Human IgM+CD27+ B cells: Memory B cells or "memory" B cells?

Journal of Immunology

Volumn 179, Issue 1, 2007, Pages 13-19

  Tangye, Stuart G ^a   Good, Kim L ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; IMMUNOGLOBULIN; IMMUNOGLOBULIN M;

ANTIGEN EXPRESSION; GENE EXPRESSION; GERMINAL CENTER; HUMAN; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; IMMUNOGLOBULIN VARIABLE REGION; LYMPHOCYTE FUNCTION; MEMORY CELL; PRIORITY JOURNAL; SHORT SURVEY; T LYMPHOCYTE;

EID: 34250883267     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.179.1.13     Document Type: Short Survey

References (84)

1. Weiss, U., and K. Rajewsky. 1990. The repertoire of somatic antibody mutants accumulating in the memory compartment after primary immunization is restricted through affinity maturation and mirrors that expressed in the secondary response. J. Exp. Med. 172: 1681-1689.
2. Berek, C., A. Berger, and M. Apel. 1991. Maturation of the immune response in germinal centers. Cell 67: 1121-1129.
3. McHeyzer-Williams, L. J., and M. G. McHeyzer-Williams. 2005. Antigen-specific memory B cell development. Annu. Rev. Immunol. 23: 487-513.
4. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science 272: 54-60.
5. Liu, Y. J., and J. Banchereau. 1996. The paths and molecular controls of peripheral B-cell development. Immunologist 4: 55-66.
6. Yuan, D., E. S. Vitetta, and J. R. Kettman. 1977. Cell surface immunoglobulin. XX. Antibody responsiveness of subpopulations of B lymphocytes bearing different isotypes. J. Exp. Med. 145: 1421-1435.
7. Coffman, R. L., and M. Cohn. 1977. The class of surface immunoglobulin on virgin and memory B lymphocytes. J. Immunol. 118: 1806-1815.
8. Yefenof, E., V. M. Sanders, E. C. Snow, R. J. Noelle, K. G. Oliver, J. W. Uhr, and E. S. Vitetta. 1985. Preparation and analysis of antigen-specific memory B cells. J. Immunol. 135: 3777-3784.
9. Yefenof, E., V. M. Sanders, J. W. Uhr, and E. S. Vitetta. 1986. In vitro activation of murine antigen-specific memory B cells by a T-dependent antigen. J. Immunol. 137: 85-90.
10. Jelinek, D. F., J. B. Splawski, and P. E. Lipsky. 1986. Human peripheral blood B lymphocyte subpopulations: functional and phenotypic analysis of surface IgD positive and negative subsets. J. Immunol. 136: 83-92.
11. Pascual, V., Y. J. Liu, A. Magalski, O. de Bouteiller, J. Banchereau, and J. D. Capra. 1994. Analysis of somatic mutation in five B cell subsets of human tonsil. J. Exp. Med. 180: 329-339.
12. + 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. 188: 1679-1689.
13. Tangye, S. G., Y. J. Liu, G. Aversa, J. H. Phillips, and J. E. de Vries. 1998. Identification of functional human splenic memory B cells by expression of CD148 and CD27. J. Exp. Med. 188: 1691-1703.
14. Maurer, D., W. Holter, O. Majdic, G. F. Fischer, and W. Knapp. 1990. CD27 expression by a distinct subpopulation of human B lymphocytes. Eur. J. Immunol. 20: 2679-2684.
15. + B lymphocyte subset. J. Immunol. 148: 3700-3705.
16. + B cells and helper T cells in immunoglobulin production. Eur. J. Immunol. 27: 2073-2079.
17. Lagresle, C., C. Bella, and T. Defrance. 1993. Phenotypic and functional heterogeneity of the IgD-B cell compartment: identification of two major tonsillar B cell subsets. Int. Immunol. 5: 1259-1268.
