Type I interferons produced by resident renal cells may promote end-organ disease in autoantibody-mediated glomerulonephritis

Journal of Immunology

Volumn 183, Issue 10, 2009, Pages 6831-6838

  Fairhurst, Anna Marie ^b   Xie, Chun ^a   Fu, Yuyang ^a   Wang, Andrew ^b   Boudreaux, Christopher ^b   Zhou, Xin J ^a   Cibotti, Ricardo ^c   Coyle, Anthony ^c   Connolly, John E ^d   Wakeland, Edward K ^b   Mohan, Chandra ^a  

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

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

^c MEDIMMUNE   (United States)

^d BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; INTERFERON;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; GLOMERULONEPHRITIS; INFLAMMATORY CELL; INTERFERON PRODUCTION; KIDNEY CELL; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIVIRAL AGENTS; AUTOANTIBODIES; CYTOKINES; DISEASE MODELS, ANIMAL; GLOMERULONEPHRITIS; HUMANS; INTERFERON TYPE I; INTERFERON TYPE I, RECOMBINANT; KIDNEY; KIDNEY FAILURE, CHRONIC; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTOR, INTERFERON ALPHA-BETA;

EID: 77649245893     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900742     Document Type: Article

References (60)

1. Preble, O. T., R. J. Black, R. M. Friedman, J. H. Klippel, and J. Vilcek. 1982. Systemic lupus erythematosus: presence in human serum of an unusual acidlabile leukocyte interferon. Science 216: 429-431.
2. Preble, O. T., K. Rothko, J. H. Klippel, R. M. Friedman, and M. I. Johnston. 1983. Interferon-induced 2′-5′ adenylate synthetase in vivo and interferon production in vitro by lymphocytes from systemic lupus erythematosus patients with and without circulating interferon. J. Exp. Med. 157: 2140-2146.
3. Vallin, H., A. Perers, G. V. Alm, and L. Ronnblom. 1999. Anti-dsDNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-α inducer in systemic lupus erythematosus. J. Immunol. 163: 6306-6313.
4. Vallin, H., S. Blomberg, G. V. Alm, B. Cederblad, and L. Ronnblom. 1999. Patients with systemic lupus erythematosus (SLE) have a circulating inducer of interferon-α (IFN-α) production acting on leucocytes resembling immature dendritic cells. Clin. Exp. Immunol. 115: 196-202.
5. Han, G. M., S. L. Chen, N. Shen, S. Ye, C. D. Bao, and Y. Y. Gu. 2003. Analysis of gene expression profiles in human systemic lupus erythematosus using oligonucleotide microarray. Genes Immun. 4: 177-186.
6. Crow, M. K., and J. Wohlgemuth. 2003. Microarray analysis of gene expression in lupus. Arthritis Res. Ther. 5: 279-287. (Pubitemid 37407977)
7. Crow, M. K., K. A. Kirou, and J. Wohlgemuth. 2003. Microarray analysis of interferon-regulated genes in SLE. Autoimmunity 36: 481-490.
8. Bennett, L., A. K. Palucka, E. Arce, V. Cantrell, J. Borvak, J. Banchereau, and V. Pascual. 2003. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 197: 711-723.
9. Baechler, E. C., F. M. Batliwalla, G. Karypis, P. M. Gaffney, W. A. Ortmann, K. J. Espe, K. B. Shark, W. J. Grande, K. M. Hughes, V. Kapur, et al. 2003. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl. Acad. Sci. USA 100: 2610-2615.
10. Santiago-Raber, M. L., R. Baccala, K. M. Haraldsson, D. Choubey, T. A. Stewart, D. H. Kono, and A. N. Theofilopoulos. 2003. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J. Exp. Med. 197: 777-788.
