Interferon regulatory factor-1 gene deletion decreases glomerulonephritis in MRL/lpr mice

European Journal of Immunology

Volumn 36, Issue 5, 2006, Pages 1296-1308

  Reilly, Christopher M ^a,b   Olgun, Selen ^b   Goodwin, David ^a   Gogal Jr , Robert M ^a,b   Santo, Arben ^b   Romesburg, Jason W ^b   Ahmed, S Ansar ^a   Gilkeson, Gary S ^c,d  

^a VIRGINIA MARYLAND REGIONAL COLLEGE OF VETERINARY MEDICINE   (United States)

^b Via College of Osteopathic Medicine ^*  (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Interferon regulatory factor 1; Kidney; Lupus; Mouse; MRL

Indexed keywords

AUTOANTIBODY; CD4 ANTIGEN; CD8 ANTIGEN; DOUBLE STRANDED DNA ANTIBODY; GAMMA INTERFERON; HERMES ANTIGEN; IMMUNOGLOBULIN G; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 12; INTERLEUKIN 2 RECEPTOR ALPHA; LIPOPOLYSACCHARIDE; MESSENGER RNA; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CELL CULTURE; CELL FUNCTION; CONTROLLED STUDY; CULTURE MEDIUM; DERMATITIS; DISEASE COURSE; FLOW CYTOMETRY; GENE DELETION; GLOMERULONEPHRITIS; IMMUNE COMPLEX DEPOSITION; INFLAMMATION; KIDNEY CELL; MESANGIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN URINE LEVEL; PROTEINURIA; SURVIVAL RATE; T LYMPHOCYTE; WESTERN BLOTTING; WILD TYPE;

ANIMALS; FLOW CYTOMETRY; GLOMERULAR MESANGIUM; GLOMERULONEPHRITIS; IMMUNOGLOBULIN G; INTERFERON REGULATORY FACTOR-1; INTERFERON TYPE II; INTERLEUKIN-12; KIDNEY; LIPOPOLYSACCHARIDES; LUPUS NEPHRITIS; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; RNA, MESSENGER; STAT1 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY;

EID: 33646597302     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200535245     Document Type: Article

References (71)

