Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation

Cole, Andrew J.; Saffen, David; Baraban, Jay M.; Worley, Paul F.

doi:10.1038/340474a0

Cited by 971 publications

(504 citation statements)

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“…In contrast, SRE-dependent transcription (discussed below) can be stimulated independently of increases in nuclear calcium by a rise in cytoplasmic calcium (Hardingham et al, 1997). This may explain why the zif/268 gene, which contains several SREs in its promoter (Changelian et al, 1989;Christy et al, 1989), is activated even with moderate LTP-inducing stimuli that may not increase the nuclear calcium concentration (Cole et al, 1989;Wisden et al, 1990;Worley et al, 1993). The molecular mechanisms controlled by nuclear calcium may involve CaM kinase IV.…”

Section: Cre-mediated Calcium-activated Transcriptionmentioning

confidence: 83%

“…for transcriptional regulation by the excitatory neurotransmitter glutamate (Cole et al, 1989;Wisden et al, 1990;Lerea et al, 1992;Bading et al, 1993Bading et al, , 1995Lerea and McNamara, 1993). A previous study has shown that the c-fos SRE can f unction as an NMDA receptor-responsive element (Bading et al, 1993).…”

Section: Nmda Receptor Activation Can Mediate Transcriptional Inductimentioning

confidence: 99%

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Calcium Controls Gene Expression via Three Distinct Pathways That Can Function Independently of the Ras/Mitogen-Activated Protein Kinases (ERKs) Signaling Cascade

et al. 1997

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Calcium ions are the principal second messenger in the control of gene expression by electrical activation of neurons. However, the full complexity of calcium-signaling pathways leading to transcriptional activation and the cellular machinery involved are not known. Using the c-fos gene as a model system, we show here that the activity of its complex promoter is controlled by three independently operating signaling mechanisms and that their functional significance is cell type-dependent. The serum response element (SRE), which is composed of a ternary complex factor (TCF) and a serum response factor (SRF) binding site, integrates two calcium-signaling pathways. In PC12 cells, calcium-regulated transcription mediated by the SRE requires the TCF site and is not inhibited by expression of the dominant-negative Ras mutant, RasN17, nor by the MAP kinase kinase 1 inhibitor PD 98059. In contrast, TCF-dependent transcriptional regulation by nerve growth factor or epidermal growth factor is mediated by a Ras/MAP kinases (ERKs) pathway targeting the TCF Elk-1. In AtT20 cells and hippocampal neurons, calcium signals can stimulate transcription via a TCFindependent mechanism that requires the SRF binding site. The cyclic AMP response element (CRE), which cooperates with the TCF site in growth factor-regulated transcription, is a target of a third calcium-regulated pathway that is little affected by the expression of RasN17 or by PD 98059. Thus, calcium can stimulate gene expression via a TCF-, SRF-, and CRE-linked pathway that can operate independently of the Ras/MAP kinases (ERKs) signaling cascade in a cell type-dependent manner.

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Section: Cre-mediated Calcium-activated Transcriptionmentioning

confidence: 83%

Section: Nmda Receptor Activation Can Mediate Transcriptional Inductimentioning

confidence: 99%

Calcium Controls Gene Expression via Three Distinct Pathways That Can Function Independently of the Ras/Mitogen-Activated Protein Kinases (ERKs) Signaling Cascade

et al. 1997

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“…Manipulation of metabotropic glutamate receptors has been associated with altered expression of c-Fos (Kaatz and Albin, 1995;Kearney et al, 1997;Zhao et al, 2006;Besheer et al, 2009), a member of a family of immediate early gene transcription factors that is commonly used as a biomarker for mapping neuronal activity Cole et al, 1989;Morgan et al, 1987;Olive et al, 2001). Furthermore, the nucleus accumbens and the amygdala are critically involved in modulating the discriminative stimulus effects of alcohol (Hodge and Aiken, 1996;Hodge and Cox, 1998;Besheer et al, 2003).…”

Section: Examination Of C-fos Ir In the Amygdala And Nucleus Accumbensmentioning

confidence: 99%

Activation of Group II Metabotropic Glutamate Receptors Inhibits the Discriminative Stimulus Effects of Alcohol via Selective Activity Within the Amygdala

Cannady

Grondin

Fisher

et al. 2011

Neuropsychopharmacol

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Metabotropic glutamate receptor subtypes (mGlu2/3) regulate a variety of alcohol-associated behaviors, including alcohol reinforcement, and relapse-like behavior. To date, the role of mGlu2/3 receptors in modulating the discriminative stimulus effects of alcohol has not been examined. Given that the discriminative stimulus effects of drugs are determinants of abuse liability and can influence drug seeking, we examined the contributions of mGlu2/3 receptors in modulating the discriminative stimulus effects of alcohol. In male Long-Evans rats trained to discriminate between alcohol (1 g/kg, IG) and water, the mGlu2/3 agonist LY379268 (0.3-10 mg/kg) did not produce alcohollike stimulus effects. However, pretreatment with LY379268 (1 and 3 mg/kg; in combination with alcohol) inhibited the stimulus effects of alcohol (1 g/kg). Systemic LY379268 (3 mg/kg, i.p.) was associated with increases in neuronal activity within the amygdala, but not the nucleus accumbens, as assessed by c-Fos immunoreactivity. Intra-amygdala activation of mGlu2/3 receptors by LY379268 (6 mg) inhibited the discriminative stimulus effects of alcohol, without altering response rate. In contrast, intra-accumbens LY379268 (3 mg) profoundly reduced response rate; however, at lower LY379268 doses (0.3, 1 mg), the discriminative stimulus effects of alcohol and response rate were not altered. These data suggest that amygdala mGlu2/3 receptors have a functional role in modulating the discriminative stimulus properties of alcohol and demonstrate differential motor sensitivity to activation of mGlu2/3 receptors in the amygdala and the accumbens. Understanding the neuronal mechanisms that underlie the discriminative stimulus effects of alcohol may prove to be important for future development of pharmacotherapies for treating alcoholism.

