Telencephalin Slows Spine Maturation

Matsuno, Hitomi; Okabe, Susumu; Mishina, Masayoshi; Yanagida, Toshio; Mori, Kensaku; Yoshihara, Yoshihiro

doi:10.1523/jneurosci.2651-05.2006

Cited by 71 publications

(114 citation statements)

References 60 publications

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“…Ontogenic appearance of TLCN parallels the timing of dendritic outgrowth, spine formation, and synaptogenesis in early postnatal life, and the expression persists into adulthood (Mori et al, 1987;. Recently, we reported that TLCN facilitates the formation and maintenance of dendritic filopodia and thereby slows spine maturation in hippocampal neurons (Matsuno et al, 2006). This function of TLCN requires both its extracellular and cytoplasmic regions, suggesting the involvement of unknown ligands/counter-receptors and cytoskeleton-associated intracellular binding partners in TLCN-mediated morphogenesis of dendritic filopodia.…”

Section: Introductionmentioning

confidence: 89%

“…Primary antibodies used in this study were as follows: guinea pig anti-mouse TLCN/Fc (1:1000) (Matsuno et al, 2006); rabbit antiphospho-ERM (1:100; Cell Signaling Technology, Beverly, MA); mouse anti-␣-actinin and mouse anti-FLAG M2 (1:400 and 1:10000, respectively; Sigma, St. Louis, MO); and rat anti-green fluorescent protein (GFP) (1:1000; Nacalai Tesque, Kyoto, Japan). Cyanine 3 (Cy3)-and Cy5-conjugated secondary antibodies were purchased from Jackson ImmunoResearch (West Grove, PA).…”

Section: Methodsmentioning

confidence: 99%

“…N2a cells were maintained in DMEM supplemented with 10% fetal bovine serum (FBS) at 37°C in a humidified atmosphere containing 5% CO 2 . cDNA encoding a variant of yellow fluorescent protein (YFP) with fast and efficient maturation, Venus (Nagai et al, 2002), was fused to a membrane-anchoring palmitoylation signal of GAP-43 and subcloned into pCAGGS vector (Niwa et al, 1991) to generate pCAG-gapVenus (Matsuno et al, 2006). Phospholipase C ␦1 (PLC␦1)-pleckstrin homology (PH), tandem PH domain-containing protein 2 (TAPP2)-PH, and early endosomal antigen 1 (EEA1) FYVE domains (Balla and Varnai, 2002;Marshall et al, 2002) were fused to enhanced GFP (Takara, Kyoto, Japan) and subcloned into pCAGGS vector to produce pCAG-PLC␦1-PH-GFP, pCAG-TAPP2-PH-GFP, and pCAG-EEA1-3ϫ-FYVE-GFP.…”

Section: Methodsmentioning

confidence: 99%

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Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Furutani

Matsuno²,

Kawasaki³

et al. 2007

J. Neurosci.

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Dendritic filopodia are long, thin, actin-rich, and dynamic protrusions that are thought to play a critical role as a precursor of spines during neural development. We reported previously that a telencephalon-specific cell adhesion molecule, telencephalin (TLCN) [intercellular adhesion molecule-5 (ICAM-5)], is highly expressed in dendritic filopodia, facilitates the filopodia formation, and slows spine maturation. Here we demonstrate that TLCN cytoplasmic region binds ERM (ezrin/radixin/moesin) family proteins that link membrane proteins to actin cytoskeleton. In cultured hippocampal neurons, phosphorylated active forms of ERM proteins are colocalized with TLCN in dendritic filopodia, whereas ␣-actinin, another binding partner of TLCN, is colocalized with TLCN at surface membranes of soma and dendritic shafts. Expression of constitutively active ezrin induces dendritic filopodia formation, whereas small interference RNA-mediated knockdown of ERM proteins decreases filopodia density and accelerates spine maturation. These results indicate the important role of TLCN-ERM interaction in the formation of dendritic filopodia, which leads to subsequent synaptogenesis and establishment of functional neural circuitry in the developing brain.

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Section: Introductionmentioning

confidence: 89%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Furutani

Matsuno²,

Kawasaki³

et al. 2007

J. Neurosci.

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“…Fragile X syndrome, a common form of mental retardation, exhibits a higher than normal density of spines but more of them exhibit an immature morphology and their turnover is not affected by sensory experience (9,20). Conversely, the protein Telencephalin arrests the maturation of spines and its removal enhances several forms of learning (13,21,22).Although many molecules have been identified that affect synapse number, it is unclear how newly formed spines mature into synapses (13,23,24). On a cellular level, learning and memory are associated with long-term potentiation (LTP) and long-term depression (LTD) of neurotransmission.…”

mentioning

confidence: 99%

mentioning

confidence: 99%

O-GlcNAc transferase regulates excitatory synapse maturity

Lagerlöf

Hart

Huganir

2017

Proc. Natl. Acad. Sci. U.S.A.

