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Glutamate-evoked gene expression in brain cells — Focus on transcription factors

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Summary

L-glutamate (L-glu) is major excitatory neurotransmitter in mammalian central nervous system. Besides short term effects on neuronal activity, L-glu affects also long term neuronal and glial responses. Neuromodulatory function of L-glu may in part be dependent on its ability to activate transcription factors — proteins regulating gene expression through interaction with specific regulatory sequences located in promoter and enhancer gene regions. This paper reviews recent data suggesting that L-glu can selectively stimulate genes encoding transcription factors like zif/268 and fos and jun gene families, as well as the factors themselves both in neurons and astroglia cultured in vitro and brain cells in vivo.

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References

  • Abe H, Rusak B, Robertson HA (1991) Photic induction of Fos protein in the suprachiasmatic nucleus is inhibited by the NMDA receptor antagonist MK-801. Neurosci Lett 127: 9–12

    Google Scholar 

  • Abe H, Rusak B, Robertson HA (1992) NMDA and non-NMDA receptor antagonists inhibit photic induction of Fos protein in the hamster suprachiasmatic nucleus. Brain Res Bull 28: 831–835

    Google Scholar 

  • Angel P, Karin M (1991) The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochem Biophys Acta 1072: 129–157

    Google Scholar 

  • Bading H, Ginty DD, Greenberg ME (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signalling pathways. Science 260: 181–186

    Google Scholar 

  • Baeuerle PA (1991) The inducible transcription factors NF-κB: regulation by distinct protein subunits. Biochim Biophys Acta 1072: 63–80

    Google Scholar 

  • Bliss TVP, Lomo TJ (1973) Long lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (London) 232: 331–356

    Google Scholar 

  • Collingridge GL, Singer W (1990) Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci 11: 290–296

    Google Scholar 

  • Colotta F, Polentarutti N, Sironi M, Mantovani A (1992) Expression and involvement ofc-fos andc-jun protooncogenes in programmed cell death induced by growth factor deprivation in lymphoid cell lines. J Biol Chem 267: 18278–18283

    Google Scholar 

  • Condorelli DF, Dell'Albani P, Amico C, Kaczmarek L, Nicoletti F, Lukasiuk K, Giuffrida-Stella AM (1993) Induction of primary response genes by excitatory amino acids receptor agonists in primary astroglial cultures. J Neurochem 60: 877–885

    Google Scholar 

  • Condorelli DF, Kaczmarek L, Nicoletti F, Arcidiacono A, Dell'Albani P, Ingrao F, Magri G, Malaguarnera L, Avola R, Messina A, Giuffrida Stella AM (1989) Induction of protooncogene c-fos by extracellular signals in primary astroglial cell cultures. J Neurosci Res 23: 234–239

    Google Scholar 

  • Curran T, Morgan JI (1987) Memories of fos. BioEssays 7: 255–258

    Google Scholar 

  • Didier M, Roux P, Piechaczyk M, Verrier B, Bockaert J, Pin J-P (1989) Cerebellar granule cell survival and maturation induced by K+ and NMDA correlate with c-fos proto-oncogene expression. Neurosci Lett 107: 55–62

    Google Scholar 

  • Didier M, Roux P, Piechaczyk M, Mangeat P, Devilliers G, Bockaert J, Pin J-P (1992) Long-term expression of thec-fos protein during the in vitro differentiation of cerebellar granule cells induced by potassium or NMDA. Mol Brain Res 12: 249–258

    Google Scholar 

  • Demmer J, Dragunow M, Lawror PA, Mason SE, Leah JD, Abraham WC, Tate WP (1993) Differential expression of immediate early genes after hippocampal long-term potentiation in awake rats. Mol Brain Res 17: 279–286

    Google Scholar 

  • Dragunow M, Faull RLM (1990) MK-801 inducesc-fos protein in thalamic and neocortical neurons in rat brain. Neurosci Lett 111: 39–45

    Google Scholar 

  • Dragunow M, Abraham WC, Goulding M, Mason SE, Roberson HA, Faull RLM (1989) Long-term potentiation and the induction ofc-fos mRNA and proteins in the dentate gyrus of unanesthetized rats. Neurosci Lett 101: 274–280

    Google Scholar 

  • Dragunow M, Young D, Hughes P, MacGibbon G, Lawlor P, Singleton K, Sirimanne E, Beilharz E, Gluckman P (1993) Is c Jun involved in nerve cell death following status epilepticus and hypoxic-ischaemic brain injury? Mol Brain Res 18: 347–352

