Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9

Murase, Sachiko; Lantz, Crystal L.; Quinlan, Elizabeth

doi:10.7554/elife.27345

Cited by 73 publications

(124 citation statements)

References 92 publications

Supporting

Mentioning

113

Contrasting

Order By: Relevance

“…Of note, previously published work suggests that basal PNN levels are comparable between wild‐type and MMP‐9 null animals (Murase et al . ).…”

Section: Resultsmentioning

confidence: 97%

“…With respect to the potential to disrupt PV to pyramidal cell input, which would likely have a profound influence on widespread population activity, MMP‐9 has also been shown to diminish PNN integrity (Murase et al . ; Wen et al . ).…”

Section: Resultsmentioning

confidence: 99%

“…) and light reintroduction following dark exposure (Murase et al . ), we examined PNN levels in control and venlafaxine‐treated mice.…”

Section: Resultsmentioning

confidence: 99%

“…MMP‐9 has been shown to reduce PNN integrity in mice that experience light reintroduction after deprivation, and also in a mouse model of FXS (Murase et al . ; Wen et al . ).…”

Section: Resultsmentioning

confidence: 99%

“…For example, light reintroduction after dark exposure triggers MMP‐9‐dependent PNN degradation (Murase et al . ). In addition, seizure activity has been shown to increase MMP‐9 levels and PNN breakdown while pretreatment with a broad‐spectrum MMP inhibitor abrogates these effects (Pollock et al .…”

mentioning

confidence: 97%

See 4 more Smart Citations

Venlafaxine stimulates PNN proteolysis and MMP‐9‐dependent enhancement of gamma power; relevance to antidepressant efficacy

Alaiyed

Bozzelli

Caccavano

et al. 2019

Journal of Neurochemistry

View full text Add to dashboard Cite

Drugs that target monoaminergic transmission represent a first‐line treatment for major depression. Though a full understanding of the mechanisms that underlie antidepressant efficacy is lacking, evidence supports a role for enhanced excitatory transmission. This can occur through two non‐mutually exclusive mechanisms. The first involves increased function of excitatory neurons through relatively direct mechanisms such as enhanced dendritic arborization. Another mechanism involves reduced inhibitory function, which occurs with the rapid antidepressant ketamine. Consistent with this, GABAergic interneuron‐mediated cortical inhibition is linked to reduced gamma oscillatory power, a rhythm also diminished in depression. Remission of depressive symptoms correlates with restoration of gamma power. As a result of strong excitatory input, reliable GABA release, and fast firing, PV‐expressing neurons (PV neurons) represent critical pacemakers for synchronous oscillations. PV neurons also represent the predominant GABAergic population enveloped by perineuronal nets (PNNs), lattice‐like structures that localize glutamatergic input. Disruption of PNNs reduces PV excitability and enhances gamma activity. Studies suggest that monoamine reuptake inhibitors reduce integrity of the PNN. Mechanisms by which these inhibitors reduce PNN integrity, however, remain largely unexplored. A better understanding of these issues might encourage development of therapeutics that best up‐regulate PNN‐modulating proteases. We observe that the serotonin/norepinephrine reuptake inhibitor venlafaxine increases hippocampal matrix metalloproteinase (MMP)‐9 levels as determined by ELISA and concomitantly reduces PNN integrity in murine hippocampus as determined by analysis of sections following their staining with a fluorescent PNN‐binding lectin. Moreover, venlafaxine‐treated mice (30 mg/kg/day) show an increase in carbachol‐induced gamma power in ex vivo hippocampal slices as determined by local field potential recording and Matlab analyses. Studies with mice deficient in matrix metalloproteinase 9 (MMP‐9), a protease linked to PNN disruption in other settings, suggest that MMP‐9 contributes to venlafaxine‐enhanced gamma power. In conclusion, our results support the possibility that MMP‐9 activity contributes to antidepressant efficacy through effects on the PNN that may in turn enhance neuronal population dynamics involved in mood and/or memory. Cover Image for this issue: doi: .

show abstract

“…Of note, previously published work suggests that basal PNN levels are comparable between wild‐type and MMP‐9 null animals (Murase et al . ).…”

Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 99%

“…) and light reintroduction following dark exposure (Murase et al . ), we examined PNN levels in control and venlafaxine‐treated mice.…”

Section: Resultsmentioning

confidence: 99%

“…MMP‐9 has been shown to reduce PNN integrity in mice that experience light reintroduction after deprivation, and also in a mouse model of FXS (Murase et al . ; Wen et al . ).…”

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 97%

See 3 more Smart Citations

Venlafaxine stimulates PNN proteolysis and MMP‐9‐dependent enhancement of gamma power; relevance to antidepressant efficacy

Alaiyed

Bozzelli

Caccavano

et al. 2019

Journal of Neurochemistry

View full text Add to dashboard Cite

show abstract

Neuregulin directed molecular mechanisms of visual cortical plasticity

Grieco

Holmes

2018

J of Comparative Neurology

View full text Add to dashboard Cite

Experience-dependent critical period (CP) plasticity has been extensively studied in the visual cortex. Monocular deprivation during the CP affects ocular dominance, limits visual performance, and contributes to the pathological etiology of amblyopia. Neuregulin-1 (NRG1) signaling through its tyrosine kinase receptor ErbB4 is essential for the normal development of the nervous system and has been linked to neuropsychiatric disorders such as schizophrenia. We discovered recently that NRG1/ErbB4 signaling in PV neurons is critical for the initiation of CP visual cortical plasticity by controlling excitatory synaptic inputs onto PV neurons and thus PV-cell mediated cortical inhibition that occurs following visual deprivation. Building on this discovery, we review the existing literature of neuregulin signaling in developing and adult cortex and address the implication of NRG/ErbB4 signaling in visual cortical plasticity at the cellular and circuit levels. NRG-directed research may lead to therapeutic approaches to reactivate plasticity in the adult cortex.

show abstract

Neuregulin and ErbB expression is regulated by development and sensory experience in mouse visual cortex

Grieco

Wang

Mahapatra

et al. 2019

J of Comparative Neurology

View full text Add to dashboard Cite

Neuregulins (NRGs) are protein ligands that impact neural development and circuit function. NRGs signal through the ErbB receptor tyrosine kinase family. NRG1/ErbB4 signaling in parvalbumin-expressing (PV) inhibitory interneurons is critical for visual cortical plasticity. There are multiple types of NRGs and ErbBs that can potentially contribute to visual cortical plasticity at different developmental stages. Thus, it is important to understand the normal developmental expression profiles of NRGs and ErbBs in specific neuron types in the visual cortex, and to study whether and how their expression changes in PV inhibitory neurons and excitatory neurons track with sensory perturbation. Cell type-specific translating ribosome affinity purification and qPCR was used to compare mRNA expression of nrg1,2,3,4 and erbB1,2,3,4 in PV and excitatory neurons in mouse visual cortex. We show that the expression of nrg1 and nrg3 decreases in PV neurons at the critical period peak, postnatal day 28 (P28) after monocular deprivation and dark rearing, and in the adult cortex (at P104) after 2-week long dark exposure. In contrast, nrg1 expression by excitatory neurons is unchanged at P28 and P104 following sensory deprivation, whereas nrg3 expression by excitatory neurons shows changes depending on the age and the mode of sensory deprivation. ErbB4 expression in PV neurons remains consistently high and does not appear to change in response to sensory deprivation. These data provide new important details of cell type-specific NRG/ErbB expression in the visual cortex and support that NRG1/ErbB4 signaling is implicated in both critical period and adult visual cortical plasticity.

show abstract

Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9

Cited by 73 publications

References 92 publications

Venlafaxine stimulates PNN proteolysis and MMP‐9‐dependent enhancement of gamma power; relevance to antidepressant efficacy

Venlafaxine stimulates PNN proteolysis and MMP‐9‐dependent enhancement of gamma power; relevance to antidepressant efficacy

Neuregulin directed molecular mechanisms of visual cortical plasticity

Neuregulin and ErbB expression is regulated by development and sensory experience in mouse visual cortex

Contact Info

Product

Resources

About