Interleukin-17 Cytokines Are Critical in Development of Fatal Lupus Glomerulonephritis

Immunity

Volumn 37, Issue 6, 2012, Pages 1104-1115

  Pisitkun, Prapaporn ^a   Ha, Hye Lin ^a   Wang, Hongshan ^a   Claudio, Estefania ^a   Tivy, Caitlyn C ^a   Zhou, Hua ^b   Mayadas, Tanya N ^c   Illei, Gabor G ^b   Siebenlist, Ulrich ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; INTRACELLULAR SIGNALING; LUPUS ERYTHEMATOSUS NEPHRITIS; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RENAL PROTECTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOANTIBODIES; B-LYMPHOCYTES; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; GERMINAL CENTER; GLOMERULAR BASEMENT MEMBRANE; INTERLEUKIN-17; KIDNEY; LUPUS NEPHRITIS; MICE; MICE, KNOCKOUT; PROTEIN BINDING; RECEPTORS, IGG; RECEPTORS, INTERLEUKIN-17; SIGNAL TRANSDUCTION;

EID: 84870919913     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.08.014     Document Type: Article

References (51)

1. Baerenwaldt A., Lux A., Danzer H., Spriewald B.M., Ullrich E., Heidkamp G., Dudziak D., Nimmerjahn F. Fcγ receptor IIB (FcγRIIB) maintains humoral tolerance in the human immune system in vivo. Proc. Natl. Acad. Sci. USA 2011, 108:18772-18777.
2. Bolland S., Ravetch J.V. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 2000, 13:277-285.
3. Boross P., Arandhara V.L., Martin-Ramirez J., Santiago-Raber M.L., Carlucci F., Flierman R., van der Kaa J., Breukel C., Claassens J.W., Camps M., et al. The inhibiting Fc receptor for IgG, FcγRIIB, is a modifier of autoimmune susceptibility. J. Immunol. 2011, 187:1304-1313.
4. Chan O., Madaio M.P., Shlomchik M.J. The roles of B cells in MRL/lpr murine lupus. Ann. NY Acad. Sci. 1997, 815:75-87.
5. Chang S.H., Reynolds J.M., Pappu B.P., Chen G., Martinez G.J., Dong C. Interleukin-17C promotes Th17 cell responses and autoimmune disease via interleukin-17 receptor E. Immunity 2011, 35:611-621.
6. Christensen S.R., Kashgarian M., Alexopoulou L., Flavell R.A., Akira S., Shlomchik M.J. Toll-like receptor 9 controls anti-DNA autoantibody production in murine lupus. J. Exp. Med. 2005, 202:321-331.
7. Claudio E., Sønder S.U., Saret S., Carvalho G., Ramalingam T.R., Wynn T.A., Chariot A., Garcia-Perganeda A., Leonardi A., Paun A., et al. The adaptor protein CIKS/Act1 is essential for IL-25-mediated allergic airway inflammation. J. Immunol. 2009, 182:1617-1630.
8. Crispín J.C., Oukka M., Bayliss G., Cohen R.A., Van Beek C.A., Stillman I.E., Kyttaris V.C., Juang Y.T., Tsokos G.C. Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. J. Immunol. 2008, 181:8761-8766.
9. Daëron M., Latour S., Malbec O., Espinosa E., Pina P., Pasmans S., Fridman W.H. The same tyrosine-based inhibition motif, in the intracytoplasmic domain of Fc gamma RIIB, regulates negatively BCR-, TCR-, and FcR-dependent cell activation. Immunity 1995, 3:635-646.
10. Daley J.M., Thomay A.A., Connolly M.D., Reichner J.S., Albina J.E. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 2008, 83:64-70.
11. Doreau A., Belot A., Bastid J., Riche B., Trescol-Biemont M.C., Ranchin B., Fabien N., Cochat P., Pouteil-Noble C., Trolliet P., et al. Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat. Immunol. 2009, 10:778-785.
12. Gaffen S.L. Structure and signalling in the IL-17 receptor family. Nat. Rev. Immunol. 2009, 9:556-567.
