In-vitro derived germinal centre B cells differentially generate memory B or plasma cells in vivo

Nature Communications

Volumn 2, Issue 1, 2011, Pages

  Nojima, Takuya ^a   Haniuda, Kei ^a   Moutai, Tatsuya ^a   Matsudaira, Moeko ^a   Mizokawa, Sho ^a   Shiratori, Ikuo ^a   Azuma, Takachika ^a   Kitamura, Daisuke ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; IMMUNOGLOBULIN D; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN M; INTERLEUKIN 21; T LYMPHOCYTE ANTIGEN; ANTIGEN; INTERLEUKIN 4; INTERLEUKIN DERIVATIVE;

ADOPTIVE TRANSFER; ANIMAL CELL; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL FATE; CELL ISOLATION; CELL MANIPULATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; GC RICH SEQUENCE; GERMINAL CENTER; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; MEMORY CELL; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPE; PLASMA CELL; PRE B LYMPHOCYTE; PROTEIN EXPRESSION; ANIMAL; B LYMPHOCYTE; BAGG ALBINO MOUSE; C57BL MOUSE; CELL STRAIN 3T3; CYTOLOGY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; PHYSIOLOGY;

3T3 CELLS; ANIMALS; ANTIGENS; B-LYMPHOCYTES; CELL PROLIFERATION; FLOW CYTOMETRY; IMMUNOLOGIC MEMORY; INTERLEUKIN-4; INTERLEUKINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PLASMA CELLS;

EID: 80052643363     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1475     Document Type: Article

References (59)

