Human Extrafollicular CD4+ Th Cells Help Memory B Cells Produce Igs

Follicular helper T (Tfh) cells are necessary for germinal center B cell maturation during primary immune responses; however, the T cells that promote humoral recall responses via memory B cells are less well defined. In this article, we characterize a human tonsillar CD4+ T cell subset with this fu...

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Published inThe Journal of immunology (1950) Vol. 201; no. 5; pp. 1359 - 1372
Main Authors Kim, Sang Taek, Choi, Jin-Young, Lainez, Begona, Schulz, Vincent P, Karas, David E, Baum, Eric D, Setlur, Jennifer, Gallagher, Patrick G, Craft, Joe
Format Journal Article
LanguageEnglish
Published United States 01.09.2018
Subjects
Adolescent
Antibody Formation
B-Lymphocytes - cytology
B-Lymphocytes - immunology
Child
Child, Preschool
Cytokines - immunology
Female
Gene Expression Regulation - immunology
Humans
Immunoglobulin G - immunology
Immunologic Memory
Male
Programmed Cell Death 1 Receptor - immunology
Proto-Oncogene Proteins c-bcl-6 - immunology
Receptors, CXCR5 - immunology
T-Lymphocytes, Helper-Inducer - cytology
T-Lymphocytes, Helper-Inducer - immunology
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Abstract Follicular helper T (Tfh) cells are necessary for germinal center B cell maturation during primary immune responses; however, the T cells that promote humoral recall responses via memory B cells are less well defined. In this article, we characterize a human tonsillar CD4+ T cell subset with this function. These cells are similar to Tfh cells in terms of expression of the chemokine receptor CXCR5 and the inhibitory receptor PD-1, IL-21 secretion, and expression of the transcription factor BCL6; however, unlike Tfh cells that are located within the B cell follicle and germinal center, they reside at the border of the T cell zone and the B cell follicle in proximity to memory B cells, a position dictated by their unique chemokine receptor expression. They promote memory B cells to produce Abs via CD40L, IL-10, and IL-21. Our results reveal a unique extrafollicular CD4+ T cell subset in human tonsils, which specialize in promoting T cell–dependent humoral recall responses.
AbstractList Follicular helper T (Tfh) cells are necessary for germinal center B cell maturation during primary immune responses; however, the T cells that promote humoral recall responses via memory B cells are less well defined. In this article, we characterize a human tonsillar CD4+ T cell subset with this function. These cells are similar to Tfh cells in terms of expression of the chemokine receptor CXCR5 and the inhibitory receptor PD-1, IL-21 secretion, and expression of the transcription factor BCL6; however, unlike Tfh cells that are located within the B cell follicle and germinal center, they reside at the border of the T cell zone and the B cell follicle in proximity to memory B cells, a position dictated by their unique chemokine receptor expression. They promote memory B cells to produce Abs via CD40L, IL-10, and IL-21. Our results reveal a unique extrafollicular CD4+ T cell subset in human tonsils, which specialize in promoting T cell–dependent humoral recall responses.
Follicular helper T (Tfh) cells are necessary for germinal center B cell maturation during primary immune responses; however, the T cells that promote humoral recall responses via memory B cells are less well defined. In this article, we characterize a human tonsillar CD4+ T cell subset with this function. These cells are similar to Tfh cells in terms of expression of the chemokine receptor CXCR5 and the inhibitory receptor PD-1, IL-21 secretion, and expression of the transcription factor BCL6; however, unlike Tfh cells that are located within the B cell follicle and germinal center, they reside at the border of the T cell zone and the B cell follicle in proximity to memory B cells, a position dictated by their unique chemokine receptor expression. They promote memory B cells to produce Abs via CD40L, IL-10, and IL-21. Our results reveal a unique extrafollicular CD4+ T cell subset in human tonsils, which specialize in promoting T cell-dependent humoral recall responses.Follicular helper T (Tfh) cells are necessary for germinal center B cell maturation during primary immune responses; however, the T cells that promote humoral recall responses via memory B cells are less well defined. In this article, we characterize a human tonsillar CD4+ T cell subset with this function. These cells are similar to Tfh cells in terms of expression of the chemokine receptor CXCR5 and the inhibitory receptor PD-1, IL-21 secretion, and expression of the transcription factor BCL6; however, unlike Tfh cells that are located within the B cell follicle and germinal center, they reside at the border of the T cell zone and the B cell follicle in proximity to memory B cells, a position dictated by their unique chemokine receptor expression. They promote memory B cells to produce Abs via CD40L, IL-10, and IL-21. Our results reveal a unique extrafollicular CD4+ T cell subset in human tonsils, which specialize in promoting T cell-dependent humoral recall responses.
