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

Immunity

Volumn 38, Issue 3, 2013, Pages 596-605

  Baumjohann, Dirk ^a,b,c   Preite, Silvia ^a   Reboldi, Andrea ^a,b   Ronchi, Francesca ^a   Ansel, K Mark ^b,c   Lanzavecchia, Antonio ^a   Sallusto, Federica ^a  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; INDUCIBLE T CELL COSTIMULATOR LIGAND;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; BYSTANDER EFFECT; CELL SIZE; CONTROLLED STUDY; GERMINAL CENTER; HELPER CELL; HUMORAL IMMUNITY; HYPERGAMMAGLOBULINEMIA; IMMUNE DYSREGULATION; IN VIVO STUDY; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; T FOLLICULAR HELPER CELL;

ANIMALS; ANTIBODIES; ANTIGENS; ANTIGENS, CD3; ANTIGENS, CD40; B-LYMPHOCYTES; CD40 LIGAND; CELL LINE, TUMOR; FLOW CYTOMETRY; GERMINAL CENTER; HUMANS; IMMUNIZATION; IMMUNOPHENOTYPING; INDUCIBLE T-CELL CO-STIMULATOR LIGAND; INDUCIBLE T-CELL CO-STIMULATOR PROTEIN; LUMINESCENT PROTEINS; LYMPHOCYTE COUNT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; PROTEIN BINDING; RECEPTORS, CXCR5; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84875549975     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.11.020     Document Type: Article

References (66)

