TLR4 signaling augments B lymphocyte migration and overcomes the restriction that limits access to germinal center dark zones

Journal of Experimental Medicine

Volumn 206, Issue 12, 2009, Pages 2641-2657

  Hwang, Il Young ^a   Park, Chung ^a   Harrison, Kathleen ^a   Kehrl, John H ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CELL TRANSFER; CHRONIC INFLAMMATION; CONTROLLED STUDY; GERMINAL CENTER; IN VIVO STUDY; LYMPH FOLLICLE; LYMPH NODE; MEMORY CELL; MICROSCOPY; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; RESTRICTION SITE; SIGNAL TRANSDUCTION; ANIMAL; AUTOIMMUNE DISEASE; CELL MOTION; CHRONIC DISEASE; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; CELL MOVEMENT; CELL PROLIFERATION; CHRONIC DISEASE; GERMINAL CENTER; IMMUNOLOGIC MEMORY; INFLAMMATION; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; PLASMA CELLS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 73349088753     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20091982     Document Type: Article

References (55)

1. Allen, C.D., K.M. Ansel, C. Low, R. Lesley, H. Tamamura, N. Fujii, and J.G. Cyster. 2004. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 5:943-952. doi:10.1038/ni1100
2. Allen, C.D., T. Okada, H.L. Tang, and J.G. Cyster. 2007. Imaging of germinal center selection events during affinity maturation. Science. 315:528-531. doi:10.1126/science.1136736
3. Aloisi, F., and R. Pujol-Borrell. 2006. Lymphoid neogenesis in chronic inflammatory diseases. Nat. Rev. Immunol. 6:205-217. doi:10.1038/nri1786
4. Anderson, S.M., M.M. Tomayko, A. Ahuja, A.M. Haberman, and M.J. Shlomchik. 2007. New markers for murine memory B cells that define mutated and unmutated subsets. J. Exp. Med. 204:2103-2114. doi:10.1084/jem.20062571
5. Bajénoff, M., J.G. Egen, L.Y. Koo, J.P. Laugier, F. Brau, N. Glaichenhaus, and R.N. Germain. 2006. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity. 25:989 -1001. doi:10.1016/j.immuni.2006.10.011
6. Benson, M.J., L.D. Erickson, M.W. Gleeson, and R.J. Noelle. 2007. Affinity of antigen encounter and other early B-cell signals determine B-cell fate. Curr. Opin. Immunol. 19:275-280. doi:10.1016/j.coi.2007.04.009
7. Bernasconi, N.L., N. Onai, and A. Lanzavecchia. 2003. 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. 101:4500-4504. doi:10.1182/blood-2002-11-3569
8. Beutler, B., and E.T. Rietschel. 2003. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3:169-176. doi:10.1038/nri1004
9. Cappione, A. III, J.H. Anolik, A. Pugh-Bernard, J. Barnard, P. Dutcher, G. Silverman, and I. Sanz. 2005. Germinal center exclusion of autoreactive B cells is defective in human systemic lupus erythematosus. J. Clin. Invest. 115:3205-3216. doi:10.1172/JCI24179
10. Cyster, J.G. 2005. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu. Rev. Immunol. 23:127-159. doi:10.1146/annurev.immunol.23.021704.115628
11. Ding, C., L. Wang, H. Al-Ghawi, J. Marroquin, M. Mamula, and J. Yan. 2006. Toll-like receptor engagement stimulates anti-snRNP autoreactive B cells for activation. Eur. J. Immunol. 36:2013-2024. doi:10.1002/eji.200635850
12. Freitas, A.A., and M. de Sousa. 1976. Control mechanism of lymphocyte traffic. Altered distribution of 51Cr-labeled mouse lymph node cells pretreated in vitro with lipopolysaccharide. Eur. J. Immunol. 6:269-273. doi:10.1002/eji.1830060407
13. Gargano, L.M., J.M. Moser, and S.H. Speck. 2008. Role for MyD88 signaling in murine gammaherpesvirus 68 latency. J. Virol. 82:3853-3863. doi:10.1128/JVI.02577-07
14. Gavin, A.L., K. Hoebe, B. Duong, T. Ota, C. Martin, B. Beutler, and D. Nemazee. 2006. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling. Science. 314:1936-1938. doi:10.1126/science.1135299
15. Goodlad, J.R., and J.C. Macartney. 1995. Germinal-center cell proliferation in response to T-independent antigens: a stathmokinetic, morphometric and immunohistochemical study in vivo. Eur. J. Immunol. 25:1918-1926. doi:10.1002/eji.1830250719