18. Liu, Y. J., C. Barthelemy, O. de Bouteiller, C. Arpin, I. Durand, and J. Banchereau. 1995. 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 2: 239-248.
19. Arpin, C., J. Banchereau, and Y. J. Liu. 1997. Memory B cells are biased towards terminal differentiation: a strategy that may prevent repertoire freezing. J. Exp. Med. 186: 931-940.
20. Kindler, V., and R. H. Zubler. 1997. 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. 159: 2085-2090.
21. Tangye, S. G., D. T. Avery, and P. D. Hodgkin. 2003. A division-linked mechanism for the rapid generation of Ig-secreting cells from human memory B cells. J. Immunol. 170: 261-269.
22. Tangye, S. G., D. T. Avery, E. K. Deenick, and P. D. Hodgkin. 2003. Intrinsic differences in the proliferation of naive and memory human B cells as a mechanism for enhanced secondary immune responses. J. Immunol. 170: 686-694.
23. Weller, S., A. Faili, C. Garcia, M. C. Braun, F. F. Le Deist, G. G. de Saint Basile, O. Hermine, A. Fischer, C. A. Reynaud, and J. C. Weill. 2001. CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans. Proc. Natl. Acad. Sci. USA 98: 1166-1170.
24. Weller, S., M. C. Braun, B. K. Tan, A. Rosenwald, C. Cordier, M. E. Conley, A. Plebani, D. S. Kumararatne, D. Bonnet, O. Tournilhac, et al. 2004. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104: 3647-3654.
25. Kuppers, R., M. Zhao, M. L. Hansmann, and K. Rajewsky. 1993. Tracing B cell development in human germinal centres by molecular analysis of single cells picked from histological sections. EMBO J. 12: 4955-4967.
26. Klein, U., R. Kuppers, and K. Rajewsky. 1994. Vatiable region gene analysis of B cell subsets derived from a 4-year-old child: somatically mutated memory B cells accumulate in the peripheral blood already at young age. J. Exp. Med. 180: 1383-1393.
27. + B cells, the major B cell subset in the peripheral blood, express V kappa genes with no or little somatic mutation throughout life. Eur. J. Immunol. 23: 3272-3277.
28. Klein, U., R. Kuppers, and K. Rajewsky. 1997. Evidence for a large compartment of IgM-expressing memory B cells in humans. Blood 89: 1288-1298.
29. Insel, R. A., W. S. Varade, and E. Marin. 1994. Human splenic IgM immunoglobulin transcripts are mutated at high frequency. Mol. Immunol. 31: 383-392.
30. van es, J. H., F. H. Meyling, and T. Logtenberg. 1992. High frequency of somatically mutated IgM molecules in the human adult blood B cell repertoire. Eur. J. Immunol. 22: 2761-2764.
31. Zan-Bar, I., S. Strober, and E. S. Vitetta. 1979. The relationship between surface immunoglobulin isotype and immune function of murine B lymphocytes. IV. Role of IgD-bearing cells in the propagation of immunologic memory. J. Immunol. 123: 925-930.
32. Lafrenz, D., S. Strober, and E. Vitetta. 1981. The relationship between surface immunoglobulin isotype and the immune function of murine B lymphocytes. V. High affinity secondary antibody responses are transferred by both IgD-positive and IgD-negative memory B cells. J. Immunol. 127: 867-872.
33. White, H., and D. Gray. 2000. Analysis of immunoglobulin (Ig) isotype diversity and IgM/D memory in the response to phenyl-oxazolone. J. Exp. Med. 191: 2209-2220.
34. Soenawan, E., I. Srivastava, S. Gupta, E. Kan, R. Janani, J. Kazzaz, M. Singh, V. Shreedhar, and M. Vajdy. 2004. Maintenance of long-term immunological memory by low avidity IgM-secreting cells in bone marrow after mucosal immunizations with cholera toxin adjuvant. Vaccine 22: 1553-1563.
