Natural and Experimental Infection of Caenorhabditis Nematodes by Novel Viruses Related to Nodaviruses

Félix, Marie‐Anne; Ashe, Alyson; Piffaretti, Joséphine; Wu, Guang; Nuez, Isabelle; Bélicard, Tony; Jiang, Yanfang; Zhao, Guoyan; Franz, Carl; Goldstein, Leonard D.; San‐Roman, Mabel; Miska, Eric A.; Wang, David

doi:10.1371/journal.pbio.1000586

Cited by 364 publications

(683 citation statements)

References 37 publications

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“…Drechmeria coniospora, Nematocida parisii, Candida albicans) and also a nodavirus (Orsay virus) [6]. Some of the used pathogens interact with C. elegans in nature, especially the microsporidian N. parisii [7], Orsay virus [8], P. aeruginosa [9], Leucobacter sp. [10], and possibly also M. nematophilum and B. thuringiensis.…”

Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

“…Nevertheless, a few pathogens show different infection characteristics. The microsporidian N. parisii and Orsay virus are intracellular pathogens [7,8] cuticle; the latter two via the anal region and tail, and the former mainly via the mouth, the vulva and the anus [10][11][12]. These pathogens therefore target distinct tissues to those infecting the gut.…”

Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

“…It is worth noting that none of the considered effector genes show a change in expression after infection with Orsay virus (except downregulation of nlp-28). This may suggest that the protective cellular response to viral infection mainly depends on the RNAi pathway in C. elegans [8], or that other as yet uncharacterized effector mechanisms contribute to virus elimination. Similarly, infection by the other known intracellular pathogen N. parisii only represses but does not activate expression of the considered effector genes.…”

Section: Future Challenges: Functional Evidence For Worm Immune Effecmentioning

confidence: 99%

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Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Dierking

Yang

Schulenburg

2016

Phil. Trans. R. Soc. B

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One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Nematodes and arthropods likely form the taxon Ecdysozoa. Information on antimicrobial effectors from the model nematode Caenorhabditis elegans may thus shed light on the evolutionary origin of these defences in arthropods. This nematode species possesses an extensive armory of putative antimicrobial effector proteins, such as lysozymes, caenopores (or saposin-like proteins), defensin-like peptides, caenacins and neuropeptide-like proteins, in addition to the production of reactive oxygen species and autophagy. As C. elegans is a bacterivore that lives in microbe-rich environments, some of its effector peptides and proteins likely function in both digestion of bacterial food and pathogen elimination. In this review, we provide an overview of C. elegans immune effector proteins and mechanisms. We summarize the experimental evidence of their antimicrobial function and involvement in the response to pathogen infection. We further evaluate the microbe-induced expression of effector genes using WormExp, a recently established database for C. elegans gene expression analysis. We emphasize the need for further analysis at the protein level to demonstrate an antimicrobial activity of these molecules both in vitro and in vivo.This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

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Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

Section: Brief Overview Of the Caenorhabditis Elegans Immune Systemmentioning

confidence: 99%

Section: Future Challenges: Functional Evidence For Worm Immune Effecmentioning

confidence: 99%

See 1 more Smart Citation

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Dierking

Yang

Schulenburg

2016

Phil. Trans. R. Soc. B

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“…Genetic studies indicate that antiviral RNAi in C. elegans requires the genes essential for RNAi induced by exogenous dsRNA (12)(13)(14)(15)(16)(17). These include Dicer-1 and dsRNA-binding protein RDE-4 (RNA interference-deficient 4), involved in the biogenesis of primary siRNAs predominantly 23 nt in length, and Argonaute protein RDE-1 (RNA interference-deficient 1) and RNA-dependent RNA polymerase RRF-1, required for the production of secondary siRNAs (18)(19)(20)(21)(22).…”

mentioning

confidence: 99%

Homologous RIG-I–like helicase proteins direct RNAi-mediated antiviral immunity in C. elegans by distinct mechanisms

