Parasite-Antigen Driven Expansion of IL-5− and IL-5+ Th2 Human Subpopulations in Lymphatic Filariasis and Their Differential Dependence on IL-10 and TGFβ
Identifieur interne : 004348 ( Pmc/Curation ); précédent : 004347; suivant : 004349Parasite-Antigen Driven Expansion of IL-5− and IL-5+ Th2 Human Subpopulations in Lymphatic Filariasis and Their Differential Dependence on IL-10 and TGFβ
Auteurs : Rajamanickam Anuradha [Inde] ; Parakkal Jovvian George [Inde] ; Luke E. Hanna [États-Unis] ; Vedachalam Chandrasekaran [Inde] ; P. Paul Kumaran [Inde] ; Thomas B. Nutman [États-Unis] ; Subash Babu [Inde, États-Unis]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2014.
Abstract
Two different Th2 subsets have been defined recently on the basis of IL-5 expression – an IL-5+Th2 subset and an IL-5−Th2 subset in the setting of allergy. However, the role of these newly described CD4+ T cells subpopulations has not been explored in other contexts.
To study the role of the Th2 subpopulation in a chronic, tissue invasive parasitic infection (lymphatic filariasis), we examined the frequency of IL-5+IL-4+IL-13+ CD4+ T cells and IL-5−IL-4 IL-13+ CD4+ T cells in asymptomatic, infected individuals (INF) and compared them to frequencies (Fo) in filarial-uninfected (UN) individuals and to those with filarial lymphedema (CP).
INF individuals exhibited a significant increase in the spontaneously expressed and antigen-induced Fo of both Th2 subpopulations compared to the UN and CP. Interestingly, there was a positive correlation between the Fo of IL-5+Th2 cells and the absolute eosinophil and neutrophil counts; in addition there was a positive correlation between the frequency of the CD4+IL-5−Th2 subpopulation and the levels of parasite antigen – specific IgE and IgG4 in INF individuals. Moreover, blockade of IL-10 and/or TGFβ demonstrated that each of these 2 regulatory cytokines exert opposite effects on the different Th2 subsets. Finally, in those INF individuals cured of infection by anti-filarial therapy, there was a significantly decreased Fo of both Th2 subsets.
Our findings suggest that both IL-5+ and IL-5−Th2 cells play an important role in the regulation of immune responses in filarial infection and that these two Th2 subpopulations may be regulated by different cytokine-receptor mediated processes.
Url:
DOI: 10.1371/journal.pntd.0002658
PubMed: 24498448
PubMed Central: 3907332
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Parasite-Antigen Driven Expansion of IL-5<sup>−</sup> and IL-5<sup>+</sup> Th2 Human Subpopulations in Lymphatic Filariasis and Their Differential Dependence on IL-10 and TGFβ</title><author><name sortKey="Anuradha, Rajamanickam" sort="Anuradha, Rajamanickam" uniqKey="Anuradha R" first="Rajamanickam" last="Anuradha">Rajamanickam Anuradha</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>National Institutes of Health—International Center for Excellence in Research, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institutes of Health—International Center for Excellence in Research, Chennai</wicri:regionArea></affiliation></author><author><name sortKey="George, Parakkal Jovvian" sort="George, Parakkal Jovvian" uniqKey="George P" first="Parakkal Jovvian" last="George">Parakkal Jovvian George</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>National Institutes of Health—International Center for Excellence in Research, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institutes of Health—International Center for Excellence in Research, Chennai</wicri:regionArea></affiliation></author><author><name sortKey="Hanna, Luke E" sort="Hanna, Luke E" uniqKey="Hanna L" first="Luke E." last="Hanna">Luke E. Hanna</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland</wicri:regionArea></affiliation></author><author><name sortKey="Chandrasekaran, Vedachalam" sort="Chandrasekaran, Vedachalam" uniqKey="Chandrasekaran V" first="Vedachalam" last="Chandrasekaran">Vedachalam Chandrasekaran</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>National Institute for Research in Tuberculosis, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institute for Research in Tuberculosis, Chennai</wicri:regionArea></affiliation></author><author><name sortKey="Kumaran, P Paul" sort="Kumaran, P Paul" uniqKey="Kumaran P" first="P. Paul" last="Kumaran">P. Paul Kumaran</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>National Institute for Research in Tuberculosis, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institute