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The extraembryonic serosa is a frontier epithelium providing the insect egg with a full-range innate immune response

ABSTRACT: Drosophila larvae and adults possess a potent innate immune response, but the response of their eggs is particularly poor. Here we show that eggs of the beetle Tribolium castaneum, in contrast, possess a full range of immune defence mechanisms, based on complete transcriptome comparisons of naïve, sterilely injured, and bacterially challenged eggs. Upon infection, we find massive upregulation of AMPs and differential regulation of 375 other genes including both IMD and Toll signalling components. Importantly, we show that this extensive response depends on the serosa, an extraembryonic epithelium enveloping yolk and embryo. When we delete the serosa using Tc-zen1 RNAi, none of the AMPs and merely 57 other genes are differentially regulated upon infection. Furthermore, unchallenged eggs reveal serosa-biased expression of several bacterial recognition genes. Thus, the serosa is an immune competent frontier epithelium, and its loss in higher flies might account for the poor immune response of Drosophila eggs.

ORGANISM(S): Tribolium castaneum

PROVIDER: GSE54018 | GEO | 2014/12/09

SECONDARY ACCESSION(S): PRJNA234363

REPOSITORIES: GEO

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The extraembryonic serosa is a frontier epithelium providing the insect egg with a full-range innate immune response

Project description:Drosophila larvae and adults possess a potent innate immune response, but the response of their eggs is particularly poor. Here we show that eggs of the beetle Tribolium castaneum, in contrast, possess a full range of immune defence mechanisms, based on complete transcriptome comparisons of naÃ¯ve, sterilely injured, and bacterially challenged eggs. Upon infection, we find massive upregulation of AMPs and differential regulation of 375 other genes including both IMD and Toll signalling components. Importantly, we show that this extensive response depends on the serosa, an extraembryonic epithelium enveloping yolk and embryo. When we delete the serosa using Tc-zen1 RNAi, none of the AMPs and merely 57 other genes are differentially regulated upon infection. Furthermore, unchallenged eggs reveal serosa-biased expression of several bacterial recognition genes. Thus, the serosa is an immune competent frontier epithelium, and its loss in higher flies might account for the poor immune response of Drosophila eggs. Three different types of eggs were analysed. Wildtype eggs, eggs of which the mother was injected with a control dsRNA, and eggs without a serosa of which the mothers were injected with Tc-zen1 dsRNA. These three egg-types were subjected to three treatments, untreated (naÃ¯ve), pricked with a sterile needle (sterile injury) and pricked with a mix of E.coli and M.luteus. This resulted in 9 samples which were all collected three times resulting in a total of 27 samples.

2014-12-09 | E-GEOD-54018 | biostudies-arrayexpress

Immune function of the serosa in a hemimetabolous insect egg

Project description:The unparalleled success of the insects comprising more than a million species has long stood out to evolutionary biologists. A much overlooked evolutionary innovation of the insects is the serosa, an extraembryonic epithelium that covers yolk and embryo in their eggs. We have shown that this epithelium provides innate immune protection to eggs of the beetle Tribolium castaneum. It remained elusive, however, if this innate immune competence evolved in the Tribolium lineage, or is ancestral to all insects. Here, we expand our studies to the bug Oncopeltus fasciatus that belongs to the basal main group of insects, the Hemimetabola. RNA sequencing reveals an extensive transcriptional response upon infection of the egg with Gram-positive and Gram-negative bacteria. We demonstrate the antimicrobial activity of upregulated peptides using in vitro bacterial growth inhibition assays, and describe two novel families of AMPs called Serosins and Ovicins. By qPCR, we determine that eggs become immune responsive when the serosa develops. Finally, in situ hybridizations show that transcripts of upregulated peptides are located in the serosal cells and not in the underlying embryo. We conclude that the serosa protects the O. fasciatus embryo against pathogens. This first evidence from hemimetabolous insect eggs suggests that immune competence is an ancestral property of the serosa. The evolutionary origin of the serosa with its immune function might have been one of the factors that facilitated the spectacular success of the insects.

2019-01-01 | GSE100429 | GEO

Tribolium castaneum

Project description:The extraembryonic serosa is a frontier epithelium providing the insect egg with a full-range innate immune response

| PRJNA234363 | ENA

Dengue virus inhibits immune responses in Aedes aegypti cells

Project description:The ability of many viruses to manipulate the host antiviral immune response often results in complex host-pathogen interactions. In order to study the interaction of dengue virus (DENV) with the Aedes aegypti immune response, we have characterized the DENV infection-responsive transcriptome of the immune-competent A. aegypti cell line Aag2. As in mosquitoes, DENV infection transcriptionally activated the cell line Toll pathway and a variety of cellular physiological systems. Most notably, however, DENV infection down-regulated the expression levels of numerous immune signaling molecules and antimicrobial peptides (AMPs). Functional assays showed that transcriptional induction of AMPs from the Toll and IMD pathways in response to bacterial challenge is impaired in DENV-infected cells. In addition, Escherichia coli, a gram-negative bacteria species, grew better when co-cultured with DENV-infected cells than with uninfected cells, suggesting a decreased production of AMPs from the IMD pathway in virus-infected cells. Pre-stimulation of the cell line with gram-positive bacteria prior to DENV infection had no effect on DENV titers, while pre-stimulation with gram-negative bacteria resulted in an increase in DENV titers. These results indicate that DENV is capable of actively suppressing immune responses in the cells it infects, a phenomenon that may have important consequences for virus transmission and insect physiology. Infected (dengue virus or heat-inactivated dengue virus) vs. naive cells. 3 replicates each.

