Temporal Memory and Its Enhancement by Estradiol Requires Surface Dynamics of Hippocampal CA1 N-Methyl-D-Aspartate Receptors

Potier, M.; Georges, François; Brayda-Bruno, Laurent; Ladépêche, Laurent; Lamothe, Valérie; Abed, Alice Shaam Al; Groc, Laurent; Marighetto, Aline

doi:10.1016/j.biopsych.2015.07.017

Cited by 50 publications

(43 citation statements)

References 64 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Interestingly, it has been reported that GluN2B-NMDAR surface dynamics are specifically altered when neurons are exposed to the extracellular protein reelin (Groc et al, 2007), to sexual hormone estrogen (Potier et al, 2016), or to strong synaptic activation (Dupuis et al, 2014). These paradigms have in common to be potent regulators of NMDAR-dependent synaptic maturation and plasticity in the hippocampus.…”

Section: Discussionmentioning

confidence: 99%

Co-agonists differentially tune GluN2B-NMDA receptor trafficking at hippocampal synapses

Ferreira

Papouin

Ladépêche

et al. 2017

eLife

Self Cite

View full text Add to dashboard Cite

The subunit composition of synaptic NMDA receptors (NMDAR), such as the relative content of GluN2A- and GluN2B-containing receptors, greatly influences the glutamate synaptic transmission. Receptor co-agonists, glycine and D-serine, have intriguingly emerged as potential regulators of the receptor trafficking in addition to their requirement for its activation. Using a combination of single-molecule imaging, biochemistry and electrophysiology, we show that glycine and D-serine relative availability at rat hippocampal glutamatergic synapses regulate the trafficking and synaptic content of NMDAR subtypes. Acute manipulations of co-agonist levels, both ex vivo and in vitro, unveil that D-serine alter the membrane dynamics and content of GluN2B-NMDAR, but not GluN2A-NMDAR, at synapses through a process requiring PDZ binding scaffold partners. In addition, using FRET-based FLIM approach, we demonstrate that D-serine rapidly induces a conformational change of the GluN1 subunit intracellular C-terminus domain. Together our data fuels the view that the extracellular microenvironment regulates synaptic NMDAR signaling.DOI: http://dx.doi.org/10.7554/eLife.25492.001

show abstract

Section: Discussionmentioning

confidence: 99%

Co-agonists differentially tune GluN2B-NMDA receptor trafficking at hippocampal synapses

Ferreira

Papouin

Ladépêche

et al. 2017

eLife

Self Cite

View full text Add to dashboard Cite

show abstract

“…26,34 However, our current understanding of this process comes essentially from in vitro investigations based on primary cultures of neurons. Yet, key aspects of the regulation of NMDAR dynamics require intact brain preparations to be addressed, a challenge particularly obvious when considering the interplay between NMDAR and the extracellular environment.…”

Section: Discussionmentioning

confidence: 99%

Single nanoparticle tracking of N -methyl-d-aspartate receptors in cultured and intact brain tissue

et al. 2016

Self Cite

View full text Add to dashboard Cite

Abstract. Recent developments in single-molecule imaging have revealed many biological mechanisms, providing high spatial and temporal resolution maps of molecular events. In neurobiology, these techniques unveiled that plasma membrane neurotransmitter receptors and transporters laterally diffuse at the surface of cultured brain cells. The photostability of bright nanoprobes, such as quantum dots (QDs), has given access to neurotransmitter receptor tracking over long periods of time with a high spatial resolution. However, our knowledge has been restricted to cultured systems, i.e., neurons and organotypic slices, therefore lacking several aspects of the intact brain rheology and connectivity. Here, we used QDs to track single glutamatergic N-methyl-D-aspartate receptors (NMDAR) in acute brain slices. By delivering functionalized nanoparticles in vivo through intraventricular injections to rats expressing genetically engineered-tagged NMDAR, we successfully tracked the receptors in native brain tissue. Comparing NMDAR tracking to different classical brain preparations (acute brain slices, cultured organotypic brain slices, and cultured neurons) revealed that the surface diffusion properties shared several features and are also influenced by the nature of the extracellular environment. Together, we describe the experimental procedures to track plasma membrane NMDAR in dissociated and native brain tissue, paving the way for investigations aiming at characterizing receptor diffusion biophysics in intact tissue and exploring the physiopathological roles of receptor surface dynamics. © The Authors. Published by SPIE under a Creative Commons Attribution 3.0 Unported License. Distribution or reproduction of this work in whole or in part requires full attribution of the original publication, including its DOI.

