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Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms

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Abstract

Long-term plasticity of the central nervous system (CNS) involves induction of a set of genes whose identity is incompletely characterized. To identify candidate plasticity-related genes (CPGs), we conducted an exhaustive screen for genes that undergo induction or downregulation in the hippocampus dentate gyrus (DG) following animal treatment with the potent glutamate analog, kainate. The screen yielded 362 upregulated CPGs and 41 downregulated transcripts (dCPGs). Of these, 66 CPGs and 5 dCPGs are known genes that encode for a variety of signal transduction proteins, transcription factors, and structural proteins. Seven novel CPGs predict the following putative functions:cpg2—a dystrophin-like cytoskeletal protein;cpg4—a heat-shock protein:cpg16—a protein kinase;cpg20—a transcription factor;cpg21—a dual-specificity MAP-kinase phosphatase; andcpg30 andcpg38—two new seven-transmembrane domain receptors. Experiments performed in vitro and with cultured hippocampal cells confirmed the ability of thecpg-21 product to inactivate the MAP-kinase. To test relevance to neural plasticity, 66 CPGs were tested for induction by stimuli producing long-term potentiation (LTP). Approximately one-fourth of the genes examined were upregulated by LTP. These results indicate that an extensive genetic response is induced in mammalian brain after glutamate receptor activation, and imply that a significant proportion of this activity is coinduced by LTP. Based on the identified CPGs, it is conceivable that multiple cellular mechanisms underlie long-term plasticity of the nervous system.

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References

  • Abdollahi A., Lord K. A., Hoffman L. B., and Liebermann D. A. (1991) Sequence and expression of a cDNA encoding MyD118: a novel myeloid differentiation primary response gene induced by multiple cytokines.Oncogene 6, 165–167.

    PubMed  CAS  Google Scholar 

  • Amaya Y., Matsubasa T., Takiguchi M., Kobayashi K., Saheki T., Kawamoto S., and Mori M. (1988) Amino acid sequence of rat argininosuccinate lyase deduced from cDNA.J. Biochem. (Tokyo) 103, 177–181.

    CAS  Google Scholar 

  • Andersen R. D., Birren B. W., Taplitz S. J. and Herschman H. R. (1986) Rat metallothionein-1 structural gene and three pseudogenes, one of which contains 5′-regulatory sequences.Mol. Cell. Biol. 6, 302–314.

    PubMed  CAS  Google Scholar 

  • Antalis T. M., Clark M. A., Barnes T., Lehrbach P. R., Devine P. L., Schevzov G., et al. (1988) Cloning and expression of a cDNA coding for a human monocyte-derived plasminogen activator inhibitor.Proc. Natl. Acad. Sci. USA 85, 985–989.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Arancio O., Kandel E. R., and Hawkins R. D. (1995) Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons.Nature 376, 74–80.

    Article  PubMed  CAS  Google Scholar 

  • Bading H., Ginty D. D., and Greenberg M. E. (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways.Science 260, 181–186.

    Article  PubMed  CAS  Google Scholar 

  • Bading H. and Greenberg M. E. (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation.Science 253, 912–914.

    Article  PubMed  CAS  Google Scholar 

  • Bailey C. H. and Kandel E. R. (1993) Structural changes accompanying memory storage.Annu. Rev. Physiol. 55, 397–426.

    Article  PubMed  CAS  Google Scholar 

  • Bekkers J. M. and Stevens C. F. (1990) Presynaptic mechanism for long-term potentiation in the hippocampus.Nature 346, 724–729.

    Article  PubMed  CAS  Google Scholar 

  • Ben-Ari Y. (1985) Limbic seizure and brain damage produced by kainic acid: Mechanisms and relevance to human temporal lobe epilepsy.Neuroscience 14, 375–403.

    Article  PubMed  CAS  Google Scholar 

  • Ben-Ari Y. and Represa A. (1990) Brief seizure episodes induce long-term potentiation and mossy fibre sprouting in the hippocampus.Trends Neurosci. 13, 312–318.

    Article  PubMed  CAS  Google Scholar 

  • Bhat S. P., Horwitz J., Srinivasan A. and Ding L. (1991) Alpha B-crystallin exists as an independent protein in the heart and in the lens.Eur. J. Biochem. 202, 775–781.

    Article  PubMed  CAS  Google Scholar 

  • Bliss T. V. P. and Collinridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus.Nature 361, 31–39.

    Article  PubMed  CAS  Google Scholar 

  • Blok L. J., Grossmann M. E., Perry J. E., and Tindalll D. J. (1995) Characterization of an early growth response gene, which encodes a zinc finger transcription factor, potentially involved in cell cycle regulation.Mol. Endocrinol. 9, 1610–1620.

