Bcl6 Protein Expression Shapes Pre-Germinal Center B Cell Dynamics and Follicular Helper T Cell Heterogeneity

Immunity

Volumn 34, Issue 6, 2011, Pages 961-972

  Kitano, Masahiro ^a   Moriyama, Saya ^a,b   Ando, Yoshikazu ^a   Hikida, Masaki ^a   Mori, Yasuo ^c   Kurosaki, Tomohiro ^a,b,d   Okada, Takaharu ^a,c  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 7 RECEPTOR; PROTEIN BCL 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CELL HETEROGENEITY; CELL PROLIFERATION; CONTROLLED STUDY; GERMINAL CENTER; HELPER CELL; MICROSCOPY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; UPREGULATION;

ANIMALS; ANTIGENS; B-LYMPHOCYTES; CELL PROLIFERATION; DNA-BINDING PROTEINS; GERMINAL CENTER; KINETICS; MICE; PHENOTYPE; RECEPTORS, INTERLEUKIN-7; T-LYMPHOCYTES, HELPER-INDUCER; UP-REGULATION;

EID: 79959343565     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.03.025     Document Type: Article

References (44)

1. Allen C.D., Ansel K.M., Low C., Lesley R., Tamamura H., Fujii N., Cyster J.G. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 2004, 5:943-952.
2. Allen C.D., Okada T., Cyster J.G. Germinal-center organization and cellular dynamics. Immunity 2007, 27:190-202.
3. 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.
4. Basso K., Dalla-Favera R. BCL6: Master regulator of the germinal center reaction and key oncogene in B cell lymphomagenesis. Adv. Immunol. 2010, 105:193-210.
5. Bauquet A.T., Jin H., Paterson A.M., Mitsdoerffer M., Ho I.C., Sharpe A.H., Kuchroo V.K. The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat. Immunol. 2009, 10:167-175.
6. Cannons J.L., Qi H., Lu K.T., Dutta M., Gomez-Rodriguez J., Cheng J., Wakeland E.K., Germain R.N., Schwartzberg P.L. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 2010, 32:253-265.
7. Carlson C.M., Endrizzi B.T., Wu J., Ding X., Weinreich M.A., Walsh E.R., Wani M.A., Lingrel J.B., Hogquist K.A., Jameson S.C. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 2006, 442:299-302.
8. Chan T.D., Gardam S., Gatto D., Turner V.M., Silke J., Brink R. In vivo control of B-cell survival and antigen-specific B-cell responses. Immunol. Rev. 2010, 237:90-103.
9. Crotty S., Johnston R.J., Schoenberger S.P. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 2010, 11:114-120.
10. Cyster J.G. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu. Rev. Immunol. 2005, 23:127-159.
11. 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.
12. Dent A.L., Shaffer A.L., Yu X., Allman D., Staudt L.M. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 1997, 276:589-592.
13. Fazilleau N., Eisenbraun M.D., Malherbe L., Ebright J.N., Pogue-Caley R.R., McHeyzer-Williams L.J., McHeyzer-Williams M.G. Lymphoid reservoirs of antigen-specific memory T helper cells. Nat. Immunol. 2007, 8:753-761.
14. Förster R., Emrich T., Kremmer E., Lipp M. Expression of the G-protein-coupled receptor BLR1 defines mature, recirculating B cells and a subset of T-helper memory cells. Blood 1994, 84:830-840.
15. Fukuda T., Yoshida T., Okada S., Hatano M., Miki T., Ishibashi K., Okabe S., Koseki H., Hirosawa S., Taniguchi M., et al. Disruption of the Bcl6 gene results in an impaired germinal center formation. J. Exp. Med. 1997, 186:439-448.
16. Gatto D., Paus D., Basten A., Mackay C.R., Brink R. Guidance of B cells by the orphan G protein-coupled receptor EBI2 shapes humoral immune responses. Immunity 2009, 31:259-269.
17. Good-Jacobson K.L., Szumilas C.G., Chen L., Sharpe A.H., Tomayko M.M., Shlomchik M.J. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 2010, 11:535-542.
