Cellular expression of ionotropic glutamate receptor subunits on specific striatal neuron types and its implication for striatal vulnerability in glutamate receptor-mediated excitotoxicity

Neuroscience

Volumn 73, Issue 3, 1996, Pages 715-731

  Chen, Q ^a   Veenman, C L ^a   Reiner, A ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

AMPA; excitatory amino acids; kainate; neurodegenerative disease; NMDA; striatum

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALBINDIN; ENKEPHALIN; GLUTAMATE RECEPTOR; KAINIC ACID RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVALBUMIN; RECEPTOR SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL TYPE; CHOLINERGIC NERVE CELL; CORPUS STRIATUM; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; NERVE CELL; NERVE PROJECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

EID: 0030218538     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00011-5     Document Type: Article

References (97)

1. 1. Albin R. L., Reiner A., Anderson K. D., Dure IV L. S., Handelin B., Balfour R., Whetsell W. O., Penney J. B. and Young A. B. (1992) Preferential loss of striato-external pallidal projection neurons in presymptomatic Huntington's disease. Ann. Neurol. 31, 425-430.
2. 2. Anderson K. D. and Reiner A. (1991) Striatonigral projection neurons: a retrograde labeling study of the percentages that contain Substance P or enkephalin in pigeons. J. comp. Neurol. 303, 658-673.
3. 3. Araki T., Kato H., Liu X. H., Itoyama Y., Kogure K. and Kato K. (1994) Delayed damage of striatal interneurons after cerebral ischemia in the gerbil. Neurosci. Lett. 176, 17-20.
4. 4. Augood S. J., Mcgowan E. M. and Emson P. C. (1994) Expression of NMDA receptor subunit NR1 messenger RNA by identified striatal somatostatin cells. Neuroscience 59, 7-12.
5. 5. Beal M. F., Ferrante R. J., Swartz K. J. and Kowall N. W. (1991) Chronic quinolinic acid lesions in rats closely resemble Huntington's Disease. J. Neurosci. 11, 1649-1659.
6. 6. Beal M. F., Marshall P. E., Burd G. D., Landis D. and Martin J. B. (1985) Excitotoxin lesions do not mimic the alteration of somatostatin in Huntington's disease. Brain Res. 361, 135-145.
7. 7. Benveniste H., Drejer J., Schousboe A. and Diemer N. H. (1984) Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43, 1369-1374.
8. 8. Boegman R. J., Smith Y. and Parent A. (1987) Quinolinic acid does not spare striatal neuropeptide Y-immunoreactive neurons. Brain Res. 415, 178-182.
9. 14C]GABA uptake in the basal ganglia of rats following lesions in the subthalamic region suggests a role for excitatory amino acid but not GABA-mediated transmission in subthalamic nucleus efferents. Expl Neurol. 113, 171-181.
10. 10. Buchan A. M., Li H., Cho S. and Pulsinelli W. A. (1991) Blockade of the AMPA receptor prevents CA1 hippocampal injury following severe but transient forebrain ischemia in adult rats. Neurosci. Lett. 132, 255-258.
11. 11. Chen Q., Harris C., Brown C. S., Surmeier D. J. and Reiner A. (1993) Glutamate-mediated excitotoxic death of cultured striatal neurons is mediated by non-NMDA glutamate receptors. Neurosci. Abstr. 19, 1342.
12. 12. Chesselet M. F., Gonzales C., Lin C. S., Polsky K. and Jin B. K. (1990) Ischemic damage in the striatum of adult gerbils: relative sparing of somatostatinergic and cholinergic interneurons contrasts with loss of efferent neurons. Expl Neurol. 110, 209-218.
13. 13. Choi D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
14. 14. Collingridge G. L. and Lester R. A. J. (1989) Excitatory amino acid receptors in the vertebrate central nervous system. Pharmac. Rev. 40, 143-209.
15. 15. Collingridge G. L. and Singer W. (1990) Excitatory amino acid receptors and synaptic plasticity. Trends Pharmac. Sci. 11, 290-296.