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“…While it is now well established that long-term potentiation (LTP), a physiological model of the memory storage process, activates immediate early genes encoding transcription factors (1,2), there is no evidence to our knowledge indicating what target genes are activated by these transcription factors. GAP-43, ¶ the presynaptically localized, growth-associated protein whose expression is up-regulated during axonal outgrowth in development and axonal regeneration (3), and whose phosphorylation is increased after LTP (4), is one likely candidate target gene (see also ref.…”

mentioning

confidence: 99%

Long-term potentiation activates the GAP-43 promoter: Selective participation of hippocampal mossy cells

Namgung

Matsuyama

Routtenberg

1997

Proc. Natl. Acad. Sci. U.S.A.

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Perforant path long-term potentiation (LTP) in intact mouse hippocampal dentate gyrus increased the neuron-specific, growth-associated protein GAP-43 mRNA in hilar cells 3 days after tetanus, but surprisingly not in granule cells While it is now well established that long-term potentiation (LTP), a physiological model of the memory storage process, activates immediate early genes encoding transcription factors (1, 2), there is no evidence to our knowledge indicating what target genes are activated by these transcription factors. GAP-43, ¶ the presynaptically localized, growth-associated protein whose expression is up-regulated during axonal outgrowth in development and axonal regeneration (3), and whose phosphorylation is increased after LTP (4), is one likely candidate target gene (see also ref. 5). A previous study of chronic recording in intact freely moving rats 3 days after LTP induction revealed that perforant path LTP altered GAP-43 mRNA expression (6). To explore the hypothesis that the alteration in GAP-43 mRNA was related to altered transcriptional activity of the GAP-43 gene in hippocampal neurons after LTP, we first studied the effect of LTP in the intact mouse on the endogenous pattern of GAP-43 mRNA transcript levels with in situ hybridization. We then studied the effect of LTP on promoter activation in transgenic mice bearing a GAP-43 promoter-lacZ reporter construct. MATERIALS AND METHODSAnimals. Mouse strain C57BL͞6 was obtained from The Jackson Laboratory. Heterozygous GAP-43͞lacZ transgenic mouse line 252 bearing 6-kb 5Ј-flanking and 11-kb first intron sequence driving lacZ reporter gene was bred with C57BL͞6 mice, and homozygous transgenic mice were initially screened by genomic DNA Southern or dot hybridization. Constitutive expression of the transgene in hippocampus in GAP-43͞lacZ transgenic mouse line 252 has been described (7, 8). Thirty-five male homozygous transgenic mice (2 months old) were used in the electrophysiological and histochemical analysis.Electrophysiology. In vivo LTP in anesthetized mice was performed essentially as described previously (9). Potentiated responses were measured by percent baseline population spike amplitude. Mean potentiation of combined 1-, 2-, and 3-day LTP group animals was 255% Ϯ 40.1% (n ϭ 20; mean Ϯ SEM) over the 2-hr recording session and did not show any significant difference from that of wild-type C57BL͞6 mice (229.4% Ϯ 36.3%, P Ͼ 0.10). Mean response of the low-frequency control (LFC) animals during the 2-hr recording period was 101.1 Ϯ 5.5 (n ϭ 15). In the LTP experiment with DL-aminophosphonovalerate (APV; Sigma) ejection, 80 nl (1.6 nmol) of APV dissolved in 20 mM Tris⅐HCl (pH 8.0) was pressure-ejected from the recording micropipette into the dentate gyrus molecular layer, using procedures described earlier (10). APV was delivered 15 min prior to high-frequency tetanic stimulation. Equivalent volumes of 20 mM Tris vehicle were ejected into the same region of the hippocampus in control group animals. Potentiated responses in the molecul...

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Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation

Cited by 971 publications

References 29 publications

Calcium Controls Gene Expression via Three Distinct Pathways That Can Function Independently of the Ras/Mitogen-Activated Protein Kinases (ERKs) Signaling Cascade

Calcium Controls Gene Expression via Three Distinct Pathways That Can Function Independently of the Ras/Mitogen-Activated Protein Kinases (ERKs) Signaling Cascade

Activation of Group II Metabotropic Glutamate Receptors Inhibits the Discriminative Stimulus Effects of Alcohol via Selective Activity Within the Amygdala

Long-term potentiation activates the GAP-43 promoter: Selective participation of hippocampal mossy cells

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