decreases focal infarct volume but not the response to topical acetylcholine in pial vessels. J Cereb Blood Flow Metab 14:924-929
52. Yoshida T, Waeber C, Huang ZH, Moskowits MA (1995) Induction of nitric oxide synthase activity in rodent brain following middle cerebral artery occlusion. Neurosci Lett 194:214-218.
53. Zhang ZG, Feif D, Macdonald J, Tang WX, Kamp DK, Gentile RJ, Shkespeare WC, Murray RJ, Chopp M (1996) ARL 17477, a potent and selective neuronal NOS inhibitor decreases infarct volume after transient middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab 16:599-604
54. Zhu PJ, Erdemli G (1995) Nitric oxide may be a mediator of effects of prolonged but not brief anoxia in CA1 neurons in slices. Neuropharmacology 34:75-80
55. Zorumski CF, Izumi Y (1993) Nitric oxide and hippocampal synaptic plasticity. Biochem Pharmacol 46:777-785
56. Zorumski CF, Mennerik S, Izumi Y (1996) Assessment of synaptic effects of nitric oxide in hippocampal neurons. Methods Neurosci 31:283-299