T follicular helper cell biology: a decade of discovery and diseases

Spatiotemporal Dynamics of Intratumoral Immune Cells Reveal the Immune Landscape in Human Cancer

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Follicular Helper CD4 T Cells (T _FH )

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Rheumatoid arthritis

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Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy

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A Large-Scale, Consortium-Based Genomewide Association Study of Asthma

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Germinal Centers

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T follicular helper cell differentiation, function, and roles in disease

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Bcl6 and Blimp-1 Are Reciprocal and Antagonistic Regulators of T Follicular Helper Cell Differentiation

Johnston, R. J., Poholek, A. C., DiToro, D., Yusuf, I., Eto, D., Barnett, B., Dent, A. L., Craft, J., & Crotty, S. (2009) · Science · doi:10.1126/science.1175870 · Cited by 1,626 · see citing works

Human Blood CXCR5+CD4+ T Cells Are Counterparts of T Follicular Cells and Contain Specific Subsets that Differentially Support Antibody Secretion

Morita, R., Schmitt, N., Bentebibel, S.-E., Ranganathan, R., Bourdery, L., Zurawski, G., Foucat, E., Dullaers, M., Oh, S., Sabzghabaei, N., et al. (2011) · Immunity · doi:10.1016/j.immuni.2010.12.012 · Cited by 1,563 · see citing works

Bcl6 mediates the development of T follicular helper cells

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The Transcriptional Repressor Bcl-6 Directs T Follicular Helper Cell Lineage Commitment

Yu, D., Rao, S., Tsai, L. M., Lee, S. K., He, Y., Sutcliffe, E. L., Srivastava, M., Linterman, M. A., Zheng, L., Simpson, N., et al. (2009) · Immunity · doi:10.1016/j.immuni.2009.07.002 · Cited by 1,216 · see citing works

Follicular helper T cells

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Pathologically expanded peripheral T helper cell subset drives B cells in rheumatoid arthritis

Rao, D. A., Gurish, M. F., Marshall, J. L., Slowikowski, K., Fonseka, C. Y., Liu, Y., Donlin, L. T., Henderson, L. A., Wei, K., Mizoguchi, F., et al. (2017) · Nature · doi:10.1038/nature20810 · Cited by 1,125 · see citing works

Dysfunctional CD8 T cells form a proliferative, dynamically regulated compartment within human melanoma

Li, H., van der Leun, A. M., Yofe, I., Lubling, Y., Gelbard-Solodkin, D., van Akkooi, A. C. J., van den Braber, M., Rozeman, E. A., Haanen, J. B. A. G., Blank, C. U., et al. (2019) · Cell · doi:10.1016/j.cell.2018.11.043 · Cited by 1,101 · see citing works

CD4+ follicular helper T cell infiltration predicts breast cancer survival

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Programming the magnitude and persistence of antibody responses with innate immunity

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ICOS Receptor Instructs T Follicular Helper Cell versus Effector Cell Differentiation via Induction of the Transcriptional Repressor Bcl6

Choi, Y. S., Kageyama, R., Eto, D. S., Escobar, T. C., Johnston, R. J., Monticelli, L. A., Lao, C., & Crotty, S. (2011) · Immunity · doi:10.1016/j.immuni.2011.03.023 · Cited by 959 · see citing works

Human Circulating PD-1+CXCR3−CXCR5+ Memory Tfh Cells Are Highly Functional and Correlate with Broadly Neutralizing HIV Antibody Responses

Locci, M., Havenar‐Daughton, C., Landais, E., Wu, J. E., Kroenke, M. A., Arlehamn, C. S. L., Su, L. F., Cubas, R. A., Davis, M. M., Sette, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.031 · Cited by 859 · see citing works

Cytokine-secreting follicular T cells shape the antibody repertoire

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Ectopic lymphoid-like structures in infection, cancer and autoimmunity

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Follicular CXCR5-expressing CD8+ T cells curtail chronic viral infection

He, R., Hou, S., Liu, C., Zhang, A.-L., Bai, Q., Han, M., Yang, Y., Wei, G., Shen, T., Yang, X.-X., et al. (2016) · Nature · doi:10.1038/nature19317 · Cited by 643 · see citing works

Circulating Precursor CCR7loPD-1hi CXCR5+ CD4+ T Cells Indicate Tfh Cell Activity and Promote Antibody Responses upon Antigen Reexposure

He, J., Tsai, L. M., Leong, Y. A., Hu, X., Ma, C. S., Chevalier, N., Sun, X., Vandenberg, K. L., Rockman, S., Ding, Y. P., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.09.007 · Cited by 642 · see citing works

