Critical role of TLR7 in the acceleration of systemic lupus erythematosus in TLR9-deficient mice

Journal of Autoimmunity

Volumn 34, Issue 4, 2010, Pages 339-348

  Santiago Raber, Marie Laure ^a   Dunand Sauthier, Isabelle ^a   Wu, Tianfu ^b   Li, Quan Zhen ^b   Uematsu, Satoshi ^c   Akira, Shizuo ^c   Reith, Walter ^a   Mohan, Chandra ^b   Kotzin, Brian L ^d   Izui, Shozo ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

Endogenous retrovirus; Lupus nephritis; Systemic lupus erythematosus; Toll like receptors

Indexed keywords

AUTOANTIBODY; CELL DNA; CELL NUCLEUS ANTIGEN; GENE PRODUCT; GLYCOPROTEIN; GLYCOPROTEIN 70; PROTEIN NBA2; RNA; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE ACTIVITY; DISEASE COURSE; DISEASE EXACERBATION; FEMALE; LUPUS ERYTHEMATOSUS NEPHRITIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SYSTEMIC LUPUS ERYTHEMATOSUS; UPREGULATION;

ANIMALS; ANTIGENS, NUCLEAR; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNITY; DISEASE PROGRESSION; GLOMERULAR BASEMENT MEMBRANE; KIDNEY GLOMERULUS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9;

EID: 77952242576     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2009.11.001     Document Type: Article

References (58)