35. Tangye, S. G., B. C. van de Weerdt, D. T. Avery, and P. D. Hodgkin. 2002. CD84 is up-regulated on a major population of human memory B cells and recruits the SH2 domain containing proteins SAP and EAT-2. Eur. J. Immunol. 32: 1640-1649.
36. Tangye, S. G., and P. D. Hodgkin. 2004. Divide and conquer: the importance of cell division in regulating B-cell responses. Immunology 112: 509-520.
37. Zandvoort, A., M. E. Lodewijk, N. K. de Boer, P. M. Dammers, F. G. Kroese, and W. Timens. 2001, CD27 expression in the human splenic marginal zone: the infant marginal zone is populated by naive B cells. Tissue Antigens 58: 234-242.
38. Dunn-Walters, D. K., P. G. Isaacson, and J. Spencer. 1995. 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. 182: 559-566.
39. Liu, Y. J., S. Oldfield, and I. C. MacLennan. 1988. Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones. Eur. J. Immunol. 18: 355-362.
40. Crotty, S., R. D. Aubert, J. Glidewell, and R. Ahmed. 2004. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J. Immunol. Methods 286: 111-122.
41. Ehrhardt, G. R., J. T. Hsu, L. Gartland, C. M. Leu, S. Zhang, R. S. Davis, and M. D. Cooper, 2005. Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J. Exp. Med. 202: 783-791.
42. +, but not Ig isotype-switched, memory B cells in X-linked lymphoproliferative disease. J. Clin. Invest. 116: 322-333.
43. + B cell population in peripheral blood expressing VH genes with low frequency of somatic mutation. J. Immunol. 177: 3728-3736.
44. Kruetzmann, S., M. M. Rosado, H. Weber, U. Germing, O. Tournilhac, H. H. Peter, R. Berner, A. Peters, T. Boehm, A. Plebani, et al. 2003. Human immunoglobulin M memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J. Exp. Med. 197: 939-945.
45. Weill, J. C., S. Weller, and C. A. Reynaud. 2004. A bird's eye view on human B cells. Semin. Immunol. 16: 277-281.
46. Bell, E. 2004. Memory B cells - or not? Nat. Rev. Immunol. 5: 6.
47. + memory B cell population in X-linked hyper-IgM syndrome. J. Clin. Invest. 102: 853-860.
48. Gulino, A. V., and L. D. Notarangelo. 2003. Hyper IgM syndromes. Curr. Opin. Rheumatol. 15: 422-429.
49. Facchetti, F., C. Appiani, L. Salvi, J. Levy, and L. D. Notarangelo. 1995. Immunohistologic analysis of ineffective CD40-CD40 ligand interaction in lymphoid tissues from patients with X-linked immunodeficiency with hyper-IgM. Abortive germinal center cell reaction and severe depletion of follicular dendritic cells. J. Immunol. 154: 6624-6633.
50. + T cells. J. Clin. Invest. 115: 1049-1059.
51. Grimbacher, B., A. Hutloff, M. Schlesier, E. Glocker, K. Warnatz, R. Drager, H. Eibel, B. Fischer, A. A. Schaffer, H. W. Mages, et al. 2003. Homozygous loss of ICOS is associated with adult-onset common variable immunodeficiency. Nat. Immunol 4: 261-268.
52. Warnatz, K., L. Bossaller, U. Salzer, A. Skrabl-Baumgartner, W. Schwinger, M. van der Burg, J. J. van Dongen, M. Orlowska-Volk, R. Knoth, A. Durandy, et al. 2006. Human ICOS-deficiency abrogates the germinal center reaction and provides a monogenic model for common variable immunodeficiency. Blood 107: 3045-3052.
53. Matsumoto, M., S. F. Lo, C. J. Carruthers, J. Min, S. Mariathasan, G. Huang, D. R. Plas, S. M. Martin, R. S. Geha, M. H. Nahm, et al. 1996. Affinity maturation without germinal centres in lymphotoxin-α-deficlent mice. Nature 382: 462-466.
