IVIg attenuates TLR-9 activation in B cells from SLE patients

Journal of Clinical Immunology

Volumn 31, Issue 1, 2011, Pages 30-38

  Kessel, Aharon ^a   Peri, Regina ^a   Haj, Tharwat ^a   Snir, Ayelet ^a   Slobodin, Gleb ^a   Sabo, Edmond ^a   Rosner, Itzhak ^a   Shoenfeld, Yehuda ^b,c   Toubi, Elias ^a  

^a BNAI ZION MEDICAL CENTER   (Israel)

^b SHEBA MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

Author keywords

IL 10; IL 6; intravenous immunoglobulin; Systemic lupus erythematosus; toll like receptor 9

Indexed keywords

AZATHIOPRINE; CORTICOSTEROID; CPG OLIGODEOXYNUCLEOTIDE; HYDROXYCHLOROQUINE; IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 6; MEPACRINE; METHOTREXATE; MYCOPHENOLIC ACID; PREDNISOLONE; TOLL LIKE RECEPTOR 9; WARFARIN;

ADOLESCENT; ADULT; ALOPECIA; APOPTOSIS; ARTHRALGIA; ARTHRITIS; ARTICLE; B LYMPHOCYTE; CELL CULTURE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HUMAN; INFLAMMATION; LEUKOPENIA; LYMPHADENOPATHY; MALE; MEMORY CELL; NEPHRITIS; PHOTOSENSITIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PURIFICATION; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOSIS;

ADJUVANTS, IMMUNOLOGIC; ADOLESCENT; ADULT; B-LYMPHOCYTES; CELLS, CULTURED; CPG ISLANDS; DOWN-REGULATION; FEMALE; HUMANS; IMMUNOGLOBULINS, INTRAVENOUS; INTERLEUKIN-10; INTERLEUKIN-6; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; OLIGODEOXYRIBONUCLEOTIDES; TOLL-LIKE RECEPTOR 9; YOUNG ADULT;

EID: 79953889735     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-010-9469-3     Document Type: Article

References (48)

