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

The DOI matches its Crossref record; 74 of the 74 references it cites were found in a registry or an index.

UNC-31 (CAPS) Is Required for Dense-Core Vesicle But Not Synaptic Vesicle Exocytosis in Caenorhabditis elegans

Open access

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

DOI 10.1523/jneurosci.1466-07.2007PMC PMC6672138

Open this paper in CoChat — free account Open PDF

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.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.1466-07.2007

Cites

74 of 74 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

THE GENETICS OF CAENORHABDITIS ELEGANS
Brenner, S. (1974) · Genetics · doi:10.1093/genetics/77.1.71 · Cited by 15,220
The structure of the nervous system of the nematode Caenorhabditis elegans
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589
C. elegans : des neurones et des gènes
Gally, C., & Bessereau, J. (2003) · médecine/sciences · doi:10.1051/medsci/20031967725 · Cited by 3,260
Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.
Mello, C. C., Kramer, J. M., Stinchcomb, D. T., & Ambros, V. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb04966.x · Cited by 3,095
Membrane Fusion
Wilschut, J. (1990) · Cited by 2,407
Membrane Fusion
Jahn, R., Lang, T., & Südhof, T. C. (2003) · Cell · doi:10.1016/s0092-8674(03)00112-0 · Cited by 1,364
[Genetics of Caenorhabditis elegans].
Munakata, N. (1989) · PubMed · Cited by 877
Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles
Augustin, I., Rosenmund, C., Südhof, T. C., & Brose, N. (1999) · Nature · doi:10.1038/22768 · Cited by 787
Optical Analysis of Synaptic Vesicle Recycling at the Frog Neuromuscular Junction
Betz, W. J., & Bewick, G. S. (1992) · Science · doi:10.1126/science.1553547 · Cited by 763
Regulation of DAF-2 receptor signaling by human insulin and ins-1 , a member of the unusually large and diverse C. elegans insulin gene familyPreprint
Pierce, S. B., Costa, M. A., Wisotzkey, R. G., Devadhar, S., Homburger, S. A., Buchman, A. R., Ferguson, K. C., Heller, J., Platt, D., Pasquinelli, A. E., et al. (2001) · Genes & Development · doi:10.1101/gad.867301 · Cited by 651

