Toll-like receptor 2 is required for autoantibody production and development of renal disease in pristane-induced lupus

Arthritis and Rheumatism

Volumn 65, Issue 6, 2013, Pages 1612-1623

  Urbonaviciute, Vilma ^a,c   Starke, Charlotte ^a   Pirschel, Wiebke ^a   Pohle, Sandy ^a   Frey, Silke ^a   Daniel, Christoph ^a   Amann, Kerstin ^a   Schett, Georg ^a   Herrmann, Martin ^a   Voll, Reinhard E ^a,b  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; AUTOANTIGEN; CARDIOLIPIN; CELL NUCLEUS ANTIGEN; CYTOKINE; DOUBLE STRANDED DNA; GLYCOPROTEIN P 15095; HIGH MOBILITY GROUP B1 PROTEIN; HISTONE; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 6; PRISTANE; SYNDECAN 1; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CELL INFILTRATION; COMPLEMENT DEPOSITION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GLOMERULUS; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; IMMUNOGLOBULIN DEPOSITION; IMMUNOPATHOGENESIS; KIDNEY DISEASE; LIPOGRANULOMA; LUPUS ERYTHEMATOSUS NEPHRITIS; LUPUS LIKE SYNDROME; LUPUS VULGARIS; MALE; MOUSE; NONHUMAN; NUCLEOSOME; PERITONEUM; PHENOTYPE; PLASMA CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEINURIA; SPLEEN CELL;

ANIMALS; AUTOANTIBODIES; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; ENZYME-LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; HMGB1 PROTEIN; KIDNEY DISEASES; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; MICE; MICE, INBRED C57BL; PROTEINURIA; TERPENES; TOLL-LIKE RECEPTOR 2;

EID: 84878597916     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37914     Document Type: Article

References (48)

