{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T12:29:24Z","timestamp":1790512164102,"version":"4.1.0"},"reference-count":48,"publisher":"Oxford University Press (OUP)","issue":"7","license":[{"start":{"date-parts":[[2021,10,1]],"date-time":"2021-10-01T00:00:00Z","timestamp":1633046400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/501100011033","name":"MEC | Agencia Estatal de Investigaci\u00f3n","doi-asserted-by":"publisher","award":["PID2019-110609RB-C21-C22\/AEI\/10.13039\/501100011033"],"award-info":[{"award-number":["PID2019-110609RB-C21-C22\/AEI\/10.13039\/501100011033"]}],"id":[{"id":"10.13039\/501100011033","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004587","name":"MEC | Instituto de Salud Carlos III","doi-asserted-by":"publisher","award":["PI13\/00598"],"award-info":[{"award-number":["PI13\/00598"]}],"id":[{"id":"10.13039\/501100004587","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008666","name":"Fundaci\u00f3 la Marat\u00f3 de TV3","doi-asserted-by":"publisher","award":["201822-10"],"award-info":[{"award-number":["201822-10"]}],"id":[{"id":"10.13039\/100008666","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004587","name":"MEC | Instituto de Salud Carlos III","doi-asserted-by":"publisher","award":["PI20\/00090"],"award-info":[{"award-number":["PI20\/00090"]}],"id":[{"id":"10.13039\/501100004587","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Human CMV infection is frequent in kidney transplant recipients (KTR). Pretransplant Ag-specific T cells and adaptive NKG2C+ NK cells associate with reduced incidence of infection in CMV+ KTR. Expansions of adaptive NKG2C+ NK cells were reported in posttransplant CMV-infected KTR. To further explore this issue, NKG2C+ NK, CD8+, and TcR\u03b3\u03b4 T cells were analyzed pretransplant and at different time points posttransplant for \u226524 mo in a cohort of CMV+ KTR (n = 112), stratified according to CMV viremia detection. In cryopreserved samples from a subgroup (n = 49), adaptive NKG2C+ NK cell markers and T cell subsets were compared after a longer follow-up (median, 56 mo), assessing the frequencies of CMV-specific T cells and viremia at the last time point. Increased proportions of NKG2C+ NK, CD8+, and TcR\u03b3\u03b4 T cells were detected along posttransplant evolution in viremia(+) KTR. However, the individual magnitude and kinetics of the NKG2C+ NK response was variable and only exceptionally detected among viremia(\u2013) KTR, presumably reflecting subclinical viral replication events. NKG2C+ expansions were independent of KLRC2 zygosity and associated with higher viral loads at diagnosis; no relation with other clinical parameters was perceived. Increased proportions of adaptive NKG2C+ NK cells (CD57+, ILT2+, Fc\u03b5RI\u03b3\u2013) were observed after resolution of viremia long-term posttransplant, coinciding with increased CD8+ and V\u03b42\u2013 \u03b3\u03b4 T cells; at that stage CMV-specific T cells were comparable to viremia(\u2013) cases. These data suggest that adaptive NKG2C+ NK cells participate with T cells to restore CMV replication control, although their relative contribution cannot be discerned.<\/jats:p>","DOI":"10.4049\/jimmunol.2100055","type":"journal-article","created":{"date-parts":[[2021,9,1]],"date-time":"2021-09-01T18:20:19Z","timestamp":1630520419000},"page":"1882-1890","source":"Crossref","is-referenced-by-count":14,"title":["Long-Term Evolution of the Adaptive NKG2C+ NK Cell Response to Cytomegalovirus Infection in Kidney Transplantation: An Insight on the Diversity of Host\u2013Pathogen Interaction"],"prefix":"10.1093","volume":"207","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9249-1083","authenticated-orcid":false,"given":"Michelle","family":"Ataya","sequence":"first","affiliation":[{"name":"Universitat Pompeu Fabra , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dolores","family":"Redondo-Pach\u00f3n","sequence":"additional","affiliation":[{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]},{"name":"Department of Nephrology, Hospital del Mar , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4696-3331","authenticated-orcid":false,"given":"Laura","family":"Llin\u00e0s-Mallol","sequence":"additional","affiliation":[{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1195-1496","authenticated-orcid":false,"given":"Jos\u00e9","family":"Y\u00e9lamos","sequence":"additional","affiliation":[{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]},{"name":"Immunology Laboratory, Department of Pathology, Hospital del Mar , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7424-5383","authenticated-orcid":false,"given":"Elisenda","family":"Alari-Pahissa","sequence":"additional","affiliation":[{"name":"Universitat Pompeu Fabra , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mar\u00eda