{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T10:01:03Z","timestamp":1792058463581,"version":"4.4.0"},"reference-count":47,"publisher":"Springer Science and Business Media LLC","issue":"8","license":[{"start":{"date-parts":[[2019,7,1]],"date-time":"2019-07-01T00:00:00Z","timestamp":1561939200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2019,7,1]],"date-time":"2019-07-01T00:00:00Z","timestamp":1561939200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Immunol"],"published-print":{"date-parts":[[2019,8]]},"DOI":"10.1038\/s41590-019-0430-1","type":"journal-article","created":{"date-parts":[[2019,7,1]],"date-time":"2019-07-01T12:02:51Z","timestamp":1561982571000},"page":"1004-1011","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":122,"title":["Mouse cytomegalovirus-experienced ILC1s acquire a memory response dependent on the viral glycoprotein m12"],"prefix":"10.1038","volume":"20","author":[{"given":"Orr-El","family":"Weizman","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5448-5865","authenticated-orcid":false,"given":"Eric","family":"Song","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5751-0480","authenticated-orcid":false,"given":"Nicholas M.","family":"Adams","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew D.","family":"Hildreth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luke","family":"Riggan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chirag","family":"Krishna","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oscar A.","family":"Aguilar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4571-5910","authenticated-orcid":false,"given":"Christina S.","family":"Leslie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James R.","family":"Carlyle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8062-9033","authenticated-orcid":false,"given":"Joseph C.","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1435-8188","authenticated-orcid":false,"given":"Timothy E.","family":"O\u2019Sullivan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2019,7,1]]},"reference":[{"key":"430_CR1","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1038\/nri.2017.146","volume":"18","author":"AN Henning","year":"2018","unstructured":"Henning, A. N., Roychoudhuri, R. & Restifo, N. P. Epigenetic control of CD8+ T cell differentiation. Nat. Rev. Immunol. 18, 340\u2013356 (2018).","journal-title":"Nat. Rev. Immunol"},{"key":"430_CR2","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1111\/imm.12074","volume":"139","author":"B Youngblood","year":"2013","unstructured":"Youngblood, B., Hale, J. S. & Ahmed, R. T-cell memory differentiation: insights from transcriptional signatures and epigenetics. Immunology 139, 277\u2013284 (2013).","journal-title":"Immunology"},{"key":"430_CR3","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1038\/nri.2017.99","volume":"18","author":"GR Bantug","year":"2018","unstructured":"Bantug, G. R., Galluzzi, L., Kroemer, G. & Hess, C. The spectrum of T cell metabolism in health and disease. Nat. Rev. Immunol. 18, 19\u201334 (2018).","journal-title":"Nat. Rev. Immunol"},{"key":"430_CR4","doi-asserted-by":"publisher","first-page":"1104","DOI":"10.1038\/ni.3031","volume":"15","author":"JT Chang","year":"2014","unstructured":"Chang, J. T., Wherry, E. J. & Goldrath, A. W. Molecular regulation of effector and memory T cell differentiation. Nat. Immunol. 15, 1104\u20131115 (2014).","journal-title":"Nat. Immunol"},{"key":"430_CR5","doi-asserted-by":"publisher","first-page":"886","DOI":"10.1016\/j.immuni.2014.12.007","volume":"41","author":"JM Schenkel","year":"2014","unstructured":"Schenkel, J. M. & Masopust, D. Tissue-resident memory T cells. Immunity 41, 886\u2013897 (2014).","journal-title":"Immunity"},{"key":"430_CR6","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1016\/j.immuni.2015.09.013","volume":"43","author":"TE O\u2019Sullivan","year":"2015","unstructured":"O\u2019Sullivan, T. E., Sun, J. C. & Lanier, L. L. Natural killer cell memory. Immunity 43, 634\u2013645 (2015).","journal-title":"Immunity"},{"key":"430_CR7","doi-asserted-by":"publisher","first-page":"aaf1098","DOI":"10.1126\/science.aaf1098","volume":"352","author":"MG Netea","year":"2016","unstructured":"Netea, M. G. et al. Trained immunity: a program of innate immune memory in health and disease. Science 352, aaf1098 (2016).","journal-title":"Science"},{"key":"430_CR8","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1016\/j.immuni.2016.06.017","volume":"45","author":"I Martinez-Gonzalez","year":"2016","unstructured":"Martinez-Gonzalez, I. et al. Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation. Immunity 45, 198\u2013208 (2016).","journal-title":"Immunity"},{"key":"430_CR9","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1038\/nature14189","volume":"517","author":"D Artis","year":"2015","unstructured":"Artis, D. & Spits, H. The biology of innate lymphoid cells. Nature 517, 293\u2013301 (2015).","journal-title":"Nature"},{"key":"430_CR10","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1038\/nri3855","volume":"15","author":"N Serafini","year":"2015","unstructured":"Serafini, N., Vosshenrich, C. A. & Di Santo, J. P. Transcriptional regulation of innate lymphoid cell fate. Nat. Rev. Immunol. 15, 415\u2013428 (2015).","journal-title":"Nat. Rev. Immunol."},{"key":"430_CR11","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1016\/j.immuni.2018.06.002","volume":"48","author":"ME Kotas","year":"2018","unstructured":"Kotas, M. E. & Locksley, R. M. Why innate lymphoid cells? Immunity 48, 1081\u20131090 (2018).","journal-title":"Immunity"},{"key":"430_CR12","doi-asserted-by":"publisher","first-page":"795","DOI":"10.1016\/j.cell.2017.09.052","volume":"171","author":"OE Weizman","year":"2017","unstructured":"Weizman, O. E. et al. ILC1 confer early host protection at initial sites of viral infection. Cell 171, 795\u2013808 e712 (2017).","journal-title":"Cell"},{"key":"430_CR13","doi-asserted-by":"publisher","first-page":"340","DOI":"10.1016\/j.cell.2014.03.030","volume":"157","author":"CSN Klose","year":"2014","unstructured":"Klose, C. S. N. et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157, 340\u2013356 (2014).","journal-title":"Cell"},{"key":"430_CR14","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.chom.2015.06.011","volume":"18","author":"MC Abt","year":"2015","unstructured":"Abt, M. C. et al. Innate immune defenses mediated by two ILC subsets are critical for protection against acute Clostridium difficile infection. Cell Host Microbe 18, 27\u201337 (2015).","journal-title":"Cell Host Microbe"},{"key":"430_CR15","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/j.immuni.2017.01.008","volume":"46","author":"S Boulenouar","year":"2017","unstructured":"Boulenouar, S. et al. Adipose type one innate lymphoid cells regulate macrophage homeostasis through targeted cytotoxicity. Immunity 46, 273\u2013286 (2017).","journal-title":"Immunity"},{"key":"430_CR16","doi-asserted-by":"publisher","first-page":"981","DOI":"10.1126\/science.aac9593","volume":"350","author":"G Gasteiger","year":"2015","unstructured":"Gasteiger, G., Fan, X., Dikiy, S., Lee, S. Y. & Rudensky, A. Y. Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 350, 981\u2013985 (2015).","journal-title":"Science"},{"key":"430_CR17","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1038\/ni.3309","volume":"17","author":"K Moro","year":"2016","unstructured":"Moro, K. et al. Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat. Immunol. 17, 76\u201386 (2016).","journal-title":"Nat. Immunol"},{"key":"430_CR18","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1038\/nature07665","volume":"457","author":"JC Sun","year":"2009","unstructured":"Sun, J. C., Beilke, J. N. & Lanier, L. L. Adaptive immune features of natural killer cells. Nature 457, 557\u2013561 (2009).","journal-title":"Nature"},{"key":"430_CR19","doi-asserted-by":"publisher","first-page":"947","DOI":"10.1084\/jem.20111760","volume":"209","author":"JC Sun","year":"2012","unstructured":"Sun, J. C. et al. Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 209, 947\u2013954 (2012).","journal-title":"J. Exp. Med"},{"key":"430_CR20","doi-asserted-by":"publisher","first-page":"546","DOI":"10.1038\/ni.2876","volume":"15","author":"AM Beaulieu","year":"2014","unstructured":"Beaulieu, A. M., Zawislak, C. L., Nakayama, T. & Sun, J. C. The transcription factor Zbtb32 controls the proliferative burst of virus-specific natural killer cells responding to infection. Nat. Immunol. 15, 546\u2013553 (2014).","journal-title":"Nat. Immunol"},{"key":"430_CR21","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/j.immuni.2018.12.024","volume":"50","author":"J Zhou","year":"2019","unstructured":"Zhou, J. et al. Liver-resident NK cells control antiviral activity of hepatic T cells via the PD-1-PD-L1 axis. Immunity 50, 403\u2013417.e4 (2019).","journal-title":"Immunity"},{"key":"430_CR22","doi-asserted-by":"publisher","first-page":"404","DOI":"10.1038\/ni.2536","volume":"14","author":"JA Best","year":"2013","unstructured":"Best, J. A. et al. Transcriptional insights into the CD8+ T cell response to infection and memory T cell formation. Nat. Immunol. 