for Research in Tuberculosis, Chennai</wicri:regionArea></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="1"><nlm:aff id="aff2"><addr-line>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland</wicri:regionArea></affiliation></author><author><name sortKey="Babu, Subash" sort="Babu, Subash" uniqKey="Babu S" first="Subash" last="Babu">Subash Babu</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>National Institutes of Health—International Center for Excellence in Research, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institutes of Health—International Center for Excellence in Research, Chennai</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24498448</idno><idno type="pmc">3907332</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3907332</idno><idno type="RBID">PMC:3907332</idno><idno type="doi">10.1371/journal.pntd.0002658</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">004349</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004349</idno><idno type="wicri:Area/Pmc/Curation">004348</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">004348</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Parasite-Antigen Driven Expansion of IL-5<sup>−</sup> and IL-5<sup>+</sup> Th2 Human Subpopulations in Lymphatic Filariasis and Their Differential Dependence on IL-10 and TGFβ</title><author><name sortKey="Anuradha, Rajamanickam" sort="Anuradha, Rajamanickam" uniqKey="Anuradha R" first="Rajamanickam" last="Anuradha">Rajamanickam Anuradha</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>National Institutes of Health—International Center for Excellence in Research, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institutes of Health—International Center for Excellence in Research, Chennai</wicri:regionArea></affiliation></author><author><name sortKey="George, Parakkal Jovvian" sort="George, Parakkal Jovvian" uniqKey="George P" first="Parakkal Jovvian" last="George">Parakkal Jovvian George</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>National Institutes of Health—International Center for Excellence in Research, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institutes of Health—International Center for Excellence in Research, Chennai</wicri:regionArea></affiliation></author><author><name sortKey="Hanna, Luke E" sort="Hanna, Luke E" uniqKey="Hanna L" first="Luke E." last="Hanna">Luke E. Hanna</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland</wicri:regionArea></affiliation></author><author><name sortKey="Chandrasekaran, Vedachalam" sort="Chandrasekaran, Vedachalam" uniqKey="Chandrasekaran V" first="Vedachalam" last="Chandrasekaran">Vedachalam Chandrasekaran</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>National Institute for Research in Tuberculosis, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institute for Research in Tuberculosis, Chennai</wicri:regionArea></affiliation></author><author><name sortKey="Kumaran, P Paul" sort="Kumaran, P Paul" uniqKey="Kumaran P" first="P. Paul" last="Kumaran">P. Paul Kumaran</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>National Institute for Research in Tuberculosis, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institute for Research in Tuberculosis, Chennai</wicri:regionArea></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="1"><nlm:aff id="aff2"><addr-line>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland</wicri:regionArea></affiliation></author><author><name sortKey="Babu, Subash" sort="Babu, Subash" uniqKey="Babu S" first="Subash" last="Babu">Subash Babu</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>National Institutes of Health—International Center for Excellence in Research, Chennai, India</addr-line></nlm:aff><country xml:lang="fr">Inde</country><wicri:regionArea>National Institutes of Health—International Center for Excellence in Research, Chennai</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland</wicri:regionArea></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="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Two different Th2 subsets have been defined recently on the basis of IL-5 expression – an IL-5<sup>+</sup>Th2 subset and an IL-5<sup>−</sup>Th2 subset in the setting of allergy. However, the role of these newly described CD4<sup>+</sup> T cells subpopulations has not been explored in other contexts.