Ancient features of the MHC class II presentation pathway, and a model for the possible origin of MHC molecules
Major histocompatibility complex (MHC) molecules are only found in jawed vertebrates and not in more primitive species. MHC class II type structures likely represent the ancestral structure of MHC molecules. Efficient MHC class II transport to endosomal compartments depends on association with a spe...
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Veröffentlicht in: | Immunogenetics (New York) 2019-03, Vol.71 (3), p.233-249 |
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description | Major histocompatibility complex (MHC) molecules are only found in jawed vertebrates and not in more primitive species. MHC class II type structures likely represent the ancestral structure of MHC molecules. Efficient MHC class II transport to endosomal compartments depends on association with a specialized chaperone, the MHC class II invariant chain (aliases Ii or CD74). The present study identifies conserved motifs in the CLIP region of CD74 molecules, used for binding in the MHC class II binding groove, throughout jawed vertebrates. Peculiarly, in CD74a molecules of Ostariophysi, a fish clade including for example Mexican tetra and zebrafish, the CLIP region has duplicated. In mammals, in endosomal compartments, the peptide-free form of classical MHC class II is stabilized by binding to nonclassical MHC class II “DM,” a process that participates in “peptide editing” (selection for high affinity peptides). Hitherto, DM-lineage genes had only been reported from the level of amphibians, but the present study reveals the existence of
DMA
and
DMB
genes in lungfish. This is the first study which details how classical and DM lineage molecules have distinguishing glycine-rich motifs in their transmembrane regions. In addition, based on extant MHC class II structures and functions, the present study proposes a model for early MHC evolution, in which, in an ancestral jawed vertebrate, the ancestral MHC molecule derived from a heavy-chain-only antibody type molecule that cycled between the cell surface and endosomal compartments. |
doi_str_mv | 10.1007/s00251-018-1090-2 |
format | Article |
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DMA
and
DMB
genes in lungfish. This is the first study which details how classical and DM lineage molecules have distinguishing glycine-rich motifs in their transmembrane regions. In addition, based on extant MHC class II structures and functions, the present study proposes a model for early MHC evolution, in which, in an ancestral jawed vertebrate, the ancestral MHC molecule derived from a heavy-chain-only antibody type molecule that cycled between the cell surface and endosomal compartments.</description><identifier>ISSN: 0093-7711</identifier><identifier>EISSN: 1432-1211</identifier><identifier>DOI: 10.1007/s00251-018-1090-2</identifier><identifier>PMID: 30377750</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Allergology ; Amphibians ; Animals ; Antigen Presentation - immunology ; Antigens, Differentiation, B-Lymphocyte - immunology ; Antigens, Differentiation, B-Lymphocyte - metabolism ; Binding ; Biology and Evolution of Antigen Presentation ; Biomedical and Life Sciences ; Biomedicine ; Cell Biology ; Cell Membrane - metabolism ; Cell surface ; Chains ; Class II-associated invariant chain peptides ; Compartments ; Free form ; Gene Function ; Genes ; Glycine ; Histocompatibility Antigens Class II - immunology ; Histocompatibility Antigens Class II - metabolism ; Human Genetics ; Humans ; Immunology ; Invariant chain ; Major histocompatibility complex ; Molecular Chaperones - immunology ; Molecular Chaperones - metabolism ; Molecular structure ; Peptides ; Protein Binding ; Review ; Vertebrates ; Zebrafish</subject><ispartof>Immunogenetics (New York), 2019-03, Vol.71 (3), p.233-249</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2018</rights><rights>Immunogenetics is a copyright of Springer, (2018). All Rights Reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c438t-1e3e1ba8576bf568683b7cc33a1c476c149cb7a4e382ac269684d134c27b2d193</citedby><cites>FETCH-LOGICAL-c438t-1e3e1ba8576bf568683b7cc33a1c476c149cb7a4e382ac269684d134c27b2d193</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00251-018-1090-2$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00251-018-1090-2$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30377750$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dijkstra, Johannes M.