Role of GluR1 in Activity-Dependent Motor System Development

Zhang, Lujia; Scheßl, J.; Werner, Markus; Bönnemann, Carsten G.; Xiong, Guoxiang; Mojsilovic-Petrovic, Jelena; Zhou, Wan; Cohen, Akiva S.; Seeburg, Peter H.; Misawa, Hidemi; Jayaram, Aditi; Personius, Kirkwood E.; Hollmann, Michael; Sprengel, Rolf; Kalb, Robert G.

doi:10.1523/jneurosci.0880-08.2008

Cited by 24 publications

(42 citation statements)

References 73 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Rat motoneurons strongly express the AMPAR subunit GluA1(Q)-flip, which controls dendritic complexity largely by altering the branching pattern rather than the dendritic length, and the calcium permeability of the subunit is important (Inglis et al, 2002;Jeong et al, 2006;Zhang et al, 2008). For example, motoneurons in mice lacking GluA1 or cultured rat motoneurons with a knockdown of GluA1 display a reduced dendritic complexity (Zhang et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

“…For example, motoneurons in mice lacking GluA1 or cultured rat motoneurons with a knockdown of GluA1 display a reduced dendritic complexity (Zhang et al, 2008). The action of GluA1 depends on normal network connectivity and seems non-cell-autonomous (Zhang et al, 2008). NMDARs contribute to motoneuron dendritic plasticity (Inglis et al, 1998) and overexpression of GluN3B promotes elongation, branching and the growth of filopodia .…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cell class-specific regulation of neocortical dendrite and spine growth by AMPA receptor splice and editing variants

et al. 2011

View full text Add to dashboard Cite

SUMMARYGlutamatergic transmission converging on calcium signaling plays a key role in dendritic differentiation. In early development, AMPA receptor (AMPAR) transcripts are extensively spliced and edited to generate subunits that differ in their biophysical properties. Whether these subunits have specific roles in the context of structural differentiation is unclear. We have investigated the role of nine GluA variants and revealed a correlation between the expression of flip variants and the period of major dendritic growth. In interneurons, only GluA1(Q)-flip increased dendritic length and branching. In pyramidal cells, GluA2(Q)-flop, GluA2(Q)-flip, GluA3(Q)-flip and calcium-impermeable GluA2(R)-flip promoted dendritic growth, suggesting that flip variants with slower desensitization kinetics are more important than receptors with elevated calcium permeability. Imaging revealed significantly higher calcium signals in pyramidal cells transfected with GluA2(R)-flip as compared with GluA2(R)-flop, suggesting a contribution of voltage-activated calcium channels. Indeed, dendritic growth induced by GluA2(R)-flip in pyramidal cells was prevented by blocking NMDA receptors (NMDARs) or voltage-gated calcium channels (VGCCs), suggesting that they act downstream of AMPARs. Intriguingly, the action of GluA1(Q)-flip in interneurons was also dependent on NMDARs and VGCCs. Cell class-specific effects were not observed for spine formation, as GluA2(Q)-flip and GluA2(Q)-flop increased spine density in pyramidal cells as well as in interneurons. The results suggest that AMPAR variants expressed early in development are important determinants for activity-dependent dendritic growth in a cell type-specific and cell compartment-specific manner.

show abstract

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Cell class-specific regulation of neocortical dendrite and spine growth by AMPA receptor splice and editing variants

et al. 2011

View full text Add to dashboard Cite

show abstract

“…Mixed spinal cord neuron cultures were prepared as described previously (Zhang et al, 2008). Briefly, neocortical astrocyte monolayers were established from the forebrain of Sprague Dawley rats (postnatal day 2).…”

Section: Methodsmentioning

confidence: 99%

“…Neonatal motor neurons display calcium-permeable AMPA receptors (Carriedo et al, 1996; Vandenberghe et al, 2000) – consistent with the observation that they express particularly high levels of GluA1 during this period (Jakowec et al, 1995a,b). Elimination of GluA1 leads to stunted motor neuron dendrite growth, deranged segmental spinal cord circuitry and sub-normal motor behavior(Zhang et al, 2008). Overexpression of GluA1 in mature motor neurons leads to remodeling of the dendritic tree with an increase in branch abundance (Inglis et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Structure–function analysis of SAP97, a modular scaffolding protein that drives dendrite growth