Follicular helper T (Tfh) cells are necessary for germinal center B cell maturation during primary immune responses; however, the T cells that promote humoral recall responses via memory B cells are less well defined. In this article, we characterize a human tonsillar CD4 T cell subset with this function. These cells are similar to Tfh cells in terms of expression of the chemokine receptor CXCR5 and the inhibitory receptor PD-1, IL-21 secretion, and expression of the transcription factor BCL6; however, unlike Tfh cells that are located within the B cell follicle and germinal center, they reside at the border of the T cell zone and the B cell follicle in proximity to memory B cells, a position dictated by their unique chemokine receptor expression. They promote memory B cells to produce Abs via CD40L, IL-10, and IL-21. Our results reveal a unique extrafollicular CD4 T cell subset in human tonsils, which specialize in promoting T cell-dependent humoral recall responses.
Author Karas, David E
Lainez, Begona
Craft, Joe
Choi, Jin-Young
Schulz, Vincent P
Setlur, Jennifer
Kim, Sang Taek
Gallagher, Patrick G
Baum, Eric D
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Cites_doi 10.1002/eji.200636136
10.1182/blood-2003-09-3109
10.1038/ni.3494
10.1111/j.1365-2567.2005.02242.x
10.1056/NEJMoa066092
10.4049/jimmunol.0904023
10.1126/science.1079490
10.1084/jem.192.11.1545
10.1016/j.immuni.2013.09.007
10.1126/scitranslmed.3005191
10.1146/annurev.immunol.23.021704.115732
10.1016/j.it.2014.06.002
10.1016/j.immuni.2007.07.009
10.1038/nature12910
10.4049/jimmunol.1002828
10.1038/nature06890
10.4049/jimmunol.178.2.817
10.1038/ni.1715
10.1016/j.immuni.2010.12.012
10.4049/jimmunol.171.10.4969
10.1038/40540
10.1016/S1074-7613(00)80541-5
10.1016/j.immuni.2011.03.023
10.1016/j.immuni.2013.02.020
10.1038/44385
10.1038/icb.2009.64
10.1038/ni.1814
10.1038/nrrheum.2012.58
10.1016/j.immuni.2011.09.009
10.1084/jem.20080840
10.1002/(SICI)1521-4141(199802)28:02<508::AID-IMMU508>3.0.CO;2-I
10.1182/blood-2002-11-3569
10.1016/S0002-9440(10)63152-5
10.1158/2326-6066.CIR-14-0040
10.1086/424571
10.4049/jimmunol.179.12.8180
10.1016/j.immuni.2013.08.031
10.4049/jimmunol.1103246
10.1126/science.1176676
10.4049/jimmunol.178.5.2872
10.4049/jimmunol.179.8.5099
10.1126/science.1076071
10.1182/blood-2014-07-585976
10.1002/eji.200939531
10.4049/jimmunol.182.2.890
10.1038/ni.1877
10.1146/annurev.immunol.23.021704.115628
10.1002/eji.200839129
10.1073/pnas.1404671111
10.1084/jem.187.6.885
10.1073/pnas.1100898108
10.1111/j.1600-065X.2012.01124.x
10.1016/j.cell.2013.04.007
10.1189/jlb.0409268
10.4049/jimmunol.1001155
10.4049/jimmunol.159.5.2085
10.1016/j.immuni.2011.03.024
10.1016/j.immuni.2009.04.016
10.4049/jimmunol.180.1.361
10.1038/ni1456
10.1038/nm.2425
10.1084/jem.20090313
10.1016/j.immuni.2009.07.002
10.1093/bioinformatics/btl567
10.1038/nm.2426
10.1093/hmg/10.7.699
10.1016/j.virol.2010.12.016
10.1038/nature08226
10.1126/scisignal.2002796
10.1038/srep26494
10.1182/blood-2007-11-123844
10.1093/nar/gkv007
10.1084/jem.20141380
10.1016/S0165-2478(03)00002-6
10.1016/j.immuni.2010.10.008
10.4049/jimmunol.177.8.5236
10.1146/annurev-immunol-031210-101400
10.1084/jem.193.12.1373
10.1016/1074-7613(95)90048-9
10.1093/bioinformatics/btn224
10.1016/S0952-7915(98)80162-3
10.1002/eji.1830130908
10.1038/nature10280
10.1084/jem.192.11.1553
10.1126/science.1175870
10.4049/jimmunol.170.2.686
10.1038/nri2217
10.1084/jem.20042060
10.1016/j.celrep.2015.06.015
10.1038/icb.2013.68
10.1038/nprot.2008.211
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References Bernasconi (2025030417572120600_r25) 2003; 101
Hatzi (2025030417572120600_r51) 2015; 212
Ma (2025030417572120600_r11) 2009; 87
Chung (2025030417572120600_r57) 2011; 17
Naniche (2025030417572120600_r2) 2004; 190
Good (2025030417572120600_r37) 2006; 177
Wrammert (2025030417572120600_r38) 2008; 453
