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Research Article

Treatment with a Toll-like receptor inhibitory GpG oligonucleotide delays and attenuates lupus nephritis in NZB/W mice

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Pages 140-155 | Received 24 Apr 2009, Accepted 03 Aug 2009, Published online: 22 Oct 2009

References

  • Kotzin BL. Systemic lupus erythematosus. Cell. 1996; 85:303–306.
  • Tsao BP. The genetics of human systemic lupus erythematosus. Trends Immunol. 2003; 24:595–602.
  • James J, Harley J, Scofield R. Epstein-Barr virus and systemic lupus erythematosus. Curr Opin Rheumatol. 2006; 18:462–467.
  • Akira S, Takeda K, Kaisho T. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat Immunol. 2001; 2:675–680.
  • Lenert P. Targeting toll-like receptor signaling in plasmacytoid dendritic cells and autoreactive B cells as a therapy for lupus. Arthritis Res Ther. 2006; 8:203.
  • Cook D, Pisetsky D, Schwartz D. Toll-like receptors in the pathogenesis of human disease. Nat Immunol. 2004; 5:975–979.
  • Medzhitov R, Preston-Hurlburt P, Kopp E, Stadlen A, Chen C, Ghosh S, Janeway C. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol Cell. 1998; 2:253–258.
  • Schnare M, Barton G, Holt A, Takeda K, Akira S, Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat Immunol. 2001; 2:947–950.
  • Deane J, Bolland S. Nucleic acid-sensing TLRs as modifiers of autoimmunity. J Immunol. 2006; 177:6573–6578.
  • Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, Matsumoto M, Hoshino K, Wagner H, Takeda K, Akira S. A Toll-like receptor recognizes bacterial DNA. Nature. 2000; 408:740–745.
  • Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature. 2002; 416:603–607.
  • Viglianti GA, Lau CM, Hanley TM, Miko BA, Shlomchik MJ, Marshak-Rothstein A. Activation of autoreactive B cells by CpG dsDNA. Immunity. 2003; 19:837–847.
  • Christensen C, Kashgarian M, Alexopoulou L, Flavell R, Akira S, Shlomchik M. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J Exp Med. 2005; 202:321–331.
  • Ho P, Fontoura P, Ruiz P, Steinman L, Garren H. An immunomodulatory GpG oligonucleotide for the treatment of autoimmunity via the innate and adaptive immune systems. J Immunol. 2003; 171:4920–4926.
  • Ho PP, Fontoura P, Platten M, Sobel RA, DeVoss JJ, Lee LY, Kidd BA, Tomooka BH, Capers J, Agrawal A, Gupta R, Zernik J, Yee MK, Lee BJ, Garren H, Robinson WH, Steinman L. A Suppressive oligodeoxynucleotide enhances the efficacy of myelin cocktail/IL-4-tolerizing DNA vaccination and treats autoimmune disease. J Immunol. 2005; 175:6226–6234.
  • Jacob C, Van Der Meide P, McDevitt H. In vivo treatment of (NZB × NZW)F1 lupus-like nephritis with monoclonal antibody to gamma-interferon. J Exp Med. 1987; 166:798–803.
  • Nakajima A, Hirose S, Yagita H, Okumura K. Roles of IL-4 and IL-12 in the development of lupus in NZB/W F1 mice. J Immunol. 1997; 158:1466–1472.
  • Peng S, Moslehi J, Craft J. Roles of interferon-gamma and interleukin-4 in murine lupus. J Clin Invest. 1997; 99:1936–1946.
  • Balomenos D, Rumold R, Theofilopoulos A. Interferon-gamma is required for lupus-like disease and lymphoaccumulation in MRL-lpr mice. J Clin Invest. 1998; 101:364–371.
  • Chu RS, Targoni OS, Krieg AM, Lehmann PV, Harding CV. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J Exp Med. 1997; 186:1623–1631.
  • Austin HA III, Muenz LR, Joyce KM, Antonovych TT, Balow JW. Diffuse proliferative lupus nephritis: Identification of specific pathologic features affecting renal outcome. Kidney Int. 1984; 25:689–695.
  • Andrews BS, Eisenberg RA, Theofilopoulos AN, Izui S, Wilson CB, McConahey PJ, Murphy ED, Roths JB, Dixon FJ. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med. 1978; 148:1198–1215.
  • Wofsy D, Seaman W. Successful treatment of autoimmunity in NZB/NZW F1 mice with monoclonal antibody to L3T4. J Exp Med. 1985; 161:378–391.
  • Connolly K, Roubinian J, Wofsy D. Development of murine lupus in CD4-depleted NZB/NZW mice. Sustained inhibition of residual CD4+T cells is required to suppress autoimmunity. J Immunol. 1992; 149:3083–3088.
  • Richards H, Satoh M, Jennette J, Croker B, Yoshida H, Reeves W. Interferon-γ is required for lupus nephritis in mice treated with the hydrocarbon oil pristane. Kidney Int. 2001; 60:2173–2180.
  • Santiago M-L, Fossati L, Jacquet C, Muller W, Izui S, Reininger L. Interleukin-4 protects against a genetically linked lupus-like autoimmune syndrome. J Exp Med. 1997; 185:65–70.
