An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection

BackgroundWe seek to provide a comprehensive overview of transcriptomics responses of immune-related features of the gastropod Biomphalaria glabrata (Bg) following exposure to Schistosoma mansoni (Sm), a trematode causing human schistosomiasis. Responses of schistosome-susceptible (M line, or SUS) a...

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Published in:Frontiers in Immunology
Main Authors: Lijun Lu, Lijing Bu, Si-Ming Zhang, Sarah K. Buddenborg, Eric S. Loker
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-01-01
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2021.805882/full
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author Lijun Lu
Lijing Bu
Si-Ming Zhang
Sarah K. Buddenborg
Eric S. Loker
author_facet Lijun Lu
Lijing Bu
Si-Ming Zhang
Sarah K. Buddenborg
Eric S. Loker
author_sort Lijun Lu
collection DOAJ
container_title Frontiers in Immunology
description BackgroundWe seek to provide a comprehensive overview of transcriptomics responses of immune-related features of the gastropod Biomphalaria glabrata (Bg) following exposure to Schistosoma mansoni (Sm), a trematode causing human schistosomiasis. Responses of schistosome-susceptible (M line, or SUS) and -resistant (BS-90, or RES) Bg strains were characterized following exposure to Sm for 0.5, 2, 8 or 40 days post-exposure (dpe).MethodsRNA-Seq and differential expression analysis were undertaken on 56 snails from 14 groups. We considered 7 response categories: 1) constitutive resistance factors; 2) constitutive susceptibility factors; 3) generalized stress responses; 4) induced resistance factors; 5) resistance factors suppressed in SUS snails; 6) suppressed/manipulated factors in SUS snails; and 7) tolerance responses in SUS snails. We also undertook a gene co-expression network analysis. Results from prior studies identifying schistosome resistance/susceptibility factors were examined relative to our findings.ResultsA total of 792 million paired-end reads representing 91.2% of the estimated 31,985 genes in the Bg genome were detected and results for the 7 categories compiled and highlighted. For both RES and SUS snails, a single most supported network of genes with highly correlated expression was found.Conclusions1) Several constitutive differences in gene expression between SUS and RES snails were noted, the majority over-represented in RES; 2) There was little indication of a generalized stress response shared by SUS and RES snails at 0.5 or 2 dpe; 3) RES snails mounted a strong, multi-faceted response by 0.5 dpe that carried over to 2 dpe; 4) The most notable SUS responses were at 40 dpe, in snails shedding cercariae, when numerous features were either strongly down-regulated indicative of physiological distress or parasite manipulation, or up-regulated, suggestive of tolerance or survival-promoting effects; 5) Of 55 genes previously identified in genome wide mapping studies, 29 (52.7%) were responsive to Sm, as were many familiar resistance-associated genes (41.0%) identified by other means; 6) Both network analysis and remarkably specific patterns of expression of lectins and G protein-coupled receptors in categories 4, 6 and 7 were indicative of orchestrated responses of different suites of genes in SUS or RES snails following exposure to Sm.
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spelling doaj-art-e564753e2d9f4ee799d8e68a84a4ddf12025-08-19T21:07:22ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-01-011210.3389/fimmu.2021.805882805882An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni InfectionLijun Lu0Lijing Bu1Si-Ming Zhang2Sarah K. Buddenborg3Eric S. Loker4Center for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, NM, United StatesCenter for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, NM, United StatesCenter for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, NM, United StatesWellcome Sanger Institute, Wellcome Genome Campus, Hinxton, United KingdomCenter for Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, NM, United StatesBackgroundWe seek to provide a comprehensive overview of transcriptomics responses of immune-related features of the gastropod Biomphalaria glabrata (Bg) following exposure to Schistosoma mansoni (Sm), a trematode causing human schistosomiasis. Responses of schistosome-susceptible (M line, or SUS) and -resistant (BS-90, or RES) Bg strains were characterized following exposure to Sm for 0.5, 2, 8 or 40 days post-exposure (dpe).MethodsRNA-Seq and differential expression analysis were undertaken on 56 snails from 14 groups. We considered 7 response categories: 1) constitutive resistance factors; 2) constitutive susceptibility factors; 3) generalized stress responses; 4) induced resistance factors; 5) resistance factors suppressed in SUS snails; 6) suppressed/manipulated factors in SUS snails; and 7) tolerance responses in SUS snails. We also undertook a gene co-expression network analysis. Results from prior studies identifying schistosome resistance/susceptibility factors were examined relative to our findings.ResultsA total of 792 million paired-end reads representing 91.2% of the estimated 31,985 genes in the Bg genome were detected and results for the 7 categories compiled and highlighted. For both RES and SUS snails, a single most supported network of genes with highly correlated expression was found.Conclusions1) Several constitutive differences in gene expression between SUS and RES snails were noted, the majority over-represented in RES; 2) There was little indication of a generalized stress response shared by SUS and RES snails at 0.5 or 2 dpe; 3) RES snails mounted a strong, multi-faceted response by 0.5 dpe that carried over to 2 dpe; 4) The most notable SUS responses were at 40 dpe, in snails shedding cercariae, when numerous features were either strongly down-regulated indicative of physiological distress or parasite manipulation, or up-regulated, suggestive of tolerance or survival-promoting effects; 5) Of 55 genes previously identified in genome wide mapping studies, 29 (52.7%) were responsive to Sm, as were many familiar resistance-associated genes (41.0%) identified by other means; 6) Both network analysis and remarkably specific patterns of expression of lectins and G protein-coupled receptors in categories 4, 6 and 7 were indicative of orchestrated responses of different suites of genes in SUS or RES snails following exposure to Sm.https://www.frontiersin.org/articles/10.3389/fimmu.2021.805882/fulltranscriptomicsRNA-sequencingBiomphalaria glabrataSchistosoma mansonischistosomiasisvector biology
spellingShingle Lijun Lu
Lijing Bu
Si-Ming Zhang
Sarah K. Buddenborg
Eric S. Loker
An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection
transcriptomics
RNA-sequencing
Biomphalaria glabrata
Schistosoma mansoni
schistosomiasis
vector biology
title An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection
title_full An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection
title_fullStr An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection
title_full_unstemmed An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection
title_short An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection
title_sort overview of transcriptional responses of schistosome susceptible m line or resistant bs 90 biomphalaria glabrata exposed or not to schistosoma mansoni infection
topic transcriptomics
RNA-sequencing
Biomphalaria glabrata
Schistosoma mansoni
schistosomiasis
vector biology
url https://www.frontiersin.org/articles/10.3389/fimmu.2021.805882/full
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