RIM-binding protein 2 regulates release probability by fine-tuning calcium channel localization at murine hippocampal synapses

The tight spatial coupling of synaptic vesicles and voltage-gated Ca2+ channels (Cavs) ensures efficient action potential-triggered neurotransmitter release from presynaptic active zones (AZs). Rab-interacting molecule-binding proteins (RIM-BPs) interact with Ca2+ channels and via RIM with other com...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 41; pp. 11615 - 11620
Main Authors Grauel, M. Katharina, Maglione, Marta, Reddy-Alla, Suneel, Willmes, Claudia G., Brockmann, Marisa M., Trimbuch, Thorsten, Rosenmund, Tanja, Pangalos, Maria, Vardar, Gülçin, Stumpf, Alexander, Walter, Alexander M., Rost, Benjamin R., Eickholt, Britta J., Haucke, Volker, Schmitz, Dietmar, Sigrist, Stephan J., Rosenmund, Christian
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 11.10.2016
Subjects
Action Potentials
Animals
Biological Sciences
Calcium
Calcium - metabolism
Calcium Channels - metabolism
Cells, Cultured
Electrophysiological Phenomena
Female
Gene Deletion
Gene Expression
Gene Targeting
Genetic Loci
Genotype & phenotype
Hippocampus - metabolism
Male
Mice
Mice, Knockout
Molecules
Neurons
Neurons - metabolism
Neurotransmitters
Phenotype
Protein Transport
Proteins
Synapses - metabolism
Synaptic Transmission - genetics
Synaptic Vesicles - metabolism
calcium channel coupling
RIM-BP2
active zone structure
release probability
short-term plasticity
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Abstract The tight spatial coupling of synaptic vesicles and voltage-gated Ca2+ channels (Cavs) ensures efficient action potential-triggered neurotransmitter release from presynaptic active zones (AZs). Rab-interacting molecule-binding proteins (RIM-BPs) interact with Ca2+ channels and via RIM with other components of the release machinery. Although human RIM-BPs have been implicated in autism spectrum disorders, little is known about the role of mammalian RIM-BPs in synaptic transmission. We investigated RIM-BP2–deficient murine hippocampal neurons in cultures and slices. Short-term facilitation is significantly enhanced in both model systems. Detailed analysis in culture revealed a reduction in initial release probability, which presumably underlies the increased short-term facilitation. Superresolution microscopy revealed an impairment in Cav2.1 clustering at AZs, which likely alters Ca2+ nanodomains at release sites and thereby affects release probability. Additional deletion of RIM-BP1 does not exacerbate the phenotype, indicating that RIM-BP2 is the dominating RIM-BP isoform at these synapses.
AbstractList The tight spatial coupling of synaptic vesicles and voltage-gated Ca channels (Ca s) ensures efficient action potential-triggered neurotransmitter release from presynaptic active zones (AZs). Rab-interacting molecule-binding proteins (RIM-BPs) interact with Ca channels and via RIM with other components of the release machinery. Although human RIM-BPs have been implicated in autism spectrum disorders, little is known about the role of mammalian RIM-BPs in synaptic transmission. We investigated RIM-BP2-deficient murine hippocampal neurons in cultures and slices. Short-term facilitation is significantly enhanced in both model systems. Detailed analysis in culture revealed a reduction in initial release probability, which presumably underlies the increased short-term facilitation. Superresolution microscopy revealed an impairment in Ca 2.1 clustering at AZs, which likely alters Ca nanodomains at release sites and thereby affects release probability. Additional deletion of RIM-BP1 does not exacerbate the phenotype, indicating that RIM-BP2 is the dominating RIM-BP isoform at these synapses.