Show all 74 references

Research works printed but not linked: 1

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

Sorted by citations

XBP-1 Is a Cell-Nonautonomous Regulator of Stress Resistance and Longevity
Taylor, R. C., & Dillin, A. G. (2013) · Cell · doi:10.1016/j.cell.2013.05.042 · Cited by 585
The Morphological and Molecular Nature of Synaptic Vesicle Priming at Presynaptic Active Zones
Imig, C., Min, S.-W., Krinner, S., Arancillo, M., Rosenmund, C., Südhof, T. C., Rhee, J., Brose, N., & Cooper, B. H. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.009 · Cited by 389
Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis
Suzuki, H., Thiele, T. R., Faumont, S., Ezcurra, M., Lockery, S. R., & Schafer, W. R. (2008) · Nature · doi:10.1038/nature06927 · Cited by 256
Neuroendocrine Coordination of Mitochondrial Stress Signaling and Proteostasis
Berendzen, K. M., Durieux, J., Shao, L.-W., Tian, Y., Kim, H.-E., Wolff, S., Liu, Y., & Dillin, A. G. (2016) · Cell · doi:10.1016/j.cell.2016.08.042 · Cited by 244
CAPS-1 and CAPS-2 Are Essential Synaptic Vesicle Priming Proteins
Jockusch, W. J., Speidel, D., Sigler, A., Sørensen, J. B., Varoqueaux, F., Rhee, J., & Brose, N. (2007) · Cell · doi:10.1016/j.cell.2007.11.002 · Cited by 209
Regulation of Organismal Proteostasis by Transcellular Chaperone Signaling
van Oosten‐Hawle, P., Porter, R. S., & Morimoto, R. I. (2013) · Cell · doi:10.1016/j.cell.2013.05.015 · Cited by 203
Degeneracy and Neuromodulation among Thermosensory Neurons Contribute to Robust Thermosensory Behaviors inCaenorhabditis elegans
Beverly, M., Anbil, S. R., & Sengupta, P. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1098-11.2011 · Cited by 190
Systemic stress signalling: understanding the cell non-autonomous control of proteostasis
Taylor, R. C., Berendzen, K. M., & Dillin, A. G. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3752 · Cited by 178
Neural signal propagation atlas of Caenorhabditis elegans
Randi, F., Sharma, A. K., Dvali, S., & Leifer, A. M. (2023) · Nature · doi:10.1038/s41586-023-06683-4 · Cited by 153
Four glial cells regulate ER stress resistance and longevity via neuropeptide signaling in C. elegans
Frakes, A. E., Metcalf, M. G., Tronnes, S. U., Bar‐Ziv, R., Durieux, J., Gildea, H. K., Kandahari, N., Monshietehadi, S., & Dillin, A. G. (2020) · Science · doi:10.1126/science.aaz6896 · Cited by 146
Neuronal circuitry regulates the response of Caenorhabditis elegans to misfolded proteins
Prahlad, V., & Morimoto, R. I. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106557108 · Cited by 145
Temperature, Oxygen, and Salt-Sensing Neurons in C. elegans Are Carbon Dioxide Sensors that Control Avoidance Behavior
Bretscher, A. J., Kodama, E., Busch, K. E., Murphy, R. J., Soltész, Z., Laurent, P., & de Bono, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.023 · Cited by 135
Defects in tRNA Modification Associated with Neurological and Developmental Dysfunctions in Caenorhabditis elegans Elongator Mutants
Chen, C., Tuck, S., & Byström, A. S. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000561 · Cited by 130
RNAi Interrogation of Dietary Modulation of Development, Metabolism, Behavior, and Aging in C. elegans
Xiao, R., Chun, L., Ronan, E. A., Friedman, D. I., Liu, J., & Xu, X. Z. S. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.04.024 · Cited by 120
Neuroendocrine signals modulate the innate immunity of Caenorhabditis elegans through insulin signaling
Kawli, T., & Tan, M. (2008) · Nature Immunology · doi:10.1038/ni.1672 · Cited by 127
Antifungal Innate Immunity in C. elegans: PKCδ Links G Protein Signaling and a Conserved p38 MAPK Cascade
Ziegler, K., Kurz, C. L., Cypowyj, S., Couillault, C., Pophillat, M., Pujol, N., & Ewbank, J. J. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.03.006 · Cited by 118
Synaptic scaffolding protein SYD-2 clusters and activates kinesin-3 UNC-104 in C. elegans
Wagner, O. I., Esposito, A., Köhler, B., Chen, C., Shen, C.-P., Wu, G., Butkevich, E., Mandalapu, S., Wenzel, D., Wouters, F. S., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902949106 · Cited by 117
