Molecular basis of NMDA receptor-coupled ion channel modulation by S- nitrosylation

Nature Neuroscience

Volumn 3, Issue 1, 2000, Pages 15-21

  Choi, Yun Beom ^a   Tenneti, Lalitha ^a   Le, Dean A ^a   Ortiz, Justin ^a   Bai, Guang ^a   Chen, Huei Sheng Vincent ^a   Lipton, Stuart A ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYSTEINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHYL METHANESULFONATE; HUMANS; INDICATORS AND REAGENTS; ION TRANSPORT; MESYLATES; MUTAGENESIS, SITE-DIRECTED; N-METHYLASPARTATE; NITRIC OXIDE; NITROSO COMPOUNDS; OOCYTES; PATCH-CLAMP TECHNIQUES; PEPTIDE FRAGMENTS; RECEPTORS, N-METHYL-D-ASPARTATE; S-NITROSOTHIOLS; TRANSFECTION; XENOPUS LAEVIS;

EID: 0033995950     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/71090     Document Type: Article

References (50)

1. Hollmann, M. & Heinemann, S. F. Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108 (1994).
2. McBrain, C. J. & Mayer, M. L. N-Methyl-D-aspartic acid receptor structure and function. Physiol. Rev. 74, 723-760 (1994).
3. Choi, D. W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634 (1988).
4. Meldrum, B. & Garthwaite, J. Excitatory amino acid neurotoxicity and neurodegenerative disease. Trends Pharmacol. Sci. 11, 379-387 (1990).
5. Dingledine, R., McBain, C. J. & McNamara, J. O. Excitatory amino acid receptors in epilepsy. Trends Pharmacol. Sci. 11, 334-338 (1990).
6. Lipton, S. A. & Rosenberg, P. A. Mechanisms of disease: Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 330, 613-622 (1994).
7. Manzoni, O. et al. Nitric oxide-induced blockade of NMDA receptors. Neuron 8, 653-662 (1992).
8. Lei, S. Z. et al. Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron 8, 1087-1099 (1992).
9. Hoyt, K. R., Tang, L.-H., Aizenman, E. & Reynolds, I. J. Nitric oxide modulates NMDA-induced increases in intracellular Ca in cultured rat forebrain neurons. Brain Res. 592, 310-316 (1992).
10. Lipton, S. A. et al. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364, 626-632 (1993).
11. Manzoni, O. & Bockaert, J. Nitric oxide synthase activity endogenously modulates NMDA receptors. J. Neurochem. 61, 368-370 (1993).
12. Fagni, L., Olivier, M., Lafon-Cazal, M. & Bockaert, J. Involvement of divalent ions in the nitric oxide-induced blockade of N-methyl-D-aspartate receptors in cerebellar granule cells. Mol. Pharmacol. 47, 1239-1247 (1995).
13. Omerovic, A., Chen, S.-J., Leonard, J. P. & Kelso, S. R. Subunit-specific redox modulation of NMDA receptors expressed in Xenopus oocytes. J. Recept. Signal Transduct. Res. 15, 811-827 (1995).
14. Sucher, N. J., Awobuluyi, M., Choi, Y.-B. & Lipton, S. A. NMDA receptors: from genes to channels. Trends Pharmacol. Sci. 17, 348-355 (1996).
15. Stamler, J. S., Toone, E. J., Lipton, S. A. & Sucher, N. J. (S)NO signals: Translocation, regulation, and a consensus motif. Neuron 18, 691-696 (1997).
16. Bolotina, V. M., Najibi, S., Palacino, J. J., Pagaon, P. J. & Cohen, R. A. Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature 368, 850-853 (1994).
17. Kurenny, D. E., Moroz, L. L., Turner, R. W., Sharkey, K. A. & Barnes, S. Modulation of ion channels in rod photoreceptors by nitric oxide. Neuron 13, 315-324 (1994).
18. Gaston, B. et al. Relaxation of human bronchial smooth muscle by S-nitrosothiols in vitro. J. Pharmacol. Exp. Ther. 268, 978-984 (1994).
19. Koivisto, A. & Nedergaard, J. Modulation of calcium-activated non-selective cation channel activity by nitric oxide in rat brown adipose tissue. J. Physiol. (Lond.) 486, 59-65 (1995).
20. Koh, S. D., Campbell, J. D., Carl, A. & Sanders, K. M. Nitric oxide activates multiple potassium channels in canine colonie smooth muscle. J. Physiol. (Lond.) 489, 735-743 (1995).
21. Campbell, D. L., Stamler, J. S. & Strauss, H. C. Redox modulation of L-type calcium channels in ferret ventricular myocytes. J. Gen. Physiol. 108, 277-293 (1996).
22. Broillet, M.-C. & Firestein, S. Direct activation of the olfactory cyclic nucleotide-gated channel through modulation of sulfhydryl groups by NO compounds. Neuron 16, 377-385 (1996).
