Two Rab2 Interactors Regulate Dense-Core Vesicle Maturation
Open accessAbstract
Peptide neuromodulators are released from a unique organelle: the dense-core vesicle. Dense-core vesicles are generated at the trans-Golgi and then sort cargo during maturation before being secreted. To identify proteins that act in this pathway, we performed a genetic screen in Caenorhabditis elegans for mutants defective in dense-core vesicle function. We identified two conserved Rab2-binding proteins: RUND-1, a RUN domain protein, and CCCP-1, a coiled-coil protein. RUND-1 and CCCP-1 colocalize with RAB-2 at the Golgi, and rab-2, rund-1, and cccp-1 mutants have similar defects in sorting soluble and transmembrane dense-core vesicle cargos. RUND-1 also interacts with the Rab2 GAP protein TBC-8 and the BAR domain protein RIC-19, a RAB-2 effector. In summary, a pathway of conserved proteins controls the maturation of dense-core vesicles at the trans-Golgi network.
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Claims the paper makes
16 of 20 cited sources checked · 10 supported · 0 flagged · accuracy not yet measured
- Background
Like rund-1 mutants, rab-2 mutants move little spontaneously on food but respond normally to UV stimulation.
“Like rund-1, rab-2 mutants exhibit little spontaneous movement on food, but move normally when stimulated by UV light (Edwards et al., 2009).”
Quote in the paperNot yet classified1 of 1 sources checked- cites Edwards et al., 2009 source
- Background
RAB-2 is a Golgi Rab in C. elegans that participates in dense-core vesicle maturation.
“RAB-2 is a Golgi Rab that functions in DCV maturation in C. elegans (Edwards et al., 2009; Sumakovic et al., 2009).”
Quote in the paperNot yet classified2 of 2 sources checked - Background
Rab2 was first localized to the ER-Golgi intermediate compartment and proposed to act in ER-to-Golgi anterograde transport, though it is now known to be distributed more broadly across the Golgi.
“Rab2 was originally localized to the ER-Golgi intermediate compartment (Chavrier et al., 1990) and was thought to function in ER to Golgi anterograde trafficking (Tisdale et al., 1992), but Rab2 is distributed more broadly across the Golgi and may have additional roles (Chun et al., 2008; Sumakovic et al., 2009).”
Quote in the paperNot yet classified2 of 3 sources checked- cites Chavrier et al., 1990 source
- cites Tisdale et al., 1992 source
- cites Chun et al., 2008 source
Chun et al. is cited for the final clause, alongside Sumakovic et al.; the earlier localization and anterograde-transport claims cite other papers. The Abstract and Discussion support an additional postendocytic role for UNC-108/Rab2, but our copy does not establish that Rab2 is distributed more broadly across the Golgi. No page numbers were supplied for these passages. (LLM, conf=0.86)
Experimental — accuracy not yet measured
- Background
Rab2 effectors include Golgi-associated coiled-coil proteins and the BAR domain protein ICA69/RIC-19.
“Known effectors of Rab2 include several coiled-coil proteins associated with the Golgi (Hayes et al., 2009; Short et al., 2001; Sinka et al., 2008) and the BAR domain protein ICA69/RIC-19 (Buffa et al., 2008; Sumakovic et al., 2009).”
Quote in the paperNot yet classified3 of 3 sources checked - Background
The RUN domain of TBC-8 also binds RIC-19.
“The TBC-8 RUN domain also binds RIC-19 (Hannemann et al., 2012).”
Quote in the paperNot yet classified1 of 1 sources checked- cites Hannemann et al., 2012 source
- Background
RIC-19 is recruited to the Golgi by GTP-bound RAB-2 and released into the cytoplasm by GDP-bound RAB-2.
“For example, RIC-19 is recruited to the Golgi by GTP-RAB-2 and dispersed into the cytoplasm by GDP-RAB-2 (Sumakovic et al., 2009).”
Quote in the paperNot yet classified1 of 1 sources checked- cites Sumakovic et al., 2009 sourceExperimental — accuracy not yet measured
- Background
rab-2 mutants show locomotion defects that resemble but are somewhat stronger than those of rund-1 mutants.
“Mutants lacking the rab-2 gene (also called unc-108) exhibit similar but somewhat stronger locomotion defects than rund-1 (Chun et al., 2008; Edwards et al., 2009; Sumakovic et al., 2009).”