11. Braun, D., P. Geraldes, and J. Demengeot. 2003. Type I interferon controls the onset and severity of autoimmune manifestations in lpr mice. J. Autoimmun. 20: 15-25.
12. Kono, D. H., R. Baccala, and A. N. Theofilopoulos. 2003. Inhibition of lupus by genetic alteration of the interferon-α/β receptor. Autoimmunity 36: 503-510.
13. Hron, J. D., and S. L. Peng. 2004. Type I IFN protects against murine lupus. J. Immunol. 173: 2134-2142. (Pubitemid 38971652)
14. 1 but not in BALB/c mice. J. Immunol. 174: 2499-2506.
15. Pawar, R. D., P. S. Patole, D. Zecher, S. Segerer, M. Kretzler, D. Schlondorff, and H. J. Anders. 2006. Toll-like receptor-7 modulates immune complex glomerulonephritis. J. Am. Soc. Nephrol. 17: 141-149.
16. Patole, P. S., H. J. Grone, S. Segerer, R. Ciubar, E. Belemezova, A. Henger, M. Kretzler, D. Schlondorff, and H. J. Anders. 2005. Viral double-stranded RNA aggravates lupus nephritis through Toll-like receptor 3 on glomerular mesangial cells and antigen-presenting cells. J. Am. Soc. Nephrol. 16: 1326-1338.
17. Anders, H. J., V. Vielhauer, V. Eis, Y. Linde, M. Kretzler, G. Perez de Lema, F. Strutz, S. Bauer, M. Rutz, H. Wagner, et al. 2004. Activation of toll-like receptor-9 induces progression of renal disease in MRL-Fas(lpr) mice. FASEB J. 18: 534-536.
18. Fairhurst, A. M., A. Mathian, J. E. Connolly, A. Wang, H. F. Gray, T. A. George, C. D. Boudreaux, X. J. Zhou, Q. Z. Li, S. Koutouzov, J. Banchereau, and E. K. Wakeland. 2008. Systemic IFN-α drives kidney nephritis in B6.Sle123 mice. Eur. J. Immunol. 38: 1948-1960.
19. Anders, H. J., B. Banas, Y. Linde, L. Weller, C. D. Cohen, M. Kretzler, S. Martin, V. Vielhauer, D. Schlondorff, and H. J. Grone. 2003. Bacterial CpG-DNA aggravates immune complex glomerulonephritis: role of TLR9-mediated expression of chemokines and chemokine receptors. J. Am. Soc. Nephrol. 14: 317-326.
20. Anders, H. J. 2005. A Toll for lupus. Lupus 14: 417-422.
21. Fu, Y., Y. Du, and C. Mohan. 2007. Experimental anti-GBM disease as a tool for studying spontaneous lupus nephritis. Clin. Immunol. 124: 109-118.
22. Xie, C., X. J. Zhou, X. Liu, and C. Mohan. 2003. Enhanced susceptibility to end-organ disease in the lupus-facilitating NZW mouse strain. Arthritis Rheum. 48: 1080-1092.
23. Xie, C., R. Sharma, H. Wang, X. J. Zhou, and C. Mohan. 2004. Strain distribution pattern of susceptibility to immune-mediated nephritis. J. Immunol. 172: 5047-5055.
24. Muller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921. (Pubitemid 24245635)
25. Li, J., Y. Liu, C. Xie, J. Zhu, D. Kreska, L. Morel, and C. Mohan. 2005. Deficiency of type I interferon contributes to Sle2-associated component lupus phenotypes. Arthritis Rheum. 52: 3063-3072.
26. Fairhurst, A. M., S. H. Hwang, A. Wang, X. H. Tian, C. Boudreaux, X. J. Zhou, J. Casco, Q. Z. Li, J. E. Connolly, and E. K. Wakeland. 2008. Yaa autoimmune phenotypes are conferred by overexpression of TLR7. Eur. J. Immunol. 38: 1971-1978.
27. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82.
28. Taylor, P. R., G. D. Brown, A. B. Geldhof, L. Martinez-Pomares, and S. Gordon. 2003. Pattern recognition receptors and differentiation antigens define murine myeloid cell heterogeneity ex vivo. Eur. J. Immunol. 33: 2090-2097.
29. + interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney Int. 70: 591-596.
