A comparative proteomics analysis of the egg secretions of three major schistosome species

•S. mansoni eggs secrete at least 266 proteins, 78 more than previously reported.•S. mansoni, S. japonicum and S. haematobium egg secretions vary in complexity.•Shared components between species include vesicle-associated and detox proteins.•Potential pathology causing proteins appear unique to each...

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Published inMolecular and biochemical parasitology Vol. 240; p. 111322
Main Authors Carson, Jack P., Robinson, Mark W., Hsieh, Michael H., Cody, James, Le, Loc, You, Hong, McManus, Donald P., Gobert, Geoffrey N.
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 01.11.2020
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Abstract •S. mansoni eggs secrete at least 266 proteins, 78 more than previously reported.•S. mansoni, S. japonicum and S. haematobium egg secretions vary in complexity.•Shared components between species include vesicle-associated and detox proteins.•Potential pathology causing proteins appear unique to each secretome.•Varied secretions likely influence species-specific pathology and disease severity. Morbidity associated with hepatic and urogenital schistosomiasis stems primarily from the host immune response directed against schistosome eggs. When eggs become entrapped in host tissues, the development of fibrotic plaques drives downstream pathology. These events occur due to the antigenic nature of egg excretory/secretory products (ESPs). Both Schistosoma mansoni and S. japonicum ESPs have been shown to interact with several cell populations in the host liver including hepatocytes, macrophages, and hepatic stellate cells, with both immunomodulatory and pathological consequences. Several protein components of the ESPs of S. mansoni and S. japonicum eggs have been characterised; however, studies into the collective contents of schistosome egg ESPs are lacking. Utilising shotgun mass spectrometry and an array of in silico analyses, we identified 266, 90 and 50 proteins within the S. mansoni, S. japonicum and S. haematobium egg secretomes respectively. We identified numerous proteins with already established immunomodulatory activities, vaccine candidates and vesicle markers. Relatively few common orthologues within the ESPs were identified by BLAST, indicating that the three egg secretomes differ in content significantly. Having a clearer understanding of these components may lead to the identification of new proteins with uncharacterised immunomodulatory potential or pathological relevance. This will enhance our understanding of host-parasite interactions, particularly those occurring during chronic schistosomiasis, and pave the way towards novel therapeutics and vaccines.
AbstractList Morbidity associated with hepatic and urogenital schistosomiasis stems primarily from the host immune response directed against schistosome eggs. When eggs become entrapped in host tissues, the development of fibrotic plaques drives downstream pathology. These events occur due to the antigenic nature of egg excretory/secretory products (ESPs). Both Schistosoma mansoni and S. japonicum ESPs have been shown to interact with several cell populations in the host liver including hepatocytes, macrophages, and hepatic stellate cells, with both immunomodulatory and pathological consequences. Several protein components of the ESPs of S. mansoni and S. japonicum eggs have been characterised; however, studies into the collective contents of schistosome egg ESPs are lacking. Utilising shotgun mass spectrometry and an array of in silico analyses, we identified 266, 90 and 50 proteins within the S. mansoni, S. japonicum and S. haematobium egg secretomes respectively. We identified numerous proteins with already established immunomodulatory activities, vaccine candidates and vesicle markers. Relatively few common orthologues within the ESPs were identified by BLAST, indicating that the three egg secretomes differ in content significantly. Having a clearer understanding of these components may lead to the identification of new proteins with uncharacterised immunomodulatory potential or pathological relevance. This will enhance our understanding of host-parasite interactions, particularly those occurring during chronic schistosomiasis, and pave the way towards novel therapeutics and vaccines.
Morbidity associated with hepatic and urogenital schistosomiasis stems primarily from the host immune response directed against schistosome eggs. When eggs become entrapped in host tissues, the development of fibrotic plaques drives downstream pathology. These events occur due to the antigenic nature of egg excretory/secretory products (ESPs). Both Schistosoma mansoni and S. japonicum ESPs have been shown to interact with several cell populations in the host liver including hepatocytes, macrophages, and hepatic stellate cells, with both immunomodulatory and pathological consequences. Several protein components of the ESPs of S. mansoni and S. japonicum eggs have been characterised; however, studies into the collective contents of schistosome egg ESPs are lacking. Utilising shotgun mass spectrometry and an array of in silico analyses, we identified 266, 90 and 50 proteins within the S. mansoni, S. japonicum and S. haematobium egg secretomes respectively. We identified numerous proteins with already established immunomodulatory activities, vaccine candidates and vesicle markers. Relatively few common orthologues within the ESPs were identified by BLAST, indicating that the three egg secretomes differ in content significantly. Having a clearer understanding of these components may lead to the identification of new proteins with uncharacterised immunomodulatory potential or pathological relevance. This will enhance our understanding of host-parasite interactions, particularly those occurring during chronic schistosomiasis, and pave the way towards novel therapeutics and vaccines.
