A metabotropic glutamate receptor agonist regulates neurotrophin messenger RNA in rat forebrain

Neuroscience

Volumn 70, Issue 3, 1996, Pages 617-630

  Murray, K D ^a,b   Wood, P L ^a,c   Rosasco, C ^a   Isackson, P J ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Department of Pharmacokinetics and Drug Metabolism   (United States)

Author keywords

1s; 3R ACPD; BDNF; c fos; hippocampus; NGF; NT 3

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; BRAIN DERIVED NEUROTROPHIC FACTOR; DIZOCILPINE; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR AGONIST; GLUTAMATE RECEPTOR ANTAGONIST; MESSENGER RNA; METABOTROPIC RECEPTOR; NEUROTROPHIN 3;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT;

EID: 0030058730     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(96)83002-8     Document Type: Article

References (84)

1. 2+ signal transduction. J. biol. Chem. 267, 13361-13368.
2. Akazawa C., Ohishi H., Nakajima Y., Okamoto N., Shigemoto R., Nakanishi S. and Mizuno N. (1994) Expression of mRNAs of L-AP4-sensitive metabotropic glutamate receptors (mGluR4, mGluR6, mGluR7) in the rat retina. Neurosci. Lett. 171, 52-54.
3. Aniksztejn L., Bregestovski P. and Ben-Ari Y. (1991) Selective activation of quisqualate metabotropic receptor potentiates NMDA but not AMPA responses. Eur. J. Pharmac. 205, 327-328.
4. Aramori I. and Nakanishi S. (1992) Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8, 757-765.
5. Bashir Z. I., Bortolotto Z. A., Davies C. H., Berretta N., Irving A. J., Seal A. J., Henley J. M., Jane D. E., Watkins J. C. and Collingridge G. L. (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363, 347-350.
6. Ben-Ari Y., Tremblay E., Riche D., Ghilini G. and Naquet R. (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience 6, 1361-1391.
7. Bengzon J., Kokaia Z., Emfors P., Kokaia M., Leanza G., Nilsson O. G., Persson H. and Lindvall O. (1993) Regulation of neurotrophin and trkA, trkB and trkC tyrosine kinase receptor messenger RNA expression in kindling. Neuroscience 53, 433-446.
8. Bengzon J., Soderstrom S., Kokaia Z., Kokaia M., Emfors P., Persson H., Ebendal T. and Lindvall O. (1992) Widespread increase of nerve growth factor protein in the rat forebrain after kindling-induced seizures. Brain Res. 587, 338-342.
9. Bessho Y., Nakanishi S. and Nawa H. (1993) Glutamate receptor agonists enhance the expression of BDNF mRNA in cultured cerebellar granule cells. Molec. Brain Res. 18, 201-208.
10. Bleakman D., Rusin K. I., Chard P. S., Glaum S. R. and Miller R. J. (1992) Metabotropic glutamate receptors potentiate ionotropic glutamate responses in the rat dorsal horn. Molec. Pharmac. 42, 192-196.
11. Bockaert J., Pin J. and Fagni L. (1993) Metabotropic glutamate receptors: an original family of G protein-coupled receptors. Fundam. clin. Pharmac. 7, 473-485.
12. Bortolotto Z. A., Bashir Z. I., Davies C. H. and Collingridge G. L. (1994) A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature 368, 740-743.
13. Calabresi P., Mercuri N. B. and Bernardi G. (1992) Activation of quisqualate metabotropic receptors reduces glutamate and GABA-mediated synaptic potentials in the rat striatum. Neurosci. Lett. 139, 41-44.
14. Castren E., Pitkanen M., Sirvio J., Parsadanian A., Lindholm D., Thoenen H. and Riekkinen P. J. (1993) The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport 4, 895-898.
15. Castren E., Zafra F., Thoenen H. and Lindholm D. (1992) Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc. natn. Acad. Sci. U.S.A. 89, 9444-9448.
16. Desai M. A. and Conn P. J. (1990) Selective activation of phosphoinositide hydrolysis by a rigid analogue of glutamate. Neurosci. Lett. 109, 157-162.
17. Dingledine R., Kleckner N. W. and McBain C. J. (1990) The glycine coagonist site of the NMDA receptor. Adv. exp. Med. Biol. 268, 17-26.
18. Dragunow M., Beilharz E., Mason B., Lawlor P., Abraham W. and Gluckman P. (1993) Brain-derived neurotrophic factor expression after long-term potentiation. Neurosci. Lett. 160, 232-236.