16. 16. Cowan R. L., Wilson C. J., Emson P. C. and Heizmann C. W. (1990) Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J. comp. Neurol. 302, 197-205.
17. 17. Coyle J. T. and Puttfarcken P. (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262, 689-695.
18. 18. Dawson T. M., Bredt D. S., Fotuhi M., Wang P. M. and Synder S. H. (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. natn. Acad. Sci. U.S.A. 88, 7797-7801.
19. 19. Dawson V. L., Dawson T. M., Bartley A. A., Uhl G. R. and Snyder S. H. (1993) Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures. J. Neurosci. 13, 2651-2661.
20. 20. Desce J. M., Godeheu G., Galli T., Artaud F., Cheramy A. and Glowinski J. (1992) L-Glutamate-evoked release of dopamine from synaptosomes of the rat striatum: involvement of AMPA and NMDA receptors. Neuroscience 47, 333-339.
21. 21. DiFiglia M. (1990) Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci. 13, 286-289.
22. 22. Ferrante R. J., Beal M. F., Kowall N. W., Richardson E. P. and Martin J. B. (1987) Sparing of acetylcholinesterase-containing striatal neurons in Huntington's disease. Brain Res. 411, 162-166.
23. 23. Ferrante R. J., Kowall N. W., Beal M. F., Richardson E. P., Bird E. D. and Martin J. B. (1985) Selective sparing of a class of striatal neurons in Huntington's disease. Science 230, 561-563.
24. 24. Ferriero D. M., Arcavi L. J., Sagar S. M., McIntosh T. K. and Simon R. P. (1988) Selective sparing of NADPH diaphorase neurons in neonatal hypoxic-ischemia. Ann. Neurol. 24, 670-676.
25. 25. Ferriero D. M. and Simon R. P. (1991) Neonatal striatal NADPH-diaphorase neurons are vulnerable to quisqualate and its analogue α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA). Neurosci. Lett. 126, 52-56.
26. 26. Figueredo-Cardenas G., Anderson K. D., Chen Q., Veenman C. L. and Reiner A. (1994) Relative survival of striatal projections neurons and interneurons after intrastriatal injection of QA in rats. Expl Neurol. 129, 37-56.
27. 27. Figueredo-Cardenas G., Baxter K., Nowak T. S., Pulsinelli W. and Reiner A. (1993) Global ischemia in rats yield striatal projection neuron and interneuron loss resembling Huntington's disease. Neurosci. Abstr. 19, 1652.
28. 28. Figueredo-Cardenas G., Chen Q. and Reiner A. (1992) Different survival pattern of striatal interneurons after slow vs fast intrastriatal injections of quinolinic acid. Neurosci. Abstr. 18, 167.
29. 29. Fonnum F., Storm-Mathisen J. and Divac I. (1981) Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibers in rat brain. Neuroscience 6, 863-873.
30. 30. Gasic G. P. and Hollmann M. (1992) Molecular neurobiology of glutamate receptors. A. Rev. Physiol. 54, 507-536.
31. 31. Gerfen C. R. (1992) The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. A. Rev. Neurosci. 15, 285-320.
32. 32. Gerfen C. R. and Young III W. S. (1988) Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res. 460, 161-167.
33. 33. Glovannini M. G., Camilli F., Mundula A., Bianchi L., Colivicchi M. A. and Pepeu G. (1995) Differential regulation by N-methyl-D-asparate and non-N-methyl-D-asparate receptors of acetylcholine release from the rat striatum in vivo. Neuroscience 65, 409-415.
34. 34. Harrington K. M. and Kowall N. W. (1991) Parvalbumin immunoreactive neurons resist degeneration in Huntington's disease striatum. J. Neuropath. exp. Neurol. 50, 309.
35. 35. Herb A., Burnashev N., Werner P., Sakmann B., Wisden W. and Seeburg P. H. (1992) The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8, 775-785.
36. 2+ permeability of KA-AMPA gated glutamate receptor channels depends on subunit composition. Science 252, 851-853.
