Innate B cell helpers reveal novel types of antibody responses

Nature Immunology

Volumn 14, Issue 2, 2013, Pages 119-126

  Vinuesa, Carola G ^a   Chang, Pheh Ping ^a  

^a Australian National University   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANTIBODY RESPONSE; B LYMPHOCYTE; BONE MARROW CELL; CROSS LINKING; HELPER CELL; INNATE IMMUNITY; MEMORY CELL; NATURAL KILLER CELL; NATURAL KILLER T CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTE SUBSETS; CELL COMMUNICATION; GERMINAL CENTER; HUMANS; IMMUNITY, HUMORAL; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; NATURAL KILLER T-CELLS; NEUTROPHILS; RECEPTORS, ANTIGEN, B-CELL; T-LYMPHOCYTES, HELPER-INDUCER; THYMUS GLAND;

EID: 84872706033     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2511     Document Type: Review

References (106)

1. MacLennan, I.C. Germinal centers. Annu. Rev. Immunol. 12, 117-139 (1994). (Pubitemid 24140411)
2. Tarlinton, D.M. Evolution in miniature: selection, survival and distribution of antigen reactive cells in the germinal centre. Immunol. Cell Biol. 86, 133-138 (2008). (Pubitemid 351301762)
3. Gershon, R.K. & Kondo, K. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 18, 723-737 (1970).
4. Bretscher, P. & Cohn, M. A theory of self-nonself discrimination. Science 169, 1042-1049 (1970).
5. Noelle, R.J. & Snow, E.C. Cognate interactions between helper T cells and B cells. Immunol. Today 11, 361-368 (1990). (Pubitemid 20292167)
6. Cyster, J.G. B cell follicles and antigen encounters of the third kind. Nat. Immunol. 11, 989-996 (2010).
7. FH). Annu. Rev. Immunol. 29, 621-663 (2011).
8. Vinuesa, C.G., Tangye, S.G., Moser, B. & Mackay, C.R. Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 5, 853-865 (2005). (Pubitemid 41581667)
9. Cannons, J.L. et al. Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32, 253-265 (2010).
10. Smith, K.G., Hewitson, T.D., Nossal, G.J. & Tarlinton, D.M. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol. 26, 444-448 (1996). (Pubitemid 26060254)
11. MacLennan, I.C. et al. Extrafollicular antibody responses. Immunol. Rev. 194, 8-18 (2003). (Pubitemid 36886424)
12. Vinuesa, C.G. & Cyster, J.G. How T cells earn the follicular rite of passage. Immunity 35, 671-680 (2011).
13. Victora, G.D. et al. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 143, 592-605 (2010).
14. Liu, Y.J. et al. Mechanism of antigen-driven selection in germinal centres. Nature 342, 929-931 (1989).
15. Good-Jacobson, K.L. et al. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 11, 535-542 (2010).
16. Bryant, V.L. 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. 179, 8180-8190 (2007).
17. 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).
18. Winter, O. et al. Megakaryocytes constitute a functional component of a plasma cell niche in the bone marrow. Blood 116, 1867-1875 (2010).
19. Mosier, D.E., Mond, J.J. & Goldings, E.A. The ontogeny of thymic independent antibody responses in vitro in normal mice and mice with an X-linked B cell defect. J. Immunol. 119, 1874-1878 (1977). (Pubitemid 8232075)
20. Mond, J.J., Lees, A. & Snapper, C.M. T cell-independent antigens type 2. Annu. Rev. Immunol. 13, 655-692 (1995).
21. Bekeredjian-Ding, I. & Jego, G. Toll-like receptors-sentries in the B-cell response. Immunology 128, 311-323 (2009).
22. Peng, S.L. Signaling in B cells via Toll-like receptors. Curr. Opin. Immunol. 17, 230-236 (2005). (Pubitemid 40692656)
23. Alugupalli, K.R., Akira, S., Lien, E. & Leong, J.M. MyD88-and Bruton's tyrosine kinase-mediated signals are essential for T cell-independent pathogen-specific IgM responses. J. Immunol. 178, 3740-3749 (2007). (Pubitemid 46417642)
24. Eckl-Dorna, J. & Batista, F.D. BCR-mediated uptake of antigen linked to TLR9 ligand stimulates B-cell proliferation and antigen-specific plasma cell formation. Blood 113, 3969-3977 (2009).
25. Minguet, S. et al. Enhanced B-cell activation mediated by TLR4 and BCR crosstalk. Eur. J. Immunol. 38, 2475-2487 (2008).