Falcon (2025030417572120600_r48) 2007; 23
Choi (2025030417572120600_r55) 2011; 34
Bentebibel (2025030417572120600_r53) 2011; 108
Linterman (2025030417572120600_r58) 2011; 17
King (2025030417572120600_r62) 2009; 206
Amanna (2025030417572120600_r1) 2007; 357
Slifka (2025030417572120600_r19) 1998; 10
Johnston (2025030417572120600_r64) 2009; 325
Morita (2025030417572120600_r86) 2011; 34
Patsoukis (2025030417572120600_r85) 2012; 5
Tubo (2025030417572120600_r41) 2013; 153
Odegard (2025030417572120600_r45) 2008; 205
Kim (2025030417572120600_r67) 2001; 193
Chevalier (2025030417572120600_r87) 2011; 186
Kindler (2025030417572120600_r35) 1997; 159
Locci (2025030417572120600_r52) 2013; 39
Veerman (2025030417572120600_r43) 2007; 8
Du (2025030417572120600_r46) 2008; 24
Ise (2025030417572120600_r89) 2014; 111
Amanna (2025030417572120600_r3) 2011; 411
Ritchie (2025030417572120600_r47) 2015; 43
Pinna (2025030417572120600_r24) 2009; 39
Crotty (2025030417572120600_r23) 2003; 171
Bernasconi (2025030417572120600_r36) 2002; 298
Locci (2025030417572120600_r74) 2016; 17
Crotty (2025030417572120600_r54) 2011; 29
Choe (2025030417572120600_r69) 1998; 28
Steiniger (2025030417572120600_r77) 2005; 116
Kroenke (2025030417572120600_r68) 2012; 188
Good-Jacobson (2025030417572120600_r13) 2010; 11
Nurieva (2025030417572120600_r65) 2009; 325
Breitfeld (2025030417572120600_r8) 2000; 192
Nevins (2025030417572120600_r61) 2001; 10
Bentebibel (2025030417572120600_r88) 2016; 6
McCausland (2025030417572120600_r90) 2007; 178
Conti (2025030417572120600_r70) 2003; 86
Bentebibel (2025030417572120600_r75) 2013; 5
Cyster (2025030417572120600_r72) 2005; 23
Agematsu (2025030417572120600_r76) 2000; 15
Pereira (2025030417572120600_r80) 2009; 460
Mamani-Matsuda (2025030417572120600_r29) 2008; 111
Sage (2025030417572120600_r59) 2015; 12
Kerfoot (2025030417572120600_r39) 2011; 34
Yu (2025030417572120600_r66) 2009; 31
Slifka (2025030417572120600_r18) 1998; 8
Hale (2025030417572120600_r42) 2013; 38
Craft (2025030417572120600_r12) 2012; 8
Segerer (2025030417572120600_r73) 2004; 164
Sallusto (2025030417572120600_r22) 2010; 33
Bryant (2025030417572120600_r9) 2007; 179
Hannedouche (2025030417572120600_r79) 2011; 475
Pepper (2025030417572120600_r40) 2011; 35
Good (2025030417572120600_r26) 2009; 182
Haynes (2025030417572120600_r83) 2007; 179
Wallin (2025030417572120600_r60) 2014; 124
Tsai (2025030417572120600_r92) 2014; 92
Ellyard (2025030417572120600_r32) 2004; 103
Tangye (2025030417572120600_r27) 2003; 170
Huang (2025030417572120600_r49) 2009; 4
He (2025030417572120600_r91) 2013; 39
Schmitt (2025030417572120600_r10) 2009; 31
Lanzavecchia (2025030417572120600_r34) 1984; 55
Schmitt (2025030417572120600_r93) 2014; 35
Reinhardt (2025030417572120600_r63) 2009; 10
Good-Jacobson (2025030417572120600_r6) 2010; 185
Tangye (2025030417572120600_r20) 2009; 39
DiLillo (2025030417572120600_r17) 2008; 180
Yoon (2025030417572120600_r71) 2009; 86
Dogan (2025030417572120600_r21) 2009; 10
Takahashi (2025030417572120600_r14) 1998; 187
Blink (2025030417572120600_r15) 2005; 201
Lanzavecchia (2025030417572120600_r33) 1983; 13
Liu (2025030417572120600_r31) 1995; 2
McHeyzer-Williams (2025030417572120600_r28) 2005; 23
Sallusto (2025030417572120600_r81) 1999; 401
Klein (2025030417572120600_r5) 2008; 8
Manz (2025030417572120600_r16) 1997; 388
Schaerli (2025030417572120600_r82) 2000; 192
Allen (2025030417572120600_r4) 2007; 27
Liu (2025030417572120600_r50) 2014; 507
Ettinger (2025030417572120600_r30) 2007; 178
Rasheed (2025030417572120600_r84) 2006; 36
Hori (2025030417572120600_r56) 2003; 299
Poholek (2025030417572120600_r44) 2010; 185
Wang (2025030417572120600_r78) 2014; 2
Shlomchik (2025030417572120600_r7) 2012; 247
References_xml – volume: 36
  start-page: 1892
  year: 2006
  ident: 2025030417572120600_r84
  article-title: Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression
  publication-title: Eur. J. Immunol.
