N-acetylaspartylglutamate stimulates metabotropic glutamate receptor 3 to regulate expression of the GABA(A) subunit in cerebellar granule cells

Journal of Neurochemistry

Volumn 69, Issue 6, 1997, Pages 2326-2335

  Ghose, Subroto ^a   Wroblewska, Barbara ^a   Corsi, Lorenzo ^a   Grayson, Dennis R ^b   De Blas, Angel L ^c   Vicini, Stefano ^a   Neale, Joseph H ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Cerebellar granule cells; Cyclic AMP; GABA(A) receptor; GABA(A) 6; Glutamate; Metabotropic glutamate receptor; mGluR3; mRNA regulation; N Acetylaspartylglutamate

Indexed keywords

GLUTAMIC ACID; N ACETYLASPARTYLGLUTAMIC ACID;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CEREBELLUM; GABAERGIC TRANSMISSION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GRANULE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; VOLTAGE CLAMP;

ANIMALIA; VERTEBRATA;

EID: 0030716812     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69062326.x     Document Type: Article

References (54)

1. Atkinson B. N. and Minneman K. P. (1991) Multiple adrenergic receptor subtypes controlling cyclic AMP formation: comparison of brain slices and primary neuronal and glial cultures. J. Neurochem. 56, 587-595.
2. A receptor subunit mRNAs in vivo and in vitro. J. Neurochem. 59, 62-72.
3. Bovolin P., Santi M. R., Puia G., Costa E., and Grayson D. R. (1992b) Expression patterns of γ-aminobutyric acid type A receptor subunit mRNAs in primary cultures of granule neurons and astrocytes from neonatal rat cerebella. Proc. Natl. Acad. Sci. USA 89, 9344-9348.
4. Burt D. R. and Kamatchi G. L. (1991) GABA-A receptor subtypes: from pharmacology to molecular biology. FASEB J. 5, 2916-2923.
5. Bzdega T., Turi T., Wroblewska B., She D., Chung H. S., Kim H., and Neale J. H. (1997) Molecular cloning of a peptidase against N-acetylaspartylglutamate (NAAG) from a rat hippocampal cDNA library. J. Neurochem. 69, 2270-2277.
6. Carter R. E., Feldman A. R., and Coyle J. T. (1996) Prostate-specific membrane antigen is a hydrolase with substrate and pharmacological characteristics of a neuropeptidase. Proc. Natl. Acad. Sci. USA 93, 749-753.
7. Ducic I., Caruncho H. J., Zhu W. J., Vicini S., and Costa E. (1995) γ-Aminobutyric acid gating of chloride channels in recombinant GABA-A receptors. J. Pharmacol. Exp. Ther. 272, 438-445.
8. Gallo V. A., Ciotti M. T., Coletti A., Aloisi F., and Levi G. (1982) Selective release of glutamate from cerebellar granule cells differentiating in culture. Proc. Natl. Acad. Sci. USA 79, 7919-7923.
9. Grayson D. R., Bovolin P., and Santi M. R. (1993) Absolute quantitation of γ-aminobutyric acid A receptor subunit messenger RNAs by competitive polymerase reaction. Methods Neurosci. 12, 191-208.
10. Gutierrez A., Khan Z. U., and De Blas A. L. (1996) Immunocytochemical localization of the α6 subunit of the γ-aminobutyric acid A receptor in the rat nervous system. J. Comp. Neurol. 365, 504-510.
11. A receptors. Mol. Pharmacol. 43, 970-975.
12. Hadingham K. L., Garrett E. M., Wafford K. A., Bain C., Heavens R. P., Sirinathsinghji D. J. S., and Whiting P. J. (1995) Cloning of cDNAs encoding the human γ-aminobutyric acid type A receptor α6 subunit and characterization of the pharmacology of α6-containing receptors. Mol. Pharmacol. 49, 253-259.
13. Hamill O. P., Marty A., Neher E., Sakmann B., and Sigworth F. J. (1981) Improved patch-clamp technique for high-resolution current recording from cell and cell-free membrane patches. Pflugers Arch. 391, 85-91.
