Thioesterase PPT1 balances viral resistance and efficient T cell crosspriming in dendritic cells
Identifieur interne : 000673 ( Pmc/Curation ); précédent : 000672; suivant : 000674Thioesterase PPT1 balances viral resistance and efficient T cell crosspriming in dendritic cells
Auteurs : Pengju Ou ; Lifen Wen ; Xiaoli Liu ; Jiancheng Huang ; Xiaoling Huang ; Chaofei Su ; Ling Wang ; Hai Ni ; Boris Reizis ; Cliff Y. YangSource :
- The Journal of Experimental Medicine [ 0022-1007 ] ; 2019.
Abstract
Crosspriming of CD8+ T cells by dendritic cells is crucial for host response against cancer and intracellular microbial infections. Ou et al. demonstrates that palmitoyl-protein thioesterase PPT1 is a phagosomal pH rheostat enabling both viral resistance and efficient crosspriming in cDC1s.
Url:
DOI: 10.1084/jem.20190041
PubMed: 31262842
PubMed Central: 6719428
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<author><name sortKey="Liu, Xiaoli" sort="Liu, Xiaoli" uniqKey="Liu X" first="Xiaoli" last="Liu">Xiaoli Liu</name>
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<front><div type="abstract" xml:lang="en"><p>Crosspriming of CD8<sup>+</sup>
T cells by dendritic cells is crucial for host response against cancer and intracellular microbial infections. Ou et al. demonstrates that palmitoyl-protein thioesterase PPT1 is a phagosomal pH rheostat enabling both viral resistance and efficient crosspriming in cDC1s.</p>
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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">J Exp Med</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Exp. Med</journal-id>
<journal-id journal-id-type="publisher-id">jem</journal-id>
<journal-id journal-id-type="hwp">jem</journal-id>
<journal-title-group><journal-title>The Journal of Experimental Medicine</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-1007</issn>
<issn pub-type="epub">1540-9538</issn>
<publisher><publisher-name>Rockefeller University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31262842</article-id>
<article-id pub-id-type="pmc">6719428</article-id>
<article-id pub-id-type="publisher-id">20190041</article-id>
<article-id pub-id-type="doi">10.1084/jem.20190041</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Articles</subject>
<subj-group><subject>Article</subject>
</subj-group>
</subj-group>
<subj-group subj-group-type="hwp-journal-coll"><subject>312</subject>
<subject>311</subject>
</subj-group>
</article-categories>
<title-group><article-title>Thioesterase PPT1 balances viral resistance and efficient T cell crosspriming in dendritic cells</article-title>
<alt-title alt-title-type="short">PPT1 balances viral resistance and crosspriming</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Ou</surname>
<given-names>Pengju</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wen</surname>
<given-names>Lifen</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Xiaoli</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Huang</surname>
<given-names>Jiancheng</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Huang</surname>
<given-names>Xiaoling</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Su</surname>
<given-names>Chaofei</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Ling</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ni</surname>
<given-names>Hai</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0003-1140-7853</contrib-id>
<name><surname>Reizis</surname>
<given-names>Boris</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
<xref ref-type="author-notes" rid="afn6">*</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0002-2162-2912</contrib-id>
<name><surname>Yang</surname>
<given-names>Cliff Y.</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff4">4</xref>
<xref ref-type="author-notes" rid="afn6">*</xref>
<xref ref-type="corresp" rid="cor5"></xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<institution>Department of Immunology, Sun Yat-sen University Zhongshan School of Medicine, Guangzhou, Guangdong, China</institution>
</aff>
<aff id="aff2"><label>2</label>
<institution>Department of Chemotherapy, First Affiliated Hospital of Fujian Medical University, Fuzhou, Fujian, China</institution>
</aff>
<aff id="aff3"><label>3</label>
<institution>Department of Pathology, New York University School of Medicine, New York, NY</institution>
</aff>
<aff id="aff4"><label>4</label>
<institution>Key Laboratory of Tropical Disease Control, Sun Yat-sen University, Ministry of Education, Guangzhou, Guangdong, China</institution>
</aff>
<author-notes><corresp id="cor5">Correspondence to Cliff Y. Yang: <email>yangkeli6@mail.sysu.edu.cn</email>
