{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T14:29:41Z","timestamp":1791296981025,"version":"4.1.0"},"reference-count":46,"publisher":"Rockefeller University Press","issue":"10","content-domain":{"domain":["rupress.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2001,5,21]]},"abstract":"<jats:p>Rheumatoid arthritis (RA) is a heterogeneous syndrome of which a subset of patients develops vascular inflammation. The genetic determinants that confer risk for rheumatoid vasculitis are not known, but patients with vascular complications are known to have an expansion of CD4+CD28null T cells, a cell population potentially involved in endothelial damage. CD4+CD28null T cell clones isolated from RA patients with vasculitis were found to express killer cell immunoglobulin\u2013like receptors (KIRs) with the stimulatory KIR2DS2 often present in the absence of opposing inhibitory receptors with related specificities. To test the hypothesis that the KIR2DS2 gene is involved in the development of vasculitis, association studies were performed. The KIR2DS2 gene was significantly enriched among patients with rheumatoid vasculitis compared with normal individuals (odds ratio 5.56, P = 0.001) and patients with RA but no vasculitis (odds ratio 7.96, P = 0.001). Also, the distribution of human histocompatibility leukocyte antigen (HLA)-C, the putative ligand for KIRs, was significantly different in patients with rheumatoid vasculitis in comparison with the control populations. These data suggest that HLA class I\u2013recognizing receptors and HLA class I genes are genetic risk determinants that modulate the pattern of RA expression. Specifically, KIR2DS2 in conjunction with the appropriate HLA-C ligand may have a role in vascular damage by regulating CD4+CD28null T cells.<\/jats:p>","DOI":"10.1084\/jem.193.10.1159","type":"journal-article","created":{"date-parts":[[2002,7,26]],"date-time":"2002-07-26T16:48:33Z","timestamp":1027702113000},"page":"1159-1168","update-policy":"https:\/\/doi.org\/10.1084\/jem.crossmarkpolicy","source":"Crossref","is-referenced-by-count":263,"title":["Major Histocompatibility Complex Class I\u2013Recognizing Receptors Are Disease Risk Genes in Rheumatoid Arthritis"],"prefix":"10.1084","volume":"193","author":[{"given":"Jeng-Hsien","family":"Yen","sequence":"first","affiliation":[{"name":"aDepartment of Medicine and the Department of Immunology, Mayo Clinic, Rochester, Minnesota 55905"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brenda E.","family":"Moore","sequence":"additional","affiliation":[{"name":"aDepartment of Medicine and the Department of Immunology, Mayo Clinic, Rochester, Minnesota 55905"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takako","family":"Nakajima","sequence":"additional","affiliation":[{"name":"aDepartment of Medicine and the Department of Immunology, Mayo Clinic, Rochester, Minnesota 55905"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dirk","family":"Scholl","sequence":"additional","affiliation":[{"name":"aDepartment of Medicine and the Department of Immunology, Mayo Clinic, Rochester, Minnesota 55905"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel J.","family":"Schaid","sequence":"additional","affiliation":[{"name":"bDepartment of Health Sciences Research, Mayo Clinic, Rochester, Minnesota 55905"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cornelia M.","family":"Weyand","sequence":"additional","affiliation":[{"name":"aDepartment of Medicine and the Department of Immunology, Mayo Clinic, Rochester, Minnesota 55905"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J\u00f6rg J.","family":"Goronzy","sequence":"additional","affiliation":[{"name":"aDepartment of Medicine and the Department of Immunology, Mayo Clinic, Rochester, Minnesota 55905"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"291","published-online":{"date-parts":[[2001,5,14]]},"reference":[{"key":"2023072214371390300_R1","first-page":"166","article-title":"The Germline and somatic genetic basis for rheumatoid arthritis","volume-title":"Current Directions in Autoimmunity","author":"Ollier","year":"1999"},{"key":"2023072214371390300_R2","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1002\/1529-0131(199906)42:6<1071::AID-ANR1>3.0.CO;2-8","article-title":"The genetics revolution and the assault on rheumatoid arthritis","volume":"42","author":"Seldin","year":"1999","journal-title":"Arthritis Rheum."},{"key":"2023072214371390300_R3","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0025-7125(05)70504-6","article-title":"Pathogenesis of rheumatoid arthritis","volume":"81","author":"Weyand","year":"1997","journal-title":"Med. Clin. N. Am."