{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T05:21:49Z","timestamp":1790572909206,"version":"4.1.0"},"reference-count":51,"publisher":"Elsevier BV","issue":"2","license":[{"start":{"date-parts":[[2019,8,1]],"date-time":"2019-08-01T00:00:00Z","timestamp":1564617600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2019,8,1]],"date-time":"2019-08-01T00:00:00Z","timestamp":1564617600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T00:00:00Z","timestamp":1690848000000},"content-version":"vor","delay-in-days":1461,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"NIH","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Immune Tolerance Network","award":["UM1AI109565"],"award-info":[{"award-number":["UM1AI109565"]}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy And Infectious Diseases","doi-asserted-by":"publisher","award":["U19 AI106754"],"award-info":[{"award-number":["U19 AI106754"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["kidney-international.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Kidney International"],"published-print":{"date-parts":[[2019,8]]},"DOI":"10.1016\/j.kint.2019.01.040","type":"journal-article","created":{"date-parts":[[2019,2,26]],"date-time":"2019-02-26T21:37:57Z","timestamp":1551217077000},"page":"436-449","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":86,"title":["T-cell exhaustion correlates with improved outcomes in kidney transplant recipients"],"prefix":"10.1016","volume":"96","author":[{"given":"Miguel","family":"Fribourg","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Anderson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clara","family":"Fischman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Cantarelli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Perin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gaetano","family":"La Manna","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adeeb","family":"Rahman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bryna E.","family":"Burrell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter S.","family":"Heeger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paolo","family":"Cravedi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.kint.2019.01.040_bib1","doi-asserted-by":"crossref","first-page":"2205","DOI":"10.1084\/jem.188.12.2205","article-title":"Viral immune evasion due to persistence of activated T cells without effector function","volume":"188","author":"Zajac","year":"1998","journal-title":"J\u00a0Exp Med"},{"key":"10.1016\/j.kint.2019.01.040_bib2","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1126\/science.271.5246.173","article-title":"Immunology taught by viruses","volume":"271","author":"Zinkernagel","year":"1996","journal-title":"Science"},{"key":"10.1016\/j.kint.2019.01.040_bib3","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1038\/nri3862","article-title":"Molecular and cellular insights into T cell exhaustion","volume":"15","author":"Wherry","year":"2015","journal-title":"Nat Rev Immunol"},{"key":"10.1016\/j.kint.2019.01.040_bib4","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1084\/jem.187.9.1383","article-title":"Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes","volume":"187","author":"Gallimore","year":"1998","journal-title":"J\u00a0Exp Med"},{"key":"10.1016\/j.kint.2019.01.040_bib5","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.it.2015.02.008","article-title":"Overcoming T cell exhaustion in infection and cancer","volume":"36","author":"Pauken","year":"2015","journal-title":"Trends Immunol"},{"key":"10.1016\/j.kint.2019.01.040_bib6","doi-asserted-by":"crossref","first-page":"e1792","DOI":"10.1038\/cddis.2015.162","article-title":"T-cell exhaustion in the tumor microenvironment","volume":"6","author":"Jiang","year":"2015","journal-title":"Cell Death Dis"},{"key":"10.1016\/j.kint.2019.01.040_bib7","doi-asserted-by":"crossref","first-page":"R3","DOI":"10.1186\/cc13176","article-title":"Targeting the programmed cell death 1: programmed cell death ligand 1 pathway reverses T cell exhaustion in patients with sepsis","volume":"18","author":"Chang","year":"2014","journal-title":"Crit Care"},{"key":"10.1016\/j.kint.2019.01.040_bib8","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1097\/MOT.0000000000000153","article-title":"T-cell exhaustion in allograft rejection and tolerance","volume":"20","author":"Thorp","year":"2015","journal-title":"Curr Opin Organ Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib9","doi-asserted-by":"crossref","first-page":"1953","DOI":"10.1111\/ajt.13702","article-title":"Immune exhaustion and transplantation","volume":"16","author":"Sanchez-Fueyo","year":"2016","journal-title":"Am J Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib10","doi-asserted-by":"crossref","first-page":"1905","DOI":"10.1056\/NEJM199812243392607","article-title":"Antigen localization and migration in immunity and tolerance","volume":"339","author":"Starzl","year":"1998","journal-title":"N\u00a0Engl J Med"},{"key":"10.1016\/j.kint.2019.01.040_bib11","doi-asserted-by":"crossref","first-page":"2634","DOI":"10.1111\/ajt.12426","article-title":"Multicenter validation of urinary CXCL9 as a risk-stratifying biomarker for kidney transplant injury","volume":"13","author":"Hricik","year":"2013","journal-title":"Am J Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib12","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/j.cell.2015.05.047","article-title":"Data-driven phenotypic dissection of AML reveals progenitor-like cells that correlate with prognosis","volume":"162","author":"Levine","year":"2015","journal-title":"Cell"},{"key":"10.1016\/j.kint.2019.01.040_bib13","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1038\/nbt.2594","article-title":"viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia","volume":"31","author":"Amir el","year":"2013","journal-title":"Nat Biotechnol"},{"key":"10.1016\/j.kint.2019.01.040_bib14","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/cei.12985","article-title":"Reconstitution of immune cell populations in multiple sclerosis patients after autologous stem cell transplantation","volume":"189","author":"Karnell","year":"2017","journal-title":"Clin Exp Immunol"},{"key":"10.1016\/j.kint.2019.01.040_bib15","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1172\/JCI92812","article-title":"Hepatitis B virus-specific T cells associate with viral control upon nucleos(t)ide-analogue therapy discontinuation","volume":"128","author":"Rivino","year":"2018","journal-title":"J\u00a0Clin Invest"},{"key":"10.1016\/j.kint.2019.01.040_bib16","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.coi.2012.12.003","article-title":"T\u00a0cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment","volume":"25","author":"Crespo","year":"2013","journal-title":"Curr Opin Immunol"},{"key":"10.1016\/j.kint.2019.01.040_bib17","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1111\/j.1600-065X.2009.00770.x","article-title":"CD28 and CTLA-4 coreceptor expression and signal transduction","volume":"229","author":"Rudd","year":"2009","journal-title":"Immunol Rev"},{"key":"10.1016\/j.kint.2019.01.040_bib18","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1189\/jlb.0912438","article-title":"Increased T-bet is associated with senescence of influenza virus-specific CD8 T cells in aged humans","volume":"93","author":"Dolfi","year":"2013","journal-title":"J\u00a0Leukoc Biol"},{"key":"10.1016\/j.kint.2019.01.040_bib19","doi-asserted-by":"crossref","first-page":"2711","DOI":"10.1182\/blood-2002-07-2103","article-title":"Expression of CD57 defines replicative senescence and antigen-induced apoptotic death of CD8+ T cells","volume":"101","author":"Brenchley","year":"2003","journal-title":"Blood"},{"key":"10.1016\/j.kint.2019.01.040_bib20","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1038\/ni.1679","article-title":"Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection","volume":"10","author":"Blackburn","year":"2009","journal-title":"Nat Immunol"},{"key":"10.1016\/j.kint.2019.01.040_bib21","doi-asserted-by":"crossref","first-page":"2350","DOI":"10.1172\/JCI46102","article-title":"Exhaustion of tumor-specific CD8(+) T cells in metastases from melanoma patients","volume":"121","author":"Baitsch","year":"2011","journal-title":"J\u00a0Clin Invest"},{"key":"10.1016\/j.kint.2019.01.040_bib22","doi-asserted-by":"crossref","first-page":"e1005349","DOI":"10.1371\/journal.ppat.1005349","article-title":"TIGIT Marks Exhausted T cells, correlates with disease progression, and serves as a target for immune restoration in HIV and SIV infection","volume":"12","author":"Chew","year":"2016","journal-title":"PLoS Pathog"},{"key":"10.1016\/j.kint.2019.01.040_bib23","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nm.3838","article-title":"4-1BB costimulation ameliorates T cell exhaustion induced by tonic signaling of chimeric antigen receptors","volume":"21","author":"Long","year":"2015","journal-title":"Nat Med"},{"key":"10.1016\/j.kint.2019.01.040_bib24","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1016\/j.celrep.2016.06.078","article-title":"Distinct metabolic requirements of exhausted and functional virus-specific CD8 T cells in the same host","volume":"16","author":"Schurich","year":"2016","journal-title":"Cell Rep"},{"key":"10.1016\/j.kint.2019.01.040_bib25","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1007\/978-1-62703-493-7_21","article-title":"Cylex ImmuKnow cell function assay","volume":"1034","author":"Zeevi","year":"2013","journal-title":"Methods Mol