Maternal Filarial Infection Influences the Development of Regulatory T Cells in Children from Infancy to Early Childhood
Identifieur interne : 008A17 ( Ncbi/Merge ); précédent : 008A16; suivant : 008A18Maternal Filarial Infection Influences the Development of Regulatory T Cells in Children from Infancy to Early Childhood
Auteurs : Madhusmita Bal ; Manoranjan Ranjit ; K. Gopinath Achary ; Ashok K. SatapathySource :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2016.
Abstract
Children born from filarial infected mothers are comparatively more susceptible to filarial infection than the children born to uninfected mothers. But the mechanism of such increased susceptibility to infection in early childhood is not exactly known. Several studies have shown the association of active filarial infection with T cell hypo-responsiveness which is mediated by regulatory T cells (Tregs). Since the Tregs develop in the thymus from CD4+ CD25hi thymocytes at an early stage of the human fetus, it can be hypothesized that the maternal infection during pregnancy affects the development of Tregs in children at birth as well as early childhood. Hence the present study was designed to test the hypothesis by selecting a cohort of pregnant mothers and children born to them subsequently in a filarial endemic area of Odisha, India.
A total number of 49 pregnant mothers and children born to them subsequently have been followed up (mean duration 4.4 years) in an area where the microfilariae (Mf) rate has come down to <1% after institution of 10 rounds of annual mass drug administration (MDA). The infection status of mother, cord and children were assessed through detection of microfilariae (Mf) and circulating filarial antigen (CFA). Expression of Tregs cells were measured by flow cytometry. The levels of IL-10 were evaluated by using commercially available ELISA kit. A significantly high level of IL-10 and Tregs have been observed in children born to infected mother compared to children of uninfected mother at the time of birth as well as during early childhood. Moreover a positive correlation between Tregs and IL-10 has been observed among the children born to infected mother.
From these observations we predict that early priming of the fetal immune system by filarial antigens modulate the development of Tregs, which ultimately scale up the production of IL-10 in neonates and creates a milieu for high rate of acquisition of infection in children born to infected mothers. The mechanism of susceptibility and implication of the results in global elimination programme of filariasis has been discussed.
Url:
DOI: 10.1371/journal.pntd.0005144
PubMed: 27861499
PubMed Central: 5115651
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Maternal Filarial Infection Influences the Development of Regulatory T Cells in Children from Infancy to Early Childhood</title><author><name sortKey="Bal, Madhusmita" sort="Bal, Madhusmita" uniqKey="Bal M" first="Madhusmita" last="Bal">Madhusmita Bal</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Ranjit, Manoranjan" sort="Ranjit, Manoranjan" uniqKey="Ranjit M" first="Manoranjan" last="Ranjit">Manoranjan Ranjit</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Achary, K Gopinath" sort="Achary, K Gopinath" uniqKey="Achary K" first="K. Gopinath" last="Achary">K. Gopinath Achary</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Satapathy, Ashok K" sort="Satapathy, Ashok K" uniqKey="Satapathy A" first="Ashok K." last="Satapathy">Ashok K. Satapathy</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27861499</idno><idno type="pmc">5115651</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5115651</idno><idno type="RBID">PMC:5115651</idno><idno type="doi">10.1371/journal.pntd.0005144</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">004298</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004298</idno><idno type="wicri:Area/Pmc/Curation">004297</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">004297</idno><idno type="wicri:Area/Pmc/Checkpoint">000797</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000797</idno><idno type="wicri:Area/Ncbi/Merge">008A17</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Maternal Filarial Infection Influences the Development of Regulatory T Cells in Children from Infancy to Early Childhood</title><author><name sortKey="Bal, Madhusmita" sort="Bal, Madhusmita" uniqKey="Bal M" first="Madhusmita" last="Bal">Madhusmita Bal</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Ranjit, Manoranjan" sort="Ranjit, Manoranjan" uniqKey="Ranjit M" first="Manoranjan" last="Ranjit">Manoranjan Ranjit</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Achary, K Gopinath" sort="Achary, K Gopinath" uniqKey="Achary K" first="K. Gopinath" last="Achary">K. Gopinath