The follicular versus marginal zone B lymphocyte cell fate decision

Nature Reviews Immunology

Volumn 9, Issue 11, 2009, Pages 767-777

  Pillai, Shiv ^a   Cariappa, Annaiah ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAKPOINT CLUSTER REGION PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOTCH2 RECEPTOR; TETRASPANIN;

B LYMPHOCYTE; CELL FATE; CELL MATURATION; CELL MIGRATION; CLONAL ANERGY; IMMUNE DEFICIENCY; NATURAL KILLER T CELL; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; B-CELL ACTIVATION FACTOR RECEPTOR; B-LYMPHOCYTES; CELL DIFFERENTIATION; HUMANS; NF-KAPPA B; RECEPTOR, NOTCH2; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; SPLEEN;

EID: 70350515662     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2656     Document Type: Review

References (105)

1. Cariappa, A. et al. Perisinusoidal B cells in the bone marrow participate in T-independent responses to blood-borne microbes. Immunity 23, 397-407 (2005).
2. Cariappa, A., Chase, C., Liu, H., Russell, P. & Pillai, S. Naive recirculating B cells mature simultaneously in the spleen and bone marrow. Blood 109, 2339-2345 (2007).
3. Cariappa, A. et al. The recirculating B cell pool contains two functionally distinct, long-lived, posttransitional, follicular B cell populations. J. Immunol. 179, 2270-2281 (2007).
4. Balazs, M., Martin, F., Zhou, T. & Kearney, J. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17, 341-352 (2002).
5. Martin, F. & Kearney, J. F. Marginal-zone B cells. Nature Rev. Immunol. 2, 323-335 (2002).
6. Pillai, S., Cariappa, A. & Moran, S. T. Marginal zone B cells. Annu. Rev. Immunol. 23, 161-196 (2005).
7. Leadbetter, E. A. et al. NK T cells provide lipid antigen-specific cognate help for B cells. Proc. Natl Acad. Sci. USA 105, 8339-8344 (2008).
8. Barral, P. et al. B cell receptor-mediated uptake of CD1d-restricted antigen augments antibody responses by recruiting invariant NKT cell help in vivo. Proc. Natl Acad. Sci. USA 105, 8345-8350 (2008).
9. Guinamard, R., Okigaki, M., Schlessinger, J. & Ravetch, J. V. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nature Immunol. 1, 31-36 (2000).
10. Cinamon, G., Zachariah, M. A., Lam, O. M., Foss, F. W. Jr & Cyster, J. G. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nature Immunol. 9, 54-62 (2008).
11. Hao, Z. & Rajewsky, K. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J. Exp. Med. 194, 1151-1164 (2001).
12. Nemazee, D. A. & Burki, K. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature 337, 562-566 (1989).
13. Hartley, S. B. et al. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353, 765-769 (1991).
14. Gay, D., Saunders, T. , Camper, S. & Weigert, M. Receptor editing: an approach by autoreactive B cells to escape tolerance. J. Exp. Med. 177, 999-1008 (1993).
15. Tiegs, S. L., Russell, D. M. & Nemazee, D. Receptor editing in self-reactive bone-marrow B cells. J. Exp. Med. 177, 1009-1020 (1993).
16. Allman, D. et al. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167, 6834-6840 (2001).
17. Goodnow, C. C. et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334, 676-682 (1988).
18. Cyster, J. G., Hartley, S. B. & Goodnow, C. C. Competition for follicular niches excludes self-reactive cells from the recirculating B-cell repertoire. Nature 371, 389-395 (1994).
19. Hippen, K. L. et al. In vivo assessment of the relative contributions of deletion, anergy, and editing to B cell self-tolerance. J. Immunol. 175, 909-916 (2005).
20. Ekland, E. H., Forster, R., Lipp, M. & Cyster, J. G. Requirements for follicular exclusion and competitive elimination of autoantigen-binding B cells. J. Immunol. 172, 4700-4708 (2004).
