Habituation of the head-shake response induces changes in brain matrix metalloproteinases-3 (MMP-3) and -9

Wright, John W.; Meighan, Starla E.; Murphy, Eric S.; Holtfreter, Kelby L.; Davis, Christopher J.; Olson, Mikel L.; Benoist, Caroline C.; Muhunthan, Kalyani; Harding, Joseph W.

doi:10.1016/j.bbr.2006.07.006

Cited by 23 publications

(24 citation statements)

References 65 publications

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“…n.s., not significant. study on MMP-9 KO slices (Wiera et al, 2013). Overall, our results indicate that LTP at mossy fiber-CA3 synapses strongly depends on the activity of MMP-9 but not MMP-3 (Fig.…”

Section: Mmp-3 Ko Abolishes Vdccltp But Not Nmdaltp In the Ca3-ca1 mentioning

confidence: 52%

“…Acute mouse hippocampal transverse slices (350 m) were prepared from C57BL/6 mice (postnatal day 60 -100) as described previously (Wiera et al, 2013). In some of the experiments, homozygous MMP-3 or MMP-9 KO mice were used.…”

Section: Methodsmentioning

confidence: 99%

“…Suppression of MMP-3 activity does not affect LTP in the mossy fiber-CA3 pathway MMP-9 deficiency impaired both early and late LTP in the mossy fiber-CA3 hippocampal pathway (Wiera et al, 2013), which is known for its predominant expression of presynaptic LTP (Castillo et al, 1997;Wiera and Mozrzymas, 2015). Considering that the lack of MMP-3 protease suppressed LTPinduced alterations in the PPR, suggesting presynaptic interference, we investigated the impact of MMP-3 inhibition on LTP in the mossy fiber-CA3 pathway, which precedes the CA3-CA1 projection in trisynaptic hippocampal connections.…”

Section: Mmp-3 Ko Abolishes Vdccltp But Not Nmdaltp In the Ca3-ca1 mentioning

confidence: 99%

“…To date, the role of gelatinases has been the most extensively studied. MMP-9 has been implicated in brain development/neurogenesis (Verslegers et al, 2013), the modification of dendritic spine morphology (Sidhu et al, 2014), synaptic plasticity (Nagy et al, 2006;Wiera et al, 2013), and memory formation (Peixoto et al, 2012;Smith et al, 2014). Although less intensively studied, MMP-3 has also been suggested to play a role in synaptic plasticity and learning (Olson et al, 2008;Conant et al, 2010), but the underlying mechanisms remain more obscure than for MMP-9.…”

Section: Introductionmentioning

confidence: 99%

“…Several substrates of proteolytic enzymes, such as membrane adhesion proteins and ECM molecules, have emerged as real or putative players in shaping plastic changes at the synaptic level and beyond (Tsien, 2013). Activity of tissue plasminogen activator (tPA), neuropsin, and matrix metalloproteinases (MMPs), has been implicated in synaptic plasticity and learning (Sonderegger and MatsumotoMiyai, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Mechanisms of NMDA Receptor- and Voltage-Gated L-Type Calcium Channel-Dependent Hippocampal LTP Critically Rely on Proteolysis That Is Mediated by Distinct Metalloproteinases

et al. 2017

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Long-term potentiation (LTP) is widely perceived as a memory substrate and in the hippocampal CA3-CA1 pathway, distinct forms of LTP depend on NMDA receptors (nmdaLTP) or L-type voltage-gated calcium channels (vdccLTP). LTP is also known to be effectively regulated by extracellular proteolysis that is mediated by various enzymes. Herein, we investigated whether in mice hippocampal slices these distinct forms of LTP are specifically regulated by different metalloproteinases (MMPs). We found that MMP-3 inhibition or knock-out impaired late-phase LTP in the CA3-CA1 pathway. Interestingly, late-phase LTP was also decreased by MMP-9 blockade. When both MMP-3 and MMP-9 were inhibited, both early-and late-phase LTP was impaired. Using immunoblotting, in situ zymography, and immunofluorescence, we found that LTP induction was associated with an increase in MMP-3 expression and activity in CA1 stratum radiatum. MMP-3 inhibition and knock-out prevented the induction of vdccLTP, with no effect on nmdaLTP. L-type channel-dependent LTP is known to be impaired by hyaluronic acid digestion. We found that slice treatment with hyaluronidase occluded the effect of MMP-3 blockade on LTP, further confirming a critical role for MMP-3inthisformofLTP.IncontrasttotheCA3-CA1pathway,LTPinthemossyfiber-CA3projectiondidnotdependonMMP-3,indicatingthe pathway specificity of the actions of MMPs. Overall, our study indicates that the activation of perisynaptic MMP-3 supports L-type channeldependent LTP in the CA1 region, whereas nmdaLTP depends solely on MMP-9.

