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Lymphangiogenesis Is Induced by Mycobacterial Granulomas via Vascular Endothelial Growth Factor Receptor-3 and Supports Systemic T-Cell Responses against Mycobacterial Antigen

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Lymphangiogenesis Is Induced by Mycobacterial Granulomas via Vascular Endothelial Growth Factor Receptor-3 and Supports Systemic T-Cell Responses against Mycobacterial Antigen

Auteurs : Jeffrey Harding ; Anna Ritter ; Aditya Rayasam ; Zsuzsanna Fabry ; Matyas Sandor

Source :

The American Journal of Pathology [ 0002-9440 ] ; 2015.

RBID : PMC:4305185

Abstract

Granulomatous inflammation is characteristic of many autoimmune and infectious diseases. The lymphatic drainage of these inflammatory sites remains poorly understood, despite an expanding understanding of lymphatic role in inflammation and disease. Here, we show that the lymph vessel growth factor Vegf-c is up-regulated in Bacillus Calmette-Guerin– and Mycobacterium tuberculosis–induced granulomas, and that infection results in lymph vessel sprouting and increased lymphatic area in granulomatous tissue. The observed lymphangiogenesis during infection was reduced by inhibition of vascular endothelial growth factor receptor 3. By using a model of chronic granulomatous infection, we also show that lymphatic remodeling of tissue persists despite resolution of acute infection and a 10- to 100-fold reduction in the number of bacteria and tissue-infiltrating leukocytes. Inhibition of vascular endothelial growth factor receptor 3 decreased the growth of new vessels, but also reduced the proliferation of antigen-specific T cells. Together, our data show that granuloma–up-regulated factors increase granuloma access to secondary lymph organs by lymphangiogenesis, and that this process facilitates the generation of systemic T-cell responses to granuloma-contained antigens.

