Epicutaneous application of toll-like receptor 7 agonists leads to systemic autoimmunity in wild-type mice: A new model of systemic lupus erythematosus

Arthritis and Rheumatology

Volumn 66, Issue 3, 2014, Pages 694-706

  Yokogawa, Maki ^a   Takaishi, Mikiro ^a   Nakajima, Kimiko ^a   Kamijima, Reiko ^a   Fujimoto, Chisa ^a   Kataoka, Sayo ^a   Terada, Yoshio ^a   Sano, Shigetoshi ^a  

^a KOCHI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CELL ANTIBODY; CREATININE; DOUBLE STRANDED DNA; IFNA PROTEIN; IMIQUIMOD; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; MX1 PROTEIN; PLASMACYTOID DENDRITIC CELL ANTIGEN 1 ANTIBODY; PROTEIN; RESIQUIMOD; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CARDITIS; CELL FUNCTION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE SEVERITY; DRUG INDUCED DISEASE; DRUG SAFETY; EDEMA; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GLOMERULONEPHRITIS; HEART; HEPATITIS; IMMUNITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOLOGY; IN VIVO STUDY; KIDNEY; KNOCKOUT MOUSE; LIVER; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PHOTOSENSITIVITY; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEINURIA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN; SKIN PHOTOSENSITIVITY; SPLEEN; SPLENOMEGALY; SYSTEMIC AUTOIMMUNITY; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC THERAPY; THROMBOCYTOPENIA; TISSUE LEVEL; TRANSGENIC MOUSE; TREATMENT DURATION; ULTRAVIOLET B RADIATION; UPREGULATION; WILD TYPE;

ADMINISTRATION, CUTANEOUS; AMINOQUINOLINES; ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; DISEASE MODELS, ANIMAL; IMIDAZOLES; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; SKIN; SPLEEN; TOLL-LIKE RECEPTOR 7;

EID: 84896264633     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.38298     Document Type: Article

References (50)

