High-affinity zinc inhibition of NMDA NR1-NR2A receptors

Journal of Neuroscience

Volumn 17, Issue 15, 1997, Pages 5711-5725

  Paoletti, Pierre ^a,b   Ascher, Philippe ^a   Neyton, Jacques ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b Ecole Normale Supérieure ^*  (United States)

Author keywords

DTT; Heavy metals; Ionic channels; NMDA; Recombinant receptors; Zinc

Indexed keywords

HEAVY METAL; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; ZINC;

ANIMAL CELL; ARTICLE; CHELATION; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR AFFINITY; RECEPTOR BINDING; SYNAPSE;

EID: 0030746608     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-15-05711.1997     Document Type: Article

References (64)

1. 2+ homeostasis in Ehrlich and Yoshida carcinomas. J Biol Chem 260:2719-2727.
2. Ascher P, Nowak L (1988) The role of divalent cations in the N-methyl-D-aspartate responses of mouse central neurones in culture. J Physiol (Lond) 399:247-266.
3. Ascher P, Bregestovski P, Nowak L (1988) N-methyl-D-aspartate-activated channels of mouse central neurones in magnesium-free solutions. J Physiol (Lond) 399:207-226.
4. Audinat E, Lambolez B, Rossier J, Crepel F (1994) Activity-dependent regulation of N-methyl-D-aspartate receptor subunit expression in rat cerebellar granule cells. Eur J Neurosci 6:1792-1800.
5. Bers D, Patton C, Nuccitelli R (1994) A practical guide to the preparation of Ca buffers. Methods Cell Biol 40:3-29.
6. Burnashev N, Schoepfer R, Monyer H, Ruppersberg JP, Gunther W, Seeburg PH, Sakmann B (1992) Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 257:1415-1419.
7. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802-805.
8. Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752.
9. Christianson DW (1991) Structural biology of zinc. Adv Protein Chem 42:281-355.
10. Christine CW, Choi DW (1990) Effect of zinc on NMDA receptor-mediated channel currents in cortical neurons. J Neurosci 10:108-116.
11. Cornell NW, Crivaro KE (1972) Stability constant for the zinc-dithio-threitol complex. Anal Biochem 47:203-208.
12. Dawson RMC, Elliott DC, Elliott WH, Jones KM (1986) Data for biochemical research, 3rd Ed. New York: Oxford Science.
13. 45Ca influx and toxicity in cultured cerebellar granule cells. Neurosci Lett 137:198-202.
14. 45Ca uptake and acute toxicity mediated by the N-methyl-D-aspartate receptor: the effect of metal binding agents and transition metal ions. J Neurochem 61:518-525.
15. Forsythe ID, Westbrook GL, Mayer ML (1988) Modulation of excitatory synaptic transmission by glycine and zinc in cultures of mouse hippocampal neurons. J Neurosci 8:3733-3741.
16. Gibb AJ, Wyllie DJA (1997) Single-cell RT-PCR reaches out to the NMDA receptor. J Physiol (Lond) 499:1.
17. Grimwood S, Hutson PH, Macaulay AJ, Priestley T (1996) Subtype-specific modulation of stably expressed recombinant human N-methyl-D-aspartate receptors by zinc ions. Soc Neurosci Abstr 22:507.11.
18. Hamill O, Marty A, Neher E, Sakmann B, Sigworth F (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
19. Hegstad E, Langmoen IA, Hablitz JJ (1989) Zinc and glycine do not modify low-magnesium-induced epileptiform activity in the immature neocortex in vitro. Epilepsy Res 3:174-177.
20. Hollmann M, Boulter J, Maron C, Beasley L, Sullivan J, Pecht G, Heinemann S (1993) Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10:943-954.
21. Hori N, Galeno T, Carpenter DO (1987) Responses of pyriform cortex neurons to excitatory amino acids: voltage dependence, conductance changes, and effects of divalent cations. Cell Mol Neurobiol 7:73-90.
22. Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, Yokoi M, Akazawa C, Shigemoto R, Mizuno N, Masu M, Nakanishi S (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268:2836-2843.
23. Jahr CE, Stevens CF (1990) Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J Neurosci 10:3178-3182.
24. Kawajiri S, Dingledine R (1993) Multiple structural determinants of voltage-dependent magnesium block in recombinant NMDA receptors. Neuropharmacology 32:1203-1211.
25. Koh JY, Choi DW (1988) Zinc alters excitatory amino acid neurotoxicity on cortical neurons. J Neurosci 8:2164-2171.
26. Koh JY, Suh SW, Gwag BJ, He YY, Hsu CY, Choi DW (1996) The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272:1013-1016.
27. Köhr G, Eckardt S, Luddens H, Monyer H, Seeburg PH (1994) NMDA receptor channels: subunit-specific potentiation by reducing agents. Neuron 12:1031-1040.
28. 2+ block in NMDA receptor channels. J Neurosci 16:3549-3558.
29. Kunkel TA (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci USA 82:488-492.
