Hypoxia activates a latent circuit for processing gustatory information in C. elegans.
Dedicated neuronal circuits enable animals to engage in specific behavioral responses to environmental stimuli. We found that hypoxic stress enhanced gustatory sensory perception via previously unknown circuitry in Caenorhabditis elegans. The hypoxia-inducible transcription factor HIF-1 upregulated serotonin (5-HT) expression in specific sensory neurons that are not normally required for chemosensation. 5-HT subsequently promoted hypoxia-enhanced sensory perception by signaling through the metabotropic G protein-coupled receptor SER-7 in an unusual peripheral neuron, the M4 motor neuron. M4 relayed this information back into the CNS via the FMRFamide-related neuropeptide FLP-21 and its cognate receptor, NPR-1. Thus, physiological detection of hypoxia results in the activation of an additional, previously unrecognized circuit for processing sensory information that is not required for sensory processing under normoxic conditions.
Pocock
Roger
R
Department of Biochemistry and Molecular Biophysics, Howard Hughes Medical Institute, Columbia University Medical Center, New York, New York, USA. roger.pocock@bric.ku.dk
Hobert
Oliver
O
D000818:Animals; D030801:Animals, Genetically Modified; D001522:Behavior, Animal; D017173:Caenorhabditis elegans / Q000235:genetics / Q000502:physiology; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism / Q000494:pharmacology; D002630:Chemotactic Factors / Q000378:metabolism; D004195:Disease Models, Animal; D019835:FMRFamide / Q000494:pharmacology; D005247:Feeding Behavior; D019205:GTP-Binding Protein alpha Subunits, Gs / Q000378:metabolism; D005786:Gene Expression Regulation / Q000187:drug effects / Q000502:physiology; D000860:Hypoxia / Q000473:pathology* / Q000503:physiopathology*; D049990:Membrane Transport Modulators / Q000494:pharmacology; D009068:Movement / Q000502:physiology*; D009154:Mutation / Q000235:genetics; D009415:Nerve Net / Q000187:drug effects / Q000502:physiology*; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D010614:Pharynx / Q000166:cytology / Q000502:physiology*; D017476:Receptors, Neuropeptide Y / Q000378:metabolism; D012701:Serotonin / Q000378:metabolism; D014157:Transcription Factors / Q000494:pharmacology; D014365:Tryptophan Hydroxylase / Q000378:metabolism; D015854:Up-Regulation / Q000187:drug effects / Q000235:genetics
D029742:Caenorhabditis elegans Proteins; D002630:Chemotactic Factors; C541178:HIF-1 protein, C elegans; D049990:Membrane Transport Modulators; C468272:NPR-1 protein, C elegans; D017476:Receptors, Neuropeptide Y; C478614:SER-7b protein, C elegans; D014157:Transcription Factors; D012701:Serotonin; D019835:FMRFamide; D014365:Tryptophan Hydroxylase; D019205:GTP-Binding Protein alpha Subunits, Gs
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