A Proteomic Analysis of the Body Wall, Digestive Tract, and Reproductive Tract of Brugia malayi
Identifieur interne : 007878 ( Ncbi/Merge ); précédent : 007877; suivant : 007879A Proteomic Analysis of the Body Wall, Digestive Tract, and Reproductive Tract of Brugia malayi
Auteurs : C. Paul Morris [États-Unis] ; Sasisekhar Bennuru [États-Unis] ; Laura E. Kropp [États-Unis] ; Jesse A. Zweben [États-Unis] ; Zhaojing Meng [États-Unis] ; Rebekah T. Taylor [États-Unis] ; King Chan [États-Unis] ; Timothy D. Veenstra [États-Unis] ; Thomas B. Nutman [États-Unis] ; Edward Mitre [États-Unis]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2015.
Abstract
Filarial worms are parasitic nematodes that cause devastating diseases such as lymphatic filariasis (LF) and onchocerciasis. Filariae are nematodes with complex anatomy including fully developed digestive tracts and reproductive organs. To better understand the basic biology of filarial parasites and to provide insights into drug targets and vaccine design, we conducted a proteomic analysis of different anatomic fractions of
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DOI: 10.1371/journal.pntd.0004054
PubMed: 26367142
PubMed Central: 4569401
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Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Meng, Zhaojing" sort="Meng, Zhaojing" uniqKey="Meng Z" first="Zhaojing" last="Meng">Zhaojing Meng</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Taylor, Rebekah T" sort="Taylor, Rebekah T" uniqKey="Taylor R" first="Rebekah T." last="Taylor">Rebekah T. Taylor</name><affiliation wicri:level="2"><nlm:aff id="aff004"><addr-line>Department of Biology, Frostburg State University, Frostburg, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, Frostburg State University, Frostburg, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Chan, King" sort="Chan, King" uniqKey="Chan K" first="King" last="Chan">King Chan</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Veenstra, Timothy D" sort="Veenstra, Timothy D" uniqKey="Veenstra T" first="Timothy D." last="Veenstra">Timothy D. Veenstra</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Nutman, Thomas B" sort="Nutman, Thomas B" uniqKey="Nutman T" first="Thomas B." last="Nutman">Thomas B. 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Kropp</name><affiliation wicri:level="2"><nlm:aff id="aff001"><addr-line>Department of Microbiology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Zweben, Jesse A" sort="Zweben, Jesse A" uniqKey="Zweben J" first="Jesse A." last="Zweben">Jesse A. Zweben</name><affiliation wicri:level="2"><nlm:aff id="aff001"><addr-line>Department of Microbiology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Meng, Zhaojing" sort="Meng, Zhaojing" uniqKey="Meng Z" first="Zhaojing" last="Meng">Zhaojing Meng</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Taylor, Rebekah T" sort="Taylor, Rebekah T" uniqKey="Taylor R" first="Rebekah T." last="Taylor">Rebekah T. Taylor</name><affiliation wicri:level="2"><nlm:aff id="aff004"><addr-line>Department of Biology, Frostburg State University, Frostburg, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biology, Frostburg State University, Frostburg, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Chan, King" sort="Chan, King" uniqKey="Chan K" first="King" last="Chan">King Chan</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Veenstra, Timothy D" sort="Veenstra, Timothy D" uniqKey="Veenstra T" first="Timothy D." last="Veenstra">Timothy D. Veenstra</name><affiliation wicri:level="2"><nlm:aff id="aff003"><addr-line>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Nutman, Thomas B" sort="Nutman, Thomas B" uniqKey="Nutman T" first="Thomas B." last="Nutman">Thomas B. Nutman</name><affiliation wicri:level="2"><nlm:aff id="aff002"><addr-line>National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Mitre, Edward" sort="Mitre, Edward" uniqKey="Mitre E" first="Edward" last="Mitre">Edward Mitre</name><affiliation wicri:level="2"><nlm:aff id="aff001"><addr-line>Department of Microbiology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author></analytic><series><title level="j">PLoS Neglected Tropical Diseases</title><idno type="ISSN">1935-2727</idno><idno type="eISSN">1935-2735</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Filarial worms are parasitic nematodes that cause devastating diseases such as lymphatic filariasis (LF) and onchocerciasis. Filariae are nematodes with complex anatomy including fully developed digestive tracts and reproductive organs. To better understand the basic biology of filarial parasites and to provide insights into drug targets and vaccine design, we conducted a proteomic analysis of different anatomic fractions of <italic>Brugia malayi</italic>, a causative agent of LF. Approximately 500 adult female <italic>B</italic>. <italic>malayi</italic> worms were dissected, and three anatomical fractions (body wall, digestive tract, and reproductive tract) were obtained. Proteins from each anatomical fraction were extracted, desalted, trypsinized, and analyzed by microcapillary reverse-phase liquid chromatography-tandem-mass spectrometry. In total, we identified 4,785 <italic>B</italic>. <italic>malayi</italic> proteins. While 1,894 were identified in all three anatomic fractions, 396 were positively identified only within the digestive tract, 114 only within the body wall, and 1,011 only within the reproductive tract. Gene set enrichment analysis revealed a bias for transporters