Memory B cells: Effectors of long-lived immune responses (European Journal of Immunology (2009) 39, (8) DOI 10.1002/eji.200939531);Memory B cells: Effectors of long-lived immune responses

European Journal of Immunology

Volumn 39, Issue 8, 2009, Pages 2065-2075

  Tangye, Stuart G ^a   Tarlinton, David M ^b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

B cells; Cell differentiation; Memory cells

Indexed keywords

ANTIGEN; CYTOKINE; TRANSCRIPTION FACTOR;

ANTIGEN EXPRESSION; B LYMPHOCYTE DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL ISOLATION; CELL SURVIVAL; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; IN VITRO STUDY; IN VIVO STUDY; LONGEVITY; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; MICROARRAY ANALYSIS; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW; SOMATIC MUTATION; ANIMAL; B LYMPHOCYTE; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; GERMINAL CENTER; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MUTATION;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; GENE EXPRESSION; GERMINAL CENTER; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; MODELS, BIOLOGICAL; MUTATION;

EID: 70249085594     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200990326     Document Type: Erratum

References (102)

1. Rajewsky, K., Clonal selection and learning in the antibody system. Nature 1996. 381: 751-758. (Pubitemid 26243107)
2. Ahmed, R. and Gray, D., Immunological memory and protective immunity: understanding their relation. Science 1996. 272: 54-60. (Pubitemid 26110754)
3. McHeyzer-Williams, L. J. and McHeyzer-Williams, M. G., Antigen-specific memory B cell development. Annu. Rev. Immunol. 2005. 23: 487-513.
4. Tarlinton, D., B-cell memory: are subsets necessary? Nat. Rev. Immunol. 2006. 6: 785-790.
5. Liu, Y. J. and Banchereau, J., The paths and molecular controls of peripheral B-cell development. The Immunologist 1996. 4: 55-66.
6. Vieira, P. and Rajewsky, K., Persistence of memory B cells in mice deprived of T cell help. Int. Immunol. 1990. 2: 487-494.
7. Coffman, R. L. and Cohn, M., The class of surface immunoglobulin on virgin and memory B lymphocytes. J. Immunol. 1977. 118: 1806-1815. (Pubitemid 8097384)
8. Jelinek, D. F., Splawski, J. B. and Lipsky, P. E., Human peripheral blood B lymphocyte subpopulations: functional and phenotypic analysis of surface IgD positive and negative subsets. J. Immunol. 1986. 136: 83-92.
9. Pascual, V., Liu, Y. J., Magalski, A., de Bouteiller, O., Banchereau, J. and Capra, J. D., Analysis of somatic mutation in five B cell subsets of human tonsil. J. Exp. Med. 1994. 180: 329-339.
10. Liu, Y. J., Barthelemy, C., de Bouteiller, O., Arpin, C., Durand, I. and Banchereau, J., 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. Immunity 1995. 2: 239-248.
11. Schittek, B. and Rajewsky, K., Maintenance of B-cell memory by long-lived cells generated from proliferating precursors. Nature 1990. 346: 749-751. (Pubitemid 20251088)
12. Hayakawa, K., Ishii, R., Yamasaki, K., Kishimoto, T. and Hardy, R. R., Isolation of high-affinity memory B cells: phycoerythrin as a probe for antigen-binding cells. Proc. Natl. Acad. Sci. USA 1987. 84: 1379-1383.
13. Leyendeckers, H., Odendahl, M., Lohndorf, A., Irsch, J., Spangfort, M., Miltenyi, S.,Hunzelmann, N. et al., Correlation analysis between frequencies of circulating antigen-specific IgG-bearing memory B cells and serum titers of antigen-specific IgG. Eur. J. Immunol. 1999. 29: 1406-1417.
14. Rojas, O. L., Narvaez, C. F., Greenberg, H. B., Angel, J. and Franco, M. A., Characterization of rotavirus specific B cells and their relation with serological memory. Virology 2008. 380: 234-242.
15. Schittek, B. and Rajewsky, K., Natural occurrence and origin of somatically mutated memory B cells in mice. J. Exp. Med. 1992. 176: 427-438.
16. Klein, U., Rajewsky, K. and Kuppers, R., Human immunoglobulin (Ig)M+ IgD+peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 1998. 188: 1679-1689.
