IFNα inducible models of murine SLE

Frontiers in Immunology

Volumn 4, Issue OCT, 2013, Pages

  Liu, Zheng ^a   Davidson, Anne ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Inflammation; Interferon a; Lupus; Mouse model; Nephritis

Indexed keywords

ABATACEPT; ALPHA INTERFERON; ANTIINFLAMMATORY AGENT; ATACICEPT; B CELL ACTIVATING FACTOR; CD137 ANTIBODY; CD40L ANTIBODY; CYCLOPHOSPHAMIDE; MICRORNA 15A; STROMAL CELL DERIVED FACTOR 1; TOLL LIKE RECEPTOR 7; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

B LYMPHOCYTE; CELL INFILTRATION; DENDRITIC CELL; IMMUNE RESPONSE; NEPHRITIS; NEW ZEALAND WHITE MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEINURIA; SHORT SURVEY; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE;

EID: 84885409854     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00306     Document Type: Short Survey

References (64)

1. Banchereau J, Pascual V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity (2006) 25(3):383-92. doi: 10.1016/j.immuni.2006.08.010.
2. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A (2003) 100(5):2610-5. doi:10.1073/pnas.0337679100.
3. Kirou KA, Lee C, George S, Louca K, Papagiannis IG, Peterson MG, et al. Coordinate overexpression of interferon-alpha-induced genes in systemic lupus erythematosus. Arthritis Rheum (2004) 50(12):3958-67. doi:10.1002/art.20798.
4. Bennett L, Palucka AK, Arce E, Cantrell V, Borvak J, Banchereau J, et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med (2003) 197(6):711-23. doi:10.1084/jem.20021553.
5. Cui Y, Sheng Y, Zhang X. Genetic susceptibility to SLE: recent progress from GWAS. J Autoimmun (2013) 41:25-33. doi:10.1016/j.jaut.2013.01.008.
6. Deng Y, Tsao BP. Genetic susceptibility to systemic lupus erythematosus in the genomic era. Nat Rev Rheumatol (2010) 6(12):683-92. doi:10.1038/nrrheum.2010.176.
7. Ng D, Gommerman JL. The regulation of immune responses by DC derived type I IFN. Front Immunol (2013) 4:94. doi:10.3389/fimmu.2013.00094.
8. Means TK, Latz E, Hayashi F, Murali MR, Golenbock DT, Luster AD. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J Clin Invest (2005) 115(2):407-17. doi:10.1172/JCI200523025.
9. Izaguirre A, Barnes BJ, Amrute S, Yeow WS, Megjugorac N, Dai J, et al. Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol (2003) 74(6):1125-38. doi:10.1189/jlb.0603255.
10. Hemmi H, Kaisho T, Takeda K, Akira S. The roles of Toll-like receptor 9, MyD88, and DNA-dependent protein kinase catalytic subunit in the effects of two distinct CpG DNAs on dendritic cell subsets. J Immunol (2003) 170(6):3059-64.
11. Lund J, Sato A, Akira S, Medzhitov R, Iwasaki A. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J Exp Med (2003) 198(3):513-20. doi:10.1084/jem.20030162.
12. Keating SE, Baran M, Bowie AG. Cytosolic DNA sensors regulating type I interferon induction. Trends Immunol (2011) 32(12):574-81. doi:10.1016/j.it.2011.08.004.
13. Kim T, Pazhoor S, Bao M, Zhang Z, Hanabuchi S, Facchinetti V, et al. Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc Natl Acad Sci U S A (2010) 107(34):15181-6. doi:10.1073/pnas.1006539107.
14. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol (2007) 8(5):487-96. doi:10.1038/ni1457.
15. Kaplan MJ. Neutrophils in the pathogenesis and manifestations of SLE. Nat Rev Rheumatol (2011) 7(12):691-9. doi:10.1038/nrrheum.2011.132.
16. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A (2010) 107(21):9813-8. doi:10.1073/pnas.0909927107.
17. Elkon KB, Wiedeman A. Type I IFN system in the development and manifestations of SLE. Curr Opin Rheumatol (2012) 24(5):499-505. doi:10.1097/BOR.0b013e3283562c3e.
