{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T15:21:14Z","timestamp":1790868074310,"version":"4.1.0"},"reference-count":38,"publisher":"Rockefeller University Press","issue":"2","content-domain":{"domain":["rupress.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[1999,7,19]]},"abstract":"<jats:p>Major histocompatibility complex (MHC) class Ib molecules have been implicated in CD8+ T cell\u2013mediated defenses against intracellular bacterial infection, but the relative importance of MHC class Ib\u2013restricted T cells in antimicrobial immunity is unknown. In this report, we use MHC tetramers to characterize T cell responses restricted by H2-M3, an MHC class Ib molecule that selectively presents N-formyl peptides. We find that sizeable H2-M3\u2013restricted T cell responses, occurring earlier than MHC class Ia\u2013restricted T cell responses, are mounted after primary infection with the intracellular bacterium Listeria monocytogenes. These H2-M3\u2013restricted T cells are cytolytic and produce interferon \u03b3. However, after a second L. monocytogenes infection, H2-M3\u2013restricted memory T cell responses are minor in comparison to the much larger MHC class Ia\u2013restricted responses. This first direct characterization of an MHC class Ib\u2013restricted T cell response indicates that CD8+ T cells responding to L. monocytogenes infection can be divided into two groups: H2-M3\u2013restricted responses, which provide rapid and quantitatively substantial effector function during primary infections but contribute relatively little to memory responses, and MHC class Ia\u2013restricted responses, which expand later during primary infection but form memory T cells that respond rapidly and dramatically in response to subsequent infections by the same pathogen.<\/jats:p>","DOI":"10.1084\/jem.190.2.195","type":"journal-article","created":{"date-parts":[[2002,7,26]],"date-time":"2002-07-26T16:48:33Z","timestamp":1027702113000},"page":"195-204","update-policy":"https:\/\/doi.org\/10.1084\/jem.crossmarkpolicy","source":"Crossref","is-referenced-by-count":93,"title":["H2-M3\u2013Restricted T Cells in Bacterial Infection"],"prefix":"10.1084","volume":"190","author":[{"given":"Kristen M.","family":"Kerksiek","sequence":"first","affiliation":[{"name":"aFrom the Section of Infectious Diseases and Section of Immunobiology, Yale University School of Medicine, New Haven, Connecticut 06520"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dirk H.","family":"Busch","sequence":"additional","affiliation":[{"name":"aFrom the Section of Infectious Diseases and Section of Immunobiology, Yale University School of Medicine, New Haven, Connecticut 06520"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ingrid M.","family":"Pilip","sequence":"additional","affiliation":[{"name":"aFrom the Section of Infectious Diseases and Section of Immunobiology, Yale University School of Medicine, New Haven, Connecticut 06520"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S. Elise","family":"Allen","sequence":"additional","affiliation":[{"name":"aFrom the Section of Infectious Diseases and Section of Immunobiology, Yale University School of Medicine, New Haven, Connecticut 06520"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric G.","family":"Pamer","sequence":"additional","affiliation":[{"name":"aFrom the Section of Infectious Diseases and Section of Immunobiology, Yale University School of Medicine, New Haven, Connecticut 06520"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"291","published-online":{"date-parts":[[1999,7,19]]},"reference":[{"key":"2023072508512293300_R1","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/S0952-7915(97)80152-5","article-title":"Innate immunityimpact on the adaptive immune response","volume":"9","author":"Medzhitov","year":"1997","journal-title":"Curr. Opin. Immunol."},{"key":"2023072508512293300_R2","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1126\/science.2402637","article-title":"Structure and function of lipopolysaccharide binding protein","volume":"249","author":"Schumann","year":"1990","journal-title":"Science."},{"key":"2023072508512293300_R3","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1126\/science.1698311","article-title":"CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein","volume":"249","author":"Wright","year":"1990","journal-title":"Science."},{"key":"2023072508512293300_R4","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.1084\/jem.181.4.1473","article-title":"CD11c\/CD18, a transmembrane signaling receptor for lipopolysaccharide","volume":"181","author":"Ingalls","year":"1995","journal-title":"J. Exp. Med."},{"key":"2023072508512293300_R5","doi-asserted-by":"crossref","first-page":"1863","DOI":"10.1073\/pnas.91.5.1863","article-title":"The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid","volume":"91","author":"Dunne","year":"1994","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072508512293300_R6","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1146\/annurev.bi.63.070194.003125","article-title":"Structures and functions of multiligand lipoprotein receptorsmacrophage scavenger receptors and LDL receptor-related protein (LRP)","volume":"63","author":"Krieger","year":"1994","journal-title":"Annu. Rev. Biochem."