Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection

Abstract Background Molluscs, including snails, are prone to parasite infection, which can lead to massive physiological and behavioural changes, yet many of the molecular components involved remain unresolved. Central to this point is the neural system that in snails consists of several ganglia tha...

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Main Authors: Tianfang Wang, Min Zhao, Di Liang, Utpal Bose, Satwant Kaur, Donald P. McManus, Scott F. Cummins
Format: Article
Language:English
Published: BMC 2017-06-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-017-2218-1
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author Tianfang Wang
Min Zhao
Di Liang
Utpal Bose
Satwant Kaur
Donald P. McManus
Scott F. Cummins
author_facet Tianfang Wang
Min Zhao
Di Liang
Utpal Bose
Satwant Kaur
Donald P. McManus
Scott F. Cummins
author_sort Tianfang Wang
collection DOAJ
description Abstract Background Molluscs, including snails, are prone to parasite infection, which can lead to massive physiological and behavioural changes, yet many of the molecular components involved remain unresolved. Central to this point is the neural system that in snails consists of several ganglia that regulate the animals’ physiology and behaviour patterns. The availability of a genomic resource for the freshwater snail Biomphalaria glabrata provides a mean towards the high throughput analysis of changes in the central nervous system (CNS) following infection with Schistosoma miracidia. Results In this study, we performed a proteomic analysis of the B. glabrata CNS at pre-patent infection, providing a list of proteins that were further used within a protein-protein interaction (PPI) framework against S. mansoni proteins. A hub with most connections for both non-infected and infected Biomphalaria includes leucine aminopeptidase 2 (LAP2), which interacts with numerous miracidia proteins that together belong to the immunoglobulin family of cell adhesion related molecules. We additionally reveal the presence of at least 165 neuropeptides derived from the precursors of buccalin, enterin, FMRF, FVRI, pedal peptide 1, 2, 3 and 4, RYamide, RFamide, pleurin and others. Many of these were present at significantly reduced levels in the snail’s CNS post-infection, such as the egg laying hormone, a neuropeptide required to initiate egg laying in gastropod molluscs. Conclusions Our analysis demonstrates that LAP2 may be a key component that regulates parasite infection physiology, as well as establishing that parasite-induced reproductive castration may be facilitated by significant reductions in reproduction-associated neuropeptides. This work helps in our understanding of molluscan neuropeptides and further stimulates advances in parasite-host interactions.
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spelling doaj.art-8f3c692705f843eca60a803b2fbf55882022-12-22T00:09:14ZengBMCParasites & Vectors1756-33052017-06-0110111310.1186/s13071-017-2218-1Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infectionTianfang Wang0Min Zhao1Di Liang2Utpal Bose3Satwant Kaur4Donald P. McManus5Scott F. Cummins6Genecology Research Centre, Faculty of Science, Health and Education, University of the Sunshine CoastGenecology Research Centre, Faculty of Science, Health and Education, University of the Sunshine CoastGenecology Research Centre, Faculty of Science, Health and Education, University of the Sunshine CoastGenecology Research Centre, Faculty of Science, Health and Education, University of the Sunshine CoastInstitute of Environment, Health and Societies, Brunel University LondonMolecular Parasitology Laboratory, QIMR Berghofer Medical Research InstituteGenecology Research Centre, Faculty of Science, Health and Education, University of the Sunshine CoastAbstract Background Molluscs, including snails, are prone to parasite infection, which can lead to massive physiological and behavioural changes, yet many of the molecular components involved remain unresolved. Central to this point is the neural system that in snails consists of several ganglia that regulate the animals’ physiology and behaviour patterns. The availability of a genomic resource for the freshwater snail Biomphalaria glabrata provides a mean towards the high throughput analysis of changes in the central nervous system (CNS) following infection with Schistosoma miracidia. Results In this study, we performed a proteomic analysis of the B. glabrata CNS at pre-patent infection, providing a list of proteins that were further used within a protein-protein interaction (PPI) framework against S. mansoni proteins. A hub with most connections for both non-infected and infected Biomphalaria includes leucine aminopeptidase 2 (LAP2), which interacts with numerous miracidia proteins that together belong to the immunoglobulin family of cell adhesion related molecules. We additionally reveal the presence of at least 165 neuropeptides derived from the precursors of buccalin, enterin, FMRF, FVRI, pedal peptide 1, 2, 3 and 4, RYamide, RFamide, pleurin and others. Many of these were present at significantly reduced levels in the snail’s CNS post-infection, such as the egg laying hormone, a neuropeptide required to initiate egg laying in gastropod molluscs. Conclusions Our analysis demonstrates that LAP2 may be a key component that regulates parasite infection physiology, as well as establishing that parasite-induced reproductive castration may be facilitated by significant reductions in reproduction-associated neuropeptides. This work helps in our understanding of molluscan neuropeptides and further stimulates advances in parasite-host interactions.http://link.springer.com/article/10.1186/s13071-017-2218-1BiomphalariaSchistosomaNeuropeptidePre-patent infectionProtein-protein interactionCentral nervous system
spellingShingle Tianfang Wang
Min Zhao
Di Liang
Utpal Bose
Satwant Kaur
Donald P. McManus
Scott F. Cummins
Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection
Parasites & Vectors
Biomphalaria
Schistosoma
Neuropeptide
Pre-patent infection
Protein-protein interaction
Central nervous system
title Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection
title_full Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection
title_fullStr Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection
title_full_unstemmed Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection
title_short Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection
title_sort changes in the neuropeptide content of biomphalaria ganglia nervous system following schistosoma infection
topic Biomphalaria
Schistosoma
Neuropeptide
Pre-patent infection
Protein-protein interaction
Central nervous system
url http://link.springer.com/article/10.1186/s13071-017-2218-1
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