to be present within the digestive tract, suggesting that the intestine of adult filariae is functional and important for nutrient uptake or waste removal. As expected, the body wall exhibited increased frequencies of cytoskeletal proteins, and the reproductive tract had increased frequencies of proteins involved in nuclear regulation and transcription. In assessing for possible vaccine candidates, we focused on proteins sequestered within the digestive tract, as these could possibly represent “hidden antigens” with low risk of prior allergic sensitization. We identified 106 proteins that are enriched in the digestive tract and are predicted to localize to the surface of cells in the the digestive tract. It is possible that some of these proteins are on the luminal surface and may be accessible by antibodies ingested by the worm. A subset of 27 of these proteins appear especially promising vaccine candidates as they contain significant non-cytoplasmic domains, only 1–2 transmembrane domains, and a high degree of homology to <italic>W</italic>. <italic>bancrofti</italic> and/or <italic>O</italic>. <italic>volvulus</italic>.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Hopkins, Dr" uniqKey="Hopkins D">DR Hopkins</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pfarr, Km" uniqKey="Pfarr K">KM Pfarr</name></author><author><name sortKey="Debrah, Ay" uniqKey="Debrah A">AY Debrah</name></author><author><name sortKey="Specht, S" uniqKey="Specht S">S Specht</name></author><author><name sortKey="Hoerauf, A" uniqKey="Hoerauf A">A Hoerauf</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ghedin, E" uniqKey="Ghedin E">E Ghedin</name></author><author><name sortKey="Wang, S" uniqKey="Wang S">S 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosntds</journal-id><journal-title-group><journal-title>PLoS Neglected Tropical Diseases</journal-title></journal-title-group><issn pub-type="ppub">1935-2727</issn><issn pub-type="epub">1935-2735</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26367142</article-id><article-id pub-id-type="pmc">4569401</article-id><article-id pub-id-type="doi">10.1371/journal.pntd.0004054</article-id><article-id pub-id-type="publisher-id">PNTD-D-15-00548</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>A Proteomic Analysis of the Body Wall, Digestive Tract, and Reproductive Tract of <italic>Brugia malayi</italic></article-title><alt-title alt-title-type="running-head">Anatomic Proteomics of <italic>B</italic>. <italic>malayi</italic></alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Morris</surname><given-names>C. Paul</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bennuru</surname><given-names>Sasisekhar</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kropp</surname><given-names>Laura E.</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zweben</surname><given-names>Jesse A.</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Meng</surname><given-names>Zhaojing</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Taylor</surname><given-names>Rebekah T.</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chan</surname><given-names>King</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Veenstra</surname><given-names>Timothy D.</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Nutman</surname><given-names>Thomas B.</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Mitre</surname><given-names>Edward</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref rid="cor001" ref-type="corresp">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Department of Microbiology, F. Edward Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America</addr-line></aff><aff id="aff002"><label>2</label><addr-line>National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Protein Characterization Laboratory Cancer Research Technology Program, Leidos Biomedical Research inc., Frederick National Laboratory, Frederick, Maryland, United States of America</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Department of Biology, Frostburg State University, Frostburg, Maryland, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Mitreva</surname><given-names>Makedonka</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Washington University School of Medicine, UNITED STATES</addr-line></aff><author-notes><fn fn-type="conflict" id="coi001"><p>I have read the journal's policy and the authors of this manuscript have the following competing interests: CPM, SB, TBN, and EM have filed a patent application for the use of digestive tract antigens as vaccine candidates in filariasis. This does not alter our adherence to all PLOS policies on sharing data and materials.</p></fn><fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: CPM SB TBN EM. Performed the experiments: CPM SB ZM KC RTT. Analyzed the data: CPM SB LEK JAZ ZM EM. Contributed reagents/materials/analysis tools: TDV TBN EM. Wrote the paper: CPM SB TBN EM.</p></fn><corresp id="cor001">* E-mail: <email>Edward.mitre@usuhs.