Biol"},{"key":"10.1016\/j.kint.2019.01.040_bib26","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1097\/01.tp.0000234837.02126.70","article-title":"Assessing relative risks of infection and rejection: a meta-analysis using an immune function assay","volume":"82","author":"Kowalski","year":"2006","journal-title":"Transplantation"},{"key":"10.1016\/j.kint.2019.01.040_bib27","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1111\/j.1399-0012.2005.00429.x","article-title":"Establishing pediatric immune response zones using the Cylex ImmuKnow assay","volume":"19","author":"Hooper","year":"2005","journal-title":"Clin Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib28","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1034\/j.1399-0012.2003.00013.x","article-title":"Immune cell function testing: an adjunct to therapeutic drug monitoring in transplant patient management","volume":"17","author":"Kowalski","year":"2003","journal-title":"Clin Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib29","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1038\/nature14468","article-title":"T-cell exhaustion, co-stimulation and clinical outcome in autoimmunity and infection","volume":"523","author":"McKinney","year":"2015","journal-title":"Nature"},{"key":"10.1016\/j.kint.2019.01.040_bib30","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1158\/2326-6066.CIR-17-0159","article-title":"CD137 (4-1BB) Costimulation modifies DNA methylation in CD8(+) T cell\u2013relevant genes","volume":"6","author":"Aznar","year":"2018","journal-title":"Cancer Immunol Res"},{"key":"10.1016\/j.kint.2019.01.040_bib31","doi-asserted-by":"crossref","first-page":"6567","DOI":"10.1158\/0008-5472.CAN-11-1487","article-title":"Prospects for TIM3-targeted antitumor immunotherapy","volume":"71","author":"Ngiow","year":"2011","journal-title":"Cancer Res"},{"key":"10.1016\/j.kint.2019.01.040_bib32","doi-asserted-by":"crossref","first-page":"2132","DOI":"10.1111\/j.1600-6143.2010.03210.x","article-title":"Immune reconstitution following rabbit antithymocyte globulin","volume":"10","author":"Gurkan","year":"2010","journal-title":"Am J Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib33","doi-asserted-by":"crossref","first-page":"1725","DOI":"10.1097\/00007890-199612270-00005","article-title":"Tolerance to rat liver allografts: IV. Acceptance depends on the quantity of donor tissue and on donor leukocytes","volume":"62","author":"Sun","year":"1996","journal-title":"Transplantation"},{"key":"10.1016\/j.kint.2019.01.040_bib34","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1056\/NEJMoa052891","article-title":"Long-term outcome of renal transplantation from older donors","volume":"354","author":"Remuzzi","year":"2006","journal-title":"N\u00a0Engl J Med"},{"key":"10.1016\/j.kint.2019.01.040_bib35","doi-asserted-by":"crossref","first-page":"12145","DOI":"10.1073\/pnas.1303676111","article-title":"Impaired selectin-dependent leukocyte recruitment induces T-cell exhaustion and prevents chronic allograft vasculopathy and rejection","volume":"111","author":"Sarraj","year":"2014","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.kint.2019.01.040_bib36","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1038\/9525","article-title":"Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients","volume":"5","author":"Lee","year":"1999","journal-title":"Nat Med"},{"key":"10.1016\/j.kint.2019.01.040_bib37","doi-asserted-by":"crossref","first-page":"10249","DOI":"10.1128\/JVI.74.21.10249-10255.2000","article-title":"A\u00a0significant number of human immunodeficiency virus epitope-specific cytotoxic T lymphocytes detected by tetramer binding do not produce gamma interferon","volume":"74","author":"Goepfert","year":"2000","journal-title":"J\u00a0Virol"},{"key":"10.1016\/j.kint.2019.01.040_bib38","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1002\/1521-4141(200103)31:3<677::AID-IMMU677>3.0.CO;2-M","article-title":"High viral burden in the presence of major HIV-specific CD8(+) T cell expansions: evidence for impaired CTL effector function","volume":"31","author":"Kostense","year":"2001","journal-title":"Eur J Immunol"},{"key":"10.1016\/j.kint.2019.01.040_bib39","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1056\/NEJMc1509268","article-title":"Tumor regression and allograft rejection after administration of anti\u2013PD-1","volume":"374","author":"Lipson","year":"2016","journal-title":"N\u00a0Engl J Med"},{"key":"10.1016\/j.kint.2019.01.040_bib40","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1038\/s41409-018-0162-0","article-title":"Homeostatic proliferation leads to telomere attrition and increased PD-1 expression after autologous hematopoietic SCT for systemic sclerosis","volume":"53","author":"Arruda","year":"2018","journal-title":"Bone