  • Graham K, Vaysberg M, Kuo A, Utz P. Autoantigen arrays for multiplex analysis of antibody isotypes. Proteomics. 2006; 6:5720–5724.
  • Stein C, Subasinghe C, Sinozuka K, Coehn J. Physicochemical properties of phosphorothioate oligodeoxynucleotides. Nucl Acids Res. 1988; 16:3209–3221.
  • Wickstrom E. Oligodeoxynucleotide stability in subcellular extracts and culture media. J Biochem Biophys Methods. 1986; 13:97–102.
  • Christensen C, Shupe J, Nickerson K, Kashgarian M, Flavell R, Shlomchik M. 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.
  • 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 USA. 1996; 93:2879–2883.
  • Barrat FJ, Meeker T, Gregorio J, Chan JH, Uematsu S, Akira S, Chang B, Duramad O, Coffman RL. 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.
  • Vollmer J, Tluk S, Schmitz C, Hamm S, Jurk M, Forsbach A, Akira S, Kelly KM, Reeves WH, Bauer S, Krieg AM. Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J Exp Med. 2005; 202:1575–1585.
  • Savarese E, Chae O-W, Trowitzsch S, Weber G, Kastner B, Akira S, Wagner H, Schmid RM, Bauer S, Krug A. U1 small nuclear ribonucleoprotein immune complexes induce type I interferon in plasmacytoid dendritic cells through TLR7. Blood. 2006; 107:3229–3234.
  • Yasuda K, Richez C, Maciaszek JW, Agrawal N, Akira S, Marshak-Rothstein A, Rifkin IR. Murine dendritic cell type I IFN production induced by human igg-rna immune complexes is IFN regulatory factor (IRF)5 and IRF7 dependent and is required for IL-6 production. J Immunol. 2007; 178:6876–6885.
  • Patole PS, Grone H-J, Segerer S, Ciubar R, Belemezova E, Henger A, Kretzler M, Schlondorff D, Anders H-J. Viral double-stranded RNA aggravates lupus nephritis through Toll-like receptor 3 on glomerular mesangial cells and antigen-presenting cells. J Am Soc Nephrol. 2005; 16:1326–1338.
  • Kirou K, Lee C, George S, Louca K, Peterson M, Crow M. Activation of the interferon-alpha pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum. 2005; 52:1491–1503.
  • Berland R, Fernandez L, Kari E, Han J, Lomakin I, Akira S, Wortis H, Kearney J, Ucci A, Imanishi-Kari T. Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immunity. 2006; 25:429–440.
  • Lau C, Broughton C, Tabor A, Akira S, Flavell R, Mamula M, Christensen S, Shlomchik M, Biglianti G, Rifkin I, Marshak-Rothstein A. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J Exp Med. 2005; 202:1171–1177.
  • Diebold S, Kaisho T, Hemmi H, Akira S, Sousa CE. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science. 2004; 303:1529–1531.
  • Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S, Lipford G, Wagner H, Bauer S. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science. 2004; 303:1526–1529.
  • Lund J, Alexopoulou L, Sato A, Karow M, Adams N, Gale N, Iwasaki A, Flavell R. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci USA. 2004; 101:5598–5603.
  • Hemmi H, Kaisho T, Takeuchi O, Sato S, Sanjo H, Hoshino K, Horiuchi T, Tomizawa H, Takeda K, Akira S. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol. 2002; 3:196–200.
  • Du X, Poltorak A, Wei Y, Beutler B. Three novel mammalian toll-like receptors: Gene structure, expression, and evolution. Eur Cytokine Netw. 2000; 11:362–371.
  • Chuang T, Ulevitch R. Cloning and characterization of a sub-family of human toll-like receptors hTLR-7, hTLR-8, and hTLR-9. Eur Cytokine Netw. 2000; 11:372–378.
  • Pisitkun P, Deane J, Difilippantonio M, Tarasenko T, Saterthwaite A, Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science. 2006; 312:1669–1672.
  • Subramanian S, Tus K, Li QZ, Wang A, Tian XH, Zhou J, Liang C, Bartov G, McDaniel LD, Zhou ZJ, Schultz RA, Wakeland EK. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Natl Acad Sci USA. 2006; 103:9970–9975.
  • Dong L, Ito S, Ishii K, Klinman D. Suppressive oligodeoxynucleotides delay the onset of glomerulonephritis and prolong survival in lupus-prone NZB × NZW mice. Arthritis Rheumat. 2005; 52:651–658.
  • Patole PS, Zecher D, Pawar RD, Grone H-J, Schlondorff D, Anders H-J. G-rich DNA suppresses systemic lupus. J Am Soc Nephrol. 2005; 16:3273–3280.
  • Pawar RD, Ramanjaneyulu A, Kulkarni OP, Lech M, Segerer S, Anders H-J. 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.
  • Krieg A, Vollmer J. Toll-like receptors 7, 8, and 9: Linking innate immunity to autoimmunity. Immunol Rev. 2007; 220:251–269.

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