The HIF-1α/LC3-II Axis Impacts Fungal Immunity in Human Macrophages
Identifieur interne : 000589 ( Pmc/Curation ); précédent : 000588; suivant : 000590The HIF-1α/LC3-II Axis Impacts Fungal Immunity in Human Macrophages
Auteurs : Dirk Friedrich [Allemagne] ; Dorinja Zapf [Allemagne] ; Björn Lohse [Allemagne] ; Roger A. Fecher [États-Unis] ; George S. Deepe [États-Unis] ; Jan Rupp [Allemagne]Source :
- Infection and Immunity [ 0019-9567 ] ; 2019.
Abstract
The fungal pathogen
Url:
DOI: 10.1128/IAI.00125-19
PubMed: 31036602
PubMed Central: 6589057
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<front><div type="abstract" xml:lang="en"><p>The fungal pathogen <named-content content-type="genus-species">Histoplasma capsulatum</named-content>
causes a spectrum of disease, ranging from local pulmonary infection to disseminated disease. The organism seeks residence in macrophages, which are permissive for its survival.</p>
</div>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Infect Immun</journal-id>
<journal-id journal-id-type="iso-abbrev">Infect. Immun</journal-id>
<journal-id journal-id-type="hwp">iai</journal-id>
<journal-id journal-id-type="pmc">iai</journal-id>
<journal-id journal-id-type="publisher-id">IAI</journal-id>
<journal-title-group><journal-title>Infection and Immunity</journal-title>
</journal-title-group>
<issn pub-type="ppub">0019-9567</issn>
<issn pub-type="epub">1098-5522</issn>
<publisher><publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31036602</article-id>
<article-id pub-id-type="pmc">6589057</article-id>
<article-id pub-id-type="publisher-id">00125-19</article-id>
<article-id pub-id-type="doi">10.1128/IAI.00125-19</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Cellular Microbiology: Pathogen-Host Cell Molecular Interactions</subject>
</subj-group>
</article-categories>
<title-group><article-title>The HIF-1α/LC3-II Axis Impacts Fungal Immunity in Human Macrophages</article-title>
<alt-title alt-title-type="running-head">Elevated HIF-1α Mounts Fungal Immunity in Macrophages</alt-title>
<alt-title alt-title-type="short-authors">Friedrich et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" equal-contrib="yes"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-8812-489X</contrib-id>
<name><surname>Friedrich</surname>
<given-names>Dirk</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Zapf</surname>
<given-names>Dorinja</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="no"><name><surname>Lohse</surname>
<given-names>Björn</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="no"><name><surname>Fecher</surname>
<given-names>Roger A.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">*</xref>
</contrib>
<contrib contrib-type="author" equal-contrib="yes"><name><surname>Deepe</surname>
<given-names>George S.</given-names>
<suffix>Jr.</suffix>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes" equal-contrib="yes"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-8722-1233</contrib-id>
<name><surname>Rupp</surname>
<given-names>Jan</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<aff id="aff1"><label>a</label>
<addr-line>Department of Infectious Diseases and Microbiology, University of Lübeck, Lübeck, Germany</addr-line>
</aff>
<aff id="aff2"><label>b</label>
<addr-line>Division of Infectious Diseases, University of Cincinnati College of Medicine, Cincinnati, Ohio, USA</addr-line>
</aff>
<aff id="aff3"><label>c</label>
<addr-line>Division of Immunobiology, Cincinnati Children’s Hospital Medical Center, University of Cincinnati, Cincinnati, Ohio, USA</addr-line>
</aff>
<aff id="aff4"><label>d</label>
<addr-line>German Center for Infection Research (DZIF), Hamburg-Lübeck-Borstel-Riems, Germany</addr-line>
</aff>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Pirofski</surname>
<given-names>Liise-anne</given-names>
</name>
<role>Editor</role>
<aff>Albert Einstein College of Medicine</aff>
</contrib>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Jan Rupp, <email>jan.rupp@uksh.de</email>
.</corresp>
<fn id="fn1" fn-type="present-address"><label>*</label>
<p>Present address: Roger A. Fecher, Montefiore Medical Center, Albert Einstein College of Medicine, New York, New York, USA.</p>
</fn>
<fn fn-type="equal"><p>G.S.D. and J.R. contributed equally to this work, and D.F. and D.Z. contributed equally to this work.</p>
</fn>
<fn fn-type="other"><p><bold>Citation</bold>
Friedrich D, Zapf D, Lohse B, Fecher RA, Deepe GS, Jr, Rupp J. 2019. The HIF-1α/LC3-II axis impacts fungal immunity in human macrophages. Infect Immun 87:e00125-19. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/IAI.00125-19">https://doi.org/10.1128/IAI.00125-19</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epreprint"><day>29</day>
<month>4</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>20</day>
<month>6</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><month>7</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>20</day>
<month>6</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>87</volume>
<issue>7</issue>
<elocation-id>e00125-19</elocation-id>
<history><date date-type="received"><day>13</day>
<month>2</month>
<year>2019</year>
</date>
<date date-type="rev-request"><day>1</day>
<month>3</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>16</day>
<month>4</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2019 Friedrich et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>Friedrich et al.</copyright-holder>
<license license-type="open-access" xlink:href="https://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="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="IAI.00125-19.pdf"></self-uri>
