Astrocytes close the mouse critical period for visual plasticity

Ribot, Jérôme; Breton, Rachel; Calvo, Charles‐Félix; Moulard, Julien; Ezan, Pascal; Zapata, Jonathan; Samama, Kevin; Moreau, Matthieu; Bemelmans, Alexis-Pierre; Sabatet, Valentin; Dingli, Florent; Loew, Damarys; Milleret, Chantal; Billuart, Pierre; Dallérac, Glenn; Rouach, Nathalie

doi:10.1126/science.abf5273

Cited by 63 publications

(59 citation statements)

References 50 publications

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“…The crucial role of MMP9 in the timing of the visual critical period was also recently observed in a study in which astrocytic connexin signaling decreased the expression of MMP9 through RhoA signaling. This process resulted in the stabilization of perineuronal nets and the closure of a critical period in visual cortex [64]. This observation underscores the potential of both astrocytic and neuronal MMP9 in controlling plasticity phenomena in the developing brain.…”

Section: Putative Targets Of Mmp9 Proteolytic Activity In the Perisynaptic Areasupporting

confidence: 52%

“…These effects are blocked by genetic ablation of MMP9, indicating that increased activity of this protease reduced constraints on structural and functional plasticity in the mature cortex [70,71]. In this regard, while additional studies are needed to elucidate the impact of MMP9 on ECM development fully, it is increasingly evident that MMP9 activity is intimately associated with ECM macroscopic integrity [64,72]. Interestingly, in most cases in which MMP9 was implicated in the plasticity of excitatory synapses, its action required integrin β1 in the hippocampus or cortex [11,33,72] or integrin β3 in nucleus accumbens [73].…”

Section: The Crucial Role Of Endogenous Mmp9 Inhibitionmentioning

confidence: 99%

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Extracellular Metalloproteinases in the Plasticity of Excitatory and Inhibitory Synapses

Wiera

Mozrzymas

2021

Cells

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Long-term synaptic plasticity is shaped by the controlled reorganization of the synaptic proteome. A key component of this process is local proteolysis performed by the family of extracellular matrix metalloproteinases (MMPs). In recent years, considerable progress was achieved in identifying extracellular proteases involved in neuroplasticity phenomena and their protein substrates. Perisynaptic metalloproteinases regulate plastic changes at synapses through the processing of extracellular and membrane proteins. MMP9 was found to play a crucial role in excitatory synapses by controlling the NMDA-dependent LTP component. In addition, MMP3 regulates the L-type calcium channel-dependent form of LTP as well as the plasticity of neuronal excitability. Both MMP9 and MMP3 were implicated in memory and learning. Moreover, altered expression or mutations of different MMPs are associated with learning deficits and psychiatric disorders, including schizophrenia, addiction, or stress response. Contrary to excitatory drive, the investigation into the role of extracellular proteolysis in inhibitory synapses is only just beginning. Herein, we review the principal mechanisms of MMP involvement in the plasticity of excitatory transmission and the recently discovered role of proteolysis in inhibitory synapses. We discuss how different matrix metalloproteinases shape dynamics and turnover of synaptic adhesome and signal transduction pathways in neurons. Finally, we discuss future challenges in exploring synapse- and plasticity-specific functions of different metalloproteinases.

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Section: Putative Targets Of Mmp9 Proteolytic Activity In the Perisynaptic Areasupporting

confidence: 52%

Section: The Crucial Role Of Endogenous Mmp9 Inhibitionmentioning

confidence: 99%

Extracellular Metalloproteinases in the Plasticity of Excitatory and Inhibitory Synapses

Wiera

Mozrzymas

2021

Cells

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“…Thus, MMP9 may indeed have a non-homeostatic role in open eye potentiation. Unexpectedly, astrocytic connexins were recently found to promote the maturation of inhibitory circuits and the extracellular matrix to close the critical period, and this process was suggested to occur through connexin mediated downregulation of MMP9 through the downregulation of RhoA activity (Ribot et al, 2021 ). It is unclear how astrocytic regulation of MMP9 and RhoA could influence heterosynaptic effects, or indeed relate to the role of astrocytic Ca 2+ activity in heterosynaptic plasticity (Letellier et al, 2016 ).…”

