Lack of SIGIRR/TIR8 aggravates hydrocarbon oil-induced lupus nephritis

Journal of Pathology

Volumn 220, Issue 5, 2010, Pages 596-607

  Lech, Maciej ^a   Skuginna, Veronika ^a   Kulkarni, Onkar P ^a   Gong, Jing ^a   Wei, Tiandi ^a   Stark, Robert W ^a   Garlanda, Cecilia ^b   Mantovani, Alberto ^b   Anders, Hans Joachim ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Dendritic cells; Innate immunity; Lupus nephritis; Toll like receptors

Indexed keywords

AUTOANTIBODY; B CELL ACTIVATING FACTOR; CD40 ANTIGEN; GLYCOPROTEIN P 15095; HYDROCARBON; IMMUNOGLOBULIN G; INTERLEUKIN 12; MEMBRANE RECEPTOR; MESSENGER RNA; MYELOID DIFFERENTIATION FACTOR 88; OIL; PRISTANE; PROTEIN BCL 2; RHEUMATOID FACTOR; SINGLE IMMUNOGLOBULIN INTERLEUKIN 1 RELATED RECEPTOR; SMALL NUCLEAR RIBONUCLEOPROTEIN; TOLL LIKE RECEPTOR 7; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CD4 CD8 RATIO; CELL ACTIVATION; CELL COUNT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; GENE DELETION; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUPUS ERYTHEMATOSUS NEPHRITIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPLEEN CELL;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, ANTINUCLEAR; ASCITIC FLUID; AUTOANTIGENS; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, INNATE; LUPUS NEPHRITIS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MYELOID DIFFERENTIATION FACTOR 88; PHENOTYPE; RECEPTORS, INTERLEUKIN-1; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTE SUBSETS; TERPENES; TOLL-LIKE RECEPTOR 7;

EID: 77949846853     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2678     Document Type: Article

References (46)