18. Kiefer K, Oropallo MA, Cancro MP, Marshak-Rothstein A. Role of type I interferons in the activation of autoreactive B cells. Immunol Cell Biol (2012) 90(5):498-504. doi:10.1038/icb.2012.10.
19. Blanco P, Palucka AK, Gill M, Pascual V, Banchereau J. Induction of dendritic cell differentiation by IFN-alpha in systemic lupus erythematosus. Science (2001) 294(5546):1540-3. doi:10.1126/science.1064890.
20. Mathian A, Weinberg A, Gallegos M, Banchereau J, Koutouzov S. IFN-alpha induces early lethal lupus in preautoimmune (New Zealand Black x New Zealand White) F1 but not in BALB/c mice. J Immunol (2005) 174(5):2499-506.
21. Litinskiy MB, Nardelli B, Hilbert DM, He B, Schaffer A, Casali P, et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol (2002) 3(9):822-9. doi:10.1038/ni829.
22. Groom JR, Fletcher CA, Walters SN, Grey ST, Watt SV, Sweet MJ, et al. BAFF and MyD88 signals promote a lupus like disease independent of T cells. J Exp Med (2007) 204(8):1959-71. doi:10.1084/jem.20062567.
23. Jego G, Palucka AK, Blanck JP, Chalouni C, Pascual V, Banchereau J. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity (2003) 19(2):225-34. doi:10.1016/S1074-7613(03)00208-5.
24. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J Exp Med (1999) 189(3):521-30. doi:10.1084/jem.189.3.521.
25. Le Bon A, Thompson C, Kamphuis E, Durand V, Rossmann C, Kalinke U, et al. Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J Immunol (2006) 176(4):2074-8.
26. Santiago-Raber ML, Baccala R, Haraldsson KM, Choubey D, Stewart TA, Kono DH, et al. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J Exp Med (2003) 197(6):777-88. doi:10.1084/jem.20021996.
27. Agrawal H, Jacob N, Carreras E, Bajana S, Putterman C, Turner S, et al. Deficiency of type I IFN receptor in lupus-prone New Zealand mixed 2328 mice decreases dendritic cell numbers and activation and protects from disease. J Immunol (2009) 183(9):6021-9. doi:10.4049/jimmunol.0803872.
28. Braun D, Geraldes P, Demengeot J. Type I Interferon controls the onset and severity of autoimmune manifestations in lpr mice. J Autoimmun (2003) 20(1):15-25. doi:10.1016/S0896-8411(02)00109-9.
29. Nickerson KM, Cullen JL, Kashgarian M, Shlomchik MJ. Exacerbated autoimmunity in the absence of TLR9 in MRL.Fas(lpr) mice depends on Ifnar1. J Immunol (2013) 190(8):3889-94. doi:10.4049/jimmunol.1203525.
30. Ramanujam M, Wang X, Huang W, Liu Z, Schiffer L, Tao H, et al. Similarities and differences between selective and nonselective BAFF blockade in murine SLE. J Clin Invest (2006) 116(3):724-34. doi:10.1172/JCI26385.
31. Wang X, Huang W, Mihara M, Sinha J, Davidson A. Mechanism of action of combined short-term CTLA4Ig and anti-CD40 ligand in murine systemic lupus erythematosus. J Immunol (2002) 168(4):2046-53.
32. Lu Q, Shen N, Li XM, Chen SL. Genomic view of IFN-alpha response in pre-autoimmune NZB/W and MRL/lpr mice. Genes Immun (2007) 8(7):590-603. doi:10.1038/sj.gene.6364421.
33. Carpenter DF, Steinberg AD, Schur PH, Talal N. The pathogenesis of autoimmunity in New Zealand mice. II. Acceleration of glomerulonephritis by polyinosinic-polycytidylic acid. Lab Invest (1970) 23(6):628-34.
34. Liu Z, Bethunaickan R, Huang W, Lodhi U, Solano I, Madaio MP, et al. Interferon-alpha accelerates murine systemic lupus erythematosus in a T cell-dependent manner. Arthritis Rheum (2011) 63(1):219-29. doi:10.1002/art.30087.
35. Yuan Y, Kasar S, Underbayev C, Vollenweider D, Salerno E, Kotenko SV, et al. Role of microRNA-15a in autoantibody production in interferon-augmented murine model of lupus. Mol Immunol (2012) 52(2):61-70. doi:10.1016/j.molimm.2012.04.007.
