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Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans

Hallem, Elissa A. and Spencer, W. Clay and McWhirter, Rebecca D. and Zeller, Georg and Henz, Stefan R. and Rätsch, Gunnar and Miller, David M., III and Horvitz, H. Robert and Sternberg, Paul W. and Ringstad, Niels (2011) Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 108 (1). pp. 254-259. ISSN 0027-8424. PMCID PMC3017194. https://resolver.caltech.edu/CaltechAUTHORS:20110224-100625385

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Abstract

CO_2 is both a critical regulator of animal physiology and an important sensory cue for many animals for host detection, food location, and mate finding. The free-living soil nematode Caenorhabditis elegans shows CO_2 avoidance behavior, which requires a pair of ciliated sensory neurons, the BAG neurons. Using in vivo calcium imaging, we show that CO_2 specifically activates the BAG neurons and that the CO_2-sensing function of BAG neurons requires TAX-2/TAX-4 cyclic nucleotide-gated ion channels and the receptor-type guanylate cyclase GCY-9. Our results delineate a molecular pathway for CO_2 sensing and suggest that activation of a receptor-type guanylate cyclase is an evolutionarily conserved mechanism by which animals detect environmental CO_2.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1017354108DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3017194/PubMed CentralArticle
ORCID:
AuthorORCID
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2011 National Academy of Sciences. Freely available online through the PNAS open access option. Contributed by Paul W. Sternberg, November 22, 2010 (sent for review August 2, 2010). Published online before print December 20, 2010. We thank Aravi Samuel, Chris Gabel, and Harrison Gabel (Harvard University, Cambridge, MA); Cori Bargmann (Rockefeller University, New York); Leon Avery (University of Texas Southwestern Medical Center, Dallas); Ikue Mori and Atsushi Kuhara (Nagoya University, Nagoya, Japan); Denise Ferkey (SUNY Buffalo, Buffalo, NY); Larry Salkoff (Washington University School of Medicine, St. Louis); Shohei Mitani (Tokyo Women’s Medical University School of Medicine, Tokyo); Anne Hart (Brown University, Providence, RI); and the Caenorhabditis Genetics Center for strains and reagents. We thank the Vanderbilt Flow Cytometry Core and Vanderbilt Functional Genomics Shared Resource (VFGSR) for help with microarray experiments. We thank Julia Brandt and Sonya Aziz-Zaman for assistance in cloning the gcy-9 cDNA. H.R.H. and P.W.S. are Investigators of the Howard Hughes Medical Institute. This work was supported by a Helen Hay Whitney postdoctoral fellowship (to E.A.H.), a National Institutes of Health Pathway to Independence award (to E.A.H.), National Institutes of Health Grants U01 HG004263 (to D.M.M.), R01 NS26115 (to D.M.M.), and R01 GM24663 (to H.R.H.), the Howard HughesMedical Institute (P.W.S.), a Whitehead Fellowship for Junior Faculty in Biomedical and Biological Sciences (to N.R.), and funds from the Helen L. and Martin S. Kimmel Center for Biology and Medicine (to N.R.). Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. HQ636455). The gene expression data have been deposited in the Gene Expression Omnibus database (accession no. GSE23769). Author contributions: E.A.H., D.M.M., H.R.H., P.W.S., and N.R. designed research; E.A.H., N.R., W.C.S., and R.D.M. performed research; E.A.H., G.Z., S.R.H., G.R., and N.R. analyzed data; and E.A.H., H.R.H., P.W.S., and N.R. wrote the paper.
Funders:
Funding AgencyGrant Number
Helen Hay Whitney FoundationUNSPECIFIED
NIHU01 HG004263
NIHR01 NS26115
NIHR01 GM24663
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Whitehead Fellowship for Junior Faculty in Biomedical and Biological SciencesUNSPECIFIED
Subject Keywords:guanylyl cyclase; olfaction; transcriptional profiling; regulator of G protein signaling; chemosensation
Issue or Number:1
PubMed Central ID:PMC3017194
Record Number:CaltechAUTHORS:20110224-100625385
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20110224-100625385
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:22472
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:25 Feb 2011 21:16
Last Modified:03 Oct 2019 02:38

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