Molecular biology of the Apteronotus NMDA receptor NR1 subunit

Journal of Experimental Biology

Volumn 202, Issue 10, 1999, Pages 1319-1326

  Dunn, Robert J ^a,b   Bottai, Daniele ^a,c   Maler, Leonard ^d  

^a MONTREAL GENERAL HOSPITAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Alternative RNA splicing; Apteronotus leptorhynchus; Electrosensory system; NMDA receptor; NR1 amino acid sequence homology; NR1 subunit

Indexed keywords

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; APTERONOTUS LEPTORHYNCHUS; CENTRAL NERVOUS SYSTEM; EVOLUTION; GENE MAPPING; IN SITU HYBRIDIZATION; MESSENGER RNA; MOLECULAR BIOLOGY; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE CELL; RECEPTOR; SENSORY RECEPTOR;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; ELECTRIC FISH; MOLECULAR SEQUENCE DATA; RECEPTORS, N-METHYL-D-ASPARTATE; SEQUENCE HOMOLOGY;

APTERONOTUS; APTERONOTUS LEPTORHYNCHUS; MAMMALIA; NEMICHTHYS; TELEOSTEI; VERTEBRATA;

EID: 0033137142     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Anantharam, V., Panchal, R. G., Wilson, A., Kolchine, V. V., Treistman, S. N. and Bayley, H. (1992). Combinatorial RNA splicing alters the surface charge on the NMDA receptor. FEBS Lett. 305, 27-30.
2. Bastian, J. (1993). The role of amino acid neurotransmitters in the descending control of electroreception. J. Comp. Physiol. A 172, 409-423.
3. Berman, N. J., Plant, J., Turner, R. W. and Maler, L. (1997). Excitatory amino acid receptors at a feedback pathway in the electrosensory system: implications for the searchlight hypothesis. J. Neurophysiol. 78, 1869-1881.
4. Bottai, D., Dunn, R. J., Ellis, W. and Maler, L. (1997). N-methyl-D-aspartate receptor 1 mRNA distribution in the central nervous system of the weakly electric fish Apteronotus leptorhychus. J. Comp. Neurol. 389, 65-80.
5. Bottai, D., Maler, L. and Dunn, R. J. (1998). Alternative RNA splicing of the NMDA receptor NR1 mRNA in the neurons of the teleost electrosensory system. J. Neurosci. 18, 5191-5202.
6. Buller, A. L., Larson, H. C., Schneider, B. E., Beaton, J. A., Morrisett, R. A. and Monaghan, D. T. (1994). The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition. J. Neurosci. 14, 5471-5484.
7. Dunah, A. W., Yasuda, R. P., Wang, Y. H., Luo, J. H., Davilagarcia, M. I., Gbadegesin, M., Vicini, S. and Wolfe, B. B. (1996). Regional and ontogenic expression of the NMDA receptor subunit Nr2d protein in rat brain using a subunit-specific antibody. J. Neurochem. 67, 2335-2345.
8. Durand, G. M., Bennett, M. V. and Zukin, R. S. (1993). Splice variants of the N-methyl-D-aspartate receptor NR1 identify domains involved in regulation by polyamines and protein kinase C. Proc. Natl. Acad. Sci. USA 90, 6731-6735.
9. Durand, J. (1993). Synaptic excitation triggers oscillations during NMDA receptor activation in rat abducens motoneurons. Eur. J. Neurosci. 5, 1389-1397.
10. Dye, J., Heiligenberg, W., Keller, C. H. and Kawasaki, M. (1989). Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus. Proc. Natl. Acad. Sci. USA 86, 8993-8997.
11. Ehlers, M. D., Fung, E. T., O'Brien, R. J. and Huganir, R. L. (1998). Splice variant-specific interaction of the NMDA receptor subunit NR1 with neuronal intermediate filaments. J. Neurosci. 18, 720-730.
12. Ehlers, M. D., Zhang, S., Bernhadt, J. P. and Huganir, R. L. (1996). Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 84, 745-755.
