Endoplasmic Reticulum-Associated Degradation-Dependent Processing in Cross-Presentation and Its Potential for Dendritic Cell Vaccinations: A Review
Identifieur interne : 000B00 ( Pmc/Curation ); précédent : 000A99; suivant : 000B01Endoplasmic Reticulum-Associated Degradation-Dependent Processing in Cross-Presentation and Its Potential for Dendritic Cell Vaccinations: A Review
Auteurs : Jun Imai ; Sayaka Ohashi ; Takahiro SakaiSource :
- Pharmaceutics [ 1999-4923 ] ; 2020.
Abstract
While the success of dendritic cell (DC) vaccination largely depends on cross-presentation (CP) efficiency, the precise molecular mechanism of CP is not yet characterized. Recent research revealed that endoplasmic reticulum (ER)-associated degradation (ERAD), which was first identified as part of the protein quality control system in the ER, plays a pivotal role in the processing of extracellular proteins in CP. The discovery of ERAD-dependent processing strongly suggests that the properties of extracellular antigens are one of the keys to effective DC vaccination, in addition to DC subsets and the maturation of these cells. In this review, we address recent advances in CP, focusing on the molecular mechanisms of the ERAD-dependent processing of extracellular proteins. As ERAD itself and the ERAD-dependent processing in CP share cellular machinery, enhancing the recognition of extracellular proteins, such as the ERAD substrate, by ex vivo methods may serve to improve the efficacy of DC vaccination.
Url:
DOI: 10.3390/pharmaceutics12020153
PubMed: 32070016
PubMed Central: 7076524
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Endoplasmic Reticulum-Associated Degradation-Dependent Processing in Cross-Presentation and Its Potential for Dendritic Cell Vaccinations: A Review</title><author><name sortKey="Imai, Jun" sort="Imai, Jun" uniqKey="Imai J" first="Jun" last="Imai">Jun Imai</name></author><author><name sortKey="Ohashi, Sayaka" sort="Ohashi, Sayaka" uniqKey="Ohashi S" first="Sayaka" last="Ohashi">Sayaka Ohashi</name></author><author><name sortKey="Sakai, Takahiro" sort="Sakai, Takahiro" uniqKey="Sakai T" first="Takahiro" last="Sakai">Takahiro Sakai</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32070016</idno><idno type="pmc">7076524</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7076524</idno><idno type="RBID">PMC:7076524</idno><idno type="doi">10.3390/pharmaceutics12020153</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000B00</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000B00</idno><idno type="wicri:Area/Pmc/Curation">000B00</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000B00</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Endoplasmic Reticulum-Associated Degradation-Dependent Processing in Cross-Presentation and Its Potential for Dendritic Cell Vaccinations: A Review</title><author><name sortKey="Imai, Jun" sort="Imai, Jun" uniqKey="Imai J" first="Jun" last="Imai">Jun Imai</name></author><author><name sortKey="Ohashi, Sayaka" sort="Ohashi, Sayaka" uniqKey="Ohashi S" first="Sayaka" last="Ohashi">Sayaka Ohashi</name></author><author><name sortKey="Sakai, Takahiro" sort="Sakai, Takahiro" uniqKey="Sakai T" first="Takahiro" last="Sakai">Takahiro Sakai</name></author></analytic><series><title level="j">Pharmaceutics</title><idno type="eISSN">1999-4923</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>While the success of dendritic cell (DC) vaccination largely depends on cross-presentation (CP) efficiency, the precise molecular mechanism of CP is not yet characterized. Recent research revealed that endoplasmic reticulum (ER)-associated degradation (ERAD), which was first identified as part of the protein quality control system in the ER, plays a pivotal role in the processing of extracellular proteins in CP. The discovery of ERAD-dependent processing strongly suggests that the properties of extracellular antigens are one of the keys to effective DC vaccination, in addition to DC subsets and the maturation of these cells. In this review, we address recent advances in CP, focusing on the molecular mechanisms of the ERAD-dependent processing of extracellular proteins. As ERAD itself and the ERAD-dependent processing in CP share cellular machinery, enhancing the recognition of extracellular proteins, such as the ERAD substrate, by ex vivo methods may serve to improve the efficacy of DC vaccination.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Finn, O J" uniqKey="Finn O">O.J. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Pharmaceutics</journal-id><journal-id journal-id-type="iso-abbrev">Pharmaceutics</journal-id><journal-id journal-id-type="publisher-id">pharmaceutics</journal-id><journal-title-group><journal-title>Pharmaceutics</journal-title></journal-title-group><issn pub-type="epub">1999-4923</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32070016</article-id><article-id pub-id-type="pmc">7076524</article-id><article-id pub-id-type="doi">10.3390/pharmaceutics12020153</article-id><article-id pub-id-type="publisher-id">pharmaceutics-12-00153</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Endoplasmic Reticulum-Associated Degradation-Dependent Processing in Cross-Presentation and Its Potential for Dendritic Cell Vaccinations: A Review</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Imai</surname><given-names>Jun</given-names></name><xref rid="c1-pharmaceutics-12-00153" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><name><surname>Ohashi</surname><given-names>Sayaka</given-names></name></contrib><contrib contrib-type="author"><name><surname>Sakai</surname><given-names>Takahiro</given-names></name></contrib></contrib-group><aff id="af1-pharmaceutics-12-00153">Laboratory of Physiological Chemistry, Faculty of Pharmacy, Takasaki University of Health and Welfare, Takasaki, Gunma 370-0033, Japan;<email>0621021@takasaki-u.ac.jp</email> (S.O.);<email>sakai@takasaki-u.ac.jp</email> (T.S.)</aff><author-notes><corresp id="c1-pharmaceutics-12-00153"><label>*</label>Correspondence: <email>jimai@takasaki-u.ac.jp</email>; Tel.: +81-27-352-1180</corresp></author-notes><pub-date pub-type="epub"><day>13</day><month>2</month><year>2020</year></pub-date><pub-date pub-type="collection"><month>2</month><year>2020</year></pub-date><volume>12</volume><issue>2</issue><elocation-id>153</elocation-id><history><date date-type="received"><day>15</day><month>1</month><year>2020</year></date><date date-type="accepted"><day>12</day><month>2</month><year>2020</year></date></history><permissions><copyright-statement>© 2020 by the authors.</copyright-statement><copyright-year>2020</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<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><p>While the success of dendritic cell (DC) vaccination largely depends on cross-presentation (CP) efficiency, the precise molecular mechanism of CP is not yet characterized. Recent research revealed that endoplasmic reticulum (ER)-associated degradation (ERAD), which was first identified as part of the protein quality control system in the ER, plays a pivotal role in the processing of extracellular proteins in CP. The discovery of ERAD-dependent processing strongly suggests that the properties of extracellular antigens are one of the keys to effective DC vaccination, in addition to DC subsets and the maturation of these cells. In this review, we address recent advances in CP, focusing on the molecular mechanisms of the ERAD-dependent processing of extracellular proteins. As ERAD itself and the ERAD-dependent processing in CP share cellular machinery, enhancing the recognition of extracellular proteins, such as the ERAD substrate, by ex vivo methods may serve to improve the efficacy of DC vaccination.</p></abstract><kwd-group><kwd>dendritic cell</kwd><kwd>cross-presentation</kwd><kwd>major histocompatibility class I</kwd><kwd>endoplasmic reticulum-associated degradation</kwd><kwd>molecular chaperone</kwd><kwd>DC vaccination</kwd></kwd-group></article-meta></front><floats-group><fig id="pharmaceutics-12-00153-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>Maturation of endosomes and cross-presentation (CP). After internalization, exogenous proteins are transported into the endosome. Endocytic compartments without danger signals are acidified, fused with the lysosome, and designated as the proteolytic endosome. Since extracellular proteins without danger signals are self-proteins, those proteins are quickly degraded by the lysosomal proteases, which results in lower CP efficiency. When danger signals are detected by pattern recognition receptors (PRRs) (TLR2, TLR4, Nod1, Nod2), the acidification of endocytic compartments is delayed by the incomplete assembly of V-ATPase and the activation of Nox2, and resulted in the less-proteolytic endosome. The activated Nox2 produces reactive oxygen species (ROS), and ROS promote nonspecific disulfide bond formation to unfold extracellular proteins. As extracellular proteins with danger signals are non-self-proteins, these proteins are recognized by the endoplasmic reticulum (ER)-resident molecular chaperones in the non-classical endosome. Recognition by the ER-resident molecular chaperones accelerates ER-associated degradation (ERAD)-dependent processing of exogenous proteins and results in higher CP efficiency. ROS also activate TFEB, and activated TFEB promotes the maturation of the less-proteolytic endosome with a time difference. The activated TFEB also induces maturation of DCs by initiating the transcription of costimulatory molecules, several cytokines, and chemokines, including IL-1β, IL-6, TNF-α, and CCL5. In contrast to the major histocompatibility complex (MHC) I, MHC II presents antigenic peptides processed by lysosomal protease. MHC II associates with antigenic peptides under acidic conditions in the lysosome.