show abstract

“…Indeed, studies by Srivastava et al (2006) were the first to demonstrate that treatment of cortical neurons with E2 resulted in transient removal of GluA1 from synapses; an effect that was accompanied by the synaptic insertion of the NMDA receptor subunit GluN1 suggesting formation of silent synapses. Conversely, increases in GluA1 surface expression have been observed in hippocampal neurons exposed to E2 (Zadran et al, 2009;Potier et al, 2015); an effect that has been attributed to the activation of ERβ as selective ERβ agonists mirror the E2-induced rise in surface GluA1 expression (Liu et al, 2008;Kramar et al, 2009). The subunit composition of hippocampal synaptic AMPA receptors also changes during the estrous cycle, indicating that fluctuations in endogenous estrogen levels also influence AMPA receptor trafficking in vivo (Tada et al, 2015).…”

Section: Regulation Of Glutamate Receptor Traffickingmentioning

confidence: 99%

“…Moreover, real time imaging studies have revealed rapid modulation of hippocampal NMDA receptor trafficking as acute exposure to E2 attenuates GluN2B surface expression, with no effect on surface GluN2A in hippocampal neurons (Potier et al, 2015). Although most studies have focussed on the role glutamate receptor trafficking in synaptic plasticity mechanisms during early postnatal development, activity-dependent alterations in the mobility of glutamate receptors also occurs in adult and aged hippocampus (Moga et al, 2006).…”

Section: Regulation Of Glutamate Receptor Traffickingmentioning

confidence: 99%

Emerging roles for the novel estrogen-sensing receptor GPER1 in the CNS

2017

View full text Add to dashboard Cite

Keywords: G protein coupled estrogen receptor, hippocampal synaptic function; receptor trafficking; learning and memory; neuroprotection; synaptic plasticity. Estrogens play a key role in regulating reproductive and neuroendocrine function by activating classical nuclear steroid receptors that act as ligand gated transcription factors.However evidence is growing that estrogens also promote rapid non-genomic responses via activation of membrane-associated estrogen receptors. The G protein-coupled estrogen receptor (GPER1; also known as GPR30) has been identified as one of the main estrogensensitive receptors responsible for the rapid non-genomic actions of estrogen. In recent years, our understanding of the CNS actions of GPER1s has significantly increased following the development of selective pharmacological tools and via the use of transgenic technologies to knockout GPER1 in mice. Here we review recent advances that have been made to uncover the role of GPER1s in the CNS.Introduction.

show abstract

Temporal Memory and Its Enhancement by Estradiol Requires Surface Dynamics of Hippocampal CA1 N-Methyl-D-Aspartate Receptors

Abstract: NMDAR surface trafficking and its modulation by the sex hormone E2 is a cellular mechanism critical for a major component of episodic memory, opening a new and noncanonical research avenue in the physiopathology of cognition.

Cited by 50 publications

References 64 publications

Co-agonists differentially tune GluN2B-NMDA receptor trafficking at hippocampal synapses

Co-agonists differentially tune GluN2B-NMDA receptor trafficking at hippocampal synapses

Single nanoparticle tracking of N -methyl-d-aspartate receptors in cultured and intact brain tissue

Emerging roles for the novel estrogen-sensing receptor GPER1 in the CNS

Contact Info

Product

Resources

About