  doi: 10.1002/eji.200636136
– volume: 103
  start-page: 3805
  year: 2004
  ident: 2025030417572120600_r32
  article-title: Antigen-selected, immunoglobulin-secreting cells persist in human spleen and bone marrow
  publication-title: Blood
  doi: 10.1182/blood-2003-09-3109
– volume: 17
  start-page: 976
  year: 2016
  ident: 2025030417572120600_r74
  article-title: Activin A programs the differentiation of human TFH cells
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.3494
– volume: 116
  start-page: 429
  year: 2005
  ident: 2025030417572120600_r77
  article-title: CD27+ B cells in human lymphatic organs: re-evaluating the splenic marginal zone
  publication-title: Immunology
  doi: 10.1111/j.1365-2567.2005.02242.x
– volume: 357
  start-page: 1903
  year: 2007
  ident: 2025030417572120600_r1
  article-title: Duration of humoral immunity to common viral and vaccine antigens
  publication-title: N. Engl. J. Med.
  doi: 10.1056/NEJMoa066092
– volume: 185
  start-page: 313
  year: 2010
  ident: 2025030417572120600_r44
  article-title: In vivo regulation of Bcl6 and T follicular helper cell development
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.0904023
– volume: 299
  start-page: 1057
  year: 2003
  ident: 2025030417572120600_r56
  article-title: Control of regulatory T cell development by the transcription factor Foxp3
  publication-title: Science
  doi: 10.1126/science.1079490
– volume: 192
  start-page: 1545
  year: 2000
  ident: 2025030417572120600_r8
  article-title: Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.192.11.1545
– volume: 39
  start-page: 770
  year: 2013
  ident: 2025030417572120600_r91
  article-title: Circulating precursor CCR7(lo)PD-1(hi) CXCR5+ CD4+ T cells indicate Tfh cell activity and promote antibody responses upon antigen reexposure
  publication-title: Immunity
  doi: 10.1016/j.immuni.2013.09.007
– volume: 5
  start-page: 176ra32
  year: 2013
  ident: 2025030417572120600_r75
  article-title: Induction of ICOS+CXCR3+CXCR5+ TH cells correlates with antibody responses to influenza vaccination
  publication-title: Sci. Transl. Med.
  doi: 10.1126/scitranslmed.3005191
– volume: 23
  start-page: 487
  year: 2005
  ident: 2025030417572120600_r28
  article-title: Antigen-specific memory B cell development
  publication-title: Annu. Rev. Immunol.
  doi: 10.1146/annurev.immunol.23.021704.115732
– volume: 35
  start-page: 436
  year: 2014
  ident: 2025030417572120600_r93
  article-title: Phenotype and functions of memory Tfh cells in human blood
  publication-title: Trends Immunol.
  doi: 10.1016/j.it.2014.06.002
– volume: 27
  start-page: 190
  year: 2007
  ident: 2025030417572120600_r4
  article-title: Germinal-center organization and cellular dynamics
  publication-title: Immunity
  doi: 10.1016/j.immuni.2007.07.009
– volume: 507
  start-page: 513
  year: 2014
  ident: 2025030417572120600_r50
  article-title: Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development
  publication-title: Nature
  doi: 10.1038/nature12910
– volume: 15
  start-page: 573
  year: 2000
  ident: 2025030417572120600_r76
  article-title: Memory B cells and CD27
  publication-title: Histol. Histopathol.
