Follicular Dendritic Cell Activation by TLR Ligands Promotes Autoreactive B Cell Responses

Immunity

Volumn 46, Issue 1, 2017, Pages 106-119

  Das, Abhishek ^a   Heesters, Balthasar A ^a   Bialas, Allison ^a   O'Flynn, Joseph ^a   Rifkin, Ian R ^c   Ochando, Jordi ^d   Mittereder, Nanette ^e   Carlesso, Gianluca ^e   Herbst, Ronald ^e   Carroll, Michael C ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e MEDIMMUNE   (United States)

Author keywords

autoimmunity; CD21; CD35; DAMP; follicular dendritic cells; immune complex; interferon ; systemic lupus erythematosus; TLR7

Indexed keywords

ALPHA INTERFERON; AUTOANTIBODY; COMPLEMENT; COMPLEMENT COMPONENT C3D RECEPTOR; INTERFERON REGULATORY FACTOR 5; MYELOID DIFFERENTIATION FACTOR 88; RIBONUCLEOTIDE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 7; AUTOANTIGEN; LIGAND; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CELL ACTIVATION; CYTOKINE RELEASE; FOLLICULAR DENDRITIC CELL; GERMINAL CENTER; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STROMA CELL; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; C57BL MOUSE; CONFOCAL MICROSCOPY; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; MALE; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; AUTOANTIGENS; AUTOIMMUNITY; B-LYMPHOCYTES; DENDRITIC CELLS, FOLLICULAR; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; INTERFERON-ALPHA; LIGANDS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTOR 7; TRANSCRIPTOME;

EID: 85009437434     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.12.014     Document Type: Article

References (70)

