Dynein light chain regulates axonal trafficking and synaptic levels of Bassoon

Bassoon and the related protein Piccolo are core components of the presynaptic cytomatrix at the active zone of neurotransmitter release. They are transported on Golgi-derived membranous organelles, called Piccolo-Bassoon transport vesicles (PTVs), from the neuronal soma to distal axonal locations, where they participate in assembling new synapses. Despite their net anterograde transport, PTVs move in both directions within the axon. How PTVs are linked to retrograde motors and the functional significance of their bidirectional transport are unclear. In this study, we report the direct interaction of Bassoon with dynein light chains (DLCs) DLC1 and DLC2, which potentially link PTVs to dynein and myosin V motor complexes. We demonstrate that Bassoon functions as a cargo adapter for retrograde transport and that disruption of the Bassoon–DLC interactions leads to impaired trafficking of Bassoon in neurons and affects the distribution of Bassoon and Piccolo among synapses. These findings reveal a novel function for Bassoon in trafficking and synaptic delivery of active zone material.

• Publication year

  2009

• Venue

  Journal of Cell Biology

• Publication date

  2009-04-20

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1083/jcb.200807155PMID 19380881PMCID 2700376
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Exchange and Redistribution Dynamics of the Cytoskeleton of the Active Zone Molecule Bassoon

  2009cited by this paper
• Piccolo modulation of Synapsin1a dynamics regulates synaptic vesicle exocytosis

  2008influential reference
• Activity-Induced Synaptic Capture and Exocytosis of the Neuronal Serine Protease Neurotrypsin

  2008cited by this paper
• Dynein light chain LC8 is a dimerization hub essential in diverse protein networks.

  2008cited by this paper
• Syntabulin–Kinesin-1 Family Member 5B-Mediated Axonal Transport Contributes to Activity-Dependent Presynaptic Assembly

  2007influential reference
• Structural and thermodynamic characterization of a cytoplasmic dynein light chain–intermediate chain complex

  2007cited by this paper
• Ultrastructural localization of active zone and synaptic vesicle proteins in a preassembled multi-vesicle transport aggregate.

  2007influential reference
• Molecular organization and assembly of the presynaptic active zone of neurotransmitter release.

  2006cited by this paper
• Local Sharing as a Predominant Determinant of Synaptic Matrix Molecular Dynamics

  2006cited by this paper
• Assembly of Active Zone Precursor Vesicles

  2006cited by this paper
• Binding to Rab3A-interacting Molecule RIM Regulates the Presynaptic Recruitment of Munc13-1 and ubMunc13-2*

  2006cited by this paper
• Formation of Presynaptic Terminals at Predefined Sites along Axons

  2006cited by this paper
• A guided tour into subcellular colocalization analysis in light microscopy

  2006cited by this paper
• A guided tour into subcellular colocalization analysis in light microscopy

  2006cited by this paper
• Dazl can bind to dynein motor complex and may play a role in transport of specific mRNAs

  2006influential reference
• Neuronal cotransport of glycine receptor and the scaffold protein gephyrin

  2006cited by this paper
• A tctex1-Ca2+ channel complex for selective surface expression of Ca2+ channels in neurons

  2005cited by this paper
• Cytoplasmic dynein nomenclature

  2005cited by this paper
• Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments

  2005cited by this paper
• Molecular motors and mechanisms of directional transport in neurons

  2005cited by this paper
• Direct observation demonstrates that Liprin-alpha is required for trafficking of synaptic vesicles.

  2005cited by this paper
• Molecular dissection of the photoreceptor ribbon synapse

  2005cited by this paper
• Dynein: An ancient motor protein involved in multiple modes of transport.

  2004cited by this paper
• Dynein light chain 1, a p21-activated kinase 1-interacting substrate, promotes cancerous phenotypes.

  2004cited by this paper
• Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons

  2004cited by this paper
• Cellulose membrane supported peptide arrays for deciphering protein-protein interaction sites: The case of PIN, a protein with multiple natural partners

  2004cited by this paper
• Postsynaptic Density Assembly Is Fundamentally Different from Presynaptic Active Zone Assembly

  2004cited by this paper
• Bidirectional transport along microtubules.