– volume: 186
  start-page: 5556
  year: 2011
  ident: 2025030417572120600_r87
  article-title: CXCR5 expressing human central memory CD4 T cells and their relevance for humoral immune responses
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.1002828
– volume: 453
  start-page: 667
  year: 2008
  ident: 2025030417572120600_r38
  article-title: Rapid cloning of high-affinity human monoclonal antibodies against influenza virus
  publication-title: Nature
  doi: 10.1038/nature06890
– volume: 178
  start-page: 817
  year: 2007
  ident: 2025030417572120600_r90
  article-title: SAP regulation of follicular helper CD4 T cell development and humoral immunity is independent of SLAM and Fyn kinase
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.178.2.817
– volume: 10
  start-page: 385
  year: 2009
  ident: 2025030417572120600_r63
  article-title: Cytokine-secreting follicular T cells shape the antibody repertoire
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1715
– volume: 34
  start-page: 108
  year: 2011
  ident: 2025030417572120600_r86
  article-title: Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion
  publication-title: Immunity
  doi: 10.1016/j.immuni.2010.12.012
– volume: 171
  start-page: 4969
  year: 2003
  ident: 2025030417572120600_r23
  article-title: Cutting edge: long-term B cell memory in humans after smallpox vaccination
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.171.10.4969
– volume: 388
  start-page: 133
  year: 1997
  ident: 2025030417572120600_r16
  article-title: Lifetime of plasma cells in the bone marrow
  publication-title: Nature
  doi: 10.1038/40540
– volume: 8
  start-page: 363
  year: 1998
  ident: 2025030417572120600_r18
  article-title: Humoral immunity due to long-lived plasma cells
  publication-title: Immunity
  doi: 10.1016/S1074-7613(00)80541-5
– volume: 34
  start-page: 932
  year: 2011
  ident: 2025030417572120600_r55
  article-title: ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6
  publication-title: Immunity
  doi: 10.1016/j.immuni.2011.03.023
– volume: 38
  start-page: 805
  year: 2013
  ident: 2025030417572120600_r42
  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
  publication-title: Immunity
  doi: 10.1016/j.immuni.2013.02.020
– volume: 401
  start-page: 708
  year: 1999
  ident: 2025030417572120600_r81
  article-title: Two subsets of memory T lymphocytes with distinct homing potentials and effector functions
  publication-title: Nature
  doi: 10.1038/44385
– volume: 87
  start-page: 590
  year: 2009
  ident: 2025030417572120600_r11
  article-title: Early commitment of naïve human CD4(+) T cells to the T follicular helper (T(FH)) cell lineage is induced by IL-12
  publication-title: Immunol. Cell Biol.
  doi: 10.1038/icb.2009.64
– volume: 10
  start-page: 1292
  year: 2009
  ident: 2025030417572120600_r21
  article-title: Multiple layers of B cell memory with different effector functions
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1814
– volume: 8
  start-page: 337
  year: 2012
  ident: 2025030417572120600_r12
  article-title: Follicular helper T cells in immunity and systemic autoimmunity
  publication-title: Nat. Rev. Rheumatol.
  doi: 10.1038/nrrheum.2012.58
– volume: 35
  start-page: 583
  year: 2011
  ident: 2025030417572120600_r40
  article-title: Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells
  publication-title: Immunity
  doi: 10.1016/j.immuni.2011.09.009
– volume: 205
  start-page: 2873
  year: 2008
  ident: 2025030417572120600_r45
  article-title: ICOS-dependent extrafollicular helper T cells elicit IgG production via IL-21 in systemic autoimmunity
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20080840
– volume: 28
  start-page: 508
  year: 1998
  ident: 2025030417572120600_r69
  article-title: IL-10 interrupts memory B cell expansion in the germinal center by inducing differentiation into plasma cells
  publication-title: Eur. J. Immunol.
  doi: 10.1002/(SICI)1521-4141(199802)28:02<508::AID-IMMU508>3.0.CO;2-I
– volume: 101
  start-page: 4500
  year: 2003
  ident: 2025030417572120600_r25
  article-title: A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells
  publication-title: Blood
  doi: 10.1182/blood-2002-11-3569
– volume: 164
  start-page: 635
  year: 2004
  ident: 2025030417572120600_r73
  article-title: CXCR3 is involved in tubulointerstitial injury in human glomerulonephritis
  publication-title: Am. J. Pathol.
  doi: 10.1016/S0002-9440(10)63152-5
– volume: 2
  start-page: 846
  year: 2014
  ident: 2025030417572120600_r78
  article-title: In vitro characterization of the anti-PD-1 antibody nivolumab, BMS-936558, and in vivo toxicology in non-human primates
  publication-title: Cancer Immunol. Res.
  doi: 10.1158/2326-6066.CIR-14-0040
– volume: 190
  start-page: 1387
  year: 2004
  ident: 2025030417572120600_r2
  article-title: Decrease in measles virus-specific CD4 T cell memory in vaccinated subjects
  publication-title: J. Infect. Dis.