Highly regulated and precise positioning of Ca 2+ channels at the active zone (AZ) controls Ca 2+ nanodomains at release sites. Their exact localization affects vesicular release probability (P VR ) and is important for proper synaptic transmission during repetitive stimulation. We provide a detailed analysis of synaptic transmission combined with superresolution imaging of the AZ organization in mouse hippocampal synapses lacking Rab-interacting molecule-binding protein 2 (RIM-BP2). By dual- and triple-channel time-gated stimulated emission depletion (gSTED) microscopy, we directly show that RIM-BP2 fine-tunes voltage-gated Ca 2+ channel 2.1 (Ca V 2.1) localization at the AZ. We reveal that RIM-BP2 likely regulates the Ca 2+ nanodomain by positioning Ca V 2.1 channels close to synaptic vesicle release sites. Loss of RIM-BP2 reduces P VR and alters short-term plasticity. The tight spatial coupling of synaptic vesicles and voltage-gated Ca 2+ channels (Ca V s) ensures efficient action potential-triggered neurotransmitter release from presynaptic active zones (AZs). Rab-interacting molecule-binding proteins (RIM-BPs) interact with Ca 2+ channels and via RIM with other components of the release machinery. Although human RIM-BPs have been implicated in autism spectrum disorders, little is known about the role of mammalian RIM-BPs in synaptic transmission. We investigated RIM-BP2–deficient murine hippocampal neurons in cultures and slices. Short-term facilitation is significantly enhanced in both model systems. Detailed analysis in culture revealed a reduction in initial release probability, which presumably underlies the increased short-term facilitation. Superresolution microscopy revealed an impairment in Ca V 2.1 clustering at AZs, which likely alters Ca 2+ nanodomains at release sites and thereby affects release probability. Additional deletion of RIM-BP1 does not exacerbate the phenotype, indicating that RIM-BP2 is the dominating RIM-BP isoform at these synapses.
The tight spatial coupling of synaptic vesicles and voltage-gated Ca2+ channels (Cavs) ensures efficient action potential-triggered neurotransmitter release from presynaptic active zones (AZs). Rab-interacting molecule-binding proteins (RIM-BPs) interact with Ca2+ channels and via RIM with other components of the release machinery. Although human RIM-BPs have been implicated in autism spectrum disorders, little is known about the role of mammalian RIM-BPs in synaptic transmission. We investigated RIM-BP2–deficient murine hippocampal neurons in cultures and slices. Short-term facilitation is significantly enhanced in both model systems. Detailed analysis in culture revealed a reduction in initial release probability, which presumably underlies the increased short-term facilitation. Superresolution microscopy revealed an impairment in Cav2.1 clustering at AZs, which likely alters Ca2+ nanodomains at release sites and thereby affects release probability. Additional deletion of RIM-BP1 does not exacerbate the phenotype, indicating that RIM-BP2 is the dominating RIM-BP isoform at these synapses.
Significance Highly regulated and precise positioning of Ca 2+ channels at the active zone (AZ) controls Ca 2+ nanodomains at release sites. Their exact localization affects vesicular release probability (P VR ) and is important for proper synaptic transmission during repetitive stimulation. We provide a detailed analysis of synaptic transmission combined with superresolution imaging of the AZ organization in mouse hippocampal synapses lacking Rab-interacting molecule-binding protein 2 (RIM-BP2). By dual- and triple-channel time-gated stimulated emission depletion (gSTED) microscopy, we directly show that RIM-BP2 fine-tunes voltage-gated Ca 2+ channel 2.1 (Ca V 2.1) localization at the AZ. We reveal that RIM-BP2 likely regulates the Ca 2+ nanodomain by positioning Ca V 2.1 channels close to synaptic vesicle release sites. Loss of RIM-BP2 reduces P VR and alters short-term plasticity. The tight spatial coupling of synaptic vesicles and voltage-gated Ca 2+ channels (Ca V s) ensures efficient action potential-triggered neurotransmitter release from presynaptic active zones (AZs). Rab-interacting molecule-binding proteins (RIM-BPs) interact with Ca 2+ channels and via RIM with other components of the release machinery. Although human RIM-BPs have been implicated in autism spectrum disorders, little is known about the role of mammalian RIM-BPs in synaptic transmission. We investigated RIM-BP2–deficient murine hippocampal neurons in cultures and slices. Short-term facilitation is significantly enhanced in both model systems. Detailed analysis in culture revealed a reduction in initial release probability, which presumably underlies the increased short-term facilitation. Superresolution microscopy revealed an impairment in Ca V 2.1 clustering at AZs, which likely alters Ca 2+ nanodomains at release sites and thereby affects release probability. Additional deletion of RIM-BP1 does not exacerbate the phenotype, indicating that RIM-BP2 is the dominating RIM-BP isoform at these synapses.
