Wounding-induced upregulation of the Bone Morphogenic Protein signaling pathway in Drosophila promotes survival against parasitic nematode infection

Patrnogic, Jelena; Heryanto, Christa; Eleftherianos, Ioannis

doi:10.1016/j.gene.2018.06.052

Cited by 10 publications

(9 citation statements)

References 24 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…On the other hand, 3 signaling genes were found to be strictly down-regulated (Fig 1D). Interestingly, these genes included a member of the TGF-β pathway (BAMBI-like) in the hemocytes and a member of the JNK pathway in the fat body (Basket), two pleiotropic pathways that are currently suspected to take a part in the D. melanogaster immune response to nematodes after NBC infestation (47, 99–101). The third down-regulated gene was found in the fat body and encoded MASK, an inducer of the Jak/Stat pathway (102).…”

Section: Resultsmentioning

confidence: 99%

Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

Huot

Bigourdan

Pagès

et al. 2019

Preprint

View full text Add to dashboard Cite

13The Steinernema carpocapsae-Xenorhabdus nematophila association is a nematobacterial complex (NBC) 14 used in biological control of insect crop pests. The ability of this dual pathogen to infest and kill an insect 15 strongly depends on the dialogue between the host's immune system and each partner of the complex. Even 16 though this dialogue has been extensively studied from the two partners' points of view in several insect 17 models, still little is known about the structure and the molecular aspects of the insects' immune response 18 to the dual infection. Here, we used the lepidopteran pest Spodoptera frugiperda as a model to analyze the 19 respective impact of each NBC partner in the spatiotemporal immune responses that are induced after 20 infestation. To this aim, we first analyzed the expression variations of the insect's immune genes in the fat 21 bodies and hemocytes of infested larvae by using previously obtained RNAseq data. We then selected 22 representative immune genes for RT-qPCR investigations of the temporal variations of their expressions 23 after infestation and of their induction levels after independent injections of each partner. We found that 24 the fat body and the hemocytes both produce potent and stable immune responses to the infestation by the 25 NBC, which correspond to combinations of bacterium-and nematode-induced ones. Consistent with the 26 nature of each pathogen, we showed that X. nematophila mainly induces genes classically involved in 27 antibacterial responses, whereas S. carpocapsae is responsible for the induction of lectins and of genes 28 expected to be involved in melanization and cellular encapsulation. In addition, we found that two clusters 29 of unknown genes dramatically induced by the NBC also present partner-specific induction profiles, which 30 paves the way for their functional characterization. Finally, we discuss putative relationships between the 31 variations of the expression of some immune genes and the NBC's immunosuppressive strategies. 32 3 33Author summary 34 Entomopathogenic nematodes (EPNs) are living in the soil and prey upon insect larvae. They enter the 35 insect by the natural orifices, and reach the hemocoel through the intestinal epithelium. There, they release 36 their symbiotic bacteria that will develop within the insect and eventually kill it. Nematodes can then feed 37 and reproduce on the insect cadaver. By using transcriptomic approaches, we previously showed that 38 Lepidoptera larvae (caterpillars of the fall armyworm Spodoptera frugiperda) produce a strong immune 39 response in reaction to infestation by EPNs. However, we do not know if this immune reaction is triggered 40 by the nematode itself -Steinernema carpacapsae -or its symbiotic bacteria -Xenorhabdus nematophila. 41 To answer this question, we present in this work a careful annotation of immunity genes in S. frugiperda 42 and surveyed their activation by quantitative PCR in reaction to an injection of the bacteria alone, the axenic 43 nematode or the ...

show abstract

Section: Resultsmentioning

confidence: 99%

Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

Huot

Bigourdan

Pagès

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…iTaq Univer SYBR Green (Bio-Rad) was used for quantitative real-time polymerase chain reaction (qRT-PCR) analysis using CFX96 Real-Time System, C1000 Thermal Cycler and the following conditions: 95°C for 2 min, 40 cycles of 95°C for 15 sec and 61°C for 30 sec, 95°C for 15 sec, 65°C for 5 sec and 95°C for 5 sec. Primer sets included RpL32FW , RpL32RV ( RpL32 ); DptFW , DptRV ( Diptericin A ); DrsFW , DrsRV ( Drosomycin ) [ 33 ]. Three biological replicates were included per treatment and each biological replicate was analysed in technical duplicates.…”