54. Forster, R., A. E. Mattis, E. Kremmer, E. Wolf, G. Brem, and M. Lipp. 1996. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87: 1037-1047.
55. Gardby, E., and N. Y. Lycke. 2000. CD19-deficient mice exhibit poor responsiveness to oral immunization despite evidence of unaltered total IgA levels, germinal centers and IgA-isotype switching in Peyer's patches. Eur. J. Immunol. 30: 1861-1871.
56. Tumanov, A., D. Kuprash, M. Lagarkova, S. Grivennikov, K. Abe, A. Shakhov, L. Drutskaya, C. Stewart, A. Chervonsky, and S. Nedospasov. 2002. Distinct role of surface lymphotoxin expressed by B cells in the organization of secondary lymphoid tissues. Immunity 17: 239-250.
57. de Vinuesa, C. G., M. C. Cook, J. Ball, M. Drew, Y. Sunners, M. Cascalho, M. Wabl, G. G. Klaus, and I. C. MacLennan. 2000. Germinal centers without T cells. J. Exp. Med. 191: 485-494.
58. Toellner, K. M., W. E. Jenkinson, D. R. Taylor, M. Khan, D. M. Sze, D. M. Sansom, C. G. Vinuesa, and I. C. MacLennan. 2002. Low-level hypermutation in T cell-independent germinal centers compared with high mutation rates associated with T cell-dependent germinal centers. J. Exp. Med. 195: 383-389.
59. Inamine, A., Y. Takahashi, N. Baba, K. Miyake, T. Tokuhisa, T. Takemori, and R. Abe. 2005. Two waves of memory B-cell generation in the primary immune response. Int. Immunol. 17: 581-589.
60. van Zelm, M. C., T. Szczepanski, M. van der Burg, and J. J. van Dongen. 2007. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J. Exp. Med. 204: 645-655.
61. Toyama, H., S. Okada, M. Hatano, Y. Takahashi, N. Takeda, H. Ichii, T. Takemori, Y. Kuroda, and T. Tokuhisa. 2002. Memory B cells without somatic hypermutation are generated from Bel6-deficient B cells. Immunity 17: 329-339.
62. Wang, Y., G. Huang, J. Wang, H. Molina, D. D. Chaplin, and Y. X. Fu. 2000. Antigen persistence is required for somatic mutation and affinity maturation of immunoglobulin. Eur. J. Immunol. 30: 2226-2234.
63. Gardby, E., J. Wrammert, K. Schon, L. Ekman, T. Leanderson, and N. Lycke. 2003. Strong differential regulation of serum and mucosal IgA responses as revealed in CD28-deficient mice using cholera toxin adjuvant. J. Immunol. 170: 55-63.
64. William, J., C. Euler, S. Christensen, and M. J. Shlomchik. 2002. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 297: 2066-2070.
65. Mao, C., L. Jiang, M. Melo-Jorge, M. Puthenveetil, X. Zhang, M. C. Carroll, and T. Imanishi-Kari. 2004. T cell-independent somatic hypermutation in murine B cells with an immature phenotype. Immunity 20: 133-144.
66. Willenbrock, K., B. Jungnickel, M. L. Hansmann, and R. Kuppers. 2005. Human splenic marginal zone B cells lack expression of activation-induced cytidine deaminase. Eur. J. Immunol. 35: 3002-3007.
67. Bauer, K., M. Zemlin, M. Hummel, S. Pfeiffer, J. Karstaedt, G. Steinhauser, X. Xiao, H. Versmold, and C. Berek. 2002. Diversification of Ig heavy chain genes in human preterm neonates prematurely exposed to environmental antigens. J. Immunol. 169: 1349-1356.
68. Zandvoort, A., and W. Timens. 2002. The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens. Clin. Exp. Immunol. 130: 4-11.
