{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,14]],"date-time":"2026-11-14T01:59:41Z","timestamp":1794621581786,"version":"4.9.1"},"reference-count":46,"publisher":"Springer Science and Business Media LLC","issue":"10","license":[{"start":{"date-parts":[[2024,9,17]],"date-time":"2024-09-17T00:00:00Z","timestamp":1726531200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2024,9,17]],"date-time":"2024-09-17T00:00:00Z","timestamp":1726531200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"funder":[{"DOI":"10.13039\/100000060","name":"U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["DP2 AI176139"],"award-info":[{"award-number":["DP2 AI176139"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["U19 AI082630"],"award-info":[{"award-number":["U19 AI082630"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["P01 AI052699"],"award-info":[{"award-number":["P01 AI052699"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R01 AI113021"],"award-info":[{"award-number":["R01 AI113021"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R01 AI113021"],"award-info":[{"award-number":["R01 AI113021"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R01 AI113021"],"award-info":[{"award-number":["R01 AI113021"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"U.S. Department of Health & Human Services | NIH | National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R01 AI113021"],"award-info":[{"award-number":["R01 AI113021"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005190","name":"Melanoma Research Alliance","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100005190","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100001368","name":"V Foundation for Cancer Research","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100001368","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32 GM007753"],"award-info":[{"award-number":["T32 GM007753"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32 GM144273"],"award-info":[{"award-number":["T32 GM144273"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32 GM144273"],"award-info":[{"award-number":["T32 GM144273"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000054","name":"U.S. Department of Health & Human Services | NIH | National Cancer Institute","doi-asserted-by":"publisher","award":["T32 CA207021"],"award-info":[{"award-number":["T32 CA207021"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000054","name":"U.S. Department of Health & Human Services | NIH | National Cancer Institute","doi-asserted-by":"publisher","award":["T32 CA921643"],"award-info":[{"award-number":["T32 CA921643"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000054","name":"U.S. Department of Health & Human Services | NIH | National Cancer Institute","doi-asserted-by":"publisher","award":["K08 CA248960"],"award-info":[{"award-number":["K08 CA248960"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Immunol"],"published-print":{"date-parts":[[2024,10]]},"DOI":"10.1038\/s41590-024-01961-3","type":"journal-article","created":{"date-parts":[[2024,9,19]],"date-time":"2024-09-19T07:13:52Z","timestamp":1726730032000},"page":"1871-1883","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":57,"title":["Epigenetic tuning of PD-1 expression improves exhausted T cell function and viral control"],"prefix":"10.1038","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4155-0346","authenticated-orcid":false,"given":"Sarah A.","family":"Weiss","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6646-6503","authenticated-orcid":false,"given":"Amy Y.","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Megan E.","family":"Fung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniela","family":"Martinez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8358-5408","authenticated-orcid":false,"given":"Alex C. Y.","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas J.","family":"LaSalle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian C.","family":"Miller","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7716-8504","authenticated-orcid":false,"given":"Christopher D.","family":"Scharer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mudra","family":"Hegde","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2767-0528","authenticated-orcid":false,"given":"Thao H.","family":"Nguyen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jared H.","family":"Rowe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jossef F.","family":"Osborn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dillon G.","family":"Patterson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia","family":"Sifnugel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8109-7339","authenticated-orcid":false,"given":"C.","family":"Mei-An