Filarial Excretory-Secretory Products Induce Human Monocytes to Produce Lymphangiogenic Mediators
Identifieur interne : 004358 ( Pmc/Curation ); précédent : 004357; suivant : 004359Filarial Excretory-Secretory Products Induce Human Monocytes to Produce Lymphangiogenic Mediators
Auteurs : Tiffany Weinkopff [États-Unis] ; Charles Mackenzie [États-Unis] ; Rob Eversole [États-Unis] ; Patrick J. Lammie [États-Unis]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2014.
Abstract
The nematodes
Url:
DOI: 10.1371/journal.pntd.0002893
PubMed: 25010672
PubMed Central: 4091784
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Filarial Excretory-Secretory Products Induce Human Monocytes to Produce Lymphangiogenic Mediators</title><author><name sortKey="Weinkopff, Tiffany" sort="Weinkopff, Tiffany" uniqKey="Weinkopff T" first="Tiffany" last="Weinkopff">Tiffany Weinkopff</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Cell Biology, University of Georgia, Athens, Georgia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cell Biology, University of Georgia, Athens, Georgia</wicri:regionArea></affiliation></author><author><name sortKey="Mackenzie, Charles" sort="Mackenzie, Charles" uniqKey="Mackenzie C" first="Charles" last="Mackenzie">Charles Mackenzie</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, Michigan, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, Michigan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan</wicri:regionArea></affiliation></author><author><name sortKey="Eversole, Rob" sort="Eversole, Rob" uniqKey="Eversole R" first="Rob" last="Eversole">Rob Eversole</name><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan</wicri:regionArea></affiliation></author><author><name sortKey="Lammie, Patrick J" sort="Lammie, Patrick J" uniqKey="Lammie P" first="Patrick J." last="Lammie">Patrick J. Lammie</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25010672</idno><idno type="pmc">4091784</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4091784</idno><idno type="RBID">PMC:4091784</idno><idno type="doi">10.1371/journal.pntd.0002893</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">004359</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004359</idno><idno type="wicri:Area/Pmc/Curation">004358</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">004358</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Filarial Excretory-Secretory Products Induce Human Monocytes to Produce Lymphangiogenic Mediators</title><author><name sortKey="Weinkopff, Tiffany" sort="Weinkopff, Tiffany" uniqKey="Weinkopff T" first="Tiffany" last="Weinkopff">Tiffany Weinkopff</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Cell Biology, University of Georgia, Athens, Georgia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Cell Biology, University of Georgia, Athens, Georgia</wicri:regionArea></affiliation></author><author><name sortKey="Mackenzie, Charles" sort="Mackenzie, Charles" uniqKey="Mackenzie C" first="Charles" last="Mackenzie">Charles Mackenzie</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, Michigan, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, Michigan</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan</wicri:regionArea></affiliation></author><author><name sortKey="Eversole, Rob" sort="Eversole, Rob" uniqKey="Eversole R" first="Rob" last="Eversole">Rob Eversole</name><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan</wicri:regionArea></affiliation></author><author><name sortKey="Lammie, Patrick J" sort="Lammie, Patrick J" uniqKey="Lammie P" first="Patrick J." last="Lammie">Patrick J. Lammie</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia</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"><p>The nematodes <italic>Wuchereria bancrofti</italic> and <italic>Brugia</italic> spp. infect over 120 million people worldwide, causing lymphedema, elephantiasis and hydrocele, collectively known as lymphatic filariasis. Most infected individuals appear to be asymptomatic, but many exhibit sub-clinical manifestations including the lymphangiectasia that likely contributes to the development of lymphedema and elephantiasis. As adult worm excretory-secretory products (ES) do not directly activate lymphatic endothelial cells (LEC), we investigated the role of monocyte/macrophage-derived soluble factors in the development of filarial lymphatic pathology. We analyzed the production of IL-8, IL-6 and VEGF-A by peripheral blood mononuclear cells (PBMC) from naïve donors following stimulation with filarial ES products. ES-stimulated PBMCs produced significantly more IL-8, IL-6 and VEGF-A compared to cells cultured in medium alone; CD14<sup>+</sup> monocytes appear to be the primary producers of IL-8 and VEGF-A, but not IL-6. Furthermore, IL-8, IL-6 and VEGF-A induced <italic>in vitro</italic> tubule formation in LEC Matrigel cultures. Matrigel plugs supplemented with IL-8, IL-6, VEGF-A, or with supernatants from ES-stimulated PBMCs and implanted <italic>in vivo</italic> stimulated lymphangiogenesis. Collectively, these data support the hypothesis that monocytes/macrophages exposed to filarial ES products may modulate lymphatic function through the secretion of soluble factors that stimulate the vessel growth associated with the pathogenesis of filarial disease.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Ottesen, Ea" uniqKey="Ottesen E">EA Ottesen</name></author><author><name sortKey="Duke, Bo" uniqKey="Duke B">BO Duke</name></author><author><name sortKey="Karam, M" uniqKey="Karam M">M Karam</name></author><author><name sortKey="Behbehani, K" uniqKey="Behbehani K">K Behbehani</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Nutman, Tb" uniqKey="Nutman T">TB Nutman</name></author><author><name sortKey="Kumaraswami, V" uniqKey="Kumaraswami V">V Kumaraswami</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Freedman, Do" 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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, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25010672</article-id><article-id pub-id-type="pmc">4091784</article-id><article-id pub-id-type="publisher-id">PNTD-D-13-00934</article-id><article-id pub-id-type="doi">10.1371/journal.pntd.0002893</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 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>Monocytes</subject></subj-group></subj-group></subj-group><subj-group><subject>Immune