Kinetics and subunit composition of NMDA receptors in respiratory-related neurons

Journal of Neurochemistry

Volumn 93, Issue 4, 2005, Pages 812-824

  Paarmann, I ^a,b   Frermann, D ^c   Keller, B U ^c   Villmann, C ^d   Breitinger, H G ^d,f   Hollmann, M ^a,e  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e RUHR UNIVERSITY BOCHUM   (Germany)

^f German University in Cairo   (Egypt)

Author keywords

Hypoglossal nucleus; N methyl D aspartate receptor kinetics; Nucleus tractus solitarius; Pre B tzinger complex; Rat; Reverse transcription polymerase chain reaction

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2C; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2D; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 3A; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; BREATHING; CELL HETEROGENEITY; CHEMICAL COMPOSITION; CONTROLLED STUDY; HYPOGLOSSAL NERVE; INTERNEURON; KINETICS; MEDULLA OBLONGATA; MOTONEURON; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOLITARY TRACT NUCLEUS; STRUCTURE ANALYSIS;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANIMALS, NEWBORN; BLOTTING, NORTHERN; BRAIN STEM; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; N-METHYLASPARTATE; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN SUBUNITS; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; RESPIRATION; RESTRAINT, PHYSICAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VALINE;

EID: 18844367663     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03027.x     Document Type: Article

References (61)

