Variation in the Susceptibility of Drosophila to Different Entomopathogenic Nematodes

Peña, Jennifer M; Carrillo, Mayra A.; Hallem, Elissa A.

doi:10.1128/iai.02740-14

Cited by 55 publications

(59 citation statements)

References 59 publications

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“…The H. bacteriophora infective juvenile stage is the only stage that is able tosurvive outside of the host and isrequired for insect infection (Ciche et al, 2006). Previous and recent work has demonstrated the power of using D. melanogaster for studying the molecular/genetic basis of insect immune responses against infections by entomopathogenic nematodes (Hallem et al, 2007; Wang et al, 2010; Hyrsl et al, 2011; Dobes et al, 2012; Castillo et al, 2012, 2013; Arefin et al, 2014, 2015; Peña et al, 2015; Kucerova et al, 2016). …”

Section: Introductionmentioning

confidence: 99%

TGF-β signaling regulates resistance to parasitic nematode infection in Drosophila melanogaster

2016

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Over the past decade important advances have been made in the field of innate immunity; however, our appreciation of the signaling pathways and molecules that participate in host immune responses to parasitic nematode infections lags behind that of responses to microbial challenges. Here we have examined the regulation and immune activity of Transforming Growth Factor-beta (TGF-β) signaling in the model host Drosophila melanogaster upon infection with the nematode parasites Heterorhabditis gerrardi and H. bacteriophora containing their mutualistic bacteria Photorhabdus. We have found that the genes encoding the Activin and Bone Morphogenic Protein (BMP) ligands Dawdle (Daw) and Decapentaplegic (Dpp) are transcriptionally induced in flies responding to infection with the nematode parasites, containing or lacking their associated bacteria. We also show that deficient Daw or Dpp regulates the survival of D. melanogaster adults to the pathogens, whereas inactivation of Daw reduces the persistence of the nematodes in the mutant flies. These findings demonstrate a novel role for the TGF-β signaling pathways in the host anti-nematode immune response. Understanding the molecular mechanisms of host anti-nematode processes will potentially lead to the development of novel means for the efficient control of parasitic nematodes.

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Section: Introductionmentioning

confidence: 99%

TGF-β signaling regulates resistance to parasitic nematode infection in Drosophila melanogaster

2016

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“…Steinernema carpocapsae nematodes mutualistically associate with the Gram-negative bacteria Xenorhabdus nematophila to invade and kill insects (Peña et al 2015). These nematodes cause infections at the infective juvenile (IJ) stage, which is the developmentally-arrested third larval stage analogous to the dauer stage of the nonpathogenic nematode Caenorhabditis elegans (Goodrich-Blair 2007).…”

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confidence: 99%

“…Therefore, S. carpocapsae can be used to explore the interplay between certain aspects of the insect immune response and nematode parasitism strategies (Castillo et al 2011; Peña et al 2015). In a previous microarray study, the transcriptome of D. melanogaster larvae infected with H. bacteriophora nematodes was analyzed.…”

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confidence: 99%

RNAseq Analysis of theDrosophilaResponse to the Entomopathogenic NematodeSteinernema

Yadav

Daugherty

Shetty

et al. 2017

G3 Genes|Genomes|Genetics

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Drosophila melanogaster is an outstanding model to study the molecular and functional basis of host–pathogen interactions. Currently, our knowledge of microbial infections in D. melanogaster is well understood; however, the response of flies to nematode infections is still in its infancy. Here, we have used the potent parasitic nematode Steinernema carpocapsae, which lives in mutualism with its endosymbiotic bacteria Xenorhabdus nematophila, to examine the transcriptomic basis of the interaction between D. melanogaster and entomopathogenic nematodes. We have employed next-generation RNA sequencing (RNAseq) to investigate the transcriptomic profile of D. melanogaster larvae in response to infection by S. carpocapsae symbiotic (carrying X. nematophila) or axenic (lacking X. nematophila) nematodes. Bioinformatic analyses have identified the strong induction of genes that are associated with the peritrophic membrane and the stress response, as well as several genes that participate in developmental processes. We have also found that genes with different biological functions are enriched in D. melanogaster larvae responding to either symbiotic or axenic nematodes. We further show that while symbiotic nematode infection enriched certain known immune-related genes, axenic nematode infection enriched several genes associated with chitin binding, lipid metabolic functions, and neuroactive ligand receptors. In addition, we have identified genes with a potential role in nematode recognition and genes with potential antinematode activity. Findings from this study will undoubtedly set the stage for the identification of key regulators of antinematode immune mechanisms in D. melanogaster, as well as in other insects of socioeconomic importance.