Cells</subject></subj-group></subj-group></subj-group></subj-group><subj-group><subject>Immunology</subject><subj-group><subject>Clinical Immunology</subject><subj-group><subject>Immunopathology</subject></subj-group></subj-group></subj-group><subj-group><subject>Microbiology</subject></subj-group><subj-group><subject>Parasitology</subject></subj-group></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Medicine and Health Sciences</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Emerging Infectious Diseases</subject></subj-group></subj-group><subj-group><subject>Pathology and Laboratory Medicine</subject><subj-group><subject>Pathogenesis</subject><subj-group><subject>Host-Pathogen Interactions</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Filarial Excretory-Secretory Products Induce Human Monocytes to Produce Lymphangiogenic Mediators</article-title><alt-title alt-title-type="running-head">Lymphangiectasia in Lymphatic Filariasis</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Weinkopff</surname><given-names>Tiffany</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 contrib-type="author"><name><surname>Mackenzie</surname><given-names>Charles</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Eversole</surname><given-names>Rob</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lammie</surname><given-names>Patrick J.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Department of Cell Biology, University of Georgia, Athens, Georgia, United States of America</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Department of Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, Michigan, United States of America</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Department of Biological Sciences, Western Michigan University, Kalamazoo, Michigan, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Specht</surname><given-names>Sabine</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University Clinic Bonn, Germany</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>wtiff@vet.upenn.edu</email></corresp><fn fn-type="conflict"><p>I have read the journal's policy and have the following conflicts: I have received funding from Glaxo SmithKline in the past, but this funding was not used or related in any way to the present study. This does not alter our adherence to all PLOS NTDs policies on sharing data and materials.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: TW PJL CM. Performed the experiments: TW CM RE. Analyzed the data: TW CM RE PJL. Contributed reagents/materials/analysis tools: CM RE PJL. Wrote the paper: TW CM PJL.</p></fn></author-notes><pub-date pub-type="collection"><month>7</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>10</day><month>7</month><year>2014</year></pub-date><volume>8</volume><issue>7</issue><elocation-id>e2893</elocation-id><history><date date-type="received"><day>12</day><month>6</month><year>2013</year></date><date date-type="accepted"><day>12</day><month>4</month><year>2014</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><p>The nematodes <italic>Wuchereria bancrofti</italic> and <italic>Brugia</italic> spp. infect over 120 million people worldwide, causing lymphedema, elephantiasis and hydrocele, collectively known as lymphatic filariasis. Most infected individuals appear to be asymptomatic, but many exhibit sub-clinical manifestations including the lymphangiectasia that likely contributes to the development of lymphedema and elephantiasis. As adult worm excretory-secretory products (ES) do not directly activate lymphatic endothelial cells (LEC), we investigated the role of monocyte/macrophage-derived soluble factors in the development of filarial lymphatic pathology. We analyzed the production of IL-8, IL-6 and VEGF-A by peripheral blood mononuclear cells (PBMC) from naïve donors following stimulation with filarial ES products. ES-stimulated PBMCs produced significantly more IL-8, IL-6 and VEGF-A compared to cells cultured in medium alone; CD14<sup>+</sup> monocytes appear to be the primary producers of IL-8 and VEGF-A, but not IL-6. Furthermore, IL-8, IL-6 and VEGF-A induced <italic>in vitro</italic> tubule formation in LEC Matrigel cultures. Matrigel plugs supplemented with IL-8, IL-6, VEGF-A, or with supernatants from ES-stimulated PBMCs and implanted <italic>in vivo</italic> stimulated lymphangiogenesis. Collectively, these data support the hypothesis that monocytes/macrophages exposed to filarial ES products may modulate lymphatic function through the secretion of soluble factors that stimulate the vessel growth associated with the pathogenesis of filarial disease.</p></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>Lymphatic filariasis is caused by parasitic worms with approximately 120 million people infected worldwide and over 1 billion people at risk. The adult worms reside in host lymphatic vessels (LV) but most infected individuals do not present with overt clinical symptoms. Individuals exhibiting lymphedema, a common form of the disease, are often antigen negative; however, infected individuals, though often asymptomatic, have dilated LVs suggesting that early damage to the lymphatic architecture may lead to lymphedema in these infected individuals. In the LVs, adult worms release excretory-secretory (ES) products. Filarial ES products do not directly activate lymphatic endothelial cells (LEC), so we hypothesized that accessory cells may activate LECs indirectly and contribute to the development of disease. Here, we show that adult filarial ES products induce human blood cells, specifically monocytes, to produce lymphangiogenic factors such as IL-8 and VEGF-A and that these factors induce the formation of LVs <italic>in vivo</italic>. These results support a role for filarial ES products in altering the lymphatic architecture in filarial-infected individuals and this may contribute to LV pathology and the development of lymphedema.</p></abstract><funding-group><funding-statement>This work was supported by a grant from Glaxo SmithKline to MSU for filarial disease investigation as well as a training grant to the Center for Tropical and Emerging Infectious Diseases (T32 AI 060546) with additional support from the Centers for Disease Control and Prevention's Emerging Infectious Disease Program. 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><page-count count="12"></page-count></counts></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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