Modulation of Presynaptic Calcium Transients by Metabotropic Glutamate Receptor Activation: A Differential Role in Acute Depression of Synaptic Transmission and Long-Term Depression

Faas, Guido C.; Adwanikar, Hita; Gereau, Robert W.; Saggau, Peter

doi:10.1523/jneurosci.22-16-06885.2002

Cited by 93 publications

(93 citation statements)

References 30 publications

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“…This form of mGluR LTD is known to require the activation of mGluR5 (Palmer et al, 1997;Fitzjohn et al, 1999;Faas et al, 2002). We therefore hypothesized that a loss of functional mGluR5 might underlie the profound reduction in mGluR LTD in the CA1 region.…”

Section: Loss Of Mglur5 Receptor Function Underlies Loss Of Mglur Ltdmentioning

confidence: 99%

“…Because PP LFS-induced, NMDAR-independent synaptic plasticity has been shown to require activation of the group I metabotropic glutamate receptor mGluR5 (Faas et al, 2002) (but see Volk et al, 2006), we examined whether LTD induced by brief application of the group I mGluR agonist ( R, S)-3,5-DHPG; 100 M, 5 min) is altered after status epilepticus. As described previously (Palmer et al, 1997;Oliet et al, 1997;Fitzjohn et al, 2001), brief application of DHPG caused an immediate depression of CA1 EPSP slope to 37 Ϯ 4% in control animals.…”

Section: Loss Of Mglur-induced Synaptic Depression After Status Epilementioning

confidence: 99%

“…During certain types of lowfrequency activity, activation of mGluRs by endogenously released glutamate also appears to result in mGluR-dependent, NMDAR-independent LTD with similar characteristics (Oliet et al, 1997;Kemp and Bashir, 1999;Huber et al, 2000). Its mechanism of expression is thought to involve a modification of the presynaptic release machinery downstream of presynaptic Ca 2ϩ influx (Fitzjohn et al, 2001;Faas et al, 2002;Zakharenko et al, 2002), in addition to postsynaptic mechanisms culminating in a reduction in synaptic AMPA receptors (Huber et al, 2000;Snyder et al, 2001;Xiao et al, 2001;Nosyreva and Huber, 2005). These results point to a coexistence of multiple forms of mechanistically distinct forms of LTD within the hippocampal CA1 region.…”

Section: Introductionmentioning

confidence: 99%

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Loss of Metabotropic Glutamate Receptor-Dependent Long-Term Depression via Downregulation of mGluR5 after Status Epilepticus

Kirschstein

Bauer²,

Müller³

et al. 2007

J. Neurosci.

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Section: Loss Of Mglur5 Receptor Function Underlies Loss Of Mglur Ltdmentioning

confidence: 99%

Section: Loss Of Mglur-induced Synaptic Depression After Status Epilementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Loss of Metabotropic Glutamate Receptor-Dependent Long-Term Depression via Downregulation of mGluR5 after Status Epilepticus

Kirschstein

Bauer²,

Müller³

et al. 2007

J. Neurosci.

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“…Indeed, evidence that active Rap1 enhances levels of active p38 MAPK, which in turn leads to the removal of synaptic AMPA receptors, resulting in occluding the induction of LTD, has been provided more recently in a study on cultured hippocampal slices (34). To date, the locus of expression of DHPG-LTD is highly controversial with evidence for both presynaptic (6,29,44,45) and postsynaptic changes (12,13). Here, we provide evidence that interventions that attenuated the DHPG-induced loss of postsynaptic surface AMPA receptors also prevented the expression of DHPG-LTD, supporting a postsynaptic locus for the induction of DHPG-LTD.…”

Section: P38 Mapk Mediates Dhpg-ltdmentioning

confidence: 99%

Rap1-induced p38 Mitogen-activated Protein Kinase Activation Facilitates AMPA Receptor Trafficking via the GDI·Rab5 Complex

Huang

You

et al. 2004

Journal of Biological Chemistry

166

198

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Recent evidence has emphasized the importance of p38 mitogen-activated protein kinase (MAPK) in the induction of metabotropic glutamate receptor (mGluR)-dependent long term depression (LTD) at hippocampal CA3-CA1 synapses. However, the cascade responsible of mGluR to activate p38 MAPK and the signaling pathway immediately downstream from it to induce synaptic depression is poorly understood. Here, we show that transient activation of group I mGluR with the selective agonist (S)-3,5-dihydroxyphenylglycine (DHPG) activates p38 MAPK through G protein ␤␥-subunit, small GTPase Rap1, and MAPK kinase 3/6 (MKK3/6), thus resulting in mGluR5-dependent LTD. Furthermore, our data clearly show that an accelerating AMPA receptor endocytosis by stimulating the formation of guanyl nucleotide dissociation inhibitor-Rab5 complex is a potential downstream processing of p38 MAPK activation to mediate DHPG-LTD. These results suggest an important role for Rap1-MKK3/6-p38 MAPK pathway in the induction of mGluR-dependent LTD by directly coupling to receptor trafficking machineries to facilitate the loss of synaptic AMPA receptors.Long term depression (LTD) 1 is a persistent activity-dependent decrease of synaptic efficacy that together with the converse process, long term potentiation, has been considered to be crucial for information storage in the brain (1, 2). In the hippocampus, LTD is divided into three categories: homosynaptic, heterosynaptic, and associative LTD (3). The bestcharacterized form of homosynaptic LTD is induced in the CA1 region of the hippocampus by prolonged low frequency synaptic stimulation via a NMDA receptor-dependent rise in postsynaptic [Ca 2ϩ ] i and the activation of serine/threonine protein phosphatases (4). Recent work has shown that mechanistically distinct type of LTD can be induced in the CA1 region by other types of synaptic stimulation or brief pharmacological treatments. For example, a prolonged period of paired-pulse stimulation or a direct application of the selective group I mGluR agonists, such as DHPG, can induce a robust mGluR-dependent form of LTD that is independent of NMDA receptor activation (5). In contrast to the mechanisms of NMDA receptor-dependent LTD, which are fairly well established, the mechanisms of induction and the site of expression of mGluR-dependent LTD are still a matter of some considerable debate. Current studies have reported that the induction of mGluR-dependent LTD does not require extracellular Ca 2ϩ (6), Ca 2ϩ release from intracellular stores (7), activation of Ca 2ϩ /calmodulin-dependent protein kinase II (8), protein kinase A or protein kinase C (7, 9), or serine/ threonine protein phosphatases (9). However, this form of LTD requires activation of G q -type G proteins (10), a local translation of dendritic mRNA (5, 11), a long-lasting loss of postsynaptic AMPA receptors (12, 13), and activation of protein tyrosine phosphatases (14). In addition, more recent studies suggest that p38 MAPK signaling also serves as a signal mediator in the induction of mGluR-depende...