    Article  PubMed  CAS  Google Scholar 

  • Bradbury A., Possenti R., Shooter E. M., and Tirone F. (1991) Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization.Proc. Natl. Acad. Sci. USA 88, 3353–3357.

    Article  PubMed  CAS  Google Scholar 

  • Brakeman P. R., Lanahan A. A., O’Brien R., Roche K., Barnes C. A., Huganir R. L., et al. (1997) Homer: a protein that selectively binds metabotropic glutamate receptors.Nature 386, 284–288.

    Article  PubMed  CAS  Google Scholar 

  • Burtchuladze R., Frenguelli B., Blendy J., Cioffi D., Schutz D., and Silva A. J. (1994) Deficient long-term memory in mice with targeted mutation of the cAMP-responsive element-binding protein.Cell 79, 59–68.

    Article  Google Scholar 

  • Chappell T. G., Welch W. J., Schlossman D. M., Palter K. B., Schlesinger M. J., and Rothman J. E. (1986) Uncoating ATPase is a member of the 70 kilodalton family of stress proteins.Cell 45, 3–13.

    Article  PubMed  CAS  Google Scholar 

  • Civelli O., Douglass J., Goldstein A., and Herbert E. (1985) Sequence and expression of the rat prodynorphin gene.Proc. Natl. Acad. Sci. USA 82, 4291–4295.

    Article  PubMed  CAS  Google Scholar 

  • Cole A. J., Saffen D. W., Baraban J. M., and Worley P. F. (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation.Nature 340, 474–476.

    Article  PubMed  CAS  Google Scholar 

  • Cowell I. G., Skinner A., and Hurst H. C. (1992) Transcriptional repression by a novel member of the bZIP family of transcription factors.Mol. Cell. Biol. 12, 3070–3077.

    PubMed  CAS  Google Scholar 

  • Criado M., Witzemann V., Koenen M., and Sakmann B. (1988) Nucleotide sequence of the rat muscle acetylcholine receptor epsilon-subunit.Nucleic Acids Res. 16, 10,920.

    Article  CAS  Google Scholar 

  • Crosby S. D., Puetz J. J., Simburger K. S., Fahrner T. J., and Milbrandt J. (1991) The early response gene NGFI-C encodes a zinc finger transcriptional activator and is a member of the GCGGGGGCG (GSG) element-binding protein family.Mol. Cell Biol. 11, 3835–3841.

    PubMed  CAS  Google Scholar 

  • Curran T., Gordon M. B., Rubino K. L., and Sambucetti L. C. (1987) Isolation and characterization of the c-fos(rat) cDNA and analysis of post-translational modification in vitro.Oncogene 2, 79–84.

    PubMed  CAS  Google Scholar 

  • Davies S. N., Lester R. A., Reymann K. G., and Collingridge G. L. (1989) Temporally distinct pre- and post-synaptic mechanisms maintain long-term potentiation.Nature 338, 500–503.

    Article  PubMed  CAS  Google Scholar 

  • Davis J. Q., McLaughlin T., and Bennett V. (1993) Ankyrin-binding proteins related to nervous system cell adhesion molecules: candidates to provide transmembrane and intercellular connections in adult brain.J. Cell. Biol. 121, 121–133.

    Article  PubMed  CAS  Google Scholar 

  • Della N. G., Senior P. V., and Bowtell D. D. (1993) Isolation and characterisation of murine homologues of the Drosophila seven in absentia gene (sina).Development 117, 1333–1343.

    PubMed  CAS  Google Scholar 

  • Demmer J., Dragunow M., Lawlor P. A., Mason S. E., Leah J. D., Abraham W. C., et al. (1993) Differential expression of immediate early genes after hippocampal long-term potentiation in awake rats.Brain Res. Mol. Brain Res. 17, 279–286.

    Article  PubMed  CAS  Google Scholar 

  • Dragunow M., Beilharz E., Sirimanne E., Lawlor P., Williams C., Bravo R., et al. (1994) Immediate-early gene protein expression in neurons undergoing delayed death, but not necrosis, following hypoxicischaemic injury to the young rat brain.Brain Res. Mol. Brain Res. 25, 19–33.

    Article  PubMed  CAS  Google Scholar 

  • Edwards D. R., Waterhouse P., Holman M. L., and Denhardt D. T. (1986) A growth-responsive gene (16C8) in normal mouse fibroblasts homologous to a human collagenase inhibitor with erythroid-potentiating activity: evidence for inducible and constitutive transcripts.Nucleic Acids Res. 14, 8863–8878.