1. Kotzin BL. Systemic lupus erythematosus. Cell 1996;85:303-6
2. Christensen SR, Shlomchik MJ. Regulation of lupus-related autoantibody production and clinical disease by Toll-like receptors. Semin Immunol 2007;19:11-23
3. Ewald SE, Barton GM. Nucleic acid sensing Toll-like receptors in autoimmunity. Curr Opin Immunol 2011;23:3-9
4. Gilliet M, Lande R. Antimicrobial peptides and self-DNA in autoimmune skin inflammation. Curr Opin Immunol 2008;20: 401-7
5. Pascual V, Farkas L, Banchereau J. Systemic lupus erythematosus: all roads lead to type I interferons. Curr Opin Immunol 2006;18: 676-82
6. Berland R, Fernandez L, Kari E, Han JH, Lomakin I, Akira S, et al. Toll-like receptor 7-dependent loss of B cell tolerance in pathogenic autoantibody knockin mice. Immunity 2006;25:429-40
7. Pasare C, Medzhitov R. Control of B-cell responses by Toll-like receptors. Nature 2005;438:364-8
8. Subramanian S, Tus K, Li QZ, Wang A, Tian XH, Zhou J, et al. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc Natl Acad Sci U S A 2006;103:9970-5
9. Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S. Autoreactive B cell responses to RNArelated antigens due to TLR7 gene duplication. Science 2006;312: 1669-72
10. Santiago-Raber ML, Baudino L, Izui S. Emerging roles of TLR7 and TLR9 in murine SLE. J Autoimmun 2009;33:231-8
11. Santiago-Raber ML, Kikuchi S, Borel P, Uematsu S, Akira S, Kotzin BL, et al. Evidence for genes in addition to Tlr7 in the Yaa translocation linked with acceleration of systemic lupus erythematosus. J Immunol 2008;181:1556-62
12. Berghofer B, Frommer T, Haley G, Fink L, Bein G, Hackstein H. TLR7 ligands induce higher IFN-α production in females. J Immunol 2006;177:2088-96
13. Anders HJ. Pseudoviral immunity: a novel concept for lupus. Trends Mol Med 2009;15:553-61
14. Amano H, Amano E, Moll T, Marinkovic D, Ibnou-Zekri N, Martinez-Soria E, et al. The Yaa mutation promoting murine lupus causes defective development of marginal zone B cells. J Immunol 2003;170:2293-301
15. Bolland S, Yim YS, Tus K, Wakeland EK, Ravetch JV. Genetic modifiers of systemic lupus erythematosus in FcγRIIB mice. J Exp Med 2002;195:1167-74
16. Deane JA, Pisitkun P, Barrett RS, Feigenbaum L, Town T, Ward JM, et al. Control of Toll-like receptor 7 expression is essential to restrict autoimmunity and dendritic cell proliferation. Immunity 2007;27:801-10
17. 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
18. Nickerson KM, Christensen SR, Shupe J, Kashgarian M, Kim D, Elkon K, et al. TLR9 regulates TLR7- and MyD88-dependent autoantibody production and disease in a murine model of lupus. J Immunol 2010;184:1840-8
19. Reeves WH, Lee PY, Weinstein JS, Satoh M, Lu L. Induction of autoimmunity by pristane and other naturally occurring hydrocarbons. Trends Immunol 2009;30:455-64
20. 1 recipients carrying mutations at H-2K and/or I-A. J Exp Med 1983;157:755-71
21. Kool M, van Loo G, Waelput W, De Prijck S, Muskens F, Sze M, et al. The ubiquitin-editing protein A20 prevents dendritic cell activation, recognition of apoptotic cells, and systemic autoimmunity. Immunity 2011;35:82-96
22. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol 2005;23:901-44
23. + dendritic cells in murine lupus and preferential chemotaxis of B1 cells towards BLC. J Exp Med 2001;193:1393-402
24. Azeredo da Silveira S, Kikuchi S, Fossati-Jimack L, Moll T, Saito T, Verbeek JS, et al. Complement activation selectively potentiates the pathogenicity of the IgG2b and IgG3 isotypes of a high affinity anti-erythrocyte autoantibody. J Exp Med 2002;195: 665-72
25. Savitsky DA, Yanai H, Tamura T, Taniguchi T, Honda K. Contribution of IRF5 in B cells to the development of murine SLE-like disease through its transcriptional control of the IgG2a locus. Proc Natl Acad Sci U S A 2010;107:10154-9
26. Banchereau J, Pascual V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 2006; 25:383-92
27. Gilliet M, Conrad C, Geiges M, Cozzio A, Thurlimann W, Burg G, et al. Psoriasis triggered by Toll-like receptor 7 agonist imiquimod in the presence of dermal plasmacytoid dendritic cell precursors. Arch Dermatol 2004;140:1490-5
28. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-α in systemic lupus erythematosus. Science 2001;294:1540-3
29. Robak E, Smolewski P, Wozniacka A, Sysa-Jedrzejowska A, Robak T. Clinical significance of circulating dendritic cells in patients with systemic lupus erythematosus. Mediators Inflamm 2004;13:171-80
30. Melen K, Ronni T, Broni B, Krug RM, von Bonsdorff CH, Julkunen I. Interferon-induced Mx proteins form oligomers and contain a putative leucine zipper. J Biol Chem 1992;267: 25898-907
31. Klinkhoff AV, Thompson CR, Reid GD, Tomlinson CW. M-mode and two-dimensional echocardiographic abnormalities in systemic lupus erythematosus. JAMA 1985;253:3273-7
32. 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
33. Fukui R, Saitoh S, Kanno A, Onji M, Shibata T, Ito A, et al. Unc93B1 restricts systemic lethal inflammation by orchestrating Toll-like receptor 7 and 9 trafficking. Immunity 2011;35:69-81
34. Fukui R, Miyake K. Controlling systems of nucleic acid sensing- TLRs restrict homeostatic inflammation. Exp Cell Res 2012;318: 1461-6
35. Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN. TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med 2007;13: 543-51
36. Blasius AL, Giurisato E, Cella M, Schreiber RD, Shaw AS, Colonna M. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J Immunol 2006;177:3260-5
37. Takagi H, Fukaya T, Eizumi K, Sato Y, Sato K, Shibazaki A, et al. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 2011;35:958-71
38. Baenziger S, Heikenwalder M, Johansen P, Schlaepfer E, Hofer U, Miller RC, et al. Triggering TLR7 in mice induces immune activation and lymphoid system disruption, resembling HIV-mediated pathology. Blood 2009;113:377-88
39. Damm J, Wiegand F, Harden LM, Gerstberger R, Rummel C, Roth J. Fever, sickness behavior, and expression of inflammatory genes in the hypothalamus after systemic and localized subcutaneous stimulation of rats with the Toll-like receptor 7 agonist imiquimod. Neuroscience 2012;201:166-83
40. Burns CA, Brown MD. Imiquimod for the treatment of skin cancer. Dermatol Clin 2005;23:151-64, vii
41. Van der Fits L, Mourits S, Voerman JS, Kant M, Boon L, Laman JD, et al. Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol 2009;182: 5836-45
42. Nestle FO, Conrad C, Tun-Kyi A, Homey B, Gombert M, Boyman O, et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-α production. J Exp Med 2005;202:135-43
43. Farkas L, Beiske K, Lund-Johansen F, Brandtzaeg P, Jahnsen FL. Plasmacytoid dendritic cells (natural interferon-α/β-producing cells) accumulate in cutaneous lupus erythematosus lesions. Am J Pathol 2001;159:237-43
44. Wollenberg A, Wagner M, Gunther S, Towarowski A, Tuma E, Moderer M, et al. Plasmacytoid dendritic cells: a new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J Invest Dermatol 2002;119:1096-102
45. Barr KL, Konia TH, Fung MA. Lupus erythematosus-like imiquimod reaction: a diagnostic pitfall. J Cutan Pathol 2011;38: 346-50
46. Baudino L, Yoshinobu K, Morito N, Santiago-Raber ML, Izui S. Role of endogenous retroviruses in murine SLE. Autoimmun Rev 2010;10:27-34
47. Meller S, Winterberg F, Gilliet M, Muller A, Lauceviciute I, Rieker J, et al. Ultraviolet radiation-induced injury, chemokines, and leukocyte recruitment: an amplification cycle triggering cutaneous lupus erythematosus. Arthritis Rheum 2005;52:1504-16
48. Bernard JJ, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J, Borkowski AW, et al. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med 2012;18:1286-90
49. Gregorio J, Meller S, Conrad C, Di Nardo A, Homey B, Lauerma A, et al. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J Exp Med 2010;207: 2921-30
50. Guiducci C, Tripodo C, Gong M, Sangaletti S, Colombo MP, Coffman RL, et al. Autoimmune skin inflammation is dependent on plasmacytoid dendritic cell activation by nucleic acids via TLR7 and TLR9. J Exp Med 2010;207:2931-42.