RIM Proteins Activate Vesicle Priming by Reversing Autoinhibitory Homodimerization of Munc13
Open accessAbstract
At a synapse, the presynaptic active zone mediates synaptic vesicle exocytosis. RIM proteins are active zone scaffolding molecules that--among others--mediate vesicle priming and directly or indirectly interact with most other essential presynaptic proteins. In particular, the Zn²+ finger domain of RIMs binds to the C₂A domain of the priming factor Munc13, which forms a homodimer in the absence of RIM but a heterodimer with it. Here, we show that RIMs mediate vesicle priming not by coupling Munc13 to other active zone proteins as thought but by directly activating Munc13. Specifically, we found that the isolated Zn²+ finger domain of RIMs autonomously promoted vesicle priming by binding to Munc13, thereby relieving Munc13 homodimerization. Strikingly, constitutively monomeric mutants of Munc13 rescued priming in RIM-deficient synapses, whereas wild-type Munc13 did not. Both mutant and wild-type Munc13, however, rescued priming in Munc13-deficient synapses. Thus, homodimerization of Munc13 inhibits its priming function, and RIMs activate priming by disrupting Munc13 homodimerization.
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RIM1/2 recruits Munc13-1s to active zones and interacts with other active zone components to enable exocytosis.
“RIM1/2 recruits Munc13-1s to AZs [72,73] and interacts with other AZ components to enable exocytosis [73–76].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [73]
The Introduction says RIMs interact with other active-zone proteins, and the Results show RIM–Munc13 binding relevant to vesicle priming. But the Discussion (Outlook; page unavailable) says the RIM Zn²⁺-finger acts downstream of Munc13 targeting to active zones and cannot physically tether Munc13 there. Thus, this paper does not support the claim that RIM recruits Munc13-1 to active zones. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThis difference might result from direct, fixed-length interaction between the PZD domain of RIM1/2 and the CaV2.1 C-terminus, which is difficult to modulate.
“This might result from direct, fixed-length interaction between the PZD domain of RIM1/2 and the CaV2.1 C-terminus [73,74], which is difficult to modulate.”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [73]
The Introduction says RIM proteins interact directly or indirectly with Ca²⁺ channels, and the Results identify PDZ among the C-terminal RIM domains involved in boosting local Ca²⁺ influx. Our copy does not establish a direct interaction between the RIM1/2 PDZ domain and the CaV2.1 C-terminus, or describe that interaction as fixed-length or difficult to modulate. (LLM, conf=0.78)
Experimental — accuracy not yet measuredThe function of RIMs in priming consists of activating Munc13 by disrupting Munc13 C2A homodimers.
“As a result, RIM-deficient synapses exhibit a severe impairment in vesicle priming that can be rescued not only by the N-terminal RIM fragment, but also by expression of mutant Munc13 that is constitutively monomeric, illustrating that the function of RIMs in priming consists of activating Munc13 (Deng et al., 2011).”
From The Presynaptic Active Zone (2012) · cites this paper as Deng et al., 2011
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- Authors
- Deng, L., Kaeser, P. S., Xu, W., & Südhof, T. C.
- Affiliations
- Stanford University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Südhof, Thomas C.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2011-01
- Volume
- 69
- Issue
- 2
- Pages
- 317-331
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3063404
- OpenAlex
- W2031522258
- Cited by
- 287
- References
- 57
- Citations by year
- 2026: 7 · 2025: 16 · 2024: 7 · 2023: 20 · 2022: 24 · 2021: 13 · 2020: 14 · 2019: 13 · 2018: 21 · 2017: 29 · 2016: 14 · 2015: 19 · 2014: 22 · 2013: 26 · 2012: 23
- FWCI
- 13.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 928 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (33564, DA029044)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- Munc13, vesicle priming, synaptic vesicle exocytosis, active zone, homodimerization, autoinhibition, C2A domain, heterodimerization, synapses
- MeSH terms
- Animals, Humans, Nerve Tissue Proteins, Neurons, Synaptic Vesicles, Zinc Fingers, Protein Structure, Tertiary, Presynaptic Terminals, Mice, Knockout, Patch-Clamp Techniques, GTP-Binding Proteins, Dimerization, rab3 GTP-Binding Proteins, Protein Structure, Quaternary, Mice, HEK293 Cells
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