26. Lanzavecchia, A. & Sallusto, F. Toll-like receptors and innate immunity in B-cell activation and antibody responses. Curr. Opin. Immunol. 19, 268-274 (2007). (Pubitemid 46687008)
27. Martin, F., Oliver, A.M. & Kearney, J.F. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14, 617-629 (2001). (Pubitemid 32520872)
28. Braley-Mullen, H. Antigen requirements for induction of B-memory cells: studies with dinitrophenyl coupled to T-dependent and T-independent carriers. J. Exp. Med. 147, 1824-1831 (1978).
29. Garcia de Vinuesa, C., O'Leary, P., Sze, D.M., Toellner, K.M. & MacLennan, I.C. T-independent type 2 antigens induce B cell proliferation in multiple splenic sites, but exponential growth is confined to extrafollicular foci. Eur. J. Immunol. 29, 1314-1323 (1999). (Pubitemid 29164178)
30. Garcia de Vinuesa, C. et al. Germinal centers without T cells. J. Exp. Med. 191, 485-494 (2000).
31. Lentz, V.M. & Manser, T. Cutting edge: germinal centers can be induced in the absence of T cells. J. Immunol. 167, 15-20 (2001). (Pubitemid 32567755)
32. Weller, S. et al. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104, 3647-3654 (2004). (Pubitemid 39564441)
33. Allman, D. & Pillai, S. Peripheral B cell subsets. Curr. Opin. Immunol. 20, 149-157 (2008).
34. Genestier, L. et al. TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses. J. Immunol. 178, 7779-7786 (2007). (Pubitemid 46898049)
35. 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). (Pubitemid 41443441)
36. Martin, F. & Kearney, J.F. Marginal-zone B cells. Nat. Rev. Immunol. 2, 323-335 (2002). (Pubitemid 37328755)
37. Liu, Y.J., Oldfield, S. & MacLennan, I.C. Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones. Eur. J. Immunol. 18, 355-362 (1988).
38. Zandvoort, A. & Timens, W. 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 (2002).
39. 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. Nat. Immunol. 1, 31-36 (2000).
40. Song, H. & Cerny, J. Functional heterogeneity of marginal zone B cells revealed by their ability to generate both early antibody-forming cells and germinal centers with hypermutation and memory in response to a T-dependent antigen. J. Exp. Med. 198, 1923-1935 (2003). (Pubitemid 38032124)
41. Phan, T.G., Gardam, S., Basten, A. & Brink, R. 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 (2005).
42. 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. Nat. Immunol. 9, 54-62 (2008). (Pubitemid 350286204)
43. Zietara, N., Lyszkiewicz, M., Krueger, A. & Weiss, S. ICOS-dependent stimulation of NKT cells by marginal zone B cells. Eur. J. Immunol. 41, 3125-3134 (2011).
44. Hayakawa, K., Hardy, R.R. & Herzenberg, L.A. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161, 1554-1568 (1985). (Pubitemid 15046047)
45. Montecino-Rodriguez, E., Leathers, H. & Dorshkind, K. Identification of a B-1 B cell-specified progenitor. Nat. Immunol. 7, 293-301 (2006).
46. Alugupalli, K.R. et al. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21, 379-390 (2004). (Pubitemid 39208339)
47. Defrance, T., Taillardet, M. & Genestier, L. T cell-independent B cell memory. Curr. Opin. Immunol. 23, 330-336 (2011).
48. Baumgarth, N., Tung, J.W. & Herzenberg, L.A. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin. Immunopathol. 26, 347-362 (2005). (Pubitemid 40468889)
49. Fagarasan, S. & Honjo, T. Intestinal IgA synthesis: regulation of front-line body defences. Nat. Rev. Immunol. 3, 63-72 (2003). (Pubitemid 37328700)
50. Macpherson, A.J. et al. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288, 2222-2226 (2000).
51. Hardy, R.R. B-1 B cells: development, selection, natural autoantibody and leukemia. Curr. Opin. Immunol. 18, 547-555 (2006). (Pubitemid 44311455)
52. 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). (Pubitemid 351904758)
53. Chang, P.P. et al. Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat. Immunol. 13, 35-43 (2012).