Nolan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard A.","family":"Davidson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3869-0150","authenticated-orcid":false,"given":"Marc A.","family":"Schwartz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander P. R.","family":"Bally","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dennis K.","family":"Neeld","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5017-774X","authenticated-orcid":false,"given":"Martin W.","family":"LaFleur","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2432-1840","authenticated-orcid":false,"given":"Jeremy M.","family":"Boss","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3707-9889","authenticated-orcid":false,"given":"John G.","family":"Doench","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7871-3762","authenticated-orcid":false,"given":"W.","family":"Nicholas Haining","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9736-2109","authenticated-orcid":false,"given":"Arlene H.","family":"Sharpe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0947-8284","authenticated-orcid":false,"given":"Debattama R.","family":"Sen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,9,17]]},"reference":[{"key":"1961_CR1","doi-asserted-by":"publisher","first-page":"2205","DOI":"10.1084\/jem.188.12.2205","volume":"188","author":"AJ Zajac","year":"1998","unstructured":"Zajac, A. J. et al. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188, 2205\u20132213 (1998).","journal-title":"J. Exp. Med."},{"key":"1961_CR2","doi-asserted-by":"publisher","first-page":"4911","DOI":"10.1128\/JVI.77.8.4911-4927.2003","volume":"77","author":"E Wherry","year":"2003","unstructured":"Wherry, E. J. et al. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77, 4911\u20134927 (2003).","journal-title":"J. Virol."},{"key":"1961_CR3","doi-asserted-by":"publisher","first-page":"682","DOI":"10.1038\/nature04444","volume":"439","author":"DL Barber","year":"2006","unstructured":"Barber, D. L. et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682\u2013687 (2006).","journal-title":"Nature"},{"key":"1961_CR4","doi-asserted-by":"publisher","first-page":"14733","DOI":"10.1073\/pnas.1009731107","volume":"107","author":"H-T Jin","year":"2010","unstructured":"Jin, H.-T. et al. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl Acad. Sci. USA 107, 14733\u201314738 (2010).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1961_CR5","doi-asserted-by":"publisher","first-page":"824","DOI":"10.1016\/j.immuni.2007.11.006","volume":"27","author":"EJ Wherry","year":"2007","unstructured":"Wherry, E. J. et al. Molecular signature of CD8 T cell exhaustion during chronic viral infection. Immunity 27, 824 (2007).","journal-title":"Immunity"},{"key":"1961_CR6","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1038\/s41586-019-1326-9","volume":"571","author":"F Alfei","year":"2019","unstructured":"Alfei, F. et al. TOX reinforces the phenotype and longevity of exhausted T cells in chronic viral infection. Nature 571, 265\u2013269 (2019).","journal-title":"Nature"},{"key":"1961_CR7","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1038\/s41586-019-1325-x","volume":"571","author":"O Khan","year":"2019","unstructured":"Khan, O. et al. TOX transcriptionally and epigenetically programs CD8+ T cell exhaustion. Nature 571, 211\u2013218 (2019).","journal-title":"Nature"},{"key":"1961_CR8","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1038\/s41586-019-1324-y","volume":"571","author":"AC Scott","year":"2019","unstructured":"Scott, A. C. et al. TOX is a critical regulator of tumour-specific T cell differentiation. Nature 571, 270\u2013274 (2019).","journal-title":"Nature"},{"key":"1961_CR9","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1038\/nature19330","volume":"537","author":"SJ Im","year":"2016","unstructured":"Im, S. J. et al. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature 537, 417\u2013421 (2016).","journal-title":"Nature"},{"key":"1961_CR10","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1016\/j.immuni.2019.11.002","volume":"51","author":"WH Hudson","year":"2019","unstructured":"Hudson, W. H. et al. Proliferating transitory T cells with an effector-like transcriptional signature emerge from PD-1+ stem-like CD8+ T cells during chronic infection. Immunity 51, 1043\u20131058 (2019).","journal-title":"Immunity"},{"key":"1961_CR11","doi-asserted-by":"publisher","first-page":"1028","DOI":"10.1016\/j.immuni.2019.10.009","volume":"51","author":"R Zander","year":"2019","unstructured":"Zander, R. et al. CD4+ T cell help is required for the formation of a cytolytic CD8+ T cell subset that protects against chronic infection and cancer. Immunity 51, 1028\u20131042 (2019).","journal-title":"Immunity"},{"key":"1961_CR12","doi-asserted-by":"publisher","first-page":"1600","DOI":"10.1038\/s41590-022-01338-4","volume":"23","author":"JR Giles","year":"2022","unstructured":"Giles, J. R. et al. Shared and distinct biological circuits in effector, memory and exhausted CD8+ T cells revealed by temporal single-cell transcriptomics and epigenetics. Nat. Immunol. 