1. Allen, C.D., Okada, T., Cyster, J.G., Germinal-center organization and cellular dynamics. Immunity 27 (2007), 190–202.
2. Allen, C.D., Okada, T., Tang, H.L., Cyster, J.G., Imaging of germinal center selection events during affinity maturation. Science 315 (2007), 528–531.
3. Allman, D., Lindsley, R.C., DeMuth, W., Rudd, K., Shinton, S.A., Hardy, R.R., Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167 (2001), 6834–6840.
4. Baccala, R., Gonzalez-Quintial, R., Schreiber, R.D., Lawson, B.R., Kono, D.H., Theofilopoulos, A.N., Anti-IFN-α/β receptor antibody treatment ameliorates disease in lupus-predisposed mice. J. Immunol. 189 (2012), 5976–5984.
5. Banchereau, R., Hong, S., Cantarel, B., Baldwin, N., Baisch, J., Edens, M., Cepika, A.M., Acs, P., Turner, J., Anguiano, E., et al. Personalized immunomonitoring uncovers molecular networks that stratify lupus patients. Cell 165 (2016), 551–565.
6. Barrington, R.A., Pozdnyakova, O., Zafari, M.R., Benjamin, C.D., Carroll, M.C., B lymphocyte memory: role of stromal cell complement and FcgammaRIIB receptors. J. Exp. Med. 196 (2002), 1189–1199.
7. Barton, G.M., Medzhitov, R., Toll-like receptor signaling pathways. Science 300 (2003), 1524–1525.
8. Berland, R., Fernandez, L., Kari, E., Han, J.H., Lomakin, I., Akira, S., Wortis, H.H., Kearney, J.F., Ucci, A.A., Imanishi-Kari, T., Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immunity 25 (2006), 429–440.
9. Blasius, A., Vermi, W., Krug, A., Facchetti, F., Cella, M., Colonna, M., A cell-surface molecule selectively expressed on murine natural interferon-producing cells that blocks secretion of interferon-alpha. Blood 103 (2004), 4201–4206.
10. Blasius, A.L., Cella, M., Maldonado, J., Takai, T., Colonna, M., Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 107 (2006), 2474–2476.
11. Boulant, S., Kural, C., Zeeh, J.C., Ubelmann, F., Kirchhausen, T., Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 13 (2011), 1124–1131.
12. Casellas, R., Shih, T.A., Kleinewietfeld, M., Rakonjac, J., Nemazee, D., Rajewsky, K., Nussenzweig, M.C., Contribution of receptor editing to the antibody repertoire. Science 291 (2001), 1541–1544.
13. Chatterjee, P., Agyemang, A.F., Alimzhanov, M.B., Degn, S., Tsiftsoglou, S.A., Alicot, E., Jones, S.A., Ma, M., Carroll, M.C., Complement C4 maintains peripheral B-cell tolerance in a myeloid cell dependent manner. Eur. J. Immunol. 43 (2013), 2441–2450.
14. Cohen, P.L., Caricchio, R., Abraham, V., Camenisch, T.D., Jennette, J.C., Roubey, R.A., Earp, H.S., Matsushima, G., Reap, E.A., Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196 (2002), 135–140.
15. Colonna, M., Trinchieri, G., Liu, Y.J., Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5 (2004), 1219–1226.
16. Cotran, R.S., Kumar, V., Robbins, S.L., Pathologic Basis of Disease. Fifth Edition, 1994, W.B. Saunders, Philadelphia.
17. Cremasco, V., Woodruff, M.C., Onder, L., Cupovic, J., Nieves-Bonilla, J.M., Schildberg, F.A., Chang, J., Cremasco, F., Harvey, C.J., Wucherpfennig, K., et al. B cell homeostasis and follicle confines are governed by fibroblastic reticular cells. Nat. Immunol. 15 (2014), 973–981.
18. Crow, M.K., Interferon-alpha: a therapeutic target in systemic lupus erythematosus. Rheum. Dis. Clin. North Am. 36 (2010), 173–186.
19. Davison, L.M., Jørgensen, T.N., Sialic acid-binding immunoglobulin-type lectin H-positive plasmacytoid dendritic cells drive spontaneous lupus-like disease development in B6.Nba2 mice. Arthritis Rheumatol. 67 (2015), 1012–1022.
20. Eloranta, M.L., Franck-Larsson, K., Lövgren, T., Kalamajski, S., Rönnblom, A., Rubin, K., Alm, G.V., Rönnblom, L., Type I interferon system activation and association with disease manifestations in systemic sclerosis. Ann. Rheum. Dis. 69 (2010), 1396–1402.
21. Garin, A., Meyer-Hermann, M., Contie, M., Figge, M.T., Buatois, V., Gunzer, M., Toellner, K.M., Elson, G., Kosco-Vilbois, M.H., Toll-like receptor 4 signaling by follicular dendritic cells is pivotal for germinal center onset and affinity maturation. Immunity 33 (2010), 84–95.
22. Gray, D., A role for antigen in the maintenance of immunological memory. Nat. Rev. Immunol. 2 (2002), 60–65.
23. Green, N.M., Moody, K.S., Debatis, M., Marshak-Rothstein, A., Activation of autoreactive B cells by endogenous TLR7 and TLR3 RNA ligands. J. Biol. Chem. 287 (2012), 39789–39799.
24. Hahn, B.H., Antibodies to DNA. N. Engl. J. Med. 338 (1998), 1359–1368.
25. Han, J.H., Umiker, B.R., Kazimirova, A.A., Fray, M., Korgaonkar, P., Selsing, E., Imanishi-Kari, T., Expression of an anti-RNA autoantibody in a mouse model of SLE increases neutrophil and monocyte numbers as well as IFN-I expression. Eur. J. Immunol. 44 (2014), 215–226.
26. Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y., Nagata, S., Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304 (2004), 1147–1150.
27. Hauser, A.E., Junt, T., Mempel, T.R., Sneddon, M.W., Kleinstein, S.H., Henrickson, S.E., von Andrian, U.H., Shlomchik, M.J., Haberman, A.M., Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity 26 (2007), 655–667.
28. Heesters, B.A., Chatterjee, P., Kim, Y.A., Gonzalez, S.F., Kuligowski, M.P., Kirchhausen, T., Carroll, M.C., Endocytosis and recycling of immune complexes by follicular dendritic cells enhances B cell antigen binding and activation. Immunity 38 (2013), 1164–1175.
29. Heesters, B.A., Das, A., Chatterjee, P., Carroll, M.C., Do follicular dendritic cells regulate lupus-specific B cells?. Mol. Immunol. 62 (2014), 283–288.
30. Heyman, B., Wiersma, E.J., Kinoshita, T., In vivo inhibition of the antibody response by a complement receptor-specific monoclonal antibody. J. Exp. Med. 172 (1990), 665–668.
31. Honda, K., Yanai, H., Negishi, H., Asagiri, M., Sato, M., Mizutani, T., Shimada, N., Ohba, Y., Takaoka, A., Yoshida, N., Taniguchi, T., IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434 (2005), 772–777.
32. Hou, B., Reizis, B., DeFranco, A.L., Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and -extrinsic mechanisms. Immunity 29 (2008), 272–282.
33. Humby, F., Bombardieri, M., Manzo, A., Kelly, S., Blades, M.C., Kirkham, B., Spencer, J., Pitzalis, C., Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med., 6, 2009, e1.
34. Iwasaki, A., Medzhitov, R., Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5 (2004), 987–995.
35. Jego, G., Palucka, A.K., Blanck, J.P., Chalouni, C., Pascual, V., Banchereau, J., Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 19 (2003), 225–234.
36. Kraus, M., Alimzhanov, M.B., Rajewsky, N., Rajewsky, K., Survival of resting mature B lymphocytes depends on BCR signaling via the Igalpha/beta heterodimer. Cell 117 (2004), 787–800.
37. Krieg, A.M., The toll of too much TLR7. Immunity 27 (2007), 695–697.
38. Lau, C.M., Broughton, C., Tabor, A.S., Akira, S., Flavell, R.A., Mamula, M.J., Christensen, S.R., Shlomchik, M.J., Viglianti, G.A., Rifkin, I.R., Marshak-Rothstein, A., RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202 (2005), 1171–1177.
39. Leadbetter, E.A., Rifkin, I.R., Hohlbaum, A.M., Beaudette, B.C., Shlomchik, M.J., Marshak-Rothstein, A., Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416 (2002), 603–607.
40. Lee, P.Y., Kumagai, Y., Li, Y., Takeuchi, O., Yoshida, H., Weinstein, J., Kellner, E.S., Nacionales, D., Barker, T., Kelly-Scumpia, K., et al. TLR7-dependent and FcgammaR-independent production of type I interferon in experimental mouse lupus. J. Exp. Med. 205 (2008), 2995–3006.
41. Li, H., Jiang, Y., Prak, E.L., Radic, M., Weigert, M., Editors and editing of anti-DNA receptors. Immunity 15 (2001), 947–957.
42. Liu, Z., Bethunaickan, R., Huang, W., Lodhi, U., Solano, I., Madaio, M.P., Davidson, A., Interferon-α accelerates murine systemic lupus erythematosus in a T cell-dependent manner. Arthritis Rheum. 63 (2011), 219–229.
43. Melamed, D., Benschop, R.J., Cambier, J.C., Nemazee, D., Developmental regulation of B lymphocyte immune tolerance compartmentalizes clonal selection from receptor selection. Cell 92 (1998), 173–182.
44. Moriyama, M., Fukuhara, T., Britschgi, M., He, Y., Narasimhan, R., Villeda, S., Molina, H., Huber, B.T., Holers, M., Wyss-Coray, T., Complement receptor 2 is expressed in neural progenitor cells and regulates adult hippocampal neurogenesis. J. Neurosci. 31 (2011), 3981–3989.
45. Nanda, S.K., Venigalla, R.K., Ordureau, A., Patterson-Kane, J.C., Powell, D.W., Toth, R., Arthur, J.S., Cohen, P., Polyubiquitin binding to ABIN1 is required to prevent autoimmunity. J. Exp. Med. 208 (2011), 1215–1228.
46. Obermoser, G., Pascual, V., The interferon-alpha signature of systemic lupus erythematosus. Lupus 19 (2010), 1012–1019.
47. Ochando, J.C., Homma, C., Yang, Y., Hidalgo, A., Garin, A., Tacke, F., Angeli, V., Li, Y., Boros, P., Ding, Y., et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7 (2006), 652–662.
48. Pitzalis, C., Jones, G.W., Bombardieri, M., Jones, S.A., Ectopic lymphoid-like structures in infection, cancer and autoimmunity. Nat. Rev. Immunol. 14 (2014), 447–462.
49. Rifkin, I.R., Leadbetter, E.A., Busconi, L., Viglianti, G., Marshak-Rothstein, A., Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol. Rev. 204 (2005), 27–42.
50. Rowland, S.L., Riggs, J.M., Gilfillan, S., Bugatti, M., Vermi, W., Kolbeck, R., Unanue, E.R., Sanjuan, M.A., Colonna, M., Early, transient depletion of plasmacytoid dendritic cells ameliorates autoimmunity in a lupus model. J. Exp. Med. 211 (2014), 1977–1991.
