TLR4 promotes B cell maturation: Independence and cooperation with B lymphocyte-activating factor

Journal of Immunology

Volumn 184, Issue 9, 2010, Pages 4662-4672

  Hayashi, Elize A ^a   Granato, Alessandra ^a   Paiva, Luciana S ^a,b   Bertho, Álvaro L ^c   Bellio, Maria ^a   Nobrega, Alberto ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; CD23 ANTIGEN; CELL SURFACE MARKER; COMPLEMENT COMPONENT C3D RECEPTOR; CYCLOSPORIN A; IMMUNOGLOBULIN D; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN M; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; TOLL LIKE RECEPTOR 4; IMMUNOGLOBULIN E RECEPTOR; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE ACTIVATION; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CROSS LINKING; DOWN REGULATION; FLOW CYTOMETRY; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; UPREGULATION; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; COCULTURE; COMPARATIVE STUDY; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE FUNCTION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; LIPOPOLYSACCHARIDES; LYMPHOCYTE COOPERATION; MICE; MICE, INBRED C57BL; RECEPTORS, IGE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 77954492453     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903253     Document Type: Article

References (48)

1. Hardy, R. R., P. W. Kincade, and K. Dorshkind. 2007. The protean nature of cells in the B lymphocyte lineage. Immunity 26: 703-714.
2. Carsetti, R., G. Köhler, and M. C. Lamers. 1995. Transitional B cells are the target of negative selection in the B cell compartment. J. Exp. Med. 181: 2129-2140.
3. Loder, F., B. Mutschler, R. J. Ray, C. J. Paige, P. Sideras, R. Torres, M. C. Lamers, and R. Carsetti. 1999. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190: 75-89.
4. Allman, D., R. C. Lindsley,W. DeMuth, K. Rudd, S. A. Shinton, and R. R. Hardy. 2001. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167: 6834-6840.
5. Chung, J. B., R. A. Sater, M. L. Fields, J. Erikson, and J. G. Monroe. 2002. CD23 defines two distinct subsets of immature B cells which differ in their responses to T cell help signals. Int. Immunol. 14: 157-166.
6. Meyer-Bahlburg, A., S. F. Andrews, K. O. Yu, S. A. Porcelli, and D. J. Rawlings. 2008. Characterization of a late transitional B cell population highly sensitive to BAFF-mediated homeostatic proliferation. J. Exp. Med. 205: 155-168.
7. Rolink, A. G., J. Andersson, and F. Melchers. 1998. Characterization of immature B cells by a novel monoclonal antibody, by turnover and by mitogen reactivity. Eur. J. Immunol. 28: 3738-3748.
8. Melamed, D.,R. J.Benschop, J. C. Cambier, and D.Nemazee. 1998.Developmental regulation of B lymphocyte immune tolerance compartmentalizes clonal selection from receptor selection. Cell 92: 173-182.
9. Sandel, P. C., and J. G. Monroe. 1999. Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 10: 289-299.
10. Schiemann, B., J. L. Gommerman, K. Vora, T. G. Cachero, S. Shulga-Morskaya, M. Dobles, E. Frew, and M. L. Scott. 2001. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293: 2111-2114.
11. Batten, M., J.Groom,T.G.Cachero, F.Qian, P. Schneider, J.Tschopp, J.L.Browning, and F.Mackay. 2000. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 192: 1453-1466.
12. Mackay, F., S. A.Woodcock, P. Lawton, C. Ambrose, M. Baetscher, P. Schneider, J. Tschopp, and J. L. Browning. 1999. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190: 1697-1710.