<abstract abstract-type="precis"><p>The fungal pathogen <named-content content-type="genus-species">Histoplasma capsulatum</named-content>
causes a spectrum of disease, ranging from local pulmonary infection to disseminated disease. The organism seeks residence in macrophages, which are permissive for its survival.</p>
</abstract>
<abstract><title>ABSTRACT</title>
<p>The fungal pathogen <named-content content-type="genus-species">Histoplasma capsulatum</named-content>
causes a spectrum of disease, ranging from local pulmonary infection to disseminated disease. The organism seeks residence in macrophages, which are permissive for its survival. Hypoxia-inducible factor 1α (HIF-1α), a principal regulator of innate immunity to pathogens, is necessary for macrophage-mediated immunity to <named-content content-type="genus-species">H. capsulatum</named-content>
in mice. In the present study, we analyzed the effect of HIF-1α in human macrophages infected with this fungus. HIF-1α stabilization was detected in peripheral blood monocyte-derived macrophages at 2 to 24 h after infection with viable yeast cells. Further, host mitochondrial respiration and glycolysis were enhanced. In contrast, heat-killed yeasts induced early, but not later, stabilization of HIF-1α. Since the absence of HIF-1α is detrimental to host control of infection, we asked if large amounts of HIF-1α protein, exceeding those induced by <named-content content-type="genus-species">H. capsulatum</named-content>
, altered macrophage responses to this pathogen. Exposure of infected macrophages to an HIF-1α stabilizer significantly reduced recovery of <named-content content-type="genus-species">H. capsulatum</named-content>
from macrophages and produced a decrement in mitochondrial respiration and glycolysis compared to those of controls. We observed recruitment of the autophagy-related protein LC3-II to the phagosome, whereas enhancing HIF-1α reduced phagosomal decoration. This finding suggested that <named-content content-type="genus-species">H. capsulatum</named-content>
exploited an autophagic process to survive. In support of this assertion, inhibition of autophagy activated macrophages to limit intracellular growth of <named-content content-type="genus-species">H. capsulatum</named-content>
. Thus, enhancement of HIF-1α creates a hostile environment for yeast cells in human macrophages by interrupting the ability of the pathogen to provoke host cell autophagy.</p>
</abstract>
<kwd-group><title>KEYWORDS</title>
<kwd>HIF-1</kwd>
<kwd><italic>Histoplasma capsulatum</italic>
</kwd>
<kwd>LC3</kwd>
<kwd>autophagy</kwd>
<kwd>fungal immunity</kwd>
<kwd>macrophages</kwd>
</kwd-group>
<funding-group><award-group id="award1"><funding-source><institution-wrap><institution>HHS | National Institutes of Health (NIH)</institution>
<institution-id>https://doi.org/10.13039/100000002</institution-id>
</institution-wrap>
</funding-source>
<award-id>AI-106269</award-id>
<principal-award-recipient><name><surname>Fecher</surname>
<given-names>Roger</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award2"><funding-source><institution-wrap><institution>HHS | National Institutes of Health (NIH)</institution>
<institution-id>https://doi.org/10.13039/100000002</institution-id>
</institution-wrap>
</funding-source>
<award-id>AI 133797</award-id>
<principal-award-recipient><name><surname>Deepe</surname>
<given-names>George S.</given-names>
<suffix>Jr.</suffix>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award3"><funding-source><institution-wrap><institution>Deutsche Forschungsgemeinschaft (DFG)</institution>
<institution-id>https://doi.org/10.13039/501100001659</institution-id>
</institution-wrap>
</funding-source>
<award-id>IRTG1911</award-id>
<principal-award-recipient><name><surname>Rupp</surname>
<given-names>Jan</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award4"><funding-source><institution-wrap><institution>Deutsche Forschungsgemeinschaft (DFG)</institution>
<institution-id>https://doi.org/10.13039/501100001659</institution-id>
</institution-wrap>
</funding-source>
<award-id>IRTG1911</award-id>
<principal-award-recipient><name><surname>Friedrich</surname>
<given-names>Dirk</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award5"><funding-source><institution-wrap><institution>Deutsche Forschungsgemeinschaft (DFG)</institution>
<institution-id>https://doi.org/10.13039/501100001659</institution-id>
</institution-wrap>
</funding-source>
<award-id>IRTG1911</award-id>
<principal-award-recipient><name><surname>Zapf</surname>
<given-names>Dorinja</given-names>
</name>
</principal-award-recipient>
</award-group>
<award-group id="award6"><funding-source><institution-wrap><institution>Deutsche Forschungsgemeinschaft (DFG)</institution>
<institution-id>https://doi.org/10.13039/501100001659</institution-id>
</institution-wrap>
</funding-source>
<award-id>IRTG1911</award-id>
<principal-award-recipient><name><surname>Lohse</surname>
<given-names>Björn</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
<counts><count count="1" count-type="supplementary-material"></count>
<fig-count count="7"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="51"></ref-count>
<page-count count="13"></page-count>
<word-count count="7359"></word-count>
</counts>
<custom-meta-group><custom-meta><meta-name>cover-date</meta-name>
<meta-value>July 2019</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>
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