Zhang

Hsu

Mojsilovic-Petrovic

et al. 2015

Molecular and Cellular Neuroscience

Self Cite

View full text Add to dashboard Cite

Activation of AMPA receptors assembled with the GluA1 subunit can promote dendrite growth in a manner that depends on its direct binding partner, SAP97. SAP97 is a modular scaffolding protein that has at least seven recognizable protein-protein interaction domains. Several complementary approaches were employed to show that the dendrite branching promoting action of full length SAP97 depends on ligand(s) that bind to the PDZ3 domain. Ligand(s) to PDZ1, PDZ2 and I3 domains also contribute to dendrite growth. The ability of PDZ3 ligand(s) to promote dendrite growth depends on localization at the plasma membrane along with GluA1 and SAP97. These results suggest that the assembly of a multi-protein complex at or near synapses is vital for the translation of AMPA-R activity into dendrite growth.

show abstract

“…Mauthner neuron ͉ glutamate ͉ NMDA ͉ synapse ͉ development A MPA receptors (Rs) mediate fast excitatory synaptic transmission in the CNS, and have critical roles in neuronal formation and synaptic plasticity (1,2). They are heterotetrameric cation channels composed of glutamate receptor subunits 1-4 (GluR 1-4) with varying stoichiometries (3).…”

mentioning

confidence: 99%

PKCγ-induced trafficking of AMPA receptors in embryonic zebrafish depends on NSF and PICK1

Patten¹,

Ali

2009

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

View full text Add to dashboard Cite

The trafficking of AMPA receptors (Rs) to and from synaptic membranes is a key component underlying synaptic plasticity mechanisms such as long-term potentiation (LTP) and long-term depression (LTD), and is likely important for synaptic development in embryonic organisms. However, some of the key biochemical components required for receptor trafficking in embryos are still unknown. Here, we report that in embryonic zebrafish, the activation of PKC␥ by phorbol 12-myristate 13-acetate, strongly potentiates the amplitude of AMPAR-mediated miniature excitatory postsynaptic currents (AMPA-mEPSCs) via a N-ethylmaleimidesensitive fusion (NSF) and protein interacting with C-kinase-1 (PICK1)-dependent process. We found that the mEPSC potentiation is DAG-and Ca 2؉ -dependent, and occurs on application of active PKC␥. Peptides that prevent the association of NSF and PICK1 with the GluR2 subunit, and the actin-polymerization blocker, latrunculin B, prevented the increase in mEPSC amplitude. Also, application of tetanus toxin (TeTx), which cleaves SNARE proteins, also blocked the increase in mEPSC amplitude. Last, application of a 5 mM K ؉ medium led to an enhancement in mEPSC amplitude that was prevented by addition of the PKC␥ and NSF-blocking peptides, and the NMDA receptor blocker, 2-amino-5-phosphonovaleric acid (APV). Thus, activation of PKC␥ is necessary for the activitydependent trafficking of AMPARs in embryonic zebrafish. This process is NMDA and SNARE-dependent and requires AMPARs to associate with both NSF and PICK1. The present data further our understanding of AMPAR trafficking, and have important implications for synaptic development and synaptic plasticity.Mauthner neuron ͉ glutamate ͉ NMDA ͉ synapse ͉ development A MPA receptors (Rs) mediate fast excitatory synaptic transmission in the CNS, and have critical roles in neuronal formation and synaptic plasticity (1, 2). They are heterotetrameric cation channels composed of glutamate receptor subunits 1-4 (GluR 1-4) with varying stoichiometries (3). Synaptic transmission at central glutamatergic synapses is enhanced by several factors including modulation by enzymes such as protein kinase A (PKA), calcium-calmodulin kinase (CaMK), tyrosine kinase (TyK), and PKC (4-6). This enhancement in synaptic transmission occurs via modulation of postsynaptic AMPA receptor activity, but more recently has been shown to occur via trafficking of AMPARs to and from synaptic membranes (7-9).AMPAR phosphorylation by PKC is involved in various forms of synaptic plasticity (10-12). For example, PKC phosphorylation of ser880 on the GluR2 subunit is critical for the expression of long-term synaptic depression (LTD) in hippocampal CA1 and pyramidal neurons (7, 13). Also, PKM phosphorylation of GluR2 has been shown to maintain a stable enhancement of synaptic transmission by increasing the number of functional postsynaptic AMPARs through trafficking mechanisms (8, 9). Regulation of the dynamic movement of AMPARs into and out of synaptic membranes requires interactions between AMPAR subu...

show abstract

Role of GluR1 in Activity-Dependent Motor System Development

Cited by 24 publications

References 73 publications

Cell class-specific regulation of neocortical dendrite and spine growth by AMPA receptor splice and editing variants

Cell class-specific regulation of neocortical dendrite and spine growth by AMPA receptor splice and editing variants

Structure–function analysis of SAP97, a modular scaffolding protein that drives dendrite growth

PKCγ-induced trafficking of AMPA receptors in embryonic zebrafish depends on NSF and PICK1

Contact Info

Product

Resources

About