19. Drejer J. and Honore T. (1988) New quinoxalinediones show potent antagonism of quisqualate responses in cultured mouse cortical neurons. Neurosci. Lett. 87, 104-108.
20. Dugich-Djordjevic M., Tocco G., Lapchak P. A., Pasinetti G. M., Najm I., Baudry M. and Hefti F. (1992) Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in the adult rat brain following seizures induced by systemic administration of kainic acid. Neuroscience 47, 303-315.
21. Ernfors P., Bengzon J., Kokaia Z., Persson H. and Lindvall O. (1991) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron 7, 165-176.
22. Ernfors P., Wetmore C., Olson L. and Persson H. (1990) Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 5, 511-526.
23. Fotuhi M., Standaert D. G., Testa C. M., Penney J. J. and Young A. B. (1994) Differential expression of metabotropic glutamate receptors in the hippocampus and entorhinal cortex of the rat. Molec. Brain Res. 21, 283-292.
24. Gall C., Lauterborn J., Bundman M., Murray K. and Isackson P. (1991) Seizures and the regulation of neurotrophic factor and neuropeptide gene expression in brain. Epilepsy Res., Suppl. 4, 225-245.
25. Gall C., Murray K. and Isackson P. J. (1991) Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Molec. Brain Res. 9, 113-123.
26. Gall C. M. (1992) Regulation of brain neurotrophin expression by physiological activity. Trends pharmac. Sci. 13, 401-403.
27. Gall C. M. and Isackson P. J. (1989) Limbic seizures increase neuronal production of mRNA for nerve growth factor. Science 245, 758-761.
28. Gerber U., Luthi A. and Gahwiler B. H. (1993) Inhibition of a slow synaptic response by a metabotropic glutamate receptor antagonist in hippocampal CA3 pyramidal cells. Proc. R. Soc. Lond. B, Biol. Sci. 254, 169-172.
29. Ghosh A., Carnahan J. and Greenberg M. E. (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263, 1618-1623.
30. Gilman M. Z., Wilson R. N. and Weinberg R. A. (1986) Multiple protein-binding sites in the 5′-flanking region regulate c-fos expression. Molec. cell. Biol. 6, 4305-4316.
31. Glaum S. R. and Miller R. J. (1992) Metabotropic glutamate receptors mediate excitatory transmission in the nucleus of the solitary tract. J. Neurosci. 12, 2251-2258.
32. Gwag B. J., Sessler F. M., Waterhouse B. D. and Springer J. E. (1993) Regulation of nerve growth factor mRNA in the hippocampal formation effects of N-methyl-D-aspartate receptor activation. Expl Neurol. 121, 160-171.
33. Gwag B. J. and Springer J. E. (1993) Activation of NMDA receptors increases brain-derived neurotrophic factor (BDNF) mRNA expression in the hippocampal formation. Neuroreport 5, 125-128.
34. Harvey J. and Collingridge G. L. (1993) Signal transduction pathways involved in the acute potentiation of NMDA responses by 1S,3R-ACPD in rat hippocampal slices. Br. J. Pharmac. 109, 1085-1090.
35. Holtzman D. M., Li Y., Chen K., Gage F. H., Epstein C. J. and Mobley W. C. (1993) Nerve growth factor reverses neuronal atrophy in a Down syndrome model of age-related neurodegeneration. Neurology 43, 2668-2673.
36. Houamed K. M., Kuijper J. L., Gilbert T. L., Haldeman B. A., O'Hara P. J., Mulvihill E. R., Almers W. and Hagen F. S. (1991) Cloning, expression, and gene structure of a G protein-coupled glutamate receptor from rat brain. Science 252, 1318-1321.
37. Hughes P., Beilharz E., Gluckman P. and Dragunow M. (1993) Brain-derived neurotrophic factor is induced as an immediate early gene following N-methyl-D-aspartate receptor activation. Neuroscience 57, 319-328.
38. Hughes P., Dragunow M., Beilharz E., Lawlor P. and Gluckman P. (1993) MK801 induces immediate early gene proteins and BDNF mRNA in rat cerebrocortical neurones. Neuroreport 4, 183-186.
39. Isackson P. J., Huntsman M. M., Murray K. D. and Gall C. M. (1991) BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 6, 937-948.
40. Kelso S. R., Nelson T. E. and Leonard J. P. (1992) Protein kinase C-mediated enhancement of NMDA currents by metabotropic glutamate receptors in Xenopus oocytes. J. Physiol. 449, 705-718.
