{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T00:19:49Z","timestamp":1791332389196,"version":"4.3.1"},"reference-count":60,"publisher":"Oxford University Press (OUP)","issue":"12","license":[{"start":{"date-parts":[[2013,6,1]],"date-time":"2013-06-01T00:00:00Z","timestamp":1370044800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2013,6,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>The microenvironment of human follicular lymphoma (FL), an incurable B cell non-Hodgkin\u2019s lymphoma, is thought to play a major role in its pathogenesis and course. Microenvironmental cells of likely importance include follicular Th cells (TFH) and regulatory T cells (Tregs), and understanding their interactions with FL tumor cells is necessary to develop novel therapeutic strategies. We found that IL-4 and CD40L are expressed by intratumoral TFH and induce production of CCL17 and CCL22 by FL tumor cells. IL-4 alone induces only CCL17 but enhances stimulation by CD40L of both CCL17 and CCL22. Consistent with our in vitro results, mRNA transcripts of IL-4 correlated with CCL17, but not CCL22, in gene expression profiling studies of FL biopsies, whereas CD40L correlated with both CCL17 and CCL22. Tumor supernatants induced preferential migration of Tregs and IL-4\u2013producing T cells rather than IFN-\u03b3\u2013producing T cells, and Abs to CCR4 significantly abrogated the migration of Tregs. Our results suggest that through two distinct mechanisms, intratumoral TFH induce production of CCL17 and CCL22 by FL tumor cells and facilitate active recruitment of Tregs and IL-4\u2013producing T cells, which, in turn, may stimulate more chemokine production in a feed-forward cycle. Thus, TFH appear to play a major role in generating an immunosuppressive tumor microenvironment that promotes immune escape and tumor survival and growth. Our results provide novel insights into the cross talk among TFH, tumor cells, and Tregs in FL, and offer potential targets for development of therapeutic strategies to overcome immune evasion.<\/jats:p>","DOI":"10.4049\/jimmunol.1201363","type":"journal-article","created":{"date-parts":[[2013,5,18]],"date-time":"2013-05-18T04:37:56Z","timestamp":1368851876000},"page":"6681-6693","source":"Crossref","is-referenced-by-count":106,"title":["Cross Talk between Follicular Th Cells and Tumor Cells in Human Follicular Lymphoma Promotes Immune Evasion in the Tumor Microenvironment"],"prefix":"10.1093","volume":"190","author":[{"given":"Seema","family":"Rawal","sequence":"first","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fuliang","family":"Chu","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Min","family":"Zhang","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hyun Jun","family":"Park","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"The University of Texas Graduate School of Biomedical Sciences , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Durga","family":"Nattamai","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shibichakravarthy","family":"Kannan","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rakesh","family":"Sharma","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Delgado","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tina","family":"Chou","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heather Y","family":"Lin","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Veerabhadran","family":"Baladandayuthapani","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amber","family":"Luong","sequence":"additional","affiliation":[{"name":"Department of Otorhinolaryngology\u2013Head and Neck Surgery, The University of Texas Medical School at Houston , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francisco","family":"Vega","sequence":"additional","affiliation":[{"name":"Department of Hematopathology, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nathan","family":"Fowler","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chen","family":"Dong","sequence":"additional","affiliation":[{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"The University of Texas Graduate School of Biomedical Sciences , Houston, TX 77030"},{"name":"Department of Immunology, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R Eric","family":"Davis","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"The University of Texas Graduate School of Biomedical Sciences , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sattva S","family":"Neelapu","sequence":"additional","affiliation":[{"name":"Division of Cancer Medicine, Department of Lymphoma and Myeloma, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"Center for Cancer Immunology Research, The University of Texas MD Anderson Cancer Center , Houston, TX 77030"},{"name":"The