•S. mansoni eggs secrete at least 266 proteins, 78 more than previously reported.•S. mansoni, S. japonicum and S. haematobium egg secretions vary in complexity.•Shared components between species include vesicle-associated and detox proteins.•Potential pathology causing proteins appear unique to each secretome.•Varied secretions likely influence species-specific pathology and disease severity. Morbidity associated with hepatic and urogenital schistosomiasis stems primarily from the host immune response directed against schistosome eggs. When eggs become entrapped in host tissues, the development of fibrotic plaques drives downstream pathology. These events occur due to the antigenic nature of egg excretory/secretory products (ESPs). Both Schistosoma mansoni and S. japonicum ESPs have been shown to interact with several cell populations in the host liver including hepatocytes, macrophages, and hepatic stellate cells, with both immunomodulatory and pathological consequences. Several protein components of the ESPs of S. mansoni and S. japonicum eggs have been characterised; however, studies into the collective contents of schistosome egg ESPs are lacking. Utilising shotgun mass spectrometry and an array of in silico analyses, we identified 266, 90 and 50 proteins within the S. mansoni, S. japonicum and S. haematobium egg secretomes respectively. We identified numerous proteins with already established immunomodulatory activities, vaccine candidates and vesicle markers. Relatively few common orthologues within the ESPs were identified by BLAST, indicating that the three egg secretomes differ in content significantly. Having a clearer understanding of these components may lead to the identification of new proteins with uncharacterised immunomodulatory potential or pathological relevance. This will enhance our understanding of host-parasite interactions, particularly those occurring during chronic schistosomiasis, and pave the way towards novel therapeutics and vaccines.
ArticleNumber 111322
Author Gobert, Geoffrey N.
McManus, Donald P.
You, Hong
Hsieh, Michael H.
Cody, James
Carson, Jack P.
Robinson, Mark W.
Le, Loc
AuthorAffiliation b Division of Urology, Children’s National Hospital, George Washington University School of Medicine and Health Sciences, Washington DC, USA
e Molecular Parasitology Laboratory, Immunology Department, QIMR Berghofer Medical Research Institute, Brisbane, Australia
a School of Biological Sciences, Queen’s University Belfast, Belfast, United Kingdom
d A-TEK, Tysons, VA, USA
c Vigene Biosciences, Rockville, MD, USA
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Keywords Schistosoma mansoni
Schistosoma haematobium
Egg
Schistosoma japonicum
Proteomics
Excretory/secretory protein
Language English
License Copyright © 2020 Elsevier B.V. All rights reserved.
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Jack P. Carson: Investigation, Methodology, Writing - original draft. Mark W. Robinson: Conceptualization, Methodology, Funding acquisition, Supervision, Writing - review & editing. Michael H. Hsieh: Investigation, Methodology, Writing - review & editing. James Cody: Investigation, Methodology. Loc Le: Investigation, Methodology. Hong You: Investigation, Methodology. Donald P. McManus: Writing - review & editing, Funding acquisition. Geoffrey N. Gobert: Conceptualization, Funding acquisition, Supervision, Writing - review & editing.
CRediT authorship contribution statement
Author statement
Design of experiments by JCa, MR, MS and GG. Collection of material by MS, JCo, LL, and HY. Analysis of data by JCa, MR, HY and GG. First draft of manuscript by JCa, and subsequent drafting by JCa, MR, DM, HY, MS and GG.
OpenAccessLink https://pure.qub.ac.uk/files/216626269/Carson_et_al_2020.pdf
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Snippet •S. mansoni eggs secrete at least 266 proteins, 78 more than previously reported.•S. mansoni, S. japonicum and S. haematobium egg secretions vary in...
Morbidity associated with hepatic and urogenital schistosomiasis stems primarily from the host immune response directed against schistosome eggs. When eggs...
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SubjectTerms Egg
Excretory/secretory protein
Proteomics
Schistosoma haematobium
Schistosoma japonicum
Schistosoma mansoni
Title A comparative proteomics analysis of the egg secretions of three major schistosome species
URI https://dx.doi.org/10.1016/j.molbiopara.2020.111322
https://www.ncbi.nlm.nih.gov/pubmed/32961206
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