{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T09:32:49Z","timestamp":1791279169182,"version":"4.1.0"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"8","license":[{"start":{"date-parts":[[2013,6,30]],"date-time":"2013-06-30T00:00:00Z","timestamp":1372550400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nat Immunol"],"published-print":{"date-parts":[[2013,8]]},"DOI":"10.1038\/ni.2648","type":"journal-article","created":{"date-parts":[[2013,7,1]],"date-time":"2013-07-01T12:09:47Z","timestamp":1372680587000},"page":"849-857","source":"Crossref","is-referenced-by-count":164,"title":["MicroRNAs of the miR-17\u223c92 family are critical regulators of TFH differentiation"],"prefix":"10.1038","volume":"14","author":[{"given":"Seung Goo","family":"Kang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Hsien","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peiwen","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyun Yong","family":"Jin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyung W","family":"Lim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jovan","family":"Shepherd","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Fremgen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric","family":"Verdin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael B A","family":"Oldstone","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hai","family":"Qi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John R","family":"Teijaro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Changchun","family":"Xiao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2013,6,30]]},"reference":[{"key":"BFni2648_CR1","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1038\/nature02871","volume":"431","author":"V Ambros","year":"2004","unstructured":"Ambros, V. The functions of animal microRNAs. Nature 431, 350\u2013355 (2004).","journal-title":"Nature"},{"key":"BFni2648_CR2","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/S0092-8674(04)00045-5","volume":"116","author":"DP Bartel","year":"2004","unstructured":"Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281\u2013297 (2004).","journal-title":"Cell"},{"key":"BFni2648_CR3","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1146\/annurev.cellbio.23.090506.123406","volume":"23","author":"N Bushati","year":"2007","unstructured":"Bushati, N. & Cohen, S.M. microRNA functions. Annu. Rev. Cell Dev. Biol. 23, 175\u2013205 (2007).","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"BFni2648_CR4","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1038\/nri2708","volume":"10","author":"RM O'Connell","year":"2010","unstructured":"O'Connell, R.M., Rao, D.S., Chaudhuri, A.A. & Baltimore, D. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111\u2013122 (2010).","journal-title":"Nat. Rev. Immunol."},{"key":"BFni2648_CR5","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.cell.2008.12.027","volume":"136","author":"C Xiao","year":"2009","unstructured":"Xiao, C. & Rajewsky, K. MicroRNA control in the immune system: basic principles. Cell 136, 26\u201336 (2009).","journal-title":"Cell"},{"key":"BFni2648_CR6","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1016\/j.cell.2008.04.001","volume":"133","author":"JT Mendell","year":"2008","unstructured":"Mendell, J.T. miRiad roles for the miR-17\u201392 cluster in development and disease. Cell 133, 217\u2013222 (2008).","journal-title":"Cell"},{"key":"BFni2648_CR7","doi-asserted-by":"publisher","first-page":"875","DOI":"10.1016\/j.cell.2008.02.019","volume":"132","author":"A Ventura","year":"2008","unstructured":"Ventura, A. et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132, 875\u2013886 (2008).","journal-title":"Cell"},{"key":"BFni2648_CR8","doi-asserted-by":"publisher","first-page":"621","DOI":"10.1146\/annurev-immunol-031210-101400","volume":"29","author":"S Crotty","year":"2011","unstructured":"Crotty, S. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29, 621\u2013663 (2011).","journal-title":"Annu. Rev. Immunol."},{"key":"BFni2648_CR9","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.1126\/science.1175870","volume":"325","author":"RJ Johnston","year":"2009","unstructured":"Johnston, R.J. et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 325, 1006\u20131010 (2009).","journal-title":"Science"},{"key":"BFni2648_CR10","doi-asserted-by":"publisher","first-page":"1001","DOI":"10.1126\/science.1176676","volume":"325","author":"RI Nurieva","year":"2009","unstructured":"Nurieva, R.I. et al. Bcl6 mediates the development of T follicular helper cells. Science 325, 1001\u20131005 (2009).","journal-title":"Science"},{"key":"BFni2648_CR11","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1016\/j.immuni.2009.07.002","volume":"31","author":"D Yu","year":"2009","unstructured":"Yu, D. et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31, 457\u2013468 (2009).","journal-title":"Immunity"},{"key":"BFni2648_CR12","doi-asserted-by":"publisher","first-page":"763","DOI":"10.1016\/S1074-7613(01)00227-8","volume":"15","author":"PP Lee","year":"2001","unstructured":"Lee, P.P. et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763\u2013774 (2001).","journal-title":"Immunity"},{"key":"BFni2648_CR13","doi-asserted-by":"publisher","first-page":"987","DOI":"10.1084\/jem.20101773","volume":"208","author":"LM Fahey","year":"2011","unstructured":"Fahey, L.M. et al. Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J. Exp. Med. 208, 987\u2013999 (2011).","journal-title":"J. Exp. Med."},{"key":"BFni2648_CR14","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1126\/science.1208421","volume":"334","author":"JA Harker","year":"2011","unstructured":"Harker, J.A., Lewis, G.M., Mack, L. & Zuniga, E.I. Late interleukin-6 escalates T follicular helper cell responses and controls a chronic viral infection. Science 334, 825\u2013829 (2011).","journal-title":"Science"},{"key":"BFni2648_CR15","doi-asserted-by":"publisher","first-page":"1719","DOI":"10.1084\/jem.167.5.1719","volume":"167","author":"R Ahmed","year":"1988","unstructured":"Ahmed, R. & Oldstone, M.B. Organ-specific selection of viral variants during chronic infection. J. Exp. Med. 167, 1719\u20131724 (1988).","journal-title":"J. Exp. Med."},{"key":"BFni2648_CR16","doi-asserted-by":"publisher","first-page":"1569","DOI":"10.1126\/science.1174182","volume":"324","author":"H Elsaesser","year":"2009","unstructured":"Elsaesser, H., Sauer, K. & Brooks, D.G. IL-21 is required to control chronic viral infection. Science 324, 1569\u20131572 (2009).","journal-title":"Science"},{"key":"BFni2648_CR17","doi-asserted-by":"publisher","first-page":"1576","DOI":"10.1126\/science.1172815","volume":"324","author":"A Fr\u00f6hlich","year":"2009","unstructured":"Fr\u00f6hlich, A. et al. IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 324, 1576\u20131580 (2009).","journal-title":"Science"},{"key":"BFni2648_CR18","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1084\/jem.20091738","volume":"207","author":"MA Linterman","year":"2010","unstructured":"Linterman, M.A. et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207, 353\u2013363 (2010).","journal-title":"J. Exp. Med."},{"key":"BFni2648_CR19","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1016\/j.immuni.2008.05.009","volume":"29","author":"RI Nurieva","year":"2008","unstructured":"Nurieva, R.I. et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29, 138\u2013149 (2008).","journal-title":"Immunity"},{"key":"BFni2648_CR20","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/j.immuni.2008.06.001","volume":"29","author":"A Vogelzang","year":"2008","unstructured":"Vogelzang, A. et al. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 29, 127\u2013137 (2008).","journal-title":"Immunity"},{"key":"BFni2648_CR21","doi-asserted-by":"publisher","first-page":"1572","DOI":"10.1126\/science.1175194","volume":"324","author":"JS Yi","year":"2009","unstructured":"Yi, J.S., Du, M. & Zajac, A.J. A vital role for interleukin-21 in the control of a chronic viral infection. Science 324, 1572\u20131576 (2009).","journal-title":"Science"},{"key":"BFni2648_CR22","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1084\/jem.20091777","volume":"207","author":"D Zotos","year":"2010","unstructured":"Zotos, D. et al. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 207, 365\u2013378 (2010).","journal-title":"J. Exp. Med."},{"key":"BFni2648_CR23","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":"BFni2648_CR24","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1038\/ni1575","volume":"9","author":"C Xiao","year":"2008","unstructured":"Xiao, C. et al. Lymphoproliferative disease and autoimmunity in mice with increased miR-17\u201392 expression in lymphocytes. Nat. Immunol. 9, 405\u2013414 (2008).","journal-title":"Nat. Immunol."},{"key":"BFni2648_CR25","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1084\/jem.20081886","volume":"206","author":"MA Linterman","year":"2009","unstructured":"Linterman, M.A. et al. Follicular helper T cells are required for systemic autoimmunity. J. Exp. Med. 206, 561\u2013576 (2009).","journal-title":"J. Exp. Med."},{"key":"BFni2648_CR26","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1002\/art.25032","volume":"62","author":"N Simpson","year":"2010","unstructured":"Simpson, N. et al. Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum. 62, 234\u2013244 (2010).","journal-title":"Arthritis Rheum."},{"key":"BFni2648_CR27","doi-asserted-by":"publisher","first-page":"452","DOI":"10.1038\/nature03555","volume":"435","author":"CG Vinuesa","year":"2005","unstructured":"Vinuesa, C.G. et al. A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 435, 452\u2013458 (2005).","journal-title":"Nature"},{"key":"BFni2648_CR28","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1046\/j.1440-1711.1998.00709.x","volume":"76","author":"MJ Barnden","year":"1998","unstructured":"Barnden, M.J., Allison, J., Heath, W.R. & Carbone, F.R. Defective TCR expression in transgenic mice constructed using cDNA-based \u03b1- and \u03b2-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76, 34\u201340 (1998).","journal-title":"Immunol. Cell Biol."