13. Farrant, M. and Cull-Candy, S. G. (1991). Excitatory amino acid receptor channels in Purkinje cells in thin cerebellar slices. Proc. R. Soc. Lond. B 244, 179-184.
14. Foldes, R. L., Rampersad, V. and Kamboj, R. K. (1993). Cloning and sequence analysis of cDNAs encoding human hippocampus N-methyl-D-aspartate receptor subunits: evidence for alternative RNA splicing. Gene 131, 293-298.
15. Forsythe, I. D. and Westbrook, G. (1988). Slow excitatry postsynaptic currents mediated by N-methyl-D-aspartate receptors an cultured mouse central neurones. J. Physiol., Lond. 396, 515-533.
16. Heiligenberg, W., Metzner, W., Wong, C. and Keller, C. (1996) Motor control of the jamming avoidance response of Apteronotus leptorhyncus - evolutionary changes of a behavior and its neuronal substrates. J. Comp. Physiol. 179, 653-674.
17. Hestrin, S., Sah, P. and Nicoll, R. A. (1990). Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5, 247-253.
18. Hollmann, M., Boulter, J., Maron, C., Beasley, J., Pecht, G. and Heinemann, S. (1993). Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor. Neuron 10, 943-954.
19. Hollmann, M. and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
20. Hollmann, M., Maron, C. and Heinemann, S. (1994). N-glycosylation site tagging suggests a three transmembrane domain topology for the glutamate receptor GluR1. Neuron 13, 1331-1343.
21. Ikeda, K., Nagasqwa, M., Mory, H., Araki, K., Sakimura, K., Watanabe, M., Inoue, Y. and Mishima, M. (1992). Cloning and expression of ε4 subunits of the NMDA receptor channel. FEBS Lett. 313, 34-38.
22. Ishii, T., Moriyoshi, K., Sugihara, H., Sakurada, K., Kadotani, H., Yokoi, M., Akazawa, C., Shigemoto, R., Mizuno, N., Masu, M. and et al. (1993). Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 268, 2836-2843.
23. Johnson, J. W. and Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
24. Johnson, R. R., Jiang, X. and Burkhalter, A. (1996). Regional and laminar differences in synaptic localization of NMDA receptor subunit NR1 splice variants in rat visual cortex and hippocampus. J. Comp. Neurol. 368, 335-355.
25. Karp, S. J., Masu, M., Eki, T., Ozawa, K. and Nakanishi, S. (1993). Molecular cloning and chromosomal localization of the key subunit of the human N-methyl-D-aspartate receptor. J. Biol. Chem. 268, 3728-3733.
26. Kleckner, N. W. and Dingledine, R. (1988). Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241, 835-837.
27. Krupa, M. and Crepel, F. (1990). Transient sensitivity of rat cerebellar Purkinje cells to N-methyl-D-aspartate during development. Eur. J. Neurosci. 2, 312-316.
28. Kurosawa, N., Kondo, K., Kimura, N., Ikeda, T. and Tsukada, Y. (1994). Molecular cloning and characterization of avian N-methyl-D-aspartate receptor type 1 (NMDA-R1) gene. Neurochem. Res. 19, 575-580.
29. Kutsuwada, T., Kashiwabuchi, N., Mori, H., Sakimura, K., Kushiya, E., Araki, K., Meguro, H., Masaki, H., Kumanishi, T., Arakawa, M. and et al. (1992). Molecular diversity of the NMDA receptor channel. Nature 358, 36-41.
30. Landwehrmeyer, G. B., Standaert, D. G., Testa, C. M., Penney, J. B. and Young, A. B. (1995). NMDA receptor subunit mRNA expression by projection neurons and interneurons in rat striatum. J. Neurosci. 15, 5297-5307.