},{"key":"2023072508512293300_R7","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1146\/annurev.iy.12.040194.003113","article-title":"The molecular biology of leukocyte chemoattractant receptors","volume":"12","author":"Murphy","year":"1994","journal-title":"Annu. Rev. Immunol."},{"key":"2023072508512293300_R8","volume-title":"ImmunobiologyThe Immune System in Health and Disease","author":"Janeway","year":"1997","edition":"3rd ed"},{"key":"2023072508512293300_R9","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1016\/0092-8674(94)90336-0","article-title":"MHC-dependent antigen processing and peptide presentationproviding ligands for T lymphocyte activation","volume":"76","author":"Germain","year":"1994","journal-title":"Cell."},{"key":"2023072508512293300_R10","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1146\/annurev.iy.12.040194.004203","article-title":"Antigen presentation by major histocompatibility complex class I-B molecules","volume":"12","author":"Shawar","year":"1994","journal-title":"Annu. Rev. Immunol."},{"key":"2023072508512293300_R11","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1146\/annurev.iy.08.040190.002441","article-title":"Molecules related to class-I major histocompatibility complex antigens","volume":"8","author":"Stroynowski","year":"1990","journal-title":"Annu. Rev. Immunol."},{"key":"2023072508512293300_R12","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1146\/annurev.immunol.15.1.851","article-title":"H2-M3, a full service class Ib histocompatibility antigen","volume":"15","author":"Lindahl","year":"1997","journal-title":"Annu. Rev. Immunol."},{"key":"2023072508512293300_R13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2776(08)60629-X","article-title":"The CD1 familya third lineage of antigen-presenting molecules","volume":"59","author":"Porcelli","year":"1995","journal-title":"Adv. Immunol."},{"key":"2023072508512293300_R14","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1126\/science.277.5324.339","article-title":"Crystal structure of mouse CD1an MHC-like fold with a large hydrophobic binding groove","volume":"277","author":"Zeng","year":"1997","journal-title":"Science."},{"key":"2023072508512293300_R15","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1038\/372691a0","article-title":"Recognition of a lipid antigen by CD1-restricted alpha\/beta T cells","volume":"372","author":"Beckman","year":"1994","journal-title":"Nature."},{"key":"2023072508512293300_R16","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1126\/science.7542404","article-title":"CD1-restricted T cell recognition of microbial lipoglycan antigens","volume":"269","author":"Sieling","year":"1995","journal-title":"Science."},{"key":"2023072508512293300_R17","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1016\/0092-8674(95)90037-3","article-title":"Nonclassical binding of formylated peptide in crystal structure of the MHC class Ib molecule H2-M3","volume":"82","author":"Wang","year":"1995","journal-title":"Cell."},{"key":"2023072508512293300_R18","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1084\/jem.164.1.363","article-title":"Listeria monocytogenes reactive T lymphocyte clones with cytolytic activity against infected target cells","volume":"164","author":"Kaufmann","year":"1986","journal-title":"J. Exp. Med."},{"key":"2023072508512293300_R19","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1111\/j.1600-065X.1997.tb00999.x","article-title":"MHC class I antigen processing of Listeria monocytogenes proteinsimplications for dominant and subdominant CTL responses","volume":"158","author":"Pamer","year":"1997","journal-title":"Immunol. Rev."},{"key":"2023072508512293300_R20","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/0092-8674(92)90097-V","article-title":"H2-M3 presents a Listeria monocytogenes peptide to cytotoxic T lymphocytes","volume":"70","author":"Pamer","year":"1992","journal-title":"Cell."},{"key":"2023072508512293300_R21","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1126\/science.1496381","article-title":"Specialized role for a murine class I-b MHC molecule in prokaryotic host defenses","volume":"257","author":"Kurlander","year":"1992","journal-title":"Science."},{"key":"2023072508512293300_R22","doi-asserted-by":"crossref","first-page":"3173","DOI":"10.4049\/jimmunol.140.9.3173","article-title":"Cloned Listeria monocytogenes specific non-MHC-restricted Lyt-2+ T cells with cytolytic and protective activity","volume":"140","author":"Kaufmann","year":"1988","journal-title":"J. Immunol."},{"key":"2023072508512293300_R23","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/S1074-7613(00)80310-6","article-title":"Identification of an H2-M3-restricted Listeria epitopeimplications for antigen presentation by M3","volume":"5","author":"Lenz","year":"1996","journal-title":"Immunity."},{"key":"2023072508512293300_R24","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S1074-7613(00)80311-8","article-title":"A Listeria monocytogenes pentapeptide is presented to cytolytic T lymphocytes by the H2-M3 MHC class Ib molecule","volume":"5","author":"Gulden","year":"1996","journal-title":"Immunity."