Presynaptic NMDA receptor subunit immunoreactivity in GABAergic terminals in rat brain

Journal of Comparative Neurology

Volumn 423, Issue 2, 2000, Pages 330-347

  Paquet, Maryse ^a   Smith, Yoland ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

aminobutyric acid; Bed nucleus of the stria terminalis; Extended amygdala; Paraventricular nucleus; Stress

Indexed keywords

4 AMINOBUTYRIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; GABAERGIC TRANSMISSION; IMMUNOCYTOCHEMISTRY; MALE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS; ULTRASTRUCTURE;

ANIMALS; BRAIN; BRAIN CHEMISTRY; BRAIN MAPPING; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MALE; NERVE FIBERS; NEURONS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0034710306     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/1096-9861(20000724)423:2<330::AID-CNE10>3.0.CO;2-9     Document Type: Article

References (101)

1. Abdullah LH, Ordronneau P, Petrusz P. 1992. Molecular requirements for hapten binding to antibodies against glutamate and aspartate. Neuroscience 51:729-738.
2. Akazawa C, Shigemoto R, Bessho Y, Nakanishi S, Mizuno N. 1994. Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J Comp Neurol 347:150-160.
3. Aoki C, Venkatesan C, Go C-G, Mong JA, Dawson TM. 1994. Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. J Neurosci 14:5202-5222.
4. Aoki C, Rhee J, Lubin M, Dawson TM. 1997. NMDA-R1 subunit of the cerebral cortex co-localizes with neuronal nitric oxide synthase at preand postsynaptic sites and in spines. Brain Res 750:25-40.
5. Attwell D, Barbour B, Szatkowski M. 1993. Nonvesicular release of neurotransmitter. Neuron 11:401-407.
6. Bauerfeind R, Jelinek R, Hellwig A, Huttner WB. 1995. Neurosecretory vesicles can be hybrids of synaptic vesicles and secretory granules. Proc Natl Acad Sci USA 92:7342-7346.
7. Berk ML, Finkelstein JA. 1981. Afferent projections to the preoptic area and hypothalamic regions in the rat brain. Neuroscience 6:1601-1624.
8. Bernard V, Somogyi P, Bolam JP. 1997. Cellular, subcellular, and subsynaptic distribution of AMPA-type glutamate receptor subunits in the neostriatum of the rat. J Neurosci 17:819-833.
9. Bernath S, Zigmond MJ. 1990. Calcium-independent GABA release from striatal slices: the role of calcium channels. Neuroscience 36:677-682.
10. Boudaba C, Szabó K, Tasker JG. 1996. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 16:7151-7160.
11. Breukel AIM, Besselsen E, Lopes de Silva FH, Ghijsen WEJM. 1998. A presynaptic N-methyl-D-aspartate autoreceptor in rat hippocampus modulating amino acid release from a cytoplasmic pool. Eur J Neurosci 10:106-114.
12. Buijs RM, Hou Y-X, Shinn S, Renaud LP. 1994. Ultrastructural evidence for intra- and extranuclear projections of GABAergic neurons of the suprachiasmatic nucleus. J Comp Neurol 340:381-391.
13. Canteras NS, Simerly RB, Swanson LW. 1995. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360:213-245.
14. Chazot PL, Stephenson FA. 1997. Biochemical evidence for the existence of a pool of unassembled C2 exon-containing NR1 subunits of the mammalian forebrain NMDA receptor. J Neurochem. 68:507-516.
15. Chéramy A, Desce JM, Godeheu G, Glowinski J. 1994. Presynaptic control of dopamine synthesis and release by excitatory amino acids in rat striatal synaptosomes. Neurochem Int 25:145-154.
16. Chéramy A, Godeheu G, L'Hirondel M, Glowinski J. 1996. Cooperative contributions of cholinergic and NMDA receptors in the presynaptic control of dopamine release from synaptosomes of the rat striatum. J Pharmacol Exp Ther 276:616-625.
17. Chittajallu R, Vignes M, Dev KK, Barnes JM, Collingridge GL, Henley JM. 1996. Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379:78-81.
18. Connick JH, Stone TW. 1988. Excitatory amino acid antagonists and endogenous aspartate and glutamate release from rat hippocampal slices. Br J Pharmacol 93:863-867.
19. Conti F, Minelli A, Molnar M, Brecha NC. 1994. Cellular localization and laminar distribution of NMDAR1 mRNA in the rat cerebral cortex. J Comp Neurol 343:554-565.
20. Conti F, Minelli A, DeBiasi S, Melone M. 1997. Neuronal and glial localization of NMDA receptors in the cerebral cortex. Mol Neurobiol 14:1-18.
21. 3H]γ-aminobutyric acid release by kainate receptor activation in rat hippocampal synaptosomes. Eur J Pharmacol 323:167-172.