54. Detre, C. et al. SAP expression in invariant NKT cells is required for cognate help to support B-cell responses. Blood 120, 122-129 (2012).
55. 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). (Pubitemid 351904757)
56. Bendelac, A., Savage, P.B. & Teyton, L. The biology of NKT cells. Annu. Rev. Immunol. 25, 297-336 (2007). (Pubitemid 46697911)
57. Venkataswamy, M.M. & Porcelli, S.A. Lipid and glycolipid antigens of CD1d-restricted natural killer T cells. Semin. Immunol. 22, 68-78 (2010).
58. Godfrey, D.I. & Berzins, S.P. Control points in NKT-cell development. Nat. Rev. Immunol. 7, 505-518 (2007). (Pubitemid 46987785)
59. Kitamura, H. et al. The natural killer T (NKT) cell ligand α-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J. Exp. Med. 189, 1121-1128 (1999).
60. King, I.L. et al. Invariant natural killer T cells direct B cell responses to cognate lipid antigen in an IL-21-dependent manner. Nat. Immunol. 13, 44-50 (2012).
61. Tonti, E. et al. Follicular helper NKT cells induce limited B cell responses and germinal center formation in the absence of CD4+ T cell help. J. Immunol. 188, 3217-3222 (2012).
62. Fujii, S., Shimizu, K., Hemmi, H. & Steinman, R.M. Innate Vα14+ natural killer T cells mature dendritic cells, leading to strong adaptive immunity. Immunol. Rev. 220, 183-198 (2007). (Pubitemid 350045564)
63. Puga, I. et al. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat. Immunol. 13, 170-180 (2012).
64. Litinskiy, M.B. et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3, 822-829 (2002).
65. Mackay, F. & Schneider, P. Cracking the BAFF code. Nat. Rev. Immunol. 9, 491-502 (2009).
66. Mosier, D.E. & Subbarao, B. Thymus-independent antigens: complexity of B-lymphocyte activation revealed. Immunol. Today 3, 217-222 (1982).
67. Garcia De Vinuesa, C. et al. Dendritic cells associated with plasmablast survival. Eur. J. Immunol. 29, 3712-3721 (1999). (Pubitemid 29527820)
68. 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). (Pubitemid 35279554)
69. Randolph, G.J., Jakubzick, C. & Qu, C. Antigen presentation by monocytes and monocyte-derived cells. Curr. Opin. Immunol. 20, 52-60 (2008).
70. Leon, B. & Ardavin, C. Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol. Cell Biol. 86, 320-324 (2008). (Pubitemid 351667991)
71. Tezuka, H. et al. Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448, 929-933 (2007). (Pubitemid 47312771)
72. Craxton, A., Magaletti, D., Ryan, E.J. & Clark, E.A. Macrophage-and dendritic cell-dependent regulation of human B-cell proliferation requires the TNF family ligand BAFF. Blood 101, 4464-4471 (2003). (Pubitemid 36857815)
73. Merluzzi, S. et al. Mast cells enhance proliferation of B lymphocytes and drive their differentiation toward IgA-secreting plasma cells. Blood 115, 2810-2817 (2010).
74. Gauchat, J.F. et al. Induction of human IgE synthesis in B cells by mast cells and basophils. Nature 365, 340-343 (1993).
75. Erazo, A. et al. Unique maturation program of the IgE response in vivo. Immunity 26, 191-203 (2007). (Pubitemid 46329433)
76. Shinkai, K., Mohrs, M. & Locksley, R.M. Helper T cells regulate type-2 innate immunity in vivo. Nature 420, 825-829 (2002). (Pubitemid 36019631)
77. Wang, H.B. & Weller, P.F. Pivotal advance: eosinophils mediate early alum adjuvant-elicited B cell priming and IgM production. J. Leukoc. Biol. 83, 817-821 (2008). (Pubitemid 351959860)
78. Henz, B.M., Maurer, M., Lippert, U., Worm, M. & Babina, M. Mast cells as initiators of immunity and host defense. Exp. Dermatol. 10, 1-10 (2001). (Pubitemid 32101358)
79. Sokol, C.L. et al. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat. Immunol. 10, 713-720 (2009).
80. Spencer, L.A. & Weller, P.F. Eosinophils and Th2 immunity: contemporary insights. Immunol. Cell Biol. 88, 250-256 (2010).
81. Tacke, F. et al. Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. J. Exp. Med. 203, 583-597 (2006).
