{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T06:21:59Z","timestamp":1790403719989,"version":"4.1.0"},"reference-count":46,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2020,9,2]],"date-time":"2020-09-02T00:00:00Z","timestamp":1599004800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01 AI039614"],"award-info":[{"award-number":["R01 AI039614"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["F32 AI114050"],"award-info":[{"award-number":["F32 AI114050"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["1K08AI141761-01A1"],"award-info":[{"award-number":["1K08AI141761-01A1"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["UL1TR002494"],"award-info":[{"award-number":["UL1TR002494"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"DOI":"10.3389\/fimmu.2020.02125","type":"journal-article","created":{"date-parts":[[2020,9,2]],"date-time":"2020-09-02T05:42:36Z","timestamp":1599025356000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":13,"title":["Antigen-Specific CD4+ T Cells Exhibit Distinct Kinetic and Phenotypic Patterns During Primary and Secondary Responses to Infection"],"prefix":"10.3389","volume":"11","author":[{"given":"Deepali","family":"Malhotra","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristina S.","family":"Burrack","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc K.","family":"Jenkins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne E.","family":"Frosch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2020,9,2]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1038\/nprot.2009.9","article-title":"Tracking epitope-specific T cells.","volume":"4","author":"Moon","year":"2009","journal-title":"Nat Protoc."},{"key":"B2","doi-asserted-by":"publisher","first-page":"1203","DOI":"10.1126\/science.1201730","article-title":"Different B cell populations mediate early and late memory during an endogenous immune response.","volume":"331","author":"Pape","year":"2011","journal-title":"Science."},{"key":"B3","doi-asserted-by":"publisher","first-page":"511","DOI":"10.1126\/science.aad0483","article-title":"Most microbe-specific naive CD4(+) T cells produce memory cells during infection.","volume":"351","author":"Tubo","year":"2016","journal-title":"Science."},{"key":"B4","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1016\/j.immuni.2011.09.009","article-title":"Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells.","volume":"35","author":"Pepper","year":"2011","journal-title":"Immunity."},{"key":"B5","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1016\/j.immuni.2013.02.020","article-title":"Distinct memory CD4+ T cells with commitment to T follicular helper- and T helper 1-cell lineages are generated after acute viral infection.","volume":"38","author":"Hale","year":"2013","journal-title":"Immunity."},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2014.00050","article-title":"The bacterial pathogen Listeria monocytogenes and the interferon family: type I, type II and type III interferons.","volume":"4","author":"Dussurget","year":"2014","journal-title":"Front Cell Infect Microbiol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"785","DOI":"10.1016\/j.cell.2013.04.007","article-title":"Single naive CD4+ T cells from a diverse repertoire produce different effector cell types during infection.","volume":"153","author":"Tubo","year":"2013","journal-title":"Cell."},{"key":"B8","doi-asserted-by":"publisher","first-page":"886","DOI":"10.1016\/j.immuni.2014.12.007","article-title":"Tissue-resident memory T cells.","volume":"41","author":"Schenkel","year":"2014","journal-title":"Immunity."},{"key":"B9","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1038\/ni.1718","article-title":"Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus.","volume":"10","author":"Gebhardt","year":"2009","journal-title":"Nat Immunol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1444","DOI":"10.1172\/jci66381","article-title":"Liver-resident NK cells confer adaptive immunity in skin-contact inflammation.","volume":"123","author":"Peng","year":"2013","journal-title":"J Clin Invest."},{"key":"B11","doi-asserted-by":"publisher","first-page":"2921","DOI":"10.1016\/j.celrep.2017.08.078","article-title":"Human tissue-resident memory t cells are defined by core transcriptional and functional signatures in lymphoid and mucosal sites.","volume":"20","author":"Kumar","year":"2017","journal-title":"Cell Rep."},{"key":"B12","doi-asserted-by":"publisher","first-page":"2467","DOI":"10.4049\/jimmunol.1402756","article-title":"Cutting edge: identification and characterization of human intrahepatic CD49a+ NK cells.","volume":"194","author":"Marquardt","year":"2015","journal-title":"J Immunol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1016\/j.immuni.2017.01.009","article-title":"CD49a expression defines tissue-resident CD8(+) T cells poised for cytotoxic function in human skin.","volume":"46","author":"Cheuk","year":"2017","journal-title":"Immunity."