1. Madaio, M. P., B cells and autoantibodies in the pathogenesis of lupus nephritis. Immunol. Res. 1998. 17: 123-132.
2. Chan, O. T., Madaio, M. P. and Shlomchik, M. J., The central and multiple roles of B cells in lupus pathogenesis. Immunol. Rev. 1999. 169: 107-121.
3. Theofilopoulos, A. N., Singer, P. A., Kofler, R., Kono, D. H., Duchosal, M. A. and Balderas, R. S., B and T cell antigen receptor repertoires in lupus/arthritis murine models. Springer Semin. Immunopathol. 1989. 11: 335-368.
4. Kuroiwa, T. and Lee, E. G., Cellular interactions in the pathogenesis of lupus nephritis: The role of T cells and macrophages in the amplification of the inflammatory process in the kidney. Lupus 1998. 7: 597-603.
5. Peng, S. L. and Craft, J., The regulation of murine lupus. Ann. N. Y. Acad. Sci. 1997. 815: 128-138.
6. Kikawada, E., Lenda, D. M. and Kelley, V. R., IL-12 deficiency in MRL-Fas(lpr) mice delays nephritis and intrarenal IFN-gamma expression, and diminishes systemic pathology. J. Immunol. 2003. 170: 3915-3925.
7. Theofilopoulos, A. N. and Kono, D. H., Mechanisms and genetics of autoimmunity. Ann. N. Y. Acad. Sci. 1998. 841: 225-235.
8. Shimizu, S., Nakashima, H., Masutani, K., Inoue, Y., Miyake, K., Akahoshi M., Tanaka, Y. et al., Anti-monocyte chemoattractant protein-1 gene therapy attenuates nephritis in MRL/lpr mice. Rheumatology (Oxford) 2004. 43: 1121-1128.
9. Kinoshita, K., Tesch, G., Schwarting, A., Maron, R., Sharpe, A. H. and Kelley, V. R., Costimulation by B7-1 and B7-2 is required for autoimmune disease in MRL-Faslpr mice. J. Immunol. 2000. 164: 6046-6056.
10. Schwarting, A., Tesch, G., Kinoshita, K., Maron, R., Weiner, H. L. and Kelley, V. R., IL-12 drives IFN-gamma-dependent autoimmune kidney disease in MRL-Fas(lpr) mice. J. Immunol. 1999. 163: 6884-6891.
11. Squadrito, G. L. and Pryor, W. A., Oxidative chemistry of nitric oxide: The roles of superoxide, peroxynitrite, and carbon dioxide. Free Radic. Biol. Med. 1998. 25: 392-403.
12. Braun, D., Geraldes, P. and Demengeot, J., Type I interferon controls the onset and severity of autoimmune manifestations in lpr mice. J. Autoimmun. 2003. 20: 15-25.
13. Schwarting, A., Wada, T., Kinoshita, K., Tesch, G. and Kelley, V. R., IFN-gamma receptor signaling is essential for the initiation, acceleration, and destruction of autoimmune kidney disease in MRL-Fas(lpr) mice. J. Immunol. 1998. 161: 494-503.
14. Cattell, V. and Jansen, A., Inducible nitric oxide synthase in inflammation. Histochem. J. 1995. 27: 777-784.
15. Theofilopoulos, A. N., Koundouris, S., Kono, D. H. and Lawson, B. R., The role of IFN-gamma in systemic lupus erythematosus: A challenge to the Th1/Th2 paradigm in autoimmunity. Arthritis Res. 2001. 3: 136-141.
16. Wieland, C. W., Siegmund, B., Senaldi, G., Vasil, M. L., Dinarello, C. A. and Fantuzzi, G., Pulmonary inflammation induced by Pseudomonas aeruginosa lipopolysaccharide, phospholipase C, and exotoxin A: Role of interferon regulatory factor 1. Infect. Immun. 2002. 70: 1352-1358.
17. Frank, S., Zacharowski, K., Wray, G. M., Thiemermann, C. and Pfeilschifter, J., Identification of copper/zinc superoxide disimitase as a novel nitric oxide-regulated gene in rat glomerular mesangial cells and kidneys of endotoxemic rats. FASEB J. 1999. 13: 869-882.
18. Oates, J. C., Levesque, M. C., Hobbs, M. R., Smith, E. G., Molano, I. D., Page, G. P., Hill, B. S. et al., Nitric oxide synthase 2 promoter polymorphisms and systemic lupus erythematosus in African-Americans. J. Rheumatol. 2003. 30: 60-67.
19. Saura, M., Zaragoza, C., Bao, C., McMillan, A. and Lowenstein, C. J., Interaction of interferon regulatory factor-1 and nuclear factor kappaB during activation of inducible nitric oxide synthase transcription. J. Mol. Biol. 1999. 289: 459-471.