21. Lindsley, R. C., Thomas, M., Srivastava, B. & Allman, D. Generation of peripheral B cells occurs via two spatially and temporally distinct pathways. Blood 109, 2521-2528 (2007).
22. Tan, J. B. et al. Lunatic and manic fringe cooperatively enhance marginal zone B cell precursor competition for delta-like 1 in splenic endothelial niches. Immunity 30, 254-263 (2009).
23. Hardy, R. R., Hayakawa, K., Parks, D. R. & Herzenberg, L. A. Demonstration of B-cell maturation in X-linked immunodeficient mice by simultaneous three-colour immunofluorescence. Nature 306, 270-272 (1983).
24. Hikida, M., Johmura, S., Hashimoto, A., Takezaki, M. & Kurosaki, T. Coupling between B cell receptor and phospholipase C-γ2 is essential for mature B cell development. J. Exp. Med. 198, 581-589 (2003).
25. Wen, R. et al. Phospholipase Cγ2 provides survival signals via Bcl2 and A1 in different subpopulations of B cells. J. Biol. Chem. 278, 43654-43662 (2003).
26. Bell, S. E. et al. PLCγ2 regulates Bcl-2 levels and is required for survival rather than differentiation of marginal zone and follicular B cells. Eur. J. Immunol. 34, 2237-2247 (2004).
27. Pani, G., Siminovitch, K. A. & Paige, C. J. The motheaten mutation rescues B cell signalling and development in CD45-deficient mice. J. Exp. Med. 186, 581-588 (1997).
28. Cariappa, A. et al. The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity 14, 603-615 (2001).
29. Cariappa, A. & Pillai, S. Antigen-dependent B-cell development. Curr. Opin. Immunol. 14, 241-249 (2002).
30. Srivastava, B., Quinn, W. J., Hazard, K., Erikson, J. & Allman, D. Characterization of marginal zone B cell precursors. J. Exp. Med. 202, 1225-1234 (2005).
31. Samardzic, T. et al. Reduction of marginal zone B cells in CD22-deficient mice. Eur. J. Immunol. 32, 561-567 (2002).
32. Kanayama, N., Cascalho, M. & Ohmori, H. Analysis of marginal zone B cell development in the mouse with limited diversity: role of the antigen receptor signals in the recruitment of B cells to the marginal zone. J. Immunol. 174, 1438-1445 (2005).
33. Wen, L. et al. Evidence of marginal-zone B cell-positive selection in spleen. Immunity 23, 297-308 (2005).
34. Walker, J. A. & Smith, K. G. CD22: an inhibitory enigma. Immunology 123, 314-325 (2008).
35. Pillai, S., Cariappa, A. & Pirnie, S. Esterases and autoimmunity: the SIAE pathway and the regulation of peripheral B cell tolerance. Trends Immunol. 21 Sep 2009 (doi:10.1016/j.it.2009.07.006).
36. Cariappa, A. et al. B cell antigen receptor signal strength and peripheral B cell development are regulated by a 9-O-acetyl sialic acid esterase. J. Exp. Med. 206, 125-138 (2009).
37. Batten, M. et al. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 192, 1453-1466 (2000).
38. Schiemann, B. et al. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293, 2111-2114 (2001).
39. Otipoby, K. L. et al. BAFF activates Akt and Erk through BAFF-R in an IKK1-dependent manner in primary mouse B cells. Proc. Natl Acad. Sci. USA 105, 12435-12438 (2008).
40. 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 90, 1073-1083 (1997).
41. Kraus, M., Alimzhanov, M. B., Rajewsky, N. & Rajewsky, K. Survival of resting mature B lymphocytes depends on BCR signalling via the Iga/(3 heterodimer. Cell 11 7, 787-800 (2004).
42. Tze, L. E. et al. Basal immunoglobulin signalling actively maintains developmental stage in immature B cells. PLoS Biol. 3, e82 (2005).