Induction of ICOS + CXCR3 + CXCR5 + T H Cells Correlates with Antibody Responses to Influenza Vaccination

Bentebibel, S.-E., Lopez, S. M. C., Obermoser, G., Schmitt, N., Mueller, C., Harrod, C., Flaño, E., Mejías, A., Albrecht, R. A., Blankenship, D., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005191 · Cited by 590 · see citing works

Immune and stromal classification of colorectal cancer is associated with molecular subtypes and relevant for precision immunotherapy

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Inflammation-induced IgA+ cells dismantle anti-liver cancer immunity

Shalapour, S., Lin, X.-J., Bastian, I. N., Brain, J., Burt, A. D., Aksenov, A. A., Vrbanac, A. F., Li, W., Perkins, A., Matsutani, T., et al. (2017) · Nature · doi:10.1038/nature24302 · Cited by 589 · see citing works

Follicular helper T cells are required for systemic autoimmunity

Linterman, M. A., Rigby, R. J., Wong, R. K., Yu, D., Brink, R. A., Cannons, J. L., Schwartzberg, P. L., Cook, M., Walters, G. D., & Vinuesa, C. G. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20081886 · Cited by 588 · see citing works

Clonal selection in the germinal centre by regulated proliferation and hypermutation

Gitlin, A. D., Shulman, Z., & Nussenzweig, M. C. (2014) · Nature · doi:10.1038/nature13300 · Cited by 577 · see citing works

Low-dose interleukin-2 treatment selectively modulates CD4+ T cell subsets in patients with systemic lupus erythematosus

He, J., Zhang, X., Wei, Y., Sun, X., Chen, Y., Deng, J., Jin, Y., Gan, Y., Hu, X., Jia, R., et al. (2016) · Nature Medicine · doi:10.1038/nm.4148 · Cited by 573 · see citing works

Innate and Adaptive Humoral Responses Coat Distinct Commensal Bacteria with Immunoglobulin A

Bunker, J. J., Flynn, T. M., Koval, J., Shaw, D. G., Meisel, M., McDonald, B. D., Ishizuka, I. E., Dent, A. L., Wilson, P. C., Jabrì, B., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.08.007 · Cited by 557 · see citing works

A brief history of T cell help to B cells

Crotty, S. (2015) · Nature reviews. Immunology · doi:10.1038/nri3803 · Cited by 552 · see citing works

Interleukin-2 Inhibits Germinal Center Formation by Limiting T Follicular Helper Cell Differentiation

Ballesteros‐Tato, A., León, B., Graf, B. A., Moquin, A., Adams, P. S., Lund, F. E., & Randall, T. D. (2012) · Immunity · doi:10.1016/j.immuni.2012.02.012 · Cited by 542 · see citing works

Ectopic Lymphoid Structures Support Ongoing Production of Class-Switched Autoantibodies in Rheumatoid Synovium

Humby, F., Bombardieri, M., Manzo, A., Kelly, S., Blades, M. C., Kirkham, B., Spencer, J., & Pitzalis, C. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.0060001 · Cited by 537 · see citing works

Cytokine-Mediated Regulation of Human B Cell Differentiation into Ig-Secreting Cells: Predominant Role of IL-21 Produced by CXCR5+ T Follicular Helper Cells

Bryant, V. L., Ma, C. S., Avery, D. T., Li, Y., Good‐Jacobson, K. L., Corcoran, L. M., Malefyt, R. D. W., & Tangye, S. G. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.12.8180 · Cited by 498 · see citing works

STAT5 is a potent negative regulator of TFH cell differentiation

Johnston, R. J., Choi, Y. S., Diamond, J. A., Kotov, J. A., & Crotty, S. (2012) · The Journal of Experimental Medicine · doi:10.1084/jem.20111174 · Cited by 486 · see citing works

Persistent Antigen and Germinal Center B Cells Sustain T Follicular Helper Cell Responses and Phenotype

Baumjohann, D., Preite, S., Reboldi, A., Ronchi, F., Ansel, K. M., Lanzavecchia, A., & Sallusto, F. (2013) · Immunity · doi:10.1016/j.immuni.2012.11.020 · Cited by 484 · see citing works

Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection

Butler, N. S., Moebius, J., Pewe, L. L., Traoré, B., Doumbo, O. K., Tygrett, L. T., Waldschmidt, T. J., Crompton, P. D., & Harty, J. T. (2011) · Nature Immunology · doi:10.1038/ni.2180 · Cited by 482 · see citing works

