Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.

The human hookworm Necator americanus infects more than 400 million people worldwide, contributing substantially to the poverty in these regions. Adult stage N. americanus live in the small intestine of the human host where they inject excretory/secretory (ES) products into the mucosa. ES products h...

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Authors: Logan, Jayden, Pearson, Mark S, Manda, Srikanth S, Choi, Young-Jun, Field, Matthew, Eichenberger, Ramon M, Mulvenna, Jason, Nagaraj, Shivashankar H, Fujiwara, Ricardo T, Gazzinelli-Guimaraes, Pedro, Bueno, Lilian, Mati, Vitor, Bethony, Jeffrey M, Mitreva, Makedonka, Loukas, Alex, Sotillo, Javier
Format: article
Publication Date:2020
Country:España
Institution:Instituto de Salud Carlos III (ISCIII)
Repository:Repisalud
Language:English
OAI Identifier:oai:repisalud.isciii.es:20.500.12105/10880
Online Access:http://hdl.handle.net/20.500.12105/10880
Access Level:Open access
Keyword:Proteome
Animals
Gene Expression Regulation
Gene Regulatory Networks
Genome, Helminth
Helminth Proteins
Necator americanus
Phylogeny
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spelling Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.Logan, JaydenPearson, Mark SManda, Srikanth SChoi, Young-JunField, MatthewEichenberger, Ramon MMulvenna, JasonNagaraj, Shivashankar HFujiwara, Ricardo TGazzinelli-Guimaraes, PedroBueno, LilianMati, VitorBethony, Jeffrey MMitreva, MakedonkaLoukas, AlexSotillo, JavierProteomeAnimalsGene Expression RegulationGene Regulatory NetworksGenome, HelminthHelminth ProteinsNecator americanusPhylogenyThe human hookworm Necator americanus infects more than 400 million people worldwide, contributing substantially to the poverty in these regions. Adult stage N. americanus live in the small intestine of the human host where they inject excretory/secretory (ES) products into the mucosa. ES products have been characterized at the proteome level for a number of animal hookworm species, but until now, the difficulty in obtaining sufficient live N. americanus has been an obstacle in characterizing the secretome of this important human pathogen. Herein we describe the ES proteome of N. americanus and utilize this information along with RNA Seq data to conduct the first proteogenomic analysis of a parasitic helminth, significantly improving the available genome and thereby generating a robust description of the parasite secretome. The genome annotation resulted in a revised prediction of 3,425 fewer genes than initially reported, accompanied by a significant increase in the number of exons and introns, total gene length and the percentage of the genome covered by genes. Almost 200 ES proteins were identified by LC-MS/MS with SCP/TAPS proteins, 'hypothetical' proteins and proteases among the most abundant families. These proteins were compared to commonly used model species of human parasitic infections, including Ancylostoma caninum, Nippostrongylus brasiliensis and Heligmosomoides polygyrus. SCP/TAPS proteins are immunogenic in nematode infections, so we expressed four of those identified in this study in recombinant form and showed that they are all recognized to varying degrees by serum antibodies from hookworm-infected subjects from a disease-endemic area of Brazil. Our findings provide valuable information on important families of proteins with both known and unknown functions that could be instrumental in host-parasite interactions, including protein families that might be key for parasite survival in the onslaught of robust immune responses, as well as vaccine and diagnostic targets.Public Library of Science (PLOS)National Health and Medical Research Council (Australia)20202020-08-1020202020-01-0120202020-01-01journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/20.500.12105/10880reponame:Repisaludinstname:Instituto de Salud Carlos III (ISCIII)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Atribución 4.0 Internacionalhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repisalud.isciii.es:20.500.12105/108802026-06-12T12:43:37Z
dc.title.none.fl_str_mv Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
title Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
spellingShingle Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
Logan, Jayden
Proteome
Animals
Gene Expression Regulation
Gene Regulatory Networks
Genome, Helminth
Helminth Proteins
Necator americanus
Phylogeny