  doi: 10.1086/424571
– volume: 179
  start-page: 8180
  year: 2007
  ident: 2025030417572120600_r9
  article-title: Cytokine-mediated regulation of human B cell differentiation into Ig-secreting cells: predominant role of IL-21 produced by CXCR5+ T follicular helper cells
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.179.12.8180
– volume: 39
  start-page: 758
  year: 2013
  ident: 2025030417572120600_r52
  article-title: Human circulating PD-1+CXCR3-CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses
  publication-title: Immunity
  doi: 10.1016/j.immuni.2013.08.031
– volume: 188
  start-page: 3734
  year: 2012
  ident: 2025030417572120600_r68
  article-title: Bcl6 and Maf cooperate to instruct human follicular helper CD4 T cell differentiation
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.1103246
– volume: 325
  start-page: 1001
  year: 2009
  ident: 2025030417572120600_r65
  article-title: Bcl6 mediates the development of T follicular helper cells
  publication-title: Science
  doi: 10.1126/science.1176676
– volume: 178
  start-page: 2872
  year: 2007
  ident: 2025030417572120600_r30
  article-title: IL-21 and BAFF/BLyS synergize in stimulating plasma cell differentiation from a unique population of human splenic memory B cells
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.178.5.2872
– volume: 179
  start-page: 5099
  year: 2007
  ident: 2025030417572120600_r83
  article-title: Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.179.8.5099
– volume: 298
  start-page: 2199
  year: 2002
  ident: 2025030417572120600_r36
  article-title: Maintenance of serological memory by polyclonal activation of human memory B cells
  publication-title: Science
  doi: 10.1126/science.1076071
– volume: 124
  start-page: 2666
  year: 2014
  ident: 2025030417572120600_r60
  article-title: Human T-follicular helper and T-follicular regulatory cell maintenance is independent of germinal centers
  publication-title: Blood
  doi: 10.1182/blood-2014-07-585976
– volume: 39
  start-page: 2065
  year: 2009
  ident: 2025030417572120600_r20
  article-title: Memory B cells: effectors of long-lived immune responses
  publication-title: Eur. J. Immunol.
  doi: 10.1002/eji.200939531
– volume: 182
  start-page: 890
  year: 2009
  ident: 2025030417572120600_r26
  article-title: Resting human memory B cells are intrinsically programmed for enhanced survival and responsiveness to diverse stimuli compared to naive B cells
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.182.2.890
– volume: 11
  start-page: 535
  year: 2010
  ident: 2025030417572120600_r13
  article-title: PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1877
– volume: 23
  start-page: 127
  year: 2005
  ident: 2025030417572120600_r72
  article-title: Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs
  publication-title: Annu. Rev. Immunol.
  doi: 10.1146/annurev.immunol.23.021704.115628
– volume: 39
  start-page: 1260
  year: 2009
  ident: 2025030417572120600_r24
  article-title: Clonal dissection of the human memory B-cell repertoire following infection and vaccination
  publication-title: Eur. J. Immunol.
  doi: 10.1002/eji.200839129
– volume: 111
  start-page: 11792
  year: 2014
  ident: 2025030417572120600_r89
  article-title: Memory B cells contribute to rapid Bcl6 expression by memory follicular helper T cells
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1404671111
– volume: 187
  start-page: 885
  year: 1998
  ident: 2025030417572120600_r14
  article-title: In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. V. Affinity maturation develops in two stages of clonal selection
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.187.6.885
– volume: 108
  start-page: E488
  year: 2011
  ident: 2025030417572120600_r53
  article-title: Human tonsil B-cell lymphoma 6 (BCL6)-expressing CD4+ T-cell subset specialized for B-cell help outside germinal centers
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1100898108
– volume: 247
  start-page: 52
  year: 2012
  ident: 2025030417572120600_r7
  article-title: Germinal center selection and the development of memory B and plasma cells
  publication-title: Immunol. Rev.
  doi: 10.1111/j.1600-065X.2012.01124.x
– volume: 153
  start-page: 785
  year: 2013
  ident: 2025030417572120600_r41
  article-title: Single naive CD4+ T cells from a diverse repertoire produce different effector cell types during infection
  publication-title: Cell
  doi: 10.1016/j.cell.2013.04.007
– volume: 86
  start-page: 1311
  year: 2009
  ident: 2025030417572120600_r71
  article-title: IL-21 and IL-10 have redundant roles but differential capacities at different stages of plasma cell generation from human germinal center B cells
  publication-title: J. Leukoc. Biol.