Autoreactivity in Human IgG+ Memory B Cells

Tiller, T., Tsuiji, M., Yurasov, S., Velinzon, K., Nussenzweig, M. C., & Wardemann, H. (2007) · Immunity · doi:10.1016/j.immuni.2007.01.009 · Cited by 477 · see citing works

BLC Expression in Pancreatic Islets Causes B Cell Recruitment and Lymphotoxin-Dependent Lymphoid Neogenesis

Luther, S. A., Lopez, T., Bai, W., Hanahan, D., & Cyster, J. G. (2000) · Immunity · doi:10.1016/s1074-7613(00)80199-5 · Cited by 468 · see citing works

PD-1+ and follicular helper T cells are responsible for persistent HIV-1 transcription in treated aviremic individuals

Banga, R., Procopio, F. A., Noto, A., Pollakis, G., Cavassini, M. L., Ohmiti, K., Corpataux, J.-M., de Leval, L., Pantaleo, G., & Perreau, M. (2016) · Nature Medicine · doi:10.1038/nm.4113 · Cited by 466 · see citing works

PD-1 Controls Follicular T Helper Cell Positioning and Function

Shi, J., Hou, S., Fang, Q., Liu, X., Liu, X., & Qi, H. (2018) · Immunity · doi:10.1016/j.immuni.2018.06.012 · Cited by 455 · see citing works

The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding

Fazilleau, N., McHeyzer‐Williams, L. J., Rosen, H., & McHeyzer‐Williams, M. G. (2009) · Nature Immunology · doi:10.1038/ni.1704 · Cited by 452 · see citing works

CXCR5+ follicular cytotoxic T cells control viral infection in B cell follicles

Leong, Y. A., Chen, Y., Hong, S. L., Wu, D., Man, K., Deleage, C., Minnich, M., Meckiff, B. J., Wei, Y.-B., Hou, Z.-H., et al. (2016) · Nature Immunology · doi:10.1038/ni.3543 · Cited by 449 · see citing works

Single Naive CD4+ T Cells from a Diverse Repertoire Produce Different Effector Cell Types during Infection

Tubo, N. J., Pagán, A. J., Taylor, J. J., Nelson, R. W., Linehan, J. L., Ertelt, J. M., Huseby, E. S., Way, S. S., & Jenkins, M. K. (2013) · Cell · doi:10.1016/j.cell.2013.04.007 · Cited by 444 · see citing works

The Coinhibitory Receptor CTLA-4 Controls B Cell Responses by Modulating T Follicular Helper, T Follicular Regulatory, and T Regulatory Cells

Sage, P. T., Paterson, A. M., Lovitch, S. B., & Sharpe, A. H. (2014) · Immunity · doi:10.1016/j.immuni.2014.12.005 · Cited by 437 · see citing works

Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity

Liang, H.-E., Reinhardt, R. L., Bando, J. K., Sullivan, B. M., Ho, I., & Locksley, R. M. (2011) · Nature Immunology · doi:10.1038/ni.2182 · Cited by 434 · see citing works

Unique Ectopic Lymph Node-Like Structures Present in Human Primary Colorectal Carcinoma Are Identified by Immune Gene Array Profiling

Coppola, D., Nebozhyn, M., Khalil, F., Dai, H., Yeatman, T., Loboda, A., & Mulé, J. J. (2011) · The American Journal of Pathology · doi:10.1016/j.ajpath.2011.03.007 · Cited by 434 · see citing works

Slow Delivery Immunization Enhances HIV Neutralizing Antibody and Germinal Center Responses via Modulation of Immunodominance

Cirelli, K. M., Carnathan, D. G., Nogal, B., Martin, J. T., Rodriguez, O. L., Upadhyay, A. A., Enemuo, C. A., Gebru, E. H., Choe, Y., Viviano, F., et al. (2019) · Cell · doi:10.1016/j.cell.2019.04.012 · Cited by 433 · see citing works

A dynamic T cell–limited checkpoint regulates affinity-dependent B cell entry into the germinal center

Schwickert, T. A., Victora, G. D., Fooksman, D., Kamphorst, A. O., Mugnier, M. R., Gitlin, A. D., Dustin, M. L., & Nussenzweig, M. C. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20102477 · Cited by 427 · see citing works

Sustained antigen availability during germinal center initiation enhances antibody responses to vaccination

Tam, H. H., Melo, M. B., Kang, M., Pelet, J. M., Ruda, V. M., Foley, M. H., Hu, J. K., Kumari, S., Crampton, J., Baldeon, A. D., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606050113 · Cited by 425 · see citing works

T–B-cell entanglement and ICOSL-driven feed-forward regulation of germinal centre reaction