17. Tangye, S. G., Liu, Y. J., Aversa, G., Phillips, J. H. and de Vries, J. E., Identification of functional human splenic memory B cells by expression of CD148 and CD27. J. Exp. Med. 1998. 188: 1691-1703.
18. Ellyard, J. I., Avery, D. T., Phan, T. G., Hare, N. J., Hodgkin, P. D. and Tangye, S. G., Antigen-selected, immunoglobulin-secreting cells persist in human spleen and bone marrow. Blood 2004. 103: 3805-3812. (Pubitemid 38596299)
19. Arpin, C., Banchereau, J. and Liu, Y. J., Memory B cells are biased towards terminal differentiation: a strategy that may prevent repertoire freezing. J. Exp. Med. 1997. 186: 931-940.
20. Kindler, V. and Zubler, R. H., 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. J. Immunol. 1997. 159: 2085-2090. (Pubitemid 127680995)
21. Bernasconi, N. L., Onai, N. and Lanzavecchia, A., 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. Blood 2003. 101: 4500-4504. (Pubitemid 36857820)
22. Bernasconi, N. L., Traggiai, E. and Lanzavecchia, A., Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002. 298: 2199-2202. (Pubitemid 35471246)
23. Bryant, V. L., Ma, C. S., Avery, D. T., Li, Y., Good, K. L., Corcoran, L. M., de Waal Malefyt, R. et al., Cytokine-mediated regulation of human B cell differentiation into Ig-secreting cells: predominant role of IL-21 produced by CXCR5+T follicular helper cells. J. Immunol. 2007. 179: 8180-8190.
24. Good, K. L., Bryant, V. L. and Tangye, S. G., Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J. Immunol. 2006. 177: 5236-5247.
25. Tangye, S. G., Avery, D. T., Deenick, E. K. and Hodgkin, P. D., Intrinsic differences in the proliferation of naive and memory human B cells as a mechanism for enhanced secondary immune responses. J. Immunol. 2003. 170: 686-694.
26. Tangye, S. G., Avery, D. T. and Hodgkin, P. D., A division-linked mechanism for the rapid generation of Ig-secreting cells from human memory B cells. J. Immunol. 2003. 170: 261-269.
27. Tangye, S. G. and Good, K. L., Human IgM+CD27+B cells: memory B cells or "memory" B cells? J. Immunol. 2007. 179: 13-19.
28. Good, K. L. and Tangye, S. G., Decreased expression of Kruppel-like factors in memory B cells induces the rapid response typical of secondary antibody responses. Proc. Natl. Acad. Sci. USA 2007. 104: 13420-13425.
29. Klein,U., Kuppers, R. and Rajewsky, K., Evidence for a large compartment of IgM-expressing memory B cells in humans. Blood 1997. 89: 1288-1298. (Pubitemid 27079993)
30. White, H. and Gray, D., Analysis of immunoglobulin (Ig) isotype diversity and IgM/D memory in the response to phenyl-oxazolone. J. Exp. Med. 2000. 191: 2209-2220.
31. Dunn-Walters, D. K., Isaacson, P. G. and Spencer, J., Analysis of mutations in immunoglobulin heavy chain variable region genes of microdissected marginal zone (MGZ) B cells suggests that the MGZ of human spleen is a reservoir of memory B cells. J. Exp. Med. 1995. 182: 559-566.
32. Insel, R. A., Varade, W. S. and Marin, E., Human splenic IgM immunoglobulin transcripts are mutated at high frequency. Mol. Immunol. 1994. 31: 383-392.
33. Paramithiotis, E. and Cooper, M. D., Memory B lymphocytes migrate to bone marrow in humans. Proc. Natl. Acad. Sci. USA 1997. 94: 208-212.
34. Weller, S., Faili, A., Garcia, C., Braun, M. C., Le Deist, F. F., de Saint Basile, G. G., Hermine, O. et al., CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans. Proc. Natl. Acad. Sci. USA 2001. 98: 1166-1170.
35. Weller, S., Braun, M. C., Tan, B. K., Rosenwald, A., Cordier, C., Conley, M. E., Plebani, A. et al., Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 2004. 104: 3647-3654.
36. Warnatz, K., Bossaller, L., Salzer, U., Skrabl-Baumgartner, A., Schwinger, W., van der Burg, M., van Dongen, J. J. et al., Human ICOS deficiency abrogates the germinal center reaction and provides a monogenic model for common variable immunodeficiency. Blood 2006. 107: 3045-3052.
