Molecular basis for SH3 domain regulation of F-BAR–mediated membrane deformation

Rao, Yijian; Ma, Qingjun; Vahedi-Faridi, A.; Sundborger, Anna; Pechstein, Arndt; Puchkov, Dmytro; Luo, Lin; Shupliakov, Oleg; Saenger, Wolfram; Haucke, Volker

doi:10.1073/pnas.1003478107

Cited by 142 publications

(203 citation statements)

References 36 publications

(62 reference statements)

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“…The interaction between PACSIN1 and PICK1 was enhanced by the SH3-domain deletion (Fig. 4B, lane 4), consistent with two earlier studies describing an intramolecular interaction between the F-BAR and the SH3 domains that inhibits PACSIN1 function (18,28). Surprisingly, we also found that the GFP-PACSIN1-ΔF-BAR domain [variable region (VAR) + SH3] was able to bind myc-PICK1 robustly (Fig.…”

Section: Pacsin Interacts With Pick1supporting

confidence: 81%

“…Both PICK1 and PACSIN1 share some structural features in that they are subjected to intramolecular interactions, which allow them to exist in "open" or "closed" conformations, and they can interact with actin cytoskeleton regulators, the Arp2/3 complex, and N-WASP, respectively (18,28,41,42). Our domain-mapping analysis showed that the binding to PICK1 is mediated by the variable region in PACSIN1, leaving the SH3 domain available to bind to endocytic proteins and actin-reorganizing molecules.…”

Section: Discussionmentioning

confidence: 99%

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PICK1 interacts with PACSIN to regulate AMPA receptor internalization and cerebellar long-term depression

Anggono

Koç-Schmitz

Widagdo

et al. 2013

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

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The dynamic trafficking of AMPA receptors (AMPARs) into and out of synapses is crucial for synaptic transmission, plasticity, learning, and memory. The protein interacting with C-kinase 1 (PICK1) directly interacts with GluA2/3 subunits of the AMPARs. Although the role of PICK1 in regulating AMPAR trafficking and multiple forms of synaptic plasticity is known, the exact molecular mechanisms underlying this process remain unclear. Here, we report a unique interaction between PICK1 and all three members of the protein kinase C and casein kinase II substrate in neurons (PACSIN) family and show that they form a complex with AMPARs. Our results reveal that knockdown of the neuronal-specific protein, PACSIN1, leads to a significant reduction in AMPAR internalization following the activation of NMDA receptors in hippocampal neurons. The interaction between PICK1 and PACSIN1 is regulated by PACSIN1 phosphorylation within the variable region and is required for AMPAR endocytosis. Similarly, the binding of PICK1 to the ubiquitously expressed PACSIN2 is also regulated by the homologous phosphorylation sites within the PACSIN2-variable region. Genetic deletion of PACSIN2, which is highly expressed in Purkinje cells, eliminates cerebellar long-term depression. This deficit can be fully rescued by overexpressing wild-type PACSIN2, but not by a PACSIN2 phosphomimetic mutant, which does not bind PICK1 efficiently. Taken together, our data demonstrate that the interaction of PICK1 and PACSIN is required for the activity-dependent internalization of AMPARs and for the expression of long-term depression in the cerebellum.syndapin | receptor trafficking

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Section: Pacsin Interacts With Pick1supporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

PICK1 interacts with PACSIN to regulate AMPA receptor internalization and cerebellar long-term depression

Anggono

Koç-Schmitz

Widagdo

et al. 2013

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

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“…2), a mechanochemical enzyme recruited to endocytic sites by interaction with SH3 domain proteins 58,59 , including intersectin [60][61][62] , amphiphysin 63 , endophilin 64,65 and syndapin 66 , suggesting a tight interplay between BAR-SH3 protein-mediated membrane deformation (FIG. 2) and dynamin-catalyzed fission 58,67 . In agreement with this, dynamin 1 knockout mice exhibit a striking, activity-dependent accumulation of tubular coated endocytic intermediates 48 .…”