Liu, D., Xu, H., Shih, C., Wan, Z., Ma, X., Ma, W., Luo, D., & Qi, H. (2014) · Nature · doi:10.1038/nature13803 · Cited by 423 · see citing works

Germinal Center T Follicular Helper Cell IL-4 Production Is Dependent on Signaling Lymphocytic Activation Molecule Receptor (CD150)

Yusuf, I., Kageyama, R., Monticelli, L. A., Johnston, R. J., Ditoro, D. F., Hansen, K., Barnett, B. E., & Crotty, S. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903505 · Cited by 421 · see citing works

TFH cells progressively differentiate to regulate the germinal center response

Weinstein, J. S., Herman, E. I., Lainez, B., Licona-Limón, P., Esplugues, E., Flavell, R. A., & Craft, J. E. (2016) · Nature Immunology · doi:10.1038/ni.3554 · Cited by 402 · see citing works

Regulated selection of germinal-center cells into the memory B cell compartment

Shinnakasu, R., Inoue, T., Kometani, K., Moriyama, S., Adachi, Y., Nakayama, M., Takahashi, Y., Fukuyama, H., Okada, T., & Kurosaki, T. (2016) · Nature Immunology · doi:10.1038/ni.3460 · Cited by 401 · see citing works

Follicular T-helper cell recruitment governed by bystander B cells and ICOS-driven motility

Xu, H., Li, X., Liu, D., Li, J., Zhang, X., Chen, X., Hou, S., Peng, L., Xu, C., Liu, W., et al. (2013) · Nature · doi:10.1038/nature12058 · Cited by 390 · see citing works

Regulatory T Cells Control Antigen-Specific Expansion of Tfh Cell Number and Humoral Immune Responses via the Coreceptor CTLA-4

Wing, J. B., Ise, W., Kurosaki, T., & Sakaguchi, S. (2014) · Immunity · doi:10.1016/j.immuni.2014.12.006 · Cited by 388 · see citing works

Dynamic signaling by T follicular helper cells during germinal center B cell selection

Shulman, Z., Gitlin, A. D., Weinstein, J. S., Lainez, B., Esplugues, E., Flavell, R. A., Craft, J. E., & Nussenzweig, M. C. (2014) · Science · doi:10.1126/science.1257861 · Cited by 387 · see citing works

CXCL13-producing TFH cells link immune suppression and adaptive memory in human breast cancer

Gu-Trantien, C., Migliori, E., Buisseret, L., de Wind, A., Brohée, S., Garaud, S., Noël, G., Dang Chi, V. L., Lodewyckx, J.-N., Naveaux, C., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.91487 · Cited by 368 · see citing works

The cytokine TGF-β co-opts signaling via STAT3-STAT4 to promote the differentiation of human TFH cells

Schmitt, N., Liu, Y., Bentebibel, S.-E., Munagala, I. D., Bourdery, L., Venuprasad, K., Banchereau, J., & Ueno, H. (2014) · Nature Immunology · doi:10.1038/ni.2947 · Cited by 363 · see citing works

T Follicular Helper Cell Dynamics in Germinal Centers

Shulman, Z., Gitlin, A. D., Targ, S., Janković, M., Pasqual, G., Nussenzweig, M. C., & Victora, G. D. (2013) · Science · doi:10.1126/science.1241680 · Cited by 363 · see citing works

In Situ B Cell-Mediated Immune Responses and Tubulointerstitial Inflammation in Human Lupus Nephritis

Chang, A., Henderson, S., Brandt, D. R., Liu, N., Guttikonda, R., Hsieh, C., Kaverina, N., Utset, T. O., Meehan, S. M., Quigg, R. J., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001983 · Cited by 361 · see citing works

Follicular Helper T Cell Differentiation Requires Continuous Antigen Presentation that Is Independent of Unique B Cell Signaling

Deenick, E. K., Chan, A., Ma, C. S., Gatto, D., Schwartzberg, P. L., Brink, R. A., & Tangye, S. G. (2010) · Immunity · doi:10.1016/j.immuni.2010.07.015 · Cited by 347 · see citing works

Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development

Liu, X., Chen, X., Zhong, B., Wang, A., Wang, X., Chu, F., Nurieva, R., Yan, X. S., Chen, P., van der Flier, L. G., et al. (2014) · Nature · doi:10.1038/nature12910 · Cited by 343 · see citing works

CXCL13 is a plasma biomarker of germinal center activity

Havenar‐Daughton, C., Lindqvist, M., Heit, A., Wu, J. E., Reiss, S. M., Kendric, K. J., Bélanger, S., Kasturi, S. P., Landais, E., Akondy, R. S., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520112113 · Cited by 343 · see citing works