1. Ambalavanar R., Ludlow C. L., Wenthold R. J., Tanaka Y., Damirjian M. and Petralia R. S. (1998) Glutamate receptor subunits in the nucleus of the tractus solitarius and other regions of the medulla oblongata in the cat. J. Comp. Neurol. 402, 75-92.
2. 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.
3. Bassand P., Bernard A., Rafiki A., Gayet D. and Khrestchatisky M. (1999) Differential interaction of the tSXV motifs of the NR1 and NR2A NMDA receptor subunits with PSD-95 and SAP97. Eur. J. Neurosci. 11, 2031-2043.
4. Benke D., Wenzel A., Scheuer L., Fritschy J. M. and Mohler H. (1995) Immunobiochemical characterization of the NMDA-receptor subunit NR1 in the developing and adult rat brain. J. Recept. Signal. Transduct. Res. 15, 393-411.
5. Bonham A. C. (1995) Neurotransmitters in the CNS control of breathing. Respir. Physiol 101, 219-230.
6. Ceccon M., Rumbaugh G. and Vicini S. (2001) Distinct effect of pregnenolone sulfate on NMDA receptor subtypes. Neuropharmacology 40, 491-500.
7. Chatterton J. E., Awobuluyi M., Premkumar L. S. et al. (2002) Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415, 793-798.
8. Cull-Candy S., Brickley S. and Farrant M. (2001) NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 11, 327-335.
9. D'Angelo E., Rossi P. and Taglietti V. (1994) Voltage-dependent kinetics of N-methyl-D-aspartate synaptic currents in rat cerebellar granule cells. Eur. J. Neurosci. 6, 640-645.
10. Das S., Sasaki Y. F., Rothe T. et al. (1998) Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393, 377-381.
11. Del Negro C. A., Koshiya N., Butera R. J. Jr and Smith J. C. (2002) Persistent sodium current, membrane properties and bursting behavior of pre-Botzinger complex inspiratory neurons in vitro. J. Neurophysiol. 88, 2242-2250.
12. Dodt H. U. and Zieglgansberger W. (1994) Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci. 17, 453-458.
13. 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.
14. 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.
15. 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.
16. Forrest D., Yuzaki M., Soares H. D., Ng L., Luk D. C., Sheng M., Stewart C. L., Morgan J. I., Connor J. A. and Curran T. (1994) Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron 13, 325-338.
17. Frermann D., Keller B. U. and Richter D. W. (1999) Calcium oscillations in rhythmically active respiratory neurones in the brainstem of the mouse. J. Physiol. (Lond.) 515, 119-131.
18. Hollmann M., Boulter J., Maron C., Beasley L., Sullivan 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. Holmes K. D., Mattar P., Marsh D. R., Jordan V., Weaver L. C. and Dekaban G. A. (2002) The C-terminal C1 cassette of the N-methyl-D-aspartate receptor 1 subunit contains a bi-partite nuclear localization sequence. J. Neurochem. 81, 1152-1165.
20. Ikeda K., Nagasawa M., Mori H., Araki K., Sakimura K., Watanabe M., Inoue Y. and Mishina M. (1992) Cloning and expression of the ε4 subunit of the NMDA receptor channel. FEBS Lett. 313, 34-38.
21. Ishii T., Moriyoshi K., Sugihara H. et al. (1993) Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J. Biol. Chem. 268, 2836-2843.
22. Jacquin T. D., Borday V., Schneider-Maunoury S., Topilko P., Ghilini G., Kato F., Charnay P. and Champagnat J. (1996) Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron 17, 747-758.
23. Katakura N., Jia L. and Nakamura Y. (1995) NMDA-induced rhythmical activity in XII nerve of isolated CNS from newborn rats. Neuroreport 6, 601-604.
24. Keller B. U., Konnerth A. and Yaari Y (1991) Patch clamp analysis of excitatory synaptic currents in granule cells of rat hippocampus. J. Physiol. (Lond.) 435, 275-293.
25. Kirson E. D. and Yaari Y. (1996) Synaptic NMDA receptors in developing mouse hippocampal neurones: functional properties and sensitivity to ifenprodil. J. Physiol. (Lond.) 497, 437-455.
26. Konnerth A., Keller B. U. and Lev-Tov A. (1990) Patch clamp analysis of excitatory synapses in mammalian spinal cord slices. Pflügers Arch. 417, 285-290.
27. Kornau H. C., Schenker L. T., Kennedy M. B. and Seeburg P. H. (1995) Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737-1740.
28. Kutsuwada T., Kashiwabuchi N., Mori H. et al. (1992) Molecular diversity of the NMDA receptor channel. Nature 358, 36-41.
29. Lambolez B., Audinat E., Bochet P., Crepel F. and Rossier J. (1992) AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247-258.
30. Laube B., Kuhse J. and Betz H. (1998) Evidence for a tetrameric structure of recombinant NMDA receptors. J. Neurosci. 18, 2954-2961.
31. 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.
32. Laurie D. J., Bartke I., Schoepfer R., Naujoks K. and Seeburg P. H. (1997) Regional, developmental and interspecies expression of the four NMDAR2 subunits, examined using monoclonal antibodies. Brain Res. Mol. Brain Res. 51, 23-32.