Author Rosenmund, Christian
Pangalos, Maria
Rost, Benjamin R.
Trimbuch, Thorsten
Rosenmund, Tanja
Brockmann, Marisa M.
Vardar, Gülçin
Maglione, Marta
Grauel, M. Katharina
Walter, Alexander M.
Schmitz, Dietmar
Reddy-Alla, Suneel
Willmes, Claudia G.
Eickholt, Britta J.
Sigrist, Stephan J.
Stumpf, Alexander
Haucke, Volker
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DocumentTitleAlternate RIM-BP2 sets release probability at mouse synapses
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Issue 41
Keywords calcium channel coupling
RIM-BP2
active zone structure
release probability
short-term plasticity
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Edited by Thomas C. Südhof, Stanford University School of Medicine, Stanford, CA, and approved August 15, 2016 (received for review March 31, 2016)
1M.K.G., M.M., and S.R.-A. contributed equally to this work.
Author contributions: M.K.G., M.M., S.R.-A., B.J.E., V.H., D.S., S.J.S., and C.R. designed research; M.K.G., M.M., S.R.-A., C.G.W., M.M.B., T.T., T.R., M.P., G.V., A.S., and B.R.R. performed research; A.M.W. contributed new reagents/analytic tools; M.K.G., M.M., S.R.-A., C.G.W., M.M.B., T.T., T.R., M.P., and B.R.R. analyzed data; A.M.W. provided data discussion; and M.K.G., M.M., S.R.-A., V.H., D.S., S.J.S., and C.R. wrote the paper.
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Snippet The tight spatial coupling of synaptic vesicles and voltage-gated Ca2+ channels (Cavs) ensures efficient action potential-triggered neurotransmitter release...
The tight spatial coupling of synaptic vesicles and voltage-gated Ca channels (Ca s) ensures efficient action potential-triggered neurotransmitter release from...
Significance Highly regulated and precise positioning of Ca 2+ channels at the active zone (AZ) controls Ca 2+ nanodomains at release sites. Their exact...
The tight spatial coupling of synaptic vesicles and voltage-gated Ca2+ channels (CaVs) ensures efficient action potential-triggered neurotransmitter release...
Highly regulated and precise positioning of Ca 2+ channels at the active zone (AZ) controls Ca 2+ nanodomains at release sites. Their exact localization...
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SourceType Open Access Repository
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StartPage 11615
SubjectTerms Action Potentials
Animals
Biological Sciences
Calcium
Calcium - metabolism
Calcium Channels - metabolism
Cells, Cultured
Electrophysiological Phenomena
Female
Gene Deletion
Gene Expression
Gene Targeting
Genetic Loci
Genotype & phenotype
Hippocampus - metabolism
Male
Mice
Mice, Knockout
Molecules
Neurons
Neurons - metabolism
Neurotransmitters
Phenotype
Protein Transport
Proteins
Synapses - metabolism
Synaptic Transmission - genetics
Synaptic Vesicles - metabolism
Title RIM-binding protein 2 regulates release probability by fine-tuning calcium channel localization at murine hippocampal synapses
URI https://www.jstor.org/stable/26472026
https://www.ncbi.nlm.nih.gov/pubmed/27671655
https://www.proquest.com/docview/1832955933
https://search.proquest.com/docview/1835416119
https://search.proquest.com/docview/1837340261
https://pubmed.ncbi.nlm.nih.gov/PMC5068320
Volume 113
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