1. Kotzin B.L. Systemic lupus erythematosus. Cell 1996, 85:303-306.
2. Lefkowith J.B., Gilkeson G.S. Nephritogenic autoantibodies in lupus: current concepts and continuing controversies. Arthritis Rheum 1996, 39:894-903.
3. Mason L.J., Ravirajan C.T., Rahman A., Putterman C., Isenberg D.A. Isα-actinin a target for pathogenic anti-DNA antibodies in lupus nephritis?. Arthritis Rheum 2004, 50:866-870.
4. Faaber P., Rijke T.P., van de Putte L.B., Capel P.J., Berden J.H. Cross-reactivity of human and murine anti-DNA antibodies with heparan sulfate. The major glycosaminoglycan in glomerular basement membranes. J Clin Invest 1986, 77:1824-1830.
5. Sabbaga J., Line S.R., Potocnjak P., Madaio M.P. A murine nephritogenic monoclonal anti-DNA autoantibody binds directly to mouse laminin, the major non-collagenous protein component of the glomerular basement membrane. Eur J Immunol 1989, 19:137-143.
6. Mohan C., Morel L., Yang P., Watanabe H., Croker B., Gilkeson G., et al. Genetic dissection of lupus pathogenesis: a recipe for nephrophilic autoantibodies. J Clin Invest 1999, 103:1685-1695.
7. Li Q.Z., Xie C., Wu T., Mackay M., Aranow C., Putterman C., et al. Identification of autoantibody clusters that best predict lupus disease activity using glomerular proteome arrays. J Clin Invest 2005, 115:3428-3439.
8. Liu K., Li Q.Z., Delgado-Vega A.M., Abelson A.K., Sanchez E., Kelly J.A., et al. Kallikrein genes are associated with lupus and glomerular basement membrane-specific antibody-induced nephritis in mice and humans. J Clin Invest 2009, 119:911-923.
9. Yoshiki T., Mellors R.C., Strand M., August J.T. The viral envelope glycoprotein of murine leukemia virus and the pathogenesis of immune complex glomerulonephritis of New Zealand mice. J Exp Med 1974, 140:1011-1027.
10. Andrews B.S., Eisenberg R.A., Theofilopoulos A.N., Izui S., Wilson C.B., McConahey P.J., et al. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med 1978, 148:1198-1215.
11. Izui S., McConahey P.J., Theofilopoulos A.N., Dixon F.J. Association of circulating retroviral gp70-anti-gp70 immune complexes with murine systemic lupus erythematosus. J Exp Med 1979, 149:1099-1116.
12. Takeda K., Akira S. Toll-like receptors in innate immunity. Int Immunol 2005, 17:1-14.
13. Barrat F.J., Meeker T., Gregorio J., Chan J.H., 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.
14. 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 2002, 416:603-607.
15. Viglianti G.A., Lau C.M., Hanley T.M., Miko B.A., Shlomchik M.J., Marshak-Rothstein A. Activation of autoreactive B cells by CpG dsDNA. Immun 2003, 19:837-847.
16. Lau C.M., Broughton C., Tabor A.S., Akira S., Flavell R.A., Mamula M.J., 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.
17. Berland R., Fernandez L., Kari E., Han J.H., Lomakin I., Akira S., et al. Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immun 2006, 25:429-440.
18. Barrat F.J., Meeker T., Chan J.H., Guiducci C., Coffman R.L. Treatment of lupus-prone mice with a dual inhibitor of TLR7 and TLR9 leads to reduction of autoantibody production and amelioration of disease symptoms. Eur J Immunol 2007, 37:3582-3586.
19. Tabeta K., Hoebe K., Janssen E.M., Du X., Georgel P., Crozat K., et al. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat Immunol 2006, 7:156-164.
20. Pisitkun P., Deane J.A., Difilippantonio M.J., Tarasenko T., Satterthwaite A.B., Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 2006, 312:1669-1672.
21. Subramanian S., Tus K., Li Q.Z., Wang A., Tian X.H., Zhou J., et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Natl Acad Sci USA 2006, 103:9970-9975.
22. Deane J.A., Pisitkun P., Barrett R.S., Feigenbaum L., Town T., Ward J.M., et al. Control of Toll-like receptor 7 expression is essential to restrict autoimmunity and dendritic cell proliferation. Immun 2007, 27:801-810.
23. Fairhurst A.M., Hwang S.H., Wang A., Tian X.H., Boudreaux C., Zhou X.J., et al. Yaa autoimmune phenotypes are conferred by overexpression of TLR7. Eur J Immunol 2008, 38:1971-1978.
24. Christensen S.R., Shupe J., Nickerson K., Kashgarian M., Flavell R.A., Shlomchik M.J. Toll-like receptor 7 and TLR9 dictate autoantibody specificity and have opposing inflammatory and regulatory roles in a murine model of lupus. Immun 2006, 25:417-428.
25. Santiago-Raber M.L., Kikuchi S., Borel P., Uematsu S., Akira S., Kotzin B.L., et al. Evidence for genes in addition to Tlr7 in the Yaa translocation linked with acceleration of systemic lupus erythematosus. J Immunol 2008, 181:1556-1562.
26. Christensen S.R., Kashgarian M., Alexopoulou L., Flavell R.A., Akira S., Shlomchik M.J. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J Exp Med 2005, 202:321-331.
27. Ehlers M., Fukuyama H., McGaha T.L., Aderem A., Ravetch J.V. TLR9/MyD88 signaling is required for class switching to pathogenic IgG2a and 2b autoantibodies in SLE. J Exp Med 2006, 203:553-561.
28. Wu X., Peng S.L. Toll-like receptor 9 signaling protects against murine lupus. Arthritis Rheum 2006, 54:336-342.
29. 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.