title_short Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
title_full Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
title_fullStr Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
title_full_unstemmed Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
title_sort Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms.
dc.creator.none.fl_str_mv Logan, Jayden
Pearson, Mark S
Manda, Srikanth S
Choi, Young-Jun
Field, Matthew
Eichenberger, Ramon M
Mulvenna, Jason
Nagaraj, Shivashankar H
Fujiwara, Ricardo T
Gazzinelli-Guimaraes, Pedro
Bueno, Lilian
Mati, Vitor
Bethony, Jeffrey M
Mitreva, Makedonka
Loukas, Alex
Sotillo, Javier
author Logan, Jayden
author_facet Logan, Jayden
Pearson, Mark S
Manda, Srikanth S
Choi, Young-Jun
Field, Matthew
Eichenberger, Ramon M
Mulvenna, Jason
Nagaraj, Shivashankar H
Fujiwara, Ricardo T
Gazzinelli-Guimaraes, Pedro
Bueno, Lilian
Mati, Vitor
Bethony, Jeffrey M
Mitreva, Makedonka
Loukas, Alex
Sotillo, Javier
author_role author
author2 Pearson, Mark S
Manda, Srikanth S
Choi, Young-Jun
Field, Matthew
Eichenberger, Ramon M
Mulvenna, Jason
Nagaraj, Shivashankar H
Fujiwara, Ricardo T
Gazzinelli-Guimaraes, Pedro
Bueno, Lilian
Mati, Vitor
Bethony, Jeffrey M
Mitreva, Makedonka
Loukas, Alex
Sotillo, Javier
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv National Health and Medical Research Council (Australia)
dc.subject.none.fl_str_mv Proteome
Animals
Gene Expression Regulation
Gene Regulatory Networks
Genome, Helminth
Helminth Proteins
Necator americanus
Phylogeny
topic Proteome
Animals
Gene Expression Regulation
Gene Regulatory Networks
Genome, Helminth
Helminth Proteins
Necator americanus
Phylogeny
description The human hookworm Necator americanus infects more than 400 million people worldwide, contributing substantially to the poverty in these regions. Adult stage N. americanus live in the small intestine of the human host where they inject excretory/secretory (ES) products into the mucosa. ES products have been characterized at the proteome level for a number of animal hookworm species, but until now, the difficulty in obtaining sufficient live N. americanus has been an obstacle in characterizing the secretome of this important human pathogen. Herein we describe the ES proteome of N. americanus and utilize this information along with RNA Seq data to conduct the first proteogenomic analysis of a parasitic helminth, significantly improving the available genome and thereby generating a robust description of the parasite secretome. The genome annotation resulted in a revised prediction of 3,425 fewer genes than initially reported, accompanied by a significant increase in the number of exons and introns, total gene length and the percentage of the genome covered by genes. Almost 200 ES proteins were identified by LC-MS/MS with SCP/TAPS proteins, 'hypothetical' proteins and proteases among the most abundant families. These proteins were compared to commonly used model species of human parasitic infections, including Ancylostoma caninum, Nippostrongylus brasiliensis and Heligmosomoides polygyrus. SCP/TAPS proteins are immunogenic in nematode infections, so we expressed four of those identified in this study in recombinant form and showed that they are all recognized to varying degrees by serum antibodies from hookworm-infected subjects from a disease-endemic area of Brazil. Our findings provide valuable information on important families of proteins with both known and unknown functions that could be instrumental in host-parasite interactions, including protein families that might be key for parasite survival in the onslaught of robust immune responses, as well as vaccine and diagnostic targets.
publishDate 2020
dc.date.none.fl_str_mv 2020
2020-08-10
2020
2020-01-01
2020
2020-01-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12105/10880
url http://hdl.handle.net/20.500.12105/10880
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Atribución 4.0 Internacional
http://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Atribución 4.0 Internacional
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Public Library of Science (PLOS)
publisher.none.fl_str_mv Public Library of Science (PLOS)
dc.source.none.fl_str_mv reponame:Repisalud
instname:Instituto de Salud Carlos III (ISCIII)
instname_str Instituto de Salud Carlos III (ISCIII)
reponame_str Repisalud
collection Repisalud
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,228081

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