TSPAN5 Enriched Microdomains Provide a Platform for Dendritic Spine Maturation through Neuroligin-1 Clustering

Moretto, Edoardo; Longatti, Anna; Murru, Luca; Chamma, Ingrid; Sessa, Alessandro; Zapata, Jonathan; Hosy, Eric; Sainlos, Matthieu; Saint-Pol, Julien; Rubinstein, Eric; Choquet, Daniel; Broccoli, Vania; Schiavo, Giampietro; Thoumine, Olivier; Passafaro, Maria

doi:10.1016/j.celrep.2019.09.051

Cited by 16 publications

(28 citation statements)

References 95 publications

(121 reference statements)

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“…Recent work from Moretto et al (2019) has demonstrated the significance of TSPAN5 in spine maturation. TSPAN5 is present during nearly every stage of spine maturation, beginning with filopodia, but seems to function primarily in the conversion of immature spines to mushroom spines.…”

Section: Tetraspanin 5 (Tspan5)mentioning

confidence: 99%

Palmitoylated Proteins in Dendritic Spine Remodeling

Albanesi

Baryłko

DeMartino

et al. 2020

Front. Synaptic Neurosci.

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Activity-responsive changes in the actin cytoskeleton are required for the biogenesis, motility, and remodeling of dendritic spines. These changes are governed by proteins that regulate the polymerization, depolymerization, bundling, and branching of actin filaments. Thus, processes that have been extensively characterized in the context of non-neuronal cell shape change and migration are also critical for learning and memory. In this review article, we highlight actin regulatory proteins that associate, at least transiently, with the dendritic plasma membrane. All of these proteins have been shown, either in directed studies or in high-throughput screens, to undergo palmitoylation, a potentially reversible, and stimulus-dependent cysteine modification. Palmitoylation increases the affinity of peripheral proteins for the membrane bilayer and contributes to their subcellular localization and recruitment to cholesterol-rich membrane microdomains.

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Section: Tetraspanin 5 (Tspan5)mentioning

confidence: 99%

Palmitoylated Proteins in Dendritic Spine Remodeling

Albanesi

Baryłko

DeMartino

et al. 2020

Front. Synaptic Neurosci.

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“…Tetraspanin nanodomains are predominantly composed of homotypic tetraspanin interactions, with heterotypic tetraspanintetraspanin interactions only occurring at the borders of nanodomains, as shown by superresolution microscopy [31]. Interactions with binding partners can occur both at the border of tetraspanin nanodomains [31] and within nanodomains [28,33] (Figure 2C).…”

Section: Tetraspanin Proteins Form Organizing Nanodomainsmentioning

confidence: 95%

“…Later, fluorescence super-resolution microscopy revealed that tetraspanin clusters have a diameter of~100 nm [29,32]; as such, we put forward the name 'tetraspanin nanodomains.' Partner proteins can be localized inside these domains and/or at the edge [31,33].…”

Section: Box 2 a Short History Of Tetraspaninsmentioning

confidence: 99%

Dynamic Plasma Membrane Organization: A Complex Symphony

Deventer

Arp

Spriel

2021

Trends in Cell Biology

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Membrane protein organization is essential for proper cellular functioning and the result of a dynamic exchange between protein monomers, nanoscale protein clusters, and microscale higher-order structures. This exchange is affected by both lipid bilayer intrinsic factors, such as lipid rafts and tetraspanins, and extrinsic factors, such as cortical actin and galectins. Because membrane organizers act jointly like instruments in a symphony, it is challenging to define the 'key' organizers. Here, we posit, for the first time, definitions of key intrinsic and extrinsic membrane organizers. Tetraspanin nanodomains are key organizers that are often overlooked. We discuss how different key organizers can collaborate, which is important to get a full grasp of plasma membrane biology. Open Questions in Plasma Membrane Biology HighlightsNovel definitions are postulated for membrane organizers intrinsic and extrinsic to the lipid bilayer.Membrane protein organization is the result of a dynamic exchange between protein monomers, nanoscale protein clusters, and microscale higher-order structures.Tetraspanins are key membrane organizers that should be considered in future plasma membrane studies.Membrane organizers act together in a dynamic manner like instruments playing a symphony.

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“…The cholesterol-binding protein TSPAN5, which belongs to the tetraspanin superfamily, is localized postsynaptically in pyramidal excitatory neurons, and is the master controller of spine maturation. Control is exerted by promoting the clustering of the postsynaptic molecule neuroligin-1 at the spine surface [ 197 ], which in turn recognizes and binds to presynaptic neurexins. TSPAN5 knockout mice have an extremely low number of spines, reinforcing the view that this tetraspanin plays a key role in excitatory synapse maturation.…”

Section: Nanodomain Cluster Organization Emerges As a Common Organizing Principle At Cns Synapsesmentioning

confidence: 99%

Nanoscale Sub-Compartmentalization of the Dendritic Spine Compartment

Vallés

Barrantes

2021

Biomolecules

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Compartmentalization of the membrane is essential for cells to perform highly specific tasks and spatially constrained biochemical functions in topographically defined areas. These membrane lateral heterogeneities range from nanoscopic dimensions, often involving only a few molecular constituents, to micron-sized mesoscopic domains resulting from the coalescence of nanodomains. Short-lived domains lasting for a few milliseconds coexist with more stable platforms lasting from minutes to days. This panoply of lateral domains subserves the great variety of demands of cell physiology, particularly high for those implicated in signaling. The dendritic spine, a subcellular structure of neurons at the receiving (postsynaptic) end of central nervous system excitatory synapses, exploits this compartmentalization principle. In its most frequent adult morphology, the mushroom-shaped spine harbors neurotransmitter receptors, enzymes, and scaffolding proteins tightly packed in a volume of a few femtoliters. In addition to constituting a mesoscopic lateral heterogeneity of the dendritic arborization, the dendritic spine postsynaptic membrane is further compartmentalized into spatially delimited nanodomains that execute separate functions in the synapse. This review discusses the functional relevance of compartmentalization and nanodomain organization in synaptic transmission and plasticity and exemplifies the importance of this parcelization in various neurotransmitter signaling systems operating at dendritic spines, using two fast ligand-gated ionotropic receptors, the nicotinic acetylcholine receptor and the glutamatergic receptor, and a second-messenger G-protein coupled receptor, the cannabinoid receptor, as paradigmatic examples.

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TSPAN5 Enriched Microdomains Provide a Platform for Dendritic Spine Maturation through Neuroligin-1 Clustering

Cited by 16 publications

References 95 publications

Palmitoylated Proteins in Dendritic Spine Remodeling

Palmitoylated Proteins in Dendritic Spine Remodeling

Dynamic Plasma Membrane Organization: A Complex Symphony

Nanoscale Sub-Compartmentalization of the Dendritic Spine Compartment

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