16. 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. doi:10.1084/jem.20062567
17. Han, S.B., C. Moratz, N.N. Huang, B. Kelsall, H. Cho, C.S. Shi, O. Schwartz, and J.H. Kehrl. 2005. Rgs1 and Gnai2 regulate the entrance of B lymphocytes into lymph nodes and B cell motility within lymph node follicles. Immunity. 22:343-354. doi:10.1016/j.immuni.2005.01.017
18. Hanten, J.A., J.P. Vasilakos, C.L. Riter, L. Neys, K.E. Lipson, S.S. Alkan, and W. Birmachu. 2008. Comparison of human B cell activation by TLR7 and TLR9 agonists. BMC Immunol. 9:39-54. doi:10.1186/1471-2172-9-39
19. Hauser, A.E., T. Junt, T.R. Mempel, M.W. Sneddon, S.H. Kleinstein, S.E. Henrickson, U.H. von Andrian, M.J. Shlomchik, and A.M. Haberman. 2007. Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity. 26:655-667. doi:10.1016/j.immuni.2007.04.008
20. Hawkins, E.D., M. Hommel, M.L. Turner, F.L. Battye, J.F. Markham, and P.D. Hodgkin. 2007. Measuring lymphocyte proliferation, survival and diff erentiation using CFSE time-series data. Nat. Protoc. 2:2057-2067. doi:10.1038/nprot.2007.297
21. Herlands, R.A., S.R. Christensen, R.A. Sweet, U. Hershberg, and M.J. Shlomchik. 2008. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity. 29:249-260. doi:10.1016/j.immuni.2008.06.009
22. Horie, K., and H. Hoshi. 1989. Induction of lymph follicle formation with several mitogens and adjuvants in the mouse popliteal lymph node. Histol. Histopathol. 4:17-25.
23. Hsu, H.C., P. Yang, J. Wang, Q. Wu, R. Myers, J. Chen, J. Yi, T. Guentert, A. Tousson, A.L. Stanus, et al. 2008. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 9:166-175. doi:10.1038/ni1552
24. Huber, C., C. Thielen, H. Seeger, P. Schwarz, F. Montrasio, M.R. Wilson, E. Heinen, Y.X. Fu, G. Miele, and A. Aguzzi. 2005. Lymphotoxin-beta receptor-dependent genes in lymph node and follicular dendritic cell transcriptomes. J. Immunol. 174:5526-5536.
25. Hwang, I.Y., C. Park, and J.H. Kehrl. 2007. Impaired trafficking of Gnai2+/- and Gnai2-/- T lymphocytes: implications for T cell movement within lymph nodes. J. Immunol. 179:439-448.
26. Jacob, J., G. Kelsoe, K. Rajewsky, and U. Weiss. 1991. Intraclonal generation of antibody mutants in germinal centres. Nature. 354:389-392. doi:10.1038/354389a0
27. Klein, U., and R. Dalla-Favera. 2008. Germinal centres: role in B-cell physiology and malignancy. Nat. Rev. Immunol. 8:22-33. doi:10.1038/nri2217
28. Krieg, A.M., and J. Vollmer. 2007. Toll-like receptors 7, 8, and 9: linking innate immunity to autoimmunity. Immunol. Rev. 220:251-269. doi:10.1111/j.1600-065X.2007.00572.x
29. Lanzavecchia, A., and F. Sallusto. 2007. Toll-like receptors and innate immunity in B-cell activation and antibody responses. Curr. Opin. Immunol. 19:268-274. doi:10.1016/j.coi.2007.04.002
30. Leadbetter, E.A., I.R. Rifkin, A.M. Hohlbaum, B.C. Beaudette, M.J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature. 416:603-607. doi:10.1038/416603a
31. Liu, B., Y. Yang, J. Dai, R. Medzhitov, M.A. Freudenberg, P.L. Zhang, and Z. Li. 2006. TLR4 up-regulation at protein or gene level is pathogenic for lupus-like autoimmune disease. J. Immunol. 177:6880-6888.
32. 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. doi:10.1002/eji.1830180306
33. Liu, Y.J., D.E. Joshua, G.T. Williams, C.A. Smith, J. Gordon, and I.C. MacLennan. 1989. Mechanism of antigen-driven selection in germinal centres. Nature. 342:929-931. doi:10.1038/342929a0
34. Luzina, I.G., S.P. Atamas, C.E. Storrer, L.C. daSilva, G. Kelsoe, J.C. Papadimitriou, and B.S. Handwerger. 2001. Spontaneous formation of germinal centers in autoimmune mice. J. Leukoc. Biol. 70:578-584.
35. MacLennan, I.C. 1994. Germinal centers. Annu. Rev. Immunol. 12:117-139. doi:10.1146/annurev.iy.12.040194.001001
36. Meyer-Bahlburg, A., S. Khim, and D.J. Rawlings. 2007. B cell-intrinsic TLR signals amplify but are not required for humoral immunity. J. Exp. Med. 204:3095-3101. doi:10.1084/jem.20071250