37. 37. Hope B. T., Michael G., Knigge K. M. and Vincent S. R. (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. natn. Acad. Sci. U.S.A. 88, 2811-2814.
38. 38. Huntley G. W., Rogers S. W., Moran T., Janssen W., Archin W., Vickers J. C., Cauley K., Heinemann S. F. and Morrison J. H. (1993) Selective distribution of kainate receptor subunit immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J. Neurosci. 13, 2965-2981.
39. 39. Inagaki S., Suzuki K., Taniguchi N. and Takagi H. (1991) Localization of Mn-superoxide dismutase (Mn-SOD) in cholinergic and somatostatin-containing neurons in the rat neostriatum. Brain Res. 549, 174-177.
40. 40. Johnston M. V. and Hudson C. (1987) Effects of postnatal hypoxia-ischemia on cholinergic neurons in the rat forebrain: cholin acetyltransferase immunocytochemistry. Devl Brain. Res. 34, 41-50.
41. 41. Judge M. E., Sheardown M. J., Jacobsen P. and Honoré T. (1991) Protection against post-ischemic behavioral pathology by the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) antagonist 2,3-dihydroxy-6-nitro-7-sulfamoyl-2 5 benzoquinoxaline (NBQX) in the gerbil. Neurosci. Lett. 133, 291-294.
42. 42. Kawaguchi Y. (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci. 13, 4908-4923.
43. 43. Kawaguchi Y., Wilson C. J. and Emson P. C. (1990) Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biotin. J. Neurosci. 10, 3421-3438.
44. 44. Kita H. and Kitai S. T. (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. comp. Neurol. 260, 435-452.
45. 45. Kitai S. T., Kocsis J. D., Preston R. J. and Sugimori M. (1976) Monosynaptic inputs to caudate neurons identified by intracellular injection of horseradish peroxidase. Brain Res. 109, 601-606.
46. 46. Koh J. Y. and Choi D. W. (1988) Cultured striatal neurons containing NADPH-diaphorase or acetylcholinesterase are selectively resistant to injury by NMDA agonists. Brain Res. 446, 374-378.
47. 47. Lees G. J. (1993) Contributory mechanisms in the causation of neurodegenerative disorders. Neuroscience 54, 287-322.
48. 3H-TCP-labeled receptors in rat brain. J. Neurosci. 8, 493-501.
49. 49. Martin L. J., Blackstone C. D., Levey A. I., Huganir R. L. and Price D. L. (1993) AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53, 327-358.
50. 50. Massieu L. and Tapia R. (1994) 2,3-Dihydroxy-6-nitro-7-sulfamoyl-benzoquinoxaline protects against both AMPA and kainate-induced lesions in rat striatum in vivo. Neuroscience 59, 931-938.
51. 51. McGeer E. G. and McGeer P. L. (1976) Duplication of biochemical changes of Huntington's chorea by intrastriatal injections of glutamate and kainic acid. Nature 263, 517-519.
52. 52. Meldrum B. and Garthwaite J. (1990) Excitatory amino acid and neurotoxicity and neurodegenerative disease. Trends Pharmac. Sci. 11, 379-387.
53. 53. Monaghan D. T. and Beaton J. A. (1991) Quinolinate differentiates between forebrain and cerebellar NMDA receptors. Eur. J. Pharmac. 194, 123-125.
54. 54. Monaghan D. T., Bridges R. J. and Cotman C. W. (1989) The excitatory amino acid receptors: their class, pharmacology, and distinct properties in the function of the central nervous system. A. Rev. Pharmac. Toxic. 29, 365-402.
55. 55. 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.
56. 56. 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.
57. 57. Muller D., Joly M. and Lynch G. (1988) Contribution of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242, 1694-1697.
58. 58. Murphy S. N., Thayer S. A. and Miller R. J. (1987) The effects of excitatory amino acids on intracellular calcium in single neurons in vitro. J. Neurosci. 7, 4145-4158.