1. Tan EM, Schur PH, Carr RI, Kunkel HG,. Deoxybonucleic acid (DNA) and antibodies to DNA in the serum of patients with systemic lupus erythematosus. J Clin Invest 1966; 45: 1732-40.
2. Ehrenstein MR, Katz DR, Griffiths MH, Papadaki L, Winkler TH, Kalden JR, et al. Human IgG anti-DNA antibodies deposit in kidneys and induce proteinuria in SCID mice. Kidney Int 1995; 48: 705-11.
3. Winfield JB, Faiferman I, Koffler D,. Avidity of anti-DNA antibodies in serum and IgG glomerular eluates from patients with systemic lupus erythematosus: association of high avidity antinative DNA antibody with glomerulonephritis. J Clin Invest 1977; 59: 90-6. (Pubitemid 8018043)
4. Kawai T, Akira S,. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010; 11: 373-84.
5. Lau CM, Broughton C, Tabor AS, Akira S, Flavell RA, Mamula MJ, et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J Exp Med 2005; 202: 1171-7. (Pubitemid 41586947)
6. Christensen SR, Shupe J, Nickerson K, Kashgarian M, Flavell RA, Shlomchik MJ,. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immunity 2006; 25: 417-28. (Pubitemid 44354217)
7. Savarese E, Steinberg C, Pawar RD, Reindl W, Akira S, Anders HJ, et al. Requirement of Toll-like receptor 7 for pristane-induced production of autoantibodies and development of murine lupus nephritis. Arthritis Rheum 2008; 58: 1107-15. (Pubitemid 351564013)
8. Demaria O, Pagni PP, Traub S, de Gassart A, Branzk N, Murphy AJ, et al. TLR8 deficiency leads to autoimmunity in mice. J Clin Invest 2010; 120: 3651-62.
9. Summers SA, Hoi A, Steinmetz OM, O'Sullivan KM, Ooi JD, Odobasic D, et al. TLR9 and TLR4 are required for the development of autoimmunity and lupus nephritis in pristane nephropathy. J Autoimmun 2010; 35: 291-8.
10. Papadimitraki ED, Tzardi M, Bertsias G, Sotsiou E, Boumpas DT,. Glomerular expression of Toll-like receptor-9 in lupus nephritis but not in normal kidneys: implications for the amplification of the inflammatory response. Lupus 2009; 18: 831-5.
11. Christensen SR, Kashgarian M, Alexopoulou L, Flavell RA, Akira S, Shlomchik MJ,. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J Exp Med 2005; 202: 321-31. (Pubitemid 41043827)
12. Wu X, Peng SL,. Toll-like receptor 9 signaling protects against murine lupus. Arthritis Rheum 2006; 54: 336-42. (Pubitemid 43122217)
13. Lartigue A, Colliou N, Calbo S, Francois A, Jacquot S, Arnoult C, et al. Critical role of TLR2 and TLR4 in autoantibody production and glomerulonephritis in lpr mutation-induced mouse lupus. J Immunol 2009; 183: 6207-16.
14. Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR,. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 1998; 41: 1241-50. (Pubitemid 28313427)
15. Baumann I, Kolowos W, Voll RE, Manger B, Gaipl U, Neuhuber WL, et al. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 2002; 46: 191-201. (Pubitemid 34121664)
16. Munoz LE, Lauber K, Schiller M, Manfredi AA, Herrmann M,. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol 2010; 6: 280-9.
17. Urbonaviciute V, Furnrohr BG, Meister S, Munoz L, Heyder P, De Marchis F, et al. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 2008; 205: 3007-18.
18. Borrello S, Nicolo C, Delogu G, Pandolfi F, Ria F,. TLR2: a crossroads between infections and autoimmunity? Int J Immunopathol Pharmacol 2011; 24: 549-56.
19. Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H,. HSP70 as endogenous stimulus of the Toll/interleukin- 1 receptor signal pathway. J Biol Chem 2002; 277: 15107-12. (Pubitemid 34952589)
20. Kirschning CJ, Schumann RR,. TLR2: cellular sensor for microbial and endogenous molecular patterns. Curr Top Microbiol Immunol 2002; 270: 121-44. (Pubitemid 35448157)
21. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D, Ishizaka A, et al. Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 2004; 279: 7370-7. (Pubitemid 38294612)
22. Calvani N, Caricchio R, Tucci M, Sobel ES, Silvestris F, Tartaglia P, et al. Induction of apoptosis by the hydrocarbon oil pristane: implications for pristane-induced lupus. J Immunol 2005; 175: 4777-82. (Pubitemid 41362020)
23. Urbonaviciute V, Furnrohr BG, Weber C, Haslbeck M, Wilhelm S, Herrmann M, et al. Factors masking HMGB1 in human serum and plasma. J Leukoc Biol 2007; 81: 67-74. (Pubitemid 46021254)
24. Wellmann U, Letz M, Schneider A, Amann K, Winkler TH,. An Ig μ-heavy chain transgene inhibits systemic lupus erythematosus immunopathology in autoimmune (NZB × NZW)F1 mice. Int Immunol 2001; 13: 1461-9. (Pubitemid 33133875)