  doi: 10.1189/jlb.0409268
– volume: 185
  start-page: 3117
  year: 2010
  ident: 2025030417572120600_r6
  article-title: Plasticity and heterogeneity in the generation of memory B cells and long-lived plasma cells: the influence of germinal center interactions and dynamics
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.1001155
– volume: 159
  start-page: 2085
  year: 1997
  ident: 2025030417572120600_r35
  article-title: Memory, but not naive, peripheral blood B lymphocytes differentiate into Ig-secreting cells after CD40 ligation and costimulation with IL-4 and the differentiation factors IL-2, IL-10, and IL-3
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.159.5.2085
– volume: 34
  start-page: 947
  year: 2011
  ident: 2025030417572120600_r39
  article-title: Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone
  publication-title: Immunity
  doi: 10.1016/j.immuni.2011.03.024
– volume: 31
  start-page: 158
  year: 2009
  ident: 2025030417572120600_r10
  article-title: Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12
  publication-title: Immunity
  doi: 10.1016/j.immuni.2009.04.016
– volume: 180
  start-page: 361
  year: 2008
  ident: 2025030417572120600_r17
  article-title: Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.180.1.361
– volume: 8
  start-page: 532
  year: 2007
  ident: 2025030417572120600_r43
  article-title: Interaction of the selectin ligand PSGL-1 with chemokines CCL21 and CCL19 facilitates efficient homing of T cells to secondary lymphoid organs
  publication-title: Nat. Immunol.
  doi: 10.1038/ni1456
– volume: 17
  start-page: 975
  year: 2011
  ident: 2025030417572120600_r58
  article-title: Foxp3+ follicular regulatory T cells control the germinal center response
  publication-title: Nat. Med.
  doi: 10.1038/nm.2425
– volume: 206
  start-page: 1001
  year: 2009
  ident: 2025030417572120600_r62
  article-title: IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20090313
– volume: 31
  start-page: 457
  year: 2009
  ident: 2025030417572120600_r66
  article-title: The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment
  publication-title: Immunity
  doi: 10.1016/j.immuni.2009.07.002
– volume: 23
  start-page: 257
  year: 2007
  ident: 2025030417572120600_r48
  article-title: Using GOstats to test gene lists for GO term association
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btl567
– volume: 17
  start-page: 983
  year: 2011
  ident: 2025030417572120600_r57
  article-title: Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions
  publication-title: Nat. Med.
  doi: 10.1038/nm.2426
– volume: 10
  start-page: 699
  year: 2001
  ident: 2025030417572120600_r61
  article-title: The Rb/E2F pathway and cancer
  publication-title: Hum. Mol. Genet.
  doi: 10.1093/hmg/10.7.699
– volume: 411
  start-page: 206
  year: 2011
  ident: 2025030417572120600_r3
  article-title: Contributions of humoral and cellular immunity to vaccine-induced protection in humans
  publication-title: Virology
  doi: 10.1016/j.virol.2010.12.016
– volume: 460
  start-page: 1122
  year: 2009
  ident: 2025030417572120600_r80
  article-title: EBI2 mediates B cell segregation between the outer and centre follicle
  publication-title: Nature
  doi: 10.1038/nature08226
– volume: 5
  start-page: ra46
  year: 2012
  ident: 2025030417572120600_r85
  article-title: Selective effects of PD-1 on Akt and Ras pathways regulate molecular components of the cell cycle and inhibit T cell proliferation
  publication-title: Sci. Signal.
  doi: 10.1126/scisignal.2002796
– volume: 6
  start-page: 26494
  year: 2016
  ident: 2025030417572120600_r88
  article-title: ICOS(+)PD-1(+)CXCR3(+) T follicular helper cells contribute to the generation of high-avidity antibodies following influenza vaccination
  publication-title: Sci. Rep.
  doi: 10.1038/srep26494
– volume: 111
  start-page: 4653
  year: 2008
  ident: 2025030417572120600_r29
  article-title: The human spleen is a major reservoir for long-lived vaccinia virus-specific memory B cells
  publication-title: Blood
  doi: 10.1182/blood-2007-11-123844
– volume: 43
  start-page: e47
  year: 2015
  ident: 2025030417572120600_r47
  article-title: limma powers differential expression analyses for RNA-sequencing and microarray studies
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkv007
– volume: 212
  start-page: 539
  year: 2015
  ident: 2025030417572120600_r51
  article-title: BCL6 orchestrates Tfh cell differentiation via multiple distinct mechanisms
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20141380
– volume: 86
  start-page: 123
  year: 2003
  ident: 2025030417572120600_r70
  article-title: IL-10, an inflammatory/inhibitory cytokine, but not always
  publication-title: Immunol. Lett.