69. Kruschinski, C., M. Zidan, A. S. Debertin, S. von Horsten, and R. Pabst. 2004. Age-dependent development of the splenic marginal zone in human infants is associated with different causes of death. Hum. Pathol. 35: 113-121.
70. Carsetti, R., M. M. Rosado, S. Donnanno, V. Guazzi, A. Soresina, A. Meini, A. Plebani, F. Aiuti, and I. Quinti. 2005. The loss of IgM memory B cells correlates with clinical disease in common variable immunodeficiency. J. Allergy Clin. Immunol. 115: 412-417.
71. Shi, Y., T. Yamazaki, Y. Okubo, Y. Uehara, K. Sugane, and K. Agematsu. 2005. Regulation of aged humoral immune defense against pneumococcal bacteria by IgM memory B cell. J. Immunol. 175: 3262-3267.
72. + memory B cell development. J. Exp. Med. 203: 393-400.
73. + memory B cells. Immunity 26: 205-213.
74. + memory B cells in humoral immunity against pneumococcal infection. Hum. Immunol. 67: 966-975.
75. Barington, T., L. Hougs, L. Juul, H. O. Madsen, L. P. Ryder, C. Heilmann, and A. Svejgaard. 1996. The progeny of a single virgin B cell predominates the human recall B cell response to the capsular polysaccharide of Haemophilus influenzae type b. J. Immunol. 157: 4016-4027.
76. Barington, T., L. Juul, A. Gyhrs, and C. Heilmann. 1994. Heavy-chain isotype patterns of human antibody-secreting cells induced by Haemophilus influenzae type b conjugate vaccines in relation to age and preimmunity. Infect. Immun. 62: 3066-3074.
77. Hougs, L., L. Juul, H. J. Ditzel, C. Heilmann, A. Svejgaard, and T. Barington. 1999. The first dose of a Haemophilus influenzae type b conjugate vaccine reactivates memory B cells: evidence for extensive clonal selection, intraclonal affinity maturation, and multiple isotype switches to IgA2. J. Immunol. 162: 224-237.
78. Lucas, A. H., K. D. Moulton, V. R. Tang, and D. C. Reason. 2001. Combinatorial library cloning of human antibodies to Streptococcus pneumoniae capsular polysaccharides: variable region primary structures and evidence for somatic mutation of Fab specific for capsular serotypes 6B, 14, and 23F. Infect. Immun. 69: 853-864.
79. Obukhanych, T. V., and M. C. Nussenzweig. 2006. T-independent type II immune responses generate memory B cells. J. Exp. Med. 203: 305-310.
80. Good, K. L., V. L. Bryant, and S. G. Tangye. 2006. Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J. Immunol. 177: 5236-5247.
81. Jefferis, R., and D. S. Kumararatne. 1990. Selective IgG subclass deficiency: quantification and clinical relevance. Clin. Exp. Immunol. 81: 357-367.
82. Fondere, J. M., M. F. Huguet, H. Yssel, V. Baillat, J. Reynes, P. van de Perre, and J. P. Vendrell. 2003. Detection of peripheral HIV-1-specific memory B cells in patients untreated or receiving highly active antiretroviral therapy. AIDS 17: 2323-2330.
83. Tuaillon, E., Y. A. Tabaa, G. Petitjean, M. F. Huguet, G. Pajeaux, J. M. Fondere, B. Ponseille, J. Ducos, P. Blanc, and J. P. Vendrell. 2006. Detection of memory B lymphocytes specific to hepatitis B virus (HBV) surface antigen (HBsAg) from HBsAg-vaccinated or HBV-immunized subjects by ELISPOT assay. J. Immunol. Methods 315: 144-152.
84. Phan, T. G., S. Gardam, A. Basten, and R. Brink. 2005. Altered migration, recruitment, and somatic hypermutation in the early response of marginal zone B cells to T cell-dependent antigen. J. Immunol. 174: 4567-4578.