1. MacLennan , I. C. Germinal centers. A nnu. Rev. Immunol. 1 2 , 117-139 ( 1994 ).
2. Tarlinton , D. B-cell memory: Are subsets necesssary? N at. Rev. Immunol. 6 , 785-790 ( 2006 ).
3. Good-Jacobson , K. L. & Shlomchik , M. J. Plasticity and heterogeneity in the hgeneration of memory B cells and long-lived plasma cells: The infl uence of germinal center interactions and dynamics. J. Immunol. 1 85 , 3117-3125 ( 2010 ).
4. McHeyzer-Williams , L. J. & McHeyzer-Williams , M. G. Antigen-specifi c memory B cell development. A nnu. Rev. Immunol. 2 3 , 487-513 ( 2005 ).
5. Erazo , A. et al. Unique maturation program of the IgE response in vivo. Immunity 26 , 191-203 ( 2007 ).
6. Renshaw , B. R. et al. Humoral immune responses in CD40 ligand-deficient mice. J. Exp. Med. 1 80 , 1889-1900 ( 1994 ).
7. Foy , T. M. et al. gp39-CD40 interactions are essential for germinal center formation and the development of B cell memory. J. Exp. Med. 1 80 , 157-163 ( 1994 ).
8. Kawabe , T. et al. The immune responses in CD40-deficient mice: Impaired immunoglobulin class switching and germinal center formation. Immunity 1 , 167-178 ( 1994 ).
9. Zotos , D. et al. IL-21 regulates germinal center B cell diff erentiation and proliferation through a B cell-intrinsic mechanism. J. Exp. Med. 2 07 , 365-378 ( 2010 ).
10. Linterman , M. A. et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207 , 353-363 ( 2010 ).
11. Bessa , J. , Kopf , M. & Bachmann , M. F. Cutting edge: IL-21 and TLR signaling regulate germinal center responses in a B cell-intrinsic manner. J. Immunol. 184 , 4615-4619 ( 2010 ).
12. Ozaki , K. et al. A critical role for IL-21 in regulating immunoglobulin production. Science 2 98 , 1630-1634 ( 2002 ).
13. Pene , J. et al. Cutting edge: IL-21 is a switch factor for the production of IgG1 and IgG3 by human B cells. J. Immunol. 1 72 , 5154-5157 ( 2004 ).
14. Ozaki , K. et al. Regulation of B cell diff erentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J. Immunol. 1 73 , 5361-5371 ( 2004 ).
15. Kwon , H. et al. Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors. Immunity 3 1 , 941-952 ( 2009 ).
16. Ettinger , R. et al. IL-21 induces diff erentiation of human naive and memory B cells into antibody-secreting plasma cells. J. Immunol. 175 , 7867-7879 ( 2005 ).
17. Kuchen , S. et al. Essential role of IL-21 in B cell activation, expansion, and plasma cell generation during CD4+ T cell-B cell collaboration. J. Immunol. 179 , 5886-5896 ( 2007 ).
18. Bryant , V. L. et al. Cytokine-mediated regulation of human B cell diff erentiation into Ig-secreting cells: Predominant role of IL-21 produced by CXCR5+ T follicular helper cells. J. Immunol. 1 79 , 8180-8190 ( 2007 ).
19. Nurieva , R. I. et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29 , 138-149 ( 2008 ).
20. Vogelzang , A. et al. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 2 9 , 127-137 ( 2008 ).
21. Yu , D. et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. I mmunity 31 , 457-468 ( 2009 ).
22. Dent , A. L. , Shaff er , A. L. , Yu , X. , Allman , D. & Staudt , L. M. Control of infl ammation, cytokine expression, and germinal center formation by BCL-6. Science 2 76 , 589-592 ( 1997 ).
23. Shapiro-Shelef , M. et al. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 1 9, 607-620 ( 2003 ).
24. Klein , U. et al. Transcription factor IRF4 controls plasma cell diff erentiation and class-switch recombination. N at. Immunol. 7 , 773-782 ( 2006 ).
25. Anderson , S. M. , Tomayko , M. M. , Ahuja , A. , Haberman , A. M. & Shlomchik , M. J. New markers for murine memory B cells that defi ne mutated and unmutated subsets. J. Exp. Med. 204 , 2103-2114 ( 2007 ).
26. Ridderstad , A. & Tarlinton , D. M. Kinetics of establishing the memory B cell population as revealed by CD38 expression. J. Immunol. 1 60 , 4688-4695 ( 1998 ).
27. Toyama , H. et al. Memory B cells without somatic hypermutation are generated from Bcl6-deficient B cells. I mmunity 1 7 , 329-339 ( 2002 ).
28. Dogan , I. et al. Multiple layers of B cell memory with diff erent eff ector functions. Nat. Immunol. 10 , 1292-1299 ( 2009 ).
29. Pape , K. A. , Taylor , J. J. , Maul , R. W. , Gearhart , P. J. & Jenkins , M. K. Different B cell populations mediate early and late memory during an endogenous immune response. Science 3 31 , 1203-1207 ( 2011 ).
30. Black , S. J. , van der Loo , W. , Loken , M. R. & Herzenberg , L. A. Expression of IgD by murine lymphocytes. Loss of surface IgD indicates maturation of memory B cells. J. Exp. Med. 147 , 984-996 ( 1978 ).
31. Fehr , T. et al. Antiviral protection and germinal center formation, but impaired B cell memory in the absence of CD19. J. Exp. Med. 1 88 , 145-155 ( 1998 ).