    Article  PubMed  CAS  Google Scholar 

  • Ehrlich M. E. and Greengard P. (1991) Characterization of rat ARPP-21 mRNA: sequence analysis, tissue distribution, and regulation.J. Neurochem. 57, 1985–1991.

    Article  PubMed  CAS  Google Scholar 

  • Fang J., Yin W., Smiley E., Wang S. Q., and Bonadio J. (1996) Molecular cloning of the mouse activin bE subunit gene.Biochem. Biophys. Res. Commun. 228, 669–674.

    Article  PubMed  CAS  Google Scholar 

  • Finnerty H., Kelleher K., Morris G. E. Bean, K., Merberg D. M., Kriz R., et al. (1993) Molecular cloning of murine FLT and FLT4.Oncogene 8, 2293–2298.

    PubMed  CAS  Google Scholar 

  • Fischer C. R., Gutierrez J., Hsu C. M., Iacangelo A., and Eiden L. E. (1990) Sequence analysis, tissue distribution and regulation by cell depolarization, and second messengers of bovine secretogranin II (chromogranin C) mRNA.J. Biol. Chem. 265, 9208–9213.

    Google Scholar 

  • Foulkes N. S., Borrelli E., and Sassone-Corsi P. (1991) CREM gene: Use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription.Cell 64, 739–749.

    Article  PubMed  CAS  Google Scholar 

  • Frank D. A. and Greenberg M. E. (1994) CREB: A mediator of long-term memory from molusks to mammals.Cell 79, 5–8.

    Article  PubMed  CAS  Google Scholar 

  • Gaestel M., Gotthardt R., and Muller T. (1993) Structure and organisation of a murine gene encoding small heat-shock protein Hsp25.Gene 128, 279–283.

    Article  PubMed  CAS  Google Scholar 

  • Gall C. (1988) Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and CCK immunoreactivities in mouse hippocampal mossy fibers.J. Neurosci. 8, 1852–1862.

    PubMed  CAS  Google Scholar 

  • Goelet P., Castellucci V. F., Shacher S., and Kandel E. R. (1986) The long and the short of long-term memory—a molecular framework.Nature 322, 419–422.

    Article  PubMed  CAS  Google Scholar 

  • Graham R. and Gilman M. (1991) Distinct protein targets for signals acting at the c-fos serum response element.Science 251, 189–192.

    Article  PubMed  CAS  Google Scholar 

  • Guan K., Haun R. S., Watson S. J., Geahlen R. L., and Dixon J. E. (1990) Cloning and expression of a protein-tyrosine-phosphatase.Proc. Natl. Acad. Sci. USA 87, 1501–1505.

    Article  PubMed  CAS  Google Scholar 

  • Guan K. L. and Dixon J. E. (1991) Eukaryotic proteins expressed in Escehrichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase.Anal. Biochem. 192, 262–267.

    Article  PubMed  CAS  Google Scholar 

  • Hanks S. K. (1991) Eukaryotic protein kinases.Cur. Op. Struct. Biol. 1, 369–383.

    Article  CAS  Google Scholar 

  • Hogan B., Constantini F., and Lacy E. (1986)Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

    Google Scholar 

  • Howard A., Feighner S., Cully D., Arena J., Liberator P., Rosenblum C., et al. (1996) A receptor in pituitary and hypothalamus that functions in growth hormone release.Science 273, 974–977.

    Article  PubMed  CAS  Google Scholar 

  • Hsu J. C., Laz T., Mohn K. L., and Taub R. (1991) Identification of LRF-1, a leucine-zipper protein that is rapidly and highly induced in regenerating liver.Proc. Natl. Acad. Sci. USA 88, 3511–3515.

    Article  PubMed  CAS  Google Scholar 

  • Huang Y. Y., Li X. C., and Kandel E. R. (1994) cAMP contributes to mossy fiber LTP by initiating both a covalently mediated phase and macromolecular synthesis-dependent late phase.Cell 79, 69–79.

    Article  PubMed  CAS  Google Scholar 

  • Imataka H., Sogawa K., Yasumoto K., Kikuchi Y., Sasano K., Kobayashi A., et al. (1992) Two regulatory proteins that bind to the basic transcription element (BTE), a GC box sequence in the promoter region of the rat P-4501A1 gene.EMBO J. 11, 3663–3671.

    PubMed  CAS  Google Scholar 

  • Jeffery K. J., Abraham W. C., Dragunow M., and Mason S. E. (1990) Induction of fos-like immunoreactivity and the maintenance of long-term potentiation in the dentate gyrus of unanesthestetized rats.Mol. Brain Res. 8, 267–274.

