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Published January 4, 2011 | Published + Supplemental Material
Journal Article Open

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

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.

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.

Attached Files

Published - Hallem2011p12638P_Natl_Acad_Sci_Usa.pdf

Supplemental Material - pnas.201017354SI.pdf

Supplemental Material - sd01.xlsx

Supplemental Material - sd02.xlsx

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Additional details

Created:
August 22, 2023
Modified:
October 23, 2023