    Google Scholar 

  • Gass P, Herdegen T, Bravo R, Kiessling M (1993) Induction and suppresion of immediate early genes in specific rat brain regions by the non-competitive N-methylD-aspartate receptor antagonist MK-801. Neuroscience 53: 749–758

    Google Scholar 

  • Goelet P, Castelluci VF, Schacher S, Kandel ER (1986) The long and the short of long term memory — a molecular framework. Nature (London) 322: 419–423

    Google Scholar 

  • Gunn AJ, Dragunow M, Faull RLM, Gluckman PD (1990) Effects of hypoxia-ischemia and seizures on neuronal and glial-likec-fos protein levels in the infant rat. Brain Res 531: 105–116

    Google Scholar 

  • Guthrie KM, Anderson AJ, Leon M, Gall C (1993) Odor-induced increases in c-fos mRNA expression reveal an anatomical “unit” for odor processing in olfactory bulb. Proc Natl Acad Sci USA 90: 3329–3333

    Google Scholar 

  • Heilig M, Engel JA, Soderpalm B (1993) C-fos antisense in the nucleus accumbens blocks the locomotor stimulant action of cocaine. Eur J Pharmacol 236: 339–340

    Google Scholar 

  • Hisanaga K, Sagar SM, Sharp FR (1992) N-methyl-D-aspartate antagonists block Fos-like protein expression induced via multiple signalling pathways in cultured cortical neurons. J Neurochem 58: 1836–1844

    Google Scholar 

  • Jensen FE, Firkusny IR, Mower GD (1993) Differences in c-fos immunoreactivity due to age of seizure induction. Mol Brain Res 17: 185–193

    Google Scholar 

  • Kaczmarek L (1986) Protooncogene expression during the cell cycle. Lab Invest 54: 365–377

    Google Scholar 

  • Kaczmarek L (1993a) Glutamate receptor-driven gene expression in learning. Acta Neurobiol Exp 53: 187–196

    Google Scholar 

  • Kaczmarek L (1993b) Molecular biology of vertebrate learning: isc-fos a new beginning? J Neurosci Res 34: 377–381

    Google Scholar 

  • Kaczmarek L, Kaminska B (1989) Molecular biology of cell activation. Exp Cell Res 183: 24–35

    Google Scholar 

  • Kaczmarek L, Siedlecki JA, Danysz W (1988) Proto-oncogenec-fos induction in rat hippocampus. Mol Brain Res 3: 188–186

    Google Scholar 

  • Le Gal La Salle G (1988) Long-lasting and sequential increase ofc-fos oncoprotein expression in kainic acid induced status epilepticus. Neurosci Lett 88: 127–130

    Google Scholar 

  • Lerea LS, Butler LS, McNamara JO (1992) NMDA and non-NMDA receptor-mediated increase ofc-fos mRNA in dentate gyrus neurons involves calcium influx via different routes. J Neurosci 12: 2973–2981

    Google Scholar 

  • Lerea LS, Mcnamara JO (1993) Ionotropic glutamate receptor subtypes activatec-fos transcription by distinct calcium-requiring intracellular signalling pathways. Neuron 10: 31–41

    Google Scholar 

  • McNaughton LA, Hunt SP (1993) Regulation of gene expression in astrocytes by excitatory amino acids. Mol Brain Res 16: 261–266

    Google Scholar 

  • Montminy MR, Gonzales GA, Yamamoto KK (1990) Regulation of cAMP-inducible genes by CREB. Trends Neurosci 13: 184–188

    Google Scholar 

  • Morgan JI, Curran T (1991a) Stimulus-transcription coupling in the nervous system: involvement of the inducible protooncogenes fos and jun. Annu Rev Neurosci 14: 421–451

    Google Scholar 

  • Morgan JI, Curran T (1991b) Proto-oncogene transcription factors and epilepsy. Trends Pharmacol Sci 12: 343–349

    Google Scholar 

  • Morgan PF, Linnoila M (1991) Regional induction ofc-fos mRNA by NMDA: a quantitative in-situ hybridization study. NeuroReport 2: 251–254

    Google Scholar 

  • Murphy TH, Worley PF, Nakabeppu Y, Christy B, Gastel J, Baraban JM (1991a) Synaptic regulation of immediate early gene expression in primary cultures of cortical neurons. J Neurochem 57: 1862–1872

    Google Scholar 

  • Murphy TH, Worley PF, Baraban JM (1991b) L-type voltage- sensitive calcium channels mediate synaptic activation of immediate early genes. Neuron 7: 625–635

    Google Scholar 

  • Nedivi E, Hevroni D, Naot D, Israeli D, Citri Y (1993) Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363: 718–722