    Article  PubMed  CAS  Google Scholar 

  • Johnston I. G., Rush S. J., Gurd J. W., and Broen I. R. (1992) Molecular cloning of novel mRNA using an antibody directed against synaptic glycoproteins.J. Neurosci. Res. 32, 159–166.

    Article  PubMed  CAS  Google Scholar 

  • Julien J. P., Ramachandran K., and Grosveld F. (1985) Cloning of a cDNA encoding the smallest neurofilament protein from the rat.Biochem. Biophys. Acta 825, 398–404.

    PubMed  CAS  Google Scholar 

  • Kandel E. R. and O’Dell T. J. (1992) Are adult learning mechanisms also used for development?Science 258, 243–245.

    Article  PubMed  CAS  Google Scholar 

  • Kaneda N., Oshimura M., Chung S. Y., and Guroff G. (1992) Sequence of rat TIS11 cDNA, an immediate early gene induced by growth factors and phorbol esters.Gene 118, 289–291.

    Article  PubMed  CAS  Google Scholar 

  • Kawakami Z., Kitabayashi I., Matsuoka T., Gachelin G., and Yokoyama K. (1992) Conserved structural motifs among mammalian junB genes.Nucleic Acids Res. 20, 914.

    Article  PubMed  CAS  Google Scholar 

  • Keyse S. M. and Emsile E. A. (1992) Oxidative stress and heat shock induce a human gene encoding a protein tyrosine phosphatase.Nature 359, 644–647.

    Article  PubMed  CAS  Google Scholar 

  • Kirchhausen T., Harrison S. C., Chow E. P., Mattaliano R. J., Ramachandran K. L., Smart J., et al. (1987) Clathrin heavy chain: molecular cloning and complete primary structure.Proc. Natl. Acad. Sci. USA 84, 8805–8809.

    Article  PubMed  CAS  Google Scholar 

  • Kitabayashi I., Saka F., Gachelin G., and Yokoyama K. (1990) Nucleotide sequence of rat c-jun protooncogene.Nucleic Acids Res. 18, 3400.

    Article  PubMed  CAS  Google Scholar 

  • Kojima T., Shworak N. W., and Rosenberg R. D. (1992) Molecular cloning and expression of two distinct cDNAs encoding heparan sulfate proteoglycan core proteins from a rat endothelial cell line.J. Biol. Chem. 267, 4870–4877.

    PubMed  CAS  Google Scholar 

  • Kulmburg P. A., Huber N. E., Scheer B. J., Wrann M., and Baumruker T. (1992) Immunoglobulin E plus antigen challenge induces a novel intercrine/chemokine in mouse mast cells.J. Exp. Med. 176, 1773–1778.

    Article  PubMed  CAS  Google Scholar 

  • Kwak S. P. and Dixon J. E. (1995) Multiple dual specificity protein tyrosine phosphatases are expressed and regulated differentially in liver cell lines.J. Biol. Chem. 270, 1156–1160.

    Article  PubMed  CAS  Google Scholar 

  • Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey Y., and Kuhl D. (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity.Proc. Natl. Acad. Sci. USA 92, 5734–5738.

    Article  PubMed  CAS  Google Scholar 

  • Liou H.-C. and Baltimore D. (1993) Regulation of NFkB/rel transcription factor and IkB inhibitor system.Curr. Op. Cell Biol. 5, 477–487.

    Article  PubMed  CAS  Google Scholar 

  • Lomri N., Perret C., Gouhier N., and Thomasset M. (1989) Cloning and analysis of calbindin-D28K cDNA and its expression in the central nervous system.Gene 80, 87–98.

    Article  PubMed  CAS  Google Scholar 

  • Lyford G. L., Yamagata K., Kaufmann W. E., Barnes C., Sanders L. K., Copeland N. G., et al. (1995) Arc, a growth factor- and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites.Neuron 14, 433–445.

    Article  PubMed  CAS  Google Scholar 

  • Maedor W. E., Means A. R., and Quiocho F. A. (1993) Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures.Science 262, 1718–1721.

    Article  Google Scholar 

  • Maisonpierre P. C., Belluscio L., Squinto S., Ip N. Y., Furth M. E., Lindsay R. M., and Yancopoulos G. D. (1990) Neurotrophin-3: a neurotrophic factor related to NGF and BDNF.Science 247, 1446–1451.

    Article  PubMed  CAS  Google Scholar 

  • Majumdar A., Brown D., Kerby S., Rudzinski I., Polte T., Randhawa Z., and Seidman M. M. (1991) Sequence of human HMG2 cDNA.Nucleic Acids Res. 19, 6643.