Guo

Zhang

Wang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

128

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RNAi-mediated antiviral immunity in Caenorhabditis elegans requires Dicer-related helicase 1 (DRH-1), which encodes the helicase and C-terminal domains homologous to the mammalian retinoic acid inducible gene I (RIG-I)-like helicase (RLH) family of cytosolic immune receptors. Here we show that the antiviral function of DRH-1 requires the RIG-I homologous domains as well as its wormspecific N-terminal domain. We also demonstrate that the helicase and C-terminal domains encoded by either worm DRH-2 or human RIG-I can functionally replace the corresponding domains of DRH-1 to mediate antiviral RNAi in C. elegans. Notably, substitutions in a three-residue motif of the C-terminal regulatory domain of RIG-I that physically interacts with viral double-stranded RNA abolish the antiviral activity of C-terminal regulatory domains of both RIG-I and DRH-1 in C. elegans. Genetic analysis revealed an essential role for both DRH-1 and DRH-3 in C. elegans antiviral RNAi targeting a natural viral pathogen. However, Northern blot and small RNA deep sequencing analyses indicate that DRH-1 acts to enhance production of viral primary siRNAs, whereas DRH-3 regulates antiviral RNAi by participating in the biogenesis of secondary siRNAs after Dicer-dependent production of primary siRNAs. We propose that DRH-1 facilitates the acquisition of viral double-stranded RNA by the worm dicing complex for the subsequent processing into primary siRNAs. The strong parallel for the antiviral function of RLHs in worms and mammals suggests that detection of viral doublestranded RNA may activate completely unrelated effector mechanisms or, alternatively, that the mammalian RLHs have a conserved activity to stimulate production of viral siRNAs for antiviral immunity by an RNAi effector mechanism.I nnate immunity refers to ancient host defense systems that act immediately after pathogen attack and are under the control of germline-encoded immune receptors. Pathogen sensing by several classes of immune receptors such as retinoic acid inducible gene I (RIG-I)-like cytosolic sensors in mammals leads to the transcriptional activation of effector genes in the nucleus (1). In contrast, detection of viral double-stranded RNA (dsRNA) by Dicer endonucleases is associated with the production of small interfering RNAs (siRNAs), which subsequently direct sequencespecific antiviral immunity through RNA interference (RNAi) (2-5). Antiviral RNAi is a major antiviral defense mechanism in fungi, plants, insects, and nematodes, so that suppression of the defense by a virus-encoded suppressor of RNAi is essential to establish infection (6-8). Although the RNAi machinery is highly conserved in mammals, conclusive evidence for a natural antiviral role of RNAi in mammals is not available (9).The nematode Caenorhabditis elegans has recently emerged as a small-animal model for innate immunity studies (10, 11). Genetic studies indicate that antiviral RNAi in C. elegans requires the genes essential for RNAi induced by exogenous dsRNA (12-17). These include Dicer-1 and dsRNA-bind...

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“…RNAi mutants, but not wild type worms, were shown to be susceptible to artificial viral replication [31][32][33], and recently RNAi-dependency was proven essential for resistance against a natural virus (the Orsay virus) as well [34]. Small RNAs targeting viral genomes (viRNA) accumulate in wild type infected worms, but not mutant worms [35,36].…”

Section: Inherited Anti-viral Immunitymentioning

confidence: 99%

Guest list or black list: heritable small RNAs as immunogenic memories

Rechavi

2014

Trends in Cell Biology

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Small RNA-mediated gene silencing plays a pivotal role in genome immunity by recognizing and eliminating viruses and transposons which otherwise may colonize the genome. However, this can be challenging since individual genomic parasites are highly diverse, and employ multiple immune evasion techniques. In this review, I discuss a new theory proposing that the integrity of the germline is maintained by transgenerationally-transmitted RNA "memories" that record ancestral gene expression patterns, and delineate "Self" from "Foreign" sequences. To maintain such recollection two tactics are employed in parallel: "black listing" of invading nucleic acids, and "guest listing" of endogenous genes. Studies in a number of organisms have shown that this memorization is used by the next generation small RNAs to act as "Inherited Vaccines" that ambush invading elements, or as "Inherited Licenses" that grant the transcription of autogenous sequences. KeywordsSmall RNA; Transgenerational Inheritance; Inherited Immunity; Self Vs. Non-Self; "Inherited Vaccines" Overview of transgenerational inheritanceEvolution progresses through an interplay between two major forces, selection and variation. Since the formulation of the Modern Synthesis the theory holds that the environment is limited in its contribution to the evolutionary course of action -it affects selection, but not the degree of variation [1,2]. However, recent discoveries in epigenetics suggest that the environment may influence variability as well [1]. If the parental environment is predictive of the conditions that the progeny will face (often for sessile or short-lived organisms), epigenetic responses can change the output of the encoded genetic information in an adaptive manner [3]. For example, the water flea Daphnia changes its normal developmental course and develops a "helmet" that protects it from predators, if it is born to a mother that survived a similar attack [4].Correspondence to: odedrechavi@gmail.com. Over the years, controversy surrounded the study of environmentally affected transgenerational inheritance. Today, an improved understanding of epigenetic mechanisms at the molecular level has provided a logical background to explain how, heretically, an adaptive acquired trait could become heritable [5]. Several epigenetic mechanisms could regulate the expression of relevant genes during transgenerational inheritance including DNA methylation, histone modification, and transmission of regulatory RNAs. Moreover, in many organisms, these pathways appear to be interconnected [5][6][7][8]. Europe PMC Funders GroupThis review will concentrate on recent discoveries that establish a role for small RNAs in transgenerational transmission of acquired defense. Furthermore, exciting examples of RNA-mediated non-Mendelian genetic effects will be discussed, along with their possible implications for the study of evolution and immunology. RNA-mediated gene silencing and inheritanceSince the original discovery that small RNAs derived from exogenously-provided dou...

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Natural and Experimental Infection of Caenorhabditis Nematodes by Novel Viruses Related to Nodaviruses

Abstract: Novel viruses have been discovered in wild Caenorahbditis nematode isolates and can now be used to explore host antiviral pathways, nematode ecology, and host-pathogen co-evolution.

Cited by 364 publications

References 37 publications

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Antimicrobial effectors in the nematode Caenorhabditis elegans : an outgroup to the Arthropoda

Homologous RIG-I–like helicase proteins direct RNAi-mediated antiviral immunity in C. elegans by distinct mechanisms

Guest list or black list: heritable small RNAs as immunogenic memories

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