Autoreactive preplasma cells break tolerance in the absence of regulation by dendritic cells and macrophages

Journal of Immunology

Volumn 189, Issue 2, 2012, Pages 711-720

  Gilbert, Mileka R ^a   Wagner, Nikki J ^a   Jones, Shannon Z ^b   Wisz, Amanda B ^a   Roques, Jose R ^a   Krum, Kristen N ^a   Lee, Sang Ryul ^a   Nickeleit, Volker ^a   Hulbert, Chrys ^c   Thomas, James W ^c   Gauld, Stephen B ^d   Vilen, Barbara J ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; IMMUNOGLOBULIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 6; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; GENETIC PREDISPOSITION; IMMUNE RESPONSE; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, NUCLEAR; AUTOANTIBODIES; BONE MARROW CELLS; CD40 LIGAND; CELLS, CULTURED; DENDRITIC CELLS; IMMUNE TOLERANCE; INTERLEUKIN-6; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MICE, KNOCKOUT; MICE, TRANSGENIC; PLASMA CELLS; RADIATION CHIMERA; STEM CELLS; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84863613729     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102973     Document Type: Article

References (66)

1. Kawai, T., and S. Akira. 2005. Pathogen recognition with Toll-like receptors. Curr. Opin. Immunol. 17: 338-344. (Pubitemid 40848534)
2. Bianchi, M. E. 2007. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 81: 1-5. (Pubitemid 46028489)
3. Rifkin, I. R., E. A. Leadbetter, L. Busconi, G. Viglianti, and A. Marshak-Rothstein. 2005. Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol. Rev. 204: 27-42. (Pubitemid 40460491)
4. 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. (Pubitemid 44715053)
5. Rakoff-Nahoum, S., and R. Medzhitov. 2008. Role of Toll-like receptors in tissue repair and tumorigenesis. Biochemistry (Mosc.) 73: 555-561. (Pubitemid 351775078)
6. Erridge, C. 2010. Endogenous ligands of TLR2 and TLR4: agonists or assistants? J. Leukoc. Biol. 87: 989-999.
7. Nishina, P. M., J. Wang, W. Toyofuku, F. A. Kuypers, B. Y. Ishida, and B. Paigen. 1993. Atherosclerosis and plasma and liver lipids in nine inbred strains of mice. Lipids 28: 599-605. (Pubitemid 23207092)
8. Imai, Y., K. Kuba, G. G. Neely, R. Yaghubian-Malhami, T. Perkmann, G. van Loo, M. Ermolaeva, R. Veldhuizen, Y. H. Leung, H. Wang, et al. 2008. Identification of oxidative stress and Toll-like receptor 4 signaling as a key pathway of acute lung injury. Cell 133: 235-249. (Pubitemid 351512299)
9. Thomas, L. M., and R. D. Salter. 2010. Activation of macrophages by P2X7-induced microvesicles from myeloid cells is mediated by phospholipids and is partially dependent on TLR4. J. Immunol. 185: 3740-3749.
10. Lorne, E., H. Dupont, and E. Abraham. 2010. Toll-like receptors 2 and 4: initiators of non-septic inflammation in critical care medicine? Intensive Care Med. 36: 1826-1835.
11. Sandri, S., D. Rodriguez, E. Gomes, H. P. Monteiro, M. Russo, and A. Campa. 2008. Is serum amyloid A an endogenous TLR4 agonist? J. Leukoc. Biol. 83: 1174-1180. (Pubitemid 351960349)
12. Johnson, G. B., G. J. Brunn, and J. L. Platt. 2004. Cutting edge: an endogenous pathway to systemic inflammatory response syndrome (SIRS)-like reactions through Toll-like receptor 4. J. Immunol. 172: 20-24. (Pubitemid 38020450)
13. Oyama, J., C. Blais, Jr., X. Liu, M. Pu, L. Kobzik, R. A. Kelly, and T. Bourcier. 2004. Reduced myocardial ischemia-reperfusion injury in Toll-like receptor 4-deficient mice. Circulation 109: 784-789. (Pubitemid 38222900)
14. Wright, S. D., C. Burton, M. Hernandez, H. Hassing, J. Montenegro, S. Mundt, S. Patel, D. J. Card, A. Hermanowski-Vosatka, J. D. Bergstrom, et al. 2000. Infectious agents are not necessary for murine atherogenesis. J. Exp. Med. 191: 1437-1442.
