Rhodnius prolixus uses the peptidoglycan recognition receptor rpPGRP-LC/LA to detect Gram-negative bacteria and activate the IMD pathway

Salcedo-Porras, Nicolás; Noor, Shireen; Cai, Charley; Oliveira, Pedro L.; Lowenberger, Carl

doi:10.1016/j.cris.2020.100006

Cited by 15 publications

(25 citation statements)

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“…These events culminate in the translocation of the NF-κΒ transcription factor Relish into the nucleus, where it induces the transcription of AMPs and initiates other immune responses [19]. In R. prolixus, the IMD pathway was originally described as being incomplete or non-functional [3], but most of its "missing" genes were identified in subsequent studies [26][27][28]. These studies also showed that the IMD pathway in R. prolixus regulates responses to Gr-bacteria and potentially Gr+ bacteria [26,27].…”

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confidence: 99%

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A fat body transcriptome analysis of the immune responses of Rhodnius prolixus to artificial infections with bacteria

Salcedo-Porras

Oliveira

Guarneri³

et al. 2022

Parasites Vectors

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Background Rhodnius prolixus is an important vector of Trypanosoma cruzi, the causal agent of Chagas disease in humans. Despite the medical importance of this and other triatomine vectors, the study of their immune responses has been limited to a few molecular pathways and processes. Insect immunity studies were first described for holometabolous insects such as Drosophila melanogaster, and it was assumed that their immune responses were conserved in all insects. However, study of the immune responses of triatomines and other hemimetabolous insects has revealed discrepancies between these and the Drosophila model. Methods To expand our understanding of innate immune responses of triatomines to pathogens, we injected fifth instar nymphs of R. prolixus with the Gram-negative (Gr−) bacterium Enterobacter cloacae, the Gram-positive (Gr+) bacterium Staphylococcus aureus, or phosphate-buffered saline (PBS), and evaluated transcript expression in the fat body 8 and 24 h post-injection (hpi). We analyzed the differential expression of transcripts at each time point, and across time, for each treatment. Results At 8 hpi, the Gr− bacteria-injected group had a large number of differentially expressed (DE) transcripts, and most of the changes in transcript expression were maintained at 24 hpi. In the Gr+ bacteria treatment, few DE transcripts were detected at 8 hpi, but a large number of transcripts were DE at 24 hpi. Unexpectedly, the PBS control also had a large number of DE transcripts at 24 hpi. Very few DE transcripts were common to the different treatments and time points, indicating a high specificity of the immune responses of R. prolixus to different pathogens. Antimicrobial peptides known to be induced by the immune deficiency pathway were induced upon Gr− bacterial infection. Many transcripts of genes from the Toll pathway that are thought to participate in responses to Gr+ bacteria and fungi were induced by both bacteria and PBS treatment. Pathogen recognition receptors and serine protease cascade transcripts were also overexpressed after Gr− bacteria and PBS injections. Gr- injection also upregulated transcripts involved in the metabolism of tyrosine, a major substrate involved in the melanotic encapsulation response to pathogens. Conclusions These results reveal time-dependent pathogen-specific regulation of immune responses in triatomines, and hint at strong interactions between the immune deficiency and Toll pathways. Graphical abstract

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confidence: 99%

“…In R. prolixus, the IMD pathway was originally described as being incomplete or non-functional [3], but most of its "missing" genes were identified in subsequent studies [26][27][28]. These studies also showed that the IMD pathway in R. prolixus regulates responses to Gr-bacteria and potentially Gr+ bacteria [26,27].…”

mentioning

confidence: 99%

A fat body transcriptome analysis of the immune responses of Rhodnius prolixus to artificial infections with bacteria

Salcedo-Porras

Oliveira

Guarneri³

et al. 2022

Parasites Vectors

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“…It was previously reported that in R. prolixus , the inhibition of pgrp-lc-la decreased the expression of defensin B , lysozyme B , and prolixicin transcripts (IMD-regulated) after a challenge with E. coli , but no effect was observed after a challenge with Gram-positive bacteria ( Staphylococcus carnosus ) [ 36 ], suggesting that there was specificity in the immune pathway activation. However, we found that in T. pallidipennis challenged with E. coli , silencing of Tp pgrp-lc resulted in decreased expression of AMP transcripts regulated by the IMD pathway, but it also produced a reduction in expression of defensin B , lysozyme B , and prolixicin transcripts after a challenge with M. luteus, suggesting that isoforms of Tp pgrp-lc could participate specifically in response to Gram-positive bacteria.…”