43. Cancro, M. P. Signalling crosstalk in B cells: managing worth and need. Nature Rev Immunol. 9, 657-661 (2009).
44. Stadanlick, J. E. et al. Tonic B cell antigen receptor signals supply an NF-KB substrate for prosurvival BLyS signalling. Nature Immunol. 9, 1379-1387 (2008).
45. Kaisho, T. et al. IKB kinase a is essential for mature B cell development and function. J. Exp. Med. 193, 417-426 (2001).
46. Senftleben, U. et al. Activation by IKKa of a second, evolutionary conserved, NF-KB signalling pathway Science 293, 1495-1499 (2001).
47. Yamada, T. et al. Abnormal immune function of hemopoietic cells from alymphoplasia (aly) mice, a natural strain with mutant NF-icB-inducing kinase. J. Immunol. 165, 804-812 (2000).
48. Siebenlist, U., Brown, K. & Claudio, E. Control of lymphocyte development by nuclear factor-icB. Nature Rev. Immunol. 5, 435-445 (2005).
49. Cariappa, A., Liou, H. C, Horwitz, B. H. & Pillai, S. Nuclear factor KB is required for the development of marginal zone B lymphocytes. J. Exp. Med. 192, 1175-1182. (2000).
50. Sasaki, Y. et al. Canonical NF-KB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity 24, 729-739 (2006).
51. Ruland, J. et al. Bcl 10 is a positive regulator of antigen receptor-induced activation of NF-KB and neural tube closure. Cell 104, 33-42 (2001).
52. Hara, H. et al. The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity 18, 763-775 (2003).
53. Jun, J. E. et al. Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity 18, 751-762 (2003).
54. Ruefli-Brasse, A. A., French, D. M. & Dixit, V. M. Regulation of NF-KB-dependent lymphocyte activation and development by paracaspase. Science 302, 1581-1584 (2003).
55. Xue, L. et al. Defective development and function of Bcl 10-deficient follicular, marginal zone and B1 B cells. Nature Immunol. 4, 857-865 (2003).
56. Pappu, B. P. & Lin, X. Potential role of CARMA 1 in CD40-induced splenic B cell proliferation and marginal zone B cell maturation. Eur. J. Immunol. 36, 3033-3043 (2006).
57. Weih, D. S., Yilmaz, Z. B. & Weih, F Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol. 167, 1909-1919 (2001).
58. Yamazaki, T & Kurosaki, T. Contribution of BCAP to maintenance of mature B cells through c-Rel. Nature Immunol. 4, 780-786 (2003).
59. Saito, T. et al. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18, 675-685 (2003).
60. Tanigaki, K. et al. Notch-RBP-J signalling is involved in cell fate determination of marginal zone B cells. Nature Immunol. 3, 443-450 (2002).
61. Oyama, T et al. Mastermind-1 is required for Notch signal-dependent steps in lymphocyte development in vivo. Proc. Natl Acad. Sci. USA 104, 9764-9769 (2007).
62. Wu, L., Maillard, I., Nakamura, M., Pear, W. S. & Griffin, J. D. The transcriptional co-activator Maml1 is required for Notch2-mediated marginal zone B-cell development. Blood 110, 3618-3623 (2007).
63. Hozumi, K. et al. Delta-like 1 is necessary for the generation of marginal zone B cells but not T cells in vivo. Nature Immunol. 5, 638-644 (2004).
64. Kuroda, K. et al. Regulation of marginal zone B cell development by MINT, a suppressor of Notch/RBP-J signalling pathway. Immunity 18, 301-312 (2003).
65. Huang, Z., Nie, L, Xu, M. & Sun, X. H. Notch-induced E2A degradation requires CHIP and Hsc70 as novel facilitators of ubiquitination. Mol. Cell. Biol. 24, 8951-8962 (2004).