University of Texas Graduate School of Biomedical Sciences , Houston, TX 77030"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2013,6,15]]},"reference":[{"key":"2025032407070625100_r1","first-page":"3909","article-title":"A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin\u2019s lymphoma. The Non-Hodgkin\u2019s Lymphoma Classification Project","volume-title":"Blood","year":"1997"},{"key":"2025032407070625100_r2","doi-asserted-by":"crossref","first-page":"1440","DOI":"10.1126\/science.3874430","article-title":"Involvement of the bcl-2 gene in human follicular lymphoma","volume":"228","author":"Tsujimoto","year":"1985","journal-title":"Science"},{"key":"2025032407070625100_r3","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1093\/jncimonographs\/lgn005","article-title":"Age-dependent prevalence and frequency of circulating t(14;18)-positive cells in the peripheral blood of healthy individuals","volume":"2008","author":"D\u00f6lken","year":"2008","journal-title":"J. Natl. Cancer Inst. Monogr."},{"key":"2025032407070625100_r4","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1200\/JCO.1996.14.4.1333","article-title":"BCL-2\/JH rearrangements in circulating B cells of healthy blood donors and patients with nonmalignant diseases","volume":"14","author":"D\u00f6lken","year":"1996","journal-title":"J. Clin. Oncol."},{"key":"2025032407070625100_r5","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1038\/349254a0","article-title":"Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18)","volume":"349","author":"McDonnell","year":"1991","journal-title":"Nature"},{"key":"2025032407070625100_r6","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1038\/nrc1589","article-title":"Mechanisms of B-cell lymphoma pathogenesis","volume":"5","author":"K\u00fcppers","year":"2005","journal-title":"Nat. Rev. Cancer"},{"key":"2025032407070625100_r7","doi-asserted-by":"crossref","first-page":"3818","DOI":"10.1182\/blood-2008-02-138933","article-title":"IL-4 protein expression and basal activation of Erk in vivo in follicular lymphoma","volume":"112","author":"Calvo","year":"2008","journal-title":"Blood"},{"key":"2025032407070625100_r8","doi-asserted-by":"crossref","first-page":"2080","DOI":"10.1038\/leu.2010.223","article-title":"Follicular lymphoma cell niche: identification of a preeminent IL-4-dependent T(FH)-B cell axis","volume":"24","author":"Pangault","year":"2010","journal-title":"Leukemia"},{"key":"2025032407070625100_r9","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1038\/leu.2011.301","article-title":"Characterization of intratumoral follicular helper T cells in follicular lymphoma: role in the survival of malignant B cells","volume":"26","author":"Am\u00e9-Thomas","year":"2012","journal-title":"Leukemia"},{"key":"2025032407070625100_r10","doi-asserted-by":"crossref","first-page":"1862","DOI":"10.1038\/sj.leu.2400822","article-title":"In vitro activation of low-grade non-Hodgkin\u2019s lymphoma by murine fibroblasts, IL-4, anti-CD40 antibodies and the soluble CD40 ligand","volume":"11","author":"Buske","year":"1997","journal-title":"Leukemia"},{"key":"2025032407070625100_r11","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1002\/(SICI)1099-1069(199711)15:4<197::AID-HON614>3.0.CO;2-V","article-title":"T-cell derived cytokines co-stimulate proliferation of CD40-activated germinal centre as well as follicular lymphoma cells","volume":"15","author":"Schmitter","year":"1997","journal-title":"Hematol. Oncol."},{"key":"2025032407070625100_r12","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1056\/NEJM198412063112303","article-title":"The natural history of initially untreated low-grade non-Hodgkin\u2019s lymphomas","volume":"311","author":"Horning","year":"1984","journal-title":"N. Engl. J. Med."},{"key":"2025032407070625100_r13","doi-asserted-by":"crossref","first-page":"3806","DOI":"10.1182\/blood.V89.10.3806","article-title":"Autologous tumor infiltrating T cells cytotoxic for follicular lymphoma cells can be expanded in vitro","volume":"89","author":"Schultze","year":"1997","journal-title":"Blood"},{"key":"2025032407070625100_r14","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.jim.2007.09.006","article-title":"A novel strategy for rapid and efficient isolation of human tumor-specific CD4(+) and CD8(+) T-cell clones","volume":"331","author":"Lee","year":"2008","journal-title":"J. Immunol. Methods"},{"key":"2025032407070625100_r15","doi-asserted-by":"crossref","first-page":"2159","DOI":"10.1056\/NEJMoa041869","article-title":"Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells","volume":"351","author":"Dave","year":"2004","journal-title":"N. Engl. J. Med."