A bioactive mammalian disaccharide associated with autoimmunity activates STING-TBK1-dependent immune response
Identifieur interne : 000140 ( Pmc/Curation ); précédent : 000139; suivant : 000141A bioactive mammalian disaccharide associated with autoimmunity activates STING-TBK1-dependent immune response
Auteurs : Charles S. Fermaintt [États-Unis] ; Kanae Sano [Japon] ; Zhida Liu [États-Unis] ; Nozomi Ishii [Japon] ; Junichi Seino [Japon] ; Nicole Dobbs [États-Unis] ; Tadashi Suzuki [Japon] ; Yang-Xin Fu [États-Unis] ; Mark A. Lehrman [États-Unis] ; Ichiro Matsuo [Japon] ; Nan Yan [États-Unis]Source :
- Nature Communications [ 2041-1723 ] ; 2019.
Abstract
Glycans from microbial pathogens are well known pathogen-associated molecular patterns that are recognized by the host immunity; however, little is known about whether and how mammalian self-glycans activate the host immune response, especially in the context of autoimmune disease. Using biochemical fractionation and two-dimensional HPLC, we identify an abundant and bioactive free glycan, the Manβ1-4GlcNAc disaccharide in
Url:
DOI: 10.1038/s41467-019-10319-5
PubMed: 31147550
PubMed Central: 6542856
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Fermaintt</name><affiliation wicri:level="2"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Immunology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>Dallas</wicri:cityArea></affiliation></author><author><name sortKey="Sano, Kanae" sort="Sano, Kanae" uniqKey="Sano K" first="Kanae" last="Sano">Kanae Sano</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9269 4097</institution-id><institution-id institution-id-type="GRID">grid.256642.1</institution-id><institution>Division of Molecular Science,</institution><institution>Gunma University,</institution></institution-wrap>Maebashi, 371-8510 Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Maebashi</wicri:regionArea></affiliation></author><author><name sortKey="Liu, Zhida" sort="Liu, Zhida" uniqKey="Liu Z" first="Zhida" last="Liu">Zhida Liu</name><affiliation wicri:level="2"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Pathology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>Dallas</wicri:cityArea></affiliation></author><author><name sortKey="Ishii, Nozomi" sort="Ishii, Nozomi" uniqKey="Ishii N" first="Nozomi" last="Ishii">Nozomi Ishii</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9269 4097</institution-id><institution-id institution-id-type="GRID">grid.256642.1</institution-id><institution>Division of Molecular Science,</institution><institution>Gunma University,</institution></institution-wrap>Maebashi, 371-8510 Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Maebashi</wicri:regionArea></affiliation></author><author><name sortKey="Seino, Junichi" sort="Seino, Junichi" uniqKey="Seino J" first="Junichi" last="Seino">Junichi Seino</name><affiliation wicri:level="1"><nlm:aff id="Aff4">Glycometabolic Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, 351-0198 Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Glycometabolic Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako</wicri:regionArea></affiliation></author><author><name sortKey="Dobbs, Nicole" sort="Dobbs, Nicole" uniqKey="Dobbs N" first="Nicole" last="Dobbs">Nicole Dobbs</name><affiliation wicri:level="2"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Immunology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>Dallas</wicri:cityArea></affiliation></author><author><name sortKey="Suzuki, Tadashi" sort="Suzuki, Tadashi" uniqKey="Suzuki T" first="Tadashi" last="Suzuki">Tadashi Suzuki</name><affiliation wicri:level="1"><nlm:aff id="Aff4">Glycometabolic Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, 351-0198 Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Glycometabolic Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako</wicri:regionArea></affiliation></author><author><name sortKey="Fu, Yang Xin" sort="Fu, Yang Xin" uniqKey="Fu Y" first="Yang-Xin" last="Fu">Yang-Xin Fu</name><affiliation wicri:level="2"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Pathology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>Dallas</wicri:cityArea></affiliation></author><author><name sortKey="Lehrman, Mark A" sort="Lehrman, Mark A" uniqKey="Lehrman M" first="Mark A." last="Lehrman">Mark A. Lehrman</name><affiliation wicri:level="2"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Pharmacology, Department of Microbiology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>Dallas</wicri:cityArea></affiliation></author><author><name sortKey="Matsuo, Ichiro" sort="Matsuo, Ichiro" uniqKey="Matsuo I" first="Ichiro" last="Matsuo">Ichiro Matsuo</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9269 4097</institution-id><institution-id institution-id-type="GRID">grid.256642.1</institution-id><institution>Division of