The carbonyl nucleobase adduct M3Ade is a potent antigen for adaptive polyclonal MR1-restricted T cells
The major histocompatibility complex (MHC) class I-related molecule MHC-class-I-related protein 1 (MR1) presents metabolites to distinct MR1-restricted T cell subsets, including mucosal-associated invariant T (MAIT) and MR1T cells. However, self-reactive MR1T cells and the nature of recognized antig...
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| creator | Chancellor, Andrew Constantin, Daniel Giuliano Berloffa Yang, Qinmei Nosi, Vladimir Loureiro, José Pedro Colombo, Rodrigo Jakob, Roman P. Joss, Daniel Pfeffer, Michael De Simone, Giulia Morabito, Aurelia Schaefer, Verena Vacchini, Alessandro Brunelli, Laura Montagna, Daniela Heim, Markus Zippelius, Alfred Davoli, Enrico Häussinger, Daniel Maier, Timm Mori, Lucia De Libero, Gennaro |
| description | The major histocompatibility complex (MHC) class I-related molecule MHC-class-I-related protein 1 (MR1) presents metabolites to distinct MR1-restricted T cell subsets, including mucosal-associated invariant T (MAIT) and MR1T cells. However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. Thus, M3Ade is an MR1-presented self-metabolite that enables stimulation and tracking of human-MR1T cells from blood and tissue, aiding our understanding of their roles in health and disease.The major histocompatibility complex (MHC) class I-related molecule MHC-class-I-related protein 1 (MR1) presents metabolites to distinct MR1-restricted T cell subsets, including mucosal-associated invariant T (MAIT) and MR1T cells. However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. Thus, M3Ade is an MR1-presented self-metabolite that enables stimulation and tracking of human-MR1T cells from blood and tissue, aiding our understanding of their |
| doi_str_mv | 10.1016/j.immuni.2024.11.019 |
| format | Article |
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However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. Thus, M3Ade is an MR1-presented self-metabolite that enables stimulation and tracking of human-MR1T cells from blood and tissue, aiding our understanding of their roles in health and disease.The major histocompatibility complex (MHC) class I-related molecule MHC-class-I-related protein 1 (MR1) presents metabolites to distinct MR1-restricted T cell subsets, including mucosal-associated invariant T (MAIT) and MR1T cells. However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. Thus, M3Ade is an MR1-presented self-metabolite that enables stimulation and tracking of human-MR1T cells from blood and tissue, aiding our understanding of their roles in health and disease.</description><identifier>ISSN: 1074-7613</identifier><identifier>ISSN: 1097-4180</identifier><identifier>EISSN: 1097-4180</identifier><identifier>DOI: 10.1016/j.immuni.2024.11.019</identifier><language>eng</language><ispartof>Immunity (Cambridge, Mass.), 2024-12</ispartof><rights>Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c787-55be3c853258b127b9d9aa670dcbe918da328b8434e8e7ccd10d142f0581d0993</cites><orcidid>0000-0001-9658-4124 ; 0000-0003-0853-7868</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids></links><search><creatorcontrib>Chancellor, Andrew</creatorcontrib><creatorcontrib>Constantin, Daniel</creatorcontrib><creatorcontrib>Giuliano Berloffa</creatorcontrib><creatorcontrib>Yang, Qinmei</creatorcontrib><creatorcontrib>Nosi, Vladimir</creatorcontrib><creatorcontrib>Loureiro, José Pedro</creatorcontrib><creatorcontrib>Colombo, Rodrigo</creatorcontrib><creatorcontrib>Jakob, Roman P.</creatorcontrib><creatorcontrib>Joss, Daniel</creatorcontrib><creatorcontrib>Pfeffer, Michael</creatorcontrib><creatorcontrib>De Simone, Giulia</creatorcontrib><creatorcontrib>Morabito, Aurelia</creatorcontrib><creatorcontrib>Schaefer, Verena</creatorcontrib><creatorcontrib>Vacchini, Alessandro</creatorcontrib><creatorcontrib>Brunelli, Laura</creatorcontrib><creatorcontrib>Montagna, Daniela</creatorcontrib><creatorcontrib>Heim, Markus</creatorcontrib><creatorcontrib>Zippelius, Alfred</creatorcontrib><creatorcontrib>Davoli, Enrico</creatorcontrib><creatorcontrib>Häussinger, Daniel</creatorcontrib><creatorcontrib>Maier, Timm</creatorcontrib><creatorcontrib>Mori, Lucia</creatorcontrib><creatorcontrib>De Libero, Gennaro</creatorcontrib><title>The carbonyl nucleobase adduct M3Ade is a potent antigen for adaptive polyclonal MR1-restricted T cells</title><title>Immunity (Cambridge, Mass.)</title><description>The major histocompatibility complex (MHC) class I-related molecule MHC-class-I-related protein 1 (MR1) presents metabolites to distinct MR1-restricted T cell subsets, including mucosal-associated invariant T (MAIT) and MR1T cells. However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. Thus, M3Ade is an MR1-presented self-metabolite that enables stimulation and tracking of human-MR1T cells from blood and tissue, aiding our understanding of their roles in health and disease.The major histocompatibility complex (MHC) class I-related molecule MHC-class-I-related protein 1 (MR1) presents metabolites to distinct MR1-restricted T cell subsets, including mucosal-associated invariant T (MAIT) and MR1T cells. However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. 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However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. Thus, M3Ade is an MR1-presented self-metabolite that enables stimulation and tracking of human-MR1T cells from blood and tissue, aiding our understanding of their roles in health and disease.The major histocompatibility complex (MHC) class I-related molecule MHC-class-I-related protein 1 (MR1) presents metabolites to distinct MR1-restricted T cell subsets, including mucosal-associated invariant T (MAIT) and MR1T cells. However, self-reactive MR1T cells and the nature of recognized antigens remain underexplored. Here, we report a cell endogenous carbonyl adduct of adenine (8-(9H-purin-6-yl)-2-oxa-8-azabicyclo[3.3.1]nona-3,6-diene-4,6-dicarbaldehyde [M3Ade]) sequestered in the A' pocket of MR1. M3Ade induced in vitro MR1-mediated stimulation of MR1T cell clones that bound MR1-M3Ade tetramers. MR1-M3Ade tetramers identified heterogeneous MR1-reactive T cells ex vivo in healthy donors, individuals with acute myeloid leukemia, and tumor-infiltrating lymphocytes from non-small cell lung adenocarcinoma and hepatocarcinoma. These cells displayed phenotypic, transcriptional, and functional diversity at distinct differentiation stages, indicating their adaptive nature. They were also polyclonal, with some preferential T cell receptor (TCRαβ) pair usage. Thus, M3Ade is an MR1-presented self-metabolite that enables stimulation and tracking of human-MR1T cells from blood and tissue, aiding our understanding of their roles in health and disease.</abstract><doi>10.1016/j.immuni.2024.11.019</doi><orcidid>https://orcid.org/0000-0001-9658-4124</orcidid><orcidid>https://orcid.org/0000-0003-0853-7868</orcidid></addata></record> |
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| title | The carbonyl nucleobase adduct M3Ade is a potent antigen for adaptive polyclonal MR1-restricted T cells |
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