</p></caption><graphic xlink:href="pharmaceutics-12-00153-g001"></graphic></fig><fig id="pharmaceutics-12-00153-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Recognition of extracellular proteins in CP. In ERAD-dependent processing, extracellular proteins are unfolded by ROS, resulting in nonspecific disulfide bonds in endocytic compartments. These unfolded extracellular proteins lose their activity and are preferentially recognized as ERAD substrates by ER-resident molecular chaperones, such as BiP, PDI, or ER-degradation enhancing α-mannosidase-like proteins (EDEMs). After recognition, these proteins are retro-transported into the cytosol. In contrast, self-proteins, which are properly folded in these cellular compartments, are not recognized as ERAD substrates and remain in endocytic compartments. After retro-transportation into the cytosol, extracellular proteins are recognized by cytosolic molecular chaperones, such as Hsp70 or Hsp90. After recognition, extracellular proteins are processed by the ubiquitin-proteasome system (UPS) into antigenic peptides and transported into membranous compartments in a transporter associated with antigen processing (TAP)-dependent manner. These two recognition steps indicate that unfolding and recognition of extracellular proteins are critical for CP.</p></caption><graphic xlink:href="pharmaceutics-12-00153-g002"></graphic></fig><table-wrap id="pharmaceutics-12-00153-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">pharmaceutics-12-00153-t001_Table 1</object-id><label>Table 1</label><caption><p>Major dendritic cell (DC) subsets and surface markers [<xref rid="B70-pharmaceutics-12-00153" ref-type="bibr">70</xref>,<xref rid="B71-pharmaceutics-12-00153" ref-type="bibr">71</xref>].</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">DC subsets</th><th colspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">Mouse</th><th colspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">Human</th></tr><tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Surface Marker</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cytokine Profile</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Surface Marker</th><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cytokine Profile</th></tr></thead><tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">cDC1</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, MHC II, CD8α, CD103, CD24, XCR1, CLEC9A, CD205</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-12 (high), IFN-III, IFN- λ</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c (low), HLA-DR, CD141, CD205, CLEC9A, XCR1, Nec12</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-12 (low), IFN-III, IFN-λ</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">cDC2</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, MHC II, CD11b, CD172a (Sirpα), ESAM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-6, TNF</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, HLA-DR, CD1c, CD11b, CD172a (Sirpα), CD1a, CD14, CD5</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-12, IL-1β, TNF, IL-6, IL-10, IL-23, IFN-γ</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">pDC</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, MHC II, B220, CD317, SIGLEC-H, CD172a, CD209, CCR2, CCR9, CXCR3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Type I and III IFN</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c (low), HLA-DR (low), CD123, CD303, CD304, CCR2, CXCR3</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Type I and III IFN</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">moDC</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, MHC II, CD11b, CD172, F4/80, Ly6C, CD64 (FcεRI)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-12, IL-23, IL-6, IL-10</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, HLA-DR, CD1c, CD1a, CD11b, CD172a, CD64 (FcεRI), CD14, CD5, CD206</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-12, IL-23, IL-6, IL-10</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LC</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, CD1d, CD207 (langerin), E-cadherin, MHC II, CD205</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">CD11c, CD1a, CD1b, CD1c, CD207 (langerin), E-cadherin, HLA-DR, CD205</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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