‘Silent’ priming of translation-dependent LTP by β-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors

Tenorio, Gustavo; Connor, Steven A.; Guévremont, Diane; Abraham, Wickliffe C.; Williams, J.H.; O’Dell, Thomas J.; Nguyen, Peter V.

doi:10.1101/lm.1974510

Cited by 63 publications

(81 citation statements)

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“…1B; mean fEPSP slope was 142% + 7% 120 min after HFS). In a previous study (Tenorio et al 2010), a 1-h time lag between washout of ISO and HFS was used successfully to elicit metaplastic enhancement of LTP maintenance similar to our present study. Thus, acute bath application of NE can prime synapses to boost subsequent expression of long-lasting LTP.…”

Section: Norepinephrine (Ne) Induces Metaplasticity Of Ltpsupporting

confidence: 62%

“…Also, NE paired with high-frequency stimulation (HFS) enhanced field EPSP (fEPSP) potentiation in CA1 of rat hippocampal slices (Katsuki et al 1997). Additionally, Tenorio et al (2010) found that ISO enhanced future LTP through a process known as "metaplasticity" (see Abraham and Bear 1996).…”

Section: Norepinephrine (Ne) Induces Metaplasticity Of Ltpmentioning

confidence: 99%

“…ISO applied prior to HFS can also promote translation-dependent LTP when one train of 100-Hz was applied well after ISO washout (Tenorio et al 2010). To determine whether the natural transmitter, NE, could prime synapses in CA1 to express translation-dependent LTP, we used two translation inhibitors, emetine (EME, 20 mM) and cycloheximide (CHX, 80 mM).…”

Section: Ne-induced Metaplasticity Requires Translationmentioning

confidence: 99%

“…Importantly, ISO engaged metaplastic mechanisms to recruit protein synthesis-dependent LTP when a subthreshold HFS was applied 1 h after ISO washout (Tenorio et al 2010). b-AR activation by ISO recruited cAMP-dependent protein kinase (PKA) to phosphorylate GluA1 subunits of AMPA receptors, which increased cell surface GluA1 expression in a protein synthesisdependent manner (Tenorio et al 2010).…”

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Norepinephrine triggers metaplasticity of LTP by increasing translation of specific mRNAs

et al. 2015

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Norepinephrine (NE) is a key modulator of synaptic plasticity in the hippocampus, a brain structure crucially involved in memory formation. NE boosts synaptic plasticity mostly through initiation of signaling cascades downstream from beta (b)-adrenergic receptors (b-ARs). Previous studies demonstrated that a b-adrenergic receptor agonist, isoproterenol, can modify the threshold for long-term potentiation (LTP), a putative cellular mechanism for learning and memory, in a process known as "metaplasticity." Metaplasticity is the ability of synaptic plasticity to be modified by prior experience. We asked whether NE itself could engage metaplastic mechanisms in area CA1 of mouse hippocampal slices. Using extracellular field potential recording and stimulation, we show that application of NE (10 mM), which did not alter basal synaptic strength, enhances the future maintenance of LTP elicited by subthreshold, high-frequency stimulation (HFS: 1 × 100 Hz, 1 sec). HFS applied 30 min after NE washout induced long-lasting (.4 h) LTP, which was significantly extended in duration relative to HFS alone. This NE-induced metaplasticity required b1-AR activation, as coapplication of the b1-receptor antagonist CGP-20712A (1 mM) attenuated maintenance of LTP. We also found that NE-mediated metaplasticity was translationand transcription-dependent. Polysomal profiles of CA1 revealed increased translation rates for specific mRNAs during NEinduced metaplasticity. Thus, activation of b-ARs by NE primes synapses for future long-lasting plasticity on time scales extending beyond fast synaptic transmission; this may facilitate neural information processing and the subsequent formation of lasting memories.

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Section: Norepinephrine (Ne) Induces Metaplasticity Of Ltpsupporting

confidence: 62%

Section: Norepinephrine (Ne) Induces Metaplasticity Of Ltpmentioning

confidence: 99%

Section: Ne-induced Metaplasticity Requires Translationmentioning

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Norepinephrine triggers metaplasticity of LTP by increasing translation of specific mRNAs

et al. 2015

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“…Rat cortical neurons were treated with NMDA or glycine, chemical stimuli shown to induce LTD or LTP, respectively (cLTD/cLTP), and which are known to regulate S845 phosphorylation (26)(27)(28). Alternatively, neurons were treated with Iso, a noradrenaline analog known to result in phosphorylation of GluA1 S845 via activation of β-adrenergic receptors and PKA (10,17,23,29,30). cLTD treatment significantly reduced the levels of phospho-S845, whereas cLTP and Iso increased the signal of phospho-S845 (Fig.…”

