Integrin regulation of cytoplasmic calcium in excitatory neurons depends upon glutamate receptors and release from intracellular stores

Lin, Ching Yi; Hilgenberg, Lutz G.W.; Smith, Martin A.; Lynch, Gary; Gall, Christine M.

doi:10.1016/j.mcn.2008.01.001

Cited by 24 publications

(20 citation statements)

References 77 publications

(113 reference statements)

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“…2(b)). Additionally, integrin interaction with synthetic RGD peptides was shown to induce LTP NMDA [56] and rapid Ca 2+ waves [57] and interfere with synaptic LTP AMPA up to 15 min post-LTP induction [58], similar to the effects of NNGH on E-S potentiation in the present study (Fig. 1).…”

Section: Discussionsupporting

confidence: 75%

Matrix Metalloprotease 3 Activity Supports Hippocampal EPSP-to-Spike Plasticity Following Patterned Neuronal Activity via the Regulation of NMDAR Function and Calcium Flux

et al. 2016

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Matrix metalloproteases (MMPs) comprise a family of endopeptidases that are involved in remodeling the extracellular matrix and play a critical role in learning and memory. At least 24 different MMP subtypes have been identified in the human brain, but less is known about the subtype-specific actions of MMP on neuronal plasticity. The long-term potentiation (LTP) of excitatory synaptic transmission and scaling of dendritic and somatic neuronal excitability are considered substrates of memory storage. We previously found that MMP-3 and MMP-2/9 may be differentially involved in shaping the induction and expression of excitatory postsynaptic potential (EPSP)-to-spike (E-S) potentiation in hippocampal brain slices. MMP-3 and MMP-2/9 proteolysis was previously shown to affect the integrity or mobility of synaptic N-methyl-d-aspartate receptors (NMDARs) in vitro. However, the functional outcome of such MMP-NMDAR interactions remains largely unknown. The present study investigated the role of these MMP subtypes in E-S plasticity and NMDAR function in mouse hippocampal acute brain slices. The temporal requirement for MMP-3/NMDAR activity in E-S potentiation within the CA1 field largely overlapped, and MMP-3 but not MMP-2/9 activity was crucial for the gain-of-function of NMDARs following LTP induction. Functional changes in E-S plasticity following MMP-3 inhibition largely correlated with the expression of cFos protein, a marker of activity-related gene transcription. Recombinant MMP-3 promoted a gain in NMDAR-mediated field potentials and somatodendritic Ca2+ waves. These results suggest that long-term hippocampal E-S potentiation requires transient MMP-3 activity that promotes NMDAR-mediated postsynaptic Ca2+ entry that is vital for the activation of downstream signaling cascades and gene transcription.

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Section: Discussionsupporting

confidence: 75%

Matrix Metalloprotease 3 Activity Supports Hippocampal EPSP-to-Spike Plasticity Following Patterned Neuronal Activity via the Regulation of NMDAR Function and Calcium Flux

et al. 2016

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“…ANOVA: p Ͻ 0.001 for all graphs; *p Ͻ 0.05 and **p Ͻ 0.01 vs con; Ն6 slices/group. pocampal neurons and other cell types (Lin et al, 2008), blocked integrin activation by TBS2 at 60 min post-TBS1, when infused starting 10 min after TBS1 (Fig. 2C).…”

Section: Synaptic Integrins Enter a Prolonged Refractory Period Follomentioning

confidence: 85%

Integrin Dynamics Produce a Delayed Stage of Long-Term Potentiation and Memory Consolidation

