ERAP1 enzyme-mediated trimming and structural analyses of MHC I–bound precursor peptides yield novel insights into antigen processing and presentation
Identifieur interne : 000D77 ( Pmc/Curation ); précédent : 000D76; suivant : 000D78ERAP1 enzyme-mediated trimming and structural analyses of MHC I–bound precursor peptides yield novel insights into antigen processing and presentation
Auteurs : Lenong Li [États-Unis] ; Mansoor Batliwala [États-Unis] ; Marlene Bouvier [États-Unis]Source :
- The Journal of Biological Chemistry [ 0021-9258 ] ; 2019.
Abstract
Endoplasmic reticulum aminopeptidase 1 (ERAP1) and ERAP2 critically shape the major histocompatibility complex I (MHC I) immunopeptidome. The ERAPs remove N-terminal residues from antigenic precursor peptides and generate optimal-length peptides (
Url:
DOI: 10.1074/jbc.RA119.010102
PubMed: 31601650
PubMed Central: 6901306
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<author><name sortKey="Li, Lenong" sort="Li, Lenong" uniqKey="Li L" first="Lenong" last="Li">Lenong Li</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">ERAP1 enzyme-mediated trimming and structural analyses of MHC I–bound precursor peptides yield novel insights into antigen processing and presentation</title>
<author><name sortKey="Li, Lenong" sort="Li, Lenong" uniqKey="Li L" first="Lenong" last="Li">Lenong Li</name>
<affiliation wicri:level="2"><nlm:aff id="aff1">Department of Microbiology and Immunology, University of Illinois, Chicago, Illinois 60612</nlm:aff>
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<wicri:cityArea>Department of Microbiology and Immunology, University of Illinois, Chicago</wicri:cityArea>
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<author><name sortKey="Batliwala, Mansoor" sort="Batliwala, Mansoor" uniqKey="Batliwala M" first="Mansoor" last="Batliwala">Mansoor Batliwala</name>
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<wicri:cityArea>Department of Microbiology and Immunology, University of Illinois, Chicago</wicri:cityArea>
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<author><name sortKey="Bouvier, Marlene" sort="Bouvier, Marlene" uniqKey="Bouvier M" first="Marlene" last="Bouvier">Marlene Bouvier</name>
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<series><title level="j">The Journal of Biological Chemistry</title>
<idno type="ISSN">0021-9258</idno>
<idno type="eISSN">1083-351X</idno>
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<front><div type="abstract" xml:lang="en"><p>Endoplasmic reticulum aminopeptidase 1 (ERAP1) and ERAP2 critically shape the major histocompatibility complex I (MHC I) immunopeptidome. The ERAPs remove N-terminal residues from antigenic precursor peptides and generate optimal-length peptides (<italic>i.e.</italic>
8–10-mers) to fit into the MHC class I groove. It is therefore intriguing that MHC class I molecules can present N-terminally extended peptides on the cell surface that can elicit CD8+ T-cell responses. This observation likely reflects gaps in our understanding of how antigens are processed by the ERAP enzymes. To better understand ERAPs' function in antigen processing, here we generated a nested set of N-terminally extended 10–20-mer peptides (RA)<italic><sub>n</sub>
</italic>
AAKKKYCL covalently bound to the human leukocyte antigen (HLA)-B*0801. We used X-ray crystallography, thermostability assessments, and an ERAP1-trimming assay to characterize these complexes. The X-ray structures determined at 1.40–1.65 Å resolutions revealed that the residue extensions (RA)<italic><sub>n</sub>
</italic>
unexpectedly protrude out of the A pocket of HLA-B*0801, whereas the AAKKKYCL core of all peptides adopts similar, bound conformations. HLA-B*0801 residue 62 was critical to open the A pocket. We also show that HLA-B*0801 and antigenic precursor peptides form stable complexes. Finally, ERAP1-mediated trimming of the MHC I–bound peptides required a minimal length of 14 amino acids. We propose a mechanistic model explaining how ERAP1-mediated trimming of MHC I–bound peptides in cells can generate peptides of canonical as well as noncanonical lengths that still serve as stable MHC I ligands. Our results provide a framework to better understand how the ERAP enzymes influence the MHC I immunopeptidome.</p>
</div>
</front>
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</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Biol Chem</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Biol. Chem</journal-id>
<journal-id journal-id-type="hwp">jbc</journal-id>
<journal-id journal-id-type="pmc">jbc</journal-id>
<journal-id journal-id-type="publisher-id">JBC</journal-id>
<journal-title-group><journal-title>The Journal of Biological Chemistry</journal-title>
</journal-title-group>
<issn pub-type="ppub">0021-9258</issn>
<issn pub-type="epub">1083-351X</issn>
<publisher><publisher-name>American Society for Biochemistry and Molecular Biology</publisher-name>
<publisher-loc>11200 Rockville Pike, Suite 302, Rockville, MD 20852-3110, U.S.A.</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31601650</article-id>
<article-id pub-id-type="pmc">6901306</article-id>
<article-id pub-id-type="publisher-id">RA119.010102</article-id>
<article-id pub-id-type="doi">10.1074/jbc.RA119.010102</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Editors' Picks</subject>
</subj-group>
</article-categories>