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“…However, since X. nematophila inhibits the expression of genes encoding AMPs in lepidopterans (3,4,20) but not D. melanogaster insects (21,22), it appears that X. nematophila targets a step in AMP induction that is present in Lepidoptera but not D. melanogaster. Alternatively, since X. nematophila kills D. melanogaster flies despite its inability to suppress immunity (21), it may be that X. nematophila toxicity is sufficiently powerful to negate the need for immune suppression in this insect.…”

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confidence: 99%

The Global Transcription Factor Lrp Is both Essential for and Inhibitory to Xenorhabdus nematophila Insecticidal Activity

Casanova-Torres

Shokal

Morag

et al. 2017

Appl Environ Microbiol

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In the entomopathogenic bacterium Xenorhabdus nematophila, cell-tocell variation in the abundance of the Lrp transcription factor leads to virulence modulation; low Lrp levels are associated with a virulent phenotype and suppression of antimicrobial peptides (AMPs) in Manduca sexta insects, while cells that lack lrp or express high Lrp levels are virulence attenuated and elicit AMP expression. To better understand the basis of these phenotypes, we examined X. nematophila strains expressing fixed Lrp levels. Unlike the lrp-null mutant, the high-lrp strain is fully virulent in Drosophila melanogaster, suggesting that these two strains have distinct underlying causes of virulence attenuation in M. sexta. Indeed, the lrp-null mutant was defective in cytotoxicity against M. sexta hemocytes relative to that in the high-lrp and low-lrp strains. Further, supernatant derived from the lrp-null mutant but not from the high-lrp strain was defective in inhibiting weight gain when fed to 1st instar M. sexta. These data suggest that contributors to the lrp-null mutant virulence attenuation phenotype are the lack of Lrp-dependent cytotoxic and extracellular oral growth inhibitory activities, which may be particularly important for virulence in D. melanogaster. In contrast, the high-Lrp strain was sensitive to the antimicrobial peptide cecropin, had a transient survival defect in M. sexta, and had reduced extracellular levels of insecticidal activity, measured by injection of supernatant into 4th instar M. sexta. Thus, high-lrp strain virulence attenuation may be explained by its hypersensitivity to M. sexta host immunity and its inability to secrete one or more insecticidal factors.IMPORTANCE Adaptation of a bacterial pathogen to host environments can be achieved through the coordinated regulation of virulence factors that can optimize success under prevailing conditions. In the insect pathogen Xenorhabdus nematophila, the global transcription factor Lrp is necessary for virulence when injected into Manduca sexta or Drosophila melanogaster insect hosts. However, high levels of Lrp, either naturally occurring or artificially induced, cause attenuation of X. nematophila virulence in M. sexta but not D. melanogaster. Here, we present evidence suggesting that the underlying cause of high-Lrp-dependent virulence attenuation in M. sexta is hypersensitivity to host immune responses and decreased insecticidal activity and that high-Lrp virulence phenotypes are insect host specific. This knowledge suggests that X. nematophila faces varied challenges depending on the type of insect host it infects and that its success in these environments depends on Lrp-dependent control of a multifactorial virulence repertoire.

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Variation in the Susceptibility of Drosophila to Different Entomopathogenic Nematodes

Cited by 55 publications

References 59 publications

TGF-β signaling regulates resistance to parasitic nematode infection in Drosophila melanogaster

TGF-β signaling regulates resistance to parasitic nematode infection in Drosophila melanogaster

RNAseq Analysis of theDrosophilaResponse to the Entomopathogenic NematodeSteinernema

The Global Transcription Factor Lrp Is both Essential for and Inhibitory to Xenorhabdus nematophila Insecticidal Activity

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