},{"key":"2023072214371390300_R4","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/S0065-2776(08)60563-5","article-title":"Major histocompatibility complex-directed susceptibility to rheumatoid arthritis","volume":"68","author":"Nepom","year":"1998","journal-title":"Adv. Immunol."},{"key":"2023072214371390300_R5","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1007\/BF00831996","article-title":"Heterogeneity of rheumatoid arthritisfrom phenotypes to genotypes","volume":"20","author":"Weyand","year":"1998","journal-title":"Springer Semin. Immunopathol."},{"key":"2023072214371390300_R6","first-page":"585","article-title":"HLA heterozygosity contributes to susceptibility to rheumatoid arthritis","volume":"51","author":"Wordsworth","year":"1992","journal-title":"Am. J. Hum. Genet."},{"key":"2023072214371390300_R7","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1172\/JCI115814","article-title":"Homozygosity for the HLA-DRB1 allele selects for extraarticular manifestations in rheumatoid arthritis","volume":"89","author":"Weyand","year":"1992","journal-title":"J. Clin. Invest."},{"key":"2023072214371390300_R8","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1002\/1529-0131(199805)41:5<817::AID-ART7>3.0.CO;2-S","article-title":"The influence of sex on the phenotype of rheumatoid arthritis","volume":"41","author":"Weyand","year":"1998","journal-title":"Arthritis Rheum."},{"key":"2023072214371390300_R9","doi-asserted-by":"crossref","first-page":"10746","DOI":"10.1073\/pnas.95.18.10746","article-title":"New susceptibility locus for rheumatoid arthritis suggested by a genome-wide linkage study","volume":"95","author":"Cornelis","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072214371390300_R10","first-page":"1","article-title":"Susceptibility genes in RA","volume-title":"Current Directions in Autoimmunity","author":"Cornelis","year":"2000"},{"key":"2023072214371390300_R11","doi-asserted-by":"crossref","first-page":"2027","DOI":"10.1172\/JCI118638","article-title":"CD4+CD7\u2212CD28\u2212 T cells are expanded in rheumatoid arthritis and are characterized by autoreactivity","volume":"97","author":"Schmidt","year":"1996","journal-title":"J. Clin. Invest."},{"key":"2023072214371390300_R12","doi-asserted-by":"crossref","first-page":"1106","DOI":"10.1002\/art.1780400615","article-title":"Expansion of unusual CD4+ T cells in severe rheumatoid arthritis","volume":"40","author":"Martens","year":"1997","journal-title":"Arthritis Rheum."},{"key":"2023072214371390300_R13","doi-asserted-by":"crossref","first-page":"2135","DOI":"10.1161\/01.CIR.100.21.2135","article-title":"Perturbation of the T-cell repertoire in patients with unstable angina","volume":"100","author":"Liuzzo","year":"1999","journal-title":"Circulation."},{"key":"2023072214371390300_R14","doi-asserted-by":"crossref","first-page":"2883","DOI":"10.1161\/01.CIR.101.25.2883","article-title":"Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes","volume":"101","author":"Liuzzo","year":"2000","journal-title":"Circulation."},{"key":"2023072214371390300_R15","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/S0047-6374(97)00161-9","article-title":"Functional properties of CD4+ CD28\u2212 T cells in the aging immune system","volume":"102","author":"Weyand","year":"1998","journal-title":"Mech. Ageing Dev."},{"key":"2023072214371390300_R16","doi-asserted-by":"crossref","first-page":"2108","DOI":"10.1002\/1529-0131(199812)41:12<2108::AID-ART5>3.0.CO;2-Q","article-title":"Functional subsets of CD4 T cells in rheumatoid synovitis","volume":"41","author":"Namekawa","year":"1998","journal-title":"Arthritis Rheum."},{"key":"2023072214371390300_R17","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1146\/annurev.immunol.16.1.359","article-title":"NK cell receptors","volume":"16","author":"Lanier","year":"1998","journal-title":"Annu. Rev. Immunol."},{"key":"2023072214371390300_R18","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1146\/annurev.immunol.17.1.875","article-title":"Regulation of immune responses through inhibitory receptors","volume":"17","author":"Long","year":"1999","journal-title":"Annu. Rev. Immunol."},{"key":"2023072214371390300_R19","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1084\/jem.187.5.813","article-title":"Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence\u2013derived peptides by CD94\/NKG2 confers protection from natural killer cell\u2013mediated lysis","volume":"187","author":"Borrego","year":"1998","journal-title":"J. Exp. Med."