59. 59. Nowak L., Bregestovski P., Ascher P., Herbert A. and Prochiantz A. (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307, 462-465.
60. 60. Patneau D. K. and Mayer M. L. (1991) Kinetic analysis of interactions between kainate and AMPA: evidence for activation of a single receptor in mouse hippocampal neurons. Neuron 6, 785-798.
61. 61. Peillet E. L., Arvin B., Moncada C. and Meldrum B. S. (1992) The non-NMDA antagonists, NBQX and GYKI 52466, protect against cortical and striatal cell loss following transient global ischemia in the rat. Brain Res. 571, 115-120.
62. 61a. Paxinos G. and Watson C. (1982) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.
63. 62. Pellegrini-Giampietro D. E., Bennett M. V. and Zukin R. S. (1991) Differential expression of three glutamate receptor genes in developing rat brain: an in situ hybridization study. Proc. natn. Acad. Sci. U.S.A. 88, 4157-4161.
64. 63. Pellegrini-Giampietro D. E., Zukin R. S., Bennett M. V., Cho S. and Pulsinelli W. A. (1992) Switch in glutamate receptor subunit gene expression in CA1 subfield of hippocampus following global ischemia in rats. Proc. natn. Acad. Sci. U.S.A. 89, 10,499-19,503.
65. 64. Perez-Velazquez J. L. and Zhang L. (1994) In vitro hypoxia induces expression of the NR2C of the NMDA receptor in rat cortex and hippocampus. J. Neurochem. 63, 1171-1173.
66. 65. Perry T. L. and Hansen S. (1990) What excitotoxin kills striatal neurons in Huntington's disease? Clues from neurochemical studies. Neurology 40, 20-24.
67. 66. Petralia R. S. and Wenthold R. J. (1992) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. comp. Neurol. 318, 329-354.
68. 67. Petralia R. S., Yokotani N. and Wenthold R. J. (1994) 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.
69. 68. Price R. H., Mayer B. and Beitz A. J. (1993) Nitric oxide synthase neurons in rat brain express more NMDA receptor mRNA than non-NOS neurons. NeuroReport 4, 807-810.
70. 69. Pulsinelli W. A., Brierley J. B. and Plum F. (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11, 491-498.
71. 70. Reiner A., Albin R. L., Anderson K. D., D'Amato C. J., Penney J. B. and Young A. B. (1988) Differential loss of striatal projection neurons in Huntington's disease. Proc. natn. Acad. Sci. U.S.A. 85, 5733-5737.
72. 71. Reiner A. and Anderson K. D. (1990) The patterns of neurotransmitter and neuropeptide co-occurrence among striatal projection neurons: conclusions based on recent findings. Brain Res. Rev. 15, 251-265.
73. 72. Reiner A. and Chen Q. (1995) Localization of the NMDA receptor NR2A/2B subunits on specific striatal neuron types in rats. Neurosci. Abstr. 21, 1425.
74. 73. Roberts R. C., Ahn A., Swartz K. J., Beal M. F. and DiFiglia M. (1993) Intrastriatal injections of quinolinic acid or kainic acid: differential patterns of cell survival and the effects of data analysis on outcome. Expl Neurol. 124, 274-282.
75. 74. Sato K., Kiyama H. and Tohyama M. (1993) The differential expression patterns of messenger RNAs encoding non-NMDA glutamate receptor subunits (GluR1-4) in the rat brain. Neuroscience 52, 515-539.
76. 3H-acetylcholine release evoked by excitatory amino acids. Nature 297, 422-424.
77. 76. Schoepfer R., Monter H., Sommer B., Wisden W., Sprengel R., Kuner T., Lomeli H., Herb A., Kohler R., Burnashev N., Gunther W., Ruppersberg P. and Seeburg P. (1994) Molecular biology of glutamate receptors. Prog. Neurobiol. 42, 353-357.
78. 77. Schoepp D. D. and Conn P. J. (1993) Metabotropic glutamate receptors in brain function and pathology. Trends Pharmac. Sci. 14, 13-19.