},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.01247","article-title":"CD49a expression identifies a subset of intrahepatic macrophages in humans.","volume":"10","author":"Martrus","year":"2019","journal-title":"Front Immunol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"3032","DOI":"10.4049\/jimmunol.0803402","article-title":"Selective priming and expansion of antigen-specific Foxp3- CD4+ T cells during Listeria monocytogenes infection.","volume":"182","author":"Ertelt","year":"2009","journal-title":"J Immunol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"477","DOI":"10.4049\/jimmunol.1701434","article-title":"Cutting edge: allograft rejection is associated with weak T Cell responses to many different graft leukocyte-derived peptides.","volume":"200","author":"Burrack","year":"2018","journal-title":"J Immunol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1038\/ni.2568","article-title":"Sensing and alarm function of resident memory CD8(+) T cells.","volume":"14","author":"Schenkel","year":"2013","journal-title":"Nat Immunol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1083\/jcb.200205009","article-title":"The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity.","volume":"158","author":"Portnoy","year":"2002","journal-title":"J Cell Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1016\/j.immuni.2007.07.007","article-title":"Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude.","volume":"27","author":"Moon","year":"2007","journal-title":"Immunity."},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1126\/sciimmunol.aay5552","article-title":"Long-lived T follicular helper cells retain plasticity and help sustain humoral immunity.","volume":"5","author":"Kunzli","year":"2020","journal-title":"Sci Immunol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1016\/j.immuni.2011.08.016","article-title":"Differential expression of Ly6C and T-bet distinguish effector and memory Th1 CD4(+) cell properties during viral infection.","volume":"35","author":"Marshall","year":"2011","journal-title":"Immunity."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1761","DOI":"10.4049\/jimmunol.1701154","article-title":"Cytokine- and TCR-Mediated Regulation of T Cell Expression of Ly6C and Sca-1.","volume":"200","author":"DeLong","year":"2018","journal-title":"J Immunol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"15818","DOI":"10.1073\/pnas.2636938100","article-title":"Antigen-driven effector CD8 T cell function regulated by T-bet.","volume":"100","author":"Sullivan","year":"2003","journal-title":"Proc Natl Acad Sci USA."},{"key":"B24","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.4049\/jimmunol.1401617","article-title":"Diverse roles for T-bet in the effector responses required for resistance to infection.","volume":"194","author":"Harms Pritchard","year":"2015","journal-title":"J Immunol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"2705","DOI":"10.1084\/jem.20180927","article-title":"Transient T-bet expression functionally specifies a distinct T follicular helper subset.","volume":"215","author":"Fang","year":"2018","journal-title":"J Exp Med."},{"key":"B26","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1084\/jem.179.1.259","article-title":"Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody.","volume":"179","author":"Conlan","year":"1994","journal-title":"J Exp Med."},{"key":"B27","doi-asserted-by":"publisher","first-page":"741","DOI":"10.1084\/jem.174.3.741","article-title":"Neutrophil-mediated dissolution of infected host cells as a defense strategy against a facultative intracellular bacterium.","volume":"174","author":"Conlan","year":"1991","journal-title":"J Exp Med."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1000041","article-title":"Tentative T cells: memory cells are quick to respond, but slow to divide.","volume":"4","author":"Whitmire","year":"2008","journal-title":"PLoS Pathog."},{"key":"B29","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1016\/j.immuni.2011.03.020","article-title":"Protective capacity of memory CD8+ T cells is dictated by antigen exposure history and nature of the infection.","volume":"34","author":"Nolz","year":"2011","journal-title":"Immunity."},{"key":"B30","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1016\/j.immuni.2013.07.003","article-title":"Preexisting high frequencies of memory CD8+ T cells favor rapid memory differentiation and preservation of proliferative potential upon boosting.","volume":"39","author":"Fraser","year":"2013","journal-title":"Immunity."