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Section: Mmp-3 Ko Abolishes Vdccltp But Not Nmdaltp In the Ca3-ca1 mentioning

confidence: 52%

Section: Methodsmentioning

confidence: 99%

Section: Mmp-3 Ko Abolishes Vdccltp But Not Nmdaltp In the Ca3-ca1 mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Mechanisms of NMDA Receptor- and Voltage-Gated L-Type Calcium Channel-Dependent Hippocampal LTP Critically Rely on Proteolysis That Is Mediated by Distinct Metalloproteinases

et al. 2017

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Matrix metalloprotease activity shapes the magnitude of EPSPs and spike plasticity within the hippocampal CA3 network

Wójtowicz

Mozrzymas

2013

Hippocampus

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Matrix metalloproteases (MMP) play a pivotal role in long-term synaptic plasticity, learning, and memory. The roles of different MMP subtypes are emerging, but the proteolytic activity of certain MMPs was shown to support these processes through the structural and functional modification of hippocampal Schaeffer collateral and mossy fiber (MF) synapses. However, certain patterns of synaptic activity are additionally associated with non-synaptic changes, such as the scaling of neuronal excitability. However, the extent to which MMPs affect this process remains unknown. We determined whether MMP activity interferes with excitatory post-synaptic potential EPSP-to-spike (E-S) coupling under conditions of varying synaptic activity. We evoked short- and long-term synaptic plasticity at associational/commissural (A/C) synapses of CA3 pyramidal neurons and simultaneously recorded population spikes (PSs) and EPSPs in acute rat (P30-60) brain slices in the presence of various MMP inhibitors. We found that MMP inhibition significantly reduced E-S coupling and shortened the PS latency associated with 4× 100 Hz stimulation or paired burst activity of MF-CA3 and A/C synapses. Moreover, MMP inhibition interfered with the scaling of amplitude of measured signals during high-frequency trains, thus affecting the induction of long-term potentiation (LTP). The inhibition of L-type voltage-gated calcium channels with 20 µM nifedipine or GABA-A receptors with 1-30 µM picrotoxin did not occlude the effects of MMP inhibitors. However, MMP inhibition significantly reduced the LTP of NMDA receptor-mediated EPSPs. Finally, the analysis of LTP saturation with multiple single (1× 100 Hz) or packed (4× 100 Hz) trains indicated that MMPs support E-S coupling evoked by selected synaptic activity patterns and set the ceiling for tetanically evoked E-S LTP. In conclusion, the activity of MMPs, particularly MMP-3, regulated the magnitude of EPSPs and spike plasticity in the CA3 network and may affect information processing. Our data provide a novel link between MMP activity and neural excitability. Therefore, by limiting the number of firing neurons, MMP may functionally act beyond the synapse.

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Matrix Metalloproteinase 9 (MMP-9) in Learning and Memory

Knapska

Kaczmarek

2015

Novel Mechanisms of Memory

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Habituation of the head-shake response induces changes in brain matrix metalloproteinases-3 (MMP-3) and -9

Cited by 23 publications

References 65 publications

Mechanisms of NMDA Receptor- and Voltage-Gated L-Type Calcium Channel-Dependent Hippocampal LTP Critically Rely on Proteolysis That Is Mediated by Distinct Metalloproteinases

Mechanisms of NMDA Receptor- and Voltage-Gated L-Type Calcium Channel-Dependent Hippocampal LTP Critically Rely on Proteolysis That Is Mediated by Distinct Metalloproteinases

Matrix metalloprotease activity shapes the magnitude of EPSPs and spike plasticity within the hippocampal CA3 network

Matrix Metalloproteinase 9 (MMP-9) in Learning and Memory

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