13. Gunaratne R., Braucht D.W., Rinschen M.M., Chou C.L., Hoffert J.D., Pisitkun T., Knepper M.A. Quantitative phosphoproteomic analysis reveals cAMP/vasopressin-dependent signaling pathways in native renal thick ascending limb cells. Proc. Natl. Acad. Sci. USA 2010, 107:15653-15658.
14. Haas C., Ryffel B., Le Hir M. IFN-gamma receptor deletion prevents autoantibody production and glomerulonephritis in lupus-prone (NZB x NZW)F1 mice. J. Immunol. 1998, 160:3713-3718.
15. Hakkim A., Fürnrohr B.G., Amann K., Laube B., Abed U.A., Brinkmann V., Herrmann M., Voll R.E., Zychlinsky A. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc. Natl. Acad. Sci. USA 2010, 107:9813-9818.
16. Harley J.B., Alarcón-Riquelme M.E., Criswell L.A., Jacob C.O., Kimberly R.P., Moser K.L., Tsao B.P., Vyse T.J., Langefeld C.D., Nath S.K., et al. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat. Genet. 2008, 40:204-210. International Consortium for Systemic Lupus Erythematosus Genetics (SLEGEN).
17. Hartupee J., Liu C., Novotny M., Li X., Hamilton T. IL-17 enhances chemokine gene expression through mRNA stabilization. J. Immunol. 2007, 179:4135-4141.
18. Hobeika E., Thiemann S., Storch B., Jumaa H., Nielsen P.J., Pelanda R., Reth M. Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 2006, 103:13789-13794.
19. Hsu H.C., Yang P., Wang J., Wu Q., Myers R., Chen J., Yi J., Guentert T., Tousson A., Stanus A.L., et al. Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat. Immunol. 2008, 9:166-175.
20. Izcue A., Hue S., Buonocore S., Arancibia-Cárcamo C.V., Ahern P.P., Iwakura Y., Maloy K.J., Powrie F. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 2008, 28:559-570.
21. Komiyama Y., Nakae S., Matsuki T., Nambu A., Ishigame H., Kakuta S., Sudo K., Iwakura Y. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 2006, 177:566-573.
22. Kozyrev S.V., Abelson A.K., Wojcik J., Zaghlool A., Linga Reddy M.V., Sanchez E., Gunnarsson I., Svenungsson E., Sturfelt G., Jönsen A., et al. Functional variants in the B-cell gene BANK1 are associated with systemic lupus erythematosus. Nat. Genet. 2008, 40:211-216.
23. Kyttaris V.C., Zhang Z., Kuchroo V.K., Oukka M., Tsokos G.C. Cutting edge: IL-23 receptor deficiency prevents the development of lupus nephritis in C57BL/6-lpr/lpr mice. J. Immunol. 2010, 184:4605-4609.
24. Matusevicius D., Kivisäkk P., He B., Kostulas N., Ozenci V., Fredrikson S., Link H. Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Mult. Scler. 1999, 5:101-104.
25. Mok C.C. Biomarkers for lupus nephritis: a critical appraisal. J. Biomed. Biotechnol. 2010, 2010:638413.
26. Muramatsu M., Kinoshita K., Fagarasan S., Yamada S., Shinkai Y., Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000, 102:553-563.
27. Nakae S., Komiyama Y., Nambu A., Sudo K., Iwase M., Homma I., Sekikawa K., Asano M., Iwakura Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002, 17:375-387.
28. Nakae S., Nambu A., Sudo K., Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 2003, 171:6173-6177.
29. Nalbandian A., Crispín J.C., Tsokos G.C. Interleukin-17 and systemic lupus erythematosus: current concepts. Clin. Exp. Immunol. 2009, 157:209-215.