15. Kiechl, S., E. Lorenz, M. Reindl, C. J. Wiedermann, F. Oberhollenzer, E. Bonora, J. Willeit, and D. A. Schwartz. 2002. Toll-like receptor 4 polymorphisms and atherogenesis. N. Engl. J. Med. 347: 185-192. (Pubitemid 34764822)
16. Ameziane, N., T. Beillat, P. Verpillat, S. Chollet-Martin, M. C. Aumont, P. Seknadji, M. Lamotte, D. Lebret, V. Ollivier, and D. de Prost. 2003. Association of the Toll-like receptor 4 gene Asp299Gly polymorphism with acute coronary events. Arterioscler. Thromb. Vasc. Biol. 23: e61-e64.
17. Lartigue, A., N. Colliou, S. Calbo, A. François, S. Jacquot, C. Arnoult, F. Tron, D. Gilbert, and P. Musette. 2009. Critical role of TLR2 and TLR4 in autoantibody production and glomerulonephritis in lpr mutation-induced mouse lupus. J. Immunol. 183: 6207-6216.
18. Summers, S. A., A. Hoi, O. M. Steinmetz, K. M. O'Sullivan, J. D. Ooi, D. Odobasic, S. Akira, A. R. Kitching, and S. R. Holdsworth. 2010. TLR9 and TLR4 are required for the development of autoimmunity and lupus nephritis in pristane nephropathy. J. Autoimmun. 35: 291-298.
19. Hang, L., J. H. Slack, C. Amundson, S. Izui, A. N. Theofilopoulos, and F. J. Dixon. 1983. Induction of murine autoimmune disease by chronic polyclonal B cell activation. J. Exp. Med. 157: 874-883. (Pubitemid 13117066)
20. Fournié, G. J., P. H. Lambert, and P. A. Meischer. 1974. Release of DNA in circulating blood and induction of anti-DNA antibodies after injection of bacterial lipopolysaccharides. J. Exp. Med. 140: 1189-1206.
21. Izui, S., P. H. Lambert, G. J. Fournié, H. Türler, and P. A. Miescher. 1977. Features of systemic lupus erythematosus in mice injected with bacterial lipopolysaccharides: identificantion of circulating DNA and renal localization of DNA-anti-DNA complexes. J. Exp. Med. 145: 1115-1130. (Pubitemid 8105358)
22. Kilmon, M. A., J. A. Rutan, S. H. Clarke, and B. J. Vilen. 2005. Low-affinity, Smith antigen-specific B cells are tolerized by dendritic cells and macrophages. J. Immunol. 175: 37-41. (Pubitemid 40884299)
23. Kilmon, M. A., N. J. Wagner, A. L. Garland, L. Lin, K. Aviszus, L. J. Wysocki, and B. J. Vilen. 2007. Macrophages prevent the differentiation of autoreactive B cells by secreting CD40 ligand and interleukin-6. Blood 110: 1595-1602. (Pubitemid 47443976)
24. Benschop, R. J., K. Aviszus, X. Zhang, T. Manser, J. C. Cambier, and L. J. Wysocki. 2001. Activation and anergy in bone marrow B cells of a novel immunoglobulin transgenic mouse that is both hapten specific and autoreactive. Immunity 14: 33-43. (Pubitemid 32144685)
25. Diz, R., S. K. McCray, and S. H. Clarke. 2008. B cell receptor affinity and B cell subset identity integrate to define the effectiveness, affinity threshold, and mechanism of anergy. J. Immunol. 181: 3834-3840.
26. Borrero, M., and S. H. Clarke. 2002. Low-affinity anti-Smith antigen B cells are regulated by anergy as opposed to developmental arrest or differentiation to B-1. J. Immunol. 168: 13-21. (Pubitemid 34014097)
27. Santulli-Marotto, S., M. W. Retter, R. Gee, M. J. Mamula, and S. H. Clarke. 1998. Autoreactive B cell regulation: peripheral induction of developmental arrest by lupus-associated autoantigens. Immunity 8: 209-219. (Pubitemid 28123748)
28. Acevedo-Suárez, C. A., C. Hulbert, E. J. Woodward, and J. W. Thomas. 2005. Uncoupling of anergy from developmental arrest in anti-insulin B cells supports the development of autoimmune diabetes. J. Immunol. 174: 827-833. (Pubitemid 40094278)
29. Culton, D. A., B. P. O'Conner, K. L. Conway, R. Diz, J. Rutan, B. J. Vilen, and S. H. Clarke. 2006. Early preplasma cells define a tolerance checkpoint for autoreactive B cells. J. Immunol. 176: 790-802. (Pubitemid 43099675)
30. Richez, C., P. Blanco, I. Rifkin, J. F. Moreau, and T. Schaeverbeke. 2011. Role for Toll-like receptors in autoimmune disease: the example of systemic lupus erythematosus. Joint Bone Spine 78: 124-130.