},{"key":"2023072214371390300_R20","doi-asserted-by":"crossref","first-page":"5199","DOI":"10.1073\/pnas.95.9.5199","article-title":"HLA-E is a major ligand for the natural killer inhibitory receptor CD94\/NKG2A","volume":"95","author":"Lee","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072214371390300_R21","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1126\/science.7716543","article-title":"Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells","volume":"268","author":"Colonna","year":"1995","journal-title":"Science."},{"key":"2023072214371390300_R22","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/1074-7613(95)90025-X","article-title":"Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains","volume":"2","author":"Wagtmann","year":"1995","journal-title":"Immunity."},{"key":"2023072214371390300_R23","doi-asserted-by":"crossref","first-page":"2306","DOI":"10.4049\/jimmunol.155.5.2306","article-title":"Molecular cloning of NKB1. A natural killer cell receptor for HLA-B allotypes","volume":"155","author":"D'Andrea","year":"1995","journal-title":"J. Immunol."},{"key":"2023072214371390300_R24","doi-asserted-by":"crossref","first-page":"4026","DOI":"10.4049\/jimmunol.158.9.4026","article-title":"A single amino acid in the p58 killer cell inhibitory receptor controls the ability of natural killer cells to discriminate between the two groups of HLA-C allotypes","volume":"158","author":"Winter","year":"1997","journal-title":"J. Immunol."},{"key":"2023072214371390300_R25","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1016\/1074-7613(95)90069-1","article-title":"Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer","volume":"3","author":"Wagtmann","year":"1995","journal-title":"Immunity."},{"key":"2023072214371390300_R26","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1084\/jem.183.2.645","article-title":"The human leukocyte antigen (HLA)-C-specific \u201cactivatory\u201d or \u201cinhibitory\u201d natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmic portions","volume":"183","author":"Biassoni","year":"1996","journal-title":"J. Exp. Med."},{"key":"2023072214371390300_R27","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1084\/jem.182.3.875","article-title":"Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells","volume":"182","author":"Moretta","year":"1995","journal-title":"J. Exp. Med."},{"key":"2023072214371390300_R28","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1111\/j.1399-0039.1997.tb02803.x","article-title":"Genomic organization and allelic polymorphism of the human killer cell inhibitory receptor gene KIR103","volume":"49","author":"Selvakumar","year":"1997","journal-title":"Tissue Antigens."},{"key":"2023072214371390300_R29","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1111\/j.1399-0039.1998.tb02981.x","article-title":"Nucleotide and amino acid sequence alignment for human killer cell inhibitory receptors (KIR), 1998","volume":"51","author":"Steffens","year":"1998","journal-title":"Tissue Antigens."},{"key":"2023072214371390300_R30","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1016\/S1074-7613(00)80394-5","article-title":"Human diversity in killer cell inhibitory receptor genes","volume":"7","author":"Uhrberg","year":"1997","journal-title":"Immunity."},{"key":"2023072214371390300_R31","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1038\/35642","article-title":"Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells","volume":"391","author":"Lanier","year":"1998","journal-title":"Nature."},{"key":"2023072214371390300_R32","doi-asserted-by":"crossref","first-page":"32934","DOI":"10.1074\/jbc.273.49.32934","article-title":"DAP12-mediated signal transduction in natural killer cells. A dominant role for the Syk protein-tyrosine kinase","volume":"273","author":"McVicar","year":"1998","journal-title":"J. Biol. Chem."},{"key":"2023072214371390300_R33","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.4049\/jimmunol.165.2.1138","article-title":"Killer cell activating receptors function as costimulatory molecules on CD4+CD28null T cells clonally expanded in rheumatoid arthritis","volume":"165","author":"Namekawa","year":"2000","journal-title":"J. Immunol."