30. Deblandre, G. A., O. Leo, G. A. Huez, and M. G. Wathelet. 1992. CD69 is expressed on Daudi cells in response to interferon-α. Cytokine 4: 36-43.
31. Lanier, L. L., D. W. Buck, L. Rhodes, A. Ding, E. Evans, C. Barney, and J. H. Phillips. 1988. Interleukin 2 activation of natural killer cells rapidly induces the expression and phosphorylation of the Leu-23 activation antigen. J. Exp. Med. 167: 1572-1585.
32. 2+] and stimulation of protein kinase C. J. Immunol. 142: 1854-1860.
33. Wang, A., A. M. Fairhurst, K. Tus, S. Subramanian, Y. Liu, F. Lin, P. Igarashi, X. J. Zhou, F. Batteux, D. Wong, E. K. Wakeland, and C. Mohan. 2009. CXCR4/ CXCL12 hyperexpression plays a pivotal role in the pathogenesis of lupus. J. Immunol. 182: 4448-4458.
34. Feng, X., H. Wu, J. M. Grossman, P. Hanvivadhanakul, J. D. FitzGerald, G. S. Park, X. Dong, W. Chen, M. H. Kim, H. H. Weng, et al. 2006. Association of increased interferon-inducible gene expression with disease activity and lupus nephritis in patients with systemic lupus erythematosus. Arthritis Rheum. 54: 2951-2962.
35. Dall'era, M. C., P. M. Cardarelli, B. T. Preston, A. Witte, and J. C. Davis, Jr. 2005. Type I interferon correlates with serological and clinical manifestations of SLE. Ann. Rheum. Dis. 64: 1692-1697.
36. Kirou, K. A., C. Lee, S. George, K. Louca, M. G. Peterson, and M. K. Crow. 2005. Activation of the interferon-α pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum. 52: 1491-1503.
37. Wenzel, J., and T. Tuting. 2007. Identification of type I interferon-associated inflammation in the pathogenesis of cutaneous lupus erythematosus opens up options for novel therapeutic approaches. Exp. Dermatol. 16: 454-463.
38. Schaefer, M., M. A. Engelbrecht, O. Gut, B. L. Fiebich, J. Bauer, F. Schmidt, H. Grunze, and K. Lieb. 2002. Interferon α(IFNα) and psychiatric syndromes: a review. Prog. Neuropsychopharm. Biol. Psy. 26: 731-746.
39. Patole, P. S., R. D. Pawar, M. Lech, D. Zecher, H. Schmidt, S. Segerer, A. Ellwart, A. Henger, M. Kretzler, and H. J. Anders. 2006. Expression and regulation of Toll-like receptors in lupus-like immune complex glomerulonephritis of MRL-Fas(lpr) mice. Nephrol. Dial. Transplant. 21: 3062-3073.
40. Anders, H. J. 2007. Innate pathogen recognition in the kidney: toll-like receptors, NOD-like receptors, and RIG-like helicases. Kidney Int. 72: 1051-1056.
41. Anders, H. J., and D. Schlondorff. 2007. Toll-like receptors: emerging concepts in kidney disease. Curr. Opin. Nephrol. Hypertens. 16: 177-183.
42. Allam, R., R. D. Pawar, O. P. Kulkarni, V. Hornung, G. Hartmann, S. Segerer, S. Akira, S. Endres, and H. J. Anders. 2008. Viral 5′- triphosphate RNA and non-CpG DNA aggravate autoimmunity and lupus nephritis via distinct TLRindependent immune responses. Eur. J. Immunol. 38: 3487-3498.
43. Fu, Y., C. Xie, J. Chen, J. Zhu, H. Zhou, J. Thomas, X. J. Zhou, and C. Mohan. 2006. Innate stimuli accentuate end-organ damage by nephrotoxic antibodies via Fc receptor and TLR stimulation and IL-1/TNF-α production. J. Immunol. 176: 632-639.
44. Tesch, G. H., S. Maifert, A. Schwarting, B. J. Rollins, and V. R. Kelley. 1999. Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J. Exp. Med. 190: 1813-1824.
45. Sironi, M., A. Guglielmotti, N. Polentarutti, F. Fioretti, C. Milanese, M. Romano, C. Vigini, I. Coletta, S. Sozzani, S. Bernasconi, et al. 1999. A small synthetic molecule capable of preferentially inhibiting the production of the CC chemokine monocyte chemotactic protein-1. Eur. Cytokine Network 10: 437-442.