</corresp>
<fn fn-type="equal" specific-use="equal" id="afn6"><label>*</label>
<p>B. Reizis and C.Y. Yang contributed equally to this paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>02</day>
<month>9</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>01</day>
<month>7</month>
<year>2019</year>
</pub-date>
<volume>216</volume>
<issue>9</issue>
<fpage>2091</fpage>
<lpage>2112</lpage>
<history><date date-type="received"><day>09</day>
<month>1</month>
<year>2019</year>
</date>
<date date-type="rev-recd"><day>05</day>
<month>5</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>12</day>
<month>6</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 Ou et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<ali:free_to_read start_date="2020-03-01"></ali:free_to_read>
<license><ali:license_ref specific-use="vor">http://www.rupress.org/terms/</ali:license_ref>
<ali:license_ref specific-use="vor" start_date="2020-03-01">https://creativecommons.org/licenses/by-nc-sa/4.0/</ali:license_ref>
<license-p>This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see <ext-link ext-link-type="uri" xlink:href="http://www.rupress.org/terms/">http://www.rupress.org/terms/</ext-link>
). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by-nc-sa/4.0/">https://creativecommons.org/licenses/by-nc-sa/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<self-uri xlink:role="icon" xlink:href="JEM_20190041_thumb.gif"></self-uri>
<abstract abstract-type="precis"><p>Crosspriming of CD8<sup>+</sup>
T cells by dendritic cells is crucial for host response against cancer and intracellular microbial infections. Ou et al. demonstrates that palmitoyl-protein thioesterase PPT1 is a phagosomal pH rheostat enabling both viral resistance and efficient crosspriming in cDC1s.</p>
</abstract>
<abstract><p>Conventional type 1 dendritic cells (cDC1s) are inherently resistant to many viruses but, paradoxically, possess fewer acidic phagosomes that enable antigen retention and cross-presentation. We report that palmitoyl-protein thioesterase 1 (PPT1), which catabolizes lipid-modified proteins in neurons, is highly expressed in cDC1s. PPT1-deficient DCs are more susceptible to vesicular stomatitis virus (VSV) infection, and mice with PPT1 deficiency in cDC1s show impaired response to VSV. Conversely, PPT1-deficient cDC1s enhance the priming of naive CD8<sup>+</sup>
T cells into tissue-resident KLRG1<sup>+</sup>
effectors and memory T cells, resulting in rapid clearance of tumors and <italic>Listeria monocytogenes</italic>
. Mechanistically, PPT1 protects steady state DCs from viruses by promoting antigen degradation and endosomal acidification via V-ATPase recruitment. After DC activation, immediate down-regulation of PPT1 is likely to facilitate efficient cross-presentation, production of costimulatory molecules and inflammatory cytokines. Thus, PPT1 acts as a molecular rheostat that allows cDC1s to crossprime efficiently without compromising viral resistance. These results suggest potential therapeutics to enhance cDC1-dependent crosspriming.</p>
</abstract>
<abstract abstract-type="graphical"><title>Graphical Abstract</title>
<p><fig id="GA" orientation="portrait" position="float"><graphic xlink:href="JEM_20190041_GA"></graphic>
</fig>
</p>
</abstract>
<funding-group><award-group id="sp1"><funding-source>National Key R&D Program of China</funding-source>
<award-id rid="sp1">2018YFA0508300</award-id>
</award-group>
<award-group id="sp2"><funding-source>National Natural Science Foundation of China</funding-source>
<award-id rid="sp2">31570863</award-id>
</award-group>
<award-group id="sp3"><funding-source><institution-wrap><institution>Guangdong Innovative and Entrepreneurial Research Team Program</institution>
<institution-id institution-id-type="DOI">https://doi.org/10.13039/100012541</institution-id>
</institution-wrap>
</funding-source>
<award-id rid="sp3">2016ZT06S638</award-id>
</award-group>
<award-group id="sp4"><funding-source><institution-wrap><institution>111 Project</institution>
<institution-id institution-id-type="DOI">https://doi.org/10.13039/501100012176</institution-id>
</institution-wrap>
</funding-source>
<award-id rid="sp4">B12003</award-id>
</award-group>
<award-group id="sp5"><funding-source><institution-wrap><institution>National Institutes of Health</institution>
<institution-id institution-id-type="DOI">https://doi.org/10.13039/100000002</institution-id>
</institution-wrap>
</funding-source>
<award-id rid="sp5">AI072571</award-id>
</award-group>
</funding-group>
<counts><page-count count="22"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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