},{"key":"BFni2648_CR29","doi-asserted-by":"publisher","first-page":"2089","DOI":"10.4049\/jimmunol.1101393","volume":"187","author":"D Baumjohann","year":"2011","unstructured":"Baumjohann, D., Okada, T. & Ansel, K.M. Cutting edge: distinct waves of BCL6 expression during T follicular helper cell development. J. Immunol. 187, 2089\u20132092 (2011).","journal-title":"J. Immunol."},{"key":"BFni2648_CR30","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1038\/nature12058","volume":"496","author":"H Xu","year":"2013","unstructured":"Xu, H. et al. Follicular T-helper cell recruitment governed by bystander B cells and ICOS-driven motility. Nature 496, 523\u2013527 (2013).","journal-title":"Nature"},{"key":"BFni2648_CR31","doi-asserted-by":"publisher","first-page":"20371","DOI":"10.1073\/pnas.0911573106","volume":"106","author":"M Gigoux","year":"2009","unstructured":"Gigoux, M. et al. Inducible costimulator promotes helper T-cell differentiation through phosphoinositide 3-kinase. Proc. Natl. Acad. Sci. USA 106, 20371\u201320376 (2009).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFni2648_CR32","doi-asserted-by":"publisher","first-page":"4042","DOI":"10.4049\/jimmunol.1001730","volume":"185","author":"J Rolf","year":"2010","unstructured":"Rolf, J. et al. Phosphoinositide 3-kinase activity in T cells regulates the magnitude of the germinal center reaction. J. Immunol. 185, 4042\u20134052 (2010).","journal-title":"J. Immunol."},{"key":"BFni2648_CR33","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1186\/1748-717X-5-100","volume":"5","author":"P Jiang","year":"2010","unstructured":"Jiang, P., Rao, E.Y., Meng, N., Zhao, Y. & Wang, J.J. MicroRNA-17\u201392 significantly enhances radioresistance in human mantle cell lymphoma cells. Radiat. Oncol. 5, 100 (2010).","journal-title":"Radiat. Oncol."},{"key":"BFni2648_CR34","doi-asserted-by":"publisher","first-page":"932","DOI":"10.1016\/j.immuni.2011.03.023","volume":"34","author":"YS Choi","year":"2011","unstructured":"Choi, Y.S. et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34, 932\u2013946 (2011).","journal-title":"Immunity"},{"key":"BFni2648_CR35","doi-asserted-by":"publisher","first-page":"5487","DOI":"10.1182\/blood-2011-05-355644","volume":"118","author":"S Jiang","year":"2011","unstructured":"Jiang, S. et al. Molecular dissection of the miR-17\u201392 cluster's critical dual roles in promoting Th1 responses and preventing inducible Treg differentiation. Blood 118, 5487\u20135497 (2011).","journal-title":"Blood"},{"key":"BFni2648_CR36","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1002\/gene.10036","volume":"32","author":"R Lesche","year":"2002","unstructured":"Lesche, R. et al. Cre\/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis 32, 148\u2013149 (2002).","journal-title":"Genesis"},{"key":"BFni2648_CR37","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1084\/jem.160.2.521","volume":"160","author":"R Ahmed","year":"1984","unstructured":"Ahmed, R., Salmi, A., Butler, L.D., Chiller, J.M. & Oldstone, M.B. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160, 521\u2013540 (1984).","journal-title":"J. Exp. Med."},{"key":"BFni2648_CR38","doi-asserted-by":"publisher","first-page":"1369","DOI":"10.1084\/jem.20072057","volume":"205","author":"A Suto","year":"2008","unstructured":"Suto, A. et al. Development and characterization of IL-21-producing CD4+ T cells. J. Exp. Med. 205, 1369\u20131379 (2008).","journal-title":"J. Exp. Med."},{"key":"BFni2648_CR39","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1016\/j.immuni.2011.07.015","volume":"35","author":"KT Lu","year":"2011","unstructured":"Lu, K.T. et al. Functional and epigenetic studies reveal multistep differentiation and plasticity of in vitro-generated and in vivo-derived follicular T helper cells. Immunity 35, 622\u2013632 (2011).","journal-title":"Immunity"}],"container-title":["Nature Immunology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/ni.2648.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/ni.2648","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/ni.2648.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,18]],"date-time":"2023-05-18T22:02:44Z","timestamp":1684447364000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/ni.2648"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,6,30]]},"references-count":39,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2013,8]]}},"alternative-id":["BFni2648"],"URL":"https:\/\/doi.org\/10.1038\/ni.2648","relation":{},"ISSN":["1529-2908","1529-2916"],"issn-type":[{"value":"1529-2908","type":"print"},{"value":"1529-2916","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,6,30]]}}}