{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,19]],"date-time":"2026-03-19T04:34:35Z","timestamp":1773894875903,"version":"3.50.1"},"reference-count":42,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2020,1,15]],"date-time":"2020-01-15T00:00:00Z","timestamp":1579046400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"DOI":"10.3389\/fimmu.2019.03113","type":"journal-article","created":{"date-parts":[[2020,1,15]],"date-time":"2020-01-15T04:32:51Z","timestamp":1579062771000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":5,"title":["Enhanced Cell Division Is Required for the Generation of Memory CD4 T Cells to Migrate Into Their Proper Location"],"prefix":"10.3389","volume":"10","author":[{"given":"Jana","family":"Sarkander","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shintaro","family":"Hojyo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mathias","family":"Mursell","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuzuru","family":"Yamasaki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tsung-Yen","family":"Wu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Damon J.","family":"Tumes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kosuke","family":"Miyauchi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cam Loan","family":"Tran","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jinfang","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Max","family":"L\u00f6hning","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andreas","family":"Hutloff","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mir-Farzin","family":"Mashreghi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Masato","family":"Kubo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andreas","family":"Radbruch","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Koji","family":"Tokoyoda","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2020,1,15]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1111\/j.0105-2896.2006.00388.x","article-title":"CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza","volume":"1","author":"Swain","year":"2008","journal-title":"Immunol Rev"},{"key":"B2","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1615\/CritRevImmunol.2014010373","article-title":"CD4 T-cell memory generation and maintenance","volume":"34","author":"Gasper","year":"2014","journal-title":"Crit Rev Immunol"},{"key":"B3","doi-asserted-by":"publisher","first-page":"670","DOI":"10.1016\/j.it.2015.09.004","article-title":"Asymmetric cell division in T lymphocyte fate diversification","volume":"36","author":"Arsenio","year":"2015","journal-title":"Trends Immunol"},{"key":"B4","doi-asserted-by":"publisher","first-page":"5039","DOI":"10.4049\/jimmunol.1003650","article-title":"Strength of TCR-peptide\/MHC interactions and in vivo T cell responses","volume":"186","author":"Corse","year":"2011","journal-title":"J Immunol"},{"key":"B5","doi-asserted-by":"publisher","first-page":"159","DOI":"10.3389\/fimmu.2012.00159","article-title":"TCR signaling emerges from the sum of many parts","volume":"3","author":"Kuhns","year":"2012","journal-title":"Front Immunol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1038\/nature07657","article-title":"Complete but curtailed T-cell response to very low-affinity antigen","volume":"458","author":"Zehn","year":"2009","journal-title":"Nature"},{"key":"B7","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1084\/jem.20101574","article-title":"High prevalence of low affinity peptide\u2013MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses","volume":"208","author":"Sabatino","year":"2011","journal-title":"J Exp Med."},{"key":"B8","doi-asserted-by":"publisher","first-page":"508","DOI":"10.1016\/j.immuni.2013.08.033","article-title":"Sustained interactions between T cell receptors and antigens promote the differentiation of CD4+ memory T cells","volume":"39","author":"Kim","year":"2013","journal-title":"Immunity"},{"key":"B9","doi-asserted-by":"publisher","first-page":"2310","DOI":"10.4049\/jimmunol.1100363","article-title":"Duration of antigen availability influences the expansion and memory differentiation of T cells","volume":"187","author":"Blair","year":"2011","journal-title":"J Immunol"},{"key":"B10","doi-asserted-by":"publisher","first-page":"1381","DOI":"10.1126\/science.286.5443.1381","article-title":"Class II-independent generation of CD4 memory T cells from effectors","volume":"286","author":"Swain","year":"1999","journal-title":"Science."