  2004cited by this paper
• Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate

  2004influential reference
• Association of the Kinesin Motor KIF1A with the Multimodular Protein Liprin-α*

  2003cited by this paper
• The molecular motor toolbox for intracellular transport.

  2003influential reference
• The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons.

  2003cited by this paper
• Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles.

  2003influential reference
• Functional regions of the presynaptic cytomatrix protein bassoon: significance for synaptic targeting and cytomatrix anchoring.

  2003influential reference
• Coordination of opposite-polarity microtubule motors

  2002cited by this paper
• Gephyrin Interacts with Dynein Light Chains 1 and 2, Components of Motor Protein Complexes

  2002cited by this paper
• Cast: a novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13-1.

  2002influential reference
• Kinesin molecular motors: Transport pathways, receptors, and human disease

  2001cited by this paper
• Structural basis of diverse sequence-dependent target recognition by the 8 kDa dynein light chain.

  2001cited by this paper
• The 8-kDa Dynein Light Chain Binds to Its Targets via a Conserved (K/R)XTQT Motif*

  2001influential reference
• Assembling the Presynaptic Active Zone: A Characterization of an Active Zone Precursor Vesicle

  2001influential reference
• Bmf: A Proapoptotic BH3-Only Protein Regulated by Interaction with the Myosin V Actin Motor Complex, Activated by Anoikis

  2001cited by this paper
• Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: Comparison with Bassoon

  2001cited by this paper
• Assembling the presynaptic active zone: a characterization of an active one precursor vesicle.

  2001influential reference
• The molecular motor dynein is involved in targeting Swallow and bicoid RNA to the anterior pole of Drosophila oocytes

  2000influential reference
• Interaction of the Postsynaptic Density-95/Guanylate Kinase Domain-Associated Protein Complex with a Light Chain of Myosin-V and Dynein

  2000influential reference
• The light chain composition of chicken brain myosin-Va: calmodulin, myosin-II essential light chains, and 8-kDa dynein light chain/PIN.

  2000cited by this paper
• Characterization of the Signal That Directs Tom20 to the Mitochondrial Outer Membrane

  2000cited by this paper
• Piccolo, a presynaptic zinc finger protein structurally related to bassoon.

  2000cited by this paper
• Dynein-Mediated Cargo Transport in Vivo

  2000cited by this paper
• Temporal appearance of the presynaptic cytomatrix protein bassoon during synaptogenesis.

  2000influential reference
• Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment.

  2000cited by this paper
• Dynein-mediated cargo transport in vivo. A switch controls travel distance.

  2000cited by this paper
• Aczonin, a 550-Kd Putative Scaffolding Protein of Presynaptic Active Zones, Shares Homology Regions with Rim and Bassoon and Binds Profilin

  1999influential reference
• Quantitative fine-structural analysis of olfactory cortical synapses.

  1999cited by this paper
• Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport.

  1999cited by this paper
• Structure of the PIN/LC8 dimer with a bound peptide

  1999cited by this paper
• Bassoon, a Novel Zinc-finger CAG/Glutamine-repeat Protein Selectively Localized at the Active Zone of Presynaptic Nerve Terminals

  1998cited by this paper
• Kinesin Light Chains Are Essential for Axonal Transport in Drosophila

  1998cited by this paper
• Kinetic analysis of the interaction between the monoclonal antibody A33 and its colonic epithelial antigen by the use of an optical biosensor. A comparison of immobilisation strategies.

  1997cited by this paper
• PIN: An Associated Protein Inhibitor of Neuronal Nitric Oxide Synthase

  1996cited by this paper
• The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors.

  1995influential reference
• Differential phosphorylation in vivo of cytoplasmic dynein associated with anterogradely moving organelles

  1994cited by this paper
• Fast axonal transport of foreign synaptic vesicles in squid axoplasm

  1985cited by this paper
• Polarity of axoplasmic microtubules in the olfactory nerve of the frog.