    Google Scholar 

  • Nitsch R, Frotscher M (1992) Reduction of posttraumatic transneuronal “early gene” activation and dendritic atrophy by the N-methyl-D-aspartae receptor antagonist MK-801. Proc Natl Acad Sci USA 89: 5197–5200

    Google Scholar 

  • Nozaki K, Beal MF (1992) Neuroprotective effects of L-kynurenine on hypoxia-ischemia and NMDA lesions in neonatal rats. J Cereb Blood Flow Metab 12: 400–407

    Google Scholar 

  • Pennypacker KR, Walczak D, Thai L, Fannin R, Mason E, Douglass J, Hong JS (1993) Kainate-induced changes in opioid peptide genes and AP-1 protein expression in rat hippocampus. J Neurochem 60: 204–211

    Google Scholar 

  • Popovici T, Represa A, Crepel V, Barbin G, Beauoin M, Ben-Ari Y (1990) Effects of kainic acid-induced seizures and ischemia on c-fos-like proteins in rat brain. Brain Res 536: 183–194

    Google Scholar 

  • Riabowol K, Schiff J, Gilman MZ (1992) Transcription factor AP-1 activity is required for initiation of DNA synthesis and is lost during cellular aging. Proc Natl Acad Sci (USA) 89: 157–161

    Google Scholar 

  • Sakurai H, Kurusu R, Sano K, Tsuchiya T, Tsuda M (1992) Stimulation of cultured cerebellar granule cells via glutamate receptors induces TRE-and CRE-binding activities mediated by common DNA-binding complexes. J Neurochem 59: 2067–2075

    Google Scholar 

  • Sakurai-Yamashita Y, Sassone-Corsi P, Gombos G(1991) Immunohistochemistry of c-fos in mouse brain during postnatal development: basal levels and changing response to metrazol and kainate injection. Eur J Neurosci 3: 764–770

    Google Scholar 

  • Sheng M, Greenberg ME (1990) The regulation of function of c-fos and other immediately early genes in the nervous system. Neuron 4: 477–485

    Google Scholar 

  • Smeyne RJ, Schilling K, Robertson L, Luk D, Oberdick J, Curran T, Morgan JI (1992) Fos-lacZ transgenic mice: mapping sites of gene induction in the central nervous system. Neuron 8: 13–23

    Google Scholar 

  • Smeyne RJ, Vendrell M, Hayward M, Baker SJ, Miao GG, Schilling K, Robertson LM, Curran T, Morgan JI (1993) Continuousc-fos expression precedes programmed cell death in vivo. Nature 363: 166–169

    Google Scholar 

  • Sonnenberg JL, Mitchelmore C, Macgregor-Leon PF, Hempstead J, Morgan JI, Curran T (1989) Glutamate receptor agonists increase the expression of Fos, Fra and AP-1 DNA binding activity in the mammalian brain. J Neurosci Res 24: 72–80

    Google Scholar 

  • Szekely AM, Barbacia ML, Costa E (1987) Activation of specific glutamate receptors increasesc-fos proto-oncogene expression in primary cultures of neonatal rat cerebellar granule cells. Neuropharmacology 26: 1779–1787

    Google Scholar 

  • Szekely AM, Barbacia ML, Alho H, Costa E (1989) In primary cultures of cerebellar granule cells the activation of N-methyl-D-aspartate-sensitive glutamate receptors inducesc-fos mRNA expression. Mol Pharmacol 35: 401–408

    Google Scholar 

  • Vaccarino FM, Hayward MD, Nestler EJ, Duman RS, Tallman JF (1991) Differential induction of immediate early genes by excitatory amino acid receptors types in primary cultures of cortical and striatal neurons. Mol Brain Res 12: 233–241

    Google Scholar 

  • Worley PF, Cole AJ, Murphy TH, Christy BA, Nakabeppu Y, Baraban JM (1990) Synaptic regulation of immediate-early genes in brain. Cold Spring Harbor Symp Quant Biol 40: 213–223

    Google Scholar 

  • Worley P, Christy BA, Nakabeppu Y, Bhat RV, Cole AJ, Baraban JM (1991) Constitutive expression ofzif/268 in neocortex is regulated by synaptic activity. Proc Natl Acad Sci USA 88: 5106–5110

    Google Scholar 

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  1. Nencki Institute of Experimental Biology, Pasteura 3, PL-02-093, Warsaw, Poland

    L. Kaczmarek

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Kaczmarek, L. Glutamate-evoked gene expression in brain cells — Focus on transcription factors. Amino Acids 7, 245–254 (1994). https://doi.org/10.1007/BF00807700

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