Section: Discussionmentioning

confidence: 99%

“…However, several components of the Imd cascade, including the IMD protein, appear to be absent or incomplete in these insects [ 33 , 35 ], and this absence appears to be a common feature in insects with incomplete metamorphosis [ 35 ]. Despite the absence of key mediators, it has been documented in Rhodnius prolixus that the IMD pathway principally regulates AMP expression against Gram-negative, but also against Gram-positive bacteria [ 36 ], which suggests that in triatomines, the generation of AMPs may not follow the canonical IMD and Toll pathway activation.…”

Section: Introductionmentioning

confidence: 99%

“…Ortholog molecules associated with the IMD and Toll pathways, their corresponding pattern-recognition receptors (PRRs) such as pgrp-lc and pgrp-la, and AMPs have been identified in various triatomine species [32][33][34][35][36]. However, several components of the Imd cascade, including the IMD protein, appear to be absent or incomplete in these insects [33,35], and this absence appears to be a common feature in insects with incomplete metamorphosis [35].…”

Section: Introductionmentioning

confidence: 99%

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The IMD and Toll canonical immune pathways of Triatoma pallidipennis are preferentially activated by Gram-negative and Gram-positive bacteria, respectively, but cross-activation also occurs

et al. 2022

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Background Antimicrobial peptides (AMPs) participate in the humoral immune response of insects eliminating invasive microorganisms. The immune deficiency pathway (IMD) and Toll are the main pathways by which the synthesis of these molecules is regulated in response to Gram-negative (IMD pathway) or Gram-positive (Toll pathway) bacteria. Various pattern-recognition receptors (PRRs) participate in the recognition of microorganisms, such as pgrp-lc and toll, which trigger signaling cascades and activate NF-κB family transcription factors, such as relish, that translocate to the cell nucleus, mainly in the fat body, inducing AMP gene transcription. Methods T. pallidipennis inhibited in Tppgrp-lc, Tptoll, and Tprelish were challenged with E. coli and M. luteus to analyze the expression of AMPs transcripts in the fat body and to execute survival assays. Results In this work we investigated the participation of the pgrp-lc and toll receptor genes and the relish transcription factor (designated as Tppgrp-lc, Tptoll, and Tprelish), in the transcriptional regulation of defensin B, prolixicin, and lysozyme B in Triatoma pallidipennis, one of the main vectors of Chagas disease. AMP transcript abundance was higher in the fat body of blood-fed than non-fed bugs. Challenge with Escherichia coli or Micrococcus luteus induced differential increases in AMP transcripts. Additionally, silencing of Tppgrp-lc, Tptoll, and Tprelish resulted in reduced AMP transcription and survival of bugs after a bacterial challenge. Conclusions Our findings demonstrated that the IMD and Toll pathways in T. pallidipennis preferentially respond to Gram-negative and Gram-positive bacteria, respectively, by increasing the expression of AMP transcripts, but cross-induction also occurs. Graphical Abstract

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Time- and tissue-specific antimicrobial activity of the common bed bug in response to blood feeding and immune activation by bacterial injection

Meraj

Mohr

Ketabchi

et al. 2021

Journal of Insect Physiology

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Rhodnius prolixus uses the peptidoglycan recognition receptor rpPGRP-LC/LA to detect Gram-negative bacteria and activate the IMD pathway

Cited by 15 publications

References 88 publications

A fat body transcriptome analysis of the immune responses of Rhodnius prolixus to artificial infections with bacteria

A fat body transcriptome analysis of the immune responses of Rhodnius prolixus to artificial infections with bacteria

The IMD and Toll canonical immune pathways of Triatoma pallidipennis are preferentially activated by Gram-negative and Gram-positive bacteria, respectively, but cross-activation also occurs

Time- and tissue-specific antimicrobial activity of the common bed bug in response to blood feeding and immune activation by bacterial injection

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