Opposite immune responses in Caenorhabditis elegans caused by a single gene, the neuropeptide receptor gene npr-1

R. Nakad, L.B. Snoek, W. Yang, K. Dierking, P.C. Rosenstiel, J.E. Kammenga, H. Schulenburg

Research output: Chapter in Book/Report/Conference proceedingAbstract

Abstract

The nematode Caenorhabditis elegans feeds on microbes in its natural environment. Some of these microbes are pathogenic and thus harmful to the worm. To minimize fitness reductions, C. elegans has evolved various defence mechanisms including behavioural responses (i.e., avoidance behaviour). In this study, we characterized the genetic architecture of natural variation in C. elegans avoidance behaviour against the infectious stages of the Gram-positive bacterium Bacillus thuringiensis. We performed an analysis of quantitative trait loci (QTLs) using recombinant inbred lines (RILs) and introgression lines (ILs) generated from a cross of two genetically distinct C. elegans strains, N2 and CB4856. The analysis identified several QTLs that underlie variation in the behavioural response to pathogenic and non-pathogenic bacteria. One of the candidates is the npr-1 gene, which encodes a homolog of the mammalian neuropeptide receptor. Npr-1 was previously indicated to fully contribute to behavioural defence against the Gram-negative bacterium Pseudomonas aeruginosa. Surprisingly, npr-1 influences both survival and avoidance behaviour toward B. thuringiensis in exactly the opposite way than toward P. aeruginosa. We subsequently used RNA-Seq to explore in what way npr-1 differentially influences C. elegans defence responses toward these two distinct pathogen taxa. The analysis suggests that npr - 1 mediates resistance towards P. aeruginosa through the induction of oxidative stress genes and activation of GATA transcription factors, while it seems to contribute to susceptibility towards B. thuringiensis through the repression of oxidative stress genes combined with activation of Ebox transcription factors. Our findings highlight the role of npr-1 in fine-tuning nematode defence responses depending on the microbe to which C. elegans is exposed.
Original languageEnglish
Title of host publicationProceedings of the 20th International C. elegans Meeting
Place of PublicationLos Angeles, USA
Pages62-62
Publication statusPublished - 2015
Event20th International C. elegans Meeting -
Duration: 24 Jun 201528 Jun 2015

Conference

Conference20th International C. elegans Meeting
Period24/06/1528/06/15

Fingerprint

Caenorhabditis elegans
immune response
avoidance behavior
Bacillus thuringiensis
Pseudomonas aeruginosa
genes
microorganisms
quantitative trait loci
oxidative stress
Nematoda
Gram-positive bacteria
defense mechanisms
Gram-negative bacteria
introgression
inbred lines
neuropeptide receptors
transcription factors
RNA
pathogens
bacteria

Cite this

Nakad, R., Snoek, L. B., Yang, W., Dierking, K., Rosenstiel, P. C., Kammenga, J. E., & Schulenburg, H. (2015). Opposite immune responses in Caenorhabditis elegans caused by a single gene, the neuropeptide receptor gene npr-1. In Proceedings of the 20th International C. elegans Meeting (pp. 62-62). Los Angeles, USA.
Nakad, R. ; Snoek, L.B. ; Yang, W. ; Dierking, K. ; Rosenstiel, P.C. ; Kammenga, J.E. ; Schulenburg, H. / Opposite immune responses in Caenorhabditis elegans caused by a single gene, the neuropeptide receptor gene npr-1. Proceedings of the 20th International C. elegans Meeting. Los Angeles, USA, 2015. pp. 62-62
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Nakad, R, Snoek, LB, Yang, W, Dierking, K, Rosenstiel, PC, Kammenga, JE & Schulenburg, H 2015, Opposite immune responses in Caenorhabditis elegans caused by a single gene, the neuropeptide receptor gene npr-1. in Proceedings of the 20th International C. elegans Meeting. Los Angeles, USA, pp. 62-62, 20th International C. elegans Meeting, 24/06/15.

Opposite immune responses in Caenorhabditis elegans caused by a single gene, the neuropeptide receptor gene npr-1. / Nakad, R.; Snoek, L.B.; Yang, W.; Dierking, K.; Rosenstiel, P.C.; Kammenga, J.E.; Schulenburg, H.