31. Laube, B., Kuhse, J. and Betz, H. (1998). Evidence for a tetrameric structure of recombinant NMDA receptors. J. Neurosci. 18, 2954-2961.
32. Laurie, D. J., Putzke, J., Zieglgansberger, W., Seeburg, P. H. and Tolle, T. R. (1995). The distribution of splice variants of the NMDAR1 subunit mRNA in adult rat brain. Mol. Brian Res. 32, 94-108.
33. Laurie, D. J. and Seeburg, P. H. (1994). Regional and developmental heterogeneity in splicing of the rat brain NMDAR1 mRNA. J. Neurosci. 14, 3180-3194.
34. Lester, R. A. J., Clements, J. D., Westbrook, G. L. and Jahr, G. (1990). Channel kinetics determine the time course of NMDA receptor mediated synaptic currents. Nature 346, 565-567.
35. Liu, H., Wang, H., Sheng, M., Jan, L. Y., Jan, Y. N. and Basbaum, A. I. (1994). Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc. Natl. Acad. Sci. USA 91, 8383-8387.
36. MacDonald, J. F., Porietis, A. V. and Wojtowicz, J. M. (1982). L-Aspartic acid induces a region of negative slope conductance in the current voltage relationship of cultured spinal cord neurones. Brain Res. 237, 248-253.
37. Maler, L. and Monaghan, D. (1991). The distribution of excitatory amino acid binding sites in the brain of an electric fish, Apteronotus leptorhynchus. J. Chem. Neuroanat. 4, 39-61.
38. 2+ of NMDA responses in spinal cord neurons. Nature 309, 261-263.
39. Meguro, H., Mori, H., Araki, K., Kushiya, E., Kutsuwada, T., Yamazaki, M., Kumanishi, T., Arakawa, M., Sakimura, K. and Mishina, M. (1992). Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357, 70-74.
40. Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B. and Seeburg, P. H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540.
41. Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lorneli, H., Burnashev, N., Sakmann, B. and Seeburg, P. H. (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221.
42. Moriyoshi, K., Masu, M., Ishii, T., Shigemoto, R., Mizuno, N. and Nakanishi, S. (1991). Molecular cloning and characterization of the rat NMDA receptor. Nature 354, 31-37.
43. Nakanishi, N., Axel, R. and Shneider, N. A. (1992). Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. USA 89, 8552-8556.
44. Nicoll, R. A., Malenka, R. C. and Kauer, J. A. (1990). Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev. 70, 513-565.
45. Nowak, L., Bregestovski, P., Ascher, P., Herbet, A. and Prochiantz, A. (1984). Magnesium gates glutamate-activated channels in mouse central neurons. Nature 307, 462-465.
46. O'Hara, P. J., Sheppard, P. O., Thogersen, H., Venezia, D., Haldeman, B. A., McGrane, V., Houamed, K. M., Thomsen, C., Gilbert, T. L. and Mulvihill, E. R. (1993). The ligand-binding domain in metabotropic glutamate receptors is related to bacterial periplasmic binding proteins. Neuron 11, 41-52.
47. Paupard, M. C., Friedman, L. K. and Zukin, R. S. (1997). Developmental regulation and cell-specific expression of N-methyl-D-aspartate receptor splice variants in rat hippocampus. Neurosci. 79, 399-409.
48. Perkel, D. J., Hestrin, S., Sah, P. and Nicholl, R. A. (1990). Excitatory synaptic currents in Purkinje cells. Proc. R. Soc. Lond. B 241, 116-121.
49. Petralia, R. S., Wang, Y. X. and Wenthold, R. J. (1994a). The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J. Neurosci. 14, 6102-6120.
50. Petralia, R. S., Yokotani, N. and Wenthold, R. J. (1994b). Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14, 667-696.