  1981cited by this paper

• Cooperative multivalency converts disorder into rods, resolving a paradox in cellular architecture

  2026cites this paper
• Microtubule networks in zebrafish hair cells facilitate presynapse transport and fusion during development

  2025cites this paper
• An integrated single-nucleus and spatial transcriptomics atlas reveals the molecular landscape of the human hippocampus

  2025cites this paper
• Bassoon, Presynaptic Scaffolding Protein: Narrative Review in Health and Disease

  2025cites this paper
• Residual flexibility in the topologically constrained multivalent complex between the GKAP scaffold and LC8 hub proteins

  2025cites this paper
• Overabundant endocannabinoids in neurons are detrimental to cognitive function

  2024cites this paper
• An integrated single-nucleus and spatial transcriptomics atlas reveals the molecular landscape of the human hippocampus

  2024cites this paper
• Presynaptic perspective: Axonal transport defects in neurodevelopmental disorders

  2024cites this paper
• Linker Length Drives Heterogeneity of Multivalent Complexes of Hub Protein LC8 and Transcription Factor ASCIZ

  2023cites this paper
• Protein transport from pre- and postsynapse to the nucleus: Mechanisms and functional implications.

  2023cites this paper
• Variants in BSN gene associated with epilepsy with favourable outcome

  2022cites this paper
• Molecular mechanisms of synaptogenesis

  2022cites this paper
• Synaptic vesicle proteins are selectively delivered to axons in mammalian neurons

  2022cites this paper
• Bassoon controls synaptic vesicle release via regulation of presynaptic phosphorylation and cAMP

  2022cites this paper
• Aβ1-16 controls synaptic vesicle pools at excitatory synapses via cholinergic modulation of synapsin phosphorylation

  2021cites this paper
• Bassoon controls synaptic vesicle pools via regulation of presynaptic phosphorylation and cAMP homeostasis

  2021cites this paper
• Coordinated bi-directional trafficking of synaptic vesicle and active zone proteins in peripheral nerves.

  2021cites this paper
• Charting a New Frontier Integrating Mathematical Modeling in Complex Biological Systems from Molecules to Ecosystems.

  2021cites this paper
• Molecular composition of developing glutamatergic synapses

  2020cites this paper
• Epigenomic diversity of cortical projection neurons in the mouse brain

  2020cites this paper
• CtBP1-Mediated Membrane Fission Contributes to Effective Recycling of Synaptic Vesicles

  2020cites this paper
• ATM loss disrupts the autophagy-lysosomal pathway

  2020cites this paper
• A Presynaptic Perspective on Transport and Assembly Mechanisms for Synapse Formation.

  2020cites this paper
• Molecular Assembly and Structural Plasticity of Sensory Ribbon Synapses—A Presynaptic Perspective

  2020cites this paper
• An integrative multi-omics approach reveals new central nervous system pathway alterations in Alzheimer’s disease

  2020cites this paper
• Bassoon inhibits proteasome activity via interaction with PSMB4

  2020cites this paper
• The dynein light chain 8 (LC8) binds predominantly “in-register” to a multivalent intrinsically disordered partner

  2020cites this paper
• Study of a kinesin adaptor in axonal transport and synapse formation.

  2019cites this paper
• Systematic identification of recognition motifs for the hub protein LC8

  2019cites this paper
• Living in Promiscuity: The Multiple Partners of Alpha-Synuclein at the Synapse in Physiology and Pathology

  2019cites this paper
• Axonal transport proteins and depressive like behavior, following Chronic Unpredictable Mild Stress in male rat.

  2018cites this paper
• Ablation of the presynaptic organizer Bassoon in excitatory neurons retards dentate gyrus maturation and enhances learning performance

  2018cites this paper
• Multivalency regulates activity in an intrinsically disordered transcription factor

  2018influential citation
• Multivalency regulates activity in an intrinsically disordered transcription factor

  2018influential citation
• Regulation of dynein‐dynactin‐driven vesicular transport

  2017cites this paper
• Maintaining the active zone: Demand, supply and disposal of core active zone proteins.