},{"key":"B11","doi-asserted-by":"publisher","first-page":"721","DOI":"10.1016\/j.immuni.2009.03.015","article-title":"Professional memory CD4+ T lymphocytes preferentially reside and rest in the bone marrow","volume":"30","author":"Tokoyoda","year":"2009","journal-title":"Immunity"},{"key":"B12","doi-asserted-by":"publisher","first-page":"9229","DOI":"10.1073\/pnas.1318731111","article-title":"Human memory T cells from the bone marrow are resting and maintain long-lasting systemic memory","volume":"111","author":"Okhrimenko","year":"2014","journal-title":"Proc Natl Acad Sci USA"},{"key":"B13","doi-asserted-by":"publisher","first-page":"7409","DOI":"10.1073\/pnas.1118539109","article-title":"Type II membrane protein CD69 regulates the formation of resting T-helper memory","volume":"109","author":"Shinoda","year":"2012","journal-title":"Proc Natl Acad Sci USA"},{"key":"B14","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1038\/icb.2013.36","article-title":"CD49b-dependent establishment of T helper cell memory","volume":"91","author":"Hanazawa","year":"2013","journal-title":"Immunol Cell Biol"},{"key":"B15","doi-asserted-by":"publisher","first-page":"26","DOI":"10.3389\/fimmu.2016.00026","article-title":"B cells negatively regulate the establishment of CD49b(+)T-bet(+) resting memory T helper cells in the bone marrow","volume":"7","author":"Hojyo","year":"2016","journal-title":"Front Immunol"},{"key":"B16","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1002\/(SICI)1521-4141(199801)28:01<390::AID-IMMU390>3.0.CO;2-O","article-title":"Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection","volume":"28","author":"Oxenius","year":"1998","journal-title":"Eur J Immunol"},{"key":"B17","doi-asserted-by":"publisher","first-page":"660","DOI":"10.1016\/j.immuni.2012.09.007","article-title":"The transcription factor T-bet is induced by multiple pathways and prevents an endogenous Th2 cell program during Th1 cell responses","volume":"37","author":"Zhu","year":"2012","journal-title":"Immunity"},{"key":"B18","doi-asserted-by":"publisher","first-page":"1584","DOI":"10.1002\/eji.201646632","article-title":"Guidelines for the use of flow cytometry and cell sorting in immunological studies","volume":"47","author":"Cossarizza","year":"2017","journal-title":"Eur J Immunol"},{"key":"B19","doi-asserted-by":"publisher","first-page":"1334","DOI":"10.1073\/pnas.1715618115","article-title":"Nonfollicular reactivation of bone marrow resident memory CD4 T cells in immune clusters of the bone marrow","volume":"115","author":"Siracusa","year":"2018","journal-title":"Proc Natl Acad Sci USA"},{"key":"B20","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1084\/jem.20141432","article-title":"ICOS maintains the T follicular helper cell phenotype by down-regulating Kr\u00fcppel-like factor 2","volume":"212","author":"Weber","year":"2015","journal-title":"J Exp Med"},{"key":"B21","doi-asserted-by":"publisher","first-page":"1192","DOI":"10.1002\/eji.201444633","article-title":"MiR-148a is upregulated by Twist1 and T-bet and promotes Th1-cell survival by regulating the proapoptotic gene Bim","volume":"45","author":"Haftmann","year":"2015","journal-title":"Eur J Immunol"},{"key":"B22","doi-asserted-by":"publisher","first-page":"1057","DOI":"10.1038\/ni.1945","article-title":"The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes","volume":"11","author":"Stittrich","year":"2010","journal-title":"Nat Immunol"},{"key":"B23","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1016\/S0092-8674(00)80702-3","article-title":"A novel transcription factor, T-bet, directs Th1 lineage commitment","volume":"100","author":"Szabo","year":"2000","journal-title":"Cell"},{"key":"B24","doi-asserted-by":"publisher","first-page":"3432","DOI":"10.1182\/blood-2005-04-1393","article-title":"T-bet is required for optimal proinflammatory CD4+ T-cell trafficking","volume":"106","author":"Lord","year":"2005","journal-title":"Blood"},{"key":"B25","doi-asserted-by":"publisher","first-page":"682","DOI":"10.1038\/nature04444","article-title":"Restoring function in exhausted CD8 T cells during chronic viral infection","volume":"439","author":"Barber","year":"2006","journal-title":"Nature"},{"key":"B26","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1002\/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-9","article-title":"The Ki-67 protein: From the known and the unknown","volume":"182","author":"Scholzen","year":"2000","journal-title":"J Cell Phys"},{"key":"B27","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1615\/CritRevImmunol.v28.i2.20","article-title":"Immune-potentiating effects of the chemotherapeutic drug cyclophosphamide","volume":"28","author":"Brode","year":"2008","journal-title":"Crit