30. Yu P., Wellmann U., Kunder S., Quintanilla-Martinez L., Jennen L., Dear N., et al. Toll-like receptor 9-independent aggravation of glomerulonephritis in a novel model of SLE. Int Immunol 2006, 18:1211-1219.
31. Rozzo S.J., Allard J.D., Choubey D., Vyse T.J., Izui S., Peltz G., et al. Evidence for an interferon-inducible gene, Ifi202, in the susceptibility to systemic lupus. Immunity 2001, 15:435-443.
32. Izui S., Higaki M., Morrow D., Merino R. The Y chromosome from autoimmune BXSB/MpJ mice induces a lupus-like syndrome in (NZW x C57BL/6)F1 male mice, but not in C57BL/6 male mice. Eur J Immunol 1988, 18:911-915.
33. Kikuchi S., Fossati-Jimack L., Moll T., Amano H., Amano E., Ida A., et al. Differential role of three major NZB-derived loci linked with Yaa-induced murine lupus nephritis. J Immunol 2005, 174:1111-1117.
34. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002, 3:196-200.
35. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., et al. A novel Toll-like receptor that recognizes bacterial DNA. Nature 2000, 408:740-745.
36. Luzuy S., Merino J., Engers H., Izui S., Lambert P.H. Autoimmunity after induction of neonatal tolerance to alloantigens: role of B cell chimerism and F1 donor B cell activation. J Immunol 1986, 136:4420-4426.
37. Merino R., Fossati L., Lacour M., Lemoine R., Higaki M., Izui S. H-2-linked control of the Yaa gene-induced acceleration of lupus-like autoimmune disease in BXSB mice. Eur J Immunol 1992, 22:295-299.
38. Li Q.Z., Zhou J., Wandstrat A.E., Carr-Johnson F., Branch V., Karp D.R., et al. Protein array autoantibody profiles for insights into systemic lupus erythematosus and incomplete lupus syndromes. Clin Exp Immunol 2007, 147:60-70.
39. Martinez-Soria E., Santiago-Raber M.L., Ho L., Moll T., Izui S. Protection of murine systemic lupus by the Ea transgene without expression of I-E heterodimers. J Immunol 2008, 181:3651-3657.
40. Qiao B., Li B., Yang X., Zhang H., Chu Y., Wang Y., et al. Specific siRNA downregulated TLR9 and altered cytokine expression pattern in macrophage after CpG DNA stimulation. Cell Mol Immunol 2005, 2:130-135.
41. Wiznerowicz M., Trono D. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 2003, 77:8957-8961.
42. Amano H., Amano E., Santiago-Raber M.L., Moll T., Martinez-Soria E., Fossati-Jimack L., et al. Selective expansion of a monocyte subset expressing the CD11c dendritic cell marker in the Yaa model of systemic lupus erythematosus. Arthritis Rheum 2005, 52:2790-2798.
43. Kikuchi S., Santiago-Raber M.L., Amano H., Amano E., Fossati-Jimack L., Moll T., et al. Contribution of Nba2 to Yaa-induced monocytosis in association with murine systemic lupus. J Immunol 2006, 176:3240-3247.
44. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82.
45. Yoshinobu K., Baudino L., Morito N., Dunand-Sauthier I., Morley B.J., Evans L.H., et al. Selective up-regulation of intact, but not defective env RNAs of endogenous modified polytropic retrovirus by the Sgp3 locus of lupus-prone mice. J Immunol 2009, 182:8094-8103.
46. Deocharan B., Qing X., Lichauco J., Putterman C. α-actinin is a cross-reactive renal target for pathogenic anti-DNA antibodies. J Immunol 2002, 168:3072-3078.
47. Mostoslavsky G., Fischel R., Yachimovich N., Yarkoni Y., Rosenmann E., Monestier M., et al. Lupus anti-DNA autoantibodies cross-react with a glomerular structural protein: a case for tissue injury by molecular mimicry. Eur J Immunol 2001, 31:1221-1227.
48. Waters S.T., McDuffie M., Bagavant H., Deshmukh U.S., Gaskin F., Jiang C., et al. Breaking tolerance to double stranded DNA, nucleosome, and other nuclear antigens is not required for the pathogenesis of lupus glomerulonephritis. J Exp Med 2004, 199:255-264.
49. Mannik M., Merrill C.E., Stamps L.D., Wener M.H. Multiple autoantibodies form the glomerular immune deposits in patients with systemic lupus erythematosus. J Rheumatol 2003, 30:1495-1504.
50. Wang J., Shao Y., Bennett T.A., Shankar R.A., Wightman P.D., Reddy L.G. The functional effects of physical interactions among Toll-like receptors 7, 8, and 9. J Biol Chem 2006, 281:37427-37434.
51. Wofsy D., Kerger C.E., Seaman W.E. Monocytosis in the BXSB model for systemic lupus erythematosus. J Exp Med 1984, 159:629-634.
52. Cella M., Jarrossay D., Facchetti F., Alebardi O., Nakajima H., Lanzavecchia A., et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999, 5:919-923.
53. Siegal F.P., Kadowaki N., Shodell M., Fitzgerald-Bocarsly P.A., Shah K., Ho S., et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999, 284:1835-1837.
54. Rönnblom L., Alm G.V. A pivotal role for the natural interferonα-producing cells (plasmacytoid dendritic cells) in the pathogenesis of lupus. J Exp Med 2001, 194:F59-F63.
55. Theofilopoulos A.N., Baccala R., Beutler B., Kono D.H. Type I interferons (α/β) in immunity and autoimmunity. Annu Rev Immunol 2005, 23:307-336.
56. Gilliet M., Cao W., Liu Y.J. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 2008, 8:594-606.
57. Brinkmann M.M., Spooner E., Hoebe K., Beutler B., Ploegh H.L., Kim Y.M. The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J Cell Biol 2007, 177:265-275.
58. Kanzler H., Barrat F.J., Hessel E.M., Coffman R.L. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat Med 2007, 13:552-559.