14. Harris B., Charlton E., Costa E., and Grayson D. R. (1993) Quantitative changes in α1 and α5 γ-aminobutyric acid type A receptor subunit mRNAs and proteins after a single treatment of cerebellar granule neurons with N-methyl-D-aspartate. Mol. Pharmacol. 45, 637-648.
15. + depolarization or to N-methyl-D-aspartate increases the transcription of genes encoding the α1 and α5 GABA-A receptor subunits. Mol. Brain Res. 28, 338-342.
16. Jane D. E., Jones P. L., Pook P. C., Tse H. W., and Watkins J. C. (1994) Actions of two new sub-type selective metabotropic glutamate receptor antagonists in the neonatal rat spinal cord. Br. J. Pharmacol. 112, 809-816.
17. A/benzodiazepine receptor from rat cerebellum. J. Neurochem. 63, 371-374.
18. A receptor maintaining their individual benzodiazepine-binding specificities. J. Neurochem. 66, 685-691.
19. Kleingoor C., Wieland H. A., Korpi E. R., Seeburg P. H., and Kettenman H. (1993) Current potentiation by diazepam but not GABA sensitivity is determined by a single histidine residue. Neuroreport 4, 187-190.
20. Korpi E. R., Kuner T., Seeburg P. H., and Lüddens H. (1995) Selective antagonist for the cerebellar granule cell-specific γ-aminobutyric acid type a receptor. Mol. Pharmacol. 47, 283-289.
21. Laurie D., Seeburg P., and Wisden W. (1992) The distribution of 13 GABA-A receptor subunit mRNAs in the brain. II: Olfactory bulb and cerebellum. J. Neurosci. 12, 1063-1076.
22. Levitan E. S., Schofield P. R., Burt D. R., Rhee L. M., Wisden W., Kohler M., Fujita N., Rodriguez H. F., Stephenson A., Darlison M. G., Barnard E. A., and Seeburg P. H. (1988) Structural and functional basis for GABA-A receptor heterogeneity. Nature 335, 76-79.
23. Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
24. Luddens H., Pritchett D. B., Kohler M., Killisch I., Keinanen K., Monyer H., Sprengel R., and Seeburg P. H. (1990) Cerebellar GABA-A receptor selective for a behavioral alcohol antagonist. Nature 346, 648-651.
25. Luddens H., Korpi E., and Seeburg P. (1995) GABA-A/benzodiazepine receptor heterogeneity: neurophysiological implications. Neuropharmacology 34, 245-254.
26. MacDonald R. and Olsen R. (1994) GABA-A receptor channels. Annu. Rev. Neurosci. 17, 569-602.
27. Mathews G. C., Bolos-Sy A. M., Holland K. D., Isenberg K. E., Covey D. F., Ferrendeli J. A., and Rothman S. M. (1994) Developmental alteration in GABA-A receptor structure and physiological properties in cultured cerebellar granule neurons. Neuron 13, 149-158.
28. Memo M., Bovolin P., Costa E., and Grayson D. R. (1991) Regulation of γ-aminobutyric acid A receptor subunit expression by activation of N-methyl-D-aspartate-selective glutamate receptors. Mol. Pharmacol. 39, 599-603.
29. 67 in the cerebellum and precerebellar nuclei of the rat utilizing enhanced carbodiimide fixation and immunohistochemistry. J. Comp. Neurol. 347, 598-618.
30. Mossman T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assays. J. Immunol. Methods 65, 55-63.
31. Murase K., Ryu P. D., and Randic M. (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci. Lett. 103, 56-63.
32. Olsen R. and Tobin A. (1990) Molecular biology of GABA-A receptors. FASEB J. 4, 1469-1480.
33. Prezeau L., Carrette J., Helpap B., Curry K., Pin J. P., and Bockaert J. (1993) Pharmacological characterization of metabotropic glutamate receptors in several types of brain cells in primary cultures. Mol. Pharmacol. 45, 570-577.
34. Rabin R. A. (1990) Direct effects of chronic ethanol exposure on β-adrenergic and adenosine-sensitive adenylate cyclase activities and cyclic AMP content in primary cerebellar cultures. J. Neurochem. 55, 122-128.