J","family":"P\u00e9rez-S\u00e1ez","sequence":"additional","affiliation":[{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]},{"name":"Department of Nephrology, Hospital del Mar , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3118-8654","authenticated-orcid":false,"given":"Mireia","family":"Altadill","sequence":"additional","affiliation":[{"name":"Universitat Pompeu Fabra , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7656-5700","authenticated-orcid":false,"given":"D\u00e0lia","family":"Ra\u00efch-Regu\u00e9","sequence":"additional","affiliation":[{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0300-9225","authenticated-orcid":false,"given":"Carlos","family":"Vilches","sequence":"additional","affiliation":[{"name":"Immunogenetics-HLA, Instituto de Investigaci\u00f3n Sanitaria Puerta de Hierro Segovia de Arana , Majadahonda, Madrid ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julio","family":"Pascual","sequence":"additional","affiliation":[{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]},{"name":"Department of Nephrology, Hospital del Mar , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marta","family":"Crespo","sequence":"additional","affiliation":[{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]},{"name":"Department of Nephrology, Hospital del Mar , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4882-065X","authenticated-orcid":false,"given":"Miguel","family":"L\u00f3pez-Botet","sequence":"additional","affiliation":[{"name":"Universitat Pompeu Fabra , Barcelona ,","place":["Spain"]},{"name":"Instituto Hospital del Mar de Investigaciones M\u00e9dicas , Barcelona ,","place":["Spain"]},{"name":"Immunology Laboratory, Department of Pathology, Hospital del Mar , Barcelona ,","place":["Spain"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2021,10,1]]},"reference":[{"key":"2025022610321581800_r1","first-page":"1960","volume-title":"Fields Virology","author":"Mocarski","year":"2013","edition":"6th Ed."},{"key":"2025022610321581800_r2","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1002\/path.4437","article-title":"The pathogenesis of human cytomegalovirus","volume":"235","author":"Griffiths","year":"2015","journal-title":"J. Pathol."},{"key":"2025022610321581800_r3","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1097\/TP.0000000000000160","article-title":"Cytomegalovirus serology and replication remain associated with solid organ graft rejection and graft loss in the era of prophylactic treatment","volume":"98","author":"Stern","year":"2014","journal-title":"Transplantation."},{"key":"2025022610321581800_r4","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/ajt.12103","article-title":"Cytomegalovirus in solid organ transplantation","volume":"13","author":"Razonable","year":"2013","journal-title":"Am. J. Transplant."},{"key":"2025022610321581800_r5","doi-asserted-by":"crossref","first-page":"2495","DOI":"10.1111\/ajt.15371","article-title":"Improving our mechanistic understanding of the indirect effects of CMV infection in transplant recipients","volume":"19","author":"L\u2019Huillier","year":"2019","journal-title":"Am. J. Transplant."},{"key":"2025022610321581800_r6","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1097\/TP.0000000000002191","article-title":"The Third International Consensus Guidelines on the Management of Cytomegalovirus in Solid-organ Transplantation","volume":"102","author":"Kotton","year":"2018","journal-title":"Transplantation."},{"key":"2025022610321581800_r7","doi-asserted-by":"crossref","first-page":"S74","DOI":"10.1093\/infdis\/jiz601","article-title":"Clinical diagnostic testing for human cytomegalovirus infections","volume":"221","author":"Razonable","year":"2020","journal-title":"J. Infect. Dis."},{"key":"2025022610321581800_r8","doi-asserted-by":"crossref","first-page":"S45","DOI":"10.1093\/infdis\/jiz428","article-title":"Immune correlates of protection against human cytomegalovirus acquisition, replication, and disease","volume":"221","author":"Nelson","year":"2020","journal-title":"J. Infect. Dis."},{"key":"2025022610321581800_r9","doi-asserted-by":"crossref","first-page":"1793","DOI":"10.1111\/ajt.12256","article-title":"Pretransplant immediately early-1-specific T cell responses provide protection for CMV infection after kidney transplantation","volume":"13","author":"Bestard","year":"2013","journal-title":"Am. J. Transplant."},{"key":"2025022610321581800_r10","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1016\/j.ekir.2017.02.016","article-title":"An early immediate early protein IE-1-specific T-cell polyfunctionality is associated with a better control of cytomegalovirus reactivation in kidney transplantation","volume":"2","author":"Dekeyser","year":"2017","journal-title":"Kidney Int. Rep."