1. Goodnow CC. Multistep pathogenesis of autoimmune disease. Cell 2007;130:25-35.
2. Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med 2008;358:929-939.
3. Harley JB, Alarcon-Riquelme ME, Criswell LA, Jacob CO, Kimberly RP, Moser KL, et al. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat Genet 2008;40:204-210.
4. Tsokos GC, Nambiar MP, Tenbrock K, Juang YT. Rewiring the T-cell: signaling defects and novel prospects for the treatment of SLE. Trends Immunol 2003;24:259-263.
5. Cohen PL, Eisenberg RA. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol 1991;9:243-269.
6. Botto M, Dell'Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 1998;19:56-59.
7. Hibbs ML, Tarlinton DM, Armes J, Grail D, Hodgson G, Maglitto R, et al. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 1995;83:301-311.
8. Napirei M, Karsunky H, Zevnik B, Stephan H, Mannherz HGMoroy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat Genet 2000;25:177-181.
9. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, et al. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 1992;359:693- 699.
10. Lartigue A, Courville P, Auquit I, Francois A, Arnoult C, Tron F, et al. Role of TLR9 in anti-nucleosome and anti-DNA antibody production in lpr mutation-induced murine lupus. J Immunol 2006;177:1349-1354.
11. Mohan C, Alas E, Morel L, Yang P, Wakeland EK. Genetic dissection of SLE pathogenesis. Sle1 on murine chromosome 1 leads to a selective loss of tolerance to H2A/H2B/DNA subnucleosomes. J Clin Invest 1998;101:1362-1372.
12. Shimizu S, Sugiyama N, Masutani K, Sadanaga A, Miyazaki Y, Inoue Y, et al. Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1). J Immunol 2005;175:7185-7192.
13. Yin Z, Bahtiyar G, Zhang N, Liu L, Zhu P, Robert ME, et al. IL-10 regulates murine lupus. J Immunol 2002;169:2148-2155.
14. Polentarutti N, Rol GP, Muzio M, Bosisio D, Camnasio M, Riva F, et al. Unique pattern of expression and inhibition of IL-1 signalling by the IL-1 receptor family member TIR8/SIGIRR. Eur Cytokine Netw 2003;14:211-218.
15. Thomassen E, Renshaw BR, Sims JE. Identification and characterization of SIGIRR, a molecule representing a novel subtype of the IL-1R superfamily. Cytokine 1999;11:389-399.
16. Wald D, Qin J, Zhao Z, Qian Y, Naramura M, Tian L, et al. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 2003;4:920-927.
17. Qin J, Qian Y, Yao J, Grace C, Li X. SIGIRR inhibits interleukin-1 receptor- and toll-like receptor 4-mediated signaling through different mechanisms. J Biol Chem 2005;280:25233-25241.
18. Garlanda C, Di Liberto D, Vecchi A, La Manna MP, Buracchi C, Caccamo N, et al. Damping excessive inflammation and tissue damage in Mycobacterium tuberculosis infection by Toll IL-1 receptor 8/single Ig IL-1-related receptor, a negative regulator of IL-1/TLR signaling. J Immunol 2007;179:3119-3125.
19. Garlanda C, Riva F, Polentarutti N, Buracchi C, Sironi M, De Bortoli M, et al. Intestinal inflammation in mice deficient in Tir8, an inhibitory member of the IL-1 receptor family. Proc Natl Acad Sci USA 2004;101:3522-3526.
20. Huang X, Hazlett LD, Du W, Barrett RP. SIGIRR promotes resistance against Pseudomonas aeruginosa keratitis by down-regulating type-1 immunity and IL-1R1 and TLR4 signaling. J Immunol 2006;177:548-556.
21. Xiao H, Gulen MF, Qin J, Yao J, Bulek K, Kish D, et al. The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity 2007;26:461-475.
22. Lech M, Kulkarni OP, Pfeiffer S, Savarese E, Krug A, Garlanda C, et al. Tir8/Sigirr prevents murine lupus by suppressing the immunostimulatory effects of lupus autoantigens. J Exp Med 2008;205:1879-1888.
23. Reap EA, Leslie D, Abrahams M, Eisenberg RA, Cohen PL. Apoptosis abnormalities of splenic lymphocytes in autoimmune lpr and gld mice. J Immunol 1995;154:936-943.
24. 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- 1177.
25. Savarese E, Chae OW, Trowitzsch S, Weber G, Kastner B, Akira S, et al. U1 small nuclear ribonucleoprotein immune complexes induce type I interferon in plasmacytoid dendritic cells through TLR7. Blood 2006;107:3229-3234.
26. Pawar RD, Ramanjaneyulu A, Kulkarni OP, Lech M, Segerer S, Anders HJ. Inhibition of Toll-like receptor-7 (TLR-7) or TLR-7 plus TLR-9 attenuates glomerulonephritis and lung injury in experimental lupus. J Am Soc Nephrol 2007;18:1721-1731.
27. 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;25:417-428.
28. Kumagai Y, Kumar H, Koyama S, Kawai T, Takeuchi O, Akira S. Cutting edge: TLR-dependent viral recognition along with type I IFN positive feedback signaling masks the requirement of viral replication for IFN-α production in plasmacytoid dendritic cells. J Immunol 2009;182:3960-3964.
29. 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- 4782.
30. Lee PY, Kumagai Y, Li Y, Takeuchi O, Yoshida H, Weinstein J, et al. TLR7-dependent and FcγR-independent production of type I interferon in experimental mouse lupus. J Exp Med 2008;205:2995- 3006.
31. 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;58:1107-1115.
32. Patole PS, Schubert S, Hildinger K, Khandoga S, Khandoga A, Segerer S, et al. Toll-like receptor-4: renal cells and bone marrow cells signal for neutrophil recruitment during pyelonephritis. Kidney Int 2005;68:2582-2587.
33. Allam R, Pawar RD, Kulkarni OP, Hornung V, Hartmann G, Segerer S, et al. Viral 5′-triphosphate RNA and non-CpG DNA aggravate autoimmunity and lupus nephritis via distinct TLR-independent immune responses. Eur J Immunol 2008;38:3487-3498.
34. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 2008;36:D13-21.
35. Berman HM, Bhat TN, Bourne PE, Feng Z, Gilliland G, Weissig H, et al. The Protein Data Bank and the challenge of structural genomics. Nat Struct Biol 2000;7:(suppl): 957-959.
36. Fiser A, Do RK, Sali A. Modeling of loops in protein structures. Protein Sci 2000;9:1753-1773.
37. Jones DT, Taylor WR, Thornton JM. A new approach to protein fold recognition. Nature 1992;358:86-89.
38. Wallner B, Elofsson A. Identification of correct regions in protein models using structural, alignment, and consensus information. Protein Sci 2006;15:900-913.
39. Pawlowski M, Gajda MJ, Matlak R, Bujnicki JM. MetaMQAP: a meta-server for the quality assessment of protein models. BMC Bioinformat 2008;9:403.
40. Tovchigrechko A, Vakser IA. GRAMM-X public web server for protein-protein docking. Nucleic Acids Res 2006;34:W310-314.
41. Chen R, Li L, Weng Z. ZDOCK: an initial-stage protein-docking algorithm. Proteins 2003;52:80-87.
42. Mackay F, Silveira PA, Brink R. B cells and the BAFF/APRIL axis: fast-forward on autoimmunity and signaling. Curr Opin Immunol 2007;19:327-336.
43. Marshak-Rothstein A, Rifkin IR. Immunologically active autoantigens: the role of toll-like receptors in the development of chronic inflammatory disease. Annu Rev Immunol 2007;25:419-441.
44. Pomeranz Krummel DA, Oubridge C, Leung AK, Li J, Nagai K. Crystal structure of human spliceosomal U1 snRNP at 5.5 Å resolution. Nature 2009;458:475-480.
45. Barrat FJ, Meeker T, Gregorio J, Chan JH, Uematsu S, Akira S, et al. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J Exp Med 2005;202:1131-1139.
46. Lech M, Garlanda C, Mantovani A, Kirschning CJ, Schlondorff D, Anders HJ. Different roles of TiR8/Sigirr on toll-like receptor signaling in intrarenal antigen-presenting cells and tubular epithelial cells. Kidney Int 2007;72:182-192.