13. Groom, J. R., C. A. Fletcher, S. N. Walters, S. T. Grey, S. V. Watt, M. J. Sweet, M. J. Smyth, C. R. Mackay, and F. Mackay. 2007. BAFF and MyD88 signals promote a lupuslike disease independent of T cells. J. Exp. Med. 204: 1959-1971.
14. Melchers, F., V. Braun, and C. Galanos. 1975. The lipoprotein of the outer membrane of Escherichia coli: a B-lymphocyte mitogen. J. Exp. Med. 142: 473-482.
15. Krieg, A. M., A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
16. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162: 3749-3752.
17. Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Toll-like receptors. Nature 438: 364-368.
18. Minguet, S., E. P. Dopfer, C. Pollmer, M. A. Freudenberg, C. Galanos, M. Reth, M. Huber, and W. W. Schamel. 2008. Enhanced B-cell activation mediated by TLR4 and BCR crosstalk. Eur. J. Immunol. 38: 2475-2487.
19. Lau, C. M., C. Broughton, A. S. Tabor, S. Akira, R. A. Flavell, M. J. Mamula, S. R. Christensen, M. J. Shlomchik, G. A. Viglianti, I. R. Rifkin, and A. Marshak-Rothstein. 2005. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202: 1171-1177.
20. Leadbetter, E. A., I. R. Rifkin, A.M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A.Marshak-Rothstein. 2002. Chromatin-IgGcomplexes activateBcells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607.
21. Azulay-Debby, H., E. Edry, and D. Melamed. 2007. CpG DNA stimulates autoreactive immature B cells in the bone marrow. Eur. J. Immunol. 37: 1463-1475.
22. Pereira, J. P., R. Girard, R. Chaby, A. Cumano, and P. Vieira. 2003. Monoallelic expression of the murine gene encoding Toll-like receptor 4. Nat. Immunol. 4: 464-470.
23. Nagai, Y., K. P. Garrett, S. Ohta, U. Bahrun, T. Kouro, S. Akira, K. Takatsu, and P. W. Kincade. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24: 801-812.
24. Akira, S., and K. Takeda. 2004. Toll-like receptor signaling. Nat. Rev. Immunol. 4: 499-511.
25. Hayashi, E. A., S.Akira, and A. Nobrega. 2005. Role of TLRinBcell development: signaling through TLR4 promotes B cell maturation and is inhibited by TLR2. J. Immunol. 174: 6639-6647.
26. Rolink, A. G., J. Tschopp, P. Schneider, and F. Melchers. 2002. BAFF is a survival and maturation factor for mouse B cells. Eur. J. Immunol. 32: 2004-2010.
27. Lindsley, R. C., M. Thomas, B. Srivastava, and D. Allman. 2007. Generation of peripheral B cells occurs via two spatially and temporally distinct pathways. Blood 109: 2521-2528.
28. Pelletier, M., J. S. Thompson, F. Qian, S. A. Bixler, D. Gong, T. Cachero, K. Gilbride, E. Day, M. Zafari, C. Benjamin, et al. 2003. Comparison of soluble decoy IgG fusion proteins of BAFF-R andBCMA as antagonists for BAFF. J. Biol. Chem. 278: 33127-33133.
29. Kang, Y. J., B. Kusler, M. Otsuka, M. Hughes, N. Suzuki, S. Suzuki, W. C. Yeh, S. Akira, J. Han, and P. P. Jones. 2007. Calcineurin negatively regulates TLR-mediated activation pathways. J. Immunol. 179: 4598-4607.
30. Ivashkiv, L. B. 2008. A signal-switch hypothesis for cross-regulation of cytokine and TLR signalling pathways. Nat. Rev. Immunol. 8: 816-822.
31. Siebenlist, U., K. Brown, and E. Claudio. 2005. Control of lymphocyte development by nuclear factor-kappaB. Nat. Rev. Immunol. 5: 435-445.