37. Ma, C. S., Pittaluga, S., Avery, D. T., Hare, N. J., Maric, I., Klion, A. D., Nichols, K. E. et al., Selective generation of functional somatically mutated IgM+CD27+, but not Ig isotype-switched, memory B cells in X-linked lymphoproliferative disease. J. Clin. Invest. 2006. 116: 322-333.
38. Kruetzmann, S., Rosado, M. M., Weber, H., Germing, U., Tournilhac, O., Peter, H. H., Berner, R. et al., Human immunoglobulin M memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J. Exp. Med. 2003. 197: 939-945.
39. Weller, S., Mamani-Matsuda, M., Picard, C., Cordier, C., Lecoeuche, D., Gauthier, F., Weill, J. C. et al., Somatic diversification in the absence of antigen-driven responses is the hallmark of the IgM+IgD+CD27+B cell repertoire in infants. J. Exp. Med. 2008. 205: 1331-1342.
40. Scheeren, F. A., Nagasawa, M., Weijer, K., Cupedo, T., Kirberg, J., Legrand, N. and Spits, H., T cell-independent development and induction of somatic hypermutation in human IgM+IgD+CD27+B cells. J. Exp. Med. 2008. 205: 2033-2042.
41. Moens, L., Wuyts, M., Meyts, I., De Boeck, K. and Bossuyt, X., Human memory B lymphocyte subsets fulfill distinct roles in the antipolysaccharide and anti-protein immune response. J. Immunol. 2008. 181: 5306-5312.
42. Tsuiji, M., Yurasov, S., Velinzon, K., Thomas, S., Nussenzweig, M. C. and Wardemann, H., A checkpoint for autoreactivity in human IgM+ memory B cell development. J. Exp. Med. 2006. 203: 393-400.
43. Wirths, S. and Lanzavecchia, A., ABCB1 transporter discriminates human resting naive B cells from cycling transitional and memory B cells. Eur. J. Immunol. 2005. 35: 3433-3441.
44. Fecteau, J. F., Cote, G. and Neron, S., A new memory CD27-IgG+B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J. Immunol. 2006. 177: 3728-3736.
45. Wei, C., Anolik, J., Cappione, A., Zheng, B., Pugh-Bernard, A., Brooks, J., Lee, E. H. et al., A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J. Immunol. 2007. 178: 6624-6633. (Pubitemid 46717447)
46. Ehrhardt, G. R., Davis, R. S., Hsu, J. T., Leu, C. M., Ehrhardt, A. and Cooper, M. D., The inhibitory potential of Fc receptor homolog 4 on memory B cells. Proc. Natl. Acad. Sci. USA 2003. 100: 13489-13494.
47. Ehrhardt, G. R., Hsu, J. T., Gartland, L., Leu, C. M., Zhang, S., Davis, R. S. and Cooper, M. D., Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J. Exp. Med. 2005. 202: 783-791.
48. Polson, A. G., Zheng, B., Elkins, K., Chang, W., Du, C., Dowd, P., Yen, L. et al., Expression pattern of the human FcRH/IRTA receptors in normal tissue and in B-chronic lymphocytic leukemia. Int. Immunol. 2006. 18: 1363-1373.
49. Moir, S., Ho, J., Malaspina, A., Wang, W., DiPoto, A. C., O'Shea, M. A., Roby, G. et al., Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 2008. 205: 1797-1805.
50. Anderson, S. M., Tomayko, M. M., Ahuja, A., Haberman, A. M. and Shlomchik, M. J., New markers for murine memory B cells that define mutated and unmutated subsets. J. Exp. Med. 2007. 204: 2103-2114.
51. Mamani-Matsuda, M., Cosma, A.,Weller, S., Faili, A., Staib, C., Garcon, L., Hermine, O. et al., The human spleen is a major reservoir for long-lived vaccinia virus-specific memory B cells. Blood 2008. 111: 4653-4659.
52. Ma, C. S., Hare, N. J., Nichols, K. E., Dupre, L., Andolfi, G., Roncarolo, M. G., Adelstein, S. et al., Impaired humoral immunity in X-linked lymphoproliferative disease is associated with defective IL-10 production by CD4+T cells. J. Clin. Invest. 2005. 115: 1049-1059.
53. Horikawa, K., Martin, S. W., Pogue, S. L., Silver, K., Peng, K., Takatsu, K. and Goodnow, C. C., Enhancement and suppression of signaling by the conserved tail of IgG memory-type B cell antigen receptors. J. Exp. Med. 2007. 204: 759-769.