</creatorcontrib><creatorcontrib>Yamaguchi, Takuya</creatorcontrib><title>Ancient features of the MHC class II presentation pathway, and a model for the possible origin of MHC molecules</title><title>Immunogenetics (New York)</title><addtitle>Immunogenetics</addtitle><addtitle>Immunogenetics</addtitle><description>Major histocompatibility complex (MHC) molecules are only found in jawed vertebrates and not in more primitive species. MHC class II type structures likely represent the ancestral structure of MHC molecules. Efficient MHC class II transport to endosomal compartments depends on association with a specialized chaperone, the MHC class II invariant chain (aliases Ii or CD74). The present study identifies conserved motifs in the CLIP region of CD74 molecules, used for binding in the MHC class II binding groove, throughout jawed vertebrates. Peculiarly, in CD74a molecules of Ostariophysi, a fish clade including for example Mexican tetra and zebrafish, the CLIP region has duplicated. In mammals, in endosomal compartments, the peptide-free form of classical MHC class II is stabilized by binding to nonclassical MHC class II “DM,” a process that participates in “peptide editing” (selection for high affinity peptides). Hitherto, DM-lineage genes had only been reported from the level of amphibians, but the present study reveals the existence of
DMA
and
DMB
genes in lungfish. This is the first study which details how classical and DM lineage molecules have distinguishing glycine-rich motifs in their transmembrane regions. In addition, based on extant MHC class II structures and functions, the present study proposes a model for early MHC evolution, in which, in an ancestral jawed vertebrate, the ancestral MHC molecule derived from a heavy-chain-only antibody type molecule that cycled between the cell surface and endosomal compartments.</description><subject>Allergology</subject><subject>Amphibians</subject><subject>Animals</subject><subject>Antigen Presentation - immunology</subject><subject>Antigens, Differentiation, B-Lymphocyte - immunology</subject><subject>Antigens, Differentiation, B-Lymphocyte - metabolism</subject><subject>Binding</subject><subject>Biology and Evolution of Antigen Presentation</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cell Biology</subject><subject>Cell Membrane - metabolism</subject><subject>Cell surface</subject><subject>Chains</subject><subject>Class II-associated invariant chain peptides</subject><subject>Compartments</subject><subject>Free form</subject><subject>Gene Function</subject><subject>Genes</subject><subject>Glycine</subject><subject>Histocompatibility Antigens Class II - immunology</subject><subject>Histocompatibility Antigens Class II - metabolism</subject><subject>Human Genetics</subject><subject>Humans</subject><subject>Immunology</subject><subject>Invariant chain</subject><subject>Major histocompatibility complex</subject><subject>Molecular Chaperones - immunology</subject><subject>Molecular Chaperones - metabolism</subject><subject>Molecular structure</subject><subject>Peptides</subject><subject>Protein Binding</subject><subject>Review</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><issn>0093-7711</issn><issn>1432-1211</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kcFO3DAQhq2qCJYtD9BLZamXHgidsRM7OaJVYVcCcaFny3EmEJTEqZ0I8fb1srSVKnHyYb7_sz0_Y58RLhBAf48AosAMsMwQKsjEB7bCXIoMBeJHtgKoZKY14gk7jfEJAItKqGN2IkFqrQtYMX85uo7Gmbdk5yVQ5L7l8yPx2-2Gu97GyHc7PqVBguzc-ZFPdn58ti_n3I4Nt3zwDfW89eE1NvkYu7on7kP30I172940-J7c0lP8xI5a20c6ezvX7OfVj_vNNru5u95tLm8yl8tyzpAkYW3LQqu6LVSpSllr56S06HKtHOaVq7XNSZbCOqEqVeYNytwJXYsGK7lm3w7eKfhfC8XZDF101Pd2JL9EI1BopaBAldCv_6FPfgljet0rlRYLskgUHigX0hcDtWYK3WDDi0Ew-zbMoQ2T2jD7NoxImS9v5qUeqPmb-LP-BIgDENNofKDw7-r3rb8BJKGS0w</recordid><startdate>20190301</startdate><enddate>20190301</enddate><creator>Dijkstra, Johannes M.