Quote in the paperNot yet classified3 of 3 sources checked- cites Chun et al., 2008 source
The Results report that unc-108/Rab2 loss-of-function mutants have uncoordinated locomotion. They do not compare those defects with rund-1 mutants or establish that they are somewhat stronger; searches for “rund-1” and the claimed comparison found no such passage. (LLM, conf=0.88)
Experimental — accuracy not yet measured - cites Edwards et al., 2009 source
The Results (Fig. 1 B–C; page not provided) report sluggish locomotion in unc-108 (Rab2) mutants, supporting the locomotion-defect portion of the claim. Our copy does not compare these mutants with rund-1 mutants, so it does not support the claim that their defects are similar but somewhat stronger. (LLM, conf=0.87)
Experimental — accuracy not yet measured - cites Sumakovic et al., 2009 source
The Results section reports locomotory defects in unc-108/rab-2 mutants, including approximately 50% reduced locomotion for two alleles compared with wild type. Our copy does not compare those defects with rund-1 mutants, so it does not support the claim that they are similar but somewhat stronger. Page numbers were not supplied. (LLM, conf=0.88)
Experimental — accuracy not yet measured
- Background
RAB-2 associates with TBC-8, a candidate GAP for RAB-2, and with the BAR-domain protein RIC-19.
“RAB-2 binds TBC-8, a putative RAB-2 GAP, and RIC-19, a BAR domain protein (Hannemann et al., 2012; Sumakovic et al., 2009).”
Quote in the paperNot yet classified2 of 2 sources checked- cites Hannemann et al., 2012 source
The Results section ('TBC-8 is a putative RAB-2 GAP') reports an interaction between active RAB-2 and catalytically inactive TBC-8, but not wild-type TBC-8, so the unqualified binding claim overstates that result. The Results section on RIC-19 identifies it as a BAR-domain RAB-2 effector and reports its recruitment by active RAB-2. (LLM, conf=0.86)
Experimental — accuracy not yet measured - cites Sumakovic et al., 2009 source
The Results section ('RAB-2 cooperates with its effector RIC-19 during DCV maturation'; page unavailable) reports that RIC-19 coimmunoprecipitates with active RAB-2. The Discussion identifies RIC-19 as a BAR-domain protein. Our copy does not support the additional claim that RAB-2 binds TBC-8 or that TBC-8 is a putative RAB-2 GAP (searched: TBC-8, putative RAB-2 GAP). (LLM, conf=0.86)
Experimental — accuracy not yet measured
- Background
IDA-1 is the C. elegans counterpart of the dense-core vesicle transmembrane protein phogrin.
“IDA-1 is the C. elegans ortholog of the DCV transmembrane protein phogrin (Cai et al., 2004).”
Quote in the paperNot yet classified1 of 1 sources checked- cites Cai et al., 2004 source
- Finding
Combining rab-2, rund-1, and cccp-1 mutations did not worsen the locomotion phenotype beyond single mutants.
“Second, double mutants among rab-2, rund-1, and cccp-1 do not show enhanced locomotion defects (Figure 2E,F; Figure S7A, and data not shown).”
Quote in the paperNot yet classified - Finding
Expressing rund-1(+) under the neuronal rab-3 promoter rescues rund-1 locomotion, whereas intestinal expression using the vha-6 promoter does not.
“Expression of rund-1(+) under the neuronal specific rab-3 promoter rescued rund-1 mutant locomotion, but expression of rund-1 in the intestine using the vha-6 promoter did not rescue (Figure 2C and Figures S3G–I).”
Quote in the paperNot yet classified - Finding
In yeast two-hybrid assays, RUND-1 bound GTP-bound RAB-2 but not GDP-bound or wild-type RAB-2.
“RUND-1 interacted with GTP-bound RAB-2, but not with the GDP-bound RAB-2 or the wild-type RAB-2 (Figure 6A).”
Quote in the paperNot yet classified - Finding
A single gene, T19D7.4, fully rescues rund-1; it encodes a 549-residue protein containing two coiled-coil domains near its N-terminus and a RUN domain near its C-terminus.
“The rund-1 phenotype is fully rescued by the single gene T19D7.4. This open reading frame encodes a novel protein of 549 amino acids that has two coiled-coil domains in its N-terminal half and a RUN domain (RPIP8, UNC-14, and NESCA) near the C-terminus (Figures 1A and 1B).”
Quote in the paperNot yet classified - Finding
RUND-1 and CCCP-1 interacted only with RAB-2 among tested Rab, Rap, Ras, and Ral GTPases, identifying them as specific RAB-2 interactors.
