Evidence for involvement of the neuronal isoform of nitric oxide synthase during induction of long-term potentiation and long-term depression in the rat dentate gyrus in vitro

Neuroscience

Volumn 78, Issue 2, 1997, Pages 393-398

  Wu, J ^a   Wang, Y ^a   Rowan, M J ^a   Anwyl, R ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

dentate gyrus; hippocampus; inhibitors LTP; LTD; neuronal nitric oxide synthase; nitric oxide; TRIM

Indexed keywords

3 BROMO 7 NITROINDAZOLE; ARGININE; NITRIC OXIDE SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; ELECTROPHYSIOLOGY; HIPPOCAMPUS; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0031562361     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)84911-1     Document Type: Article

References (39)

1. 1. Al-Ghoul W. M., Meeker R. B. and Greenwood R. S. (1995) Kindling induces a long-lasting increase in brain nitric oxide synthase activity. NeuroReport 6, 457-460.
2. 2. Babbedge R. C., Blandward P. A., Hart S. L. and Moore P. K. (1993) Inhibition of rat cerebellar nitric oxide synthase by 7-nitro-indazole and related substituted indazoles. Br. J. Pharmac. 110, 225-228.
3. 3. Bannerman D. M., Chapman P. F., Kelly P. A. T., Butcher S. P. and Morris R. G. M. (1994) Inhibition of nitric oxide synthase does not prevent the induction of long-term potentiation in vivo. J. Neurosci. 14, 7415-7425.
4. 4. Barrionuevo G., Schottler F. and Lynch G. (1980) The effects of repetitive low frequency stimulation on control and potentiated responses in the hippocampus. Life Sci. 27, 2385-2389.
5. 5. Bland-Ward P. A., Pitcher A., Wallace P., Gaffen Z., Babbedge R. C. and Moore P. K. (1994) Isoform selectivity of indazole-based nitric oxide synthase inhibitors. Br. J. Pharmac. 112, 351P.
6. 6. Bland-Ward P. A. and Moore P. K. (1995) 7-Nitroindazole derivatives are potent inhibitors of brain endothelium and inducible isoforms of nitric oxide synthase. Life Sci. 57, 131-135.
7. 7. Bliss T. V. P. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
8. 8. Bliss T. V. P. and Lomo T. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of anaesthetized rabbit following stimulation of the perforant pathway. J. Physiol. 232, 331-356.
9. 9. Bohme G. A., Bon C., Stutzmann J.-M., Doble A. and Blanchard J.-C. (1991) Possible involvement of nitric oxide in long-term potentiation. Eur. J. Pharmac. 199, 379-381.
10. 10. Bon C., Bohme A., Doble A., Stutzmann J.-M. and Blanchard J.-C. (1992) A role for nitric oxide in long-term potentiation. Eur. J. Neurosci. 4, 420-424.
11. 11. Boulton C., Irving A. J., Southam E., Potier B., Garthwaite J. and Collingridge G. L. (1994) The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur. J. Neurosci. 6, 1528-1535.
12. 12. Bredt D. S. and Snyder S. H. (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc. natn. Acad. Sci. U.S.A. 86, 9030-9033.
13. 13. Chetkovitch D. M., Klann E. and Sweatt M. (1993) Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. NeuroReport 4, 919-922.
14. 14. Chiang L. W., Schweizer F. E., Tsien R. W. and Schulman H. (1994) Nitric oxide synthase expression in single hippocampal neurons. Molec. Brain Res. 27, 183-188.
15. 15. Cummings J. A., Nicola S. M. and Malenka R. C. (1994) Induction in the rat hippocampus of long-term potentiation (LTP) and long-term depression (LTD) in the presence of a nitric oxide synthase inhibitor. Neurosci. Lett. 176, 110-114.
16. 16. Doyle C., Holscer C., Rowan M. J. and Anwyl R. (1996) The selective neuronal NO synthase inhibitor 7-nitroindazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. J. Neurosci. 16, 418-424.
17. 17. Dudek S. M. and Bear M. F. (1993) Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. Proc. natn. Acad. Sci. U.S.A. 89, 4363-4367.
18. 18. Gally J. A., Read-montague P., Reeke G. N. and Edelman G. M. (1990) The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system. Proc. natn. Acad. Sci. U.S.A. 87, 3547-3551.
19. 19. Garthwaite J., Charles S. L. and Chess-Williams R. (1988) Endothelial-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336, 385-387.