1. Alexander C.M., Tygrett L.T., Boyden A.W., Wolniak K.L., Legge K.L., Waldschmidt T.J. T regulatory cells participate in the control of germinal centre reactions. Immunology 2011, 133:452-468.
2. Allen C.D., Okada T., Tang H.L., Cyster J.G. Imaging of germinal center selection events during affinity maturation. Science 2007, 315:528-531.
3. Ansel K.M., McHeyzer-Williams L.J., Ngo V.N., McHeyzer-Williams M.G., Cyster J.G. In vivo-activated CD4 T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J. Exp. Med. 1999, 190:1123-1134.
4. Batista F.D., Harwood N.E. The who, how and where of antigen presentation to B cells. Nat. Rev. Immunol. 2009, 9:15-27.
5. Baumjohann D., Okada T., Ansel K.M. Cutting Edge: Distinct waves of BCL6 expression during T follicular helper cell development. J. Immunol. 2011, 187:2089-2092.
6. Breitfeld D., Ohl L., Kremmer E., Ellwart J., Sallusto F., Lipp M., Förster R. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J. Exp. Med. 2000, 192:1545-1552.
7. Choi Y.S., Kageyama R., Eto D., Escobar T.C., Johnston R.J., Monticelli L., Lao C., Crotty S. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 2011, 34:932-946.
8. Chtanova T., Tangye S.G., Newton R., Frank N., Hodge M.R., Rolph M.S., Mackay C.R. T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J. Immunol. 2004, 173:68-78.
9. Chung Y., Tanaka S., Chu F., Nurieva R.I., Martinez G.J., Rawal S., Wang Y.H., Lim H., Reynolds J.M., Zhou X.H., et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 2011, 17:983-988.
10. Crotty S. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 2011, 29:621-663.
11. Cyster J.G. B cell follicles and antigen encounters of the third kind. Nat. Immunol. 2010, 11:989-996.
12. Deenick E.K., Chan A., Ma C.S., Gatto D., Schwartzberg P.L., Brink R., Tangye S.G. Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 2010, 33:241-253.
13. Fahey L.M., Wilson E.B., Elsaesser H., Fistonich C.D., McGavern D.B., Brooks D.G. Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J. Exp. Med. 2011, 208:987-999.
14. Fazilleau N., Mark L., McHeyzer-Williams L.J., McHeyzer-Williams M.G. Follicular helper T cells: lineage and location. Immunity 2009, 30:324-335.
15. Gatto D., Brink R. The germinal center reaction. J Allergy Clin Immunol 2010, 126:898-907. quiz 908-899.
16. Glatman Zaretsky A., Taylor J.J., King I.L., Marshall F.A., Mohrs M., Pearce E.J. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J. Exp. Med. 2009, 206:991-999.
17. Goenka R., Barnett L.G., Silver J.S., O'Neill P.J., Hunter C.A., Cancro M.P., Laufer T.M. Cutting edge: dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J. Immunol. 2011, 187:1091-1095.
18. Gong Q., Ou Q., Ye S., Lee W.P., Cornelius J., Diehl L., Lin W.Y., Hu Z., Lu Y., Chen Y., et al. Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J. Immunol. 2005, 174:817-826.
19. Good-Jacobson K.L., Shlomchik M.J. Plasticity and heterogeneity in the generation of memory B cells and long-lived plasma cells: the influence of germinal center interactions and dynamics. J. Immunol. 2010, 185:3117-3125.
20. Goodnow C.C., Vinuesa C.G., Randall K.L., Mackay F., Brink R. Control systems and decision making for antibody production. Nat. Immunol. 2010, 11:681-688.
21. Hauser A.E., Junt T., Mempel T.R., Sneddon M.W., Kleinstein S.H., Henrickson S.E., von Andrian U.H., Shlomchik M.J., Haberman A.M. Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity 2007, 26:655-667.
22. Hauser S.L., Waubant E., Arnold D.L., Vollmer T., Antel J., Fox R.J., Bar-Or A., Panzara M., Sarkar N., Agarwal S., et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 2008, 358:676-688. HERMES Trial Group.
23. Haynes N.M., Allen C.D., Lesley R., Ansel K.M., Killeen N., Cyster J.G. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J. Immunol. 2007, 179:5099-5108.
24. Hebel K., Griewank K., Inamine A., Chang H.D., Müller-Hilke B., Fillatreau S., Manz R.A., Radbruch A., Jung S. Plasma cell differentiation in T-independent type 2 immune responses is independent of CD11c(high) dendritic cells. Eur. J. Immunol. 2006, 36:2912-2919.
25. Johnston R.J., Poholek A.C., DiToro D., Yusuf I., Eto D., Barnett B., Dent A.L., Craft J., Crotty S. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science 2009, 325:1006-1010.
26. Jung S., Unutmaz D., Wong P., Sano G., De los Santos K., Sparwasser T., Wu S., Vuthoori S., Ko K., Zavala F., et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 2002, 17:211-220.
27. Kerfoot S.M., Yaari G., Patel J.R., Johnson K.L., Gonzalez D.G., Kleinstein S.H., Haberman A.M. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 2011, 34:947-960.
28. Kim C.H., Rott L.S., Clark-Lewis I., Campbell D.J., Wu L., Butcher E.C. Subspecialization of CXCR5+ T cells: B helper activity is focused in a germinal center-localized subset of CXCR5+ T cells. J. Exp. Med. 2001, 193:1373-1381.
29. King C. New insights into the differentiation and function of T follicular helper cells. Nat. Rev. Immunol. 2009, 9:757-766.
30. Kingston D., Schmid M.A., Onai N., Obata-Onai A., Baumjohann D., Manz M.G. The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 2009, 114:835-843.
31. Kitano M., Moriyama S., Ando Y., Hikida M., Mori Y., Kurosaki T., Okada T. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 2011, 34:961-972.
32. Langenkamp A., Nagata K., Murphy K., Wu L., Lanzavecchia A., Sallusto F. Kinetics and expression patterns of chemokine receptors in human CD4+ T lymphocytes primed by myeloid or plasmacytoid dendritic cells. Eur. J. Immunol. 2003, 33:474-482.
33. Lanzavecchia A., Sallusto F. Regulation of T cell immunity by dendritic cells. Cell 2001, 106:263-266.
34. Lindquist R.L., Shakhar G., Dudziak D., Wardemann H., Eisenreich T., Dustin M.L., Nussenzweig M.C. Visualizing dendritic cell networks in vivo. Nat. Immunol. 2004, 5:1243-1250.