Section: Box 1 | Presynaptic Organization -Exocytic and Endocytic Zonesmentioning

confidence: 99%

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

2011

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Communication between nerve cells largely occurs at chemical synapses -specialized sites of cell-cell contact where electrical signals trigger the exocytic release of neurotransmitter, which in turn activates postsynaptic receptor channels. The efficacy with which such chemical signals are transmitted is crucial for the functioning of the nervous system. Modulation of neurotransmission enables nerve cells to respond to a vast range of stimulus patterns. Synaptic activity can also be tremendously diverse; from the fast synapses of the hippocampus, to slow neuropeptide-containing synapses. Indeed, some signalling pathways are active in the absence of stimulation, such as those involved in the processing of sensory information, which transmit tonically at high rates of up to 100 Hz or more 1,2 .Intriguing questions arise from these facts, including how high rates of neurotransmission can be maintained over long periods of time, and what limits the ability of a given synapse to release neurotransmitter during sustained periods of activity. Recent data indicate that in many synapses, exocytosis of neurotransmitter is coupled to endocytosis, and that synapses have evolved a specialized apparatus of scaffolding proteins to comply with these demands. Such scaffolds aid the temporal and spatial coupling of exocytosis and endocytosis, and are crucial for maintaining rapid neurotransmission during sustained activity 3 .Exocytosis of neurotransmitter is triggered by stimulusinduced calcium influx into the nerve terminal 4,5 and the subsequent fusion of synaptic vesicles with the presynaptic plasma membrane at specialized regions called active zones (BOX 1). Exocytosed synaptic vesicle membrane proteins and lipids in turn are recycled at the endocytic or periactive zone (BOX 1) that surrounds the release site, to restore functional synaptic vesicle pools for reuse and to ensure long-term functionality of the synapse 6-8 (FIG. 1). Depending on the type of synapse and the stimulation frequency, several modes of endocytosis with different time constants -for example, fast and slow endocytosisseem to operate 7,9,10 . Clathrin-mediated endocytosis arguably represents the main pathway of synaptic vesicle endocytosis 6,8,11 , although other modes -for example, fast kiss-and-run exocytosis and endocytosis -could operate in parallel.Although the machineries for exocytic membrane fusion 12,13 and for endocytic retrieval of synaptic vesicle membranes have been studied separately in some detail 6,14 , comparatively little is known about the coupling between exocytosis and endocytosis. Here we synthesize recent data from physiological, morphological and biochemical studies in several model systems into hypothetical models for scaffold-based mechanisms underlying exocytic-endocytic coupling.The synaptic vesicle cycle Synaptic vesicle pools. Some defining features of chemical synapses are the presence of one or several clusters of synaptic vesicles in the presynaptic nerve terminal, and ultrastructural specializations at the pre-and postsy...

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“…WASp itself is autoregulated by inhibitory interactions between its N terminus and its C-terminal Arp2/3-activating verprolin-central-acidic (VCA) domain, and can be activated by the combined effects of SH3 domain-containing binding partners, charged phospholipids, Rho family GTPases, and induced multimerization (6). For several BAR family members, including Syndapin, Amphiphysin, and Nervous Wreck (Nwk), C-terminal SH3 domains also bind directly to the BAR domain, inhibiting membrane association (7)(8)(9)(10)(11)(12)(13)(14)(15)(16).…”

mentioning

confidence: 99%

Coordinated autoinhibition of F-BAR domain membrane binding and WASp activation by Nervous Wreck

Stanishneva‐Konovalova

Kelley

Eskin

et al. 2016

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

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Membrane remodeling by Fes/Cip4 homology-Bin/Amphiphysin/Rvs167 (F-BAR) proteins is regulated by autoinhibitory interactions between their SRC homology 3 (SH3) and F-BAR domains. The structural basis of autoregulation, and whether it affects interactions of SH3 domains with other cellular ligands, remain unclear. Here we used single-particle electron microscopy to determine the structure of the F-BAR protein Nervous Wreck (Nwk) in both soluble and membrane-bound states. On membrane binding, Nwk SH3 domains do not completely dissociate from the F-BAR dimer, but instead shift from its concave surface to positions on either side of the dimer. Unexpectedly, along with controlling membrane binding, these autoregulatory interactions inhibit the ability of Nwk-SH3a to activate Wiskott–Aldrich syndrome protein (WASp)/actin related protein (Arp) 2/3-dependent actin filament assembly. In Drosophila neurons, Nwk autoregulation restricts SH3a domain-dependent synaptopod formation, synaptic growth, and actin organization. Our results define structural rearrangements in Nwk that control F-BAR–membrane interactions as well as SH3 domain activities, and suggest that these two functions are tightly coordinated in vitro and in vivo.

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Molecular basis for SH3 domain regulation of F-BAR–mediated membrane deformation

Cited by 142 publications

References 36 publications

PICK1 interacts with PACSIN to regulate AMPA receptor internalization and cerebellar long-term depression

PICK1 interacts with PACSIN to regulate AMPA receptor internalization and cerebellar long-term depression

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

Coordinated autoinhibition of F-BAR domain membrane binding and WASp activation by Nervous Wreck

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