Lymphangiogenesis and Lymphatic Remodeling Induced by Filarial Parasites: Implications for Pathogenesis
Identifieur interne : 003684 ( Pmc/Checkpoint ); précédent : 003683; suivant : 003685Lymphangiogenesis and Lymphatic Remodeling Induced by Filarial Parasites: Implications for Pathogenesis
Auteurs : Sasisekhar Bennuru ; Thomas B. NutmanSource :
- PLoS Pathogens [ 1553-7366 ] ; 2009.
Abstract
Even in the absence of an adaptive immune system in murine models, lymphatic dilatation and dysfunction occur in filarial infections, although severe irreversible lymphedema and elephantiasis appears to require an intact adaptive immune response in human infections. To address how filarial parasites and their antigens influence the lymphatics directly, human lymphatic endothelial cells were exposed to filarial antigens, live parasites, or infected patient serum. Live filarial parasites or filarial antigens induced both significant LEC proliferation and differentiation into tube-like structures
Url:
DOI: 10.1371/journal.ppat.1000688
PubMed: 20011114
PubMed Central: 2781552
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Lymphangiogenesis and Lymphatic Remodeling Induced by Filarial Parasites: Implications for Pathogenesis</title><author><name sortKey="Bennuru, Sasisekhar" sort="Bennuru, Sasisekhar" uniqKey="Bennuru S" first="Sasisekhar" last="Bennuru">Sasisekhar Bennuru</name><affiliation><nlm:aff id="aff1"></nlm:aff></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><nlm:aff id="aff1"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">20011114</idno><idno type="pmc">2781552</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2781552</idno><idno type="RBID">PMC:2781552</idno><idno type="doi">10.1371/journal.ppat.1000688</idno><date when="2009">2009</date><idno type="wicri:Area/Pmc/Corpus">004532</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004532</idno><idno type="wicri:Area/Pmc/Curation">004531</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">004531</idno><idno type="wicri:Area/Pmc/Checkpoint">003684</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">003684</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Lymphangiogenesis and Lymphatic Remodeling Induced by Filarial Parasites: Implications for Pathogenesis</title><author><name sortKey="Bennuru, Sasisekhar" sort="Bennuru, Sasisekhar" uniqKey="Bennuru S" first="Sasisekhar" last="Bennuru">Sasisekhar Bennuru</name><affiliation><nlm:aff id="aff1"></nlm:aff></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><nlm:aff id="aff1"></nlm:aff></affiliation></author></analytic><series><title level="j">PLoS Pathogens</title><idno type="ISSN">1553-7366</idno><idno type="eISSN">1553-7374</idno><imprint><date when="2009">2009</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Even in the absence of an adaptive immune system in murine models, lymphatic dilatation and dysfunction occur in filarial infections, although severe irreversible lymphedema and elephantiasis appears to require an intact adaptive immune response in human infections. To address how filarial parasites and their antigens influence the lymphatics directly, human lymphatic endothelial cells were exposed to filarial antigens, live parasites, or infected patient serum. Live filarial parasites or filarial antigens induced both significant LEC proliferation and differentiation into tube-like structures <italic>in vitro</italic>. Moreover, serum from patently infected (microfilaria positive) patients and those with longstanding chronic lymphatic obstruction induced significantly increased LEC proliferation compared to sera from uninfected individuals. Differentiation of LEC into tube-like networks was found to be associated with significantly increased levels of matrix metalloproteases and inhibition of their TIMP inhibitors (Tissue inhibitors of matrix metalloproteases). Comparison of global gene expression induced by live parasites in LEC to parasite-unexposed LEC demonstrated that filarial parasites altered the expression of those genes involved in cellular organization and development as well as those associated with junction adherence pathways that in turn decreased trans-endothelial transport as assessed by FITC-Dextran. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plospath</journal-id><journal-title-group><journal-title>PLoS Pathogens</journal-title></journal-title-group><issn pub-type="ppub">1553-7366</issn><issn pub-type="epub">1553-7374</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">20011114</article-id><article-id pub-id-type="pmc">2781552</article-id><article-id pub-id-type="publisher-id">09-PLPA-RA-0612R3</article-id><article-id pub-id-type="doi">10.1371/journal.ppat.1000688</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline"><subject>Infectious Diseases/Helminth Infections</subject><subject>Infectious Diseases/Neglected Tropical Diseases</subject></subj-group></article-categories><title-group><article-title>Lymphangiogenesis and Lymphatic Remodeling Induced by Filarial Parasites: Implications for Pathogenesis</article-title><alt-title alt-title-type="running-head">Lymphangiogenesis in Lymphatic Filariasis</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Bennuru</surname><given-names>Sasisekhar</given-names></name><xref ref-type="aff" rid="aff1"></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Nutman</surname><given-names>Thomas B.