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1841","DOI":"10.1084\/jem.20120219","article-title":"Bcl6 expression specifies the T follicular helper cell program in vivo.","volume":"209","author":"Liu","year":"2012","journal-title":"J Exp Med."},{"key":"B32","first-page":"255","article-title":"Mouse Ly-6 proteins and their extended family: markers of cell differentiation and regulators of cell signaling.","volume":"52","author":"Bamezai","year":"2004","journal-title":"Arch Immunol Ther Exp (Warsz)."},{"key":"B33","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1084\/jem.20052237","article-title":"Secondary memory CD8+ T cells are more protective but slower to acquire a central-memory phenotype.","volume":"203","author":"Jabbari","year":"2006","journal-title":"J Exp Med."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-50614-1","article-title":"12 signaling drives the differentiation and function of a TH1-derived TFH1-like cell population.","volume":"9","author":"Powell","year":"2019","journal-title":"Sci Rep."},{"key":"B35","doi-asserted-by":"publisher","first-page":"4014","DOI":"10.4049\/jimmunol.1202963","article-title":"Bcl6 expressing follicular helper CD4 T cells are fate committed early and have the capacity to form memory.","volume":"190","author":"Choi","year":"2013","journal-title":"J Immunol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/j.immuni.2018.12.019","article-title":"The Emergence and functional fitness of memory CD4(+) T cells require the transcription factor thpok.","volume":"50","author":"Ciucci","year":"2019","journal-title":"Immunity."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1294","DOI":"10.1038\/ni.2744","article-title":"The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin.","volume":"14","author":"Mackay","year":"2013","journal-title":"Nat Immunol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"679","DOI":"10.1046\/j.1365-2567.1999.00812.x","article-title":"Integrin alpha1beta1 (VLA-1) mediates adhesion of activated intraepithelial lymphocytes to collagen.","volume":"97","author":"Roberts","year":"1999","journal-title":"Immunology."},{"key":"B39","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/s1074-7613(04)00021-4","article-title":"The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection.","volume":"20","author":"Ray","year":"2004","journal-title":"Immunity."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1214","DOI":"10.1084\/jem.20181365","article-title":"CD4(+) resident memory T cells dominate immunosurveillance and orchestrate local recall responses.","volume":"216","author":"Beura","year":"2019","journal-title":"J Exp Med."},{"key":"B41","doi-asserted-by":"publisher","first-page":"2748","DOI":"10.1084\/jem.20181308","article-title":"CXCR6 regulates localization of tissue-resident memory CD8 T cells to the airways.","volume":"216","author":"Wein","year":"2019","journal-title":"J Exp Med."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1467","DOI":"10.1038\/ni.3589","article-title":"Programs for the persistence, vigilance and control of human CD8(+) lung-resident memory T cells.","volume":"17","author":"Hombrink","year":"2016","journal-title":"Nat Immunol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"1508","DOI":"10.1093\/infdis\/jiu281","article-title":"The chemokine receptor CXCR6 is required for the maintenance of liver memory CD8(+) T cells specific for infectious pathogens.","volume":"210","author":"Tse","year":"2014","journal-title":"J Infect Dis."},{"key":"B44","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1111\/imm.13059","article-title":"Origins of CD4(+) circulating and tissue-resident memory T-cells.","volume":"157","author":"Nguyen","year":"2019","journal-title":"Immunology."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1458","DOI":"10.1093\/cid\/cit048","article-title":"Complex correlates of protection after vaccination.","volume":"56","author":"Plotkin","year":"2013","journal-title":"Clin Infect Dis."},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-12464-3","article-title":"Single-cell transcriptomics of human T cells reveals tissue and activation signatures in health and disease.","volume":"10","author":"Szabo","year":"2019","journal-title":"Nat Commun."}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2020.02125\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,9,2]],"date-time":"2020-09-02T05:42:40Z","timestamp":1599025360000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2020.02125\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,9,2]]},"references-count":46,"alternative-id":["10.3389\/fimmu.2020.02125"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2020.02125","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,9,2]]},"article-number":"2125"}}