79. 78. Schwarcz B., Foster A. C., French E. D., Whetsell W. O. and Köhler C. (1984) Excitotoxic models for neurodegenerative disorders. II. Life Sci. 35, 19-32.
80. 79. Seeburg P. H. (1993) The molecular biology of mammalian glutamate receptor channels. Trends Neurosci. 16, 359-365.
81. 80. Sheardown M. J., Suzdak P. D. and Nordholm L. (1993) AMPA, but not NMDA, receptor antagonism is neuroprotective in gerbil global ischemia, even when delayed 24 h. Eur. J. Pharmac. 236, 347-353.
82. 81. Siegel S. J., Brose N., Janssen N., Gasic N., Jahn R., Heinemann R. and Morrison J. H. (1994) Regional, cellular and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc. natn. Acad. Sci. U.S.A. 91, 564-568.
83. 82. Sommer B., Burnashev N., Verdoorn T. A., Keinánen K., Sakmann B. and Seeburg P. H. (1992) A glutamate receptor channel with high affinity for domoate and kainate. Eur. molec. Biol. Org. J. 4, 1651-1656.
84. 83. Sommer B. and Seeburg P. H. (1992) Glutamate receptor channels: novel properties and new clones. Trends Pharmac. Sci. 13, 291-296.
85. 84. Spencer P. S., Nunn P. B., Hugon J., Ludolph A. C., Ross S. M., Roy D. N. and Robertson R. C. (1987) Guam amyotrophic lateral sclerosis-Parkinsonism-dementia linked to a plant excitant neurotoxin. Science 237, 517-522.
86. 85. Standaert D. G., Testa C. M., Young A. B. and Penney J. B. (1994) Organization of N-methyl-D-aspartate glutamate receptor gene expression in the basal ganglia of the rat. J. comp. Neurol. 343, 1-16.
87. 86. 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. Res. Commun. 185, 826-832.
88. 87. Tallaksen-Greene S. J. and Albin R. L. (1994) Localization of AMPA-selective excitatory amino acid receptor subunits in identified populations of striatal neurons. Neuroscience 61, 509-519.
89. 88. Tang F., Costa E. and Schwartz J. P. (1983) Increase of proenkephalin mRNA and enkephalin content of rat striatum after daily injection of haloperidol for 2 to 3 weeks. Proc. natn. Acad. Sci. U.S.A. 80, 3841-3844.
90. 89. Tempel A., Kremer N. E., Kessler J. A. and Zukin R. S. (1986) Chronic blockade of brain opioid receptors leads to increased synthesis of methonine enkaphalin and substance P. Neurosci. Abstr. 12, 171.
91. 90. Vickers J. C., Huntley G. W., Edwards A. M., Moran T., Rogers S. W., Heinemann S. F. and Morrison J. H. (1993) Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the Macaque monkey. J. Neurosci. 13, 2982-2992.
92. 91. Vincent S. R. and Johansson O. (1983) Striatal neurons containing both somatostatin an avian pancreatic polypeptide (APP)-like immunoreactivies and NADPH-diaphorase activity: a light and electron microscopic study. J. comp. Neurol. 217, 252-263.
93. 92. Watanabe M., Inoue Y., Sakimura K. and Mishina M. (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. NeuroReport 3, 1138-1140.
94. 3H]aminobutyric acid from striatal neurons in primary culture. J. Pharmac. exp. Ther. 252, 380-386.
95. 94. Williams J. S., Berbekar I. and Weiss S. (1991) NMDA evokes the release of somatostatin from striatal interneurons in primary culture. Neuroscience 43, 437-444.
96. 95. Yoneda Y. and Ogita K. (1991) Heterogeneity of the N-methyl-D-asparate receptor ionophore complex in rat brain, as revealed by ligand binding techniques. J. Pharmac. exp. Ther. 259, 86-96.
97. 96. Young A. B., Greenamyre J. T. and Hollingsworth Z. (1988) NMDA receptor losses in putamen from patients with Huntington's disease. Science 241, 981-983.