</given-names></name><xref ref-type="aff" rid="aff1"></xref></contrib></contrib-group><aff id="aff1"><addr-line>Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Kazura</surname><given-names>James W.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1">Case Western Reserve University, United States of America</aff><author-notes><corresp id="cor1">* E-mail: <email>bennurus@niaid.nih.gov</email></corresp><fn fn-type="con"><p>Conceived and designed the experiments: SB TBN. Performed the experiments: SB. Analyzed the data: SB TBN. Contributed reagents/materials/analysis tools: TBN. Wrote the paper: SB.</p></fn></author-notes><pub-date pub-type="collection"><month>12</month><year>2009</year></pub-date><pub-date pub-type="epub"><day>11</day><month>12</month><year>2009</year></pub-date><volume>5</volume><issue>12</issue><elocation-id>e1000688</elocation-id><history><date date-type="received"><day>17</day><month>4</month><year>2009</year></date><date date-type="accepted"><day>11</day><month>11</month><year>2009</year></date></history><permissions><copyright-statement>This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.</copyright-statement><copyright-year>2009</copyright-year><license xlink:href="https://creativecommons.org/publicdomain/zero/1.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.</license-p></license></permissions><abstract><p>Even in the absence of an adaptive immune system in murine models, lymphatic dilatation and dysfunction occur in filarial infections, although severe irreversible lymphedema and elephantiasis appears to require an intact adaptive immune response in human infections. To address how filarial parasites and their antigens influence the lymphatics directly, human lymphatic endothelial cells were exposed to filarial antigens, live parasites, or infected patient serum. Live filarial parasites or filarial antigens induced both significant LEC proliferation and differentiation into tube-like structures <italic>in vitro</italic>. Moreover, serum from patently infected (microfilaria positive) patients and those with longstanding chronic lymphatic obstruction induced significantly increased LEC proliferation compared to sera from uninfected individuals. Differentiation of LEC into tube-like networks was found to be associated with significantly increased levels of matrix metalloproteases and inhibition of their TIMP inhibitors (Tissue inhibitors of matrix metalloproteases). Comparison of global gene expression induced by live parasites in LEC to parasite-unexposed LEC demonstrated that filarial parasites altered the expression of those genes involved in cellular organization and development as well as those associated with junction adherence pathways that in turn decreased trans-endothelial transport as assessed by FITC-Dextran. The data suggest that filarial parasites directly induce lymphangiogenesis and lymphatic differentiation and provide insight into the mechanisms underlying the pathology seen in lymphatic filariasis.</p></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>The nematode parasites <italic>Brugia malayi</italic> and <italic>Wuchereria bancrofti</italic> are the major organisms responsible for lymphatic filariasis. Lymphatic filariasis is characterized by the dysfunction of the lymphatics that can lead to severe (and often) irreversible lymphedema and elephantiasis. Current advances in distinguishing blood vascular from lymphatic endothelial cells have allowed the direct study of the interaction between live filarial parasites and their lymphatic niche. In the quest towards understanding parasite-lymphatic endothelium interactions, we observed that the filarial antigens have a specific but differential stimulatory capacity towards the lymphatics and cause them to differentiate into tube-like vascular networks <italic>in vitro</italic> that resemble the formation of collateral lymphatics <italic>in vivo</italic>. This was a lymphatic-specific phenomenon, as the filarial parasites or antigen did not exhibit similar effects on the human umbilical vein endothelial cells. The differentiation of the lymphatic endothelial monolayers into vascular networks was not dependent on typical markers of lymphangiogenesis but rather involves the matrix metalloproteases and their inhibitors that suggest lymphatic matrix remodeling rather than rendering of the lymphatics hyper-permeable as has been postulated previously.</p></abstract><counts><page-count count="12"></page-count></counts></article-meta></front></pmc><affiliations><list></list><tree><noCountry><name sortKey="Bennuru, Sasisekhar" sort="Bennuru, Sasisekhar" uniqKey="Bennuru S" first="Sasisekhar" last="Bennuru">Sasisekhar Bennuru</name><name sortKey="Nutman, Thomas B" sort="Nutman, Thomas B" uniqKey="Nutman T" first="Thomas B." last="Nutman">Thomas B. Nutman</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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