20. Ko, J., Gendron-Fitzpatrick, A. and Splitter, G. A., Susceptibility of IFN regulatory factor-1 and IFN consensus sequence binding protein-deficient mice to brucellosis. J. Immunol. 2002. 168: 2433-2440.
21. Nakazawa, T., Satoh, J., Takahashi, K., Sakata, Y., Ikehata, F., Takizawa, Y., Bando, S. I. et al., Complete suppression of insulitis and diabetes in NOD mice lacking interferon regulatory factor-1. J. Autoimmun. 2001. 17: 119-125.
22. Pollard, K. M., Hultman, P. and Kono, D. H., Using single-gene deletions to identify checkpoints in the progression of systemic autoimmunity. Ann. N. Y. Acad. Sci. 2003. 987: 236-239.
23. Peng, S. L., Transcription factors in the pathogenesis of autoimmunity. Clin. Immunol. 2004. 110: 112-123.
24. Saito, H., Tada, S., Ebinuma, H., Wakabayashi, K., Takagi, T., Saito, Y., Nakamoto, N. et al., Interferon regulatory factor 1 promoter polymorphism and response to type 1 interferon. J. Cell. Biochem. 2001. 81 Suppl 36: 191-200.
25. Lee, K. Y., Anderson, E., Madani, K. and Rosen, G. D., Loss of STAT1 expression confers resistance to IFN-gamma-induced apoptosis in ME180 cells. FFBS Lett. 1999. 459: 323-326.
26. Jacobson, B. A., Rothstein, T. L. and Marshak-Rothstein, A., Unique site of IgG2a and rheumatoid factor production in MRL/lpr mice. Immunol. Rev. 1997. 156: 103-110.
27. Baechler, E. C., Batliwalla, F. M., Karypis, G., Gaffney, P. M., Ortmann, W. A., Espe, K. J., Shark, K. B. et al., Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl. Acad. Sci. USA 2003. 100: 2610-2615.
28. Baechler, E. C., Batliwalla, F. M., Karypis, G., Gaffney, P. M., Moser, K., Ortmann, W. A., Espe, K. J. et al., Expression levels for many genes in human peripheral blood cells are highly sensitive to ex vivo incubation. Genes Immun. 2004. 5: 347-353.
29. Mamane, Y., Heylbroeck, C., Genin, P., Algarte, M., Servant, M. J., LePage, C., DeLuca, C. et al., Interferon regulatory factors: The next generation. Gene 1999. 237: 1-14.
30. Kirou, K. A., Lee, C., George, S., Louca, K., Papagiannis, I. G., Peterson, M. G., Ly, N. et al., Coordinate overexpression. of interferon-alpha-induced genes in systemic lupus erythematosus. Arthritis Rheum. 2004. 50: 3958-3967.
31. Siegmund, B., Sennello, J. A., Lehr, H. A., Senaldi G., Dinarello, C. A. and Fantuzzi, G., Frontline: Interferon regulatory factor-1 as a protective gene in intestinal inflammation: Role of TCR gamma delta T cells and interleukin-18-binding protein. Eur. J. Immunol. 2004. 34: 2356-2364.
32. Kashem, A., Endoh, M., Yano, N., Yamauchi, F., Nomoto, Y. and Sakai, H., Expression of inducible-NOS in human glomerulonephritis: The possible source is infiltrating monocytes/macrophages. Kidney Int. 1996. 50: 392-399.
33. Jansen, A., Cook, T., Taylor, G. M., Largen, P., Riveros-Moreno, V., Moncada, S. and Cattell, V., Induction of nitric oxide synthase in rat immune complex glomerulonephritis. Kidney Int. 1994. 45: 1215-1219.
34. Kleinert, H., Pautz, A., Linker, K. and Schwarz, P. M., Regulation of the expression of inducible nitric oxide synthase. Eur J. Pharmacol. 2004. 500: 255-266.
35. Kleinert, H., Schwarz, P. M. and Forstermann, U., Regulation of the expression of inducible nitric oxide synthase. Biol. Chem. 2003. 384: 1343-1364.
36. Gao, J. J., Morrison, D. C., Parmely, T. J., Russell, S. W. and Murphy, W. J., An interferon-gamma-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-gamma and lipopoly-saccharide. J. Biol. Chem. 1997. 272: 1226-1230.