Proceedings of the 20th International C. elegans Meeting. Los Angeles, USA, 2015. p. 62-62.

Research output: Chapter in Book/Report/Conference proceedingAbstract

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T1 - Opposite immune responses in Caenorhabditis elegans caused by a single gene, the neuropeptide receptor gene npr-1

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AU - Dierking, K.

AU - Rosenstiel, P.C.

AU - Kammenga, J.E.

AU - Schulenburg, H.

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N2 - The nematode Caenorhabditis elegans feeds on microbes in its natural environment. Some of these microbes are pathogenic and thus harmful to the worm. To minimize fitness reductions, C. elegans has evolved various defence mechanisms including behavioural responses (i.e., avoidance behaviour). In this study, we characterized the genetic architecture of natural variation in C. elegans avoidance behaviour against the infectious stages of the Gram-positive bacterium Bacillus thuringiensis. We performed an analysis of quantitative trait loci (QTLs) using recombinant inbred lines (RILs) and introgression lines (ILs) generated from a cross of two genetically distinct C. elegans strains, N2 and CB4856. The analysis identified several QTLs that underlie variation in the behavioural response to pathogenic and non-pathogenic bacteria. One of the candidates is the npr-1 gene, which encodes a homolog of the mammalian neuropeptide receptor. Npr-1 was previously indicated to fully contribute to behavioural defence against the Gram-negative bacterium Pseudomonas aeruginosa. Surprisingly, npr-1 influences both survival and avoidance behaviour toward B. thuringiensis in exactly the opposite way than toward P. aeruginosa. We subsequently used RNA-Seq to explore in what way npr-1 differentially influences C. elegans defence responses toward these two distinct pathogen taxa. The analysis suggests that npr - 1 mediates resistance towards P. aeruginosa through the induction of oxidative stress genes and activation of GATA transcription factors, while it seems to contribute to susceptibility towards B. thuringiensis through the repression of oxidative stress genes combined with activation of Ebox transcription factors. Our findings highlight the role of npr-1 in fine-tuning nematode defence responses depending on the microbe to which C. elegans is exposed.

AB - The nematode Caenorhabditis elegans feeds on microbes in its natural environment. Some of these microbes are pathogenic and thus harmful to the worm. To minimize fitness reductions, C. elegans has evolved various defence mechanisms including behavioural responses (i.e., avoidance behaviour). In this study, we characterized the genetic architecture of natural variation in C. elegans avoidance behaviour against the infectious stages of the Gram-positive bacterium Bacillus thuringiensis. We performed an analysis of quantitative trait loci (QTLs) using recombinant inbred lines (RILs) and introgression lines (ILs) generated from a cross of two genetically distinct C. elegans strains, N2 and CB4856. The analysis identified several QTLs that underlie variation in the behavioural response to pathogenic and non-pathogenic bacteria. One of the candidates is the npr-1 gene, which encodes a homolog of the mammalian neuropeptide receptor. Npr-1 was previously indicated to fully contribute to behavioural defence against the Gram-negative bacterium Pseudomonas aeruginosa. Surprisingly, npr-1 influences both survival and avoidance behaviour toward B. thuringiensis in exactly the opposite way than toward P. aeruginosa. We subsequently used RNA-Seq to explore in what way npr-1 differentially influences C. elegans defence responses toward these two distinct pathogen taxa. The analysis suggests that npr - 1 mediates resistance towards P. aeruginosa through the induction of oxidative stress genes and activation of GATA transcription factors, while it seems to contribute to susceptibility towards B. thuringiensis through the repression of oxidative stress genes combined with activation of Ebox transcription factors. Our findings highlight the role of npr-1 in fine-tuning nematode defence responses depending on the microbe to which C. elegans is exposed.

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Nakad R, Snoek LB, Yang W, Dierking K, Rosenstiel PC, Kammenga JE et al. Opposite immune responses in Caenorhabditis elegans caused by a single gene, the neuropeptide receptor gene npr-1. In Proceedings of the 20th International C. elegans Meeting. Los Angeles, USA. 2015. p. 62-62