Nitric oxide acts directly in the presynaptic neuron to produce long- term potentiation in cultured hippocampal neurons

Cell

Volumn 87, Issue 6, 1996, Pages 1025-1035

  Arancio, Ottavio ^a   Kiebler, Michael ^a   Lee, C Justin ^a   Lev Ram, Varda ^d   Tsien, Roger Y ^d,e   Kandel, Eric R ^a,b,c   Hawkins, Robert D ^a,b  

^a Columbia University ^*  (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d San Diego   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANYLATE CYCLASE; MYOGLOBIN; N(G) METHYLARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SYNAPTOPHYSIN;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRACELLULAR SPACE; HIPPOCAMPUS; LONG TERM POTENTIATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOTOLYSIS; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; ULTRAVIOLET RADIATION;

ANIMALIA;

EID: 0030582674     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81797-3     Document Type: Article

References (30)

1. Arancio, O., Kandel, E.R., and Hawkins, R.D. (1995). Activity-dependent long-term enhancement of transmitter release by presynaptic 3′, 5′-cyclic cGMP in cultured hippocampal neurons. Nature 376, 74-80.
2. Bekkers, J.M., and Stevens, C.F. (1990). Presynaptic mechanism for long-term potentiation in the hippocampus. Nature 346, 724-729.
3. Bliss, T.V.P., and Collingridge, G.L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
4. Böhme, 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. Pharmacol. 199, 379-381.
5. Boulton, C.L., 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. Pharmacol. 6, 1528-1535.
6. G-nitroarginine inhibits NMDA-induced cyclic GMP formation in rat cerebellum. Eur. J. Pharmacol. 184, 311-313.
7. East, S.J., and Garthwaite, J. (1991). NMDA receptor activation in rat hippocampus induces cGMP formation through the L-arginine-nitric oxide pathway. Neurosci. Lett. 123, 17-19.
8. Fletcher, T.L., Cameron, P., DeCamilli, P., and Banker, G. (1991). The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11, 1617-1626.
9. Gorbunov, N.V., Osipov, A.N., Day, B.W., Zoyas-Rivera, B., Kagan, V.E., and Elsayed, N.M. (1995). Reduction of ferrylmyoglobin and ferrylhemoglobin by nitric oxide: a protective mechanism against ferryl hemoprotein-induced oxidations. Biochemistry 34, 6689-6699.
10. Haley, J.E., Wilcox, G.L., and Chapman, P.F. (1992). The role of nitric oxide in hippocampal long-term potentiation. Neuron 8, 211-216.
11. Hawkins, R.D. (1996). NO Honey, I don't remember. Neuron 16, 465-467.
12. Hawkins, R.D., Kandel, E.R., and Siegelbaum, S.A. (1993). Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16, 625-665.
13. Isaac, J.T., Nicoll, R.A., and Malenka, R.C. (1995). Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434.
14. Kelso, S.R., Ganong, A.H., and Brown, T.H. (1986). Hebbian synapses in hippocampus. Proc. Natl. Acad. Sci. USA 83, 5326-5330.
15. 2+ transients. Neuron 15, 407-415.
16. Liao, D., Hessler, N.A., and Malinow, R. (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slices. Nature 375, 400-404.
17. Makings, L.R., and Tsien, R.Y. (1994). Caged nitric oxide. Stable organic molecules from which nitric oxide can be photoreleased. J. Biol. Chem. 269, 6282-6285.
18. Malgaroli, A., and Tsien, R.W. (1992). Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature 357, 134-139.
19. Meffert, M.K., Calakos, N.C., Scheller, R.H., and Schulman, H. (1996). Nitric oxide modulates synaptic vesicle docking/fusion reactions. Neuron 16, 1229-1236.
20. Murphey, R.K., and Davis, G.W. (1994). Retrograde signaling at the synapse. J. Neurobiol. 25, 595-598.
21. 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.
22. 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 early retrograde messenger. Proc. Natl. Acad. Sci. USA 88, 11285-11289.
23. Popov, S., and Poo, M.-M. (1992). Diffusional transport of macromolecules in developing nerve processes. J. Neurosci. 12, 77-85.
24. Schuman, E.M., and Madison, D.V. (1991). A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254, 1503-1506.
25. Schuman, E.M., Meffert, M.K., Schulman, H., and Madison, D.V. (1994). An ADP-ribosyl transferase as a potential target for nitric oxide action in hippocampal long-term potentiation. Proc. Natl. Acad. Sci. USA 91, 11958-11962.
26. Son, H., Hawkins, R.D., Martin, K., Kiebler, M., Huang, P.L., Fishman, M.C., and Kandel, E.R. (1996). Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell, this issue.
27. Stevens, C.F., and Wang, Y.Y. (1993). Reversal of long-term potentiation by inhibitors of heme oxygenase. Nature 364, 147-149.
28. Vogel, A.I. (1989). Textbook of Quantitative Chemical Analysis (Harlow, Essex, UK: Longman Scientific and Technical).
29. Zhuo, M., Small, S.A., Kandel, E.R., and Hawkins, R.D. (1993). Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in the hippocampus. Science 260, 1946-1950.
30. Zhuo, M., Hu, Y., Schultz, C., Kandel, E.R., and Hawkins, R.D. (1994). Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368, 635-639.