14, 404\u2013412 (2013).","journal-title":"Nat. Immunol"},{"key":"430_CR23","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1016\/j.cell.2016.07.006","volume":"166","author":"J van der Veeken","year":"2016","unstructured":"van der Veeken, J. et al. Memory of inflammation in regulatory T cells. Cell 166, 977\u2013990 (2016).","journal-title":"Cell"},{"key":"430_CR24","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1016\/j.it.2005.01.004","volume":"26","author":"LM Bradley","year":"2005","unstructured":"Bradley, L. M., Haynes, L. & Swain, S. L. IL-7: maintaining T-cell memory and achieving homeostasis. Trends Immunol. 26, 172\u2013176 (2005).","journal-title":"Trends Immunol"},{"key":"430_CR25","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1111\/imr.12644","volume":"283","author":"ME Raeber","year":"2018","unstructured":"Raeber, M. E., Zurbuchen, Y., Impellizzieri, D. & Boyman, O. The role of cytokines in T-cell memory in health and disease. Immunol. Rev. 283, 176\u2013193 (2018).","journal-title":"Immunol. Rev."},{"key":"430_CR26","doi-asserted-by":"publisher","first-page":"9971","DOI":"10.1073\/pnas.1203543109","volume":"109","author":"BE Freeman","year":"2012","unstructured":"Freeman, B. E., Hammarlund, E., Raue, H. P. & Slifka, M. K. Regulation of innate CD8+\u2009T-cell activation mediated by cytokines. Proc. Natl Acad. Sci. USA 109, 9971\u20139976 (2012).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"430_CR27","doi-asserted-by":"publisher","first-page":"2399","DOI":"10.4049\/jimmunol.170.5.2399","volume":"170","author":"T Kambayashi","year":"2003","unstructured":"Kambayashi, T., Assarsson, E., Lukacher, A. E., Ljunggren, H. G. & Jensen, P. E. Memory CD8+cells provide an early source of IFN-gamma. J. Immunol. 170, 2399\u20132408 (2003).","journal-title":"J. Immunol"},{"key":"430_CR28","doi-asserted-by":"publisher","first-page":"1000","DOI":"10.1038\/ni.2395","volume":"13","author":"NA Bezman","year":"2012","unstructured":"Bezman, N. A. et al. Molecular definition of the identity and activation of natural killer cells. Nat. Immunol. 13, 1000\u20131009 (2012).","journal-title":"Nat. Immunol"},{"key":"430_CR29","doi-asserted-by":"publisher","first-page":"1327","DOI":"10.1016\/j.immuni.2016.10.028","volume":"45","author":"JP Scott-Browne","year":"2016","unstructured":"Scott-Browne, J. P. et al. Dynamic changes in chromatin accessibility occur in CD8+\u2009T cells responding to viral infection. Immunity 45, 1327\u20131340 (2016).","journal-title":"Immunity"},{"key":"430_CR30","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1038\/s41590-018-0176-1","volume":"19","author":"CM Lau","year":"2018","unstructured":"Lau, C. M. et al. Epigenetic control of innate and adaptive immune memory. Nat. Immunol. 19, 963\u2013972 (2018).","journal-title":"Nat. Immunol."},{"key":"430_CR31","doi-asserted-by":"publisher","first-page":"2238","DOI":"10.4049\/jimmunol.1602086","volume":"198","author":"CD Scharer","year":"2017","unstructured":"Scharer, C. D., Bally, A. P., Gandham, B. & Boss, J. M. cutting edge: chromatin accessibility programs CD8 T cell memory. J. Immunol. 198, 2238\u20132243 (2017).","journal-title":"J. Immunol."},{"key":"430_CR32","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1126\/science.aad2035","volume":"352","author":"LK Mackay","year":"2016","unstructured":"Mackay, L. K. et al. Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352, 459\u2013463 (2016).","journal-title":"Science"},{"key":"430_CR33","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1016\/j.cell.2017.03.002","volume":"169","author":"OA Aguilar","year":"2017","unstructured":"Aguilar, O. A. et al. A viral immunoevasin controls innate immunity by targeting the prototypical natural killer cell receptor family. Cell 169, 58\u201371 e14 (2017).","journal-title":"Cell"},{"key":"430_CR34","doi-asserted-by":"publisher","first-page":"362","DOI":"10.3390\/v1030362","volume":"1","author":"JC Sun","year":"2009","unstructured":"Sun, J. C. & Lanier, L. L. The natural selection of herpesviruses and virus-specific NK cell receptors. Viruses 1, 362 (2009).","journal-title":"Viruses"},{"key":"430_CR35","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1016\/j.immuni.2008.07.017","volume":"29","author":"CM Snyder","year":"2008","unstructured":"Snyder, C. M. et al. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29, 650\u2013659 (2008).","journal-title":"Immunity"},{"key":"430_CR36","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1126\/science.1070884","volume":"296","author":"H Arase","year":"2002","unstructured":"Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B. & Lanier, L. L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296, 1323\u20131326 (2002).","journal-title":"Science"},{"key":"430_CR37","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1038\/ni1332","volume":"7","author":"JG O\u2019Leary","year":"2006","unstructured":"O\u2019Leary, J. G., Goodarzi, M., Drayton, D. L. & von Andrian, U. H. T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat. Immunol. 