  2017cites this paper
• Physiological Concentrations of Amyloid Beta Regulate Recycling of Synaptic Vesicles via Alpha7 Acetylcholine Receptor and CDK5/Calcineurin Signaling

  2017cites this paper
• Microtubule Motor Proteins and the Mechanisms of Synaptic Plasticity

  2017cites this paper
• Explorer Physiological Concentrations of Amyloid Beta Regulate Recycling of Synaptic Vesicles via Alpha 7 Acetylcholine Receptor and CDK 5 / Calcineurin Signaling

  2017cites this paper
• The Drosophila LC8 homolog cut up specifies the axonal transport of proteasomes

  2017influential citation
• Vertebrate Presynaptic Active Zone Assembly: a Role Accomplished by Diverse Molecular and Cellular Mechanisms

  2017cites this paper
• Role of Bassoon and Piccolo in Assembly and Molecular Organization of the Active Zone

  2016cites this paper
• Puzzling out presynaptic differentiation

  2016cites this paper
• Building a Terminal

  2016cites this paper
• The Anchored Flexibility Model in LC8 Motif Recognition: Insights from the Chica Complex.

  2016cites this paper
• From Axons to Synapses: Cryo-Electron Tomography of Neurons

  2016cites this paper
• [Motor Proteins of Microtubules and Mechanisms of Synaptic Plasticity].

  2016cites this paper
• Orientation and organization of the presynaptic active zone protein Bassoon: from the Golgi to the synapse

  2016cites this paper
• Active Zone Assembly

  2015cites this paper
• Polybivalency and disordered proteins in ordering macromolecular assemblies.

  2015cites this paper
• The dynein inhibitor Ciliobrevin D inhibits the bidirectional transport of organelles along sensory axons and impairs NGF‐mediated regulation of growth cones and axon branches

  2015cites this paper
• Multivalent IDP assemblies: Unique properties of LC8‐associated, IDP duplex scaffolds

  2015cites this paper
• A high affinity RIM-binding protein/Aplip1 interaction prevents the formation of ectopic axonal active zones

  2015cites this paper
• Examining Dynamic Aspects of Presynaptic Terminal Formation via Live Confocal Microscopy

  2015cites this paper
• Synaptic activity controls localization and function of CtBP1 via binding to Bassoon and Piccolo

  2015influential citation
• A PIK3C3–Ankyrin-B–Dynactin pathway promotes axonal growth and multiorganelle transport

  2014cites this paper
• The Pathophysiology of Axonal Transport in Alzheimer's Disease

  2014cites this paper
• The interplay between dynein, accessory proteins and the endocytic pathway

  2014cites this paper
• DYNLL2 dynein light chain binds to an extended linear motif of myosin 5a tail that has structural plasticity.

  2014cites this paper
• Structural studies on protein-protein interactions: Analysis of the regulation of the DYNLL/LC8 binding to Nek9 and characterization of the enzymes composing the arginine deiminase pathway in mycoplasma penetrans

  2014cites this paper
• The regulation of dynein function in membrane movement by NudEL

  2014cites this paper
• The Molecular Mechanisms Underlying Synaptic Transmission

  2014cites this paper
• Seminars in Cell & Developmental Biology

  2014cites this paper
• NMR Characterization of Self-Association Domains Promoted by Interactions with LC8 Hub Protein

  2014cites this paper
• Bassoon specifically controls presynaptic P/Q-type Ca(2+) channels via RIM-binding protein.