Marrow Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib41","doi-asserted-by":"crossref","first-page":"1967","DOI":"10.1056\/NEJMoa060068","article-title":"Rabbit antithymocyte globulin versus basiliximab in renal transplantation","volume":"355","author":"Brennan","year":"2006","journal-title":"N\u00a0Engl J Med"},{"key":"10.1016\/j.kint.2019.01.040_bib42","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1097\/01.tp.0000219817.18049.36","article-title":"Disassociation between risk of graft loss and risk of non-Hodgkin lymphoma with induction agents in renal transplant recipients","volume":"81","author":"Opelz","year":"2006","journal-title":"Transplantation"},{"key":"10.1016\/j.kint.2019.01.040_bib43","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1097\/TP.0b013e3181612ead","article-title":"Pretransplant donor-specific and non-specific immune parameters associated with early acute rejection","volume":"85","author":"Reinsmoen","year":"2008","journal-title":"Transplantation"},{"key":"10.1016\/j.kint.2019.01.040_bib44","doi-asserted-by":"crossref","DOI":"10.1172\/jci.insight.99281","article-title":"Cytometry TOF identifies alveolar macrophage subtypes in acute respiratory distress syndrome","volume":"3","author":"Morrell","year":"2018","journal-title":"JCI Insight"},{"key":"10.1016\/j.kint.2019.01.040_bib45","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1182\/blood-2018-04-843714","article-title":"Mass cytometry of Hodgkin lymphoma reveals a CD4(+) regulatory T-cell\u2013rich and exhausted T-effector microenvironment","volume":"132","author":"Cader","year":"2018","journal-title":"Blood"},{"key":"10.1016\/j.kint.2019.01.040_bib46","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1016\/j.cell.2017.04.014","article-title":"Innate immune landscape in early lung adenocarcinoma by paired single-cell analyses","volume":"169","author":"Lavin","year":"2017","journal-title":"Cell"},{"key":"10.1016\/j.kint.2019.01.040_bib47","doi-asserted-by":"crossref","first-page":"3166","DOI":"10.1111\/ajt.13401","article-title":"Interferon gamma ELISPOT testing as a risk-stratifying biomarker for kidney transplant injury: results from the CTOT-01 multicenter study","volume":"15","author":"Hricik","year":"2015","journal-title":"Am J Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib48","doi-asserted-by":"crossref","first-page":"247","DOI":"10.7326\/0003-4819-145-4-200608150-00004","article-title":"Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate","volume":"145","author":"Levey","year":"2006","journal-title":"Ann Intern Med"},{"key":"10.1016\/j.kint.2019.01.040_bib49","doi-asserted-by":"crossref","first-page":"588","DOI":"10.1002\/cyto.b.21588","article-title":"PhenoGraph and viSNE facilitate the identification of abnormal T-cell populations in routine clinical flow cytometric data","volume":"94","author":"DiGiuseppe","year":"2018","journal-title":"Cytometry B Clin Cytom"},{"key":"10.1016\/j.kint.2019.01.040_bib50","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1111\/j.1600-6143.2009.02987.x","article-title":"Banff '09 meeting report: antibody mediated graft deterioration and implementation of Banff working groups","volume":"10","author":"Sis","year":"2010","journal-title":"Am J Transplant"},{"key":"10.1016\/j.kint.2019.01.040_bib51","doi-asserted-by":"crossref","first-page":"2377","DOI":"10.1681\/ASN.2016101100","article-title":"Erythropoietin receptor-mediated molecular crosstalk promotes T cell immunoregulation and transplant survival","volume":"28","author":"Purroy","year":"2017","journal-title":"J\u00a0Am Soc Nephrol"}],"container-title":["Kidney International"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0085253819301929?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0085253819301929?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,25]],"date-time":"2025-09-25T00:53:15Z","timestamp":1758761595000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0085253819301929"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8]]},"references-count":51,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2019,8]]}},"alternative-id":["S0085253819301929"],"URL":"https:\/\/doi.org\/10.1016\/j.kint.2019.01.040","relation":{},"ISSN":["0085-2538"],"issn-type":[{"value":"0085-2538","type":"print"}],"subject":[],"published":{"date-parts":[[2019,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"T-cell exhaustion correlates with improved outcomes in kidney transplant recipients","name":"articletitle","label":"Article Title"},{"value":"Kidney International","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.kint.2019.01.040","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2019 International Society of Nephrology. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}