</creator><creator>Yamaguchi, Takuya</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QL</scope><scope>7T5</scope><scope>7T7</scope><scope>7TK</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20190301</creationdate><title>Ancient features of the MHC class II presentation pathway, and a model for the possible origin of MHC molecules</title><author>Dijkstra, Johannes M. ; Yamaguchi, Takuya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c438t-1e3e1ba8576bf568683b7cc33a1c476c149cb7a4e382ac269684d134c27b2d193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Allergology</topic><topic>Amphibians</topic><topic>Animals</topic><topic>Antigen Presentation - immunology</topic><topic>Antigens, Differentiation, B-Lymphocyte - immunology</topic><topic>Antigens, Differentiation, B-Lymphocyte - metabolism</topic><topic>Binding</topic><topic>Biology and Evolution of Antigen Presentation</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cell Biology</topic><topic>Cell Membrane - metabolism</topic><topic>Cell surface</topic><topic>Chains</topic><topic>Class II-associated invariant chain peptides</topic><topic>Compartments</topic><topic>Free form</topic><topic>Gene Function</topic><topic>Genes</topic><topic>Glycine</topic><topic>Histocompatibility Antigens Class II - immunology</topic><topic>Histocompatibility Antigens Class II - metabolism</topic><topic>Human Genetics</topic><topic>Humans</topic><topic>Immunology</topic><topic>Invariant chain</topic><topic>Major histocompatibility complex</topic><topic>Molecular Chaperones - immunology</topic><topic>Molecular Chaperones - metabolism</topic><topic>Molecular structure</topic><topic>Peptides</topic><topic>Protein Binding</topic><topic>Review</topic><topic>Vertebrates</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dijkstra, Johannes M.</creatorcontrib><creatorcontrib>Yamaguchi, Takuya</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Immunogenetics (New York)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dijkstra, Johannes M.</au><au>Yamaguchi, Takuya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ancient features of the MHC class II presentation pathway, and a model for the possible origin of MHC molecules</atitle><jtitle>Immunogenetics (New York)</jtitle><stitle>Immunogenetics</stitle><addtitle>Immunogenetics</addtitle><date>2019-03-01</date><risdate>2019</risdate><volume>71</volume><issue>3</issue><spage>233</spage><epage>249</epage><pages>233-249</pages><issn>0093-7711</issn><eissn>1432-1211</eissn><abstract>Major histocompatibility complex (MHC) molecules are only found in jawed vertebrates and not in more primitive species. MHC class II type structures likely represent the ancestral structure of MHC molecules. Efficient MHC class II transport to endosomal compartments depends on association with a specialized chaperone, the MHC class II invariant chain (aliases Ii or CD74). The present study identifies conserved motifs in the CLIP region of CD74 molecules, used for binding in the MHC class II binding groove, throughout jawed vertebrates. Peculiarly, in CD74a molecules of Ostariophysi, a fish clade including for example Mexican tetra and zebrafish, the CLIP region has duplicated. In mammals, in endosomal compartments, the peptide-free form of classical MHC class II is stabilized by binding to nonclassical MHC class II “DM,” a process that participates in “peptide editing” (selection for high affinity peptides). Hitherto, DM-lineage genes had only been reported from the level of amphibians, but the present study reveals the existence of
DMA
and
DMB
genes in lungfish. This is the first study which details how classical and DM lineage molecules have distinguishing glycine-rich motifs in their transmembrane regions. In addition, based on extant MHC class II structures and functions, the present study proposes a model for early MHC evolution, in which, in an ancestral jawed vertebrate, the ancestral MHC molecule derived from a heavy-chain-only antibody type molecule that cycled between the cell surface and endosomal compartments.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>30377750</pmid><doi>10.1007/s00251-018-1090-2</doi><tpages>17</tpages></addata></record> |
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subjects | Allergology Amphibians Animals Antigen Presentation - immunology Antigens, Differentiation, B-Lymphocyte - immunology Antigens, Differentiation, B-Lymphocyte - metabolism Binding Biology and Evolution of Antigen Presentation Biomedical and Life Sciences Biomedicine Cell Biology Cell Membrane - metabolism Cell surface Chains Class II-associated invariant chain peptides Compartments Free form Gene Function Genes Glycine Histocompatibility Antigens Class II - immunology Histocompatibility Antigens Class II - metabolism Human Genetics Humans Immunology Invariant chain Major histocompatibility complex Molecular Chaperones - immunology Molecular Chaperones - metabolism Molecular structure Peptides Protein Binding Review Vertebrates Zebrafish |
title | Ancient features of the MHC class II presentation pathway, and a model for the possible origin of MHC molecules |
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