33. Lin J. W., Wyszynski M., Madhavan R., Sealock R., Kim J. U. and Sheng M. (1998) Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1. J. Neurosci. 18, 2017-2027.
34. Malayev A., Yaghoubi N., Russek S., Gibbs T. and Farb D. (1998) Effects of neurosteroids on NMDA receptors comprising different isoforms of the NMDAR1 subunit. Soc. Neurosci. Abstr. 24, 847.
35. Matsuda K., Kamiya Y., Matsuda S. and Yuzaki M. (2002) Cloning and characterization of a novel NMDA receptor subunit NR3B: a dominant subunit that reduces calcium permeability. Brain Res. Mol. Brain Res. 100, 43-52.
36. Matsuda K., Fletcher M., Kamiya Y. and Yuzaki M. (2003) Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors. J. Neurosci. 23, 10 064-10 073.
37. Monyer H., Sprengel R., Schoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B. and Seeburg P. H. (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221.
38. 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.
39. Morino M., Maeda M., Nakai M., Krieger A. J. and Sapru H. N. (1994) Effects of microinjection of N-methyl-D-aspartic acid into the nucleus tractus solitarii on cerebral blood flow in anesthetized rats. J. Auton. Nerv. Syst. 49, 159-170.
40. Mu Y., Otsuka T., Horton A. C., Scott D. B. and Ehlers M. D. (2003) Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 40, 581-594.
41. Nishi M., Hinds H., Lu H.-P., Kawata M. and Hayashi Y. (2001) Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J. Neurosci. 21, 1-6.
42. O'Brien J. A., Isaacson J. S. and Berger A. J. (1997) NMDA and non-NMDA receptors are co-localized at excitatory synapses of rat hypoglossal motoneurons. Neurosci. Lett. 227, 5-8.
43. Otsuka H., Lindahl S. G., Lagercrantz H. and Yamamoto Y. (1994) Effects of NMDA and non-NMDA receptor antagonists on inspiratory neurons in the in vitro brainstem-spinal cord preparation of newborn rat. Neurosci. Lett. 171, 94-96.
44. Paarmann I., Frermann D., Keller B. U. and Hollmann M. (2000) Expression of 15 glutamate receptor subunits and various splice variants in tissue slices and single neurons of brainstem nuclei and potential functional implications. J. Neurochem. 74, 1335-1345.
45. Perouansky M. and Yaari Y. (1993) Kinetic properties of NMDA receptor-mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones. J. Physiol. (Lond.) 465, 223-244.
46. 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.
47. 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.
48. Pierrefiche O., Foutz A. S., Champagnat J. and Denavit-Saubie M. (1994) NMDA and non-NMDA receptors may play distinct roles in timing mechanisms and transmission in the feline respiratory network. J. Physiol. (Lond.) 474, 509-523.
49. Rumbaugh G., Prybylowski K., Wang J. F. and Vicini S. (2000) Exon 5 and spermine regulate deactivation of NMDA receptor subtypes. J. Neurophysiol. 83, 1300-1306.
50. Sachs L. (1974) Angewandte Stastistik, 4th edn. Springer-Verlag, Berlin/ Heidelberg/New York.
51. Smith J. C., Greer J. J., Liu G. S. and Feldman J. L. (1990) Neural mechanisms generating respiratory pattern in mammalian brain stem-spinal cord in vitro. I. Spatiotemporal patterns of motor and medullary neuron activity. J. Neurophysiol. 64, 1149-1169.
52. Standley S., Roche K. W., McCallum J., Sans N. and Wenthold R. J. (2000) PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887-898.
53. Sucher N. J., Akbarian S., Chi C. L., Leclerc C. L., Awobuluyi M., Deitcher D. L., Wu M. K., Yuan J. P., Jones E. G. and Lipton S. A. (1995) Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J. Neurosci. 15, 6509-6520.
54. Sugihara H., Moriyoshi K., Ishii T., Masu M. and Nakanishi S. (1992) Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem. Biophys. Res. Commun. 185, 826-832.
55. Titz S. and Keller B. U. (1997) Rapidly deactivating AMPA receptors determine excitatory synaptic transmission to interneurons in the nucleus tractus solitarius from rat. J. Neurophysiol. 78, 82-91.
56. Vicini S., Wang J. F., Li J. H., Zhu W. J., Wang Y. H., Luo J. A. 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.
57. Watanabe M., Inoue Y., Sakimura K. and Mishina M. (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3, 1138-1140.
58. Watanabe M., Mishina M. and Inoue Y. (1994) Distinct distributions of five NMDA receptor channel subunit mRNAs in the brainstem. J. Comp. Neurol. 343, 520-531.
59. Wenzel A., Scheurer L., Kunzi R., Fritschy J. M., Mohler H. and Benke D. (1995) Distribution of NMDA receptor subunit proteins NR2A, 2B, 2C and 2D in rat brain. Neuroreport 7, 45-48.
60. Wenzel A., Villa M., Mohler H. and Benke D. (1996) Developmental and regional expression of NMDA receptor subtypes containing the NR2D subunit in rat brain. J. Neurochem. 66, 1240-1248.
61. Zheng X., Zhang L., Durand G. M., Bennett M. V. and Zukin R. S. (1994) Mutagenesis rescues spermine and Zn2+ potentiation of recombinant NMDA receptors. Neuron 12, 811-818.