</p></sec><sec><title>Methods</title><p>To study the role of the Th2 subpopulation in a chronic, tissue invasive parasitic infection (lymphatic filariasis), we examined the frequency of IL-5<sup>+</sup>IL-4<sup>+</sup>IL-13<sup>+</sup> CD4<sup>+</sup> T cells and IL-5<sup>−</sup>IL-4 IL-13<sup>+</sup> CD4<sup>+</sup> T cells in asymptomatic, infected individuals (INF) and compared them to frequencies (F<sub>o</sub>) in filarial-uninfected (UN) individuals and to those with filarial lymphedema (CP).</p></sec><sec><title>Results</title><p>INF individuals exhibited a significant increase in the spontaneously expressed and antigen-induced F<sub>o</sub> of both Th2 subpopulations compared to the UN and CP. Interestingly, there was a positive correlation between the F<sub>o</sub> of IL-5<sup>+</sup>Th2 cells and the absolute eosinophil and neutrophil counts; in addition there was a positive correlation between the frequency of the CD4<sup>+</sup>IL-5<sup>−</sup>Th2 subpopulation and the levels of parasite antigen – specific IgE and IgG4 in INF individuals. Moreover, blockade of IL-10 and/or TGFβ demonstrated that each of these 2 regulatory cytokines exert opposite effects on the different Th2 subsets. Finally, in those INF individuals cured of infection by anti-filarial therapy, there was a significantly decreased F<sub>o</sub> of both Th2 subsets.</p></sec><sec><title>Conclusions</title><p>Our findings suggest that both IL-5<sup>+</sup> and IL-5<sup>−</sup>Th2 cells play an important role in the regulation of immune responses in filarial infection and that these two Th2 subpopulations may be regulated by different cytokine-receptor mediated processes.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Mosmann, Tr" uniqKey="Mosmann T">TR Mosmann</name></author><author><name sortKey="Cherwinski, H" uniqKey="Cherwinski H">H Cherwinski</name></author><author><name sortKey="Bond, Mw" uniqKey="Bond M">MW Bond</name></author><author><name sortKey="Giedlin, Ma" uniqKey="Giedlin M">MA Giedlin</name></author><author><name sortKey="Coffman, Rl" uniqKey="Coffman R">RL 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Nolan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Maizels, Rm" uniqKey="Maizels R">RM Maizels</name></author><author><name sortKey="Yazdanbakhsh, M" uniqKey="Yazdanbakhsh M">M Yazdanbakhsh</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<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, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24498448</article-id><article-id pub-id-type="pmc">3907332</article-id><article-id pub-id-type="publisher-id">PNTD-D-13-01028</article-id><article-id pub-id-type="doi">10.1371/journal.pntd.0002658</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune Cells</subject><subj-group><subject>T Cells</subject></subj-group></subj-group><subj-group><subject>Immune Response</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Parasitic Diseases</subject><subj-group><subject>Filariasis</subject><subject>Helminth Infection</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Parasite-Antigen Driven Expansion of IL-5<sup>−</sup> and IL-5<sup>+</sup> Th2 Human Subpopulations in Lymphatic Filariasis and Their Differential Dependence on IL-10 and TGFβ</article-title><alt-title alt-title-type="running-head">Th2 Subsets in Human Lymphatic Filariasis</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Anuradha</surname><given-names>Rajamanickam</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>George</surname><given-names>Parakkal Jovvian</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Hanna</surname><given-names>Luke E.</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Chandrasekaran</surname><given-names>Vedachalam</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kumaran</surname><given-names>P. Paul</given-names></name><xref ref-type="aff" rid="aff3"><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="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Babu</surname><given-names>Subash</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>National Institutes of Health—International Center for Excellence in Research, Chennai, India</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Laboratory of Parasitic Diseases, National Institutes of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></aff><aff id="aff3"><label>3</label><addr-line>National Institute for Research in Tuberculosis, Chennai, India</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Yazdanbakhsh</surname><given-names>Maria</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Leiden University Medical Center, Netherlands</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>sbabu@mail.nih.gov</email></corresp><fn fn-type="conflict"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: TBN SB. Performed the experiments: RA PJG. Analyzed the data: RA PJG. Contributed reagents/materials/analysis tools: LEH VC PPK. Wrote the paper: TBN SB.