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Experience-driven synaptic plasticity is believed to underlie adaptive behavior by rearranging the way neuronal circuits process information. We have previously discovered that O-GlcNAc transferase (OGT), an enzyme that modifies protein function by attaching β-N-acetylglucosamine (GlcNAc) to serine and threonine residues of intracellular proteins (O-GlcNAc), regulates food intake by modulating excitatory synaptic function in neurons in the hypothalamus. However, how OGT regulates excitatory synapse function is largely unknown. Here we demonstrate that OGT is enriched in the postsynaptic density of excitatory synapses. In the postsynaptic density, O-GlcNAcylation on multiple proteins increased upon neuronal stimulation. Knockout of the OGT gene decreased the synaptic expression of the AMPA receptor GluA2 and GluA3 subunits, but not the GluA1 subunit. The number of opposed excitatory presynaptic terminals was sharply reduced upon postsynaptic knockout of OGT. There were also fewer and less mature dendritic spines on OGT knockout neurons. These data identify OGT as a molecular mechanism that regulates synapse maturity.O-GlcNAc | OGT | excitatory synapses | AMPA receptors N euronal synapses, the cell-cell junctions over which neurons communicate, are formed and eliminated throughout life, and their turnover has for decades been associated with the way neuronal circuits adapt to environmental challenges to optimize behavior (1, 2). In both humans and animals, early development is characterized by massive generation of new synapses. About half of all synapses are then lost during adolescence (2, 3). Most mature excitatory synapses occur on dendritic protrusions called spines and essentially all spines contain an excitatory synapse (4-6). In vivo imaging of individual spines for days to months has shown that adult spines are largely stable but a small subpopulation remains plastic (3, 7) and spine turnover is increased by novel experience (5,(8)(9)(10). Whereas most new spines are thin and withdraw rapidly, some enlarge and form stable synaptic contacts (2,3,7,(11)(12)(13)(14). In fact, the stabilization of a subset of new spines correlates with behavioral performance in several different tasks in multiple animal species (13,(15)(16)(17). Rather than synapse formation or density, the selection of which spines are retained once formed has been suggested to match circuit architecture with behavior (18). Without affecting spine formation, deleting β-adducin, which regulates actin, perturbed the process by which nascent spines establish functional synapses and impaired long-term memory (19). Fragile X syndrome, a common form of mental retardation, exhibits a higher than normal density of spines but more of them exhibit an immature morphology and their turnover is not affected by sensory experience (9,20). Conversely, the protein Telencephalin arrests the maturation of spines and its removal enhances several forms of learning (13,21,22).Although many molecules have been identified that affect synapse number, it is unclear h...

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Perisomatic‐targeting granule cells in the mouse olfactory bulb

Naritsuka

Sakai

Hashikawa

et al. 2009

J of Comparative Neurology

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Inhibitory interneurons in the hippocampus and neocortex are differentiated into several morphological and functional subtypes that innervate distinct subcellular domains of principal neurons. In the olfactory bulb (OB), odor information is processed by local neuronal circuits that include the major inhibitory interneuron, granule cells (GCs). All GCs reported to date target their inhibitory output synapses mainly to dendrites of mitral cells (MCs) and tufted cells (TCs) in the external plexiform layer (EPL). Here we identified a novel type of GC that targets output synapses selectively to the perisomatic region of MCs. In the OB of adult transgenic mice expressing green fluorescent protein (GFP) under the control of nestin gene regulatory regions, we observed cells in the granule cell layer (GCL) that have GC-like morphology and strongly express GFP (referred to as type S cells). Type S cells expressed NeuN and GAD67, molecular markers for GCs. Intracellular labeling of type S cells revealed that their dendrites did not enter the EPL, but formed branches and spines within the GCL, internal plexiform layer, and mitral cell layer. Type S cells typically had huge spines at the ends of the apical dendrites. Some of the terminal spines attached to the perisomatic region of MCs and formed dendrosomatic reciprocal synapses with a presumed granule-to-mitral inhibitory synapse and a mitral-to-granule excitatory synapse. These findings indicate the morphological differentiation of GCs into dendritic-targeting and perisomatic-targeting subsets, and suggest the functional differentiation of the GC subsets in the processing of odor information in the OB.

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Telencephalin Slows Spine Maturation

Cited by 71 publications

References 60 publications

Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

Interaction between Telencephalin and ERM Family Proteins Mediates Dendritic Filopodia Formation

O-GlcNAc transferase regulates excitatory synapse maturity

Perisomatic‐targeting granule cells in the mouse olfactory bulb

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