2011-10-31 | E-GEOD-33274 | biostudies-arrayexpress

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16S V3-V4 -based microbial profiling of matched healthy and inflamed ileal mucosa from patients affected by Crohn’s disease

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Regulation of Antimicrobial Peptides in Hermetia illucens in Response to Fungal Exposure

Project description:The black soldier fly (Hermetia illucens) is important in antimicrobial peptides (AMP) research due to its exposure to diverse microbial environments. However, the impact of different fungal exposures on AMP abundance in H. illucens has not been thoroughly explored. Our study focused on basal conditions and interactions with three fungi: the non-pathogenic Candida tropicalis (isolated from larval gut), Saccharomyces cerevisiae, and the pathogenic Beauveria bassiana. Using RNA-seq and LC-MS/MS, we found that under standard conditions, the majority of AMPs belonged to the Lysozyme, Cecropin, and Defensin classes, with Defensins exhibiting the highest quantification levels. Exposure to any of the fungi upregulated AMP gene expression, indicating immune activation. Notably, exposure to C. tropicalis and B. bassiana led to notable downregulation of AMPs in H. illucens larvae compared to S. cerevisiae, suggesting these fungi may suppress or modulate the host immune response to aid their survival and colonization. The immune response of H. illucens larvae revealed that S. cerevisiae and B. bassiana trigger similar AMP pathways, whereas C. tropicalis elicits a distinct response with upregulation of Defensins and Cecropins. Lysozymes, known for their antibacterial and antifungal activity, were upregulated in response to S. cerevisiae and B. bassiana, but downregulated with C. tropicalis, potentially facilitating fungal survival in the larvae’s gut. This suggests that C. tropicalis adapts to reduce immune pressure, while B. bassiana may suppress AMPs to persist. Understanding these mechanisms opens possibilities for leveraging AMPs in combating C. tropicalis, which is implicated in human diseases.

2024-11-19 | GSE272202 | GEO

Dengue virus inhibits immune responses in Aedes aegypti cells

2011-10-31 | GSE33274 | GEO

Anti-tumor effects of antimicrobial peptides, targets of the innate immune system, against hematopoietic tumors in Drosophila mxc mutants

Project description:The innate immune response is the first line of defence against microbial infections. In Drosophila, two major immune pathways induce the synthesis of antimicrobial peptides (AMPs) in the fat body. Recently, it has been reported that certain cationic AMPs exhibit selective cytotoxicity against human cancer cells. However, not much is known about their anti-tumour effects. Drosophila mxc(mbn1) mutants exhibit malignant hyperplasia in a larval haematopoietic organ called the lymph gland (LG). Here, using RNA-Seq analysis, we found that many immunoresponsive genes, including AMP genes, were up-regulated in the mutants. Down-regulation of these pathways by either a Toll or an imd mutation enhanced the tumour phenotype of the mxc mutants. Conversely, ectopic expression of each of five different AMPs in the fat body significantly suppressed the LG hyperplasia phenotype in the mutants. Thus, we propose that the Drosophila innate immune system can suppress the progression of haematopoietic tumours by inducing AMP gene expression. Overexpression of any one of these five AMPs resulted in enhanced apoptosis in the mutant LGs, while no apoptotic signals were detected in the controls. We observed that two AMPs, Drosomycin and Defensin, were taken up by circulating haemocyte-like cells, which were associated with the LG regions showing reduced cell-to-cell adhesion in the mutants. On the other hand, another AMP, Diptericin, was directly localised at the tumour site without intermediating haemocytes. These results indicate that AMPs have a specific cytotoxic effect that enhance apoptosis exclusively in the tumour cells.

2019-06-12 | GSE121551 | GEO

Transcription profiling by array of E. coli NCTC 9001 challenged with four different cationic antimicrobial peptides

Project description:Obtaining an in depth understanding of the arms races between peptides comprising the innate immune response and bacterial pathogens is of fundamental interest and will inform the development of new antibacterial therapeutics. Many cationic antimicrobial peptides (AMPs) share a range of structural and physical features that have been linked to antibacterial activity and yet they vary dramatically in their potency towards the same bacterial target. We hypothesised that a whole organism view of AMP challenge on Escherichia coli could provide a sophisticated, bacterial perspective enabling understanding of how potency is linked to mode of action. We used a 1H NMR metabolomic approach to characterise the effect on E. coli of challenge with four structurally and physically related AMPs: magainin 2, pleurocidin, buforin II and a designed peptide comprising D-amino acids only. Sub-inhibitory conditions, where these peptides nevertheless induced a bacterial response, were identified enabling electron microscopic and transcriptomic analyses. Although some common features of the bacterial response to AMP challenge could be identified, the metabolomes, morphological changes and the vast majority of the changes in gene expression were specific to each AMP. We show the antibacterial mode of action of AMPs can be accurately predicted by comparing ontological profiles generated by transcriptomic analyses. The response of E. coli to AMP challenge is highly plastic, with the bacteria capable of deploying a multifaceted response adapted to the mode of action rather than the physical properties of the AMP.

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