36. Mathian A, Gallegos M, Pascual V, Banchereau J, Koutouzov S. Interferon-alpha induces unabated production of short-lived plasma cells in pre-autoimmune lupus-prone (NZBxNZW)F1 mice but not in BALB/c mice. Eur J Immunol (2011) 41(3):863-72. doi:10.1002/eji.201040649.
37. Hoyer BF, Moser K, Hauser AE, Peddinghaus A, Voigt C, Eilat D, et al. Short-lived plasmablasts and long-lived plasma cells contribute to chronic humoral autoimmunity in NZB/W mice. J Exp Med (2004) 199(11):1577-84. doi:10.1084/jem.20040168.
38. dalid-Peralta LA, Mathian A, Tran T, Delbos L, Durand-Gasselin I, Berrebi D, et al. Leukocytes and the kidney contribute to interstitial inflammation in lupus nephritis. Kidney Int (2008) 73(2):172-80. doi:10.1038/sj.ki.5002625.
39. Jacob N, Guo S, Mathian A, Koss MN, Gindea S, Putterman C, et al. B Cell and BAFF dependence of IFN-alpha-exaggerated disease in systemic lupus erythematosus-prone NZM 2328 mice. J Immunol (2011) 186(8):4984-93. doi:10.4049/jimmunol.1000466.
40. Thacker SG, Zhao W, Smith CK, Luo W, Wang H, Vivekanandan-Giri A, et al. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum (2012) 64(9):2975-85. doi:10.1002/art.34504.
41. Pisitkun P, Deane JA, Difilippantonio MJ, Tarasenko T, Satterthwaite AB, Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science (2006) 312(5780):1669-72. doi:10.1126/science.1124978.
42. Yoshida H, Fujiwara H, Fujiwara T, Ikehara S, Hamashima Y. Quantitative analysis of myocardial infarction in (NZW x BXSB)F1 hybrid mice with systemic lupus erythematosus and small coronary artery disease. Am J Pathol (1987) 129(3):477-85.
43. Baccala R, Gonzalez-Quintial R, Schreiber RD, Lawson BR, Kono DH, Theofilopoulos AN. Anti-IFN-alpha/beta receptor antibody treatment ameliorates disease in lupus-predisposed mice. J Immunol (2012) 189(12):5976-84. doi:10.4049/jimmunol.1201477.
44. Ramanujam M, Kahn P, Huang W, Tao H, Madaio MP, Factor SM, et al. Interferon-alpha treatment of female (NZW x BXSB)F(1) mice mimics some but not all features associated with the Yaa mutation. Arthritis Rheum (2009) 60(4):1096-101. doi:10.1002/art.24414.
45. Moisini I, Huang W, Bethunaickan R, Sahu R, Ricketts PG, Akerman M, et al. The Yaa locus and IFN-alpha fine-tune germinal center B cell selection in murine systemic lupus erythematosus. J Immunol (2012) 189(9):4305-12. doi:10.4049/jimmunol.1200745.
46. Fairhurst AM, Mathian A, Connolly JE, Wang A, Gray HF, George TA, et al. Systemic IFN-alpha drives kidney nephritis in B6.Sle123 mice. Eur J Immunol (2008) 38(7):1948-60. doi:10.1002/eji.200837925.
47. Donnelly RP, Kotenko SV. Interferon-lambda: a new addition to an old family. J Interferon Cytokine Res (2010) 30(8):555-64. doi:10.1089/jir.2010.0078.
48. Tang Y, Luo X, Cui H, Ni X, Yuan M, Guo Y, et al. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum (2009) 60(4):1065-75. doi:10.1002/art.24436.
49. Pan Y, Jia T, Zhang Y, Zhang K, Zhang R, Li J, et al. MS2 VLP-based delivery of microRNA-146a inhibits autoantibody production in lupus-prone mice. Int J Nanomed (2012) 7:5957-67. doi:10.2147/IJN.S37990.
50. Zagury D, Le Buanec H, Mathian A, Larcier P, Burnett R, Amoura Z, et al. IFNalpha kinoid vaccine-induced neutralizing antibodies prevent clinical manifestations in a lupus flare murine model. Proc Natl Acad Sci U S A (2009) 106(13):5294-9. doi:10.1073/pnas.0900615106.