22. DeBiasi S, Minelli A, Melone M, Conti F. 1996. Presynaptic NMDA receptors in the neocortex are both auto- and heteroreceptors. Neuroreport 7:2773-2776.
23. Decavel C, VanDenPol AN. 1992. Converging GABA- and glutamate-immunoreactive axons make synaptic contact with identified hypothalamic neurosecretory neurons. J Comp Neurol 316:104-116.
24. Desce JM, Godeheu G, Galli T, Artaud F, Chéramy A, Glowinski J. 1992. L-glutamate-evoked release of dopamine from synaptosomes of the rat striatum: involvement of AMPA and N-methyl-D-aspartate receptors. Neuroscience 47:333-339.
25. Farb CR, Aoki C, Ledoux JE. 1995. Differential localization of NMDA and AMPA receptor subunits in the lateral and basal nuclei of the amygdala: a light and electron microscopic study. J Comp Neurol. 362:86-108.
26. Fillenz M. 1995. Physiological release of excitatory amino acids. Behav Brain Res 71:51-67.
27. Fink K, Göthert M. 1992. Presynaptic site of action underlying the ethanol-induced inhibition of norepinephrine release evoked by stimulation of N-methyl-D-aspartate (NMDA) receptors in rat cerebral cortex. Brain Res 572:27-32.
28. Gannon RL, Terrian DM. 1991. Presynaptic modulation of glutamate and dynorphin release by excitatory amino acids in the guinea-pig hippocampus. Neuroscience 41:401-410.
29. Glitsch M, Marty A. 1999 Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci 19:511-519.
30. Göthert M, Fink K. 1991. Stimulation of noradrenaline release in the cerebral cortex via presynaptic N-methyl-D-aspartate (NMDA) receptors and their pharmacological characterization. J Neural Transm [Suppl] 34:121-127.
31. Gracy KN, Pickel VM. 1995. Comparative ultrastructural localization of the NMDAR1 glutamate receptor in the rat basolateral amygdala and bed nucleus of the stria terminalis. J Comp Neurol 362:71-85.
32. Gracy KN Pickel VM. 1996. Ultrastructural immunocytochemical localization of the N-methyl-D-aspartate receptor and tyrosine hydroxylase in the shell of the rat nucleus accumbens. Brain Res 739:169-181.
33. Gracy KN, Svingos AL, Pickel VM. 1997. Dual ultrastructural localization of μ-opioid receptors and NMDA-type glutamate receptors in the shell of the rat nucleus accumbens. J Neurosci 17:4839-4848.
34. Gray TS, Magnuson DJ. 1992. Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat. Peptides 13:451-460.
35. Gray TS, Carney ME, Magnuson DJ. 1989. Direct projections from the central amygdaloid nucleus to the hypothalamic paraventricular nucleus: possible role in stress-induced adrenocorticotropin release. Neuroendocrinology 50:433-446.
36. Gritti I, Mainville L, Jones BE. 1994. Projections of GABAergic and cholinergic basal forebrain and GABAergic preoptic-anterior hypothalamic neurons to the posterior lateral hypothalamus of the rat. J Comp Neurol 339:251-268.
37. Hepler JR, Toomim CS, McCarthy KD, Conti F, Battaglia G, Rustioni A, Petrusz P. 1988. Characterization of antisera to glutamate and aspartate. J Histochem Cytochem 36:13-22.
38. Herman JP, Cullinan WE. 1997. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20: 78-84.
39. Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P. 1985. Antisera to γ-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229-239.
40. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Annu Rev Neurosci 17: 31-108.
41. 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.
42. Holstege G, Meiners L, Tan K. 1985. Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons, and medulla oblongata in the cat. Exp Brain Res 58:379-391.
43. Janáky R, Saransaari P, Oja SS. 1993. Release of GABA from rat hippocampal slices: involvement of quisqualate/N-methyl-D-aspartate-gated ionophores and extracellular magnesium. Neuroscience 53:779-785.
44. Jongen-Rêlo AL, Amaral DG. 1998. Evidence for a GABAergic projection from the central nucleus of the amygdala to the brainstem of the macaque monkey: a combined retrograde tracing and in situ hybridization study. Eur J Neurosci 10:2924-2933.
45. Kharazia VN, Wenthold RJ, Weinberg RJ. 1996. GluR1-immunopositive interneurons in rat neocortex. J Comp Neurol 368:399-412.
46. Krebs MO, Desce JM, Kernel ML, Gauchy C, Godeheu G, Chéramy A, Glowinski J. 1991. Glutamatergic control of dopamine release in the rat striatum: evidence for presynaptic N-methyl-D-aspartate receptors on dopaminergic nerve terminals. J Neurochem 56:81-85.
47. Kullmann DM, Asztely F. 1998. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci 21:8-14.