<title-group><article-title>ERAP1 enzyme-mediated trimming and structural analyses of MHC I–bound precursor peptides yield novel insights into antigen processing and presentation</article-title>
<alt-title alt-title-type="short">EDITORS' PICK: ERAP1, MHC I, and precursor peptides</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-0489-8869</contrib-id>
<name><surname>Li</surname>
<given-names>Lenong</given-names>
</name>
<ext-link ext-link-type="uri" xlink:href="http://www.jbc.org/content/294/49/18534/suppl/DCAuthor_profile"></ext-link>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Batliwala</surname>
<given-names>Mansoor</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-9965-9096</contrib-id>
<name><surname>Bouvier</surname>
<given-names>Marlene</given-names>
</name>
<xref ref-type="aff" rid="aff1"></xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
</contrib>
<aff id="aff1">Department of Microbiology and Immunology, University of Illinois, Chicago, Illinois 60612</aff>
</contrib-group>
<author-notes><corresp id="cor1"><label>1</label>
To whom correspondence should be addressed:
<addr-line>Dept. of Microbiology and Immunology, University of Illinois at Chicago, 909 S. Wolcott Ave., Chicago, IL 60612.</addr-line>
Tel.:
<phone>312-355-0664</phone>
; E-mail:
<email>mbouvier@uic.edu</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Peter Cresswell</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>6</day>
<month>12</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>10</day>
<month>10</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>10</day>
<month>10</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>294</volume>
<issue>49</issue>
<fpage>18534</fpage>
<lpage>18544</lpage>
<history><date date-type="received"><day>8</day>
<month>7</month>
<year>2019</year>
</date>
<date date-type="rev-recd"><day>20</day>
<month>9</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 Li et al.</copyright-statement>
<copyright-year>2019</copyright-year>
<copyright-holder>Li et al.</copyright-holder>
<license license-type="open-access"><license-p><italic>Author's Choice</italic>
—Final version open access under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0">Creative Commons CC-BY license</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="zbc04919018534.pdf"></self-uri>
<abstract><p>Endoplasmic reticulum aminopeptidase 1 (ERAP1) and ERAP2 critically shape the major histocompatibility complex I (MHC I) immunopeptidome. The ERAPs remove N-terminal residues from antigenic precursor peptides and generate optimal-length peptides (<italic>i.e.</italic>
8–10-mers) to fit into the MHC class I groove. It is therefore intriguing that MHC class I molecules can present N-terminally extended peptides on the cell surface that can elicit CD8+ T-cell responses. This observation likely reflects gaps in our understanding of how antigens are processed by the ERAP enzymes. To better understand ERAPs' function in antigen processing, here we generated a nested set of N-terminally extended 10–20-mer peptides (RA)<italic><sub>n</sub>
</italic>
AAKKKYCL covalently bound to the human leukocyte antigen (HLA)-B*0801. We used X-ray crystallography, thermostability assessments, and an ERAP1-trimming assay to characterize these complexes. The X-ray structures determined at 1.40–1.65 Å resolutions revealed that the residue extensions (RA)<italic><sub>n</sub>
</italic>
unexpectedly protrude out of the A pocket of HLA-B*0801, whereas the AAKKKYCL core of all peptides adopts similar, bound conformations. HLA-B*0801 residue 62 was critical to open the A pocket. We also show that HLA-B*0801 and antigenic precursor peptides form stable complexes. Finally, ERAP1-mediated trimming of the MHC I–bound peptides required a minimal length of 14 amino acids. We propose a mechanistic model explaining how ERAP1-mediated trimming of MHC I–bound peptides in cells can generate peptides of canonical as well as noncanonical lengths that still serve as stable MHC I ligands. Our results provide a framework to better understand how the ERAP enzymes influence the MHC I immunopeptidome.</p>
</abstract>
<kwd-group><kwd>immunology</kwd>
<kwd>antigen presentation</kwd>
<kwd>antigen processing</kwd>
<kwd>structural biology</kwd>
<kwd>endoplasmic reticulum (ER)</kwd>
<kwd>CD8+ T cells</kwd>
<kwd>endoplasmic reticulum aminopeptidase (ERAP)</kwd>
<kwd>immunopeptidome</kwd>
<kwd>major histocompatibility complex I (MHC I)</kwd>
<kwd>adaptive immunity</kwd>
<kwd>HLA-B*0801</kwd>
</kwd-group>
<funding-group><award-group id="award1"><funding-source><institution-wrap><institution>HHS | NIH | National Institute of Allergy and Infectious Diseases (NIAID)
</institution>
<institution-id institution-id-type="open-funder-registry">10.13039/100000060</institution-id>
</institution-wrap>
</funding-source>
<award-id>AI114467</award-id>
<award-id>AI108546</award-id>
<principal-award-recipient><name><surname>Li</surname>
<given-names>Lenong</given-names>
</name>
</principal-award-recipient>
<principal-award-recipient><name><surname>Batliwala</surname>
<given-names>Mansoor</given-names>
</name>
</principal-award-recipient>
<principal-award-recipient><name><surname>Bouvier</surname>
<given-names>Marlene</given-names>
</name>
</principal-award-recipient>
</award-group>
</funding-group>
</article-meta>
</front>
</pmc>
</record>
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