Section: Quantification Of Phospho-glua1 Containing Ampar Tetramers Umentioning

confidence: 99%

Extensive phosphorylation of AMPA receptors in neurons

Diering

Heo

Hussain

et al. 2016

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

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Regulation of AMPA receptor (AMPAR) function is a fundamental mechanism controlling synaptic strength during long-term potentiation/depression and homeostatic scaling. AMPAR function and membrane trafficking is controlled by protein-protein interactions, as well as by posttranslational modifications. Phosphorylation of the GluA1 AMPAR subunit at S845 and S831 play especially important roles during synaptic plasticity. Recent controversy has emerged regarding the extent to which GluA1 phosphorylation may contribute to synaptic plasticity. Here we used a variety of methods to measure the population of phosphorylated GluA1-containing AMPARs in cultured primary neurons and mouse forebrain. Phosphorylated GluA1 represents large fractions from 12% to 50% of the total population under basal and stimulated conditions in vitro and in vivo. Furthermore, a large fraction of synapses are positive for phospho-GluA1-containing AMPARs. Our results support the large body of research indicating a prominent role of GluA1 phosphorylation in synaptic plasticity. up from the subunits GluA1-4, mediate the majority of the fast excitatory synaptic transmission in the central nervous system (1). Regulation of AMPAR function is highly dynamic and represents a fundamental mechanism to control synaptic strength for many forms of synaptic plasticity, including long-term potentiation and depression (LTP/LTD) and homeostatic scaling (1).The function and membrane trafficking of AMPARs is regulated by multiple interacting proteins, as well as by posttranslational modifications, including phosphorylation, palmitoylation, and ubiquitination (1). In particular, phosphorylation of GluA1 at S845 by cyclic-AMP-dependent protein kinase (PKA) (2) and at S831 by calcium/calmodulin-dependent protein kinase II (CaMKII) or protein kinase C (PKC) (3, 4) have been extensively studied. PKA-mediated phosphorylation of GluA1 S845 has been shown to promote GluA1 cell-surface insertion and synaptic retention, increase channel open-probability, facilitate the induction of LTP, and mediate homeostatic scaling-up, whereas dephosphorylation of S845 is associated with receptor endocytosis, LTD, and homeostatic scaling-down (5-13). CaMKII-mediated phosphorylation of GluA1 S831 increases channel conductance and regulates LTP (8,(13)(14)(15)(16). Perhaps the strongest evidence for roles of GluA1 S845 and S831 phosphorylation comes from studies of mice with knockin mutations in which GluA1 phosphorylation is disrupted or mimicked. Several forms of behavior and synaptic plasticity in multiple brain regions require S845 or S831 phosphorylation, including hippocampal/cortical LTP and LTD, homeostatic plasticity, modulation of plasticity by neuromodulators, hippocampal spatial memory, fear-learning/extinction, appetitive incentive learning, and the action of antidepressants (8,(10)(11)(12)(17)(18)(19)(20)(21)(22)(23).A recent study (24) used a variant of SDS/PAGE, called Phostag, to quantify the stoichiometry of GluA1 S845/S831 phosphorylation. Surprisingly, the authors of th...

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Hippocampal long‐term potentiation that is elicited by perforant path stimulation or that occurs in conjunction with spatial learning is tightly controlled by beta‐adrenoreceptors and the locus coeruleus

Hansen

Manahan‐Vaughan

2015

Hippocampus

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The noradrenergic system, driven by locus coeruleus (LC) activation, plays a key role in the regulating and directing of changes in hippocampal synaptic efficacy. The LC releases noradrenaline in response to novel experience and LC activation leads to an enhancement of hippocampus-based learning, and facilitates synaptic plasticity in the form of long-term depression (LTD) and long-term potentiation (LTP) that occur in association with spatial learning. The predominant receptor for mediating these effects is the badrenoreceptor. Interestingly, the dependency of synaptic plasticity on this receptor is different in the hippocampal subfields whereby in the CA1 in vivo, LTP, but not LTD requires b-adrenoreceptor activation, whereas in the mossy fiber synapse LTP and LTD do not depend on this receptor. By contrast, synaptic plasticity that is facilitated by spatial learning is highly dependent on b-adrenoreceptor activation in both hippocampal subfields. Here, we explored whether LTP induced by perforant-path (pp) stimulation in vivo or that is facilitated by spatial learning depends on b-adrenoreceptors. We found that under both LTP conditions, antagonising the receptors disabled the persistence of LTP. badrenoreceptor-antagonism also prevented spatial learning. Strikingly, activation of the LC before high-frequency stimulation (HFS) of the pp prevented short-term potentiation but not LTP, and LC stimulation after pp-HFS-induced depotentiation of LTP. This depotentiation was prevented by b-adrenoreceptor-antagonism. These data suggest that badrenoreceptor-activation, resulting from noradrenaline release from the LC during enhanced arousal and learning, comprises a mechanism whereby the duration and degree of LTP is regulated and fine tuned. This may serve to optimize the creation of a spatial memory engram by means of LTP and LTD. This process can be expected to support the special role of the dentate gyrus as a crucial subregional locus for detecting and processing novelty within the hippocampus. V C 2015 The Authors Hippocampus Published by Wiley Periodicals, Inc.

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‘Silent’ priming of translation-dependent LTP by β-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors

Cited by 63 publications

References 65 publications

Norepinephrine triggers metaplasticity of LTP by increasing translation of specific mRNAs

Norepinephrine triggers metaplasticity of LTP by increasing translation of specific mRNAs

Extensive phosphorylation of AMPA receptors in neurons

Hippocampal long‐term potentiation that is elicited by perforant path stimulation or that occurs in conjunction with spatial learning is tightly controlled by beta‐adrenoreceptors and the locus coeruleus

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