  2014cites this paper
• Dynamic mechanisms of neuroligin-dependent presynaptic terminal assembly in living cortical neurons

  2014cites this paper
• Polybivalency and Disordered Proteins in Ordering Macromolecular

  2014cites this paper
• Analyse du transport intracytoplasmique de la capside du virus de l’hépatite B : analyse des interactions entre les capsides du VHB et les chaînes du complexe de la dynéine

  2014cites this paper
• JCB_201407063 1..18

  2014cites this paper
• Nup159 Provide a Stable and Rigid Multiple Recognition Motifs in Nucleoporin

  2014cites this paper
• The stoichiometry of scaffold complexes in living neurons – DLC2 functions as a dimerization engine for GKAP

  2014cites this paper
• Functional analysis of candidate orthologues of Synapse-Detective-1 (SYD-1) in mice

  2013cites this paper
• Regulation of Presynaptic Anchoring of the Scaffold Protein Bassoon by Phosphorylation-Dependent Interaction with 14-3-3 Adaptor Proteins

  2013influential citation
• Studying synaptic efficiency by post-hoc immunolabelling

  2013cites this paper
• Axonal Translation of β-Catenin Regulates Synaptic Vesicle Dynamics

  2013cites this paper
• Dynein Interacts with the Neural Cell Adhesion Molecule (NCAM180) to Tether Dynamic Microtubules and Maintain Synaptic Density in Cortical Neurons*

  2013influential citation
• Viral interactions with microtubules: orchestrators of host cell biology?

  2013cites this paper
• The cytoplasmic dynein motor complex at microtubule plus-ends and in long range motility of early endosomes, microtubule plus-end anchorage and processivity of cytoplasmic dynein

  2013cites this paper
• Bioinformatic survey for new physiological substrates of Cyclin-dependent kinase 5.

  2013cites this paper
• Molecular organization and plasticity of the cytomatrix at the active zone.

  2012cites this paper
• Global Identification and Characterization of Both O-GlcNAcylation and Phosphorylation at the Murine Synapse*

  2012cites this paper
• Multiple Recognition Motifs in Nucleoporin Nup159 Provide a Stable and Rigid Nup159-Dyn2 Assembly*

  2012cites this paper
• GKAP–DLC2 interaction organizes the postsynaptic scaffold complex to enhance synaptic NMDA receptor activity

  2012cites this paper
• Cellular mechanisms for the biogenesis and transport of synaptic and dense-core vesicles.

  2012cites this paper
• Molecular motors in cargo trafficking and synapse assembly.

  2012cites this paper
• Structural Analysis of Dynein Intermediate and Light Chains

  2012cites this paper
• Consequences of the ‘Legs at odd angles’ mutation within the motor protein dynein and its possible implications in neurological disease

  2012cites this paper
• The versatile molecular complex component LC8 promotes several distinct steps of flagellar assembly

  2012cites this paper
• Formation of Golgi-Derived Active Zone Precursor Vesicles

  2012cites this paper
• ATM Substrate Chk2-interacting Zn2+ Finger (ASCIZ) Is a Bi-functional Transcriptional Activator and Feedback Sensor in the Regulation of Dynein Light Chain (DYNLL1) Expression*

  2011cites this paper
• Analysis of the adaptor proteins, gephyrin and GRIP1, in KIF5-driven neuronal transport in Mus musculus, (Linnaeus, 1758)

  2011cites this paper
• Cytoplasmic dynein.

  2011cites this paper
• The pleiotropic effects of LC8 on the anchoring protein in flagellar radial spoke complex

  2011cites this paper
• DYNLL/LC8: a light chain subunit of the dynein motor complex and beyond

  2011cites this paper
• Resonance Assignments and Secondary Structure Analysis of Dynein Light Chain 8 by Magic Angle Spinning NMR Spectroscopy.

  2011cites this paper
• Directed Evolution Reveals the Binding Motif Preference of the LC8/DYNLL Hub Protein and Predicts Large Numbers of Novel Binders in the Human Proteome

  2011cites this paper
• The p25 subunit of the dynactin complex is required for dynein–early endosome interaction

  2011cites this paper
• Absence of functional active zone protein Bassoon affects assembly and transport of ribbon precursors during early steps of photoreceptor synaptogenesis.

  2010influential citation
• Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis

  2010cites this paper
• Visual deprivation increases accumulation of dense core vesicles in developing optic tectal synapses in Xenopus laevis

  2010cites this paper