Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection

Abstract Background Malaria remains to be one of the deadliest infectious diseases and imposes substantial financial and social costs in the world. Mosquitoes rely on the immune system to control parasite infection. Peptidoglycan recognition proteins (PGRPs), a family of pattern-recognition receptor...

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Main Authors: Li Gao, Xiumei Song, Jingwen Wang
Format: Article
Language:English
Published: BMC 2020-01-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-019-3876-y
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spelling doaj-eb1e5a42f3464a1fbd83e3211c36c7e72021-01-10T12:17:20ZengBMCParasites & Vectors1756-33052020-01-011311910.1186/s13071-019-3876-yGut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infectionLi Gao0Xiumei Song1Jingwen Wang2State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan UniversityState Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan UniversityState Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan UniversityAbstract Background Malaria remains to be one of the deadliest infectious diseases and imposes substantial financial and social costs in the world. Mosquitoes rely on the immune system to control parasite infection. Peptidoglycan recognition proteins (PGRPs), a family of pattern-recognition receptors (PRR), are responsible for initiating and regulating immune signaling pathways. PGRP-LA is involved in the regulation of immune defense against the Plasmodium parasite, however, the underlying mechanism needs to be further elucidated. Methods The spatial and temporal expression patterns of pgrp-la in Anopheles stephensi were analyzed by qPCR. The function of PGRP-LA was examined using a dsRNA-based RNA interference strategy. Western blot and periodic acid schiff (PAS) staining were used to assess the structural integrity of peritrophic matrix (PM). Results The expression of pgrp-la in An. stephensi was induced in the midgut in response to the rapid proliferating gut microbiota post-blood meal. Knocking down of pgrp-la led to the downregulation of immune effectors that control gut microbiota growth. The decreased expression of these immune genes also facilitated P. berghei infection. However, such dsLA treatment did not influence the structural integrity of PM. When gut microbiota was removed by antibiotic treatment, the regulation of PGRP-LA on immune effectors was abolished and the knock down of pgrp-la failed to increase susceptibility of mosquitoes to parasite infection. Conclusions PGRP-LA regulates the immune responses by sensing the dynamics of gut microbiota. A mutual interaction between gut microbiota and PGRP-LA contributes to the immune defense against Plasmodium parasites in An. stephensi.https://doi.org/10.1186/s13071-019-3876-yPGRP-LAGut microbiotaPeritrophic matrixImmune effectorsPlasmodium bergheiAnopheles stephensi
collection DOAJ
language English
format Article
sources DOAJ
author Li Gao
Xiumei Song
Jingwen Wang
spellingShingle Li Gao
Xiumei Song
Jingwen Wang
Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection
Parasites & Vectors
PGRP-LA
Gut microbiota
Peritrophic matrix
Immune effectors
Plasmodium berghei
Anopheles stephensi
author_facet Li Gao
Xiumei Song
Jingwen Wang
author_sort Li Gao
title Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection
title_short Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection
title_full Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection
title_fullStr Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection
title_full_unstemmed Gut microbiota is essential in PGRP-LA regulated immune protection against Plasmodium berghei infection
title_sort gut microbiota is essential in pgrp-la regulated immune protection against plasmodium berghei infection
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2020-01-01
description Abstract Background Malaria remains to be one of the deadliest infectious diseases and imposes substantial financial and social costs in the world. Mosquitoes rely on the immune system to control parasite infection. Peptidoglycan recognition proteins (PGRPs), a family of pattern-recognition receptors (PRR), are responsible for initiating and regulating immune signaling pathways. PGRP-LA is involved in the regulation of immune defense against the Plasmodium parasite, however, the underlying mechanism needs to be further elucidated. Methods The spatial and temporal expression patterns of pgrp-la in Anopheles stephensi were analyzed by qPCR. The function of PGRP-LA was examined using a dsRNA-based RNA interference strategy. Western blot and periodic acid schiff (PAS) staining were used to assess the structural integrity of peritrophic matrix (PM). Results The expression of pgrp-la in An. stephensi was induced in the midgut in response to the rapid proliferating gut microbiota post-blood meal. Knocking down of pgrp-la led to the downregulation of immune effectors that control gut microbiota growth. The decreased expression of these immune genes also facilitated P. berghei infection. However, such dsLA treatment did not influence the structural integrity of PM. When gut microbiota was removed by antibiotic treatment, the regulation of PGRP-LA on immune effectors was abolished and the knock down of pgrp-la failed to increase susceptibility of mosquitoes to parasite infection. Conclusions PGRP-LA regulates the immune responses by sensing the dynamics of gut microbiota. A mutual interaction between gut microbiota and PGRP-LA contributes to the immune defense against Plasmodium parasites in An. stephensi.
topic PGRP-LA
Gut microbiota
Peritrophic matrix
Immune effectors
Plasmodium berghei
Anopheles stephensi
url https://doi.org/10.1186/s13071-019-3876-y
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AT xiumeisong gutmicrobiotaisessentialinpgrplaregulatedimmuneprotectionagainstplasmodiumbergheiinfection
AT jingwenwang gutmicrobiotaisessentialinpgrplaregulatedimmuneprotectionagainstplasmodiumbergheiinfection
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