54. Martin, S. W. and Goodnow, C. C., Burst-enhancing role of the IgG membrane tail as a molecular determinant of memory. Nat. Immunol. 2002. 3: 182-188.
55. Good, K. L., Avery, D. T. and Tangye, S. G., Resting human memory B cells are intrinsically programmed for enhanced survival and responsiveness to diverse stimuli compared to naive B cells. J. Immunol. 2009. 182: 890-901.
56. Bhattacharya, D., Cheah, M. T., Franco, C. B., Hosen, N., Pin, C. L., Sha, W. C. and Weissman, I. L., Transcriptional profiling of antigen-dependent murine B cell differentiation and memory formation. J. Immunol. 2007. 179: 6808-6819.
57. Klein, U., Tu, Y., Stolovitzky, G. A., Keller, J. L., Haddad J., Jr., Milijkovic, V., Cattoretti, G. et al., Transcriptional analysis of the B cell germinal center reaction. Proc. Natl. Acad. Sci. USA 2003. 100: 2639-2644.
58. Ehrhardt, G. R., Hijikata, A., Kitamura, H., Ohara, O., Wang, J. Y. and Cooper, M. D., Discriminating gene expression profiles of memory B cell subpopulations. J. Exp. Med. 2008. 205: 1807-1817.
59. Kuo, T. C., Shaffer, A. L., Haddad J., Jr., Choi, Y. S., Staudt, L. M. and Calame, K., Repression of BCL-6 is required for the formation of human memory B cells in vitro. J. Exp. Med. 2007. 204: 819-830.
60. Tomayko, M. M., Anderson, S. M., Brayton, C. E., Sadanand, S., Steinel, N. C., Behrens, T. W. and Shlomchik, M. J., Systematic comparison of gene expression between murine memory and naive B cells demonstrates that memory B cells have unique signaling capabilities. J. Immunol. 2008. 181: 27-38.
61. Hammarlund, E., Lewis, M.W., Hansen, S. G., Strelow, L. I., Nelson, J. A., Sexton, G. J., Hanifin, J. M. et al., Duration of antiviral immunity after smallpox vaccination. Nat. Med. 2003. 9: 1131-1137.
62. Crotty, S., Felgner, P., Davies, H., Glidewell, J., Villarreal, L. and Ahmed, R., Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 2003. 171: 4969-4973. (Pubitemid 37432774)
63. Gray, D. and Skarvall, H., B-cell memory is short-lived in the absence of antigen. Nature 1988. 336: 70-73. (Pubitemid 18262136)
64. Maruyama, M., Lam, K. P. and Rajewsky, K., Memory B-cell persistence is independent of persisting immunizing antigen. Nature 2000. 407: 636-642. (Pubitemid 30775375)
65. Macallan, D. C., Wallace, D. L., Zhang, Y., Ghattas, H., Asquith, B., de Lara, C., Worth, A. et al., B-cell kinetics in humans: rapid turnover of peripheral blood memory cells. Blood 2005. 105: 3633-3640. (Pubitemid 40628210)
66. Scheeren, F. A., Naspetti, M., Diehl, S., Schotte, R., Nagasawa, M., Wijnands, E., Gimeno, R. et al., STAT5 regulates the self-renewal capacity and differentiation of human memory B cells and controls Bcl-6 expression. Nat. Immunol. 2005. 6: 303-313.
67. Tangye, S. G., Bryant, V. L., Cuss, A. K. and Good, K. L., BAFF, APRIL and human B cell disorders. Semin. Immunol. 2006. 18: 305-317.
68. Salzer, U., Bacchelli, C., Buckridge, S., Pan-Hammarstrom, Q., Jennings, S., Lougaris, V., Bergbreiter, A. et al., Relevance of biallelic versus monoallelic TNFRSF13B mutations in distinguishing disease-causing from risk-increasing TNFRSF13B variants in antibody deficiency syndromes. Blood 2009. 113: 1967-1976.
69. Vugmeyster, Y., Seshasayee, D., Chang, W., Storn, A., Howell, K., Sa, S., Nelson, T. et al., A soluble BAFF antagonist, BR3-Fc, decreases peripheral blood B cells and lymphoid tissue marginal zone and follicular B cells in cynomolgus monkeys. Am. J. Pathol. 2006. 168: 476-489.