66. Zhang, X. K. et al. The transcription factor Fli-1 modulates marginal zone and follicular B cell development in mice. J. Immunol. 181, 1644-1654 (2008).
67. Quong, M. W. et al. Receptor editing and marginal zone B cell development are regulated by the helix-loop-helix protein, E2A. J. Exp. Med. 199, 1101-1112 (2004).
68. Song, R. et al. Mind bomb 1 in the lymphopoietic niches is essential for T and marginal zone B cell development. J. Exp. Med. 205, 2525-2536 (2008).
69. Cinamon, G. et al. Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nature Immunol. 5, 713-720 (2004).
70. Lu, T. T & Cyster, J. G. Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 297, 409-412 (2002).
71. Thrasher, A. J. WASp in immune-system organization and function. Nature Rev. Immunol. 2, 635-646 (2002).
72. Westerberg, L. S. et al. WASP confers selective advantage for specific haematopoietic cell populations and serves a unique role in marginal zone B-cell homeostasis and function. Blood 112, 4139-4147 (2008).
73. Croker, B. A. et al. The Rac2 guanosine triphosphatase regulates B lymphocyte antigen receptor responses and chemotaxis and is required for establishment of B-1a and marginal zone B lymphocytes. J. Immunol. 168, 3376-3386 (2002).
74. Walmsley, M. J. et al. Critical roles for Rac1 and Rac2 GTPases in B cell development and signalling. Science 302, 459-462 (2003).
75. Girkontaite, I. et al. Lsc is required for marginal zone B cells, regulation of lymphocyte motility and immune responses. Nature Immunol. 2, 855-862 (2001).
76. Rubtsov, A. et al. Lsc regulates marginal-zone B cell migration and adhesion and is required for the IgM T-dependent antibody response. Immunity 23, 527-538 (2005).
77. Rieken, S. et al. G12/G13 family G. proteins regulate marginal zone B cell maturation, migration, and polarization. J. Immunol. 177, 2985-2993 (2006).
78. Otero, D. C, Anzelon, A. N. & Rickert, R. C. CD 19 function in early and late B cell development: I. Maintenance of follicular and marginal zone B cells requires CD19-dependent survival signals. J. Immunol. 170, 73-83 (2003).
79. You, Y, Zhao, H., Wang, Y. & Carter, R. H. Cutting edge: primary and secondary effects of CD 19 deficiency on cells of the marginal zone. J. Immunol. 182, 7343-7347 (2009).
80. Behr, S. & Schriever, F Engaging CD 19 or target of an antiproliferative antibody 1 on human B lymphocytes induces binding of B cells to the interfollicular stroma of human tonsils via integrin alpha 4/beta 1 and fibronectin. J. Exp. Med. 182, 1191-1199 (1995).
81. Okkenhaug, K. et al. Impaired B and T cell antigen receptor signalling in p1106 PI3-kinase mutant mice. Science 297, 1031-1034 (2002).
82. Clayton, E. et al. A crucial role for the p1 106 subunit of phosphatidylinositol 3-kinase in B cell development and activation. J. Exp. Med. 196, 753-763 (2002).
83. Dai, X. et al. Distinct roles of phosphoinositide-3 kinase and phospholipase Cy2 in B-cell receptor-mediated signal transduction. Mol. Cell. Biol. 26, 88-99 (2006).
84. Anzelon, A. N., Wu, H. & Rickert, R. C. Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 function. Nature Immunol. 4, 287-294 (2003).
85. Samardzic, T, Marinkovic, D., Nielsen, P. J., Nitschke, L. & Wirth, T. BOB.1/OBF 1 deficiency affects marginal-zone B-cell compartment. Mol. Cell. Biol. 22, 8320-8331 (2002).
86. Lo, C. G., Lu, T T & Cyster, J. G. Integrin-dependence of lymphocyte entry into the splenic white pulp. J. Exp. Med. 197, 353-361 (2003).