20. 20. Gribkoff V. K. and Lum-Raga J. (1992) Evidence for nitric oxide synthase inhibitor-sensitive and insensitive hippocampal synaptic potentiation. J. Neurophysiol. 68, 639-642.
21. 21. Haley J. E., Malen P. L. and Chapman P. F. (1993) Nitric oxide synthase inhibitors block long-term potentiation induced by weak but not strong tetanic stimulation at physiological brain temperatures in rat hippocampal slices. Neurosci. Lett. 160, 85-88.
22. 22. Haley J., Wilcox G. L. and Chapman P. F. (1992) The role of nitric oxide in hippocampal long-term potentiation. Neuron 8, 211-216.
23. 23. Handy R. L. C., Wallace P., Gaffen Z. A., Whitehead K. J. and Moore P. K. (1995) The antinocieptive effect of 1-(2-trifluoromethylpheny)imidazole (TRIM), a potent inhibitor of neuronal nitric oxide synthase in vitro, in the mouse. Br. J. Pharmac. 116, 2349-2350.
24. 24. Handy R. L. C., Wallace P., Gaffen Z. A., Whitehead K. J. and Moore P. K. (1996) Inhibition of nitric oxide synthase by 1-(2-trifluoromethylpheny)imidazole (TRIM) in vitro: antinociceptive and cardiovascular effects. Br. J. Pharmac. 119, 423-431.
25. 25. Izumi Y. and Zorumski C. F. X. (1995) Nitric oxide and long-term synaptic depression in the rat hippocampus. NeuroReport 4, 1131-1134.
26. 26. Kato K. and Zorumski C. F. (1993) Nitric oxide inhibitors facilitate the induction of hippocampal long-term potentiation by modulating NMDA responses. J. Neurophysiol. 70, 1260-1263.
27. 27. Linden D. J. (1994) Long-term synaptic depression in the mammalian brain. Neuron 12, 457-472.
28. 28. Lum-Ragan J. T. and Gribkoff V. K. (1993) The sensitivity of hippocampal long-term potentiation to nitric oxide synthase inhibitors is dependent upon the pattern of conditioning stimulation. Neuroscience 57, 973-983.
29. 29. Mackenzie G. M., Rose S., Blandward P. A., Moore P. K., Jenner P. and Marsden C. D. (1994) Time course of inhibition of brain nitric oxide synthase by 7-nitro indazole. NeuroReport 5, 1993-1996.
30. 30. Moore P. K., Babbedge R. C., Wallace P., Garren Z. A. and Hart S. L. (1993) 7-Nitro indazole, an inhibitor of nitric oxide synthase, exhibits anti-nociceptive activity in the mouse without increasing blood pressure. Br. J. Pharmac. 108, 296-297.
31. 31. Moore P. K., Wallace P., Gaffen Z., Hart S. L. and Babbedge R. C. (1993) Characterization of the novel nitric oxide synthase inhibitor 7-nitro indazole and related indazoles - antinociceptive and cardiovascular effects. Br. J. Pharmac. 110, 219-224.
32. 32. Mulkey R. M. and Malenka R. C. (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9, 967-975.
33. 33. Murphy K. P. S. J., Williams J. H., Bettache N. and Bliss T. V. P. (1994) Photolytic release of nitric oxide modulates NMDA receptor-mediated transmission but does not induce long-term potentiation at hippocampal synapses. Neuropharmacology 33, 1375-1385.
34. 34. O'Dell T. J., Hawkins R. D., Kandel E. R. and Arancio O. (1991) Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible retrograde messenger. Proc. natn. Acad. Sci. U.S.A. 88, 11285-11289.
35. 35. O'Dell T. J., Huang P. L., Dawson T. M., Dinerman J. L., Snyder S. H., Kandel E. R. and Fishman M. C. (1994) Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science 265, 542-546.
36. 36. Rose S., Hindmarsh J. G., Silva M. T., Pitcher A., Aislaitner G., Moore P. K., Gorrod J. W., Jenner P. and Marsden C. D. (1994) The novel monosodium salt of 7-nitroindazole inhibits brain nitric oxide synthase and elevates striatal dopamine efflux in vivo. Br. J. Pharmac. 112, 506P.
37. 37. Schuman E. M. and Madison D. V. (1991) A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254, 1503-1506.
38. 38. Silva M. T., Rose S., Hindmarsh J. G., Aislaitner G., Gorrod J. W., Moore P. K., Jenner P. and Marsden C. D. (1994) Increased striatal dopamine efflux in vivo following inhibition of cerebral nitric oxide synthase by the novel monosodium salt of 7-nitro indazole. Br. J. Pharmac. 114, 257-258.
39. 39. Williams J. H., Li Y.-G., Nayak A., Errington M. L., Murphy K. P. S. J. and Bliss T. V. P. (1993) The suppression of long-term potentiation in the rat hippocampus by inhibitors of nitric oxide synthase is temperature and age dependent. Neuron 11, 877-884.