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Innate Immunity in the C. elegans Intestine Is Programmed by a Neuronal Regulator of AWC Olfactory Neuron Development

Overview
Journal Cell Rep
Publisher Cell Press
Date 2020 Apr 9
PMID 32268082
Citations 28
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Abstract

Olfactory neurons allow animals to discriminate nutritious food sources from potential pathogens. From a forward genetic screen, we uncovered a surprising requirement for the olfactory neuron gene olrn-1 in the regulation of intestinal epithelial immunity in Caenorhabditis elegans. During nematode development, olrn-1 is required to program the expression of odorant receptors in the AWC olfactory neuron pair. Here, we show that olrn-1 also functions in AWC neurons in the cell non-autonomous suppression of the canonical p38 MAPK PMK-1 immune pathway in the intestine. Low activity of OLRN-1, which activates the p38 MAPK signaling cassette in AWC neurons during larval development, also de-represses the p38 MAPK PMK-1 pathway in the intestine to promote immune effector transcription, increased clearance of an intestinal pathogen, and resistance to bacterial infection. These data reveal an unexpected connection between olfactory receptor development and innate immunity and show that anti-pathogen defenses in the intestine are developmentally programmed.

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References
1.
Pukkila-Worley R . Surveillance Immunity: An Emerging Paradigm of Innate Defense Activation in Caenorhabditis elegans. PLoS Pathog. 2016; 12(9):e1005795. PMC: 5025020. DOI: 10.1371/journal.ppat.1005795. View

2.
Anderson S, Cheesman H, Peterson N, Salisbury J, Soukas A, Pukkila-Worley R . The fatty acid oleate is required for innate immune activation and pathogen defense in Caenorhabditis elegans. PLoS Pathog. 2019; 15(6):e1007893. PMC: 6597122. DOI: 10.1371/journal.ppat.1007893. View

3.
Styer K, Singh V, Macosko E, Steele S, Bargmann C, Aballay A . Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science. 2008; 322(5900):460-4. PMC: 2831475. DOI: 10.1126/science.1163673. View

4.
Richardson C, Kooistra T, Kim D . An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature. 2010; 463(7284):1092-5. PMC: 2834299. DOI: 10.1038/nature08762. View

5.
Bargmann C, Hartwieg E, Horvitz H . Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell. 1993; 74(3):515-27. DOI: 10.1016/0092-8674(93)80053-h. View