7, 507\u2013516 (2006).","journal-title":"Nat. Immunol."},{"key":"430_CR38","doi-asserted-by":"publisher","first-page":"1127","DOI":"10.1038\/ni.1953","volume":"11","author":"S Paust","year":"2010","unstructured":"Paust, S. et al. Critical role for the chemokine receptor CXCR6 in NK cell-mediated antigen-specific memory of haptens and viruses. Nat. Immunol. 11, 1127\u20131135 (2010).","journal-title":"Nat. Immunol."},{"key":"430_CR39","doi-asserted-by":"publisher","first-page":"1444","DOI":"10.1172\/JCI66381","volume":"123","author":"H Peng","year":"2013","unstructured":"Peng, H. et al. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123, 1444\u20131456 (2013).","journal-title":"J. Clin. Invest."},{"key":"430_CR40","doi-asserted-by":"publisher","first-page":"1915","DOI":"10.1073\/pnas.0813192106","volume":"106","author":"MA Cooper","year":"2009","unstructured":"Cooper, M. A. et al. Cytokine-induced memory-like natural killer cells. Proc. Natl Acad. Sci. USA 106, 1915\u20131919 (2009).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"430_CR41","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/j.chom.2012.06.006","volume":"12","author":"J Quintin","year":"2012","unstructured":"Quintin, J. et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12, 223\u2013232 (2012).","journal-title":"Cell Host Microbe"},{"key":"430_CR42","doi-asserted-by":"publisher","first-page":"2669","DOI":"10.1084\/jem.20141172","volume":"211","author":"G Min-Oo","year":"2014","unstructured":"Min-Oo, G. & Lanier, L. L. Cytomegalovirus generates long-lived antigen-specific NK cells with diminished bystander activation to heterologous infection. J. Exp. Med. 211, 2669\u20132680 (2014).","journal-title":"J. Exp. Med"},{"key":"430_CR43","doi-asserted-by":"publisher","first-page":"1258","DOI":"10.1038\/sj.gt.3300947","volume":"6","author":"F Liu","year":"1999","unstructured":"Liu, F., Song, Y. & Liu, D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6, 1258\u20131266 (1999).","journal-title":"Gene Ther."},{"key":"430_CR44","doi-asserted-by":"publisher","first-page":"12565","DOI":"10.1073\/pnas.1814589115","volume":"115","author":"M Tokuyama","year":"2018","unstructured":"Tokuyama, M. et al. ERVmap analysis reveals genome-wide transcription of human endogenous retroviruses. Proc. Natl Acad. Sci. USA 115, 12565\u201312572 (2018).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"430_CR45","doi-asserted-by":"publisher","first-page":"1213","DOI":"10.1038\/nmeth.2688","volume":"10","author":"JD Buenrostro","year":"2013","unstructured":"Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213\u20131218 (2013).","journal-title":"Nat. Methods"},{"key":"430_CR46","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2008-9-9-r137","volume":"9","author":"Y Zhang","year":"2008","unstructured":"Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).","journal-title":"Genome Biol"},{"key":"430_CR47","doi-asserted-by":"publisher","first-page":"1876","DOI":"10.1214\/11-AOAS477","volume":"5","author":"CM Zigler","year":"2011","unstructured":"Zigler, C. M. & Belin, T. R. The potential for bias in principal causal effect estimation when treatment received depends on a key covariate. Ann. Appl. Stat. 5, 1876\u20131892 (2011).","journal-title":"Ann. Appl. Stat"}],"container-title":["Nature Immunology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/s41590-019-0430-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41590-019-0430-1","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41590-019-0430-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,20]],"date-time":"2023-05-20T17:51:55Z","timestamp":1684605115000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41590-019-0430-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,7,1]]},"references-count":47,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2019,8]]}},"alternative-id":["430"],"URL":"https:\/\/doi.org\/10.1038\/s41590-019-0430-1","relation":{},"ISSN":["1529-2908","1529-2916"],"issn-type":[{"value":"1529-2908","type":"print"},{"value":"1529-2916","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,7,1]]},"assertion":[{"value":"14 September 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 May 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 July 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}