Rev Immunol"},{"key":"B28","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1084\/jem.174.3.561","article-title":"CTLA-4 is a second receptor for the B cell activation antigen B7","volume":"174","author":"Linsley","year":"1991","journal-title":"J Exp Med"},{"key":"B29","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/S0092-8674(00)80059-8","article-title":"CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs","volume":"99","author":"F\u00f6rster","year":"1999","journal-title":"Cell"},{"key":"B30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/ncomms6377","article-title":"Effector CD4 T-cell transition to memory requires late cognate interactions that induce autocrine IL-2","volume":"5","author":"McKinstry","year":"2014","journal-title":"Nat Commun"},{"key":"B31","doi-asserted-by":"publisher","first-page":"1255","DOI":"10.1038\/ni1513","article-title":"Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells","volume":"8","author":"Link","year":"2007","journal-title":"Nat Immunol"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1266","DOI":"10.1002\/eji.200939921","article-title":"CCL21 is sufficient to mediate DC migration, maturation and function in the absence of CCL19","volume":"40","author":"Britschgi","year":"2010","journal-title":"Eur J Immunol"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1925","DOI":"10.1084\/jem.20161864","article-title":"Essential role of CCL21 in establishment of central self-tolerance in T cells","volume":"214","author":"Kozai","year":"2017","journal-title":"J Exp Med"},{"key":"B34","doi-asserted-by":"publisher","first-page":"1792","DOI":"10.1002\/1521-4141(200206)32:6<1792::AID-IMMU1792>3.0.CO;2-0","article-title":"Induction of the chemokine receptor CXCR3 on TCR-stimulated T cells: dependence on the release from persistent TCR-triggering and requirement for IFN-gamma stimulation","volume":"32","author":"Nakajima","year":"2002","journal-title":"Eur J Immunol"},{"key":"B35","doi-asserted-by":"publisher","first-page":"701","DOI":"10.1093\/intimm\/dxg066","article-title":"Differential regulation of VLA-2 expression on Th1 and Th2 cells: a novel marker for the classification of Th subsets","volume":"15","author":"Sasaki","year":"2003","journal-title":"Int Immunol"},{"key":"B36","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1146\/annurev-immunol-042617-053352","article-title":"Signaling and Function of Interleukin-2 in T Lymphocytes","volume":"36","author":"Ross","year":"2018","journal-title":"Annu Rev Immunol"},{"key":"B37","doi-asserted-by":"publisher","first-page":"1687","DOI":"10.1126\/science.1139393","article-title":"Asymmetric T lymphocyte adaptive immune responses","volume":"315","author":"Chang","year":"2007","journal-title":"Science"},{"key":"B38","doi-asserted-by":"publisher","first-page":"3640","DOI":"10.4049\/jimmunol.165.7.3640","article-title":"Cellular interactions involved in Th cell memory","volume":"165","author":"van Essen","year":"2000","journal-title":"J Immunol"},{"key":"B39","doi-asserted-by":"publisher","first-page":"5558","DOI":"10.4049\/jimmunol.165.10.5558","article-title":"A critical role for B cells in the development of memory CD4 cells","volume":"165","author":"Linton","year":"2000","journal-title":"J Immunol"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1868","DOI":"10.4049\/jimmunol.0802501","article-title":"Requirement of B cells for generating CD4+ T cell memory","volume":"182","author":"Whitmire","year":"2009","journal-title":"J Immunol"},{"key":"B41","doi-asserted-by":"publisher","first-page":"6052","DOI":"10.4049\/jimmunol.1302033","article-title":"Temporal requirements for B cells in the establishment of CD4 T cell memory","volume":"191","author":"Mollo","year":"2013","journal-title":"J Immunol"},{"key":"B42","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1084\/jem.20062381","article-title":"Interleukin-2 enhances CD4+ T cell memory by promoting the generation of IL-7R\u03b1-expressing cells","volume":"204","author":"Dooms","year":"2007","journal-title":"J Exp Med"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2019.03113\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,1,15]],"date-time":"2020-01-15T04:32:53Z","timestamp":1579062773000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2019.03113\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,15]]},"references-count":42,"alternative-id":["10.3389\/fimmu.2019.03113"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2019.03113","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,15]]},"article-number":"3113"}}