70. Benson, M. J., Dillon, S. R., Castigli, E., Geha, R. S., Xu, S., Lam, K. P. and Noelle, R. J., Cutting edge: the dependence of plasma cells and independence of memory B cells on BAFF and APRIL. J. Immunol. 2008. 180: 3655-3659.
71. Scholz, J. L., Crowley, J. E., Tomayko, M. M., Steinel, N., O'Neill, P. J., Quinn W. J., III, Goenka, R. et al., BLyS inhibition eliminates primary B cells but leaves natural and acquired humoral immunity intact. Proc. Natl. Acad. Sci. USA 2008. 105: 15517-15522.
72. Jain, A., Ma, C. A., Lopez-Granados, E., Means, G., Brady, W., Orange, J. S., Liu, S. et al., Specific NEMO mutations impair CD40-mediated c-Rel activation and B cell terminal differentiation. J. Clin. Invest. 2004. 114: 1593-1602.
73. van Zelm, M. C., Reisli, I., van der Burg, M., Castano, D., van Noesel, C. J., van Tol, M. J., Woellner, C. et al., An antibody-deficiency syndrome due to mutations in the CD19 gene. N. Engl. J. Med. 2006. 354: 1901-1912.
74. Kanegane, H., Agematsu, K., Futatani, T., Sira, M. M., Suga, K., Sekiguchi, T., van Zelm, M. C. et al., Novel mutations in a Japanese patient with CD19 deficiency. Genes Immun. 2007. 8: 663-670. (Pubitemid 350238436)
75. Anolik, J. H., Ravikumar, R., Barnard, J., Owen, T., Almudevar, A., Milner, E. C., Miller, C. H. et al., Cutting edge: anti-tumor necrosis factor therapy in rheumatoid arthritis inhibits memory B lymphocytes via effects on lymphoid germinal centers and follicular dendritic cell networks. J. Immunol. 2008. 180: 688-692.
76. Casola, S., Cattoretti, G., Uyttersprot, N., Koralov, S. B., Seagal, J., Hao, Z., Waisman, A. et al., Tracking germinal center B cells expressing germline immunoglobulin gamma1 transcripts by conditional gene targeting. Proc. Natl. Acad. Sci. USA 2006. 103: 7396-7401.
77. Kwon, K., Hutter, C., Sun, Q., Bilic, I., Cobaleda, C., Malin, S. and Busslinger, M., Instructive role of the transcription factor E2A in early B lymphopoiesis and germinal center B cell development. Immunity 2008. 28: 751-762.
78. Klein, U., Casola, S., Cattoretti, G., Shen, Q., Lia, M., Mo, T., Ludwig, T. et al., Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 2006. 7: 773-782.
79. Hikida, M., Casola, S., Takahashi, N., Kaji, T., Takemori, T., Rajewsky, K. and Kurosaki, T., PLC-gamma2 is essential for formation and maintenance of memory B cells. J. Exp. Med. 2009. 206: 681-689.
80. Schenten, D., Kracker, S., Esposito, G., Franco, S., Klein, U., Murphy, M., Alt, F. W. et al., Pol zeta ablation in B cells impairs the germinal center reaction, class switch recombination, DNA break repair, and genome stability. J. Exp. Med. 2009. 206: 477-490.
81. Smith, K. G., Nossal, G. J. and Tarlinton, D. M., FAS is highly expressed in the germinal center but is not required for regulation of the B-cell response to antigen. Proc. Natl. Acad. Sci. USA 1995. 92: 11628-11632.
82. Takahashi, Y., Ohta, H. and Takemori, T., Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 2001. 14: 181-192. (Pubitemid 32206520)
83. Hao, Z., Duncan, G. S., Seagal, J., Su, Y. W., Hong, C., Haight, J., Chen, N. J. et al., Fas receptor expression in germinal-center B cells is essential for T and B lymphocyte homeostasis. Immunity 2008. 29: 615-627.
84. Takahashi, Y., Inamine, A., Hashimoto, S., Haraguchi, S., Yoshioka, E., Kojima, N., Abe, R. et al., Novel role of the Ras cascade in memory B cell response. Immunity 2005. 23: 127-138. (Pubitemid 41169283)
85. Sakaguchi, N., Kimura, T., Matsushita, S., Fujimura, S., Shibata, J., Araki, M., Sakamoto, T. et al., Generation of high-affinity antibody against T cell-dependent antigen in the Ganp gene-transgenic mouse. J. Immunol. 2005. 174: 4485-4494. (Pubitemid 40504527)
86. Kuwahara, K., Fujimura, S., Takahashi, Y., Nakagata, N., Takemori, T., Aizawa, S. and Sakaguchi, N., Germinal center-associated nuclear protein contributes to affinity maturation of B cell antigen receptor in T cell-dependent responses. Proc. Natl. Acad. Sci. USA 2004. 101: 1010-1015.