82. Chorny, A., Puga, I. & Cerutti, A. Innate signaling networks in mucosal IgA class switching. Adv. Immunol. 107, 31-69 (2010).
83. Chu, V.T. et al. Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat. Immunol. 12, 151-159 (2011).
84. Mack, M. et al. Identification of antigen-capturing cells as basophils. J. Immunol. 174, 735-741 (2005).
85. Kim, S., Shen, T. & Min, B. Basophils can directly present or cross-present antigen to CD8 lymphocytes and alter CD8 T cell differentiation into IL-10-producing phenotypes. J. Immunol. 183, 3033-3039 (2009).
86. Denzel, A. et al. Basophils enhance immunological memory responses. Nat. Immunol. 9, 733-742 (2008). (Pubitemid 351859156)
87. Ruprecht, C.R. & Lanzavecchia, A. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur. J. Immunol. 36, 810-816 (2006).
88. Gavin, A.L. et al. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling. Science 314, 1936-1938 (2006). (Pubitemid 46026117)
89. Pasare, C. & Medzhitov, R. Control of B-cell responses by Toll-like receptors. Nature 438, 364-368 (2005). (Pubitemid 41643953)
90. Day, N. et al. Interleukin receptor-associated kinase (IRAK-4) deficiency associated with bacterial infections and failure to sustain antibody responses. J. Pediatr. 144, 524-526 (2004). (Pubitemid 38457359)
91. Ku, C.L. et al. IRAK4 and NEMO mutations in otherwise healthy children with recurrent invasive pneumococcal disease. J. Med. Genet. 44, 16-23 (2007).
92. Sweet, R.A. et al. Facultative role for T cells in extrafollicular Toll-like receptor-dependent autoreactive B-cell responses in vivo. Proc. Natl. Acad. Sci. USA 108, 7932-7937 (2011).
93. Snapper, C.M. et al. Distinct types of T-cell help for the induction of a humoral immune response to Streptococcus pneumoniae. Trends Immunol. 22, 308-311 (2001). (Pubitemid 32675243)
94. Khan, A.Q., Chen, Q., Wu, Z.Q., Paton, J.C. & Snapper, C.M. Both innate immunity and type 1 humoral immunity to Streptococcus pneumoniae are mediated by MyD88 but differ in their relative levels of dependence on toll-like receptor 2. Infect. Immun. 73, 298-307 (2005). (Pubitemid 40041121)
95. Chu, V.T. & Berek, C. Immunization induces activation of bone marrow eosinophils required for plasma cell survival. Eur. J. Immunol. 42, 130-137 (2012).
96. Wollenberg, I. et al. Regulation of the germinal center reaction by Foxp3+ follicular regulatory T cells. J. Immunol. 187, 4553-4560 (2011).
97. Linterman, M.A. et al. Foxp3+ follicular regulatory T cells control the germinal center response. Nat. Med. 17, 975-982 (2011).
98. Chan, T.D. et al. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol. 183, 3139-3149 (2009).
99. Inamine, A. et al. Two waves of memory B-cell generation in the primary immune response. Int. Immunol. 17, 581-589 (2005). (Pubitemid 41417855)
100. Toyama, H. et al. Memory B cells without somatic hypermutation are generated from Bcl6-deficient B cells. Immunity 17, 329-339 (2002). (Pubitemid 35279553)
101. Hsu, M.C., Toellner, K.M., Vinuesa, C.G. & Maclennan, I.C. B cell clones that sustain long-term plasmablast growth in T-independent extrafollicular antibody responses. Proc. Natl. Acad. Sci. USA 103, 5905-5910 (2006).
102. Obukhanych, T.V. & Nussenzweig, M.C. T-independent type II immune responses generate memory B cells. J. Exp. Med. 203, 305-310 (2006). (Pubitemid 43290839)
103. Nie, Y. et al. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J. Exp. Med. 200, 1145-1156 (2004). (Pubitemid 39507054)
104. Taillardet, M. et al. The thymus-independent immunity conferred by a pneumococcal polysaccharide is mediated by long-lived plasma cells. Blood 114, 4432-4440 (2009).
105. Gaspal, F.M. et al. The generation of thymus-independent germinal centers depends on CD40 but not on CD154, the T cell-derived CD40-ligand. Eur. J. Immunol. 36, 1665-1673 (2006). (Pubitemid 44089034)
106. Toellner, K.M. et al. 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 (2002).