  doi: 10.1016/S0165-2478(03)00002-6
– volume: 33
  start-page: 451
  year: 2010
  ident: 2025030417572120600_r22
  article-title: From vaccines to memory and back
  publication-title: Immunity
  doi: 10.1016/j.immuni.2010.10.008
– volume: 177
  start-page: 5236
  year: 2006
  ident: 2025030417572120600_r37
  article-title: Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.177.8.5236
– volume: 29
  start-page: 621
  year: 2011
  ident: 2025030417572120600_r54
  article-title: Follicular helper CD4 T cells (TFH)
  publication-title: Annu. Rev. Immunol.
  doi: 10.1146/annurev-immunol-031210-101400
– volume: 193
  start-page: 1373
  year: 2001
  ident: 2025030417572120600_r67
  article-title: Subspecialization of CXCR5+ T cells: B helper activity is focused in a germinal center-localized subset of CXCR5+ T cells
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.193.12.1373
– volume: 2
  start-page: 239
  year: 1995
  ident: 2025030417572120600_r31
  article-title: Memory B cells from human tonsils colonize mucosal epithelium and directly present antigen to T cells by rapid up-regulation of B7-1 and B7-2
  publication-title: Immunity
  doi: 10.1016/1074-7613(95)90048-9
– volume: 24
  start-page: 1547
  year: 2008
  ident: 2025030417572120600_r46
  article-title: lumi: a pipeline for processing Illumina microarray
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btn224
– volume: 10
  start-page: 252
  year: 1998
  ident: 2025030417572120600_r19
  article-title: Long-lived plasma cells: a mechanism for maintaining persistent antibody production
  publication-title: Curr. Opin. Immunol.
  doi: 10.1016/S0952-7915(98)80162-3
– volume: 13
  start-page: 733
  year: 1983
  ident: 2025030417572120600_r33
  article-title: Activation of human B lymphocytes: frequency of antigen-specific B cells triggered by alloreactive or by antigen-specific T cell clones
  publication-title: Eur. J. Immunol.
  doi: 10.1002/eji.1830130908
– volume: 475
  start-page: 524
  year: 2011
  ident: 2025030417572120600_r79
  article-title: Oxysterols direct immune cell migration via EBI2
  publication-title: Nature
  doi: 10.1038/nature10280
– volume: 192
  start-page: 1553
  year: 2000
  ident: 2025030417572120600_r82
  article-title: CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.192.11.1553
– volume: 325
  start-page: 1006
  year: 2009
  ident: 2025030417572120600_r64
  article-title: Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation
  publication-title: Science
  doi: 10.1126/science.1175870
– volume: 170
  start-page: 686
  year: 2003
  ident: 2025030417572120600_r27
  article-title: Intrinsic differences in the proliferation of naive and memory human B cells as a mechanism for enhanced secondary immune responses
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.170.2.686
– volume: 8
  start-page: 22
  year: 2008
  ident: 2025030417572120600_r5
  article-title: Germinal centres: role in B-cell physiology and malignancy
  publication-title: Nat. Rev. Immunol.
  doi: 10.1038/nri2217
– volume: 201
  start-page: 545
  year: 2005
  ident: 2025030417572120600_r15
  article-title: Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20042060
– volume: 12
  start-page: 163
  year: 2015
  ident: 2025030417572120600_r59
  article-title: Defective TFH cell function and increased TFR cells contribute to defective antibody production in aging
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2015.06.015
– volume: 55
  start-page: 197
  year: 1984
  ident: 2025030417572120600_r34
  article-title: In vitro stimulation of IgE production at a single precursor level by human alloreactive T helper clones
  publication-title: Clin. Exp. Immunol.
– volume: 92
  start-page: 57
  year: 2014
  ident: 2025030417572120600_r92
  article-title: Follicular helper T-cell memory: establishing new frontiers during antibody response
  publication-title: Immunol. Cell Biol.
  doi: 10.1038/icb.2013.68
– volume: 4
  start-page: 44
  year: 2009
  ident: 2025030417572120600_r49
  article-title: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2008.211
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Snippet Follicular helper T (Tfh) cells are necessary for germinal center B cell maturation during primary immune responses; however, the T cells that promote humoral...
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StartPage 1359
SubjectTerms Adolescent
Antibody Formation
B-Lymphocytes - cytology
B-Lymphocytes - immunology
Child
Child, Preschool
Cytokines - immunology
Female
Gene Expression Regulation - immunology
Humans
Immunoglobulin G - immunology
Immunologic Memory
Male
Programmed Cell Death 1 Receptor - immunology
Proto-Oncogene Proteins c-bcl-6 - immunology
Receptors, CXCR5 - immunology
T-Lymphocytes, Helper-Inducer - cytology
T-Lymphocytes, Helper-Inducer - immunology
Title Human Extrafollicular CD4+ Th Cells Help Memory B Cells Produce Igs
URI https://www.ncbi.nlm.nih.gov/pubmed/30030323
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Volume 201
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