},{"key":"2023072214371390300_R34","doi-asserted-by":"crossref","first-page":"12000","DOI":"10.1073\/pnas.90.24.12000","article-title":"HLA-C is the inhibitory ligand that determines dominant resistance to lysis by NK1- and NK2-specific natural killer cells","volume":"90","author":"Colonna","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072214371390300_R35","doi-asserted-by":"crossref","first-page":"7983","DOI":"10.1073\/pnas.89.17.7983","article-title":"Alloantigen recognition by two human natural killer cell clones is associated with HLA-C or a closely linked gene","volume":"89","author":"Colonna","year":"1992","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072214371390300_R36","doi-asserted-by":"crossref","first-page":"571","DOI":"10.4049\/jimmunol.161.2.571","article-title":"Direct binding and functional transfer of NK cell inhibitory receptors reveal novel patterns of HLA-C allotype recognition","volume":"161","author":"Winter","year":"1998","journal-title":"J. Immunol."},{"key":"2023072214371390300_R37","doi-asserted-by":"crossref","first-page":"14326","DOI":"10.1073\/pnas.95.24.14326","article-title":"Differential binding to HLA-C of p50-activating and p58-inhibitory natural killer cell receptors","volume":"95","author":"Vales-Gomez","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072214371390300_R38","doi-asserted-by":"crossref","first-page":"4250","DOI":"10.1093\/emboj\/18.15.4250","article-title":"Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94\/NKG2-A and the activating receptor CD94\/NKG2-C to HLA-E","volume":"18","author":"Vales-Gomez","year":"1999","journal-title":"EMBO J."},{"key":"2023072214371390300_R39","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1016\/S0092-8674(00)81398-7","article-title":"Follow the leaderNK cell receptors for classical and nonclassical MHC class I","volume":"92","author":"Lanier","year":"1998","journal-title":"Cell."},{"key":"2023072214371390300_R40","doi-asserted-by":"crossref","first-page":"4604","DOI":"10.1073\/pnas.94.9.4604","article-title":"Self and viral peptides can initiate lysis by autologous natural killer cells","volume":"94","author":"Mandelboim","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072214371390300_R41","doi-asserted-by":"crossref","first-page":"3350","DOI":"10.4049\/jimmunol.157.8.3350","article-title":"Peptide sequence requirements for the recognition of HLA-B*2705 by specific natural killer cells","volume":"157","author":"Peruzzi","year":"1996","journal-title":"J. Immunol."},{"key":"2023072214371390300_R42","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1046\/j.1365-2249.1998.00695.x","article-title":"Costimulatory molecules in Wegener's granulomatosis (WG)lack of expression of CD28 and preferential up-regulation of its ligands B7-1 (CD80) and B7-2 (CD86) on T cells","volume":"114","author":"Moosig","year":"1998","journal-title":"Clin. Exp. Immunol."},{"key":"2023072214371390300_R43","doi-asserted-by":"crossref","first-page":"S419","DOI":"10.1016\/S0002-8703(99)70266-8","article-title":"Atherosclerosis is an inflammatory disease","volume":"138","author":"Ross","year":"1999","journal-title":"Am. Heart J."},{"key":"2023072214371390300_R44","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1016\/S0733-8651(05)70074-6","article-title":"Plaque disruption and thrombosis. Potential role of inflammation and infection","volume":"17","author":"Shah","year":"1999","journal-title":"Cardiol. Clin."},{"key":"2023072214371390300_R45","doi-asserted-by":"crossref","first-page":"2097","DOI":"10.1126\/science.274.5295.2097","article-title":"Enhancement of class II-restricted T cell responses by costimulatory NK receptors for class I MHC proteins","volume":"274","author":"Mandelboim","year":"1996","journal-title":"Science."},{"key":"2023072214371390300_R46","doi-asserted-by":"crossref","first-page":"3798","DOI":"10.1073\/pnas.95.7.3798","article-title":"Natural killer activating receptors trigger interferon gamma secretion from T cells and natural killer cells","volume":"95","author":"Mandelboim","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA."}],"container-title":["The Journal of Experimental Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/rupress.org\/jem\/article-pdf\/193\/10\/1159\/1525804\/000661.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/rupress.org\/jem\/article-pdf\/193\/10\/1159\/1525804\/000661.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,22]],"date-time":"2023-07-22T14:37:43Z","timestamp":1690036663000},"score":1,"resource":{"primary":{"URL":"https:\/\/rupress.org\/jem\/article\/193\/10\/1159\/25866\/Major-Histocompatibility-Complex-Class-I"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2001,5,14]]},"references-count":46,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2001,5,21]]}},"URL":"https:\/\/doi.org\/10.1084\/jem.193.10.1159","relation":{},"ISSN":["0022-1007","1540-9538"],"issn-type":[{"value":"0022-1007","type":"print"},{"value":"1540-9538","type":"electronic"}],"subject":[],"published":{"date-parts":[[2001,5,14]]}}}