51. Planells-Cases, R., Sun, W., Ferrer-Montiel, A. V. and Montai, M. (1993). Molecular cloning, functional expression and pharmacological characterization of an N-methyl-D-aspartate receptor subunit from human brain. Proc. Natl. Acad. Sci. USA 90, 5057-5061.
52. Sheng, M. and Kim, E. (1996). Ion channel associated proteins. Curr. Opin. Neurobiol. 6, 602-608.
53. Shumway, C. A. (1989a). Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. I. Physiological differences. J. Neurosci. 9, 4388-4399.
54. Shumway, C. A. (1989b). Multiple electrosensory maps in the medulla of weakly electric gymnotiform fish. II. Anatomical differences. J. Neurosci. 9, 4400-4415.
55. Soloviev, M. M., Brierley, M. J., Shao, Z. Y., Mellor, I. R., Volkova, T. M., Kamboj, R., Ishimaru, H., Sudan, H., Harris, J., Feldes, R. L., Grishin, E. V., Usherwood, P. N. R. and Barnard, E. A. (1996). Functional expression of a recombinant unitary glutamate receptor from Xenopus, which contains N-methyl-D-aspartate (NMDA) and non-NMDA receptor subunits. J. Biol. Chem. 271, 32572-32579.
56. Standaert, D. G., Landwehrmeyer, G. B., Kerner, J. A., Penney, J. B. and Young, A. B. (1996). Expression Of NMDAr2d glutamate receptor subunit mRNA in neurochemically identified interneurons in the rat neostriatum, neocortex and hippocampus. Mol. Brain Res. 42, 89-102.
57. Standaert, D. G., Testa, C. M., Young, A. B. and Penney, J. B., Jr (1994). Organization of N-methyl-D-aspartate glutamate receptor gene expression in the basal ganglia of the rat. J. Comp. Neurol. 343, 1-16.
58. Stern-Bach, Y., Bettler, B., Hartley, M., Sheppard, P. O., O'Hara, P. J. and Heinemann, S. F. (1994). Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid-binding proteins. Neuron 13, 1345-1357.
59. Sugihara, H., Moriyoshi, K., Ishii, T., Masu, M. and Nakanishi, S. (1992). Structures and properties of 7 isoforms of the NMDA receptor generated by alternative splicing. Biochem. Biophys. Res. Commun. 185, 826-832.
60. Traynelis, S. F., Burgess, M. F., Zheng, F., Lyuboslavsky, P. and Powers, J. L. (1998). Control of voltage-independent zinc inhibition of NMDA receptors by the NR1 subunit. J. Neurosci. 18, 6163-6175.
61. Traynelis, S. F., Hartley, M. and Heinemann, S. F. (1995). Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science 268, 873-876.
62. Vicini, S., Wang, J. F., Li, J. H., Zhu, W. J., Wang, Y. H., Luo, J. H., Wolfe, B. B. and Grayson, D. R. (1998). Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J. Neurophysiol. 79, 555-566.
63. Watanabe, M., Mishina, M. and Inoue, Y. (1994). Distinct spatiotemporal distributions of the N-methyl-D-aspartate receptor channel subunit mRNAs in the mouse cervical cord. J. Comp. Neurol. 345, 314-319.
64. Wo, G. Z. and Oswald, R. E. (1994). Transmembrane topology of two kainate receptor subunits revealed by N-glycosylation. Proc. Natl. Acad. Sci. USA 91, 7154-7158.
65. Zhang, S., Ehlers, M. D., Bernhardt, J. P., Su, C.-T. and Huganir, R. L. (1998). Calmodulin mediates calcium-dependent inactivation of N-methyl-D-aspartate receptors. Neuron 21, 443-453.
66. Zheng, F., Gingrich, M. B., Traynelis, S. F. and Conn, P. J. (1998). Tyrosine kinase potentiates NMDA receptor currents by reducing tonic zinc inhibition. Nature Neurosci. 1, 185-191.
67. 2+ potentiation of recombinant NMDA receptors. Neuron 12, 811-818.