Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata

Abstract Background Schistosomiasis is a harmful neglected tropical disease caused by infection with Schistosoma spp., such as Schistosoma mansoni. Schistosoma must transition within a molluscan host to survive. Chemical analyses of schistosome-molluscan interactions indicate that host identificatio...

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Main Authors: Conor E. Fogarty, Min Zhao, Donald P. McManus, Mary G. Duke, Scott F. Cummins, Tianfang Wang
Format: Article
Language:English
Published: BMC 2019-09-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-019-3708-0
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author Conor E. Fogarty
Min Zhao
Donald P. McManus
Mary G. Duke
Scott F. Cummins
Tianfang Wang
author_facet Conor E. Fogarty
Min Zhao
Donald P. McManus
Mary G. Duke
Scott F. Cummins
Tianfang Wang
author_sort Conor E. Fogarty
collection DOAJ
description Abstract Background Schistosomiasis is a harmful neglected tropical disease caused by infection with Schistosoma spp., such as Schistosoma mansoni. Schistosoma must transition within a molluscan host to survive. Chemical analyses of schistosome-molluscan interactions indicate that host identification involves chemosensation, including naïve host preference. Proteomic technique advances enable sophisticated comparative analyses between infected and naïve snail host proteins. This study aimed to compare resistant, susceptible and naïve Biomphalaria glabrata snail-conditioned water (SCW) to identify potential attractants and deterrents. Methods Behavioural bioassays were performed on S. mansoni miracidia to compare the effects of susceptible, F1 resistant and naïve B. glabrata SCW. The F1 resistant and susceptible B. glabrata SCW excretory–secretory proteins (ESPs) were fractionated using SDS-PAGE, identified with LC-MS/MS and compared to naïve snail ESPs. Protein-protein interaction (PPI) analyses based on published studies (including experiments, co-expression, text-mining and gene fusion) identified S. mansoni and B. glabrata protein interaction. Data are available via ProteomeXchange with identifier PXD015129. Results A total of 291, 410 and 597 ESPs were detected in the susceptible, F1 resistant and naïve SCW, respectively. Less overlap in ESPs was identified between susceptible and naïve snails than F1 resistant and naïve snails. F1 resistant B. glabrata ESPs were predominately associated with anti-pathogen activity and detoxification, such as leukocyte elastase and peroxiredoxin. Susceptible B. glabrata several proteins correlated with immunity and anti-inflammation, such as glutathione S-transferase and zinc metalloproteinase, and S. mansoni sporocyst presence. PPI analyses found that uncharacterised S. mansoni protein Smp_142140.1 potentially interacts with numerous B. glabrata proteins. Conclusions This study identified ESPs released by F1 resistant, susceptible and naïve B. glabrata to explain S. mansoni miracidia interplay. Susceptible B. glabrata ESPs shed light on potential S. mansoni miracidia deterrents. Further targeted research on specific ESPs identified in this study could help inhibit B. glabrata and S. mansoni interactions and stop human schistosomiasis.
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spelling doaj.art-148077675bae4aee99c3172d000d4c552022-12-21T19:26:27ZengBMCParasites & Vectors1756-33052019-09-0112111710.1186/s13071-019-3708-0Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrataConor E. Fogarty0Min Zhao1Donald P. McManus2Mary G. Duke3Scott F. Cummins4Tianfang Wang5Genecology Research Centre, University of the Sunshine CoastGenecology Research Centre, University of the Sunshine CoastQIMR Berghofer Medical Research InstituteQIMR Berghofer Medical Research InstituteGenecology Research Centre, University of the Sunshine CoastGenecology Research Centre, University of the Sunshine CoastAbstract Background Schistosomiasis is a harmful neglected tropical disease caused by infection with Schistosoma spp., such as Schistosoma mansoni. Schistosoma must transition within a molluscan host to survive. Chemical analyses of schistosome-molluscan interactions indicate that host identification involves chemosensation, including naïve host preference. Proteomic technique advances enable sophisticated comparative analyses between infected and naïve snail host proteins. This study aimed to compare resistant, susceptible and naïve Biomphalaria glabrata snail-conditioned water (SCW) to identify potential attractants and deterrents. Methods Behavioural bioassays were performed on S. mansoni miracidia to compare the effects of susceptible, F1 resistant and naïve B. glabrata SCW. The F1 resistant and susceptible B. glabrata SCW excretory–secretory proteins (ESPs) were fractionated using SDS-PAGE, identified with LC-MS/MS and compared to naïve snail ESPs. Protein-protein interaction (PPI) analyses based on published studies (including experiments, co-expression, text-mining and gene fusion) identified S. mansoni and B. glabrata protein interaction. Data are available via ProteomeXchange with identifier PXD015129. Results A total of 291, 410 and 597 ESPs were detected in the susceptible, F1 resistant and naïve SCW, respectively. Less overlap in ESPs was identified between susceptible and naïve snails than F1 resistant and naïve snails. F1 resistant B. glabrata ESPs were predominately associated with anti-pathogen activity and detoxification, such as leukocyte elastase and peroxiredoxin. Susceptible B. glabrata several proteins correlated with immunity and anti-inflammation, such as glutathione S-transferase and zinc metalloproteinase, and S. mansoni sporocyst presence. PPI analyses found that uncharacterised S. mansoni protein Smp_142140.1 potentially interacts with numerous B. glabrata proteins. Conclusions This study identified ESPs released by F1 resistant, susceptible and naïve B. glabrata to explain S. mansoni miracidia interplay. Susceptible B. glabrata ESPs shed light on potential S. mansoni miracidia deterrents. Further targeted research on specific ESPs identified in this study could help inhibit B. glabrata and S. mansoni interactions and stop human schistosomiasis.http://link.springer.com/article/10.1186/s13071-019-3708-0Schistosoma mansoniBiomphalaria glabrataMiracidiaExcretory–secretory proteinsProteomicsPPI
spellingShingle Conor E. Fogarty
Min Zhao
Donald P. McManus
Mary G. Duke
Scott F. Cummins
Tianfang Wang
Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata
Parasites & Vectors
Schistosoma mansoni
Biomphalaria glabrata
Miracidia
Excretory–secretory proteins
Proteomics
PPI
title Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata
title_full Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata
title_fullStr Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata
title_full_unstemmed Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata
title_short Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata
title_sort comparative study of excretory secretory proteins released by schistosoma mansoni resistant susceptible and naive biomphalaria glabrata
topic Schistosoma mansoni
Biomphalaria glabrata
Miracidia
Excretory–secretory proteins
Proteomics
PPI
url http://link.springer.com/article/10.1186/s13071-019-3708-0
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