46. Perez de Lema, G., H. Maier, T. J. Franz, M. Escribese, S. Chilla, S. Segerer, N. Camarasa, H. Schmid, B. Banas, S. Kalaydjiev, et al. 2005. Chemokine receptor Ccr2 deficiency reduces renal disease and prolongs survival in MRL/lpr lupus-prone mice. J. Am. Soc. Nephrol. 16: 3592-3601.
47. Lit, L. C., C. K. Wong, L. S. Tam, E. K. Li, and C. W. Lam. 2006. Raised plasma concentration and ex vivo production of inflammatory chemokines in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 65: 209-215.
48. Kulkarni, O., R. D. Pawar, W. Purschke, D. Eulberg, N. Selve, K. Buchner, V. Ninichuk, S. Segerer, V. Vielhauer, S. Klussmann, and H. J. Anders. 2007. Spiegelmer inhibition of CCL2/MCP-1 ameliorates lupus nephritis in MRL-(Fas)lpr mice. J. Am. Soc. Nephrol. 18: 2350-2358.
49. Chan, R. W., F. M. Lai, E. K. Li, L. S. Tam, K. M. Chow, K. B. Lai, P. K. Li, and C. C. Szeto. 2007. Intrarenal cytokine gene expression in lupus nephritis. Ann. Rheum. Dis. 66: 886-892.
50. Zoja, C., X. H. Liu, R. Donadelli, M. Abbate, D. Testa, D. Corna, G. Taraboletti, A. Vecchi, Q. G. Dong, B. J. Rollins, et al. 1997. Renal expression of monocyte chemoattractant protein-1 in lupus autoimmune mice. J. Am. Soc. Nephrol. 8: 720-729.
51. Zavala, F., A. Masson, K. Hadaya, S. Ezine, E. Schneider, O. Babin, and J. F. Bach. 1999. Granulocyte-colony stimulating factor treatment of lupus autoimmune disease in MRL-lpr/lpr mice. J. Immunol. 163: 5125-5132. (Pubitemid 29501282)
52. Rutella, S. 2007. Granulocyte colony-stimulating factor for the induction of Tcell tolerance. Transplantation 84: S26-30.
53. Zhu, J., X. Liu, C. Xie, M. Yan, Y. Yu, E. S. Sobel, E. K. Wakeland, and C. Mohan. 2005. T cell hyperactivity in lupus as a consequence of hyperstimulatory antigen-presenting cells. J. Clin. Invest. 115: 1869-1878.
54. Subramanian, S., K. Tus, Q. Z. Li, A. Wang, X. H. Tian, J. Zhou, C. Liang, G. Bartov, L. D. McDaniel, X. J. Zhou, et al. 2006. A Tlr7 translocation accelerates systemic autoimmunity in murine lupus. Proc. Natl. Acad. Sci. USA 103: 9970-9975.
55. Sela, U., A. Sharabi, M. Dayan, R. Hershkoviz, and E. Mozes. 2009. The role of dendritic cells in the mechanism of action of a peptide that ameliorates lupus in murine models. Immunology 128: e395-e405.
56. Ding, D., H. Mehta, W. J. McCune, and M. J. Kaplan. 2006. Aberrant phenotype and function of myeloid dendritic cells in systemic lupus erythematosus. J. Immunol. 177: 5878-5889.
57. Decker, P., I. Kotter, R. Klein, B. Berner, and H. G. Rammensee. 2006. Monocyte-derived dendritic cells over-express CD86 in patients with systemic lupus erythematosus. Rheumatology. 45: 1087-1095. (Pubitemid 44542093)
58. Fairhurst, A. M., A. E. Wandstrat, and E. K. Wakeland. 2006. Systemic lupus erythematosus: multiple immunological phenotypes in a complex genetic disease. Adv. Immunol. 92: 1-69.
59. Wakeland, E. K., K. Liu, R. R. Graham, and T. W. Behrens. 2001. Delineating the genetic basis of systemic lupus erythematosus. Immunity 15: 397-408.
60. Kanta, H., and C. Mohan. 2009. Three checkpoints in lupus development: central tolerance in adaptive immunity, peripheral amplification by innate immunity and end-organ inflammation. Genes Immun. 10: 390-396.