CAPS and syntaxin dock dense core vesicles to the plasma membrane in neurons
Hammarlund, M., Watanabe, S., Schuske, K. R., & Jørgensen, E. M. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200708018 · Cited by 106
Self-citation
The chemical brain hypothesis for the origin of nervous systems
Jékely, G. (2021) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2019.0761 · Cited by 108
Two Rab2 Interactors Regulate Dense-Core Vesicle Maturation
Ailion, M., Hannemann, M., Dalton, S., Pappas, A., Watanabe, S., Hegermann, J., Liu, Q., Han, H.-F., Gu, M., Goulding, M. Q., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.017 · Cited by 86
Self-citation
A Self-Regulating Feed-Forward Circuit Controlling C. elegans Egg-Laying Behavior
Zhang, M., Chung, S., Fang-Yen, C. M., Craig, C., Kerr, R. A., Suzuki, H., Samuel, A. D. T., Mazur, E., & Schafer, W. R. (2008) · Current Biology · doi:10.1016/j.cub.2008.08.047 · Cited by 99
Hypoxia and the Hypoxic Response Pathway Protect against Pore-Forming Toxins in C. elegans
Bellier, A., Chen, C., Kao, C., Cinar, H. N., & Aroian, R. V. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000689 · Cited by 103
Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans
Leinwand, S. G., & Chalasani, S. H. (2013) · Nature Neuroscience · doi:10.1038/nn.3511 · Cited by 103
A Cold-Sensing Receptor Encoded by a Glutamate Receptor Gene
Gong, J., Liu, J., Ronan, E. A., He, F., Cai, W., Fatima, M., Zhang, W., Lee, H. K., Li, Z., Kim, G.-H., et al. (2019) · Cell · doi:10.1016/j.cell.2019.07.034 · Cited by 92
A TRPV Channel Modulates C. elegans Neurosecretion, Larval Starvation Survival, and Adult Lifespan
Lee, B. H., & Ashrafi, K. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000213 · Cited by 94
Profiling Synaptic Proteins Identifies Regulators of Insulin Secretion and Lifespan
Ch'ng, Q.-L., Sieburth, D., & Kaplan, J. M. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000283 · Cited by 93
Impaired dense core vesicle maturation in Caenorhabditis elegans mutants lacking Rab2
Edwards, S. L., Charlie, N. K., Richmond, J. E., Hegermann, J., Eimer, S., & Miller, K. G. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200902095 · Cited by 83
Temperature- and Touch-Sensitive Neurons Couple CNG and TRPV Channel Activities to Control Heat Avoidance in Caenorhabditis elegans
Liu, S., Schulze, E., & Baumeister, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032360 · Cited by 91
Olfactory specificity regulates lipid metabolism through neuroendocrine signaling in Caenorhabditis elegans
Mutlu, A. S., Gao, S. M., Zhang, H., & Wang, M. C. (2020) · Nature Communications · doi:10.1038/s41467-020-15296-8 · Cited by 90
A Neuropeptide-Mediated Stretch Response Links Muscle Contraction to Changes in Neurotransmitter Release
Hu, Z., Pym, E. C. G., Babu, K., Murray, A. V., & Kaplan, J. M. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.021 · Cited by 90
Hypoxia and the HIF-1 transcriptional pathway reorganize a neuronal circuit for oxygen-dependent behavior in Caenorhabditis elegans
Chang, A. J., & Bargmann, C. I. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802164105 · Cited by 90
PKA Activation Bypasses the Requirement for UNC-31 in the Docking of Dense Core Vesicles from C. elegans Neurons
Zhou, K.-M., Dong, Y., Ge, Q., Zhu, D. Y., Zhou, W., Lin, X., Liang, T., Wu, Z., & Xu, T. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.015 · Cited by 88
Neuropeptide Secreted from a Pacemaker Activates Neurons to Control a Rhythmic Behavior
Wang, H., Girskis, K. M., Janssen, T., Chan, J., Dasgupta, K., Knowles, J. A., Schoofs, L., & Sieburth, D. (2013) · Current Biology · doi:10.1016/j.cub.2013.03.049 · Cited by 87
Behavioral States
Flavell, S. W., Raizen, D. M., & You, Y. (2020) · Genetics · doi:10.1534/genetics.120.303539 · Cited by 86
Neurodegeneration in C. elegans models of ALS requires TIR-1/Sarm1 immune pathway activation in neurons
Vérièpe, J., Fossouo, L., & Parker, J. A. (2015) · Nature Communications · doi:10.1038/ncomms8319 · Cited by 86
Cell-cycle quiescence maintains Caenorhabditis elegans germline stem cells independent of GLP-1/Notch
