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Cited by 37Neurobiology and Insect Physiology ResearchIon Channels and ReceptorsGenetics, Aging, and Longevity in Model Organisms

Polymodal Responses in C. elegans Phasmid Neurons Rely on Multiple Intracellular and Intercellular Signaling Pathways

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Zou, Wenjuan, Cheng, Hankui, Li, Shitian, Yue, Xiaomin, Xue, Yadan, Chen, Sixi, Kang, Lijun·2017·Scientific Reports
DOI 10.1038/srep42295PMC PMC5307315
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Abstract

Animals utilize specialized sensory neurons enabling the detection of a wide range of environmental stimuli from the presence of toxic chemicals to that of touch. However, how these neurons discriminate between different kinds of stimuli remains poorly understood. By combining in vivo calcium imaging and molecular genetic manipulation, here we investigate the response patterns and the underlying mechanisms of the C. elegans phasmid neurons PHA/PHB to a variety of sensory stimuli. Our observations demonstrate that PHA/PHB neurons are polymodal sensory neurons which sense harmful chemicals, hyperosmotic solutions and mechanical stimulation. A repulsive concentration of IAA induces calcium elevations in PHA/PHB and both OSM-9 and TAX-4 are essential for IAA-sensing in PHA/PHB. Nevertheless, the PHA/PHB neurons are inhibited by copper and post-synaptically activated by copper removal. Neuropeptide is likely involved in copper removal-induced calcium elevations in PHA/PHB. Furthermore, mechanical stimulation activates PHA/PHB in an OSM-9-dependent manner. Our work demonstrates how PHA/PHB neurons respond to multiple environmental stimuli and lays a foundation for the further understanding of the mechanisms of polymodal signaling, such as nociception, in more complex organisms.

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  • C. elegans sensory neurons usually respond to several stimuli, so sensory integration starts within the sensory neurons.

    “As the sensory neurons of C. elegans generally respond to multiple stimuli, sensory integration begins within the sensory neurons themselves25,26.”

    From Whole-animal connectomes of both Caenorhabditis elegans sexes (2019) · cites this paper as [25]

    The Abstract reports that C. elegans PHA/PHB neurons respond to multiple stimuli and use intracellular and intercellular pathways to process them; the Discussion describes encoding and discrimination in those neurons. This supports sensory processing within particular sensory neurons, but the paper does not establish that C. elegans sensory neurons generally respond to multiple stimuli or that integration always begins within them. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 26