Achary</name><affiliation><nlm:aff id="aff001"></nlm:aff></affiliation></author><author><name sortKey="Satapathy, Ashok K" sort="Satapathy, Ashok K" uniqKey="Satapathy A" first="Ashok K." last="Satapathy">Ashok K. Satapathy</name><affiliation><nlm:aff id="aff001"></nlm:aff></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="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec id="sec001"><title>Background</title><p>Children born from filarial infected mothers are comparatively more susceptible to filarial infection than the children born to uninfected mothers. But the mechanism of such increased susceptibility to infection in early childhood is not exactly known. Several studies have shown the association of active filarial infection with T cell hypo-responsiveness which is mediated by regulatory T cells (Tregs). Since the Tregs develop in the thymus from CD4+ CD25<sup>hi</sup> thymocytes at an early stage of the human fetus, it can be hypothesized that the maternal infection during pregnancy affects the development of Tregs in children at birth as well as early childhood. Hence the present study was designed to test the hypothesis by selecting a cohort of pregnant mothers and children born to them subsequently in a filarial endemic area of Odisha, India.</p></sec><sec id="sec002"><title>Methodology and Principal finding</title><p>A total number of 49 pregnant mothers and children born to them subsequently have been followed up (mean duration 4.4 years) in an area where the microfilariae (Mf) rate has come down to <1% after institution of 10 rounds of annual mass drug administration (MDA). The infection status of mother, cord and children were assessed through detection of microfilariae (Mf) and circulating filarial antigen (CFA). Expression of Tregs cells were measured by flow cytometry. The levels of IL-10 were evaluated by using commercially available ELISA kit. A significantly high level of IL-10 and Tregs have been observed in children born to infected mother compared to children of uninfected mother at the time of birth as well as during early childhood. Moreover a positive correlation between Tregs and IL-10 has been observed among the children born to infected mother.</p></sec><sec id="sec003"><title>Significance</title><p>From these observations we predict that early priming of the fetal immune system by filarial antigens modulate the development of Tregs, which ultimately scale up the production of IL-10 in neonates and creates a milieu for high rate of acquisition of infection in children born to infected mothers. The mechanism of susceptibility and implication of the results in global elimination programme of filariasis has been discussed.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Rebollo, Mp" uniqKey="Rebollo M">MP Rebollo</name></author><author><name sortKey="Bockarie, Mj" uniqKey="Bockarie M">MJ Bockarie</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bal, Ms" uniqKey="Bal M">MS Bal</name></author><author><name sortKey="Mandal, Nn" uniqKey="Mandal N">NN Mandal</name></author><author><name sortKey="Das, Mk" uniqKey="Das M">MK Das</name></author><author><name sortKey="Kar, Sk" uniqKey="Kar S">SK Kar</name></author><author><name sortKey="Sarangi, Ss" uniqKey="Sarangi S">SS Sarangi</name></author><author><name sortKey="Beuria, Mk" uniqKey="Beuria M">MK Beuria</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bal, Ms" uniqKey="Bal M">MS 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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">27861499</article-id><article-id pub-id-type="pmc">5115651</article-id><article-id pub-id-type="doi">10.1371/journal.pntd.0005144</article-id><article-id pub-id-type="publisher-id">PNTD-D-16-00911</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Cell biology</subject><subj-group><subject>Cellular types</subject><subj-group><subject>Animal cells</subject><subj-group><subject>Blood cells</subject><subj-group><subject>White blood cells</subject><subj-group><subject>T cells</subject><subj-group><subject>Regulatory T cells</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Cell biology</subject><subj-group><subject>Cellular types</subject><subj-group><subject>Animal cells</subject><subj-group><subject>Immune cells</subject><subj-group><subject>White blood cells</subject><subj-group><subject>T cells</subject><subj-group><subject>Regulatory T cells</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune cells</subject><subj-group><subject>White blood cells</subject><subj-group><subject>T cells</subject><subj-group><subject>Regulatory T cells</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune cells</subject><subj-group><subject>White blood cells</subject><subj-group><subject>T cells</subject><subj-group><subject>Regulatory T