Section: Methodsmentioning

confidence: 99%

Pre-exposure to non-pathogenic bacteria does not protect Drosophila against the entomopathogenic bacterium Photorhabdus

et al. 2018

Self Cite

View full text Add to dashboard Cite

Immune priming in insects involves an initial challenge with a non-pathogenic microbe or exposure to a low dose of pathogenic microorganisms, which provides a certain degree of protection against a subsequent pathogenic infection. The protective effect of insect immune priming has been linked to the activation of humoral or cellular features of the innate immune response during the preliminary challenge, and these effects might last long enough to promote the survival of the infected animal. The fruit fly Drosophila melanogaster is a superb model to dissect immune priming processes in insects due to the availability of molecular and genetic tools, and the comprehensive understanding of the innate immune response in this organism. Previous investigations have indicated that the D. melanogaster immune system can be primed efficiently. Here we have extended these studies by examining the result of immune priming against two potent entomopathogenic bacteria, Photorhabdus luminescens and P. asymbiotica. We have found that rearing D. melanogaster on diet containing a non-pathogenic strain of Escherichia coli alone or in combination with Micrococcus luteus upregulates the antibacterial peptide immune response in young adult flies, but it does not prolong fly life span. Also, subsequent intrathoracic injection with P. luminescens or P. asymbiotica triggers the Immune deficiency and Toll signaling pathways in flies previously exposed to a live or heat-killed mix of the non-pathogenic bacteria, but the immune activation fails to promote fly survival against the pathogens. These findings suggest that immune priming in D. melanogaster, and probably in other insects, is determined by the type of microbes involved as well as the mode of microbial exposure, and possibly requires a comprehensive and precise alteration of immune signaling and function to provide efficient protection against pathogenic infection.

show abstract

“…In addition to its contribution to wounding response and anti-bacterial immunity, the role of TGF-ß signaling has been implicated in anti-nematode immunity in D. melanogaster (10)(11)(12)(13)(14). In particular, gene transcript levels of the ligands Daw (activin branch) and Dpp (BMP branch) are upregulated following infection with the parasitic nematodes, Heterorhabditis gerrardi and Heterorhabditis bacteriophora in adult flies (12).…”

Section: Introductionmentioning

confidence: 99%

Activin and BMP Signaling Activity Affects Different Aspects of Host Anti-Nematode Immunity in Drosophila melanogaster

2021

Self Cite

View full text Add to dashboard Cite

The multifaceted functions ranging from cellular and developmental mechanisms to inflammation and immunity have rendered TGF-ß signaling pathways as critical regulators of conserved biological processes. Recent studies have indicated that this evolutionary conserved signaling pathway among metazoans contributes to the Drosophila melanogaster anti-nematode immune response. However, functional characterization of the interaction between TGF-ß signaling activity and the mechanisms activated by the D. melanogaster immune response against parasitic nematode infection remains unexplored. Also, it is essential to evaluate the precise effect of entomopathogenic nematode parasites on the host immune system by separating them from their mutualistic bacteria. Here, we investigated the participation of the TGF-ß signaling branches, activin and bone morphogenetic protein (BMP), to host immune function against axenic or symbiotic Heterorhabditis bacteriophora nematodes (parasites lacking or containing their mutualistic bacteria, respectively). Using D. melanogaster larvae carrying mutations in the genes coding for the TGF-ß extracellular ligands Daw and Dpp, we analyzed the changes in survival ability, cellular immune response, and phenoloxidase (PO) activity during nematode infection. We show that infection with axenic H. bacteriophora decreases the mortality rate of dpp mutants, but not daw mutants. Following axenic or symbiotic H. bacteriophora infection, both daw and dpp mutants contain only plasmatocytes. We further detect higher levels of Dual oxidase gene expression in dpp mutants upon infection with axenic nematodes and Diptericin and Cecropin gene expression in daw mutants upon infection with symbiotic nematodes compared to controls. Finally, following symbiotic H. bacteriophora infection, daw mutants have higher PO activity relative to controls. Together, our findings reveal that while D. melanogaster Dpp/BMP signaling activity modulates the DUOX/ROS response to axenic H. bacteriophora infection, Daw/activin signaling activity modulates the antimicrobial peptide and melanization responses to axenic H. bacteriophora infection. Results from this study expand our current understanding of the molecular and mechanistic interplay between nematode parasites and the host immune system, and the involvement of TGF-ß signaling branches in this process. Such findings will provide valuable insight on the evolution of the immune role of TGF-ß signaling, which could lead to the development of novel strategies for the effective management of human parasitic nematodes.

show abstract

Wounding-induced upregulation of the Bone Morphogenic Protein signaling pathway in Drosophila promotes survival against parasitic nematode infection

Cited by 10 publications

References 24 publications

Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

Partner-specific induction ofSpodoptera frugiperdaimmune genes in response to the entomopathogenic nematobacterial complexSteinernema carpocapsae-Xenorhabdus nematophila

Pre-exposure to non-pathogenic bacteria does not protect Drosophila against the entomopathogenic bacterium Photorhabdus

Activin and BMP Signaling Activity Affects Different Aspects of Host Anti-Nematode Immunity in Drosophila melanogaster

Contact Info

Product

Resources

About