18. 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.
19. Hsu H.C., Yang P., Wang J., Wu Q., Myers R., Chen J., Yi J., Guentert T., Tousson A., Stanus A.L., et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 2008, 9:166-175.
20. 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.
21. Klein U., Dalla-Favera R. Germinal centres: Role in B-cell physiology and malignancy. Nat. Rev. Immunol. 2008, 8:22-33.
22. Kurosaki T., Aiba Y., Kometani K., Moriyama S., Takahashi Y. Unique properties of memory B cells of different isotypes. Immunol. Rev. 2010, 237:104-116.
23. Linterman M.A., Vinuesa C.G. Signals that influence T follicular helper cell differentiation and function. Semin. Immunopathol. 2010, 32:183-196.
24. MacLennan I.C. Germinal centers. Annu. Rev. Immunol. 1994, 12:117-139.
25. Martins G., Calame K. Regulation and functions of Blimp-1 in T and B lymphocytes. Annu. Rev. Immunol. 2008, 26:133-169.
26. Morita R., Schmitt N., Bentebibel S.E., Ranganathan R., Bourdery L., Zurawski G., Foucat E., Dullaers M., Oh S., Sabzghabaei N., et al. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 2011, 34:108-121.
27. 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.
28. Nutt S.L., Fairfax K.A., Kallies A. BLIMP1 guides the fate of effector B and T cells. Nat. Rev. Immunol. 2007, 7:923-927.
29. Okada T., Miller M.J., Parker I., Krummel M.F., Neighbors M., Hartley S.B., O'Garra A., Cahalan M.D., Cyster J.G. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 2005, 3:e150.
30. Pereira J.P., Kelly L.M., Xu Y., Cyster J.G. EBI2 mediates B cell segregation between the outer and centre follicle. Nature 2009, 460:1122-1126.
31. Pereira J.P., Kelly L.M., Cyster J.G. Finding the right niche: B-cell migration in the early phases of T-dependent antibody responses. Int. Immunol. 2010, 22:413-419.
32. 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.
33. 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.
34. Reinhardt R.L., Liang H.E., Locksley R.M. Cytokine-secreting follicular T cells shape the antibody repertoire. Nat. Immunol. 2009, 10:385-393.
35. Schwickert T.A., Alabyev B., Manser T., Nussenzweig M.C. Germinal center reutilization by newly activated B cells. J. Exp. Med. 2009, 206:2907-2914.
36. Shaffer A.L., Rosenwald A., Hurt E.M., Giltnane J.M., Lam L.T., Pickeral O.K., Staudt L.M. Signatures of the immune response. Immunity 2001, 15:375-385.
37. Shih T.A., Roederer M., Nussenzweig M.C. Role of antigen receptor affinity in T cell-independent antibody responses in vivo. Nat. Immunol. 2002, 3:399-406.
38. Simpson N., Gatenby P.A., Wilson A., Malik S., Fulcher D.A., Tangye S.G., Manku H., Vyse T.J., Roncador G., Huttley G.A., et al. Expansion of circulating T cells resembling follicular helper T cells is a fixed phenotype that identifies a subset of severe systemic lupus erythematosus. Arthritis Rheum. 2010, 62:234-244.
39. Tokoyoda K., Zehentmeier S., Hegazy A.N., Albrecht I., Grün J.R., Löhning M., Radbruch A. Professional memory CD4+ T lymphocytes preferentially reside and rest in the bone marrow. Immunity 2009, 30:721-730.
40. 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.
41. Vinuesa C.G., Sanz I., Cook M.C. Dysregulation of germinal centres in autoimmune disease. Nat. Rev. Immunol. 2009, 9:845-857.
42. 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.
43. Ye B.H., Cattoretti G., Shen Q., Zhang J., Hawe N., de Waard R., Leung C., Nouri-Shirazi M., Orazi A., Chaganti R.S., et al. The BCL-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat. Genet. 1997, 16:161-170.
44. 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.