31. Björkbacka, H., K. A. Fitzgerald, F. Huet, X. Li, J. A. Gregory, M. A. Lee, C. M. Ordija, N. E. Dowley, D. T. Golenbock, and M. W. Freeman. 2004. The induction of macrophage gene expression by LPS predominantly utilizes Myd88-independent signaling cascades. Physiol. Genomics 19: 319-330. (Pubitemid 40039937)
32. Hirohashi, N., and D. C. Morrison. 1996. Low-dose lipopolysaccharide (LPS) pretreatment of mouse macrophages modulates LPS-dependent interleukin-6 production in vitro. Infect. Immun. 64: 1011-1015. (Pubitemid 26065580)
33. O'Neill, S. K., M. L. Veselits, M. Zhang, C. Labno, Y. Cao, A. Finnegan, M. Uccellini, M. L. Alegre, J. C. Cambier, and M. R. Clark. 2009. Endocytic sequestration of the B cell antigen receptor and Toll-like receptor 9 in anergic cells. Proc. Natl. Acad. Sci. USA 106: 6262-6267.
34. Rui, L., J. I. Healy, J. Blasioli, and C. C. Goodnow. 2006. ERK signaling is a molecular switch integrating opposing inputs from B cell receptor and T cell cytokines to control TLR4-driven plasma cell differentiation. J. Immunol. 177: 5337-5346. (Pubitemid 44527606)
35. Rui, L., C. G. Vinuesa, J. Blasioli, and C. C. Goodnow. 2003. Resistance to CpG DNA-induced autoimmunity through tolerogenic B cell antigen receptor ERK signaling. Nat. Immunol. 4: 594-600. (Pubitemid 36701344)
36. Gilbert, M. R., D. G. Carnathan, P. C. Cogswell, L. Lin, A. S. Baldwin, Jr., and B. J. Vilen. 2007. Dendritic cells from lupus-prone mice are defective in repressing immunoglobulin secretion. J. Immunol. 178: 4803-4810. (Pubitemid 46595262)
37. Renshaw, B. R., W. C. Fanslow, III, R. J. Armitage, K. A. Campbell, D. Liggitt, B. Wright, B. L. Davison, and C. R. Maliszewski. 1994. Humoral immune responses in CD40 ligand-deficient mice. J. Exp. Med. 180: 1889-1900. (Pubitemid 24328578)
38. Körner, H., M. Cook, D. S. Riminton, F. A. Lemckert, R. M. Hoek, B. Ledermann, F. Köntgen, B. Fazekas de St Groth, and J. D. Sedgwick. 1997. Distinct roles for lymphotoxin-α and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur. J. Immunol. 27: 2600-2609. (Pubitemid 27453850)
39. Pasparakis, M., L. Alexopoulou, V. Episkopou, and G. Kollias. 1996. Immune and inflammatory responses in TNFα-deficient mice: a critical requirement for TNFα in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 184: 1397-1411. (Pubitemid 26354696)
40. Cook, M. C., H. Körner, D. S. Riminton, F. A. Lemckert, J. Hasbold, M. Amesbury, P. D. Hodgkin, J. G. Cyster, J. D. Sedgwick, and A. Basten. 1998. Generation of splenic follicular structure and B cell movement in tumor necrosis factor-deficient mice. J. Exp. Med. 188: 1503-1510. (Pubitemid 28489587)
41. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629. (Pubitemid 32520872)
42. Herlands, R. A., J. William, U. Hershberg, and M. J. Shlomchik. 2007. Anti-chromatin antibodies drive in vivo antigen-specific activation and somatic hypermutation of rheumatoid factor B cells at extrafollicular sites. Eur. J. Immunol. 37: 3339-3351.
43. Peeva, E., D. Michael, J. Cleary, J. Rice, X. Chen, and B. Diamond. 2003. Prolactin modulates the naive B cell repertoire. J. Clin. Invest. 111: 275-283. (Pubitemid 36105927)
44. Allen, C. D., T. Okada, and J. G. Cyster. 2007. Germinal-center organization and cellular dynamics. Immunity 27: 190-202. (Pubitemid 47284923)
45. Cozine, C. L., K. L. Wolniak, and T. J. Waldschmidt. 2005. The primary germinal center response in mice. Curr. Opin. Immunol. 17: 298-302. (Pubitemid 40692665)
46. Elgueta, R., V. C. de Vries, and R. J. Noelle. 2010. The immortality of humoral immunity. Immunol. Rev. 236: 139-150.
47. García De Vinuesa, C., A. Gulbranson-Judge, M. Khan, P. O'Leary, M. Cascalho, M. Wabl, G. G. Klaus, M. J. Owen, and I. C. MacLennan. 1999. Dendritic cells associated with plasmablast survival. Eur. J. Immunol. 29: 3712-3721. (Pubitemid 29527820)
48. 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.