51. Salomonsson, S., Jonsson, M.V., Skarstein, K., Brokstad, K.A., Hjelmström, P., Wahren-Herlenius, M., Jonsson, R., Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjögren's syndrome. Arthritis Rheum. 48 (2003), 3187–3201.
52. Schwickert, T.A., Lindquist, R.L., Shakhar, G., Livshits, G., Skokos, D., Kosco-Vilbois, M.H., Dustin, M.L., Nussenzweig, M.C., In vivo imaging of germinal centres reveals a dynamic open structure. Nature 446 (2007), 83–87.
53. Sheehan, K.C., Lai, K.S., Dunn, G.P., Bruce, A.T., Diamond, M.S., Heutel, J.D., Dungo-Arthur, C., Carrero, J.A., White, J.M., Hertzog, P.J., Schreiber, R.D., Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J. Interferon Cytokine Res. 26 (2006), 804–819.
54. Shlomchik, M.J., Madaio, M.P., Ni, D., Trounstein, M., Huszar, D., The role of B cells in lpr/lpr-induced autoimmunity. J. Exp. Med. 180 (1994), 1295–1306.
55. Sisirak, V., Ganguly, D., Lewis, K.L., Couillault, C., Tanaka, L., Bolland, S., D'Agati, V., Elkon, K.B., Reizis, B., Genetic evidence for the role of plasmacytoid dendritic cells in systemic lupus erythematosus. J. Exp. Med. 211 (2014), 1969–1976.
56. Steiner, L.A., Eisen, H.N., Sequential changes in the relative affinity of antibodies synthesized during the immune response. J. Exp. Med. 126 (1967), 1161–1183.
57. Stott, D.I., Hiepe, F., Hummel, M., Steinhauser, G., Berek, C., Antigen-driven clonal proliferation of B cells within the target tissue of an autoimmune disease. The salivary glands of patients with Sjögren's syndrome. J. Clin. Invest. 102 (1998), 938–946.
58. Takaoka, A., Yanai, H., Kondo, S., Duncan, G., Negishi, H., Mizutani, T., Kano, S., Honda, K., Ohba, Y., Mak, T.W., Taniguchi, T., Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434 (2005), 243–249.
59. Thibault, D.L., Graham, K.L., Lee, L.Y., Balboni, I., Hertzog, P.J., Utz, P.J., Type I interferon receptor controls B-cell expression of nucleic acid-sensing Toll-like receptors and autoantibody production in a murine model of lupus. Arthritis Res. Ther., 11, 2009, R112.
60. Umiker, B.R., Andersson, S., Fernandez, L., Korgaokar, P., Larbi, A., Pilichowska, M., Weinkauf, C.C., Wortis, H.H., Kearney, J.F., Imanishi-Kari, T., Dosage of X-linked Toll-like receptor 8 determines gender differences in the development of systemic lupus erythematosus. Eur. J. Immunol. 44 (2014), 1503–1516.
61. Victoratos, P., Kollias, G., Induction of autoantibody-mediated spontaneous arthritis critically depends on follicular dendritic cells. Immunity 30 (2009), 130–142.
62. Victoratos, P., Lagnel, J., Tzima, S., Alimzhanov, M.B., Rajewsky, K., Pasparakis, M., Kollias, G., FDC-specific functions of p55TNFR and IKK2 in the development of FDC networks and of antibody responses. Immunity 24 (2006), 65–77.
63. Vinuesa, C.G., Sanz, I., Cook, M.C., Dysregulation of germinal centres in autoimmune disease. Nat. Rev. Immunol. 9 (2009), 845–857.
64. Wang, X., Cho, B., Suzuki, K., Xu, Y., Green, J.A., An, J., Cyster, J.G., Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers. J. Exp. Med. 208 (2011), 2497–2510.
65. Watkins, A.A., Yasuda, K., Wilson, G.E., Aprahamian, T., Xie, Y., Maganto-Garcia, E., Shukla, P., Oberlander, L., Laskow, B., Menn-Josephy, H., et al. IRF5 deficiency ameliorates lupus but promotes atherosclerosis and metabolic dysfunction in a mouse model of lupus-associated atherosclerosis. J. Immunol. 194 (2015), 1467–1479.
66. Yasuda, K., Richez, C., Maciaszek, J.W., Agrawal, N., Akira, S., Marshak-Rothstein, A., Rifkin, I.R., Murine dendritic cell type I IFN production induced by human IgG-RNA immune complexes is IFN regulatory factor (IRF)5 and IRF7 dependent and is required for IL-6 production. J. Immunol. 178 (2007), 6876–6885.
67. Yasuda, K., Nündel, K., Watkins, A.A., Dhawan, T., Bonegio, R.G., Ubellacker, J.M., Marshak-Rothstein, A., Rifkin, I.R., Phenotype and function of B cells and dendritic cells from interferon regulatory factor 5-deficient mice with and without a mutation in DOCK2. Int. Immunol. 25 (2013), 295–306.
68. Yasuda, K., Watkins, A.A., Kochar, G.S., Wilson, G.E., Laskow, B., Richez, C., Bonegio, R.G., Rifkin, I.R., Interferon regulatory factor-5 deficiency ameliorates disease severity in the MRL/lpr mouse model of lupus in the absence of a mutation in DOCK2. PLoS ONE, 9, 2014, e103478.
69. Yau, I.W., Cato, M.H., Jellusova, J., Hurtado de Mendoza, T., Brink, R., Rickert, R.C., Censoring of self-reactive B cells by follicular dendritic cell-displayed self-antigen. J. Immunol. 191 (2013), 1082–1090.
70. Zagury, D., Le Buanec, H., Mathian, A., Larcier, P., Burnett, R., Amoura, Z., Emilie, D., Peltre, G., Bensussan, A., Bizzini, B., et al. IFNalpha kinoid vaccine-induced neutralizing antibodies prevent clinical manifestations in a lupus flare murine model. Proc. Natl. Acad. Sci. USA 106 (2009), 5294–5299.