Url:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4305185

DOI: 10.1016/j.ajpath.2014.09.020
PubMed: 25597700
PubMed Central: 4305185

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PMC:4305185

Le document en format XML

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<author><name sortKey="Harding, Jeffrey" sort="Harding, Jeffrey" uniqKey="Harding J" first="Jeffrey" last="Harding">Jeffrey Harding</name>
<affiliation><nlm:aff id="aff1">Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<affiliation><nlm:aff id="aff2">Cellular and Molecular Pathology Training Program, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<author><name sortKey="Ritter, Anna" sort="Ritter, Anna" uniqKey="Ritter A" first="Anna" last="Ritter">Anna Ritter</name>
<affiliation><nlm:aff id="aff1">Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<author><name sortKey="Rayasam, Aditya" sort="Rayasam, Aditya" uniqKey="Rayasam A" first="Aditya" last="Rayasam">Aditya Rayasam</name>
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<author><name sortKey="Fabry, Zsuzsanna" sort="Fabry, Zsuzsanna" uniqKey="Fabry Z" first="Zsuzsanna" last="Fabry">Zsuzsanna Fabry</name>
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<affiliation><nlm:aff id="aff2">Cellular and Molecular Pathology Training Program, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<author><name sortKey="Sandor, Matyas" sort="Sandor, Matyas" uniqKey="Sandor M" first="Matyas" last="Sandor">Matyas Sandor</name>
<affiliation><nlm:aff id="aff1">Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<affiliation><nlm:aff id="aff2">Cellular and Molecular Pathology Training Program, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Lymphangiogenesis Is Induced by Mycobacterial Granulomas via Vascular Endothelial Growth Factor Receptor-3 and Supports Systemic T-Cell Responses against Mycobacterial Antigen</title>
<author><name sortKey="Harding, Jeffrey" sort="Harding, Jeffrey" uniqKey="Harding J" first="Jeffrey" last="Harding">Jeffrey Harding</name>
<affiliation><nlm:aff id="aff1">Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<affiliation><nlm:aff id="aff2">Cellular and Molecular Pathology Training Program, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<author><name sortKey="Ritter, Anna" sort="Ritter, Anna" uniqKey="Ritter A" first="Anna" last="Ritter">Anna Ritter</name>
<affiliation><nlm:aff id="aff1">Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<author><name sortKey="Rayasam, Aditya" sort="Rayasam, Aditya" uniqKey="Rayasam A" first="Aditya" last="Rayasam">Aditya Rayasam</name>
<affiliation><nlm:aff id="aff3">Neuroscience Training Program, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
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<author><name sortKey="Fabry, Zsuzsanna" sort="Fabry, Zsuzsanna" uniqKey="Fabry Z" first="Zsuzsanna" last="Fabry">Zsuzsanna Fabry</name>
<affiliation><nlm:aff id="aff1">Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Cellular and Molecular Pathology Training Program, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
</affiliation>
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<author><name sortKey="Sandor, Matyas" sort="Sandor, Matyas" uniqKey="Sandor M" first="Matyas" last="Sandor">Matyas Sandor</name>
<affiliation><nlm:aff id="aff1">Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
</affiliation>
<affiliation><nlm:aff id="aff2">Cellular and Molecular Pathology Training Program, University of Wisconsin Madison, Madison, Wisconsin</nlm:aff>
</affiliation>
</author>
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<series><title level="j">The American Journal of Pathology</title>
<idno type="ISSN">0002-9440</idno>
<idno type="eISSN">1525-2191</idno>
<imprint><date when="2015">2015</date>
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<front><div type="abstract" xml:lang="en"><p>Granulomatous inflammation is characteristic of many autoimmune and infectious diseases. The lymphatic drainage of these inflammatory sites remains poorly understood, despite an expanding understanding of lymphatic role in inflammation and disease. Here, we show that the lymph vessel growth factor Vegf-c is up-regulated in Bacillus Calmette-Guerin– and <italic>Mycobacterium tuberculosis</italic>
–induced granulomas, and that infection results in lymph vessel sprouting and increased lymphatic area in granulomatous tissue. The observed lymphangiogenesis during infection was reduced by inhibition of vascular endothelial growth factor receptor 3. By using a model of chronic granulomatous infection, we also show that lymphatic remodeling of tissue persists despite resolution of acute infection and a 10- to 100-fold reduction in the number of bacteria and tissue-infiltrating leukocytes. Inhibition of vascular endothelial growth factor receptor 3 decreased the growth of new vessels, but also reduced the proliferation of antigen-specific T cells. Together, our data show that granuloma–up-regulated factors increase granuloma access to secondary lymph organs by lymphangiogenesis, and that this process facilitates the generation of systemic T-cell responses to granuloma-contained antigens.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
  <front><journal-meta><journal-id journal-id-type="nlm-ta">Am J Pathol</journal-id>
<journal-id journal-id-type="iso-abbrev">Am. J. Pathol</journal-id>
<journal-title-group><journal-title>The American Journal of Pathology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0002-9440</issn>
<issn pub-type="epub">1525-2191</issn>
<publisher><publisher-name>American Society for Investigative Pathology</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25597700</article-id>
<article-id pub-id-type="pmc">4305185</article-id>
<article-id pub-id-type="publisher-id">S0002-9440(14)00594-X</article-id>
<article-id pub-id-type="doi">10.1016/j.ajpath.2014.09.020</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Regular Article</subject>
<subj-group><subject>Immunopathology and Infectious Diseases</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Lymphangiogenesis Is Induced by Mycobacterial Granulomas via Vascular Endothelial Growth Factor Receptor-3 and Supports Systemic T-Cell Responses against Mycobacterial Antigen</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Harding</surname>
<given-names>Jeffrey</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
<xref rid="aff2" ref-type="aff">†</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ritter</surname>
<given-names>Anna</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rayasam</surname>
<given-names>Aditya</given-names>
</name>
<xref rid="aff3" ref-type="aff">‡</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fabry</surname>
<given-names>Zsuzsanna</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
<xref rid="aff2" ref-type="aff">†</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sandor</surname>
<given-names>Matyas</given-names>
</name>
<email>msandor@wisc.edu</email>
<xref rid="aff1" ref-type="aff">∗</xref>
<xref rid="aff2" ref-type="aff">†</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>∗</label>
Department of Pathology and Laboratory Medicine, School of Medicine and Public Health, University of Wisconsin Madison, Madison, Wisconsin</aff>
<aff id="aff2"><label>†</label>
Cellular and Molecular Pathology Training Program, University of Wisconsin Madison, Madison, Wisconsin</aff>
<aff id="aff3"><label>‡</label>
Neuroscience Training Program, University of Wisconsin Madison, Madison, Wisconsin</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Address correspondence to Matyas Sandor, Ph.D., 5468 MSC, 1300 University Ave., Madison, WI 53705. <email>msandor@wisc.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>1</day>
<month>2</month>
<year>2016</year>
</pub-date>
<pmc-comment> PMC Release delay is 12 months and 0 days 
 					and was based on .</pmc-comment>
      <pub-date pub-type="ppub"><month>2</month>
<year>2015</year>
</pub-date>
<volume>185</volume>
<issue>2</issue>
<fpage>432</fpage>
<lpage>445</lpage>
<history><date date-type="accepted"><day>30</day>
<month>9</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>© 2015 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>American Society for Investigative Pathology</copyright-holder>
<license><license-p>This document may be redistributed and reused, subject to <ext-link ext-link-type="uri" xlink:href="http://www.elsevier.com/wps/find/authorsview.authors/supplementalterms1.0">certain conditions</ext-link>
.</license-p>
</license>
</permissions>
<abstract><p>Granulomatous inflammation is characteristic of many autoimmune and infectious diseases. The lymphatic drainage of these inflammatory sites remains poorly understood, despite an expanding understanding of lymphatic role in inflammation and disease. Here, we show that the lymph vessel growth factor Vegf-c is up-regulated in Bacillus Calmette-Guerin– and <italic>Mycobacterium tuberculosis</italic>
–induced granulomas, and that infection results in lymph vessel sprouting and increased lymphatic area in granulomatous tissue. The observed lymphangiogenesis during infection was reduced by inhibition of vascular endothelial growth factor receptor 3. By using a model of chronic granulomatous infection, we also show that lymphatic remodeling of tissue persists despite resolution of acute infection and a 10- to 100-fold reduction in the number of bacteria and tissue-infiltrating leukocytes. Inhibition of vascular endothelial growth factor receptor 3 decreased the growth of new vessels, but also reduced the proliferation of antigen-specific T cells. Together, our data show that granuloma–up-regulated factors increase granuloma access to secondary lymph organs by lymphangiogenesis, and that this process facilitates the generation of systemic T-cell responses to granuloma-contained antigens.</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>

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Lymphangiogenesis Is Induced by Mycobacterial Granulomas via Vascular Endothelial Growth Factor Receptor-3 and Supports Systemic T-Cell Responses against Mycobacterial Antigen

Lymphangiogenesis Is Induced by Mycobacterial Granulomas via Vascular Endothelial Growth Factor Receptor-3 and Supports Systemic T-Cell Responses against Mycobacterial Antigen

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