51. Mathian A, Amoura Z, Adam E, Colaone F, Hoekman MF, Dhellin O, et al. Active immunisation of human interferon alpha transgenic mice with a human interferon alpha Kinoid induces antibodies that neutralise interferon alpha in sera from patients with systemic lupus erythematosus. Ann Rheum Dis (2011) 70(6):1138-43. doi:10.1136/ard.2010.141101.
52. Lauwerys BR, Hachulla E, Spertini F, Lazaro E, Jorgensen C, Mariette X, et al. Down-regulation of interferon signature in systemic lupus erythematosus patients by active immunization with interferon alpha-kinoid. Arthritis Rheum (2013) 65(2):447-56. doi:10.1002/art.37785.
53. Gross JA, Johnston J, Mudri S, Enselman R, Dillon SR, Madden K, et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature (2000) 404(6781):995-9. doi:10.1038/35010115.
54. Liu Z, Bethunaickan R, Huang W, Ramanujam M, Madaio MP, Davidson A. IFN-{alpha} confers resistance of systemic lupus erythematosus nephritis to therapy in NZB/W F1 mice. J Immunol (2011) 187(3):1506-13. doi:10.4049/jimmunol.1004142.
55. Daikh DI, Finck BK, Linsley PS, Hollenbaugh D, Wofsy D. Long-term inhibition of murine lupus by brief simultaneous blockade of the B7/CD28 and CD40/gp39 costimulation pathways. J Immunol (1997) 159(7):3104-8.
56. Finck BK, Linsley PS, Wofsy D. Treatment of murine lupus with CTLA4Ig. Science (1994) 265(5176):1225-7. doi:10.1126/science.7520604.
57. Bethunaickan R, Sahu R, Liu Z, Tang YT, Huang W, Edegbe O, et al. Anti-tumor necrosis factor alpha treatment of interferon-alpha-induced murine lupus nephritis reduces the renal macrophage response but does not alter glomerular immune complex formation. Arthritis Rheum (2012) 64(10):3399-408. doi:10.1002/art.34553.
58. Foell J, Strahotin S, O'Neil SP, McCausland MM, Suwyn C, Haber M, et al. CD137 costimulatory T cell receptor engagement reverses acute disease in lupus-prone NZB x NZW F1 mice. J Clin Invest (2003) 111(10):1505-18. doi:10.1172/JCI17662.
59. Mittler RS, Bailey TS, Klussman K, Trailsmith MD, Hoffmann MK. Anti-4-1BB monoclonal antibodies abrogate T cell-dependent humoral immune responses in vivo through the induction of helper T cell anergy. J Exp Med (1999) 190(10):1535-40. doi:10.1084/jem.190.10.1535.
60. Schiffer L, Sinha J, Wang X, Huang W, von Gersdorff G, Schiffer M, et al. Short term administration of costimulatory blockade and cyclophosphamide induces remission of systemic lupus erythematosus nephritis in NZB/W F1 mice by a mechanism downstream of renal immune complex deposition. J Immunol (2003) 171(1):489-97.
61. McBride JM, Jiang J, Abbas AR, Morimoto A, Li J, Maciuca R, et al. Safety and pharmacodynamics of rontalizumab in patients with systemic lupus erythematosus: results of a phase I, placebo-controlled, double-blind, dose-escalation study. Arthritis Rheum (2012) 64(11):3666-76. doi:10.1002/art.34632.
62. Bacher N, Raker V, Hofmann C, Graulich E, Schwenk M, Baumgrass R, et al. Interferon-alpha suppresses cAMP to disarm human regulatory T cells. Cancer Res (2013) 73(18):5647-56. doi:10.1158/0008-5472.CAN-12-3788.
63. Kalunian K, Merrill J, Maciuca R, Ouyang W, McBride JM, Townsend MJ, et al. Efficacy and safety of rontalizumab (anti-interferon alpha) in SLE subjects with restricted immunosuppressant use: results of a randomized, double-blind, placebo-controlled phase 2 study. Arthritis Rheum (2012) 64(Suppl 10):S1111.
64. Petri M, Wallace DJ, Sindler A, Chindalore V, Kalunian K, Mysler E, et al. Sifalimumab, a human anti-interferon-a monoclonal antibody, in systemic lupus erythematosus: a phase I randomized, controlled, dose-escalation study. Arthritis Rheum (2013) 65(4):1011-21. doi:10.1002/art.37824.