49. Kontoyiannis, D., and G. Kollias. 2000. Accelerated autoimmunity and lupus nephritis in NZB mice with an engineered heterozygous deficiency in tumor necrosis factor. Eur. J. Immunol. 30: 2038-2047. (Pubitemid 30456200)
50. Jacob, C. O., and H. O. McDevitt. 1988. Tumour necrosis factor-α in murine autoimmune "lupus" nephritis. Nature 331: 356-358. (Pubitemid 18042493)
51. Ramos-Casals, M., P. Brito-Zerón, S. Muñoz, N. Soria, D. Galiana, L. Bertolaccini, M. J. Cuadrado, and M. A. Khamashta. 2007. Autoimmune diseases induced by TNF-targeted therapies: analysis of 233 cases. Medicine (Baltimore) 86: 242-251. (Pubitemid 47067483)
52. Debandt, M., O. Vittecoq, V. Descamps, X. Le Loët, and O. Meyer. 2003. Anti- TNF-α-induced systemic lupus syndrome. Clin. Rheumatol. 22: 56-61. (Pubitemid 41510416)
53. Boswell, J. M., M. A. Yui, D. W. Burt, and V. E. Kelley. 1988. Increased tumor necrosis factor and IL-1β gene expression in the kidneys of mice with lupus nephritis. J. Immunol. 141: 3050-3054.
54. Brennan, D. C., M. A. Yui, R. P. Wuthrich, and V. E. Kelley. 1989. Tumor necrosis factor and IL-1 in New Zealand Black/White mice: enhanced gene expression and acceleration of renal injury. J. Immunol. 143: 3470-3475. (Pubitemid 20007007)
55. Maury, C. P., and A. M. Teppo. 1989. Tumor necrosis factor in the serum of patients with systemic lupus erythematosus. Arthritis Rheum. 32: 146-150. (Pubitemid 19056401)
56. Jego, G., A. K. Palucka, J. P. Blanck, C. Chalouni, V. Pascual, and J. Banchereau. 2003. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 19: 225-234. (Pubitemid 37011337)
57. Linker-Israeli, M., R. J. Deans, D. J. Wallace, J. Prehn, T. Ozeri-Chen, and J. R. Klinenberg. 1991. Elevated levels of endogenous IL-6 in systemic lupus erythematosus: a putative role in pathogenesis. J. Immunol. 147: 117-123.
58. Gray, D., P. Dullforce, and S. Jainandunsing. 1994. Memory B cell development but not germinal center formation is impaired by in vivo blockade of CD40-CD40 ligand interaction. J. Exp. Med. 180: 141-155. (Pubitemid 24181063)
59. Silvy, A., C. Lagresle, C. Bella, and T. Defrance. 1996. The differentiation of human memory B cells into specific antibody-secreting cells is CD40 independent. Eur. J. Immunol. 26: 517-524. (Pubitemid 26091377)
60. Baer, P. C., B. Wegner, and H. Geiger. 2004. Effects of mycophenolic acid on IL-6 expression of human renal proximal and distal tubular cells in vitro. Nephrol. Dial. Transplant. 19: 47-52. (Pubitemid 38072614)
61. Hervé, M., I. Isnardi, Y. S. Ng, J. B. Bussel, H. D. Ochs, C. Cunningham-Rundles, and E. Meffre. 2007. CD40 ligand and MHC class II expression are essential for human peripheral B cell tolerance. J. Exp. Med. 204: 1583-1593. (Pubitemid 47048025)
62. Fuentes-Pananá, E. M., G. Bannish, and J. G. Monroe. 2004. Basal B-cell receptor signaling in B lymphocytes: mechanisms of regulation and role in positive selection, differentiation, and peripheral survival. Immunol. Rev. 197: 26-40. (Pubitemid 38142165)
63. Marshak-Rothstein, A., and I. R. Rifkin. 2007. Immunologically active autoantigens: the role of Toll-like receptors in the development of chronic inflammatory disease. Annu. Rev. Immunol. 25: 419-441. (Pubitemid 46697913)
64. Hurst, J., and P. von Landenberg. 2008. Toll-like receptors and autoimmunity. Autoimmun. Rev. 7: 204-208.
65. Muñoz, L. E., K. Lauber, M. Schiller, A. A. Manfredi, and M. Herrmann. 2010. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol 6: 280-289.
66. Kono, D. H., M. K. Haraldsson, B. R. Lawson, K. M. Pollard, Y. T. Koh, X. Du, C. N. Arnold, R. Baccala, G. J. Silverman, B. A. Beutler, and A. N. Theofilopoulos. 2009. Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc. Natl. Acad. Sci. USA 106: 12061-12066.