cells</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Pediatrics</subject><subj-group><subject>Pediatric Infections</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cell Processes</subject><subj-group><subject>Cell Cycle and Cell Division</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>People and Places</subject><subj-group><subject>Population Groupings</subject><subj-group><subject>Age Groups</subject><subj-group><subject>Children</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>People and Places</subject><subj-group><subject>Population Groupings</subject><subj-group><subject>Families</subject><subj-group><subject>Children</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Parasitic Diseases</subject><subj-group><subject>Helminth Infections</subject><subj-group><subject>Filariasis</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Immune Physiology</subject><subj-group><subject>Cytokines</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Immune Physiology</subject><subj-group><subject>Cytokines</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune System</subject><subj-group><subject>Innate Immune System</subject><subj-group><subject>Cytokines</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune System</subject><subj-group><subject>Innate Immune System</subject><subj-group><subject>Cytokines</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Developmental Biology</subject><subj-group><subject>Molecular Development</subject><subj-group><subject>Cytokines</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Body Fluids</subject><subj-group><subject>Blood</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Body Fluids</subject><subj-group><subject>Blood</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Body Fluids</subject><subj-group><subject>Blood</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Body Fluids</subject><subj-group><subject>Blood</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Hematology</subject><subj-group><subject>Blood</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune Response</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune Response</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Maternal Filarial Infection Influences the Development of Regulatory T Cells in Children from Infancy to Early Childhood</article-title><alt-title alt-title-type="running-head">Maternal Filarial Infection and Regulatory T Cells</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Bal</surname><given-names>Madhusmita</given-names></name><xref ref-type="corresp" rid="cor001">*</xref><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Ranjit</surname><given-names>Manoranjan</given-names></name><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Achary</surname><given-names>K. Gopinath</given-names></name><xref ref-type="aff" rid="aff001"></xref></contrib><contrib contrib-type="author"><name><surname>Satapathy</surname><given-names>Ashok K.</given-names></name><xref ref-type="aff" rid="aff001"></xref></contrib></contrib-group><aff id="aff001"><addr-line>Division of Immunology, Regional Medical Research Center (Indian Council of Medical Research), Chandrasekharpur, Odisha, India</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Layland</surname><given-names>Laura Elizabeth</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University Hospital of Bonn, GERMANY</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold> MB.</p></list-item><list-item><p><bold>Formal analysis:</bold> KGA.</p></list-item><list-item><p><bold>Investigation:</bold> MB MR KGA AKS.</p></list-item><list-item><p><bold>Methodology:</bold> MB.</p></list-item><list-item><p><bold>Project administration:</bold> MB.</p></list-item><list-item><p><bold>Resources:</bold> MB MR KGA.</p></list-item><list-item><p><bold>Writing – original draft:</bold> MB MR.</p></list-item></list></p></fn><corresp id="cor001">* E-mail: <email>balmadhusmita@gmail.com</email></corresp></author-notes><pub-date pub-type="epub"><day>18</day><month>11</month><year>2016</year></pub-date><pub-date pub-type="collection"><month>11</month><year>2016</year></pub-date><volume>10</volume><issue>11</issue><elocation-id>e0005144</elocation-id><history><date date-type="received"><day>18</day><month>5</month><year>2016</year></date><date date-type="accepted"><day>27</day><month>10</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 Bal et al</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Bal et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pntd.0005144.pdf"></self-uri><abstract><sec id="sec001"><title>Background</title><p>Children born from filarial infected mothers are comparatively more susceptible to filarial infection than the children born to uninfected mothers. But the mechanism of such increased susceptibility to infection in early childhood is not exactly known. Several studies have shown the association of active filarial infection with T cell hypo-responsiveness which is mediated by regulatory T cells (Tregs). Since the Tregs develop in the thymus from CD4+ CD25<sup>hi</sup> thymocytes at an early stage of the human fetus, it can be hypothesized that the maternal infection during pregnancy affects the development of Tregs in children at birth as well as early childhood. Hence the present study was designed to test the hypothesis by selecting a cohort of pregnant mothers and children born to them subsequently in a filarial endemic area of Odisha, India.