},{"key":"2025032407070625100_r16","doi-asserted-by":"crossref","first-page":"1171","DOI":"10.1038\/13928","article-title":"Complete molecular remissions induced by patient-specific vaccination plus granulocyte-monocyte colony-stimulating factor against lymphoma","volume":"5","author":"Bendandi","year":"1999","journal-title":"Nat. Med."},{"key":"2025032407070625100_r17","doi-asserted-by":"crossref","first-page":"8309","DOI":"10.1158\/1078-0432.CCR-04-1071","article-title":"Human autologous tumor-specific T-cell responses induced by liposomal delivery of a lymphoma antigen","volume":"10","author":"Neelapu","year":"2004","journal-title":"Clin. Cancer Res."},{"key":"2025032407070625100_r18","doi-asserted-by":"crossref","first-page":"2825","DOI":"10.1200\/JCO.1998.16.8.2825","article-title":"Rituximab chimeric anti-CD20 monoclonal antibody therapy for relapsed indolent lymphoma: half of patients respond to a four-dose treatment program","volume":"16","author":"McLaughlin","year":"1998","journal-title":"J. Clin. Oncol."},{"key":"2025032407070625100_r19","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1200\/JCO.2005.12.052","article-title":"Rituximab therapy for patients with newly diagnosed, advanced-stage, follicular grade I non-Hodgkin\u2019s lymphoma: a phase II trial in the North Central Cancer Treatment Group","volume":"23","author":"Witzig","year":"2005","journal-title":"J. Clin. Oncol."},{"key":"2025032407070625100_r20","doi-asserted-by":"crossref","first-page":"5530","DOI":"10.1182\/blood-2008-01-136242","article-title":"Eight-year experience with allogeneic stem cell transplantation for relapsed follicular lymphoma after nonmyeloablative conditioning with fludarabine, cyclophosphamide, and rituximab","volume":"111","author":"Khouri","year":"2008","journal-title":"Blood"},{"key":"2025032407070625100_r21","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1038\/nrc1586","article-title":"Immunosuppressive networks in the tumour environment and their therapeutic relevance","volume":"5","author":"Zou","year":"2005","journal-title":"Nat. Rev. Cancer"},{"key":"2025032407070625100_r22","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1038\/nri1806","article-title":"Regulatory T cells, tumour immunity and immunotherapy","volume":"6","author":"Zou","year":"2006","journal-title":"Nat. Rev. Immunol."},{"key":"2025032407070625100_r23","doi-asserted-by":"crossref","first-page":"3639","DOI":"10.1182\/blood-2005-08-3376","article-title":"Intratumoral CD4+CD25+ regulatory T-cell-mediated suppression of infiltrating CD4+ T cells in B-cell non-Hodgkin lymphoma","volume":"107","author":"Yang","year":"2006","journal-title":"Blood"},{"key":"2025032407070625100_r24","doi-asserted-by":"crossref","first-page":"2957","DOI":"10.1182\/blood-2006-04-018218","article-title":"High numbers of tumor-infiltrating FOXP3-positive regulatory T cells are associated with improved overall survival in follicular lymphoma","volume":"108","author":"Carreras","year":"2006","journal-title":"Blood"},{"key":"2025032407070625100_r25","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1182\/blood-2009-07-235598","article-title":"The architectural pattern of FOXP3-positive T cells in follicular lymphoma is an independent predictor of survival and histologic transformation","volume":"115","author":"Farinha","year":"2010","journal-title":"Blood"},{"key":"2025032407070625100_r26","doi-asserted-by":"crossref","first-page":"5359","DOI":"10.1182\/blood-2007-08-105395","article-title":"Local and systemic induction of CD4+CD25+ regulatory T-cell population by non-Hodgkin lymphoma","volume":"111","author":"Mittal","year":"2008","journal-title":"Blood"},{"key":"2025032407070625100_r27","doi-asserted-by":"crossref","first-page":"10145","DOI":"10.1158\/0008-5472.CAN-06-1822","article-title":"Attenuation of CD8(+) T-cell function by CD4(+)CD25(+) regulatory T cells in B-cell non-Hodgkin\u2019s lymphoma","volume":"66","author":"Yang","year":"2006","journal-title":"Cancer Res."},{"key":"2025032407070625100_r28","doi-asserted-by":"crossref","first-page":"4051","DOI":"10.4049\/jimmunol.178.7.4051","article-title":"Follicular lymphoma intratumoral CD4+CD25+GITR+ regulatory T cells potently suppress CD3\/CD28-costimulated autologous and allogeneic CD8+CD25- and CD4+CD25- T cells","volume":"178","author":"Hilchey","year":"2007","journal-title":"J. Immunol."},{"key":"2025032407070625100_r29","doi-asserted-by":"crossref","first-page":"2537","DOI":"10.1182\/blood-2007-03-082578","article-title":"CD70+ non-Hodgkin lymphoma B cells induce Foxp3 expression and regulatory function in intratumoral CD4+CD25 T cells","volume":"110","author":"Yang","year":"2007","journal-title":"Blood"},{"key":"2025032407070625100_r30","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1002\/ijc.23881","article-title":"Follicular lymphoma B cells induce the conversion of conventional CD4+ T cells to T-regulatory cells","volume":"124","author":"Ai","year":"2009","journal-title":"Int. J. Cancer"},{"key":"2025032407070625100_r31","doi-asserted-by":"crossref","first-page":"2760","DOI":"10.1002\/(SICI)1521-4141(199809)28:09<2760::AID-IMMU2760>3.0.CO;2-N","article-title":"Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation","volume":"28","author":"Sallusto","year":"1998","journal-title":"Eur. J. Immunol."