23. Takeuchi, T., Kishi, M., Ishii, T., Nishio, H. & Hata, F. Nitric oxide-mediated relaxation without concomitant changes in cyclic GMP content of rat proximal colon. Br. J. Pharmacol. 117, 1204-1208 (1996).
24. + channels. Proc. Natl. Acad. Sci. USA 93, 10489-10494 (1996).
25. Xu, L., Eu, J. P., Meissner, G. & Stamler, J. S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279, 234-237 (1998).
26. Kendrick, K. M. et al. NMDA and kainate-evoked release of nitric oxide and classical transmitters in the rat striatum: in vivo evidence that nitric oxide may play a neuroprotective role. Eur. J. Neurosci. 8, 1619-1634 (1996).
27. Lipton, S. A., Rayudu, P. V., Choi, Y.-B., Sucher, N. J. & Chen, H.-S. V. Redox modulation of the NMDA receptor by NO-related species. Prog. Brain Res. 118, 73-82 (1998).
28. Dawson, V. L., Dawson, T. M., London, E. D., Bredt, D. S. & Snyder, S. H. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc. Natl. Acad. Sci. USA 88, 6368-6371 (1991).
29. Dawson, V. L., Dawson, T. M., Bartley, D. A., Uhl, G. R. & Snyder, S. H. Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661 (1993).
30. Bonfoco, E., Krainc, D., Ankarcrona, M., Nicotera, P. & Lipton, S. A. Apoptosis and necrosis: two distinct events induced respectively by mild and intense insults with NMDA or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92, 7162-7166 (1995).
31. Adamson, D. C. et al. Immunologic NO synthase: elevation in severe AIDS dementia and induction by HIV-1 gp41. Science 274, 1917-1921 (1996).
32. Garthwaite, J., Charles, S. L. & Chess, W. R. Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336, 385-388 (1988).
33. Bredt, D. S. & Snyder, S. H. Nitric oxide, a novel neuronal messenger. Neuron 8, 3-11 (1992).
34. Shibuki, K. & Okada, D. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349, 326-328 (1991).
35. Akabas, M. H., Stauffer, D. A., Xu, M. & Karlin, A. Acetylcholine receptor channel structure probed in cysteine-substitution mutants. Science 258, 307-310 (1992).
36. Aizenman, E., Brimecombe, J. C., Potthoff, W. K. & Rosenberg, P. A. Why is the role of nitric oxide in NMDA receptor function and dysfunction so controversial? Prog. Brain Res. 118, 53-71 (1998).
37. Wo, Z. G. & Oswald, R. E. Transmembrane topology of two kainate receptor subunits revealed by N-glycosylation. Proc. Natl. Acad. Sci. USA 91, 7154-7158 (1994).
38. Hollmann, M., Maron, C. & Heinemann, S. F. N-glycosylation site tagging suggests a three transmembrane domain topology for the glutamate receptor GluR1. Neuron 13, 1331-1343 (1994).
39. Wood, M. W., VanDongen, H. M. & VanDongen, A. M. Structural conservation of ion conduction pathways in K channels and glutamate receptors. Proc. Natl. Acad. Sci. USA 92, 4882-4886 (1995).
40. Armstrong, N., Sun, Y., Chen, G.-Q, & Gouaux, E. Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395, 913-917 (1998).
41. Aizenman, E. & Potthoff, W. K. Lack of interaction between nitric oxide and the redox modulatory site of the NMDA receptor. Br. J. Pharmacol. 126, 296-300 (1999).
42. Bredt, D. S. et al. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351, 714-719 (1991).
43. Kojima, H. et al. Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal Chem. 70, 2446-2453 (1998).
44. Stamler, J. S. & Feelisch, M. in Methods in Nitric Oxide Research (eds. Feelisch, M. & Stamler, J. S.) 521-539 (Wiley, Chichester, 1996).
45. Brenman, J. E. et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell 84, 757-767 (1996).
46. Lander, H. M. et al. A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J. Biol. Chem. 272, 4323-4326 (1997).
47. Mannick, J. B. et al. Fas-induced caspase denitrosylation. Science 284, 651-654 (1999).
48. Monyer, H. et al. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221 (1992).
49. Sullivan, J. M. et al. Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron 13, 929-936 (1994).
50. 2+ inhibition of the NMDA receptor. Neuron 23, 171-180 (1999).