23, 1600\u20131613 (2022).","journal-title":"Nat. Immunol."},{"key":"1961_CR13","doi-asserted-by":"publisher","first-page":"1614","DOI":"10.1038\/s41590-022-01337-5","volume":"23","author":"B Daniel","year":"2022","unstructured":"Daniel, B. et al. Divergent clonal differentiation trajectories of T cell exhaustion. Nat. Immunol. 23, 1614\u20131627 (2022).","journal-title":"Nat. Immunol."},{"key":"1961_CR14","doi-asserted-by":"publisher","first-page":"12293","DOI":"10.1073\/pnas.192461099","volume":"99","author":"Y Iwai","year":"2002","unstructured":"Iwai, Y. et al. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl Acad. Sci. USA 99, 12293\u201312297 (2002).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1961_CR15","doi-asserted-by":"publisher","first-page":"2443","DOI":"10.1056\/NEJMoa1200690","volume":"366","author":"SL Topalian","year":"2012","unstructured":"Topalian, S. L. et al. Safety, activity, and immune correlates of anti\u2013PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443\u20132454 (2012).","journal-title":"N. Engl. J. Med."},{"key":"1961_CR16","doi-asserted-by":"publisher","first-page":"1823","DOI":"10.1056\/NEJMoa1606774","volume":"375","author":"M Reck","year":"2016","unstructured":"Reck, M. et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N. Engl. J. Med. 375, 1823\u20131833 (2016).","journal-title":"N. Engl. J. Med."},{"key":"1961_CR17","doi-asserted-by":"publisher","first-page":"1856","DOI":"10.1056\/NEJMoa1602252","volume":"375","author":"RL Ferris","year":"2016","unstructured":"Ferris, R. L. et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N. Engl. J. Med. 375, 1856\u20131867 (2016).","journal-title":"N. Engl. J. Med."},{"key":"1961_CR18","doi-asserted-by":"publisher","first-page":"2542","DOI":"10.1056\/NEJMoa1603702","volume":"374","author":"PT Nghiem","year":"2016","unstructured":"Nghiem, P. T. et al. PD-1 blockade with pembrolizumab in advanced Merkel-cell carcinoma. N. Engl. J. Med. 374, 2542\u20132552 (2016).","journal-title":"N. Engl. J. Med."},{"key":"1961_CR19","doi-asserted-by":"publisher","first-page":"1803","DOI":"10.1056\/NEJMoa1510665","volume":"373","author":"RJ Motzer","year":"2015","unstructured":"Motzer, R. J. et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N. Engl. J. Med. 373, 1803\u20131813 (2015).","journal-title":"N. Engl. J. Med."},{"key":"1961_CR20","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.ccell.2015.06.012","volume":"28","author":"S Kelderman","year":"2015","unstructured":"Kelderman, S., Schumacher, T. N. & Kvistborg, P. Mismatch repair-deficient cancers are targets for anti-PD-1 therapy. Cancer Cell 28, 11\u201313 (2015).","journal-title":"Cancer Cell"},{"key":"1961_CR21","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2020.107827","volume":"31","author":"KE Pauken","year":"2020","unstructured":"Pauken, K. E. et al. The PD-1 pathway regulates development and function of memory CD8+ T cells following respiratory viral infection. Cell Rep. 31, 107827 (2020).","journal-title":"Cell Rep."},{"key":"1961_CR22","doi-asserted-by":"publisher","first-page":"eaba6006","DOI":"10.1126\/scitranslmed.aba6006","volume":"13","author":"V Kalia","year":"2021","unstructured":"Kalia, V. et al. Metabolic regulation by PD-1 signaling promotes long-lived quiescent CD8 T cell memory in mice. Sci. Transl. Med. 13, eaba6006 (2021).","journal-title":"Sci. Transl. Med."},{"key":"1961_CR23","doi-asserted-by":"publisher","first-page":"1125","DOI":"10.1084\/jem.20142237","volume":"212","author":"PM Odorizzi","year":"2015","unstructured":"Odorizzi, P. M. et al. Genetic absence of PD-1 promotes accumulation of terminally differentiated exhausted CD8+ T cells. J. Exp. Med. 212, 1125\u20131137 (2015).","journal-title":"J. Exp. Med."},{"key":"1961_CR24","doi-asserted-by":"publisher","first-page":"1165","DOI":"10.1126\/science.aae0491","volume":"354","author":"DR Sen","year":"2016","unstructured":"Sen, D. R. et al. The epigenetic landscape of T cell exhaustion. Science 354, 1165\u20131169 (2016).","journal-title":"Science"},{"key":"1961_CR25","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1038\/s41590-019-0312-6","volume":"20","author":"BC Miller","year":"2019","unstructured":"Miller, B. C. et al. Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade. Nat. Immunol. 20, 326\u2013336 (2019).","journal-title":"Nat. Immunol."