1. Shlomchik MJ, Craft JE, Mamula MJ. From T to B and back again: positive feedback in systemic autoimmune disease. Nat Rev Immunol. 2001;1:147-53. (Pubitemid 33741968)
2. Bernasconi NL, Onai N, Lanzavecchia A. 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. 2003;101(11):4500-4. (Pubitemid 36857820)
3. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science. 2002;298:2199-202. (Pubitemid 35471246)
4. Nakano S, Morimoto S, Suzuki J, et al. Role of pathogenic auto-antibody production by Toll-like receptor 9 of B cells in active systemic lupus erythematosus. Rheumatol (Oxf Print). 2008;47 (2):145-9. (Pubitemid 351168222)
5. Papadimitraki ED, Choulaki C, Koutala E, et al. Expansion of toll-like receptor 9-expressing B cells in active systemic lupus erythematosus: implications for the induction and maintenance of the autoimmune process. Arthritis Rheum. 2006;54(11):3601-11. (Pubitemid 44737172)
6. Krieg AM, Yi AK, Matson S, et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature. 1995;374:546-9.
7. Hartmann G, Krieg AM. Mechanism and function of a newly identified CpG DNA motif in human primary B cells. J Immunol. 2000;164:944-53.
8. Klinman DM, Yi AK, Beaucage SL, Conover J, Krieg AM. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc Natl Acad Sci U S A. 1996;93:2879-83. (Pubitemid 26116242)
9. Rousset F, Garcia E, Defrance T, et al. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A. 1992;89:1890-3.
10. Llorente L, Zou W, Levy Y, et al. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J Exp Med. 1995;181:839-44.
11. Linker-Israeli M, Deans RJ, Wallace DJ, et al. Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. J Immunol. 1991;147(1):117-23.
12. Hirohata S, Miyamoto T. Elevated levels of interleukin-6 in cerebrospinal fluid from patients with systemic lupus erythematosus and central nervous system involvement. Arthritis Rheum. 1990;33(5):644-9. (Pubitemid 20166565)
13. Kazatchkine MD, Kaveri SV. Immunomodulation of autoimmune and inflammatory diseases with intravenous immune globulin. N Engl J Med. 2001;345:747-55.
14. Schroeder JO, Zeuner RA, Euler HH, Loffler H. High dose intravenous immunoglobulins in systemic lupus erythematosus: clinical and serological results of a pilot study. J Rheumatol. 1996;23:71-5. (Pubitemid 26037213)
15. Akashi K, Nagasawa K, Mayumi T, et al. Successful treatment of refractory systemic lupus erythematosus with intravenous immunoglobulins. J Rheumatol. 1990;17:375-9. (Pubitemid 20106618)
16. Levy Y, Sherer Y, Ahmed A, et al. A study of 20 SLE patients with intravenous immunoglobulin-clinical and serologic response. Lupus. 1999;8:705-12.
17. Kessel A, Ammuri H, Peri R, et al. Intravenous immunoglobulin therapy affects T regulatory cells by increasing their suppressive function. J Immunol. 2007;179(8):5571-5.
18. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725.
19. Bauer S, Kirschning CJ, Häcker H, et al. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci U S A. 2001;98:9237-42. (Pubitemid 32743900)
20. Richardson B, Scheinbart L, Strahler J, et al. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum. 1990;33:1665-73.
21. Shoshan Y, Shapira I, Toubi E, et al. Accelerated Fas-mediated apoptosis of monocytes and maturing macrophages from patients with systemic lupus erythematosus: relevance to in vitro impairment of interaction with iC3b-opsonized apoptotic cells. J Immunol. 2000;167(10):5963-9. (Pubitemid 33062793)
22. Herrmann M, Voll RE, Zoller OM, et al. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum. 1998;41(7):1241-50. (Pubitemid 28313427)
23. Emlen W, Niebur J, Kadera R. Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J Immunol. 1994;152(7):3685-92. (Pubitemid 24098067)
24. Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol. 2006;6:823-35. (Pubitemid 44631651)
25. Christensen SR, Shlomchik MJ. Regulation of lupus-related autoantibody production and clinical disease by Toll-like receptors. Semin Immunol. 2007;19:11-23. (Pubitemid 46498753)
26. Leadbetter EA, Rifkin IR, Hohlbaum AM, et al. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Tolllike receptors. Nature. 2002;416:603-7. (Pubitemid 34406754)
27. Lau CM, Broughton C, Tabor AS, et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J Exp Med. 2005;202 (9):1171-7. (Pubitemid 41586947)
28. Hagiwara E, Gourley MF, Lee S, Klinman DK. Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin-10:interferon-gamma-secreting cells in the peripheral blood. Arthritis Rheum. 1996;39:379-85. (Pubitemid 26085213)
29. Llorente L, Richaud-Patin Y, Fior R, et al. In vivo production of interleukin-10 by non-T cells in rheumatoid arthritis, Sjogren's syndrome, and systemic lupus erythematosus: a potential mechanism of B lymphocyte hyperactivity and autoimmunity. Arthritis Rheum. 1994;37:1647-55.
30. Lacki JK, Samborski W, Mackiewicz SH. Interleukin-10 and interleukin-6 in lupus erythematosus and rheumatoid arthritis, correlations with acute phase proteins. Clin Rheumatol. 1997;16:275-8. (Pubitemid 27273174)
31. Houssiau FA, Lefebvre C, van den Berghe M, et al. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus. 1995;4:393-5.
32. Park YB, Lee SK, Kim DS, et al. Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin Exp Rheumatol. 1998;16:283-8. (Pubitemid 28219167)
33. Llorente L, Richaud-Patin Y, García-Padilla C, et al. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum. 2000;43(8):1790-800.
34. Mocellin S, Marincola F, Rossi CR, Nitti D, Lise M. The multifaceted relationship between IL-10 and adaptive immunity: putting together the pieces of a puzzle. Cytokine Growth Factor Rev. 2004;15:61-76. (Pubitemid 38121291)
35. Bayry J, Lacroix-Desmazes S, Carbonneil C, et al. Inhibition of maturation and function of dendritic cells by intravenous immunoglobulin. Blood. 2003;101(2):758-65. (Pubitemid 36077604)
36. Nagafuchi H, Suzuki N, Mizushima Y, Sakane T. Constitutive expression of IL-6 receptors and their role in the excessive B cell function in patients with systemic lupus erythematosus. J Immunol. 1993;151:6525-34. (Pubitemid 23340399)
37. Kitani A, Hara M, Hirose T, et al. Autostimulatory effects of IL-6 on excessive B cell differentiation in patients with SLE: analysis of IL-6 production and IL-6R expression. Clin Exp Immunol. 1992;88:75-83.
38. Finck BK, Chan B, Wofsy D. IL-6 promotes murine lupus in NZB/NZW F1 mice. J Clin Invest. 1994;94:585-91. (Pubitemid 24250987)
39. Illei GG, Shirota Y, Yarboro CH, et al. Tocilizumab in systemic lupus erythematosus: data on safety, preliminary efficacy, and impact on circulating plasma cells from an open-label phase I dosage-escalation study. Arthritis Rheum. 2010;62(2):542-52.
40. Toyoda M, Pao A, Petrosian A, Jordan SC. Pooled human gamma globulin modulates surface molecule expression and induces apoptosis in human B cells. Am J Transplant. 2003;3:156-66. (Pubitemid 36323113)
41. Schiff RI. Half-life and clearance of pH 6.8 and pH 4.25 immunoglobulin G intravenous preparations in patients with primary disorders of humoral immunity. Rev Infect Dis. 1986;8 suppl 4:S449-56.
42. Mankarious S, Lee M, Fischer S, et al. The half-lives of IgG subclasses and specific antibodies in patients with primary immunodeficiency who are receiving intravenously administered immunoglobulin. J Lab Clin Med. 1988;112:634-40. (Pubitemid 19006797)
43. Guiducci C, Gong M, Xu Z, et al. TLR recognition of self nucleic acids hampers glucocorticoid activity in lupus. Nature. 2010;465 (7300):937-41.
44. Ott VL, Fong DC, Cambier JC. Fc gamma RIIB as a potential molecular target for intravenous gamma globulin therapy. J Allergy Clin Immunol. 2001;108:S95-8.
45. Proulx DP, Aubin E, Lemieux R, Bazin R. Spontaneous internalization of IVIg in activated B cells. Immunol Lett. 2009;124(1):18-26.
46. Paquin Proulx D, Aubin E, Lemieux R, Bazin R. Inhibition of B cell-mediated antigen presentation by intravenous immunoglobulins (IVIg). Clin Immunol. 2010;135(3):422-9.
47. Séïté JF, Cornec D, Renaudineau Y, et al. IVIg modulates BCR-signaling through CD22 and promotes apoptosis in mature human B lymphocytes. Blood. 2010;116:1698-704.
48. Macfarlane DE, Manzel I. Antagonism of immunostimulatory CpG-oligodeoxynucleotides by quinacrine, chloroquine, and structurally related compounds. J Immunol. 1998;160:1122-31. (Pubitemid 28093406)