    Article  PubMed  CAS  Google Scholar 

  • Malenka R. C. (1994) Synaptic plasticity in the hippocampus: LTP and LTD.Cell 78, 535–538.

    Article  PubMed  CAS  Google Scholar 

  • Manabe T., Renner P., and Nicoll R. A. (1992) Post-synaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents.Nature 355, 50–55.

    Article  PubMed  CAS  Google Scholar 

  • Mayford M., Wang J., Kandel E. R., and O’Dell T. J. (1995) CaMKII regulates the frequency-response function of hippocamppal synapses for the production of both LTD and LTP.Cell 81, 891–904.

    Article  PubMed  CAS  Google Scholar 

  • Mellor H., Flowers K. M., Kimball S. R., and Jefferson L. S. (1994) Cloning and characterization of a cDNA encoding rat PKR, the double-stranded RNA-dependent eukaryotic initiation factor-2 kinase.Biochem. Biophys. Acta 1219, 693–696.

    PubMed  Google Scholar 

  • Monard D. (1988) Cell-derived proteases and ptotease inhibitors as regulators of neurite outgrowth.Trends Neurosci. 11, 541–544.

    Article  PubMed  CAS  Google Scholar 

  • Morgan J. I. and Curran T. (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenesfos andjun.Ann. Rev. Neurosci. 14, 421–451.

    Article  PubMed  CAS  Google Scholar 

  • Mulkey R. M., Endo S., Shenolikar S., and Malenka R. C. (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression.Nature 369, 486–488.

    Article  PubMed  CAS  Google Scholar 

  • Muller R. M., Taguchi H., and Shibahara S. (1987) Nucleotide sequence and organization of the rat heme oxygenase gene.J. Biol. Chem. 262, 6795–6802.

    PubMed  CAS  Google Scholar 

  • Nadler J. V. (1978) Kainic acid as a tool for the study of temporal lobe epilepsy.Life Sci. 29, 2031–2042.

    Article  Google Scholar 

  • Naeve G. S., Ramakrishnan M., Kramer R., Hevroni D., Citri Y., and Theill L. E. (1997) Neuritin: A gene induced by neural activity and neurotrophins that promotes neuritogenesis.Proc. Natl. Acad. Sci. USA 94, 2648–2653.

    Article  PubMed  CAS  Google Scholar 

  • Nedivi E., Fieldust S., Theill L. E., and Hevroni D. (1996) A set of genes expressed in response to light in the adult cerebral cortex and regulated during development.Proc. Natl. Acad. Sci. USA 93, 2048–2053.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nedivi E., Wu G.-Y., and Cline H. T. (1997) cpg15, a candidate plasticity-related gene involved in dendritic arbor growth.Soc. Neurosci. Abstract 23, 607.

    Google Scholar 

  • Nguyen P. V., Abel T., and Kandel E. R. (1994) Requirement of a critical period of transcription for induction of a late phase of LTP.Science 265, 1104–1107.

    Article  PubMed  CAS  Google Scholar 

  • Noda M., Teranishi Y., Takahashi H., Toyosato M., Notake M., Nakanishi S., and Numa S. (1982) Isolation and structural organization of the human preproenkephalin gene.Nature 297, 431–434.

    Article  PubMed  CAS  Google Scholar 

  • O’Banion M. K., Winn V. D., and Young D. A. (1992) cDNA cloning and functional activity of a glucocorticoid-regulated inflammatory cyclooxygenase.Proc. Natl. Acad. Sci. USA 89, 4888–4892.

    Article  PubMed  CAS  Google Scholar 

  • Ohkura N., Hijikuro M., Yamamoto A., and Miki K. (1994) Molecular cloning of a novel thyroid/steroid receptor superfamily gene from cultured rat neuronal cells.Biochem. Biophys. Res. Commun. 205, 1959–1965.

    Article  PubMed  CAS  Google Scholar 

  • Ohmstede C. A., Bland M. M., Merrill B. M., and Sahyoun N. (1991) Relationship of genes encoding Ca+2/calmodulin-dependent protein kinase Gr and calsperin.Proc. Natl. Acad. Sci. USA 88, 5784–5788.

    Article  PubMed  CAS  Google Scholar 

  • Pajunen A., Crozat A., Janne O. A., Ihalainen R., Laitinen P. H., Stanley B., et al. (1988) Structure and regulation of mammalian S-adenosyl methionine decarboxylase.J. Biol. Chem. 263, 17,040–17,049.