},{"key":"1961_CR26","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1126\/science.aaf2807","volume":"354","author":"KE Pauken","year":"2016","unstructured":"Pauken, K. E. et al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354, 1160\u20131165 (2016).","journal-title":"Science"},{"key":"1961_CR27","doi-asserted-by":"publisher","first-page":"897","DOI":"10.1016\/j.cell.2018.12.036","volume":"176","author":"H Yoshida","year":"2019","unstructured":"Yoshida, H. et al. The cis-regulatory atlas of the mouse immune system. Cell 176, 897\u2013912 (2019).","journal-title":"Cell"},{"key":"1961_CR28","doi-asserted-by":"publisher","first-page":"8056","DOI":"10.1128\/jvi.68.12.8056-8063.1994","volume":"68","author":"M Matloubian","year":"1994","unstructured":"Matloubian, M., Concepcion, R. J. & Ahmed, R. CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J. Virol. 68, 8056\u20138063 (1994).","journal-title":"J. Virol."},{"key":"1961_CR29","doi-asserted-by":"publisher","first-page":"840","DOI":"10.1016\/j.immuni.2019.09.013","volume":"51","author":"Z Chen","year":"2019","unstructured":"Chen, Z. et al. TCF-1-centered transcriptional network drives an effector versus exhausted CD8 T cell-fate decision. Immunity 51, 840\u2013855 (2019).","journal-title":"Immunity"},{"key":"1961_CR30","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1016\/j.immuni.2020.04.014","volume":"52","author":"J-C Beltra","year":"2020","unstructured":"Beltra, J.-C. et al. Developmental relationships of four exhausted CD8+ T cell subsets reveals underlying transcriptional and epigenetic landscape control mechanisms. Immunity 52, 825\u2013841 (2020).","journal-title":"Immunity"},{"key":"1961_CR31","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-18035-1","volume":"11","author":"M Bentsen","year":"2020","unstructured":"Bentsen, M. et al. ATAC-seq footprinting unravels kinetics of transcription factor binding during zygotic genome activation. Nat. Commun. 11, 4267 (2020).","journal-title":"Nat. Commun."},{"key":"1961_CR32","doi-asserted-by":"publisher","first-page":"D165","DOI":"10.1093\/nar\/gkab1113","volume":"50","author":"JA Castro-Mondragon","year":"2022","unstructured":"Castro-Mondragon, J. A. et al. JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 50, D165\u2013D173 (2022).","journal-title":"Nucleic Acids Res."},{"key":"1961_CR33","doi-asserted-by":"publisher","first-page":"530","DOI":"10.1038\/s41586-019-0985-x","volume":"567","author":"J Chen","year":"2019","unstructured":"Chen, J. et al. NR4A transcription factors limit CAR T cell function in solid tumours. Nature 567, 530\u2013534 (2019).","journal-title":"Nature"},{"key":"1961_CR34","doi-asserted-by":"publisher","first-page":"1130","DOI":"10.1016\/j.immuni.2012.08.021","volume":"37","author":"TA Doering","year":"2012","unstructured":"Doering, T. A. et al. Network analysis reveals centrally connected genes and pathways involved in CD8+ T cell exhaustion versus memory. Immunity 37, 1130\u20131144 (2012).","journal-title":"Immunity"},{"key":"1961_CR35","doi-asserted-by":"publisher","first-page":"15545","DOI":"10.1073\/pnas.0506580102","volume":"102","author":"A Subramanian","year":"2005","unstructured":"Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545\u201315550 (2005).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1961_CR36","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1016\/j.cels.2015.12.004","volume":"1","author":"A Liberzon","year":"2015","unstructured":"Liberzon, A. et al. The Molecular Signatures Database (MSigDB) hallmark gene set collection. Cell Syst. 1, 417\u2013425 (2015).","journal-title":"Cell Syst."},{"key":"1961_CR37","doi-asserted-by":"publisher","first-page":"2485","DOI":"10.1084\/jem.20121015","volume":"209","author":"H Frebel","year":"2012","unstructured":"Frebel, H. et al. Programmed death 1 protects from fatal circulatory failure during systemic virus infection of mice. J. Exp. Med. 209, 2485\u20132499 (2012).","journal-title":"J. Exp. Med."},{"key":"1961_CR38","doi-asserted-by":"publisher","first-page":"eaba7365","DOI":"10.1126\/science.aba7365","volume":"367","author":"EA Stadtmauer","year":"2020","unstructured":"Stadtmauer, E. A. et al. CRISPR-engineered T cells in patients with refractory cancer. Science 367, eaba7365 (2020).","journal-title":"Science"},{"key":"1961_CR39","doi-asserted-by":"publisher","first-page":"2188","DOI":"10.1038\/s41423-021-00749-x","volume":"18","author":"Z Wang","year":"2021","unstructured":"Wang, Z. et al. Phase I study of CAR-T cells with PD-1 and TCR disruption in mesothelin-positive solid tumors. Cell. Mol. Immunol. 18, 2188\u20132198 (2021).","journal-title":"Cell. Mol. Immunol."