},{"key":"2025032407070625100_r32","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.jdermsci.2006.06.002","article-title":"Thymus and activation regulated chemokine (TARC)\/CCL17 and skin diseases","volume":"43","author":"Saeki","year":"2006","journal-title":"J. Dermatol. Sci."},{"key":"2025032407070625100_r33","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1189\/jlb.68.3.400","article-title":"Macrophage-derived chemokine (MDC)","volume":"68","author":"Mantovani","year":"2000","journal-title":"J. Leukoc. Biol."},{"key":"2025032407070625100_r34","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1172\/JCI200316624","article-title":"Identification of Hodgkin and Reed-Sternberg cell-specific genes by gene expression profiling","volume":"111","author":"K\u00fcppers","year":"2003","journal-title":"J. Clin. Invest."},{"key":"2025032407070625100_r35","doi-asserted-by":"crossref","first-page":"2787","DOI":"10.1200\/JCO.2010.33.3005","article-title":"Vaccination with patient-specific tumor-derived antigen in first remission improves disease-free survival in follicular lymphoma","volume":"29","author":"Schuster","year":"2011","journal-title":"J. Clin. Oncol."},{"key":"2025032407070625100_r36","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.1158\/0008-5472.CAN-10-2907","article-title":"Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer","volume":"71","author":"Tosolini","year":"2011","journal-title":"Cancer Res."},{"key":"2025032407070625100_r37","doi-asserted-by":"crossref","first-page":"R14","DOI":"10.1007\/BF01470994","article-title":"Detection of keyhole limpet hemocyanin (KLH)-specific immune responses by intracellular cytokine assay in patients vaccinated with idiotype-KLH vaccine","volume":"127","author":"Neelapu","year":"2001","journal-title":"J. Cancer Res. Clin. Oncol."},{"key":"2025032407070625100_r38","doi-asserted-by":"crossref","first-page":"1424","DOI":"10.1182\/blood-2008-01-133769","article-title":"Vorinostat inhibits STAT6-mediated TH2 cytokine and TARC production and induces cell death in Hodgkin lymphoma cell lines","volume":"112","author":"Buglio","year":"2008","journal-title":"Blood"},{"key":"2025032407070625100_r39","doi-asserted-by":"crossref","first-page":"1258","DOI":"10.1182\/blood-2003-12-4434","article-title":"Follicular lymphoma international prognostic index","volume":"104","author":"Solal-C\u00e9ligny","year":"2004","journal-title":"Blood"},{"key":"2025032407070625100_r40","first-page":"51","article-title":"Manipulation of signaling to control allergic inflammation","volume":"7","author":"Colgan","year":"2007","journal-title":"Curr. Opin. Allergy Clin. Immunol."},{"key":"2025032407070625100_r41","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.cytogfr.2006.01.004","article-title":"Signaling mechanisms, interaction partners, and target genes of STAT6","volume":"17","author":"Hebenstreit","year":"2006","journal-title":"Cytokine Growth Factor Rev."},{"key":"2025032407070625100_r42","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1186\/1471-2199-7-45","article-title":"Interleukin-4 induction of the CC chemokine TARC (CCL17) in murine macrophages is mediated by multiple STAT6 sites in the TARC gene promoter","volume":"7","author":"Liddiard","year":"2006","journal-title":"BMC Mol. Biol."},{"key":"2025032407070625100_r43","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1182\/blood.V98.3.533","article-title":"Chemoattractants MDC and TARC are secreted by malignant B-cell precursors following CD40 ligation and support the migration of leukemia-specific T cells","volume":"98","author":"Ghia","year":"2001","journal-title":"Blood"},{"key":"2025032407070625100_r44","first-page":"27","article-title":"TARC and MDC are produced by CD40 activated human B cells and are elevated in the sera of infantile atopic dermatitis patients","volume":"50","author":"Lin","year":"2003","journal-title":"J. Med. Dent. Sci."},{"key":"2025032407070625100_r45","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.jim.2007.07.012","article-title":"Loss of T cell responses following long-term cryopreservation","volume":"326","author":"Owen","year":"2007","journal-title":"J. Immunol. Methods"},{"key":"2025032407070625100_r46","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1084\/jem.194.6.847","article-title":"Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells","volume":"194","author":"Iellem","year":"2001","journal-title":"J. Exp. Med."