48. Landwehrmeyer GB, Standaert DG, Testa CM, Penney JB Jr, Young AB. 1995. NMDA receptor subunit mRNA expression by projection neurons and interneurons in rat striatum. J Neurosci 15:5297-5307.
49. Lauweryns JM, Van Ranst L, Verhofstad AA. 1986. Ultrastructural localization of serotonin in the intrapulmonary neuroepithelial bodies of neonatal rabbits by use of immunoelectron microscopy. Cell Tissue Res 243:455-459.
50. Levi G, Raiteri M. 1993. Carrier-mediated release of neurotransmitters. Trends Neurosci 16:415-419.
51. Liu H, Wang H, Sheng M, Jan LY, Jan YN, Basbaum AI. 1994a. Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci USA 91:8383-8387.
52. Liu H, Mantyh PW, Basbaum AI. 1997. NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature 386: 721-724.
53. Liu J, Moghaddam B. 1995. Regulation of glutamate efflux by excitatory amino acid receptors: evidence for tonic inhibitory and phasic excitatory regulation. J Pharmacol Exp Ther 274:1209-1215.
54. Liu Y, Schweitzer ES, Nirenberg MJ, Pickel VM, Evans CJ, Edwards RH. 1994b. Preferential localization of a vesicular monoamine transporter to dense core vesicles in PC12 cells. J Cell Biol 127:1419-1433.
55. Liu X-B. 1997. Subcellular distribution of AMPA and NMDA receptor subunit immunoreactivity in ventral posterior and reticular nuclei of rat and cat thalamus. J Comp Neurol 388:587-602.
56. Llona I, Annaert WG, Jacob W, De Potter WP. 1994. Co-storage in large "dense-core" vesicles of dopamine and cholecystokinin in rat striatum. Neurochem Int 25:573-581.
57. MacDermott AB, Role LW, Siegelbaum SA. 1999. Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22:443-485.
58. Martin D, Bustos GA, Bowe MA, Bray SD, Nadler JV. 1991. Autoreceptor regulation of glutamate and aspartate release from slices of the hippocampal CA1 area. J Neurochem 56:1647-1655.
59. Martin LJ, Blackstone CD, Levey AI, Huganir RL, Price DL. 1993. AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53:327-358.
60. 1A receptors in guinea pig dentate gyrus. Brain Res 761:105-112.
61. Meister B, Hökfelt T, Geffard M, Oertel W. 1988. Glutamic acid decarboxylase- and γ-aminobutyric acid-like immunoreactivities in corticotropin-releasing factor-containing parvocellular neurons of the hypothalamic paraventricular nucleus. Neuroendocrinology 48:516-526.
62. Moga MM, Saper CB, Gray TS. 1989. Bed nucleus of the stria terminalis: cytoarchitecture, immunohistochemistry, and projection to the parabrachial nucleus in the rat. J Comp Neurol 283:315-332.
63. Moga MM, Herbert H, Hurley KM, Yasui Y, Gray TS, Saper CB. 1990. Organization of cortical, basal forebrain, and hypothalamic afferents to the parabrachial nucleus in the rat. J Comp Neurol 295:624-661.
64. Monck JR, Fernandez JM. 1994. The exocytic fusion pore and neurotransmitter release. Neuron 12:707-716.
65. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S. 1991. Molecular cloning and characterization of the rat NMDA receptor. Nature 354: 31-37.
66. Nash NR, Heilman CJ, Rees HD, Levey AI. 1997. Cloning and localization of exon 5-containing isoforms of the NMDAR1 subunit in human and rat brains. J Neurochem 69:485-493.
67. Paxinos G. 1995. The rat nervous system. San Diego: Academic Press.
68. Perouansky M, Grantyn R. 1990. Is GABA release modulated by presynaptic excitatory amino acid receptors? Neurosci Lett 113:292-297.
69. Petralia RS, Wenthold RJ. 1992. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J Comp Neurol 318:329-354.
70. Petralia RS, Wang Y-X, Wenthold RJ. 1994a. Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J Comp Neurol 349:85-110.
71. Petralia RS, Yokotani N, Wenthold RJ. 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.
72. Petralia RS, Wang Y-X, Wenthold RJ. 1994c. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14:6102-6120.
73. Phend KD, Weinberg RJ, Rustioni A. 1992. Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J Histochem Cytochem 40:1011-1020.
74. Pickel VM, Chan J, Veznedaroglu E, Milner JA. 1995a. Neuropeptide Y and dynorphin-immunoreactive large dense-core vesicles are strategically localized for presynaptic modulation in the hippocampal formation and substantia nigra. Synapse 19:160-169.
75. Pickel VM, Van Bockstaele EJ, Chan J, Cestari DM. 1995b. Amygdala efferents form inhibitory-type synapses with a subpopulation of catecholaminergic neurons in the rat nucleus tractus solitarius. J Comp Neurol 362:510-523.