    CAS  Google Scholar 

  • Patwardhan S., Gashler A., Siegel M. G., Chang L. C., Joseph L. J., Shows T. B., et al. (1991) EGR3, a novel member of the Egr family of genes encoding immediate-early transcription factors.Oncogene 6, 917–928.

    PubMed  CAS  Google Scholar 

  • Petropoulos D., Part A., Ochoa M., Zakin M., and Lamas E. (1995) NOR-2 (neuron-derived orphan receptor), a brain zinc finger protein, is highly induced during liver regeneration.FEBS Lett. 372, 273–278.

    Article  PubMed  CAS  Google Scholar 

  • Possenti R., Eldridge J. D., Paterson B. M., Grasso A., and Levi A. (1989) A protein induced by NGF in PC12 cells is stored in secretory vesicles and released through the regulated pathway.EMBO J. 8, 2217–2223.

    PubMed  CAS  Google Scholar 

  • Powell M. J. and Watts F. Z. (1990) Isolation of a gene encoding a mitochondrial HSP70 protein from Schizosaccharomyces pombe.Gene 95, 105–110.

    Article  PubMed  CAS  Google Scholar 

  • Pragnell M., Sakamoto J., Jay S. D., and Campbell K. P. (1991) Cloning and tissue-specific expression of the brain calcium channel beta-subunit.FEBS Lett. 291, 253–258.

    Article  PubMed  CAS  Google Scholar 

  • Qian Z., Gilbert M. E., Colicos M. A., Kandel E. R., and Kuhl D. (1993) Tissue-plasminogen activator is induced as an immediate early gene during seizure, kindling and long-term potentiation.Nature 361, 453–457.

    Article  PubMed  CAS  Google Scholar 

  • Raff M. C., Barres B. A., Burne J. F., Coles H. S., Ishizaki Y., and Jacobson M. D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system.Science 262, 695–700.

    Article  PubMed  CAS  Google Scholar 

  • Rapp G., Freudenstein J., Klaudiny J., Mucha J., Wempe F., Zimmer M., and Scheit K. H. (1990) Characterization of three abundant mRNAs from human ovarian granulosa cells.DNA Cell Biol. 9, 479–485.

    Article  PubMed  CAS  Google Scholar 

  • Rattner A., Korner M., Walker M. D., and Citri Y. (1993) NF-kB activates the HIV promoter in neurons.EMBO J. 12, 4261–4267.

    PubMed  CAS  Google Scholar 

  • Ripperger J. A., Fritz S., Richter K., Hocke G. M., Lottspeich F., and Fey G. H. (1995) Transcription factors Stat3 and Stat5b are present in rat liver nuclei late in an acute phase response and bind interleukin-6 response elements.J. Biol. Chem. 270, 29,998–30,006.

    CAS  Google Scholar 

  • Saga Y., Tsukamoto T., Jing N., Kusakabe M., and Sakakura T. (1991) Murine tenascin: cDNA cloning, structure and temporal expression of isoforms.Gene 104, 177–185.

    Article  PubMed  CAS  Google Scholar 

  • Salminen M., Lundstorm K., Tilgmann C., Savolainen R., Kalkkinen N., and Ulmanen I. (1990) Molecular cloning and characterization of rat liver catechol-O-methyltransferase.Gene 93, 241–247.

    Article  PubMed  CAS  Google Scholar 

  • Salton S. R. (1991) Nucleotide sequence and regulatory studies of VGF, a nervous system-specific mRNA that is rapidly and relatively selectively induced by nerve growth factor.J. Neurochem. 57, 991–996.

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J., Fritsch E. F., and Maniatis T. (1989)Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

    Google Scholar 

  • Scearce L. M., Laz T. M., Hazel T. G., Lau L. F., and Taub R. (1993) RNR-1, a nuclear receptor in the NGFI-B/Nur77 family that is rapidly induced in regenerating liver.J. Biol. Chem. 268, 8855–8861.

    PubMed  CAS  Google Scholar 

  • Seger R., Seger D., Reszka A. A., Munar E. S., Eldar-Finkelman H., Dobrowolska G., Jensen A. M., et al. (1994) Overexpression of mitogen-activated protein kinase kinase (MAPKK) and its mutants in NIH3T3 cells.J. Biol. Chem. 269, 25,699–25,709.

    CAS  Google Scholar 

  • Shatz C. J. (1990) Impulse activity and the patterning of connections during CNS development.Neuron 5, 745–756.

    Article  PubMed  CAS  Google Scholar 

  • Sheng M. and Greenberg M. E. (1990) The regulation and function ofc-fos and other immediate early genes in the nervous system.Neuron 4, 477–485.

