Remembering your enemies: mechanisms of within‐generation and multigenerational immune priming in <i>Caenorhabditis elegans</i>

Willis, Alexandra R.; Sukhdeo, Ronesh; Reinke, Aaron W.

doi:10.1111/febs.15509

Cited by 23 publications

(18 citation statements)

References 88 publications

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“…Studies in the genetically tractable nematode C. elegans have enabled fundamental immune advances and shed light on many epigenetically inherited and stress-induced phenotypes [7][8][9] . As such, C. elegans has recently become a powerful model for the study of inherited innate immunity 10 . In this host, antiviral immunity, mediated by the small RNA mediated silencing of viral transcripts, was shown to last for at least three generations and be dependent on RNA interference (RNAi) pathways 11 .…”

Section: Several Reports Have Described the Deposition Of Bacterial Cmentioning

confidence: 99%

A parental transcriptional response to microsporidia infection induces inherited immunity in offspring

Willis

Zhao

Sukhdeo

et al. 2020

Preprint

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Inherited immunity is an emerging field and describes how the transfer of immunity from parents to offspring can promote progeny survival in the face of infection. The mechanisms of how inherited immunity is induced are mostly unknown. The intracellular parasite Nematocida parisii is a natural microsporidian pathogen of Caenorhabditis elegans. Here, we show that N. parisii-infected worms produce primed offspring that are resistant to microsporidia infection. We find that immunity is induced in a dose dependent manner and lasts for a single generation. Intergenerational immunity prevents host cell invasion by N. parisii and also enhances survival to the bacterial pathogen Pseudomonas aeruginosa. Further, we show that inherited immunity is triggered by the host transcriptional response to infection, which can also be induced through maternal somatic depletion of negative regulators PALS-22 and the retinoblastoma protein ortholog LIN-35. We show that other biotic and abiotic stresses, such as viral infection and cadmium exposure, that induce a similar transcriptional response to microsporidia can also induce immunity in progeny. Our results demonstrate that distinct stimuli can induce inherited immunity to provide resistance against multiple classes of pathogens. These results show that activation of an innate immune response can provide protection against pathogens not only within a generation, but also in the next generation.

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Section: Several Reports Have Described the Deposition Of Bacterial Cmentioning

confidence: 99%

A parental transcriptional response to microsporidia infection induces inherited immunity in offspring

Willis

Zhao

Sukhdeo

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Studies in the genetically tractable nematode Caenorhabditis elegans have enabled fundamental immune advances and shed light on many epigenetically inherited and stress-induced phenotypes (7)(8)(9). Hence, C. elegans has recently become a powerful model for the study of inherited innate immunity (10). In this host, antiviral immunity, mediated by the small RNA-mediated silencing of viral transcripts, was shown to last for at least three generations and be dependent on RNA interference (RNAi) pathways (11).…”

Section: Introductionmentioning

confidence: 99%

A parental transcriptional response to microsporidia infection induces inherited immunity in offspring

et al. 2021

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Parental infection can result in the production of offspring with enhanced immunity phenotypes. Critically, the mechanisms underlying inherited immunity are poorly understood. Here, we show that Caenorhabditis elegans infected with the intracellular microsporidian parasite N. parisii produce progeny that are resistant to microsporidia infection. We determine the kinetics of the response and show that intergenerational immunity prevents host-cell invasion by Nematocida parisii and enhances survival to the bacterial pathogen Pseudomonas aeruginosa. We demonstrate that immunity is induced by the parental transcriptional response to infection, which can be mimicked through maternal somatic depletion of PALS-22 and the retinoblastoma protein ortholog, LIN-35. We find that other biotic and abiotic stresses (viral infection and cadmium exposure) that induce a similar transcriptional response as microsporidia also induce immunity in progeny. Together, our results reveal how a parental transcriptional signal can be induced by distinct stimuli and protect offspring against multiple classes of pathogens.

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“…There have been many reviews of the field in the last couple of years (e.g. Garcia-Sanchez et al 2021;Harding and Ewbank 2021;Kim and Flavell 2020;Martineau et al 2021;Miles et al 2019;Penkov et al 2019;Radeke and Herman 2021;Singh and Aballay 2020;Wani et al 2020;Willis et al 2021), and we will not attempt to be exhaustive here. Rather we will mainly take an evolutionary perspective to examine in what ways innate immunity in C. elegans resembles that of other animals and in what ways it differs.…”

Section: Introductionmentioning

confidence: 99%

C. elegans: out on an evolutionary limb

Pujol

Ewbank

2021

Immunogenetics

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The natural environment of the free-living nematode Caenorhabditis elegans is rich in pathogenic microbes. There is now ample evidence to indicate that these pathogens exert a strong selection pressure on C. elegans, and have shaped its genome, physiology, and behaviour. In this short review, we concentrate on how C. elegans stands out from other animals in terms of its immune repertoire and innate immune signalling pathways. We discuss how C. elegans often detects pathogens because of their effects on essential cellular processes, or organelle integrity, in addition to direct microbial recognition. We illustrate the extensive molecular plasticity that is characteristic of immune defences in C. elegans and highlight some remarkable instances of lineage-specific innovation in innate immune mechanisms.

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Remembering your enemies: mechanisms of within‐generation and multigenerational immune priming in Caenorhabditis elegans

Cited by 23 publications

References 88 publications

A parental transcriptional response to microsporidia infection induces inherited immunity in offspring

A parental transcriptional response to microsporidia infection induces inherited immunity in offspring

A parental transcriptional response to microsporidia infection induces inherited immunity in offspring

C. elegans: out on an evolutionary limb

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