35. A receptor research. Synapse 21, 189-274.
36. 2-Adrenergic receptors in neuronal and glial cultures: characterization and comparison. J. Neurochem. 53, 287-296.
37. Robinson M. B., Blakely R. D., Couto R., and Coyle T. (1987) Hydrolysis of the brain dipeptide N-acetylaspartylglutamate. J. Biol. Chem. 262, 14498-14506.
38. A receptor subunit mRNAs in individual cerebellar neurons after whole-cell recordings. J. Neurochem. 63, 2357-2360.
39. Santi M. R., Ikonomovic S., Wroblewski J. T., and Grayson D. R. (1994b) Temporal and depolarization-induced changes in the absolute amounts of mRNAs encoding metabotropic glutamate receptors in cerebellar granule neurons in vitro. J. Neurochem. 63, 1207-1217.
40. Schofield P. R., Darlison M. G., Fujita N., Burt D. R., Stephenson F. A., Rodriguez H., Rhee L. M., Ramachandran J., Reala V., Glencorse T. A., Seeburg P., and Barnard E. A. (1987) Sequence and functional expression of the GABA-A receptor shows a ligand-gated superfamily. Nature 328, 221-227.
41. Sieghart W. (1992) GABA-A receptors: ligand-gated Cl ion channels modulated by multiple drug-binding sites. Trends Pharmacol. Sci. 13, 446-450.
42. Smith G. B. and Olsen R. W. (1995) Functional domains of GABA-A receptors. Trends Pharmacol. Sci. 16, 162-168.
43. Tanabe Y., Nomura A., Masu M., Shigemoto R., Mizuno N., and Nakanishi S. (1993) Signal transduction, pharmacological properties and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J. Neurosci. 13, 1372-1378.
44. Thomas N. K. (1996) (S)-α-Ethylglutamic acid and (RS)-α-cyclopropyl-4-phosphonophenylglycine as antagonists of L-AP4 and (1 S,3 S)-ACPD-induced depression of monosynaptic excitation of neonatal rat motoneurons. (Abstr.) Br. J. Pharmacol. 117, 70.
45. A receptor subtypes expressed in cerebellar granule cells: a developmental study. J. Neurochem. 62, 2037-2044.
46. A receptor α1 and α6 subunit expression by a cyclic AMP-mediated signaling mechanism in cerebellar granule cells in primary culture. J. Neurochem. 67, 434-437.
47. Verdoorn T. A. (1994) Formation of heteromeric gamma-aminobutyric acid type A receptors containing two different alpha subunits. Mol. Pharmacol. 45, 475-480.
48. Verdoom T., Draguhn A., Ymer S., Seeburg P., and Sakmann B. (1990) Functional properties of recombinant rat GABA-A receptors depend upon subunit composition. Neuron 4, 919-928.
49. Whiting P. J., McKernan R. M., and Iversen L. L. (1990) Another mechanism for creating diversity in γ-aminobutyrate type A receptors: RNA splicing directs expression of two forms of γ2 subunit, one of which contains a protein kinase C phosphorylation site. Proc. Natl. Acad. Sci. USA 87, 9966-9970.
50. Wojcik W. J. and Neff N. H. (1983) Adenosine A1 receptors are associated with cerebellar granule cells. J. Neurochem. 41, 759-763.
51. Wroblewska B., Wroblewski J. T., Saab O. H., and Neale J. H. (1993) N-Acetylaspartylglutamate inhibits forskolin-stimulated cyclic AMP levels via a metabotropic glutamate receptor in cultured cerebellar granule cells. J. Neurochem. 61, 943-948.
52. Wroblewska B., Santi M. R., and Neale J. H. (1995) NAAG activates cloned mGluR3 receptor. Soc. Neurosci. Abstr. 21, 847.
53. Wroblewska B., Wroblewski J. T., Pshenichkin S., Surin A., Sullivan S. E., and Neale J. H. (1997) N-Acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J. Neurochem. 69, 174-181.
54. Zheng T., Santi M. R., Bovolin P., Marlier L. N. J. L., and Grayson D. R. (1993) Developmental expression of the α6 GABA-A receptor subunit mRNA occurs only after cerebellar granule cell migration. Dev. Brain Res. 75, 91-103.