Seidel, H. S., & Kimble, J. E. (2015) · eLife · doi:10.7554/elife.10832 · Cited by 84
CAPS Facilitates Filling of the Rapidly Releasable Pool of Large Dense-Core Vesicles
Liu, Y., Schirra, C., Stevens, D. R., Matti, U., Speidel, D., Hof, D., Bruns, D., Brose, N., & Rettig, J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5672-07.2008 · Cited by 87
Context-dependent reversal of odorant preference is driven by inversion of the response in a single sensory neuron type
Khan, M., Hartmann, A. H., O’Donnell, M. P., Piccione, M., Pandey, A., Chao, P.-H., Dwyer, N. D., Bargmann, C. I., & Sengupta, P. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001677 · Cited by 89
Estradiol Facilitates the Release of Neuropeptide Y to Suppress Hippocampus-Dependent Seizures
Ledoux, V. A., Smejkalová, T., May, R. M., Cooke, B. M., & Woolley, C. S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4688-08.2009 · Cited by 85
CAPS and Munc13: CATCHRs that SNARE Vesicles
James, D. J., & Martin, T. F. J. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00187 · Cited by 83
Self-citation
Regulation of Extrasynaptic 5-HT by Serotonin Reuptake Transporter Function in 5-HT-Absorbing Neurons Underscores Adaptation Behavior in Caenorhabditis elegans
Jafari, G., Xie, Y., Kullyev, A., Liang, B., & Sze, J. Y. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1692-11.2011 · Cited by 82
Remote Homology between Munc13 MUN Domain and Vesicle Tethering Complexes
Pei, J., Ma, C., Rizo, J., & Grishin, N. V. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.06.054 · Cited by 81
Sexual Dimorphism and Sex Differences in Caenorhabditis elegans Neuronal Development and Behavior
Barr, M. M., Garcia, L. R., & Portman, D. (2018) · Genetics · doi:10.1534/genetics.117.300294 · Cited by 81
Brain–gut communications via distinct neuroendocrine signals bidirectionally regulate longevity in C. elegansPreprint
Zhang, B., Gong, J., Zhang, W., Xiao, R., Liu, J., & Xu, X. Z. S. (2018) · Genes & Development · doi:10.1101/gad.309625.117 · Cited by 88
Monoamines and neuropeptides interact to inhibit aversive behaviour in Caenorhabditis elegans
Mills, H., Wragg, R. T., Hapiak, V., Castelletto, M. L., Zahratka, J. A., Harris, G. P., Summers, P., Korchnak, A. C., Law, W., Bamber, B. A., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.422 · Cited by 81
A C. elegans Thermosensory Circuit Regulates Longevity through crh-1 /CREB-Dependent flp-6 Neuropeptide Signaling
Chen, Y.-C., Chen, H.-J., Tseng, W.-C., Hsu, J.-M., Huang, T., Chen, C., & Pan, C. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.021 · Cited by 77
The Monoaminergic Modulation of Sensory-Mediated Aversive Responses in Caenorhabditis elegans Requires Glutamatergic/Peptidergic Cotransmission
Harris, G., Mills, H., Wragg, R. T., Hapiak, V., Castelletto, M. L., Korchnak, A. C., & Komuniecki, R. W. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0497-10.2010 · Cited by 79
Mitochondrial hydrogen peroxide positively regulates neuropeptide secretion during diet-induced activation of the oxidative stress response
Jia, Q., & Sieburth, D. (2021) · Nature Communications · doi:10.1038/s41467-021-22561-x · Cited by 79
Fast cAMP Modulation of Neurotransmission via Neuropeptide Signals and Vesicle Loading
Costa, W. S., Yu, S.-C., Liewald, J. F., & GOTTSCHALK, A. R. (2017) · Current Biology · doi:10.1016/j.cub.2016.12.055 · Cited by 76
CAPS1 and CAPS2 Regulate Stability and Recruitment of Insulin Granules in Mouse Pancreatic β Cells
Speidel, D., Salehi, A., Obermueller, S., Lundquist, I., Brose, N., Renström, E., & Rorsman, P. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.009 · Cited by 75
The neuropeptide NLP-22 regulates a sleep-like state in Caenorhabditis elegans
Nelson, M. D., Trojanowski, N. F., George-Raizen, J. B., Smith, C. J., Yu, C.-C., Fang-Yen, C. M., & Raizen, D. M. (2013) · Nature Communications · doi:10.1038/ncomms3846 · Cited by 80
Distinct Neural Circuits Control Rhythm Inhibition and Spitting by the Myogenic Pharynx of C. elegans
Bhatla, N., Droste, R., Sando, S. R., Huang, A., & Horvitz, H. R. (2015) · Current Biology · doi:10.1016/j.cub.2015.06.052 · Cited by 71