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“…There is no agreement on the site of induction or maintenance of mGluR LTD, and conflicting results suggest both presynaptic (5,11,12) or postsynaptic (13,14) mechanisms of expression, although participation of the presynaptic side in the induction phase of mGluR LTD can be consistent with all of the above studies. Although this interpretation of the literature is congruent with our findings, it is not the aim and scope of this work to study the presynaptic versus postsynaptic mechanisms for mGluR LTD exhaustively or extensively but to focus on the role of m1 in this type of synaptic plasticity.…”

mentioning

confidence: 92%

Presynaptic m1 muscarinic receptors are necessary for mGluR long-term depression in the hippocampus

Kamsler

McHugh

Gerber

et al. 2010

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

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To investigate the role of M1 muscarininc acetylcholine receptors (m1 receptors) in metabotropic glutamate receptor (mGluR)-mediated long-term depression (LTD), we produced mouse lines in which deletion of the m1 gene is restricted to the forebrain (FB-m1KO) or hippocampal CA3 pyramidal neurons (CA3-m1KO). Stimulation in FB-m1KO hippocampal slices resulted in excitatory postsynaptic potentials and long-term synaptic plasticity (long-term potentiation and LTD) similar to controls. The mice were deficient in (S)-3,5-dihydroxyphenylglycine hydrate (DHPG)-induced mGluR LTD, which correlated with a presynaptic increase in the release of neurotransmitters. Protein kinase C (PKC) activity, which is downstream from both mGluRs and m1 receptors, was reduced in CA3 but not in CA1. The presynaptic requirement of m1 receptors was confirmed by the lack of DHPG-induced mGluR LTD in the CA1 of slices from CA3-m1KO mice. mGluR LTD was rescued by stimulating PKC activity pharmacologically in CA3-m1KO mice. These data confirm a role for PKC activation in presynaptic induction of mGluR LTD and distinguish between the roles of mGluRs and m1 receptors. M 1 muscarinic acetylcholine receptors (m1 receptors) and group I metabotropic glutamate receptors (mGluRs) are expressed in hippocampal pyramidal neurons, activate protein kinase C (PKC) via a "q" type G protein (Gq)-coupled cascade (1-3), and have been implicated in inducing and modulating plasticity in CA3-CA1 synapses. The nature of the interaction between these two overlapping signal pathways is unknown. Although ionotropic N-methyl-d-aspartate (NMDA) receptors have been most prominently implicated in the phenomena of long-term potentiation (LTP) and long-term depression (LTD), changes in synaptic efficacy can also be mediated by metabotropic-receptor-mediated processes. G-protein-coupled receptors (such as m1 receptors and mGluRs) can change synaptic efficacy when stimulated and can also act as neuromodulators by changing synaptic responses to other parallel stimuli (1).Stimulating mGluRs by perfusing the agonist (S)-3,5-dihydroxyphenylglycine hydrate (DHPG) causes a long-lasting decrease in synaptic efficacy (mGluR LTD) (4-6). Similarly, muscarinic agonists also produce transient or long-lasting depression in synaptic efficacy (6, 7). These muscarinic effects vary with the concentration of the agonists used and may be the result of the simultaneous activation of different kinds of muscarinic receptors at distinct synaptic locations (8). It is still not clear which cholinergic receptors mediate cholinergic LTD and whether they act presynaptically or postsynaptically. It is also not clear what the relationship is between mGluR LTD and cholinergic LTD. Recently, Volk et al. (6) have shown that mGluR LTD can be blocked by applying a muscarinic antagonist and that LTD produced by a muscarinic agonist occludes mGluR LTD. They concluded that mGluR LTD and muscarinic LTD are the same process and that mGluRs are required for LTD only when m1 muscarinic receptors are blocked.The mechani...

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Modulation of Presynaptic Calcium Transients by Metabotropic Glutamate Receptor Activation: A Differential Role in Acute Depression of Synaptic Transmission and Long-Term Depression

Cited by 93 publications

References 30 publications

Loss of Metabotropic Glutamate Receptor-Dependent Long-Term Depression via Downregulation of mGluR5 after Status Epilepticus

Loss of Metabotropic Glutamate Receptor-Dependent Long-Term Depression via Downregulation of mGluR5 after Status Epilepticus

Rap1-induced p38 Mitogen-activated Protein Kinase Activation Facilitates AMPA Receptor Trafficking via the GDI·Rab5 Complex

Presynaptic m1 muscarinic receptors are necessary for mGluR long-term depression in the hippocampus

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