Cytomegalovirus Impairs Cytotrophoblast-Induced Lymphangiogenesis and Vascular Remodeling in an in Vivo Human Placentation Model
Identifieur interne : 002B64 ( Pmc/Curation ); précédent : 002B63; suivant : 002B65Cytomegalovirus Impairs Cytotrophoblast-Induced Lymphangiogenesis and Vascular Remodeling in an in Vivo Human Placentation Model
Auteurs : Takako Tabata [États-Unis] ; Matthew Petitt [États-Unis] ; June Fang-Hoover [États-Unis] ; Jose Rivera [États-Unis] ; Naoki Nozawa [Japon] ; Stephen Shiboski [États-Unis] ; Naoki Inoue [Japon] ; Lenore Pereira [États-Unis]Source :
- The American Journal of Pathology [ 0002-9440 ] ; 2012.
Abstract
We investigated human cytomegalovirus pathogenesis by comparing infection with the low-passage, endotheliotropic strain VR1814 and the attenuated laboratory strain AD169 in human placental villi as explants
Url:
DOI: 10.1016/j.ajpath.2012.08.003
PubMed: 22959908
PubMed Central: 3483806
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Human Placentation Model</title>
<author><name sortKey="Tabata, Takako" sort="Tabata, Takako" uniqKey="Tabata T" first="Takako" last="Tabata">Takako Tabata</name>
<affiliation wicri:level="2"><nlm:aff id="aff1">Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco</wicri:cityArea>
</affiliation>
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<author><name sortKey="Petitt, Matthew" sort="Petitt, Matthew" uniqKey="Petitt M" first="Matthew" last="Petitt">Matthew Petitt</name>
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<country>États-Unis</country>
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<wicri:cityArea>Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco</wicri:cityArea>
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<author><name sortKey="Fang Hoover, June" sort="Fang Hoover, June" uniqKey="Fang Hoover J" first="June" last="Fang-Hoover">June Fang-Hoover</name>
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<wicri:cityArea>Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco</wicri:cityArea>
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<author><name sortKey="Rivera, Jose" sort="Rivera, Jose" uniqKey="Rivera J" first="Jose" last="Rivera">Jose Rivera</name>
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<author><name sortKey="Nozawa, Naoki" sort="Nozawa, Naoki" uniqKey="Nozawa N" first="Naoki" last="Nozawa">Naoki Nozawa</name>
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<country xml:lang="fr">Japon</country>
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<author><name sortKey="Inoue, Naoki" sort="Inoue, Naoki" uniqKey="Inoue N" first="Naoki" last="Inoue">Naoki Inoue</name>
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<author><name sortKey="Pereira, Lenore" sort="Pereira, Lenore" uniqKey="Pereira L" first="Lenore" last="Pereira">Lenore Pereira</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Cytomegalovirus Impairs Cytotrophoblast-Induced Lymphangiogenesis and Vascular Remodeling in an <italic>in Vivo</italic>
Human Placentation Model</title>
<author><name sortKey="Tabata, Takako" sort="Tabata, Takako" uniqKey="Tabata T" first="Takako" last="Tabata">Takako Tabata</name>
<affiliation wicri:level="2"><nlm:aff id="aff1">Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Petitt, Matthew" sort="Petitt, Matthew" uniqKey="Petitt M" first="Matthew" last="Petitt">Matthew Petitt</name>
<affiliation wicri:level="2"><nlm:aff id="aff1">Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Fang Hoover, June" sort="Fang Hoover, June" uniqKey="Fang Hoover J" first="June" last="Fang-Hoover">June Fang-Hoover</name>
<affiliation wicri:level="2"><nlm:aff id="aff1">Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Rivera, Jose" sort="Rivera, Jose" uniqKey="Rivera J" first="Jose" last="Rivera">Jose Rivera</name>
<affiliation wicri:level="2"><nlm:aff id="aff2">Division of Experimental Medicine, Department of Medicine, San Francisco General Hospital, University of California, San Francisco, San Francisco, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Division of Experimental Medicine, Department of Medicine, San Francisco General Hospital, University of California, San Francisco, San Francisco</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Nozawa, Naoki" sort="Nozawa, Naoki" uniqKey="Nozawa N" first="Naoki" last="Nozawa">Naoki Nozawa</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">National Institutes of Infectious Diseases, Tokyo, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>National Institutes of Infectious Diseases, Tokyo</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Shiboski, Stephen" sort="Shiboski, Stephen" uniqKey="Shiboski S" first="Stephen" last="Shiboski">Stephen Shiboski</name>
<affiliation wicri:level="2"><nlm:aff id="aff4">Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, San Francisco, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, San Francisco</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Inoue, Naoki" sort="Inoue, Naoki" uniqKey="Inoue N" first="Naoki" last="Inoue">Naoki Inoue</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">National Institutes of Infectious Diseases, Tokyo, Japan</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>National Institutes of Infectious Diseases, Tokyo</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Pereira, Lenore" sort="Pereira, Lenore" uniqKey="Pereira L" first="Lenore" last="Pereira">Lenore Pereira</name>
<affiliation wicri:level="2"><nlm:aff id="aff1">Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco</wicri:cityArea>
</affiliation>
</author>
</analytic>
<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="2012">2012</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p>We investigated human cytomegalovirus pathogenesis by comparing infection with the low-passage, endotheliotropic strain VR1814 and the attenuated laboratory strain AD169 in human placental villi as explants <italic>in vitro</italic>
and xenografts transplanted into kidney capsules of SCID mice (ie, mice with severe combined immunodeficiency). In this <italic>in vivo</italic>