Late Interleukin-6 escalates T follicular helper cell responses and controls a chronic viral infection

Harker, J., Lewis, G. M., Mack, L. A., & Zuniga, E. (2011) · Science · doi:10.1126/science.1208421 · Cited by 341 · see citing works

Precursor Frequency and Affinity Determine B Cell Competitive Fitness in Germinal Centers, Tested with Germline-Targeting HIV Vaccine Immunogens

Abbott, R. K., Lee, J. H., Menis, S., Skog, P. D., Rossi, M., Ota, T., Kulp, D. W., Bhullar, D., Kalyuzhniy, O., Havenar‐Daughton, C., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.11.023 · Cited by 340 · see citing works

IgA production requires B cell interaction with subepithelial dendritic cells in Peyer’s patches

Reboldi, A., Arnon, T. I., Rodda, L. B., Atakilit, A., Sheppard, D., & Cyster, J. G. (2016) · Science · doi:10.1126/science.aaf4822 · Cited by 339 · see citing works

LEF-1 and TCF-1 orchestrate TFH differentiation by regulating differentiation circuits upstream of the transcriptional repressor Bcl6

Choi, Y. S., Gullicksrud, J. A., Xing, S., Zeng, Z., Shan, Q., Li, F., Love, P. E., Peng, W., Xue, H., & Crotty, S. (2015) · Nature Immunology · doi:10.1038/ni.3226 · Cited by 329 · see citing works

MyD88 Signaling in T Cells Directs IgA-Mediated Control of the Microbiota to Promote Health

Kubinak, J. L., Petersen, C., Stephens, W. Z., Soto, R., Bake, E., O’Connell, R. M., & Round, J. L. (2015) · Cell Host & Microbe · doi:10.1016/j.chom.2014.12.009 · Cited by 328 · see citing works

T follicular regulatory cells

Sage, P. T., & Sharpe, A. H. (2016) · Immunological Reviews · doi:10.1111/imr.12411 · Cited by 327 · see citing works

T Follicular Helper Cell-Germinal Center B Cell Interaction Strength Regulates Entry into Plasma Cell or Recycling Germinal Center Cell Fate

Ise, W., Fujii, K., Shiroguchi, K., Ito, A., Kometani, K., Takeda, K., Kawakami, E., Yamashita, K., Suzuki, K., Okada, T., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.03.027 · Cited by 324 · see citing works

Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand T fh cells and promote germinal center induction

Moon, J. J., Suh, H., Li, A. V., Ockenhouse, C. F., Yadava, A., & Irvine, D. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112648109 · Cited by 320 · see citing works

Immune homeostasis enforced by co-localized effector and regulatory T cells

Liu, Z., Gerner, M. Y., van Panhuys, N., Levine, A. G., Rudensky, A. Y., & Germain, R. N. (2015) · Nature · doi:10.1038/nature16169 · Cited by 318 · see citing works

The Interleukin-2-mTORc1 Kinase Axis Defines the Signaling, Differentiation, and Metabolism of T Helper 1 and Follicular B Helper T Cells

Ray, J. P., Staron, M. M., Shyer, J. A., Ho, P.-C., Marshall, H. D., Gray, S. M., Laidlaw, B. J., Araki, K., Ahmed, R., Kaech, S. M., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.08.017 · Cited by 315 · see citing works

B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells

Lee, S. K., Rigby, R. J., Zotos, D., Tsai, L. M., Kawamoto, S., Marshall, J. L., Ramiscal, R. R., Chan, T. D., Gatto, D., Brink, R. A., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20102065 · Cited by 312 · see citing works

Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers

Wang, X., Cho, B. K., Suzuki, K., Xu, Y., Green, J. A., An, J., & Cyster, J. G. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20111449 · Cited by 302 · see citing works

Germinal Center Selection and Affinity Maturation Require Dynamic Regulation of mTORC1 Kinase

Ersching, J., Efeyan, A., Mesin, L., Jacobsen, J. T., Pasqual, G., Grabiner, B. C., Dominguez-Sola, D., Sabatini, D. M., & Victora, G. D. (2017) · Immunity · doi:10.1016/j.immuni.2017.06.005 · Cited by 302 · see citing works

Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses

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B Cells Are the Dominant Antigen-Presenting Cells that Activate Naive CD4+ T Cells upon Immunization with a Virus-Derived Nanoparticle Antigen

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マウスおよびヒトはい中心におけるCCR6は記憶B細胞前駆体,光帯を明らかにする位置と主要な低抗原親和性【Powered by NICT】

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