41. Kleckner N. W. and Dingledine R. (1989) Selectivity of quinoxalines and kynurenines as antagonists of the glycine site on N-methyl-D-aspartate receptors. Molec. Pharmac. 36, 430-436.
42. Koh J.-Y., Palmer E. and Cotman C. W. (1991) Activation of the metabotropic glutamate receptor attenuates N-methyl-D-aspartate neurotoxicity in cortical cultures. Proc. natn. Acad. Sci. U.S.A. 88, 9431-9435.
43. Lapchak P. A., Araujo D. M. and Hefti F. (1993) Cholinergic regulation of hippocampal brain-derived neurotrophic factor mRNA expression: evidence from lesion and chronic cholinergic drug treatment studies. Neuroscience 52, 575-585.
44. Lauterborn J. C., Tran T. M., Isackson P. J. and Gall C. M. (1993) Nerve growth factor mRNA is expressed by GABAergic neurons in rat hippocampus. Neuroreport 5, 273-276.
45. Lauterborn J. L., Stinis C. T., Hayes V. H., Isackson P. J. and Gall C. M. (1994) Exon III of the rat BDNF gene can be induced in the presence of protein synthesis inhibitors: evidence for an immediate-early gene. Soc. Neurosci. Abstr. 20, 1308.
46. Lindefors N., Ernfors P., Falkenberg T. and Persson H. (1992) Septal cholinergic afferents regulate expression of brain-derived neurotrophic factor and beta-nerve growth factor mRNA in rat hippocampus. Expl Brain Res. 88, 78-90.
47. Linden D. J., Dickinson M. H., Smeyne M. and Connor J. A. (1991) A long-term depression of AMPA currents in cultured cerebellar Purkinje neurons. Neuron 7, 81-89.
48. Lindvall O., Ernfors P., Bengzon J., Kokaia Z., Smith M. L., Siesjo B. K. and Persson H. (1992) Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin 3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc. natn. Acad. Sci. U.S.A. 89, 648-652.
49. Masu M., Tanabe Y., Tsuchida K., Shigemoto R. and Nakanishi S. (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349, 760-765.
50. McDonald J. W., Fix A. S., Tizzano J. P. and Schoepp D. D. (1993) Seizures and brain injury in neonatal rats induced by 1S,3R-ACPD, a metabotropic glutamate receptor agonist. J. Neurosci. 13, 4445-4455.
51. McDonald J. W. and Schoepp D. D. (1992) The metabotropic excitatory amino acid receptor agonist 1S,3R-ACPD selectively potentiates N-methyl-D-aspartate-induced brain injury. Eur. J. Pharmac. 215, 353-354.
52. Minakami R., Katsuki F. and Sugiyama H. (1993) A variant of metabotropic glutamate receptor subtype 5: an evolutionally conserved insertion with no termination codon. Biochem. biophys. Res. Commun. 194, 622-627.
53. Monaghan D. T., Bridges R. J. and Cotman C. W. (1989) The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. A. Rev. Pharmac. Toxic. 29, 365-402.
54. Morgan J. I., Cohen D. R., Hempstead J. L. and Curran T. (1987) Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237, 192-197.
55. Nakajima Y., Iwakabe H., Akazawa C., Nawa H., Shigemoto R., Mizuno N. and Nakanishi S. (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J. biol. Chem. 268, 11868-11873.
56. Nakanishi S. (1994) Metabotropic glutamate receptors - synaptic transmission, modulation, and plasticity. Neuron 13, 1031-1037.
57. O'Connor J. J., Rowan M. J. and Anwyl R. (1994) Long-lasting enhancement of NMDA receptor-mediated synaptic transmission by metabotropic glutamate receptor activation. Nature 367, 557-559.
58. Ohishi H., Shigemoto R., Nakanishi S. and Mizuno N. (1993) Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience 53, 1009-1018.
59. Ohishi H., Shigemoto R., Nakanishi S. and Mizuno N. (1993) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J. comp. Neurol. 335, 252-266.
60. Palmer E., Monaghan D. T. and Cotman C. W. (1989) Trans-ACPD, a selective agonist of the phosphoinositide-coupled excitatory amino acid receptor. Eur. J. Pharmac. 166, 585-587.
61. Patterson S. L., Grover L. M., Schwartzkroin P. A. and Bothwell M. (1992) Neurotrophin expression in rat hippocampal slices: stimulus paradigm including LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9, 1081-1088.
62. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, Orlando, FL.