Molecular Science,</institution><institution>Gunma University,</institution></institution-wrap>Maebashi, 371-8510 Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Maebashi</wicri:regionArea></affiliation></author><author><name sortKey="Yan, Nan" sort="Yan, Nan" uniqKey="Yan N" first="Nan" last="Yan">Nan Yan</name><affiliation wicri:level="2"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Immunology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>Dallas</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Microbiology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Texas</region></placeName><wicri:cityArea>Dallas</wicri:cityArea></affiliation></author></analytic><series><title level="j">Nature Communications</title><idno type="eISSN">2041-1723</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Glycans from microbial pathogens are well known pathogen-associated molecular patterns that are recognized by the host immunity; however, little is known about whether and how mammalian self-glycans activate the host immune response, especially in the context of autoimmune disease. Using biochemical fractionation and two-dimensional HPLC, we identify an abundant and bioactive free glycan, the Manβ1-4GlcNAc disaccharide in <italic>TREX1</italic>-associated autoimmune diseases. We report that both monosaccharide residues and the β1-4 linkage are critical for bioactivity of this disaccharide. We also show that Manβ1-4GlcNAc is produced by oligosaccharyltransferase hydrolysis of lipid-linked oligosaccharides in the ER lumen, followed by ENGase and mannosidase processing in the cytosol and lysosomes. Furthermore, synthetic Manβ1-4GlcNAc disaccharide stimulates a broad immune response in vitro, which is in part dependent on the STING-TBK1 pathway, and enhances antibody response in vivo. Together, our data identify Manβ1-4GlcNAc as a novel innate immune modulator associated with chronic autoimmune diseases.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Sancho, D" uniqKey="Sancho D">D Sancho</name></author><author><name sortKey="Reis E Sousa, C" uniqKey="Reis E Sousa C">C Reis e Sousa</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rabinovich, Ga" uniqKey="Rabinovich G">GA Rabinovich</name></author><author><name sortKey="Van Kooyk, Y" uniqKey="Van Kooyk Y">Y van Kooyk</name></author><author><name sortKey="Cobb, Ba" uniqKey="Cobb B">BA Cobb</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Green, Rs" uniqKey="Green R">RS Green</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Yan, N" uniqKey="Yan N">N Yan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hasan, M" uniqKey="Hasan 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Nat Commun</journal-id><journal-id journal-id-type="iso-abbrev">Nat Commun</journal-id><journal-title-group><journal-title>Nature Communications</journal-title></journal-title-group><issn pub-type="epub">2041-1723</issn><publisher><publisher-name>Nature Publishing Group UK</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31147550</article-id><article-id pub-id-type="pmc">6542856</article-id><article-id pub-id-type="publisher-id">10319</article-id><article-id pub-id-type="doi">10.1038/s41467-019-10319-5</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>A bioactive mammalian disaccharide associated with autoimmunity activates STING-TBK1-dependent immune response</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Fermaintt</surname><given-names>Charles S.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Sano</surname><given-names>Kanae</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Liu</surname><given-names>Zhida</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Ishii</surname><given-names>Nozomi</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Seino</surname><given-names>Junichi</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Dobbs</surname><given-names>Nicole</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Suzuki</surname><given-names>Tadashi</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-4809-825X</contrib-id><name><surname>Fu</surname><given-names>Yang-Xin</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Lehrman</surname><given-names>Mark A.