Immediate activation of chemosensory neuron gene expression by bacterial metabolites is selectively induced by distinct cyclic GMP-dependent pathways in Caenorhabditis elegans.

Anne C Hart,Jaeseok Park,Joshua D Meisel,Dennis H Kim

doi:10.1371/journal.pgen.1008505

Anne C Hart, Jaeseok Park + Show 2 more

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https://doi.org/10.1371/journal.pgen.1008505

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Abstract

Dynamic gene expression in neurons shapes fundamental processes in the nervous systems of animals. However, how neuronal activation by different stimuli can lead to distinct transcriptional responses is not well understood. We have been studying how microbial metabolites modulate gene expression in chemosensory neurons of Caenorhabditis elegans. Considering the diverse environmental stimuli that can activate chemosensory neurons of C. elegans, we sought to understand how specific transcriptional responses can be generated in these neurons in response to distinct cues. We have focused on the mechanism of rapid (<6 min) and selective transcriptional induction of daf-7, a gene encoding a TGF-β ligand, in the ASJ chemosensory neurons in response to the pathogenic bacterium Pseudomonas aeruginosa. DAF-7 is required for the protective behavioral avoidance of P. aeruginosa by C. elegans. Here, we define the involvement of two distinct cyclic GMP (cGMP)-dependent pathways that are required for daf-7 expression in the ASJ neuron pair in response to P. aeruginosa. We show that a calcium-independent pathway dependent on the cGMP-dependent protein kinase G (PKG) EGL-4, and a canonical calcium-dependent signaling pathway dependent on the activity of a cyclic nucleotide-gated channel subunit CNG-2, function in parallel to activate rapid, selective transcription of daf-7 in response to P. aeruginosa metabolites. Our data suggest that fast, selective early transcription of neuronal genes require PKG in shaping responses to distinct microbial stimuli in a pair of C. elegans chemosensory neurons.

Highlights

Chemosensory systems of animals transduce external chemical stimuli into neuronal signals, with diverse roles in animal physiology [1,2,3]
When the free-living microscopic roundworm C. elegans is exposed to the pathogenic bacteria Pseudomonas aeruginosa, sensory neurons detect metabolites produced by the pathogen and induce expression of the gene for a neuroendocrine ligand called DAF-7
We investigated how the behavior of C. elegans is modulated by pathogenic bacteria, Pseudomonas aeruginosa, a devastating opportunistic pathogen of humans that is commonly found in soil and water and can kill C. elegans [15]

Summary

Introduction

Chemosensory systems of animals transduce external chemical stimuli into neuronal signals, with diverse roles in animal physiology [1,2,3]. A challenge for chemosensory systems is detecting and processing a diverse set of environmental information to generate appropriate neuronal and behavioral responses. Whereas neurons utilize electrical impulses in rapid data transmission, changes in gene expression serve as a mechanism for transducing information over a longer time scale. Our recent work has focused on understanding how changes in gene expression in chemosensory neurons of C. elegans can be modulated by interactions with its microbial environment and internal cues [5,6,7]. There has been an increasing appreciation for the role of the nervous system in recognizing and responding to microbes in the environment

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