},{"key":"1961_CR40","doi-asserted-by":"publisher","first-page":"10437","DOI":"10.1073\/pnas.1512503112","volume":"112","author":"K Schumann","year":"2015","unstructured":"Schumann, K. et al. Generation of knock-in primary human T cells using Cas9 ribonucleoproteins. Proc. Natl Acad. Sci. USA 112, 10437\u201310442 (2015).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1961_CR41","doi-asserted-by":"publisher","first-page":"745286","DOI":"10.3389\/fmolb.2021.745286","volume":"8","author":"RS Kalinin","year":"2021","unstructured":"Kalinin, R. S. et al. Engineered removal of PD-1 from the surface of CD19 CAR-T cells results in increased activation and diminished survival. Front. Mol. Biosci. 8, 745286 (2021).","journal-title":"Front. Mol. Biosci."},{"key":"1961_CR42","doi-asserted-by":"publisher","first-page":"1335","DOI":"10.1038\/s41590-019-0480-4","volume":"20","author":"MW LaFleur","year":"2019","unstructured":"LaFleur, M. W. et al. PTPN2 regulates the generation of exhausted CD8+ T cell subpopulations and restrains tumor immunity. Nat. Immunol. 20, 1335\u20131347 (2019).","journal-title":"Nat. Immunol."},{"key":"1961_CR43","doi-asserted-by":"publisher","first-page":"1039","DOI":"10.4049\/jimmunol.1701470","volume":"200","author":"M Guo","year":"2018","unstructured":"Guo, M. et al. EZH2 represses the B cell transcriptional program and regulates antibody-secreting cell metabolism and antibody production. J. Immunol. 200, 1039\u20131052 (2018).","journal-title":"J. Immunol."},{"key":"1961_CR44","doi-asserted-by":"publisher","first-page":"1193","DOI":"10.1038\/ng.3646","volume":"48","author":"MR Corces","year":"2016","unstructured":"Corces, M. R. et al. Lineage-specific and single-cell chromatin accessibility charts human hematopoiesis and leukemia evolution. Nat. Genet. 48, 1193\u20131203 (2016).","journal-title":"Nat. Genet."},{"key":"1961_CR45","doi-asserted-by":"publisher","first-page":"eaah4573","DOI":"10.1126\/science.aah4573","volume":"356","author":"AC Villani","year":"2017","unstructured":"Villani, A. C. et al. Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors. Science 356, eaah4573 (2017).","journal-title":"Science"},{"key":"1961_CR46","doi-asserted-by":"publisher","first-page":"102125","DOI":"10.1016\/j.xpro.2023.102125","volume":"4","author":"ALK Gonye","year":"2023","unstructured":"Gonye, A. L. K. et al. Protocol for bulk RNA sequencing of enriched human neutrophils from whole blood and estimation of sample purity. STAR Protoc. 4, 102125 (2023).","journal-title":"STAR Protoc."}],"container-title":["Nature Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41590-024-01961-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41590-024-01961-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41590-024-01961-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,30]],"date-time":"2024-09-30T03:43:22Z","timestamp":1727667802000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41590-024-01961-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,17]]},"references-count":46,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2024,10]]}},"alternative-id":["1961"],"URL":"https:\/\/doi.org\/10.1038\/s41590-024-01961-3","relation":{},"ISSN":["1529-2908","1529-2916"],"issn-type":[{"value":"1529-2908","type":"print"},{"value":"1529-2916","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,17]]},"assertion":[{"value":"29 November 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 August 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 September 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"A.H.S. has patents\/pending royalties on the PD-1 pathway from Roche and Novartis and has research funding from IOME, AbbVie, Taiwan Bio and Calico unrelated to the submitted work. A.H.S. serves on advisory boards for Elpiscience, Monopteros, Alixia, IOME, Corner Therapeutics, BioEntre, GlaxoSmithKline, Amgen and Janssen and is also on scientific advisory boards for the Massachusetts General Cancer Center, Program in Cellular and Molecular Medicine at Boston Children\u2019s Hospital, the Human Oncology and Pathogenesis Program at Memorial Sloan Kettering Cancer Center, Perlmutter Cancer Center at New York University, the Gladstone Institutes and the Bloomberg-Kimmel Institute for Cancer Immunotherapy at Johns Hopkins. A.H.S. is an academic editor for the <i>Journal of Experimental Medicine<\/i>. W.N.H. and D.R.S. have a patent application on T cell exhaustion-specific enhancers held by the Dana-Farber Cancer Institute. W.N.H. is a cofounder, employee of and equity holder in Arsenal Biosciences. W.N.H. holds equity in Tango Therapeutics and Arsenal Biosciences. B.C.M. has consulted for Cellarity, LifeOmic and Telix Pharmaceuticals. The remaining authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}