</p></sec><sec id="sec002"><title>Methodology and Principal finding</title><p>A total number of 49 pregnant mothers and children born to them subsequently have been followed up (mean duration 4.4 years) in an area where the microfilariae (Mf) rate has come down to <1% after institution of 10 rounds of annual mass drug administration (MDA). The infection status of mother, cord and children were assessed through detection of microfilariae (Mf) and circulating filarial antigen (CFA). Expression of Tregs cells were measured by flow cytometry. The levels of IL-10 were evaluated by using commercially available ELISA kit. A significantly high level of IL-10 and Tregs have been observed in children born to infected mother compared to children of uninfected mother at the time of birth as well as during early childhood. Moreover a positive correlation between Tregs and IL-10 has been observed among the children born to infected mother.</p></sec><sec id="sec003"><title>Significance</title><p>From these observations we predict that early priming of the fetal immune system by filarial antigens modulate the development of Tregs, which ultimately scale up the production of IL-10 in neonates and creates a milieu for high rate of acquisition of infection in children born to infected mothers. The mechanism of susceptibility and implication of the results in global elimination programme of filariasis has been discussed.</p></sec></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>Lymphatic filariasis caused by thread like filarial worms involves asymptomatic to acute and/or disfiguring chronic conditions like lymphoedema, elephantiasis and scrotal swelling. Infection occurs when filarial parasites are transmitted to humans through mosquitoes. Adult worms lodge in the lymphatic system and disrupt the immune system that causes the disease. Nonetheless the infection if present during pregnancy, it affects the immune system of the unborn child in such a way that they become more susceptible to infection. But how the immune system of a fetus is affected by the maternal filarial infection is not known. Since regulatory T cells are responsible for development of hyporesponsiveness, a condition that supports the active filarial infection, and develops in thymus at an early stage of the human fetal development, we hypothesized that maternal filarial infection might be affecting the development of Tregs cell. Because Tregs secret IL-10, a regulatory cytokine, we have also measured its level in children born to infected and uninfected mother and correlate it with Tregs. We have observed a significantly high as well as a positive correlation between Tregs and IL-10 levels in children born to infected mother than the children of uninfected mother at the time of birth as well as early childhood indicating that Tregs and IL-10 contribute to immune modulation during pregnancy. Since ongoing MDA excludes pregnant mothers and children below 2 years of age, hence implementation of supervised therapy at the time of adolescent through MDA may help the programme in achieving the target of global elimination of LF by 2020.</p></abstract><funding-group><funding-statement>This study was funded as intramural project by Indian Council of Medical Research, New Delhi. The funder 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="6"></fig-count><table-count count="1"></table-count><page-count count="15"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper.</p></notes></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Achary, K Gopinath" sort="Achary, K Gopinath" uniqKey="Achary K" first="K. Gopinath" last="Achary">K. Gopinath Achary</name><name sortKey="Bal, Madhusmita" sort="Bal, Madhusmita" uniqKey="Bal M" first="Madhusmita" last="Bal">Madhusmita Bal</name><name sortKey="Ranjit, Manoranjan" sort="Ranjit, Manoranjan" uniqKey="Ranjit M" first="Manoranjan" last="Ranjit">Manoranjan Ranjit</name><name sortKey="Satapathy, Ashok K" sort="Satapathy, Ashok K" uniqKey="Satapathy A" first="Ashok K." last="Satapathy">Ashok K. Satapathy</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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