30. Kupper J, Ascher P, Neyton J (1996) Probing the pore region of recombinant N-methyl-D-aspartate channels using external and internal magnesium block. Proc Natl Acad Sci USA 93:8648-8653.
31. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, Mishina M (1992) Molecular diversity of the NMDA receptor channel. Nature 358:36-41.
32. Legendre P, Westbrook GL (1990) The inhibition of single N-methyl-D-aspartate-activated channels by zinc ions on cultured rat neurones. J Physiol (Lond) 429:429-449.
33. Leonard JP, Kelso SR (1990) Apparent desensitization of NMDA responses in Xenopus oocytes involves calcium-dependent chloride current Neuron 4:53-60.
34. Mayer ML, Vyklicky Jr L (1989) The action of zinc on synaptic transmission and neuronal excitability in cultures of mouse hippocampus. J Physiol (Lond) 415:351-365.
35. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
36. Mayer ML, Westbrook GL, Vyklicky Jr L (1988) Sites of antagonist action on N-methyl-D-aspartic acid receptors studied using fluctuation analysis and a rapid perfusion technique. J Neurophysiol 60:645-663.
37. Mayer ML, Vyklicky Jr L, Westbrook GL (1989) Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurones. J Physiol (Lond) 415:329-350.
38. McBain CJ, Mayer ML (1994) N-methyl-D-aspartic acid receptor structure and function. Physiol Rev 74:723-760.
39. Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimura K, Mishina M (1992) Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357:70-74.
40. 2+ in rat central neurones. J Physiol (Lond) 494:479-492.
41. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
42. Monver H, Burnashev, N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-40.
43. 2+-block site of the NMDA receptor channel. Nature 358:673-675.
44. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakamshi S (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37.
45. Moshaver A, Raymond LA (1996) Differential sensitivity of recombinant NMDA receptor subtypes to zinc: implications for glutamate excitotoxicity. Soc Neurosci Abstr 22:671.2.
46. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-465.
47. 2+. Neuron 15:1109-1120.
48. Peters S, Koh J, Choi DW (1987) Zinc selectively blocks the action of N-methyl-D-aspartate on cortical neurons. Science 236:589-593.
49. Premkumar LS, Auerbach A (1996) Identification of a high-affinity divalent cation binding site near the entrance of the NMDA receptor channel. Neuron 16:869-880.
50. Rassendren FA, Lory P, Pin JP, Nargeot J (1990) Zinc has opposite effects on NMDA and non-NMDA receptors expressed in Xenopus oocytes. Neuron 4:733-740.
51. 2+ and channel blockers by a single amino acid substitution in the N-methyl-D-aspartate receptor. J Biol Chem 268:410-415.
52. Sather W, Dieudonné S, MacDonald JF, Ascher P (1992) Activation and desensitization of N-methyl-D-aspartate receptors in nucleated outside-out patches from mouse neurones. J Physiol (Lond) 450:643-672.
53. Smart TG, Xie X, Krishek BJ (1994) Modulation of inhibitory and excitatory amino acid receptor ion channels by zinc. Prog Neurobiol 42:393-441.
54. Sullivan JM, Traynelis SF, Chen HS, Escobar W, Heinemann SF, Lipton SA (1994) Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron 13:929-936.
55. Trombley PQ, Shepherd G (1996) Differential modulation of zinc and copper of amino acid receptors from rat olfactory bulb neurons. J Neurophysiol 76:2536-2546.
56. Vlachova V, Zemkova H, Vyklicky Jr L (1996) Copper modulation of NMDA responses in mouse and rat cultured hippocampal neurons. Eur J Neurosci 8:2257-2264.
57. 2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature 328:640-643.
58. Williams K (1994) Subunit-specific potentiation of recombinant N-methyl-D-aspartate receptors by histamine. Mol Pharmacol 46:531-541.
59. Williams K (1996) Separating dual effects of zinc at recombinant N-methyl-D-aspartate receptors. Neurosci Lett 215:9-12.
60. Williams K, Russell SL, Shen YM, Molinoff PB (1993) Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10:267-278.
61. Williams K, Zappia AM, Pritchett DB, Shen YM, Molinoff PB (1994) Sensitivity of the N-methyl-D-aspartate receptor to polyamines is controlled by NR2 subunits. Mol Pharmacol 45:803-809.
62. Woodhull AM (1973) Ionic blockade of sodium channels in nerve. J Gen Phvsiol 61:687-708.
63. Zhang L, Zheng X, Paupard MC, Wang AP, Santehi L, Friedman LK, Zukin RS, Bennett MV (1994) Spermine potentiation of recombinant N-methyl-D-aspartate receptors is affected by subunit composition. Proc Natl Acad Sci USA 91:10883-10887.
64. 2+ potentiation of recombinant NMDA receptors. Neuron 12:811-818.