37. Miller, M.J., S.H. Wei, I. Parker, and M.D. Cahalan. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science. 296:1869-1873. doi:10.1126/science.1070051
38. Moratz, C., J.R. Hayman, H. Gu, and J.H. Kehrl. 2004. Abnormal B-cell responses to chemokines, disturbed plasma cell localization, and distorted immune tissue architecture in Rgs1-/- mice. Mol. Cell. Biol. 24:5767-5775. doi:10.1128/MCB.24.13.5767-5775.2004
39. Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 102:553-563. doi:10.1016/S0092-8674(00)00078-7
40. Okada, T., M.J. Miller, I. Parker, M.F. Krummel, M. Neighbors, S.B. Hartley, A. O'Garra, M.D. Cahalan, and J.G. Cyster. 2005. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 3:e150. doi:10.1371/journal.pbio.0030150
41. Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Toll-like receptors. Nature. 438:364-368. doi:10.1038/nature04267
42. Paus, D., T.G. Phan, T.D. Chan, S. Gardam, A. Basten, and R. Brink. 2006. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell diff erentiation. J. Exp. Med. 203:1081-1091. doi:10.1084/jem.20060087
43. Peng, S.L. 2005. Signaling in B cells via Toll-like receptors. Curr. Opin. Immunol. 17:230-236. doi:10.1016/j.coi.2005.03.003
44. Quah, B.J., H.S. Warren, and C.R. Parish. 2007. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fluorescent dye carboxyfluorescein diacetate succinimidyl ester. Nat. Protoc. 2:2049-2056. doi:10.1038/nprot.2007.296
45. Reif, K., E.H. Ekland, L. Ohl, H. Nakano, M. Lipp, R. Förster, and J.G. Cyster. 2002. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature. 416:94-99. doi:10.1038/416094a
46. Ruprecht, C.R., and A. Lanzavecchia. 2006. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur. J. Immunol. 36:810-816. doi:10.1002/eji.200535744
47. Schaniel, C., E. Pardali, F. Sallusto, M. Speletas, C. Ruedl, T. Shimizu, T. Seidl, J. Andersson, F. Melchers, A.G. Rolink, and P. Sideras. 1998. Activated murine B lymphocytes and dendritic cells produce a novel CC chemokine which acts selectively on activated T cells. J. Exp. Med. 188:451-463. doi:10.1084/jem.188.3.451
48. Schaniel, C., F. Sallusto, C. Ruedl, P. Sideras, F. Melchers, and A.G. Rolink. 1999. Three chemokines with potential functions in T lymphocyte-independent and-dependent B lymphocyte stimulation. Eur. J. Immunol. 29:2934-2947. doi:10.1002/(SICI)1521-4141(199909)29:09<2934:: AID-IMMU2934>3.0.CO;2-Q
49. Schwickert, T.A., R.L. Lindquist, G. Shakhar, G. Livshits, D. Skokos, M.H. Kosco-Vilbois, M.L. Dustin, and M.C. Nussenzweig. 2007. In vivo imaging of germinal centres reveals a dynamic open structure. Nature. 446:83-87. doi:10.1038/nature05573
50. Shi, G.X., K. Harrison, S.B. Han, C. Moratz, and J.H. Kehrl. 2004. Toll-like receptor signaling alters the expression of regulator of G protein signaling proteins in dendritic cells: implications for G protein-coupled receptor signaling. J. Immunol. 172:5175-5184.
51. Souvannavong, V., C. Lemaire, and R. Chaby. 2004. Lipopolysaccharide protects primary B lymphocytes from apoptosis by preventing mitochondrial dysfunction and bax translocation to mitochondria. Infect. Immun. 72:3260-3266. doi:10.1128/IAI.72.6.3260-3266.2004
52. Tarlinton, D.M. 2008. Evolution in miniature: selection, survival and distribution of antigen reactive cells in the germinal centre. Immunol. Cell Biol. 86:133-138. doi:10.1038/sj.icb.7100148
53. Taylor, P.R., M.C. Pickering, M.H. Kosco-Vilbois, M.J. Walport, M. Botto, S. Gordon, and L. Martinez-Pomares. 2002. The follicular dendritic cell restricted epitope, FDC-M2, is complement C4; localization of immune complexes in mouse tissues. Eur. J. Immunol. 32:1888-1896.
54. 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. doi:10.1126/science.1073924
55. William, J., C. Euler, N. Primarolo, and M.J. Shlomchik. 2006. B cell tolerance checkpoints that restrict pathways of antigen-driven diff erentiation. J. Immunol. 176:2142-2151.