32. Treml, L. S., G. Carlesso, K. L. Hoek, J. E. Stadanlick, T. Kambayashi, R. J. Bram, M. P. Cancro, and W. N. Khan. 2007. TLR stimulation modifies BLyS receptor expression in follicular and marginal zone B cells. J. Immunol. 178: 7531-7539.
33. Acosta-Rodríguez, E. V., A. Craxton, D. W. Hendricks, M. C. Merino, C. L. Montes, E. A. Clark, and A. Gruppi. 2007. BAFF and LPS cooperate to induce B cells to become susceptible to CD95/Fas-mediated cell death. Eur. J. Immunol. 37: 990-1000.
34. Ceredig, R., E. ten Boekel, A. Rolink, F. Melchers, and J. Andersson. 1998. Fetal liver organ cultures allow the proliferative expansion of pre-B receptor-expressing pre-B-II cells and the differentiation of immature and mature B cells in vitro. Int. Immunol. 10: 49-59.
35. Sasaki, Y., S. Casola, J. L. Kutok, K. Rajewsky, and M. Schmidt-Supprian. 2004. TNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiology. J. Immunol. 173: 2245-2252.
36. Thien, M., T. G. Phan, S. Gardam, M. Amesbury, A. Basten, F. Mackay, and R. Brink. 2004. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20: 785-798.
37. Benschop, R. J., E. Brandl, A. C. Chan, and J. C. Cambier. 2001. Unique signaling properties of B cell antigen receptor in mature and immature B cells: implications for tolerance and activation. J. Immunol. 167: 4172-4179.
38. Poovassery, J. S., T. J. Vanden Bush, and G. A. Bishop. 2009. Antigen receptor signals rescue B cells from TLR tolerance. J. Immunol. 183: 2974-2983.
39. Derudder, E., E. J. Cadera, J. C. Vahl, J. Wang, C. J. Fox, S. Zha, G. van Loo, M. Pasparakis, M. S. Schlissel, M. Schmidt-Supprian, and K. Rajewsky. 2009. Development of immunoglobulin lambda-chain-positive B cells, but not editing of immunoglobulin k-chain, depends on NF-kB signals. Nat. Immunol. 10: 647-654.
40. Morrison, M. D., W. Reiley, M. Zhang, and S. C. Sun. 2005. An atypical tumor necrosis factor (TNF) receptor-associated factor-binding motif of B cellactivating factor belonging to the TNF family (BAFF) receptor mediates induction of the noncanonical NF-kB signaling pathway. J. Biol. Chem. 280: 10018-10024.
41. Xue, L., S. W. Morris, C. Orihuela, E. Tuomanen, X. Cui, R. Wen, and D. Wang. 2003. Defective development and function of Bcl10-deficient follicular, marginal zone and B1 B cells. Nat. Immunol. 4: 857-865.
42. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122.
43. Freitas, A. A., M. M. Rosado, A. C. Viale, and A. Grandien. 1995. The role of cellular competition in B cell survival and selection of B cell repertoires. Eur. J. Immunol. 25: 1729-1738.
44. Silver, K., H. Ferry, T. Crockford, and R. J. Cornall. 2006. TLR4, TLR9 and MyD88 are not required for the positive selection of autoreactive B cells into the primary repertoire. Eur. J. Immunol. 36: 1404-1412.
45. Cariappa, A., C. Chase, H. Liu, P. Russell, and S. Pillai. 2007. Naive recirculating B cells mature simultaneously in the spleen and bone marrow. Blood 109: 2339-2345.
46. Sapoznikov, A., Y. Pewzner-Jung, V. Kalchenko, R. Krauthgamer, I. Shachar, and S. Jung. 2008. Perivascular clusters of dendritic cells provide critical survival signals to B cells in bone marrow niches. Nat. Immunol. 9: 388-395.
47. Ueda, Y., K. Yang, S. J. Foster, M. Kondo, and G. Kelsoe. 2004. Inflammation controls B lymphopoiesis by regulating chemokine CXCL12 expression. J. Exp. Med. 199: 47-58.
48. Thomas, M. D., B. Srivastava, and D. Allman. 2006. Regulation of peripheral B cell maturation. Cell. Immunol. 239: 92-102.