76. Pin J-P, Bockaert J. 1989. Two distinct mechanisms, differentially affected by excitatory amino acids, trigger GABA release from fetal mouse striatal neurons in primary culture. J Neurosci 9:648-656.
77. Pin J-P, Duvoisin R. 1995. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26.
78. Pittaluga A, Raiteri M. 1990. Release-enhancing glycine-dependent presynaptic NMDA receptors exist on noradrenergic terminals of hippocampus. Eur J Pharmacol 191:231-234.
79. Prewitt CMF, Herman JP. 1998. Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis. J Chem Neuroanatomy 15:173-185.
80. Reynolds ES. 1963. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208-212.
81. Rizvi TA, Ennis M, Behbehani MM, Shipley MT. 1991. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303:121-131.
82. Rodriguez-Moreno A, Herreras O, Lerma J. 1997. Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19:893-901.
83. Roland BL, Sawchenko PE. 1993. Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 332:123-143.
84. Sato K, Mick G, Kiyama H, Tohyama M. 1995. Expression patterns of a glutamate-binding protein in the rat central nervous system: comparison with N-methyl-D-aspartate receptor subunit 1 in rat. Neuroscience 64:459-475.
85. Sawchenko PE, Swanson LW. 1983. The organization of forebrain afferents to the paraventricular and supraoptic nuclei of the rat. J Comp Neurol 218:121-144.
86. Seeburg PH, Monyer H, Sprengel R, Burnashev N. 1994. Molecular biology of NMDA receptors. In: Collingridge GL, Watkins JC, editors: The NMDA receptor . New York: Oxford University Press. p 147-157.
87. Sidibé M, Paquet M, Levey AI, Smith Y. 1997. NMDAR1 subunit immunoreactivity in presynaptic terminals: electron microscopic characterization and species difference between rats and monkeys. Soc Neurosci 23:1752.
88. Smith Y, Koylu EO, Couceyro P, Kuhar MJ. 1997. Ultrastructural localization of CART (cocaine- and amphetamine-regulated transcript) peptides in the nucleus accumbens of monkeys. Synapse 27:90-94.
89. Smith Y, Kieval J, Couceyro PR, Kuhar MJ. 1999. CART peptide-immunoreactive neurones in the nucleus accumbens in monkeys: ultrastructural analysis, colocalization studies, and synaptic interactions with dopaminergic afferents. J Comp Neurol 407:491-511.
90. Standaert DG, Testa CM, Young AB, Penney JB 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.
91. Sugihara H, Moriyoshi K, Ishii T, Masu M, Nakanishi S. 1992. Structures and properties of seven isoforms of the NMDA receptor generated by alternative splicing. Biochem Biophys Res Commun 185:826-832.
92. Swanson LW. 1992. Brain maps: structure of the rat brain. Amsterdam: Elsevier Press.
93. Tasker JG, Dudek FE. 1993. Local inhibitory synaptic inputs to neurones of the paraventricular nucleus in slices of rat hypothalamus. J Physiol 469:179-192.
94. Van Bockstaele EJ, Colago EEO. 1996. Selective distribution of the NMDA-R1 glutamate receptor in astrocytes and presynaptic axon terminals in the nucleus locus coeruleus of the rat brain: an immunoelectron microscopic study. J Comp Neurol 369:483-496.
95. Van Bockstaele EJ, Char J, Pickel VM. 1996. Input from central nucleus of the amygdala efferents to pericoerulear dendrites, some of which contain tyrosine hydroxylase immunoreactivity. J Neurosci Res 45:289-302.
96. Wang JKT. 1991. Presynaptic glutamate receptors modulate dopamine release from striatal synaptosomes. J Neurochem 57:819-822.
97. Wang JKT, Andrews H, Thukral V. 1992. Presynaptic glutamate receptors regulate noradrenaline release from isolated nerve terminals. J Neurochem 58:204-211.
98. Weiss S. 1990. Pharmacological properties of the N-methyl-D-aspartate receptor system coupled to the evoked release of γ-[3H]aminobutyric acid from striatal neurons in primary culture. J Pharmacol Exp Ther 252:380-386.
99. Young AMJ, Bradford HF. 1993. N-methyl-D-aspartate releases γ-aminobutyric acid from rat striatum in vivo: a microdialysis study using a novel preloading method. J Neurochem 60:487-492.
100. Zhang X, Bao L, Arvidsson U, Elde R, Hökfelt T. 1998. Localization and regulation of the delta-opioid receptor in dorsal root ganglia and spinal cord of the rat and monkey: evidence for association with the membrane of large dense-core vesicles. Neuroscience 82:1225-1242.
101. Zukin RS, Bennett MVL. 1995. Alternatively spliced isoforms of the NMDAR1 receptor subunit. Trends Neurosci 18:306-313.