</given-names></name><xref ref-type="aff" rid="Aff5">5</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-0740-1184</contrib-id><name><surname>Matsuo</surname><given-names>Ichiro</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0002-0637-3989</contrib-id><name><surname>Yan</surname><given-names>Nan</given-names></name><address><email>nan.yan@utsouthwestern.edu</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff6">6</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Immunology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9269 4097</institution-id><institution-id institution-id-type="GRID">grid.256642.1</institution-id><institution>Division of Molecular Science,</institution><institution>Gunma University,</institution></institution-wrap>Maebashi, 371-8510 Japan</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Pathology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</aff><aff id="Aff4"><label>4</label>Glycometabolic Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, 351-0198 Japan</aff><aff id="Aff5"><label>5</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Pharmacology, Department of Microbiology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</aff><aff id="Aff6"><label>6</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0000 9482 7121</institution-id><institution-id institution-id-type="GRID">grid.267313.2</institution-id><institution>Department of Microbiology,</institution><institution>University of Texas Southwestern Medical Center,</institution></institution-wrap>Dallas, TX 75390 USA</aff></contrib-group><pub-date pub-type="epub"><day>30</day><month>5</month><year>2019</year></pub-date><pub-date pub-type="pmc-release"><day>30</day><month>5</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>10</volume><elocation-id>2377</elocation-id><history><date date-type="received"><day>24</day><month>4</month><year>2018</year></date><date date-type="accepted"><day>25</day><month>4</month><year>2019</year></date></history><permissions><copyright-statement>© The Author(s) 2019</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold> This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Glycans from microbial pathogens are well known pathogen-associated molecular patterns that are recognized by the host immunity; however, little is known about whether and how mammalian self-glycans activate the host immune response, especially in the context of autoimmune disease. Using biochemical fractionation and two-dimensional HPLC, we identify an abundant and bioactive free glycan, the Manβ1-4GlcNAc disaccharide in <italic>TREX1</italic>-associated autoimmune diseases. We report that both monosaccharide residues and the β1-4 linkage are critical for bioactivity of this disaccharide. We also show that Manβ1-4GlcNAc is produced by oligosaccharyltransferase hydrolysis of lipid-linked oligosaccharides in the ER lumen, followed by ENGase and mannosidase processing in the cytosol and lysosomes. Furthermore, synthetic Manβ1-4GlcNAc disaccharide stimulates a broad immune response in vitro, which is in part dependent on the STING-TBK1 pathway, and enhances antibody response in vivo. Together, our data identify Manβ1-4GlcNAc as a novel innate immune modulator associated with chronic autoimmune diseases.</p></abstract><abstract id="Abs2" abstract-type="web-summary"><p id="Par2">Mammalian glycans have a role in host immunity but little is known about how they activate the host response in the context of autoimmune diseases. Here, the authors identify Manβ1-4GlcNAc as a novel innate immune modulator associated with chronic autoimmune diseases.</p></abstract><kwd-group kwd-group-type="npg-subject"><title>Subject terms</title><kwd>Glycobiology</kwd><kwd>Autoimmunity</kwd><kwd>Autoimmune diseases</kwd></kwd-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">https://doi.org/10.13039/100000057</institution-id><institution>U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS)</institution></institution-wrap></funding-source><award-id>GM038545</award-id><principal-award-recipient><name><surname>Lehrman</surname><given-names>Mark A.</given-names></name></principal-award-recipient></award-group></funding-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">https://doi.org/10.13039/100012051</institution-id><institution>Lupus Research Alliance (Lupus Research Alliance, Inc.)</institution></institution-wrap></funding-source><award-id>585101</award-id><principal-award-recipient><name><surname>Yan</surname><given-names>Nan</given-names></name></principal-award-recipient></award-group></funding-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">https://doi.org/10.13039/100000069</institution-id><institution>U.S. Department of Health & Human Services | NIH | National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS)</institution></institution-wrap></funding-source><award-id>AR067135</award-id><principal-award-recipient><name><surname>Yan</surname><given-names>Nan</given-names></name></principal-award-recipient></award-group></funding-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">https://doi.org/10.13039/100000928</institution-id><institution>Welch Foundation</institution></institution-wrap></funding-source><award-id>I-1831</award-id><principal-award-recipient><name><surname>Yan</surname><given-names>Nan</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2019</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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