  1. Hilliard M. A.. In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. The EMBO journal 24, 63– 72, doi: 10.1038/sj.emboj.7600493 (2005). 15577941 PMC544906 · DOI
  2. Lee Y., Lee C. H. & Oh U. Painful channels in sensory neurons. Molecules and cells 20, 315– 324 (2005). 16404144
  3. Li Z., Liu J., Zheng M. & Xu X. Z. Encoding of both analog- and digital-like behavioral outputs by one C. elegans interneuron. Cell 159, 751– 765, doi: 10.1016/j.cell.2014.09.056 (2014). 25417153 PMC4243084 · DOI
  4. Bargmann C. I. Chemosensation in C. elegans. WormBook: the online review of C. elegans biology, 1– 29, doi: 10.1895/wormbook.1.123.1 (2006). PMC4781564 18050433 · DOI
  5. Hilliard M. A., Bargmann C. I. & Bazzicalupo P. C. Elegans responds to chemical repellents by integrating sensory inputs from the head and the tail. Curr Biol 12, 730– 734 (2002). 12007416
  6. Li W., Kang L., Piggott B. J., Feng Z. & Xu X. Z. The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nature communications 2, 315, doi: 10.1038/ncomms1308 (2011). PMC3098610 21587232 · DOI
  7. Tobin D. M.. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35, 307– 318 (2002). 12160748
  8. Yang X.. Syntaxin opening by the MUN domain underlies the function of Munc13 in synaptic-vesicle priming. Nature structural & molecular biology 22, 547– 554, doi: 10.1038/nsmb.3038 (2015). PMC4809529 26030875 · DOI
  9. Zhou K. M.. PKA activation bypasses the requirement for UNC-31 in the docking of dense core vesicles from C. elegans neurons. Neuron 56, 657– 669, doi: 10.1016/j.neuron.2007.09.015 (2007). 18031683 · DOI
  10. Harris G.. Dissecting the signaling mechanisms underlying recognition and preference of food odors. The Journal of neuroscience: the official journal of the Society for Neuroscience 34, 9389– 9403, doi: 10.1523/JNEUROSCI.0012-14.2014 (2014). 25009271 PMC4087214 · DOI
  11. Wang X., Li G., Liu J., Liu J. & Xu X. Z. TMC-1 Mediates Alkaline Sensation in C. elegans through Nociceptive Neurons. Neuron 91, 146– 154, doi: 10.1016/j.neuron.2016.05.023 (2016). 27321925 PMC4938749 · DOI
  12. Colbert H. A., Smith T. L. & Bargmann C. I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. The Journal of neuroscience: the official journal of the Society for Neuroscience 17, 8259– 8269 (1997). 9334401 PMC6573730
  13. Yoshida K.. Odour concentration-dependent olfactory preference change in C. elegans. Nature communications 3, 739, doi: 10.1038/ncomms1750 (2012). 22415830 · DOI
  14. Geffeney S. L.. DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron 71, 845– 857, doi: 10.1016/j.neuron.2011.06.038 (2011). 21903078 PMC3170654 · DOI
  15. Kang L., Gao J., Schafer W. R., Xie Z. & Xu X. Z. C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron 67, 381– 391, doi: 10.1016/j.neuron.2010.06.032 (2010). 20696377 PMC2928144 · DOI
  16. O’Hagan R., Chalfie M. & Goodman M. B. The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nature neuroscience 8, 43– 50, doi: 10.1038/nn1362 (2005). 15580270 · DOI
  17. Li W., Feng Z., Sternberg P. W. & Xu X. Z. A. C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440, 684– 687, doi: 10.1038/nature04538 (2006). 16572173 PMC2865900 · DOI
  18. Chalasani S. H.. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450, 63– 70, doi: 10.1038/nature06292 (2007). 17972877 · DOI
  19. Wang D., O’Halloran D. & Goodman M. B. GCY-8, PDE-2, and NCS-1 are critical elements of the cGMP-dependent thermotransduction cascade in the AFD neurons responsible for C. elegans thermotaxis. J Gen Physiol 142, 437– 449, doi: 10.1085/jgp.201310959 (2013). 24081984 PMC3787776 · DOI
  20. Liu J.. C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nature neuroscience 13, 715– 722, doi: 10.1038/nn.2540 (2010). 20436480 PMC2882063 · DOI
  21. Delmas P. & Coste B. Mechano-gated ion channels in sensory systems. Cell 155, 278– 284, doi: 10.1016/j.cell.2013.09.026 (2013). 24120130 · DOI
  22. Zhang W.. Ankyrin Repeats Convey Force to Gate the NOMPC Mechanotransduction Channel. Cell 162, 1391– 1403, doi: 10.1016/j.cell.2015.08.024 (2015). 26359990 PMC4568062 · DOI
  23. Ibsen S., Tong A., Schutt C., Esener S. & Chalasani S. H. Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans. Nature communications 6, 8264, doi: 10.1038/ncomms9264 (2015). PMC4571289 26372413 · DOI
  24. Wu Z. & Muller U. Molecular Identity of the Mechanotransduction Channel in Hair Cells: Not Quiet There Yet. The Journal of neuroscience: the official journal of the Society for Neuroscience 36, 10927– 10934, doi: 10.1523/JNEUROSCI.1149-16.2016 (2016). 27798175 PMC5098834 · DOI
  25. Corey D. P. & Holt J. R. Are TMCs the Mechanotransduction Channels of Vertebrate Hair Cells? The Journal of neuroscience: the official journal of the Society for Neuroscience 36, 10921– 10926, doi: 10.1523/JNEUROSCI.1148-16.2016 (2016). 27798174 PMC5098833 · DOI
  26. Brenner S. The genetics of Caenorhabditis elegans. Genetics 77, 71– 94 (1974). 4366476 PMC1213120

Cited by

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Authors
Zou, W., Cheng, H., Li, S., Yue, X., Xue, Y., Chen, S., & Kang, L.
Affiliations
  • Zhejiang University (CN)
  • Fuzhou University (CN)
Corresponding author
  • Chen, Sixi
  • Kang, Lijun
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2017-02-14
Volume
7
Issue
1
Pages
42295-42295
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/srep42295
PMC
PMC5307315
OpenAlex
W2588937528
Cited by
37
References
2
Citations by year
2025: 2 · 2024: 3 · 2023: 2 · 2022: 4 · 2021: 6 · 2020: 5 · 2019: 4 · 2018: 8 · 2017: 3
FWCI
2.68
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
National Institutes of Health (OD010440, P40OD010440)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords
Caenorhabditis elegans, osm-9, copper removal, neuropeptide signaling, mechanical stimulation, nociception, calcium imaging, sensory discrimination
MeSH terms
Animals, Calcium, Copper, Extracellular Space, Ion Channels, Nerve Tissue Proteins, Neurons, Odorants, Physical Stimulation, Sensory Receptor Cells, Touch, Signal Transduction, Caenorhabditis elegans, Caenorhabditis elegans Proteins, Intracellular Space, TRPV Cation Channels

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