    Article  PubMed  CAS  Google Scholar 

  • Shimasaki S., Koba A., Mercado M., Shimonaka M., and Ling N. (1989) Complementary DNA structure of the high molecular weight rat insulin-like growth factor binding protein (IGF-BP3) and tissue distribution of its mRNA.Biochem. Biophys. Res. Commun. 165, 907–912.

    Article  PubMed  CAS  Google Scholar 

  • Silva A. J. and Giese K. P. (1994) Plastic genes are in!Curr. Opin. Neurobiol. 4, 413–420.

    Article  PubMed  CAS  Google Scholar 

  • Silva A. J., Stevens C. F., Tonegawa S., and Wang Y. (1992) Deficient hippocampal long-term potentiation in a-Calcium-Calmodulin Kinase II mutant mice.Science 257, 201–206.

    Article  PubMed  CAS  Google Scholar 

  • Sloviter R. S. (1992) Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats.Neurosci. Lett. 137, 91–96.

    Article  PubMed  CAS  Google Scholar 

  • Smeyene R. J., Vendrell M., Hayward M., Baker S. J., Miao G. G., Shilling K., et al. (1993) Continuousc-fos expression precedes programmed cell death.Nature 363, 166–169.

    Article  Google Scholar 

  • Steele F. R., Chader G. J., Johnson L. V., and Tombran T. J. (1993) Pigment epithelium-derived factor: neurotrophic activity and identification as a member of the serine protease inhibitor gene family.Proc. Natl. Acad. Sci. USA 90, 1526–1530.

    Article  PubMed  CAS  Google Scholar 

  • Stevens C. F. and Wang Y. (1993) Reversal of long-term potentiation by inhibitors of haem oxygenase.Nature 364, 147–149.

    Article  PubMed  CAS  Google Scholar 

  • Subramaniam M., Harris S. A., Oursler M. J., Rasmussen K., Riggs B. L., and Spelsberg T. C. (1995) Identification of a novel TGF-beta-regulated gene encoding a putative zinc finger protein in human osteoblasts.Nucleic Acids Res. 23, 4907–4912.

    Article  PubMed  CAS  Google Scholar 

  • Sun H., Charles C. H., Lau L. F., and Tonks N. K. (1993) MKP-1 (3CH134), an immediate early gene product, is a dual specificity phospahatase that dephosphorylates MAP kinase in vivo.Cell 75, 487–493.

    Article  PubMed  CAS  Google Scholar 

  • Tauck D. L. and nadler J. V. (1985) Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats.Neuroscience 5, 1016–1022.

    PubMed  CAS  Google Scholar 

  • Tewari M., Mohn K. L., Yue F. E., and Taub R. (1992) Sequence of rat RL/IF-1 encoding an IkappaB, and comparison with related proteins containing notch-like repeats.Nucleic Acids Res. 20, 607.

    Article  PubMed  CAS  Google Scholar 

  • Thomas K. L., Laroche S., Errington M. L., Bliss T. V., and Hunt S. P. (1994) Spatial and temporal changes in signal transduction pathways during LTP.Neuron 13, 737–745.

    Article  PubMed  CAS  Google Scholar 

  • Turley S. J., Tan E. M., and Pollard K. M. (1993) Molecular cloning and sequence analysis of U3 snoRNA-associated mouse fibrillarin.Biochem. Biophys. Acta 1216, 119–122.

    PubMed  CAS  Google Scholar 

  • Ward Y., Gupta S., Jensen P., Waterman M., and Kelly K. (1994) Control of MAP kinase activation by the mitogen-induced threoine/tyrosine phosphatase PAC-1.Nature 367, 651–654.

    Article  PubMed  CAS  Google Scholar 

  • Watson J. B., Battenberg E. F., Wong K. K., Bloom F. E., and Sutcliffe J. G. (1990) Subtractive cDNA cloning of RC3, a rodent cortex-enriched mRNA encoding a novel 78 residue protein.J. Neurosci. Res. 26, 397–408.

    Article  PubMed  CAS  Google Scholar 

  • Williams J. H., Errington M. L., Lynch M. A., and Bliss T. V. (1989) Arachidonic acid induces a long-term activity-dependent enhancement of synaptic transmission in the hippocampus.Nature 341, 739–742.

    Article  PubMed  CAS  Google Scholar 

  • Yamagata K., Andreasson K. I., Kaufmann W. E., Barnes C. A., and Worley P. F. (1993) Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids.Neuron 11, 371–386.