},{"key":"2025022610321581800_r11","doi-asserted-by":"crossref","first-page":"2375","DOI":"10.1093\/cid\/ciz1209","article-title":"Cellular immunity to predict the risk of cytomegalovirus infection in kidney transplantation: a prospective, interventional, multicenter clinical trial","volume":"71","author":"Jarque","year":"2020","journal-title":"Clin. Infect. Dis."},{"key":"2025022610321581800_r12","doi-asserted-by":"crossref","first-page":"2505","DOI":"10.1111\/ajt.15315","article-title":"A prospective multicenter observational study of cell-mediated immunity as a predictor for cytomegalovirus infection in kidney transplant recipients","volume":"19","author":"Kumar","year":"2019","journal-title":"Am. J. Transplant."},{"key":"2025022610321581800_r13","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1681\/ASN.2014100985","article-title":"Surveillance of \u03b3\u03b4 T cells predicts cytomegalovirus infection resolution in kidney transplants","volume":"27","author":"Kaminski","year":"2016","journal-title":"J. Am. Soc. Nephrol."},{"key":"2025022610321581800_r14","doi-asserted-by":"crossref","first-page":"3664","DOI":"10.1182\/blood-2004-05-2058","article-title":"Imprint of human cytomegalovirus infection on the NK cell receptor repertoire","volume":"104","author":"Gum\u00e1","year":"2004","journal-title":"Blood."},{"key":"2025022610321581800_r15","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.smim.2014.03.002","article-title":"The CD94\/NKG2C+ NK-cell subset on the edge of innate and adaptive immunity to human cytomegalovirus infection","volume":"26","author":"L\u00f3pez-Botet","year":"2014","journal-title":"Semin. Immunol."},{"key":"2025022610321581800_r16","doi-asserted-by":"crossref","first-page":"2678","DOI":"10.1182\/blood-2012-10-459545","article-title":"NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs","volume":"121","author":"B\u00e9ziat","year":"2013","journal-title":"Blood."},{"key":"2025022610321581800_r17","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1016\/j.immuni.2015.02.008","article-title":"Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function","volume":"42","author":"Schlums","year":"2015","journal-title":"Immunity."},{"key":"2025022610321581800_r18","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/j.immuni.2015.02.013","article-title":"Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals","volume":"42","author":"Lee","year":"2015","journal-title":"Immunity."},{"key":"2025022610321581800_r19","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1086\/504719","article-title":"Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94\/NKG2C receptor in aviremic HIV-1-positive patients","volume":"194","author":"Gum\u00e1","year":"2006","journal-title":"J. Infect. Dis."},{"key":"2025022610321581800_r20","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1182\/blood-2011-08-372003","article-title":"Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus?","volume":"119","author":"Della Chiesa","year":"2012","journal-title":"Blood."},{"key":"2025022610321581800_r21","doi-asserted-by":"crossref","first-page":"2665","DOI":"10.1182\/blood-2011-10-386995","article-title":"Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function","volume":"119","author":"Foley","year":"2012","journal-title":"Blood."},{"key":"2025022610321581800_r22","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1093\/intimm\/dxh013","article-title":"Molecular genetic analyses of human NKG2C (KLRC2) gene deletion","volume":"16","author":"Miyashita","year":"2004","journal-title":"Int. Immunol."},{"key":"2025022610321581800_r23","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1111\/j.1399-0039.2012.01911.x","article-title":"Assessment of copy-number variation in the NKG2C receptor gene in a single-tube and characterization of a reference cell panel, using standard polymerase chain reaction","volume":"80","author":"Moraru","year":"2012","journal-title":"Tissue Antigens."},{"key":"2025022610321581800_r24","doi-asserted-by":"crossref","first-page":"2213","DOI":"10.1182\/blood-2014-05-576124","article-title":"Rapid NK cell differentiation in a population with near-universal human cytomegalovirus infection is attenuated by NKG2C deletions","volume":"124","author":"Goodier","year":"2014","journal-title":"Blood."},{"key":"2025022610321581800_r25","doi-asserted-by":"crossref","first-page":"3268","DOI":"10.1002\/eji.201343773","article-title":"NKG2C zygosity influences CD94\/NKG2C receptor function and the NK-cell compartment redistribution in response to human cytomegalovirus","volume":"43","author":"Muntasell","year":"2013","journal-title":"Eur. J. Immunol."