87. Moran, S. T. et al. Synergism between NF-KB 1/p50 and Notch2 during the development of marginal zone B lymphocytes. J. Immunol. 179, 195-200 (2007).
88. Achtman, A. H., Khan, M., Maclennan, I. C. & Langhorne, J. Plasmodium chabaudi chabaudi infection in mice induces strong B cell responses and striking but temporary changes in splenic cell distribution. J. Immunol. 171, 317-324 (2003).
89. Schmidt, E. E., Macdonald, I. C. & Groom, A. C. Microcirculation in mouse spleen (nonsinusal) studied by means of corrosion casts. J. Morphol. 186, 17-29 (1985).
90. Groom, A. C., Schmidt, E. E. & Macdonald, I. C. Microcirculatory pathways and blood flow in spleen: new insights from washout kinetics, corrosion casts, and quantitative intravital videomicroscopy. Scanning Microsc. 5, 159-173 (1991).
91. Carey, J. B., Moffatt-Blue, C. S., Watson, L. C., Gavin, A. L. & Feeney, A. J. Repertoire-based selection into the marginal zone compartment during B cell development. J. Exp. Med. 205, 2043-2052 (2008).
92. Stoddart, A., Zhang, Y. & Paige, C. J. Molecular cloning of the cDNA encoding a murine sialic acid-specific 9-O-acetylesterase and RNA expression in cells of haematopoietic and non-haematopoietic origin. Nucleic Acids Res. 24, 4003-4008 (1996).
93. Stoddart, A., Ray, R. J. & Paige, C. J. Analysis of murine CD22 during B cell development: CD22 is expressed on B cell progenitors before IgM. Int. Immunol. 9, 1571-1579 (1997).
94. Schmidt, E. E., Macdonald, I. C. & Groom, A. C. Microcirculatory pathways in normal human spleen, demonstrated by scanning electron microscopy of corrosion casts. Am. J. Anat. 181, 253-266 (1988).
95. Mebius, R. E. & Kraal, G. Structure and function of the spleen. Nature Rev. Immunol. 5, 606-616 (2005).
96. Steiniger, B., Timphus, E. M. & Barth, P. J. The splenic marginal zone in humans and rodents: an enigmatic compartment and its inhabitants. Histochem. Cell. Biol. 126, 641-648 (2006).
97. Allman, D. & Pillai, S. Peripheral B cell subsets. Curr. Opin. Immunol. 20, 149-157 (2008).
98. Weill, J. C., Weller, S. & Reynaud, C. A. Human marginal zone B cells. Annu. Rev. Immunol. 27, 267-285 (2009).
99. Tangye, S. G. & Good, K. L. Human IgM+CD27+ B cells: memory B cells or "memory" B cells? J. Immunol. 179, 13-19 (2007).
100. Tarlinton, D. Sheepish B cells: evidence for antigen-independent antibody diversification in humans and mice. J. Exp. Med. 205, 1251-1254 (2008).
101. Moens, L., Wuyts, M., Meyts, I., De Boeck, K. & Bossuyt, X. Human memory B lymphocyte subsets fulfill distinct roles in the anti-polysaccharide and anti-protein immune response. J. Immunol. 181, 5306-5312 (2008).
102. Weller, S. 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. 205, 1331-1342 (2008).
103. Weller, S. et al. CD40-CD40L independent Ig gene hypermutation suggests a second B cell diversification pathway in humans. Proc. Natl Acad. Sci. USA 98, 1166-1170 (2001).
104. Wasserstrom, H., Bussel, J., Lim, L. C. & Cunningham-Rundles, C. Memory B cells and pneumococcal antibody after splenectomy. J. Immunol. 181, 3684-3689 (2008).
105. Martin, F. & Kearney, J. F. Positive selection from newly formed to marginal zone B cells depends on the rate of clonal production, CD19 and btk. Immunity 12, 39-49 (2000).