37. Bogdan, C., Vodovotz, Y., Paik, J., Xie, Q. W. and Nathan, C., Traces of bacterial lipopolysaccharide suppress IFN-gamma-induced nitric oxide synthase gene expression in primary mouse macrophages. J. Immunol. 1993. 151: 301-309.
38. Wang, I. M., Contursi, C., Masumi, A., Ma, X., Trinchieri, G. and Ozato, K., An IFN-gamma-inducible transcription factor, IFN consensus sequence binding protein (ICSBP), stimulates IL-12 p40 expression in macrophages. J. Immunol. 2000. 165: 271-279.
39. Salkowski, C. A., Kopydlowski, K., Blanco, J., Cody, M. J., McNally, R. and Vogel, S. N., IL-12 is dysregulated in macrophages from IRF-1 and IRF-2 knockout mice. J. Immunol. 1999. 163: 1529-1536.
40. Huang, F. P., Feng, G. J., Lindop, G., Stott, D. I. and Liew, F. Y., The role of interleukin 12 and nitric oxide in the development of spontaneous autoimmune disease in MRL:MP-lpr:lpr mice. J. Exp. Med. 1996. 183: 1447-1459.
41. Fantuzzi, G., Reed, D., Qi, M., Scully, S., Dinarello, C. A. and Senaldi, G., Role of interferon regulatory factor-1 in the regulation of IL-18 production and activity. Eur. J. Immunol. 2001. 31: 369-375.
42. Tada, Y., Ho, A., Matsuyama, T. and Mak, T. W., Reduced incidence and severity of antigen-induced autoimmune diseases in mice lacking interferon regulatory factor-1. J. Exp. Med. 1997. 185: 231-238.
43. Tan, R. S., Kara, A. U., Feng, C., Asano, Y. and Sinniah R., Differential interleukin-10 expression in interferon regulatory factor-1 deficient mice during Plasmodium berghei blood-stage infection. Parasite Immunol. 2000. 22: 425-435.
44. + regulatory T cells inhibit experimental anti-glomerular basement membrane glomerulonephritis in mice. J. Am. Soc. Nephrol. 2005. 16: 1360-1370.
45. Crispin, J. C., Martinez, A. and Alcocer-Varela, J., Quantification of regulatory T cells in patients with systemic lupus erythematosus. J. Autoimmun. 2003. 21: 273-276.
46. + T cells permits the development of spontaneous lupus-like disease in mice, and can be reversed by induction of mucosal tolerance to histone peptide autoantigen. Lupus 2004. 13: 192-200.
47. + T-regulatory cell subset has optimal suppressive and proliferative potential. Am. J. Transplant. 2004. 4: 65-78.
48. + splenocytes that delays adoptive transfer of diabetes expresses L-selectin and high levels of CCR7. J. Immunol. 2002. 169: 2461-2465.
49. + regulatory T cells in the control of autoimmune diabetes in T cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA 2004. 101 Suppl 2: 14580-14585.
50. Do, Y., Rafi-Janajreh, A. Q., McKallip, R. J., Nagarkatti, P. S. and Nagarkatti, M., Combined deficiency in CD44 and Fas leads to exacerbation of lymphoproliferative and autoimmune disease. Int. Immunol. 2003. 15: 1327-1340.
51. McKallip, R. J., Do, Y., Fisher, M. T., Robertson, J. L., Nagarkatti, P. S. and Nagarkatti, M., Role of CD44 in activation-induced cell death: CD44-deficient mice exhibit enhanced T cell response to conventional and superantigens. Int. Immunol. 2002. 14: 1015-1026.
52. Siegel, R. M. and Fleisher, T. A, The role of Fas and related death receptors in autoimmune and other disease states. J. Allergy Clin. Immunol. 1999. 103: 729-738.
53. Martin, D. A., Zheng, L, Siegel, R. M., Huang, B., Fisher, G. H., Wang, J., Jackson, C. E. et al., Defective CD95/APO-1/Fas signal complex formation in the human autoimmune lymphoproliferative syndrome, type Ia. Proc. Natl. Acad. Sci. USA 1999. 96: 4552-4557.
54. Satoh, M., Weintraub, J. P., Yoshida, H., Shaheen, V. M., Richards, H. B., Shaw, M. and Reeves, W. H., Fas and Fas ligand mutations inhibit autoantibody production in pristane-induced lupus. J. Immunol. 2000. 165: 1036-1043.