32. Takahashi , Y. et al. Novel role of the Ras cascade in memory B cell response. Immunity 2 3 , 127-138 ( 2005 ).
33. Arpin , C. et al. Generation of memory B cells and plasma cells i n vitro. Science 268 , 720-722 ( 1995 ).
34. Choe , J. , Kim , H.S. , Zhang , X. , Armitage , R. J. & Choi , Y. S. Cellular and molecular factors that regulate the diff erentiation and apoptosis of germinal center B cells. Anti-Ig down-regulates Fas expression of CD40 ligandstimulated germinal center B cells and inhibits Fas-mediated apoptosis. J. Immunol. 1 57 , 1006-1016 ( 1996 ).
35. Choe , J. , Kim , H. S. , Armitage , R. J. & Choi , Y. S. The functional role of B cell antigen receptor stimulation and IL-4 in the generation of human memory B cells from germinal center B cells. J. Immunol. 159 , 3757-3766 ( 1997 ).
36. Allen , C. D. et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 5 , 943-952 ( 2004 ).
37. Reif , K. et al. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 416 , 94-99 ( 2002 ).
38. Vikstrom , I. et al. Mcl-1 is essential for germinal center formation and B cell memory. Science 330 , 1095-1099 ( 2010 ).
39. Schittek , B. & Rajewsky , K. Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature 3 46 , 749-751 ( 1990 ).
40. Allen , C. D. , Okada , T. , Tang , H. L. & Cyster , J. G. Imaging of germinal center selection events during affi nity maturation. Science 3 15 , 528-531 ( 2007 ).
41. Phan , T. G. , Green , J. A. , Gray , E. E. , Xu , Y. & Cyster , J. G. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affi nity maturation. Nat. Immunol. 1 0 , 786-793 ( 2009 ).
42. Lam , K. P. , Kuhn , R. & Rajewsky , K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 9 0 , 1073-1083 ( 1997 ).
43. Benson , M. J. et al. Distinction of the memory B cell response to cognate antigen versus bystander infl ammatory signals. J. Exp. Med. 2 06 , 2013-2025 ( 2009 ).
44. Jin , H. , Carrio , R. , Yu , A. & Malek , T. R. Distinct activation signals determine whether IL-21 induces B cell costimulation, growth arrest, or Bim-dependent apoptosis. J. Immunol. 1 73 , 657-665 ( 2004 ).
45. Kasaian , M. T. et al. IL-21 limits NK cell responses and promotes antigenspecifi c T cell activation: A mediator of the transition from innate to adaptive immunity. I mmunity 1 6 , 559-569 ( 2002 ).
46. Rajewsky , K. , Forster , I. & Cumano , A. Evolutionary and somatic selection of the antibody repertoire in the mouse. Science 2 38 , 1088-1094 ( 1987 ).
47. Casali , P. , Pal , Z. , Xu , Z. & Zan , H. DNA repair in antibody somatic hypermutation. T rends Immunol. 2 7 , 313-321 ( 2006 ).
48. Good , K. L. , Bryant , V. L. & Tangye , S. G. Kinetics of human B cell behavior and amplifi cation of proliferative responses following stimulation with IL-21. J. Immunol. 177 , 5236-5247 ( 2006 ).
49. O ' Connor , B. P. , Cascalho , M. & Noelle , R. J. Short-lived and long-lived bone marrow plasma cells are derived from a novel precursor population. J. Exp. Med. 1 95 , 737-745 ( 2002 ).
50. Kwakkenbos , M. J. et al. Generation of stable monoclonal antibody-producing B cell receptor-positive human memory B cells by genetic programming. Nat. Med. 16 , 123-128 ( 2010 ).
51. Allman , D. et al. BCL-6 expression during B-cell activation. B lood 87 , 5257-5268 ( 1996 ).
52. Saito , M. et al. A signaling pathway mediating downregulation of BCL6 in germinal center B cells is blocked by BCL6 gene alterations in B cell lymphoma. Cancer Cell 1 2 , 280-292 ( 2007 ).
53. Shaff er , A. L. et al. Blimp-1 orchestrates plasma cell diff erentiation by extinguishing the mature B cell gene expression program. I mmunity 1 7 , 51-62 ( 2002 ).
54. Ridderstad , A. & Tarlinton , D. M. B cell memory in xid mice is long-lived despite reduced memory B cell frequency. S cand. J. Immunol. 4 5 , 655-659 ( 1997 ).
55. Yamamoto , M. et al. BASH-deficient mice: Limited primary repertoire and antibody formation, but suffi cient affi nity maturation and memory B cell generation, in anti-NP response. Int. Immunol. 16 , 1161-1171 ( 2004 ).
56. Inamine , A. et al. Two waves of memory B-cell generation in the primary immune response. Int. Immunol. 17 , 581-589 ( 2005 ).
57. Morimura , T. et al. Cell cycle arrest and apoptosis induced by Notch1 in B cells. J. Biol. Chem. 2 75 , 36523-36531 ( 2000 ).
58. Oda , M. et al. Evaluation of the conformational equilibrium of reduced hen egg lysozyme by antibodies to the native form. A rch. Biochem. Biophys. 494 , 145-150 ( 2010 ).
59. Terauchi , A. et al. A pivotal role for DNase I-sensitive regions 3b and/or 4 in the induction of somatic hypermutation of IgH genes. J. Immunol. 167 , 811-820 (2001).