    Article  PubMed  CAS  Google Scholar 

  • Yamagata K., Kaufmann W. E., Lanahan A. A., Papavlou M., Barnes C. A., Andreasson K. I., and Worley P. F. (1994a)Egr3/Pilot, a zinc-finger transcription factor, is rapidly regulated by activity in brain neurons and colocalizes withEgr1/Zif268.Learning & Memory 1, 140–152.

    CAS  Google Scholar 

  • Yamagata K., Sanders L. K., Kaufman W. E., Yee W., Barnes C. A., Nathans D., and Worley P. F. (1994b) rheb, a growth factor-and synaptic activity-regulated gene, encodes a novel Ras-related protein.J. Biol. Chem. 269, 16,333–16,339.

    CAS  Google Scholar 

  • Yamaguchi M., Hirose F., Hayashi Y., Nishimoto Y., and Matsukage A. (1987) Murine DNA polymerase beta gene: mapping of transcription initiation sites and the nucleotide sequence of the putative promoter region.Mol. Cell. Biol. 7, 2012–2018.

    PubMed  CAS  Google Scholar 

  • Yoshimura T., Takeya M., and Takahashi K. (1991) Molecular cloning of rat monocyte chemoattractant protein-1 (MCP-1) and its expression in rat spleen cells and tumor cell lines.Biochem. Biophys. Res. Commun. 174, 504–509.

    Article  PubMed  CAS  Google Scholar 

  • Youssoufian H., McAfee M., and Kwiatkowski D. J. (1990) Cloning and chromosomal localization of the human cytoskeletal alpha-actinin gene reveals linkage to the beta-spectrin gene.Am. J. Hum. Genet. 47, 62–71.

    PubMed  CAS  Google Scholar 

  • Zerial M., Toschi L., Ryseck R. P., Schuermann M., Muller R., and Bravo R. (1989) The product of a novel growth factor activated gene, fos B, interacts with JUN proteins enhancing their DNA binding activity.EMBO J. 8, 805–813.

    PubMed  CAS  Google Scholar 

  • Zhuo M., Small S. A., Kandel E. R., and Hawkins R. D. (1993) Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus.Science 260, 1946–1950.

    Article  PubMed  CAS  Google Scholar 

  • Zmudzka B. Z., SenGupta D., Matsukage A., Cobianchi F., Kumar P., and Wilson S. H. (1986) Structure of rat DNA polymerase beta revealed by partial amino acid sequencing and cDNA cloning.Proc. Natl. Acad. Sci. USA 83, 5106–5110.

    Article  PubMed  CAS  Google Scholar 

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Author notes

  1. Dana Hevroni

    Present address: QBI Enterprises, P.O. Box 741, 74106, Nes-Ziona, Israel

  2. Amir Rattner

    Present address: Department of Molecular Biology and Medicine, Johns Hopkins University School of Medicine, 21205, Baltimore, MD

  3. Marsha Bundman

    Present address: Center for Molecular Neurobiology, University of Hamburg, D-20246, Hamburg, Germany

  4. Doron Lederfein

    Present address: Center for Neurobiology and Behavior, College of Physicians and Surgeons of Columbia University, 10032, New York, NY

  5. Michael A. Silverman

    Present address: Department of Neuroscience, University of Virginia School of Medicine, 22908, Charlottesville, VA

  6. Elly Nedivi

    Present address: Cold Spring Harbor Laboratory, 11724, Cold Spring Harbor, NY

Authors and Affiliations

  1. Department of Hormone Research, The Weizmann Institute of Science, 76100, Rehovot, Israel

    Dana Hevroni, Amir Rattner, Marsha Bundman, Doron Lederfein, Awni Gabarah, Miriam Mangelus, Michael A. Silverman, Hilla Kedar, Cathy Naor, Elly Nedivi & Yoav Citri

  2. Membrane Research and Biophysics, The Weizmann Institute of Science, 76100, Rehovot, Israel

    Tamar Hanoch & Rony Seger

  3. Molecular Biology Department, Amgen Center, 91320-1789, Thousand Oaks, CA

    Masayo Kornuc & Lars E. Theill

  4. Department of Psychology, University of Haifa, 31905, Haifa, Israel

    Gal Richter-Levin

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  1. Dana Hevroni
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Additional information

This article is dedicated to the memory of our mentor, friend, and colleague, Dr. Yoav Citri, who died tragically in a road accident on December 13, 1995.

Address to which all correspondence and reprint requests should be sent: Department of Biological Regulation, The Weizmann Institute of Science, Rehovot 76100, Israel

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Hevroni, D., Rattner, A., Bundman, M. et al. Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. J Mol Neurosci 10, 75–98 (1998). https://doi.org/10.1007/BF02737120

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  • DOI: https://doi.org/10.1007/BF02737120

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