A sensory-motor neuron type mediates proprioceptive coordination of steering in C. elegans via two TRPC channels
Yeon, J., Kim, J., Kim, D., Kim, H., Kim, J., Du, E. J., Kang, K., Lim, H., Moon, D., & Kim, K. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2004929 · Cited by 67
Neuronal mitochondrial dynamics coordinate systemic mitochondrial morphology and stress response to confer pathogen resistance in C. elegans
Chen, L., Lin, C.-T., Lin, L.-Y., Hsu, J.-M., Wu, Y., & Pan, C. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.04.021 · Cited by 70
RNAi screen identifies a role for adaptor protein AP-3 in sorting to the regulated secretory pathway
Asensio, C. S., Sirkis, D. W., & Edwards, R. H. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201006131 · Cited by 70
Transfer characteristics of a thermosensory synapse in Caenorhabditis elegans
Narayan, A., Laurent, G., & Sternberg, P. W. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106617108 · Cited by 69
An Afferent Neuropeptide System Transmits Mechanosensory Signals Triggering Sensitization and Arousal in C. elegans
Chew, Y. L., Tanizawa, Y., Cho, Y., Zhao, B., Yu, A. J., Ardiel, E. L., Rabinowitch, I., Bai, J., Rankin, C. H., Lu, H., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.08.003 · Cited by 70
Tomosyn Negatively Regulates CAPS-Dependent Peptide Release at Caenorhabditis elegans Synapses
Gracheva, E. O., Burdina, A. O., Touroutine, D., Berthelot-Grosjean, M., Parekh, H., & Richmond, J. E. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2339-07.2007 · Cited by 65
Two distinct secretory vesicle–priming steps in adrenal chromaffin cells
Liu, Y., Schirra, C., Edelmann, L., Matti, U., Rhee, J., Hof, D., Bruns, D., Brose, N., Rieger, H., Stevens, D. R., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201001164 · Cited by 67
Homeostasis in C. elegans sleep is characterized by two behaviorally and genetically distinct mechanisms
Nagy, S., Tramm, N., Sanders, J., Iwanir, S., Shirley, I. A., Levine, E., & Biron, D. (2014) · eLife · doi:10.7554/elife.04380 · Cited by 63
Sphingosine Kinase Activates the Mitochondrial Unfolded Protein Response and Is Targeted to Mitochondria by Stress
Kim, S., & Sieburth, D. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.037 · Cited by 66
Developmentally Regulated Ca2+-Dependent Activator Protein for Secretion 2 (CAPS2) is Involved in BDNF Secretion and is Associated with Autism Susceptibility
Sadakata, T., & Furuichi, T. (2009) · The Cerebellum · doi:10.1007/s12311-009-0097-5 · Cited by 63
Olfaction regulates organismal proteostasis and longevity via microRNA-dependent signalling
Finger, F., Ottens, F., Springhorn, A., Drexel, T., Proksch, L., Metz, S., Cochella, L., & Hoppe, T. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0033-z · Cited by 65
Neurotransmitter signaling through heterotrimeric G proteins: insights from studies in C. elegans
Koelle, M. R. (2016) · WormBook · doi:10.1895/wormbook.1.75.2 · Cited by 58
RAB-5 and RAB-10 cooperate to regulate neuropeptide release in Caenorhabditis elegans
Sasidharan, N., Sumakovic, M., Hannemann, M., Hegermann, J., Liewald, J. F., Olendrowitz, C., Koenig, S., Grant, B. D., Rizzoli, S. O., GOTTSCHALK, A. R., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203306109 · Cited by 55
Direct glia-to-neuron transdifferentiation gives rise to a pair of male-specific neurons that ensure nimble male mating
Molina-García, L., Lloret-Fernández, C., Cook, S. J., Kim, B., Bonnington, R. C., Sammut, M., O’Shea, J. M., Gilbert, S. P. R., Elliott, D. J. S., Hall, D. H., et al. (2020) · eLife · doi:10.7554/elife.48361 · Cited by 58
Parasite neuropeptide biology: Seeding rational drug target selection?
McVeigh, P., Atkinson, L. E., Marks, N. J., Mousley, A., Dalzell, J. J., Sluder, A. E., Hammerland, L. G., & Maule, A. G. (2011) · International Journal for Parasitology Drugs and Drug Resistance · doi:10.1016/j.ijpddr.2011.10.004 · Cited by 56
UNC-108/Rab2 Regulates Postendocytic Trafficking in Caenorhabditis elegans
Chun, D. K., McEwen, J. M., Burbea, M., & Kaplan, J. M. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-11-1120 · Cited by 56