</p></fn></author-notes><pub-date pub-type="collection"><month>1</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>30</day><month>1</month><year>2014</year></pub-date><volume>8</volume><issue>1</issue><elocation-id>e2658</elocation-id><history><date date-type="received"><day>11</day><month>7</month><year>2013</year></date><date date-type="accepted"><day>7</day><month>12</month><year>2013</year></date></history><permissions><copyright-year>2014</copyright-year><license><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 Creative Commons CC0 public domain dedication.</license-p></license></permissions><abstract><sec><title>Background</title><p>Two different Th2 subsets have been defined recently on the basis of IL-5 expression – an IL-5<sup>+</sup>Th2 subset and an IL-5<sup>−</sup>Th2 subset in the setting of allergy. However, the role of these newly described CD4<sup>+</sup> T cells subpopulations has not been explored in other contexts.</p></sec><sec><title>Methods</title><p>To study the role of the Th2 subpopulation in a chronic, tissue invasive parasitic infection (lymphatic filariasis), we examined the frequency of IL-5<sup>+</sup>IL-4<sup>+</sup>IL-13<sup>+</sup> CD4<sup>+</sup> T cells and IL-5<sup>−</sup>IL-4 IL-13<sup>+</sup> CD4<sup>+</sup> T cells in asymptomatic, infected individuals (INF) and compared them to frequencies (F<sub>o</sub>) in filarial-uninfected (UN) individuals and to those with filarial lymphedema (CP).</p></sec><sec><title>Results</title><p>INF individuals exhibited a significant increase in the spontaneously expressed and antigen-induced F<sub>o</sub> of both Th2 subpopulations compared to the UN and CP. Interestingly, there was a positive correlation between the F<sub>o</sub> of IL-5<sup>+</sup>Th2 cells and the absolute eosinophil and neutrophil counts; in addition there was a positive correlation between the frequency of the CD4<sup>+</sup>IL-5<sup>−</sup>Th2 subpopulation and the levels of parasite antigen – specific IgE and IgG4 in INF individuals. Moreover, blockade of IL-10 and/or TGFβ demonstrated that each of these 2 regulatory cytokines exert opposite effects on the different Th2 subsets. Finally, in those INF individuals cured of infection by anti-filarial therapy, there was a significantly decreased F<sub>o</sub> of both Th2 subsets.</p></sec><sec><title>Conclusions</title><p>Our findings suggest that both IL-5<sup>+</sup> and IL-5<sup>−</sup>Th2 cells play an important role in the regulation of immune responses in filarial infection and that these two Th2 subpopulations may be regulated by different cytokine-receptor mediated processes.</p></sec></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>Th2 cells are CD4<sup>+</sup> T cells that produce a unique set of cytokines - IL-4, IL-5 and IL-13. Th2 cells are commonly associated with allergies, asthma and helminth infections. A common helminth infection that infects over 120 million people worldwide is lymphatic filarial infection caused by filarial parasites. We show here data that filarial infection is associated with the expansion of two types of Th2 cells, one which produces IL-4 and IL-13 alone without IL-5 and the other which produces all three cytokines. Interestingly, while the former subset is associated with the levels of antibodies - IgG4 and IgE; the latter is associated with the presence of eosinophilia in filarial infected individuals. In addition, these subsets appear to be modulated differently by the immunoregulatory cytokines - IL-10 and TGFβ. Therefore, our study highlights a novel regulation of Th2 cells and suggests that the Th2 compartment is quite heterogeneous in phenotype with possible functional consequences.</p></abstract><funding-group><funding-statement>This work was supported by the Intramural Research Program of the Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health. The funders had no role in study design, data collection and analysis, decision to publish or preparation of manuscript.</funding-statement></funding-group><counts><page-count count="11"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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