Babayan

Kramár

Barrett³

et al. 2012

J. Neurosci.

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Memory consolidation theory posits that newly acquired information passes through a series of stabilization steps before being firmly encoded. We report here that in rat and mouse, hippocampus cell adhesion receptors belonging to the ␤1-integrin family exhibit dynamic properties in adult synapses and that these contribute importantly to a previously unidentified stage of consolidation. Quantitative dual immunofluorescence microscopy showed that induction of long-term potentiation (LTP) by theta burst stimulation (TBS) activates ␤1 integrins, and integrin-signaling kinases, at spine synapses in adult hippocampal slices. Neutralizing antisera selective for ␤1 integrins blocked these effects. TBS-induced integrin activation was brief (Ͻ7 min) and followed by an ϳ45 min period during which the adhesion receptors did not respond to a second application of TBS. Brefeldin A, which blocks integrin trafficking to the plasma membrane, prevented the delayed recovery of integrin responses to TBS. ␤1 integrin-neutralizing antisera erased LTP when applied during, but not after, the return of integrin responsivity. Similarly, infusions of anti-␤1 into rostral mouse hippocampus blocked formation of long-term, object location memory when started 20 min after learning but not 40 min later. The finding that ␤1 integrin neutralization was effective in the same time window for slice and behavioral experiments strongly suggests that integrin recovery triggers a temporally discrete, previously undetected second stage of consolidation for both LTP and memory.

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“…They have functions in both the developing and mature nervous system, with roles in neurite outgrowth, synaptic plasticity, and peripheral nerve regeneration (Werner et al, 2000;Brakebusch and Fässler, 2005;Gardiner et al, 2005Gardiner et al, , 2007Webb et al, 2007;Lin et al, 2008;Plantman et al, 2008;McGeachie et al, 2011;Myers and Gomez, 2011). Integrins exist as heterodimers, composed of an ␣-and a ␤-subunit, with the specificity for their ligands being governed by the combined properties of both subunits.…”

Section: Introductionmentioning

confidence: 99%

ARF6 Directs Axon Transport and Traffic of Integrins and Regulates Axon Growth in Adult DRG Neurons

Eva¹,

Crisp²,

Marland³

et al. 2012

Journal of Neuroscience

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Integrins are involved in axon growth and regeneration. Manipulation of integrins is a route to promoting axon regeneration and understanding regeneration failure in the CNS. Expression of ␣9 integrin promotes axon regeneration, so we have investigated ␣9␤1 trafficking and transport in axons and at the growth cone. We have previously found that ␣9 and ␤1 integrins traffic via Rab11-positive recycling endosomes in peripheral axons and growth cones. However, transport via Rab11 is slow, while rapid transport occurs in vesicles lacking Rab11. We have further studied ␣9 and ␤1 integrin transport and traffic in adult rat dorsal root ganglion axons and PC12 cells. Integrins are in ARF6 vesicles during rapid axonal transport and during trafficking in the growth cone. We report that rapid axonal transport of these integrins and their trafficking at the cell surface is regulated by ARF6. ARF6 inactivation by expression of ACAP1 leads to increased recycling of ␤1 integrins to the neuronal surface and to increased anterograde axonal transport. ARF6 activation by expression of the neuronal guanine nucleotide exchange factors, ARNO or EFA6, increases retrograde integrin transport in axons and increases integrin internalization. ARF6 inactivation increases integrin-mediated outgrowth, while activation decreases it. The coordinated changes in integrin transport and recycling resulting from ARF6 activation or inactivation are the probable mechanism behind this regulation of axon growth. Our data suggest a novel mechanism of integrin traffic and transport in peripheral axons, regulated by the activation state of ARF6, and suggest that ARF6 might be targeted to enhance integrin-dependent axon regeneration after injury.

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Integrin regulation of cytoplasmic calcium in excitatory neurons depends upon glutamate receptors and release from intracellular stores

Cited by 24 publications

References 77 publications

Matrix Metalloprotease 3 Activity Supports Hippocampal EPSP-to-Spike Plasticity Following Patterned Neuronal Activity via the Regulation of NMDAR Function and Calcium Flux

Matrix Metalloprotease 3 Activity Supports Hippocampal EPSP-to-Spike Plasticity Following Patterned Neuronal Activity via the Regulation of NMDAR Function and Calcium Flux

Integrin Dynamics Produce a Delayed Stage of Long-Term Potentiation and Memory Consolidation

ARF6 Directs Axon Transport and Traffic of Integrins and Regulates Axon Growth in Adult DRG Neurons

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