“RUND-1 and CCCP-1 showed an interaction only with RAB-2 (Figure 6B; data not shown). Thus, RUND-1 and CCCP-1 are specific RAB-2 interactors.”
Quote in the paperNot yet classified - Finding
RUND-1 and CCCP-1 are found together with RAB-2 at the Golgi, and rab-2, rund-1, and cccp-1 mutants have comparable cargo-sorting defects for soluble and transmembrane dense-core vesicle components.
“RUND-1 and CCCP-1 colocalize with RAB-2 at the Golgi, and rab-2, rund-1 and cccp-1 mutants have similar defects in sorting soluble and transmembrane dense-core vesicle cargos.”
Quote in the paperNot yet classified - Finding
RUND-1 additionally binds TBC-8, a Rab2 GAP, and RIC-19, a BAR-domain RAB-2 effector.
“RUND-1 also interacts with the Rab2 GAP protein TBC-8 and the BAR domain protein RIC-19, a RAB-2 effector.”
Quote in the paperNot yet classified - Finding
After stimulation, rund-1 mutants move at about half the wild-type speed and become mostly inactive after 15 minutes; a single-copy wild-type rund-1(+) insertion fully rescues this.
“For rund-1 mutants, the speed after stimulation is about half that of the wild type (Figures 2B and 2C and Figure S3B–D) and the animals become mostly inactive after 15 minutes; the phenotype is fully rescued by a single-copy insertion of the wild-type rund-1(+) gene (Figure 2C and Figure S3E).”
Quote in the paperNot yet classified - Finding
rund-1 mutants lack defects in synaptic vesicle number or cargo localization and have normal-appearing dense-core vesicles at synapses, with a small increase in dense-core vesicle number.
“rund-1 does not exhibit defects in synaptic vesicle number (Figure 3) or localization of synaptic vesicle cargo (Figures S5A and S5B). Nor is synaptic function defective in rund-1 and cccp-1 mutants as determined by electrophysiological recordings (Figures S5C–G). Also, DCVs of a normal size and appearance are present at synapses in both the ventral and dorsal nerve cords of the rund-1(tm3622) mutant (Figure 3). In fact, there is actually a small increase in the number of DCVs.”
Quote in the paperNot yet classified - Finding
CCCP-1 bound RAB-2 in its GTP-bound and wild-type forms, but did not bind the GDP-bound form.
“CCCP-1 interacted with both the GTP-bound and wild-type RAB-2, but not with the GDP-bound RAB-2 (Figure 6A).”
Quote in the paperNot yet classified - Finding
RUND-1's RUN domain alone can mediate binding to RAB-2.
“We demonstrate that the RUN domain of RUND-1 is sufficient to interact with RAB-2.”
Quote in the paperNot yet classified - Finding
The paper concludes that a new pathway of conserved proteins controls dense-core vesicle maturation at the trans-Golgi network.
“In summary, a new pathway of conserved proteins controls the maturation of dense-core vesicles at the trans-Golgi network.”
Quote in the paperNot yet classified - Finding
A C. elegans genetic screen uncovered RUND-1, a RUN-domain-containing protein, and CCCP-1, a coiled-coil protein, as two conserved interactors of Rab2.
“We identified two conserved Rab2-binding proteins: RUND-1, a RUN domain protein, and CCCP-1, a coiled-coil protein.”
Quote in the paperNot yet classified - Background
RUN domain proteins were initially proposed as possible Rab and Rap effectors.
“RUN domain proteins were originally proposed to be potential Rab and Rap effectors (Callebaut et al., 2001).”
Quote in the paperNot yet classified0 of 1 sources checked- cites Callebaut et al., 2001 source
- Background
RUN domains occur in proteins that bind activated Rab and Rap GTPases and have been suggested to act as effectors for these GTPases.
“RUN domains have been found in several proteins that bind to activated small GTPases of the Rab and Rap families and have been proposed to be effectors of these small G proteins (Callebaut et al., 2001).”
Quote in the paperNot yet classified0 of 1 sources checked- cites Callebaut et al., 2001 source
- Background
The crystal structure of the Rab6 IP1 RUN domain bound to Rab6 indicates that a RUN domain can be sufficient for Rab binding in some cases.
“Moreover, the crystal structure of the RUN domain of Rab6 IP1 in complex with Rab6 provides evidence that the RUN domain is sufficient to mediate binding to Rabs in at least some cases (Recacha et al., 2009).”
Quote in the paperNot yet classified0 of 1 sources checked- cites Recacha et al., 2009 source
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Rab2a is a Golgi-resident GTPase governing intra-Golgi trafficking.
“Rab2a is known to be a Golgi-resident GTPase, governing intra-Golgi trafficking (Buffa et al., 2008; Ailion et al., 2014).”
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Self-citationTBC-8, a putative RAB-2 GAP, regulates dense core vesicle maturation in Caenorhabditis elegans
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Self-citationRab2 regulates presynaptic precursor vesicle biogenesis at the trans-Golgi
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Self-citationModulation of Gq-Rho Signaling by the ERK MAPK Pathway Controls Locomotion in Caenorhabditis elegans
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Self-citationSNX5 targets a monoamine transporter to the TGN for assembly into dense core vesicles by AP-3
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RAB 2 A Polymorphism impacts prefrontal morphology, functional connectivity, and working memory
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Fast genetic mapping using insertion-deletion polymorphisms in Caenorhabditis elegans
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TBC1D4 antagonizes RAB2A-mediated autophagic and endocytic pathways
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The exocyst complex controls multiple events in the pathway of regulated exocytosisPreprint
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Advances in the study of axon–associated vesicles
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The exocyst complex controls multiple events in the pathway of regulated exocytosis
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Self-citationRab10 regulates neuropeptide release by maintaining Ca2+ homeostasis and protein synthesisPreprint
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Self-citationRab10 regulates neuropeptide release by maintaining Ca2+ homeostasis and protein synthesis
Dong, J., Chen, M., van Weering, J. R. T., Domínguez, N., Li, K. W., SMIT, A. B., Toonen, R. F. G., & Verhage, M. (2025) · eLife · doi:10.1101/2024.01.02.573873 · Cited by 2 · see citing works
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Self-citationThe Functions of RAB GTPases at the Golgi Complex
Goud, B. (2026) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-3-032-16833-7_3
Rab10 regulates neuropeptide release by maintaining Ca2+ homeostasis and protein synthesisPreprint
Dong, J., Chen, M., van Weering, J. R. T., Li, K. W., Smit, A. B., Toonen, R. F. G., & Verhage, M. (2025) · eLife · doi:10.7554/elife.94930.2
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The ERK MAPK pathway modulates Gq-dependent locomotion in >Caenorhabditis elegans
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A Syd and RUFY dynein adaptor complex mediates axonal circulation of dense core vesicles
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Rab10 regulates neuropeptide release by maintaining Ca2+ homeostasis and protein synthesisPreprint
Dong, J., Chen, M., van Weering, J. R. T., Li, K. W., Smit, A. B., Toonen, R. F. G., & Verhage, M. (2024) · eLife · doi:10.7554/elife.94930.1
- Self-citation
- Authors
- Ailion, M., Hannemann, M., Dalton, S., Pappas, A., Watanabe, S., Hegermann, J., Liu, Q., Han, H.-F., Gu, M., Goulding, M. Q., Sasidharan, N., Schuske, K., Hullett, P., Eimer, S., & Jorgensen, E. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- European Neuroscience Institute Göttingen (DE)
- University of Washington (US)
- Corresponding author
- Ailion, Michael
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-04
- Volume
- 82
- Issue
- 1
- Pages
- 167-180
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3997996
- OpenAlex
- W1976286688
- Cited by
- 86
- References
- 93
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 16 · 2023: 11 · 2022: 3 · 2021: 9 · 2020: 3 · 2019: 3 · 2018: 8 · 2017: 12 · 2016: 9 · 2015: 3
- FWCI
- 3.99
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (P40OD010440)
- National Institute of Mental Health (R00MH082109)
- National Institute of Neurological Disorders and Stroke (R37NS034307, NS034307, R01NS034307)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- Rab2, trans-Golgi network, cargo sorting, Caenorhabditis elegans, Golgi apparatus, BAR domain proteins
- MeSH terms
- Analysis of Variance, Animals, Chromosome Mapping, Cloning, Molecular, Golgi Apparatus, Molecular Sequence Data, Mutation, Endosomes, Caenorhabditis elegans, rab2 GTP-Binding Protein, Protein Transport, Secretory Vesicles, Caenorhabditis elegans Proteins, Animals, Genetically Modified, Microscopy, Electron, Transmission, Green Fluorescent Proteins
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