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


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
08 2020
Historique:
received: 30 10 2019
accepted: 15 06 2020
entrez: 11 8 2020
pubmed: 11 8 2020
medline: 24 9 2020
Statut: epublish

Résumé

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.

Identifiants

pubmed: 32776934
doi: 10.1371/journal.pgen.1008505
pii: PGENETICS-D-19-01805
pmc: PMC7416920
doi:

Substances chimiques

Caenorhabditis elegans Proteins 0
Cyclic Nucleotide-Gated Cation Channels 0
DAF-7 protein, C elegans 0
Transforming Growth Factor beta 0
Cyclic GMP-Dependent Protein Kinases EC 2.7.11.12
EGL-4 protein, C elegans EC 2.7.11.12
Cyclic GMP H2D2X058MU

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1008505

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM084477
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007287
Pays : United States
Organisme : NIH HHS
ID : P40 OD010440
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Jaeseok Park (J)

Division of Infectious Diseases, Boston Children's Hospital, and Department of Pediatrics, Harvard Medical School, Boston, Massachusetts, United States of America.
Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America.

Joshua D Meisel (JD)

Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America.

Dennis H Kim (DH)

Division of Infectious Diseases, Boston Children's Hospital, and Department of Pediatrics, Harvard Medical School, Boston, Massachusetts, United States of America.

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Classifications MeSH