55. Morse, H. C., 3rd, Davidson, W. F., Yetter, R. A., Murphy, E. D., Roths, J. B. and Coffman, R. L., Abnormalities induced by the mutant gene Ipr: Expansion of a unique lymphocyte subset. J. Immunol. 1982. 129: 2612-2615.
56. Dumont, F. J., Habbersett, R. C. and Nichols, E. A., A new lymphocyte surface antigen defined by a monoclonal antibody (9F3) to the T cell population expanding in MRL/Mp-lpr/lpr mice. J. Immunol. 1984. 133: 809-815.
57. Hammond, D. M., Nagarkatti, P. S., Gote, L. R., Seth, A., Hassuneh, M. R. and Nagarkatti, M., Double-negative T cells from MRL-lpr/lpr mice mediate cytolytic activity when triggered through adhesion molecules and constitutively express perforin gene. J. Exp. Med. 1993. 178: 2225-2230.
58. Haas, C., Ryffel, B. and Le Hir, M., IFN-gamma receptor deletion prevents autoantibody production and glomerulonephritis in lupus-prone (NZB × NZW)F1 mice. J. Immunol. 1998. 160: 3713-3718.
59. Carvalho-Pinto, C. E., Garcia, M. I., Mellado, M., Rodriguez-Frade, J. M., Martin-Caballero, J., Flores, J., Martinez, A. C. and Balomenos, D., Autocrine production of IFN-gamma by macrophages controls their recruitment to kidney and the development of glomerulonephritis in MRL/ lpr mice. J. Immunol. 2002. 169: 1058-1067.
60. Ring, G. H., Dai, Z., Saleem, S., Baddoura, F. K. and Lakkis, F. G., Increased susceptibility to immunologically mediated glomerulonephritis in IFN-gamma-deficient mice. J. Immunol. 1999. 163: 2243-2248.
61. Fu, Y., Xie, C., Yan, M., Li, Q., Joh, J. W., Lu, C. and Mohan, C., The lipopolysaccharide-triggered mesangial transcriptome: Evaluating the role of interferon regulatory factor-1. Kidney Int. 2005. 67: 1350-1361.
62. Matsuyama, T., Kimura, T., Kitagawa, M., Pfeffer, K, Kawakami, T., Watanabe, N., Kundig, T. M. et al., Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell 1993. 75: 83-97.
63. Kim, E. J., Lee, J. M., Namkoong, S. E., Um, S. J. and Park J. S., Interferon regulatory factor-1 mediates interferon-gamma-induced apoptosis in ovarian carcinoma cells. J. Cell. Biochem. 2002. 85: 369-380.
64. Kim, E. J., Park, C. H., Park J. S. and Um, S. J., Functional dissection of the transactivation domain of interferon regulatory factor-1. Biochem. Biophys. Res. Commun. 2003. 304: 253-259.
65. Nose, M., Nishihara, M., Kamogawa, J., Terada, M. and Nakatsuru, S., Genetic basis of autoimmune disease in MRL/lpr mice: Dissection of the complex pathological manifestations and their susceptibility loci. Rev. Immunogenet. 2000. 2: 154-164.
66. Morel, L., Croker, B. P., Blenman, K. R., Mohan, C., Huang, G., Gilkeson, G. and Wakeland, E. K., Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenic murine strains. Proc. Nati. Acad. Sci. USA 2000. 97: 6670-6675.
67. Reilly, C. M., Oates, J. C., Cook, J. A., Morrow, J. D., Halushka, P. V. and Gilkeson, G. S., Inhibition of mesangial cell nitric oxide in MRL/ lpr mice by prostaglandin J(2) and proliferator activation receptor-gamma agonists. J. Immunol. 2000. 164: 1498-1504.
68. Gilkeson, G., Cannon, C., Oates, J., Reilly, C., Goldman, D. and Petri, M., Correlation of serum measures of nitric oxide production with lupus disease activity. J. Rheumatol. 1999. 26: 318-324.
69. 3H]thymidine incorporation assay. J. Immunol. Methods 1994. 170: 211-224.
70. Gilkeson, G. S., Pippen, A. M. and Pisetsky, D. S., Induction of cross-reactive anti-dsDNA antibodies in preautoimmune NZB/NZW mice by immunization with bacterial DNA. J. Clin. Invest. 1995. 95: 1398-1402.
71. Reilly, C. M., Mishra, N., Miller, J. M., Joshi, D., Ruiz, P., Richon, V. M., Marks, P. A. and Gilkeson, G. S., Modulation of renal disease in MRL/lpr mice by suberoylanilide hydroxamic acid. J. Immunol. 2004. 173: 4171-4178.