Section: Developmental Plasticity In Visual Cortex and Heterosynaptic Plasticitymentioning

confidence: 99%

“…Therefore, the abnormal open eye depression may in part arise through the restoration of sufficient glutamate clearance to reduce unintentional synaptic crosstalk. As is becoming clear, astrocytes influence ODP through far more than the release of TNFα (Stellwagen and Malenka, 2006 ; Kaneko et al, 2008 ), and there are potentially many contributions that still remain unexplored (Muller and Best, 1989 ; Singh et al, 2016 ; Ribot et al, 2021 ).…”

Section: Developmental Plasticity In Visual Cortex and Heterosynaptic Plasticitymentioning

confidence: 99%

Heterosynaptic Plasticity and the Experience-Dependent Refinement of Developing Neuronal Circuits

Jenks

Tsimring

et al. 2021

Front. Neural Circuits

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Neurons remodel the structure and strength of their synapses during critical periods of development in order to optimize both perception and cognition. Many of these developmental synaptic changes are thought to occur through synapse-specific homosynaptic forms of experience-dependent plasticity. However, homosynaptic plasticity can also induce or contribute to the plasticity of neighboring synapses through heterosynaptic interactions. Decades of research in vitro have uncovered many of the molecular mechanisms of heterosynaptic plasticity that mediate local compensation for homosynaptic plasticity, facilitation of further bouts of plasticity in nearby synapses, and cooperative induction of plasticity by neighboring synapses acting in concert. These discoveries greatly benefited from new tools and technologies that permitted single synapse imaging and manipulation of structure, function, and protein dynamics in living neurons. With the recent advent and application of similar tools for in vivo research, it is now feasible to explore how heterosynaptic plasticity contribute to critical periods and the development of neuronal circuits. In this review, we will first define the forms heterosynaptic plasticity can take and describe our current understanding of their molecular mechanisms. Then, we will outline how heterosynaptic plasticity may lead to meaningful refinement of neuronal responses and observations that suggest such mechanisms are indeed at work in vivo. Finally, we will use a well-studied model of cortical plasticity—ocular dominance plasticity during a critical period of visual cortex development—to highlight the molecular overlap between heterosynaptic and developmental forms of plasticity, and suggest potential avenues of future research.

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“…Using STED and SIM, researchers have shown that neuronal activity increased connexin 30 expression and localisation in perisynaptic processes in hippocampal astrocytes in mouse brain slices [ 111 ]. The same group recently showed that astrocytes close the critical period for visual plasticity via developmental upregulation of connexin 30 which in turn inhibits expression of the extracellular matrix degrading enzyme matrix metalloproteinase 9 [ 112 ].…”

Section: Super-resolution Imaging Of Tripartite Synapsesmentioning

confidence: 99%

Super-resolution imaging to reveal the nanostructure of tripartite synapses

Aleksejenko

Heller

2021

Neuronal Signaling

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Even though neurons are the main drivers of information processing in the brain and spinal cord, other cell types are important to mediate adequate flow of information. These include electrically-passive glial cells such as microglia and astrocytes, which recently emerged as active partners facilitating proper signal transduction. In disease, these cells undergo pathophysiological changes that propel disease progression and change synaptic connections and signal transmission. In the healthy brain, astrocytic processes contact pre- and postsynaptic structures. These processes can be nanoscopic, and therefore only electron microscopy has been able to reveal their structure and morphology. However, electron microscopy is not suitable in revealing dynamic changes, and it is labour- and time-intensive. The dawn of super-resolution microscopy, techniques that ‘break’ the diffraction limit of conventional light microscopy, over the last decades has enabled researchers to reveal the nanoscopic synaptic environment. In this review, we highlight and discuss recent advances in our understanding of the nano-world of the so-called tripartite synapses, the relationship between pre- and postsynapse as well as astrocytic processes. Overall, novel super-resolution microscopy methods are needed to fully illuminate the intimate relationship between glia and neuronal cells that underlies signal transduction in the brain and that might be affected in diseases such as Alzheimer’s disease and epilepsy.

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Astrocytes close the mouse critical period for visual plasticity

Cited by 63 publications

References 50 publications

Extracellular Metalloproteinases in the Plasticity of Excitatory and Inhibitory Synapses

Extracellular Metalloproteinases in the Plasticity of Excitatory and Inhibitory Synapses

Heterosynaptic Plasticity and the Experience-Dependent Refinement of Developing Neuronal Circuits

Super-resolution imaging to reveal the nanostructure of tripartite synapses

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