35. Lindqvist M., van Lunzen J., Soghoian D.Z., Kuhl B.D., Ranasinghe S., Kranias G., Flanders M.D., Cutler S., Yudanin N., Muller M.I., et al. Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J. Clin. Invest. 2012, 122:3271-3280.
36. Linterman M.A., Pierson W., Lee S.K., Kallies A., Kawamoto S., Rayner T.F., Srivastava M., Divekar D.P., Beaton L., Hogan J.J., et al. Foxp3+ follicular regulatory T cells control the germinal center response. Nat. Med. 2011, 17:975-982.
37. Ma C.S., Deenick E.K., Batten M., Tangye S.G. The origins, function, and regulation of T follicular helper cells. J. Exp. Med. 2012, 209:1241-1253.
38. MacLennan I.C., Toellner K.M., Cunningham A.F., Serre K., Sze D.M., Zúñiga E., Cook M.C., Vinuesa C.G. Extrafollicular antibody responses. Immunol. Rev. 2003, 194:8-18.
39. Malissen M., Gillet A., Ardouin L., Bouvier G., Trucy J., Ferrier P., Vivier E., Malissen B. Altered T cell development in mice with a targeted mutation of the CD3-epsilon gene. EMBO J. 1995, 14:4641-4653.
40. McHeyzer-Williams M., Okitsu S., Wang N., McHeyzer-Williams L. Molecular programming of B cell memory. Nat. Rev. Immunol. 2011, 12:24-34.
41. Murphy K.M. Comment on " Activation of β-catenin in dendritic cells regulates immunity versus tolerance in the intestine" Science 2011, 333:405.
42. Nakayamada S., Kanno Y., Takahashi H., Jankovic D., Lu K.T., Johnson T.A., Sun H.W., Vahedi G., Hakim O., Handon R., et al. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011, 35:919-931.
43. Nurieva R.I., Chung Y., Hwang D., Yang X.O., Kang H.S., Ma L., Wang Y.H., Watowich S.S., Jetten A.M., Tian Q., Dong C. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 2008, 29:138-149.
44. Nurieva R.I., Chung Y., Martinez G.J., Yang X.O., Tanaka S., Matskevitch T.D., Wang Y.H., Dong C. Bcl6 mediates the development of T follicular helper cells. Science 2009, 325:1001-1005.
45. O'Shea J.J., Paul W.E. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 2010, 327:1098-1102.
46. Oestreich K.J., Mohn S.E., Weinmann A.S. Molecular mechanisms that control the expression and activity of Bcl-6 in TH1 cells to regulate flexibility with a TFH-like gene profile. Nat. Immunol. 2012, 13:405-411.
47. Oxenius A., Bachmann M.F., Zinkernagel R.M., Hengartner H. Virus-specific MHC-class II-restricted TCR-transgenic mice: effects on humoral and cellular immune responses after viral infection. Eur. J. Immunol. 1998, 28:390-400.
48. Pepper M., Pagán A.J., Igyártó B.Z., Taylor J.J., Jenkins M.K. Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 2011, 35:583-595.
49. Phan T.G., Amesbury M., Gardam S., Crosbie J., Hasbold J., Hodgkin P.D., Basten A., Brink R. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J. Exp. Med. 2003, 197:845-860.
50. Poholek A.C., Hansen K., Hernandez S.G., Eto D., Chandele A., Weinstein J.S., Dong X., Odegard J.M., Kaech S.M., Dent A.L., et al. In vivo regulation of Bcl6 and T follicular helper cell development. J. Immunol. 2010, 185:313-326.
51. Probst H.C., Tschannen K., Odermatt B., Schwendener R., Zinkernagel R.M., Van Den Broek M. Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin. Exp. Immunol. 2005, 141:398-404.
52. Qi H., Cannons J.L., Klauschen F., Schwartzberg P.L., Germain R.N. SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 2008, 455:764-769.
53. Reboldi A., Coisne C., Baumjohann D., Benvenuto F., Bottinelli D., Lira S., Uccelli A., Lanzavecchia A., Engelhardt B., Sallusto F. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 2009, 10:514-523.
54. Recher M., Lang K.S., Hunziker L., Freigang S., Eschli B., Harris N.L., Navarini A., Senn B.M., Fink K., Lötscher M., et al. Deliberate removal of T cell help improves virus-neutralizing antibody production. Nat. Immunol. 2004, 5:934-942.
55. Schaerli P., Willimann K., Lang A.B., Lipp M., Loetscher P., Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 2000, 192:1553-1562.
56. Schwickert T.A., Lindquist R.L., Shakhar G., Livshits G., Skokos D., Kosco-Vilbois M.H., Dustin M.L., Nussenzweig M.C. In vivo imaging of germinal centres reveals a dynamic open structure. Nature 2007, 446:83-87.
57. Tangye S.G., Tarlinton D.M. Memory B cells: effectors of long-lived immune responses. Eur. J. Immunol. 2009, 39:2065-2075.
58. Tsuji M., Komatsu N., Kawamoto S., Suzuki K., Kanagawa O., Honjo T., Hori S., Fagarasan S. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 2009, 323:1488-1492.
59. Victora G.D., Nussenzweig M.C. Germinal centers. Annu. Rev. Immunol. 2012, 30:429-457.
60. Victora G.D., Schwickert T.A., Fooksman D.R., Kamphorst A.O., Meyer-Hermann M., Dustin M.L., Nussenzweig M.C. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 2010, 143:592-605.
61. Vinuesa C.G., Cyster J.G. How T cells earn the follicular rite of passage. Immunity 2011, 35:671-680.
62. Vinuesa C.G., Linterman M.A., Goodnow C.C., Randall K.L. T cells and follicular dendritic cells in germinal center B-cell formation and selection. Immunol. Rev. 2010, 237:72-89.
63. Vogelzang A., McGuire H.M., Yu D., Sprent J., Mackay C.R., King C. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 2008, 29:127-137.
64. Wollenberg I., Agua-Doce A., Hernández A., Almeida C., Oliveira V.G., Faro J., Graca L. Regulation of the germinal center reaction by Foxp3+ follicular regulatory T cells. J. Immunol. 2011, 187:4553-4560.
65. Yu D., Rao S., Tsai L.M., Lee S.K., He Y., Sutcliffe E.L., Srivastava M., Linterman M., Zheng L., Simpson N., et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 2009, 31:457-468.
66. Yusuf I., Kageyama R., Monticelli L., Johnston R.J., Ditoro D., Hansen K., Barnett B., Crotty S. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J. Immunol. 2010, 185:190-202.