87. Schmidlin, H., Diehl, S. A., Nagasawa, M., Scheeren, F. A., Schotte, R., Uittenbogaart, C. H., Spits, H. et al., Spi-B inhibits human plasma cell differentiation by repressing BLIMP1 and XBP-1 expression. Blood 2008. 112: 1804-1812.
88. Xiao, C. and Rajewsky, K., MicroRNA control in the immune system: basic principles. Cell 2009. 136: 26-36.
89. Rodriguez, A., Vigorito, E., Clare, S.,Warren, M. V., Couttet, P., Soond, D. R., van Dongen, S. et al., Requirement of bic/microRNA-155 for normal immune function. Science 2007. 316: 608-611. (Pubitemid 46683148)
90. Thai, T. H., Calado, D. P., Casola, S., Ansel, K. M., Xiao, C., Xue, Y., Murphy, A. et al., Regulation of the germinal center response by microRNA-155. Science 2007. 316: 604-608. (Pubitemid 46683147)
91. Vigorito, E., Perks, K. L., Abreu-Goodger, C., Bunting, S., Xiang, Z., Kohlhaas, S., Das, P. P. et al., microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 2007. 27: 847-859. (Pubitemid 350258623)
92. Dorsett, Y., McBride, K. M., Jankovic, M., Gazumyan, A., Thai, T. H., Robbiani, D. F., Di Virgilio, M. et al., MicroRNA-155 suppresses activation-induced cytidine deaminase-mediated Myc-Igh translocation. Immunity 2008. 28: 630-638.
93. Teng, G., Hakimpour, P., Landgraf, P., Rice, A., Tuschl, T., Casellas, R. and Papavasiliou, F. N., MicroRNA-155 is a negative regulator of activation-induced cytidine deaminase. Immunity 2008. 28: 621-629.
94. de Yebenes, V. G., Belver, L., Pisano, D. G., Gonzalez, S., Villasante, A., Croce, C., He, L. et al., miR-181b negatively regulates activation-induced cytidine deaminase in B cells. J. Exp. Med. 2008. 205: 2199-2206.
95. Tan, L. P.,Wang, M., Robertus, J. L., Schakel, R. N., Gibcus, J. H., Diepstra, A., Harms, G. et al., miRNA profiling of B-cell subsets: specific miRNA profile for germinal center B cells with variation between centroblasts and centrocytes. Lab Invest. 2009. 89: 708-716
96. Zhang, J., Jima, D. D., Jacobs, C., Fischer, R., Gottwein, E., Huang, G., Lugar, P. L. et al., Patterns of microRNA expression characterize stages of human B cell differentiation. Blood 2009. 113: 4586-4594
97. Pichiorri, F., Suh, S. S., Ladetto, M., Kuehl, M., Palumbo, T., Drandi, D., Taccioli, C. et al., MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc. Natl. Acad. Sci. USA 2008. 105: 12885-12890.
98. Tarlinton, D., Radbruch, A., Hiepe, F. and Dorner, T., Plasma cell differentiation and survival. Curr. Opin. Immunol. 2008. 20: 162-169.
99. Lee, C. H., Melchers, M., Wang, H., Torrey, T. A., Slota, R., Qi, C. F., Kim, J. Y. et al., Regulation of the germinal center gene program by interferon (IFN) regulatory factor 8/IFN consensus sequence-binding protein. J. Exp. Med. 2006. 203: 63-72.
100. Arguni, E., Arima, M., Tsuruoka, N., Sakamoto, A., Hatano, M. and Tokuhisa, T., JunD/AP-1 and STAT3 are the major enhancer molecules for high Bcl6 expression in germinal center B cells. Int. Immunol. 2006. 18: 1079-1089.
101. Saito, M., Gao, J., Basso, K., Kitagawa,Y., Smith, P. M., Bhagat, G., Pernis, A. 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 2007. 12: 280-292. (Pubitemid 47333420)
102. Allen, C. D., Okada, T. and Cyster, J. G., Germinal-center organization and cellular dynamics. Immunity 2007. 27: 190-202.