},{"key":"2023072508512293300_R25","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1084\/jem.187.10.1711","article-title":"H2-M3 restricted presentation of a Listeria-derived leader peptide","volume":"187","author":"Princiotta","year":"1998","journal-title":"J. Exp. Med."},{"key":"2023072508512293300_R26","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/S1074-7613(00)80540-3","article-title":"Coordinate regulation of complex T cell populations responding to bacterial infection","volume":"8","author":"Busch","year":"1998","journal-title":"Immunity."},{"key":"2023072508512293300_R27","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1084\/jem.188.1.61","article-title":"Evolution of a complex T cell receptor repertoire during primary and recall bacterial infection","volume":"188","author":"Busch","year":"1998","journal-title":"J. Exp. Med."},{"key":"2023072508512293300_R28","doi-asserted-by":"crossref","first-page":"5403","DOI":"10.4049\/jimmunol.157.12.5403","article-title":"Assembly, specific binding, and crystallization of a human TCR-alphabeta with an antigenic Tax peptide from human T lymphotropic virus type 1 and the class I MHC molecule HLA-A2","volume":"157","author":"Garboczi","year":"1996","journal-title":"J. Immunol."},{"key":"2023072508512293300_R29","doi-asserted-by":"crossref","first-page":"3366","DOI":"10.4049\/jimmunol.158.7.3366","article-title":"Immunodominant and subdominant CTL responses to Listeria monocytogenes infection","volume":"158","author":"Vijh","year":"1997","journal-title":"J. Immunol."},{"key":"2023072508512293300_R30","doi-asserted-by":"crossref","first-page":"3301","DOI":"10.4049\/jimmunol.156.9.3301","article-title":"The COI mitochondrial gene encodes a minor histocompatibility antigen presented by H2-M3","volume":"156","author":"Morse","year":"1996","journal-title":"J. Immunol."},{"key":"2023072508512293300_R31","first-page":"1138","article-title":"Use of peptide libraries to map the substrate specificity of a peptide modifying enzymea 13 residue consensus peptide specifies biotinylation in Escherichia coli","volume":"11","author":"Schatz","year":"1993","journal-title":"Biotechnology."},{"key":"2023072508512293300_R32","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1126\/science.274.5284.94","article-title":"Phenotypic analysis of antigen specific T lymphocytes","volume":"274","author":"Altman","year":"1996","journal-title":"Science."},{"key":"2023072508512293300_R33","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1093\/intimm\/10.1.7","article-title":"H2M3wt-restricted, Listeria monocytogenes-immune CD8 T cells respond to multiple formylated peptides and to a variety of gram-positive and gram-negative bacteria","volume":"10","author":"Nataraj","year":"1998","journal-title":"Int. Immunol."},{"key":"2023072508512293300_R34","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1126\/science.272.5258.54","article-title":"Immunological memory and protective immunityunderstanding their relation","volume":"272","author":"Ahmed","year":"1996","journal-title":"Science."},{"key":"2023072508512293300_R35","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1084\/jem.189.4.701","article-title":"T cell affinity maturation by selective expansion during infection","volume":"189","author":"Busch","year":"1999","journal-title":"J. Exp. Med."},{"key":"2023072508512293300_R36","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1084\/jem.179.1.155","article-title":"Availability of endogenous peptides limits expression of an M3a-Ld major histocompatibility complex class I chimera","volume":"179","author":"Vyas","year":"1994","journal-title":"J. Exp. Med."},{"key":"2023072508512293300_R37","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1111\/j.1600-065X.1997.tb00997.x","article-title":"CTL responses to H2-M3-restricted Listeria epitopes","volume":"158","author":"Lenz","year":"1997","journal-title":"Immunol. Rev."},{"key":"2023072508512293300_R38","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1128\/iai.19.3.763-770.1978","article-title":"Resistance and susceptibility of mice to bacterial infectioncourse of Listeriosis in resistant or susceptible mice","volume":"19","author":"Cheers","year":"1978","journal-title":"Infect. Immun."}],"container-title":["The Journal of Experimental Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/rupress.org\/jem\/article-pdf\/190\/2\/195\/1695138\/99-0255.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/rupress.org\/jem\/article-pdf\/190\/2\/195\/1695138\/99-0255.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,25]],"date-time":"2023-07-25T10:00:44Z","timestamp":1690279244000},"score":1,"resource":{"primary":{"URL":"https:\/\/rupress.org\/jem\/article\/190\/2\/195\/20538\/H2-M3-Restricted-T-Cells-in-Bacterial"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1999,7,19]]},"references-count":38,"journal-issue":{"issue":"2","published-print":{"date-parts":[[1999,7,19]]}},"URL":"https:\/\/doi.org\/10.1084\/jem.190.2.195","relation":{},"ISSN":["0022-1007","1540-9538"],"issn-type":[{"value":"0022-1007","type":"print"},{"value":"1540-9538","type":"electronic"}],"subject":[],"published":{"date-parts":[[1999,7,19]]}}}