human placentation model, human cytotrophoblasts invade the renal parenchyma, remodel resident arteries, and induce a robust lymphangiogenic response. VR1814 replicated in villous and cell column cytotrophoblasts and reduced formation of anchoring villi <italic>in vitro</italic>
. In xenografts, infected cytotrophoblasts had a severely diminished capacity to invade and remodel resident arteries. Infiltrating lymphatic endothelial cells proliferated, aggregated, and failed to form lymphatic vessels. In contrast, AD169 grew poorly in cytotrophoblasts in explants, and anchoring villi formed normally <italic>in vitro</italic>
. Likewise, viral replication was impaired in xenografts, and cytotrophoblasts retained invasive capacity, but some partially remodeled blood vessels incorporated lymphatic endothelial cells and were permeable to blood. The expression of both vascular endothelial growth factor (VEGF)-C and basic fibroblast growth factor increased in VR1814-infected explants, whereas VEGF-A and soluble VEGF receptor-3 increased in those infected with AD169. Our results suggest that viral replication and paracrine factors could undermine vascular remodeling and cytotrophoblast-induced lymphangiogenesis, contributing to bleeding, hypoxia, and edema in pregnancies complicated by congenital human cytomegalovirus infection.</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">22959908</article-id>
<article-id pub-id-type="pmc">3483806</article-id>
<article-id pub-id-type="publisher-id">AJPA1040</article-id>
<article-id pub-id-type="doi">10.1016/j.ajpath.2012.08.003</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Regular Article</subject>
<subj-group><subject>Animal Models</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Cytomegalovirus Impairs Cytotrophoblast-Induced Lymphangiogenesis and Vascular Remodeling in an <italic>in Vivo</italic>
Human Placentation Model</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Tabata</surname>
<given-names>Takako</given-names>
</name>
<xref rid="aff1" ref-type="aff">⁎</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Petitt</surname>
<given-names>Matthew</given-names>
</name>
<xref rid="aff1" ref-type="aff">⁎</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fang-Hoover</surname>
<given-names>June</given-names>
</name>
<xref rid="aff1" ref-type="aff">⁎</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rivera</surname>
<given-names>Jose</given-names>
</name>
<xref rid="aff2" ref-type="aff">†</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nozawa</surname>
<given-names>Naoki</given-names>
</name>
<xref rid="aff3" ref-type="aff">‡</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shiboski</surname>
<given-names>Stephen</given-names>
</name>
<xref rid="aff4" ref-type="aff">§</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Inoue</surname>
<given-names>Naoki</given-names>
</name>
<xref rid="aff3" ref-type="aff">‡</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pereira</surname>
<given-names>Lenore</given-names>
</name>
<email>lenore.pereira@ucsf.edu</email>
<xref rid="aff1" ref-type="aff">⁎</xref>
<xref rid="cor1" ref-type="corresp">⁎</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>⁎</label>
Department of Cell and Tissue Biology, School of Dentistry, University of California, San Francisco, San Francisco, California</aff>
<aff id="aff2"><label>†</label>
Division of Experimental Medicine, Department of Medicine, San Francisco General Hospital, University of California, San Francisco, San Francisco, California</aff>
<aff id="aff4"><label>§</label>
Department of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco, San Francisco, California</aff>
<aff id="aff3"><label>‡</label>
National Institutes of Infectious Diseases, Tokyo, Japan</aff>
<author-notes><corresp id="cor1"><label>⁎</label>
Address reprint requests to Lenore Pereira, Ph.D., University of California, San Francisco, 513 Parnassus Ave, San Francisco, CA 94143-0640 <email>lenore.pereira@ucsf.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>1</day>
<month>11</month>
<year>2013</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>11</month>
<year>2012</year>
</pub-date>
<volume>181</volume>
<issue>5</issue>
<fpage>1540</fpage>
<lpage>1559</lpage>
<history><date date-type="accepted"><day>1</day>
<month>8</month>
<year>2012</year>
</date>
</history>
<permissions><copyright-statement>© 2012 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved.</copyright-statement>
<copyright-year>2012</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>We investigated human cytomegalovirus pathogenesis by comparing infection with the low-passage, endotheliotropic strain VR1814 and the attenuated laboratory strain AD169 in human placental villi as explants <italic>in vitro</italic>
and xenografts transplanted into kidney capsules of SCID mice (ie, mice with severe combined immunodeficiency). In this <italic>in vivo</italic>
human placentation model, human cytotrophoblasts invade the renal parenchyma, remodel resident arteries, and induce a robust lymphangiogenic response. VR1814 replicated in villous and cell column cytotrophoblasts and reduced formation of anchoring villi <italic>in vitro</italic>
. In xenografts, infected cytotrophoblasts had a severely diminished capacity to invade and remodel resident arteries. Infiltrating lymphatic endothelial cells proliferated, aggregated, and failed to form lymphatic vessels. In contrast, AD169 grew poorly in cytotrophoblasts in explants, and anchoring villi formed normally <italic>in vitro</italic>
. Likewise, viral replication was impaired in xenografts, and cytotrophoblasts retained invasive capacity, but some partially remodeled blood vessels incorporated lymphatic endothelial cells and were permeable to blood. The expression of both vascular endothelial growth factor (VEGF)-C and basic fibroblast growth factor increased in VR1814-infected explants, whereas VEGF-A and soluble VEGF receptor-3 increased in those infected with AD169. Our results suggest that viral replication and paracrine factors could undermine vascular remodeling and cytotrophoblast-induced lymphangiogenesis, contributing to bleeding, hypoxia, and edema in pregnancies complicated by congenital human cytomegalovirus infection.</p>
</abstract>
</article-meta>
</front>
</pmc>
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