63. Pin J. P., Waeber C., Prezeau L., Bockaert J. and Heinemann S. F. (1992) Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopus oocytes. Proc. natn. Acad. Sci. U.S.A. 89, 10331-10335.
64. Pizzi M., Fallacara C., Arrighi V., Memo M. and Spano P. F. (1993) Attenuation of excitatory amino acid toxicity by metabotropic glutamate receptor agonists and aniracetam in primary cultures of cerebellar granule cells. J. Neurochem. 61, 683-689.
65. Riedel G. and Reymann K. (1993) An antagonist of the metabotropic glutamate receptor prevents LTP in the dentate gyrus of freely moving rats. Neuropharmacology 32, 929-931.
66. Rocamora N., Palacios J. M. and Mengod G. (1992) Limbic seizures induce a differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3, in the rat hippocampus. Molec. Brain Res. 13, 27-33.
67. Runkel L., Shaw P. E., Herrera R. E., Hipskind R. A. and Nordheim A. (1991) Multiple basal promoter elements determine the level of human c-fos transcription. Molec. cell. Biol. 11, 1270-1280.
68. Sacaan A. I. and Schoepp D. D. (1992) Activation of hippocampal metabotropic excitatory amino acid receptors leads to seizures and neuronal damage. Neurosci. Lett. 139, 77-82.
69. Saugstad J. A., Kinzie J. M., Mulvihill E. R., Segerson T. P. and Westbrook G. L. (1994) Cloning and expression of a new member of the L-2-amino-4-phosphonobutyric acid-sensitive class of metabotropic glutamate receptors. Molec. Pharmac. 45, 367-372.
70. Scarisbrick I. A., Jones E. G. and Isackson P. J. (1993) Coexpression of mRNAs for NGF, BDNF, and NT-3 in the cardiovascular system of the pre- and postnatal rat. J. Neurosci. 13, 875-893.
71. Schoepp D. D. (1994) Novel functions for subtypes of metabotropic glutamate receptors. Neurochem. Int. 24, 439-449.
72. Schoepp D. D. and Conn P. J. (1993) Metabotropic glutamate receptors in brain function and pathology. Trends pharmac. Sci. 14, 13-20.
73. Shigemoto R., Nakanishi S. and Mizuno N. (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J. comp. Neurol. 322, 121-135.
74. Siliprandi R., Lipartiti M., Fadda E., Sautter J. and Manev H. (1992) Activation of the glutamate metabotropic receptor protects retina against N-methyl-D-aspartate toxicity. Eur. J. Pharmac. 219, 173-174.
75. Sugiyama H., Ito I. and Hirono C. (1987) A new type of glutamate receptor linked to phospholipid metabolism. Nature 325, 531-533.
76. Tanabe Y., Masu M., Ishii T., Shigemoto R. and Nakanishi S. (1992) A family of metabotropic glutamate receptors. Neuron 8, 169-179.
77. Testa C. M., Standaert D. G., Young A. B. and Penney J. J. (1994) Metabotropic glutamate receptor mRNA expression in the basal ganglia of the rat. J. Neurosci. 14, 3005-3018.
78. Tsukahara T., Yonekawa Y., Tanaka K., Ohara O., Wantanabe S., Kimura T., Nishijima T. and Taniguchi T. (1994) The role of brain-derived neurotrophic factor in transient forebrain ischemia in the rat brain. Neurosurgery 34, 323-331.
79. Verdoorn T. A., Kleckner N. W. and Dingledine R. (1989) N-Methyl-D-aspartate/glycine and quisqualate/kainate receptors expressed in Xenopus oocytes: antagonist pharmacology. Molec. Pharmac. 35, 360-368.
80. Wetmore C., Olson L. and Bean A. J. (1994) Regulation of brain-derived neurotrophic factor (BDNF) expression and release from hippocampal neurons is mediated by non-NMDA type glutamate receptors. J. Neurosci. 14, 1688-1700.
81. Zafra F., Castren E., Thoenen H. and Lindholm D. (1991) Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc. natn. Acad. Sci. U.S.A. 88, 10037-10041.
82. Zafra F., Hengerer B., Leibrock J., Thoenen H. and Lindholm D. (1990) Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. Eur. molec. Biol. Org. J. 9, 3545-3550.
83. Zafra F., Lindholm D., Castren E., Hartikka J. and Thoenen H. (1992) Regulation of brain-derived neurotrophic factor and nerve growth factor mRNA in primary cultures of hippocampal neurons and astrocytes. J. Neurosci. 12, 4793-4799.
84. Zheng F. and Gallagher J. P. (1992) Metabotropic glutamate receptors are required for the induction of long-term potentiation. Neuron 9, 163-172.