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>14</day><month>9</month><year>2015</year></pub-date><pub-date pub-type="collection"><month>9</month><year>2015</year></pub-date><volume>9</volume><issue>9</issue><elocation-id>e0004054</elocation-id><history><date date-type="received"><day>3</day><month>4</month><year>2015</year></date><date date-type="accepted"><day>14</day><month>8</month><year>2015</year></date></history><permissions><license xlink:href="https://creativecommons.org/publicdomain/zero/1.0/"><license-p>This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/publicdomain/zero/1.0/">Creative Commons CC0</ext-link> public domain dedication</license-p></license></permissions><self-uri content-type="pdf" xlink:type="simple" xlink:href="pntd.0004054.pdf"></self-uri><abstract><p>Filarial worms are parasitic nematodes that cause devastating diseases such as lymphatic filariasis (LF) and onchocerciasis. Filariae are nematodes with complex anatomy including fully developed digestive tracts and reproductive organs. To better understand the basic biology of filarial parasites and to provide insights into drug targets and vaccine design, we conducted a proteomic analysis of different anatomic fractions of <italic>Brugia malayi</italic>, a causative agent of LF. Approximately 500 adult female <italic>B</italic>. <italic>malayi</italic> worms were dissected, and three anatomical fractions (body wall, digestive tract, and reproductive tract) were obtained. Proteins from each anatomical fraction were extracted, desalted, trypsinized, and analyzed by microcapillary reverse-phase liquid chromatography-tandem-mass spectrometry. In total, we identified 4,785 <italic>B</italic>. <italic>malayi</italic> proteins. While 1,894 were identified in all three anatomic fractions, 396 were positively identified only within the digestive tract, 114 only within the body wall, and 1,011 only within the reproductive tract. Gene set enrichment analysis revealed a bias for transporters to be present within the digestive tract, suggesting that the intestine of adult filariae is functional and important for nutrient uptake or waste removal. As expected, the body wall exhibited increased frequencies of cytoskeletal proteins, and the reproductive tract had increased frequencies of proteins involved in nuclear regulation and transcription. In assessing for possible vaccine candidates, we focused on proteins sequestered within the digestive tract, as these could possibly represent “hidden antigens” with low risk of prior allergic sensitization. We identified 106 proteins that are enriched in the digestive tract and are predicted to localize to the surface of cells in the the digestive tract. It is possible that some of these proteins are on the luminal surface and may be accessible by antibodies ingested by the worm. A subset of 27 of these proteins appear especially promising vaccine candidates as they contain significant non-cytoplasmic domains, only 1–2 transmembrane domains, and a high degree of homology to <italic>W</italic>. <italic>bancrofti</italic> and/or <italic>O</italic>. <italic>volvulus</italic>.</p></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>Filarial worms are parasitic worms that can live for years within humans and cause diseases such as elephantiasis and river blindness. In this study, we identified the proteins that exist within the worm's digestive tract, reproductive tract, and body wall. In addition to increasing our understanding of the basic biology of these parasites, this information is valuable for predicting which proteins may be candidates for vaccine development and rational drug design. Specifically, by analyzing which intestinal proteins are likely expressed on the surface of cells contained within the parasite's digestive tract and have little similarity to human proteins, we identified 27 possible vaccine candidates that warrant further study.</p></abstract><funding-group><funding-statement>This project was funded by Uniformed Services University of the Health Sciences Grant number R073UE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="4"></fig-count><table-count count="4"></table-count><page-count count="21"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevent data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevent data are within the paper and its Supporting Information files.</p></notes></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Maryland</li></region></list><tree><country name="États-Unis"><region name="Maryland"><name sortKey="Morris, C Paul" sort="Morris, C Paul" uniqKey="Morris C" first="C. Paul" last="Morris">C. Paul Morris</name></region><name sortKey="Bennuru, Sasisekhar" sort="Bennuru, Sasisekhar" uniqKey="Bennuru S" first="Sasisekhar" last="Bennuru">Sasisekhar Bennuru</name><name sortKey="Chan, King" sort="Chan, King" uniqKey="Chan K" first="King" last="Chan">King Chan</name><name sortKey="Kropp, Laura E" sort="Kropp, Laura E" uniqKey="Kropp L" first="Laura E." last="Kropp">Laura E. Kropp</name><name sortKey="Meng, Zhaojing" sort="Meng, Zhaojing" uniqKey="Meng Z" first="Zhaojing" last="Meng">Zhaojing Meng</name><name sortKey="Mitre, Edward" sort="Mitre, Edward" uniqKey="Mitre E" first="Edward" last="Mitre">Edward Mitre</name><name sortKey="Morris, C Paul" sort="Morris, C Paul" uniqKey="Morris C" first="C. Paul" last="Morris">C. Paul Morris</name><name sortKey="Nutman, Thomas B" sort="Nutman, Thomas B" uniqKey="Nutman T" first="Thomas B." last="Nutman">Thomas B. Nutman</name><name sortKey="Taylor, Rebekah T" sort="Taylor, Rebekah T" uniqKey="Taylor R" first="Rebekah T." last="Taylor">Rebekah T. Taylor</name><name sortKey="Veenstra, Timothy D" sort="Veenstra, Timothy D" uniqKey="Veenstra T" first="Timothy D." last="Veenstra">Timothy D. Veenstra</name><name sortKey="Zweben, Jesse A" sort="Zweben, Jesse A" uniqKey="Zweben J" first="Jesse A." last="Zweben">Jesse A. Zweben</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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