Environmental CO 2 inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity
Fenk, L. A., & de Bono, M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423808112 · Cited by 55
The EARP Complex and Its Interactor EIPR-1 Are Required for Cargo Sorting to Dense-Core Vesicles
Topalidou, I., Cattin‐Ortolá, J., Pappas, A. L., Cooper, K., Merrihew, G. E., MacCoss, M. J., & Ailion, M. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006074 · Cited by 55
Self-citation
The cell non-autonomous function of ATG-18 is essential for neuroendocrine regulation of Caenorhabditis elegans lifespan
Minnerly, J., Zhang, J., Parker, T., Kaul, T. K., & Jia, K. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006764 · Cited by 57
Concerted pulsatile and graded neural dynamics enables efficient chemotaxis in C. elegans
Itskovits, E., Ruach, R., Kazakov, A., & Zaslaver, A. (2018) · Nature Communications · doi:10.1038/s41467-018-05151-2 · Cited by 55
Olfactory perception of food abundance regulates dietary restriction-mediated longevity via a brain-to-gut signal
Zhang, B., Jun, H., Wu, J., Liu, J., & Xu, X. Z. S. (2021) · Nature Aging · doi:10.1038/s43587-021-00039-1 · Cited by 58
Neuronal DAF-16-to-intestinal DAF-16 communication underlies organismal lifespan extension in C. elegans
Uno, M., Tani, Y., Nono, M., Okabe, E., Kishimoto, S., Takahashi, C., Abe, R., Kurihara, T., & Nishida, E. (2021) · iScience · doi:10.1016/j.isci.2021.102706 · Cited by 54
Investigating the molecular mechanisms of learning and memory using Caenorhabditis elegans
Rahmani, A., & Chew, Y. L. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15510 · Cited by 57
Identification of a Munc13-sensitive step in chromaffin cell large dense-core vesicle exocytosis
Man, K. N. M., Imig, C., Walter, A. M., Pinheiro, P. S., Stevens, D. R., Rettig, J., Sørensen, J. B., Cooper, B. H., Brose, N., & Wojcik, S. M. (2015) · eLife · doi:10.7554/elife.10635 · Cited by 63
Circuit mechanisms encoding odors and driving aging-associated behavioral declines in Caenorhabditis elegans
Leinwand, S. G., Yang, C. J., Bazopoulou, D., Chronis, N., Srinivasan, J., & Chalasani, S. H. (2015) · eLife · doi:10.7554/elife.10181 · Cited by 57
Neuropeptidergic Signaling and Active Feeding State Inhibit Nociception inCaenorhabditis elegans
Ezcurra, M., Walker, D. S., Beets, I., Swoboda, P., & Schafer, W. R. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1128-15.2016 · Cited by 52
Mechanisms of exocytosis
Sugita, S. (2007) · Acta Physiologica · doi:10.1111/j.1748-1716.2007.01803.x · Cited by 60
Neuromedin U signaling regulates retrieval of learned salt avoidance in a C. elegans gustatory circuit
Watteyne, J., Peymen, K., der Auwera, P. V., Borghgraef, C., Vandewyer, E., Damme, S. V., Rutten, I., Lammertyn, J., Jelier, R., Schoofs, L., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15964-9 · Cited by 52
Molecular biology of thermosensory transduction in C. elegans
Aoki, I., & Mori, I. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.03.011 · Cited by 49
Neuropeptides Amplify and Focus the Monoaminergic Inhibition of Nociception in Caenorhabditis elegans
Hapiak, V., Summers, P., Ortega, A., Law, W. J., Stein, A., & Komuniecki, R. W. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1324-13.2013 · Cited by 54
Role of Phosphoinositides at the Neuronal Synapse
Frère, S. G. A., Chang-Ileto, B., & Paolo, G. D. (2012) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-94-007-3015-1_5 · Cited by 48
Munc13 Homology Domain-1 in CAPS/UNC31 Mediates SNARE Binding Required for Priming Vesicle Exocytosis
Khodthong, C., Kabachinski, G., James, D. J., & Martin, T. F. J. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.07.002 · Cited by 48
Self-citation
Functionally asymmetric motor neurons contribute to coordinating locomotion of Caenorhabditis elegans
Tolstenkov, O. O., der Auwera, P. V., Liewald, J. F., Costa, W. S., Bazhanova, O., Gemeinhard, T., Bergs, A. C. F., & GOTTSCHALK, A. R. (2018) · eLife · doi:10.7554/elife.34997 · Cited by 48
Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron
Zou, W., Fu, J., Zhang, H., Du, K., Huang, W., Yu, J., Li, S., Fan, Y., Baylis, H. A., Gao, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06819-5 · Cited by 47
Differential Regulation of the Heat Shock Factor 1 and DAF-16 by Neuronal nhl-1 in the Nematode C. elegans
Volovik, Y., Moll, L., Marques, F. C., Maman, M., Bejerano‐Sagie, M., & Cohen, E. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.028 · Cited by 45
UNC-31/CAPS docks and primes dense core vesicles in C. elegans neurons
Lin, X., Ming, M., Chen, M., Niu, W., Zhang, Y., Liu, B., Jiu, Y., Yu, J.-W., Xu, T., & Wu, Z. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.05.148 · Cited by 44
Endocrine aspects of organelle stress — cell non-autonomous signaling of mitochondria and the ER
Schinzel, R. T., & Dillin, A. G. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2015.01.006 · Cited by 42
Resident CAPS on dense-core vesicles docks and primes vesicles for fusion
Kabachinski, G., Kielar-Grevstad, D. M., Zhang, X., James, D. J., & Martin, T. F. J. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-07-0509 · Cited by 42
Self-citation
The nematode C. elegans senses airborne sound
Iliff, A. J., Wang, C., Ronan, E. A., Hake, A. E., Guo, Y., Li, X., Zhang, X., Zheng, M., Liu, J., Grosh, K., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.08.035 · Cited by 41
Neural-Immune Communication in Caenorhabditis elegans
Zhang, X., & Zhang, Y. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.05.003 · Cited by 40
Glutamate signaling from a single sensory neuron mediates experience-dependent bidirectional behavior in Caenorhabditis elegans
Sato, H., Kunitomo, H., Fei, X., Hashimoto, K., & Iino, Y. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109177 · Cited by 39
Genetic dissection of neuropeptide cell biology at high and low activity in a defined sensory neuron
Laurent, P., Ch'ng, Q.-L., Jospin, M., Chen, C., Lorenzo, R., & de Bono, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714610115 · Cited by 37
Feeding State, Insulin and NPR-1 Modulate Chemoreceptor Gene Expression via Integration of Sensory and Circuit Inputs
Gruner, M., Nelson, D., Winbush, A., Hintz, R., Ryu, L., Chung, S., Kim, K., Gabel, C. V., & van der Linden, A. M. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004707 · Cited by 38
Olfaction Modulates Reproductive Plasticity through Neuroendocrine Signaling in Caenorhabditis elegans
Sowa, J. N., Mutlu, A. S., Xia, F., & Wang, M. C. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.023 · Cited by 35
C. elegans neurons have functional dendritic spines
Cuentas-Condori, A., Mulcahy, B., He, S., Palumbos, S. D., Zhen, M., & Miller, D. M. (2019) · eLife · doi:10.7554/elife.47918 · Cited by 38
Presynaptic Inhibition Selectively Weakens Peptidergic Cotransmission in a Small Motor System
DeLong, N. D., Beenhakker, M. P., & Nusbaum, M. P. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00833.2009 · Cited by 36
Multiple excitatory and inhibitory neural signals converge to fine‐tune Caenorhabditis elegans feeding to food availability
Dallière, N., Bhatla, N., Luedtke, Z., Dengke, K., Woolman, J., Walker, R. J., Holden-Dye, L. M., & O'Connor, V. M. (2015) · The FASEB Journal · doi:10.1096/fj.15-279257 · Cited by 34
A Novel CaM Kinase II Pathway Controls the Location of Neuropeptide Release from Caenorhabditis elegans Motor Neurons
Hoover, C., Edwards, S. L., Yu, S.-C., Kittelmann, M., Richmond, J. E., Eimer, S., Yorks, R. M., & Miller, K. G. (2014) · Genetics · doi:10.1534/genetics.113.158568 · Cited by 34

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)
ORCID: Speese, S.
Ailion, M.
Ann, K.
Martin, T. F. J.
Venue: Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2007-06-06
Volume: 27
Issue: 23
Pages: 6150-6162
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.1466-07.2007
PMC: PMC6672138
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: bronze
doi.org
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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

UNC-31 (CAPS) Is Required for Dense-Core Vesicle But Not Synaptic Vesicle Exocytosis in Caenorhabditis elegans

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks