Cited by 333Cellular transport and secretionNeuroscience and Neuropharmacology ResearchExtracellular vesicles in disease

UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans

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Speese, S., Petrie, M., Schuske, K., Ailion, M., Ann, K., Iwasaki, K., Jorgensen, E. M., Martin, T. F. J.·2007·Journal of Neuroscience

Abstract

Previous studies indicated that CAPS (calcium-dependent activator protein for secretion) functions as an essential component for the Ca2+-dependent exocytosis of dense-core vesicles in neuroendocrine cells. However, recent mouse knock-out studies suggested an alternative role in the vesicular uptake or storage of catecholamines. To genetically assess the functional role of CAPS, we characterized the sole Caenorhabditis elegans CAPS ortholog UNC-31 (uncoordinated family member) and determined its role in dense-core vesicle-mediated peptide secretion and in synaptic vesicle recycling. Novel assays for dense-core vesicle exocytosis were developed by expressing a prepro-atrial natriuretic factor-green fluorescent protein fusion protein in C. elegans. unc-31 mutants exhibited reduced peptide release in vivo and lacked evoked peptide release in cultured neurons. In contrast, cultured neurons from unc-31 mutants exhibited normal stimulated synaptic vesicle recycling measured by FM4-64 [N-(3-triethylammoniumpropyl)-4-(6-(4-diethylamino)phenyl)hexatrienyl)pyridinium dibromide] dye uptake. Conversely, UNC-13, which exhibits sequence homology to CAPS/UNC-31, was found to be essential for synaptic vesicle but not dense-core vesicle exocytosis. These findings indicate that CAPS/UNC-31 function is not restricted to catecholaminergic vesicles but is generally required for and specific to dense-core vesicle exocytosis. Our results suggest that CAPS/UNC-31 and UNC-13 serve parallel and dedicated roles in dense-core vesicle and synaptic vesicle exocytosis, respectively, in the C. elegans nervous system.

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Crossref · 10.1523/jneurosci.1466-07.2007

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  • rund-1 and unc-31 mutants have defects in egg-laying and defecation and enter the dauer diapause stage at high temperature.

    “rund-1 and unc-31 mutants also have defects in egg-laying and defecation, and enter the dauer diapause stage at high temperature”

    From Two Rab2 Interactors Regulate Dense-Core Vesicle Maturation (2014) · cites this paper as Speese et al., 2007

    The Discussion and Results (pages unavailable in our copy) report egg-laying and defecation defects in unc-31 mutants. They describe reduced recovery from the dauer state, not entry into dauer diapause at high temperature. Our copy does not address rund-1 mutants. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • CAPS is required for dense-core vesicle fusion and may also regulate synaptic vesicle exocytosis.

    “CAPS is required for DCV fusion”

    From Two Rab2 Interactors Regulate Dense-Core Vesicle Maturation (2014) · cites this paper as Speese et al., 2007

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Research works printed but not linked: 1

  1. Livingstone D (1991) Studies on the unc-31 gene of Caenorhabditis elegans. PhD thesis, University of Cambridge.

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Authors
Speese, S., Petrie, M., Schuske, K., Ailion, M., Ann, K., Iwasaki, K., Jorgensen, E. M., & Martin, T. F. J.
Affiliations
  • University of Utah (US)
  • University of Wisconsin–Madison (US)
  • Northwestern University (US)
Venue
Journal of Neuroscience
Published
2007-06-06
Volume
27
Issue
23
Pages
6150-6162
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2025681452
Cited by
333
References
74
Citations by year
2026: 18 · 2025: 26 · 2024: 35 · 2023: 19 · 2022: 22 · 2021: 24 · 2020: 15 · 2019: 10 · 2018: 17 · 2017: 13 · 2016: 12 · 2015: 16 · 2014: 18 · 2013: 14 · 2012: 11
FWCI
6.48
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Howard Hughes Medical Institute
  • U.S. Department of Agriculture
  • McKnight Foundation
  • National Institutes of Health
  • Cooperative State Research, Education, and Extension Service
  • National Institute of Mental Health (MH60997, R01MH060997)
  • National Institute of Diabetes and Digestive and Kidney Diseases (DK 40428, R01DK040428)
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
unc-31, CAPS, synaptic vesicle recycling, UNC-13, peptide secretion, atrial natriuretic peptide, Caenorhabditis elegans neurons, calcium-dependent exocytosis, neuroendocrine cells
MeSH terms
Amino Acid Sequence, Animals, Calcium-Binding Proteins, Carrier Proteins, Exocytosis, Molecular Sequence Data, Synaptic Vesicles, Caenorhabditis elegans, Secretory Vesicles, Caenorhabditis elegans Proteins

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