},{"key":"2025022610321581800_r26","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1111\/ajt.15658","article-title":"Pretransplant adaptive NKG2C+ NK cells protect against cytomegalovirus infection in kidney transplant recipients","volume":"20","author":"Ataya","year":"2020","journal-title":"Am. J. Transplant."},{"key":"2025022610321581800_r27","doi-asserted-by":"crossref","first-page":"94","DOI":"10.4049\/jimmunol.1601236","article-title":"Adaptive NKG2C+ NK cell response and the risk of cytomegalovirus infection in kidney transplant recipients","volume":"198","author":"Redondo-Pach\u00f3n","year":"2017","journal-title":"J. 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Blood Marrow Transplant."},{"key":"2025022610321581800_r29","doi-asserted-by":"crossref","first-page":"1860","DOI":"10.3324\/haematol.2014.108407","article-title":"Favorable impact of natural killer cell reconstitution on chronic graft-versus-host disease and cytomegalovirus reactivation after allogeneic hematopoietic stem cell transplantation","volume":"99","author":"Kheav","year":"2014","journal-title":"Haematologica."},{"key":"2025022610321581800_r30","doi-asserted-by":"crossref","first-page":"14725","DOI":"10.1073\/pnas.1110900108","article-title":"Expansion of a unique CD57+NKG2Chi natural killer cell subset during acute human cytomegalovirus infection","volume":"108","author":"Lopez-Verg\u00e8s","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2025022610321581800_r31","doi-asserted-by":"crossref","first-page":"166","DOI":"10.3389\/fimmu.2017.00166","article-title":"Dual role of natural killer cells on graft rejection and control of cytomegalovirus infection in renal transplantation","volume":"8","author":"L\u00f3pez-Botet","year":"2017","journal-title":"Front. Immunol."},{"key":"2025022610321581800_r32","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.1002\/eji.201646422","article-title":"Asymptomatic CMV infections in long-term renal transplant recipients are associated with the loss of FcR\u03b3 from LIR-1+ NK cells","volume":"46","author":"Makwana","year":"2016","journal-title":"Eur. J. Immunol."},{"key":"2025022610321581800_r33","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1111\/ajt.13010","article-title":"Circulating NK-cell subsets in renal allograft recipients with anti-HLA donor-specific antibodies","volume":"15","author":"Crespo","year":"2015","journal-title":"Am. J. 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Transplant."},{"key":"2025022610321581800_r36","doi-asserted-by":"crossref","first-page":"e118","DOI":"10.1097\/TP.0000000000003138","article-title":"New insights into the molecular mechanisms and immune control of cytomegalovirus reactivation","volume":"104","author":"Heald-Sargent","year":"2020","journal-title":"Transplantation."},{"key":"2025022610321581800_r37","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.1002\/eji.201747018","article-title":"CMV drives the expansion of highly functional memory T cells expressing NK-cell receptors in renal transplant recipients","volume":"47","author":"Makwana","year":"2017","journal-title":"Eur. J. Immunol."},{"key":"2025022610321581800_r38","doi-asserted-by":"crossref","first-page":"46","DOI":"10.3389\/fimmu.2013.00046","article-title":"The peripheral NK cell repertoire after kidney transplantation is modulated by different immunosuppressive drugs","volume":"4","author":"Neudoerfl","year":"2013","journal-title":"Front. 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Immunol."},{"key":"2025022610321581800_r42","doi-asserted-by":"crossref","first-page":"1402","DOI":"10.4049\/jimmunol.1203034","article-title":"Cutting edge: antibody-dependent memory-like NK cells distinguished by FcR\u03b3 deficiency","volume":"190","author":"Zhang","year":"2013","journal-title":"J. Immunol."},{"key":"2025022610321581800_r43","doi-asserted-by":"crossref","first-page":"7717","DOI":"10.1128\/JVI.01096-13","article-title":"Human cytomegalovirus-induced NKG2C(hi) CD57(hi) natural killer cells are effectors dependent on humoral antiviral immunity","volume":"87","author":"Wu","year":"2013","journal-title":"J. Virol."},{"key":"2025022610321581800_r44","doi-asserted-by":"crossref","first-page":"1676","DOI":"10.4049\/jimmunol.1500872","article-title":"NK cell and Ig interplay in defense against herpes simplex virus type 1: epistatic interaction of CD16A and IgG1 allotypes of variable affinities modulates antibody-dependent cellular cytotoxicity and susceptibility to clinical reactivation","volume":"195","author":"Moraru","year":"2015","journal-title":"J. Immunol."},{"key":"2025022610321581800_r45","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1038\/s41590-018-0082-6","article-title":"Peptide-specific recognition of human cytomegalovirus strains controls adaptive natural killer cells","volume":"19","author":"Hammer","year":"2018","journal-title":"Nat. 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