25. Comby E, Tanaff P, Mariotte D, Costentin-Pignol V, Marcelli C, Ballet JJ,. Evolution of antinuclear antibodies and clinical patterns in patients with active rheumatoid arthritis with longterm infliximab therapy. J Rheumatol 2006; 33: 24-30. (Pubitemid 43054275)
26. Pierangeli SS, Harris EN,. A protocol for determination of anticardiolipin antibodies by ELISA. Nat Protoc 2008; 3: 840-8. (Pubitemid 351639028)
27. Maseda D, Meister S, Neubert K, Herrmann M, Voll RE,. Proteasome inhibition drastically but reversibly impairs murine lymphocyte development. Cell Death Differ 2008; 15: 600-12. (Pubitemid 351267310)
28. Lang VR, Mielenz D, Neubert K, Bohm C, Schett G, Jack HM, et al. The early marginal zone B cell-initiated T-independent type 2 response resists the proteasome inhibitor bortezomib. J Immunol 2010; 185: 5637-47.
29. Starke C, Frey S, Wellmann U, Urbonaviciute V, Herrmann M, Amann K, et al. High frequency of autoantibody-secreting cells and long-lived plasma cells within inflamed kidneys of NZB/W F1 lupus mice. Eur J Immunol 2011; 41: 2107-12.
30. Hoffmann A, Kerr S, Jellusova J, Zhang J, Weisel F, Wellmann U, et al. Siglec-G is a B1 cell-inhibitory receptor that controls expansion and calcium signaling of the B1 cell population. Nat Immunol 2007; 8: 695-704. (Pubitemid 46965345)
31. Nacionales DC, Kelly KM, Lee PY, Zhuang H, Li Y, Weinstein JS, et al. Type I interferon production by tertiary lymphoid tissue developing in response to 2,6,10,14-tetramethyl-pentadecane (pristane). Am J Pathol 2006; 168: 1227-40.
32. Shaheen VM, Satoh M, Richards HB, Yoshida H, Shaw M, Jennette JC, et al. Immunopathogenesis of environmentally induced lupus in mice. Environ Health Perspect 1999; 107 Suppl 5: 723-7. (Pubitemid 29527776)
33. Fairfax KA, Kallies A, Nutt SL, Tarlinton DM,. Plasma cell development: from B-cell subsets to long-term survival niches. Semin Immunol 2008; 20: 49-58.
34. Lacki JK, Leszczynski P, Kelemen J, Muller W, Mackiewicz SH,. Cytokine concentration in serum of lupus erythematosus patients: the effect on acute phase response. J Med 1997; 28: 99-107. (Pubitemid 27306337)
35. Beebe AM, Cua DJ, de Waal Malefyt R,. The role of interleukin-10 in autoimmune disease: systemic lupus erythematosus (SLE) and multiple sclerosis (MS). Cytokine GroWTh Factor Rev 2002; 13: 403-12.
36. Ronnblom L, Alm GV, Eloranta ML,. The type I interferon system in the development of lupus. Semin Immunol 2011; 23: 113-21.
37. Kim HS, Han MS, Chung KW, Kim S, Kim E, Kim MJ, et al. Toll-like receptor 2 senses beta-cell death and contributes to the initiation of autoimmune diabetes. Immunity 2007; 27: 321-33. (Pubitemid 47284922)
38. Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med 2011; 3: 73ra20.
39. Weinstein JS, Nacionales DC, Lee PY, Kelly-Scumpia KM, Yan XJ, Scumpia PO, et al. Colocalization of antigen-specific B and T cells within ectopic lymphoid tissue following immunization with exogenous antigen. J Immunol 2008; 181: 3259-67.
40. Chen H, Liao D, Holl TM, Snowden P, Ueda Y, Kelsoe G,. Genetic regulation of pristane-induced oil granuloma responses. Int J Exp Pathol 2010; 91: 472-83.
41. Booth J, Wilson H, Jimbo S, Mutwiri G,. Modulation of B cell responses by Toll-like receptors. Cell Tissue Res 2010; 343: 131-40.
42. Chiron D, Bekeredjian-Ding I, Pellat-Deceunynck C, Bataille R, Jego G,. Toll-like receptors: lessons to learn from normal and malignant human B cells. Blood 2008; 112: 2205-13.
43. Bekeredjian-Ding I, Jego G,. Toll-like receptors: sentries in the B-cell response. Immunology 2009; 128: 311-23.
44. Davas EM, Tsirogianni A, Kappou I, Karamitsos D, Economidou I, Dantis PC,. Serum IL-6, TNFα, p55 srTNFα, p75srTNFα, srIL-2α levels and disease activity in systemic lupus erythematosus. Clin Rheumatol 1999; 18: 17-22. (Pubitemid 29104747)
45. Kuroda Y, Nacionales DC, Akaogi J, Reeves WH, Satoh M,. Autoimmunity induced by adjuvant hydrocarbon oil components of vaccine. Biomed Pharmacother 2004; 58: 325-37. (Pubitemid 38759732)
46. Espeli M, Bokers S, Giannico G, Dickinson HA, Bardsley V, Fogo AB, et al. Local renal autoantibody production in lupus nephritis. J Am Soc Nephrol 2011; 22: 296-305.
47. Moreth K, Brodbeck R, Babelova A, Gretz N, Spieker T, Zeng-Brouwers J, et al. The proteoglycan biglycan regulates expression of the B cell chemoattractant CXCL13 and aggravates murine lupus nephritis. J Clin Invest 2010; 120: 4251-72.
48. Brown HJ, Lock HR, Sacks SH, Robson MG,. TLR2 stimulation of intrinsic renal cells in the induction of immune-mediated glomerulonephritis. J Immunol 2006; 177: 1925-31. (Pubitemid 44092533)