},{"key":"2025032407070625100_r47","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1084\/jem.187.1.129","article-title":"Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s","volume":"187","author":"Bonecchi","year":"1998","journal-title":"J. Exp. Med."},{"key":"2025032407070625100_r48","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1038\/ni.1715","article-title":"Cytokine-secreting follicular T cells shape the antibody repertoire","volume":"10","author":"Reinhardt","year":"2009","journal-title":"Nat. Immunol."},{"key":"2025032407070625100_r49","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.it.2010.07.001","article-title":"The elusive identity of T follicular helper cells","volume":"31","author":"Yu","year":"2010","journal-title":"Trends Immunol."},{"key":"2025032407070625100_r50","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.immuni.2010.12.012","article-title":"Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion","volume":"34","author":"Morita","year":"2011","journal-title":"Immunity"},{"key":"2025032407070625100_r51","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1182\/blood-2006-06-028985","article-title":"Expansion of Vdelta1 T lymphocytes producing IL-4 in low-grade non-Hodgkin lymphomas expressing UL-16-binding proteins","volume":"109","author":"Catellani","year":"2007","journal-title":"Blood"},{"key":"2025032407070625100_r52","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.1080\/10428190290026259","article-title":"The role of interleukin 13 in classical Hodgkin lymphoma","volume":"43","author":"Skinnider","year":"2002","journal-title":"Leuk. Lymphoma"},{"key":"2025032407070625100_r53","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1111\/j.1349-7006.2006.00307.x","article-title":"CCR4 as a novel molecular target for immunotherapy of cancer","volume":"97","author":"Ishida","year":"2006","journal-title":"Cancer Sci."},{"key":"2025032407070625100_r54","doi-asserted-by":"crossref","first-page":"10221","DOI":"10.1073\/pnas.0803453105","article-title":"In silico identified CCR4 antagonists target regulatory T cells and exert adjuvant activity in vaccination","volume":"105","author":"Bayry","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025032407070625100_r55","doi-asserted-by":"crossref","first-page":"5350","DOI":"10.1200\/JCO.2006.06.4766","article-title":"Immunohistochemical patterns of reactive microenvironment are associated with clinicobiologic behavior in follicular lymphoma patients","volume":"24","author":"Alvaro","year":"2006","journal-title":"J. Clin. Oncol."},{"key":"2025032407070625100_r56","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1038\/ni.1731","article-title":"The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation","volume":"10","author":"Koch","year":"2009","journal-title":"Nat. Immunol."},{"key":"2025032407070625100_r57","doi-asserted-by":"crossref","first-page":"986","DOI":"10.1126\/science.1172702","article-title":"CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner","volume":"326","author":"Chaudhry","year":"2009","journal-title":"Science"},{"key":"2025032407070625100_r58","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1038\/nature07674","article-title":"Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses","volume":"458","author":"Zheng","year":"2009","journal-title":"Nature"},{"key":"2025032407070625100_r59","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1038\/nm.2426","article-title":"Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions","volume":"17","author":"Chung","year":"2011","journal-title":"Nat. Med."},{"key":"2025032407070625100_r60","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1038\/nm.2425","article-title":"Foxp3+ follicular regulatory T cells control the germinal center response","volume":"17","author":"Linterman","year":"2011","journal-title":"Nat. Med."}],"container-title":["The Journal of Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/190\/12\/6681\/61763607\/1201363.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/190\/12\/6681\/61763607\/1201363.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,26]],"date-time":"2025-03-26T11:19:23Z","timestamp":1742987963000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jimmunol\/article\/190\/12\/6681\/8001895"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,6]]},"references-count":60,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2013,6,15]]}},"URL":"https:\/\/doi.org\/10.4049\/jimmunol.1201363","relation":{},"ISSN":["0022-1767","1550-6606"],"issn-type":[{"value":"0022-1767","type":"print"},{"value":"1550-6606","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2013,6]]},"published":{"date-parts":[[2013,6]]}}}