30. Navarra S.V., Guzmán R.M., Gallacher A.E., Hall S., Levy R.A., Jimenez R.E., Li E.K., Thomas M., Kim H.Y., León M.G., et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet 2011, 377:721-731. BLISS-52 Study Group.
31. Odobasic D., Gan P.Y., Summers S.A., Semple T.J., Muljadi R.C., Iwakura Y., Kitching A.R., Holdsworth S.R. Interleukin-17A promotes early but attenuates established disease in crescentic glomerulonephritis in mice. Am. J. Pathol. 2011, 179:1188-1198.
32. Oppmann B., Lesley R., Blom B., Timans J.C., Xu Y., Hunte B., Vega F., Yu N., Wang J., Singh K., et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000, 13:715-725.
33. Paust H.J., Turner J.E., Riedel J.H., Disteldorf E., Peters A., Schmidt T., Krebs C., Velden J., Mittrücker H.W., Steinmetz O.M., et al. Chemokines play a critical role in the cross-regulation of Th1 and Th17 immune responses in murine crescentic glomerulonephritis. Kidney Int. 2012, 82:72-83.
34. Peng S.L., Moslehi J., Craft J. Roles of interferon-gamma and interleukin-4 in murine lupus. J. Clin. Invest. 1997, 99:1936-1946.
35. Pisitkun P., Claudio E., Ren N., Wang H., Siebenlist U. The adaptor protein CIKS/ACT1 is necessary for collagen-induced arthritis, and it contributes to the production of collagen-specific antibody. Arthritis Rheum. 2010, 62:3334-3344.
36. Qian Y., Liu C., Hartupee J., Altuntas C.Z., Gulen M.F., Jane-Wit D., Xiao J., Lu Y., Giltiay N., Liu J., et al. The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat. Immunol. 2007, 8:247-256.
37. Ramirez-Carrozzi V., Sambandam A., Luis E., Lin Z., Jeet S., Lesch J., Hackney J., Kim J., Zhou M., Lai J., et al. IL-17C regulates the innate immune function of epithelial cells in an autocrine manner. Nat. Immunol. 2011, 12:1159-1166.
38. Richards H.B., Satoh M., Jennette J.C., Croker B.P., Yoshida H., Reeves W.H. Interferon-gamma is required for lupus nephritis in mice treated with the hydrocarbon oil pristane. Kidney Int. 2001, 60:2173-2180.
39. Rosas M., Thomas B., Stacey M., Gordon S., Taylor P.R. The myeloid 7/4-antigen defines recently generated inflammatory macrophages and is synonymous with Ly-6B. J. Leukoc. Biol. 2010, 88:169-180.
40. Rosenkranz A.R., Mendrick D.L., Cotran R.S., Mayadas T.N. P-selectin deficiency exacerbates experimental glomerulonephritis: a protective role for endothelial P-selectin in inflammation. J. Clin. Invest. 1999, 103:649-659.
41. Ruddy M.J., Shen F., Smith J.B., Sharma A., Gaffen S.L. Interleukin-17 regulates expression of the CXC chemokine LIX/CXCL5 in osteoblasts: implications for inflammation and neutrophil recruitment. J. Leukoc. Biol. 2004, 76:135-144.
42. Sanz I., Lee F.E. B cells as therapeutic targets in SLE. Nat Rev Rheumatol 2010, 6:326-337.
43. Sato-Hayashizaki A., Ohtsuji M., Lin Q., Hou R., Ohtsuji N., Nishikawa K., Tsurui H., Sudo K., Ono M., Izui S., et al. Presumptive role of 129 strain-derived Sle16 locus in rheumatoid arthritis in a new mouse model with Fcγ receptor type IIb-deficient C57BL/6 genetic background. Arthritis Rheum. 2011, 63:2930-2938.
44. Shahrara S., Pickens S.R., Mandelin A.M., Karpus W.J., Huang Q., Kolls J.K., Pope R.M. IL-17-mediated monocyte migration occurs partially through CC chemokine ligand 2/monocyte chemoattractant protein-1 induction. J. Immunol. 2010, 184:4479-4487.
45. Smith K.G., Clatworthy M.R. FcgammaRIIB in autoimmunity and infection: evolutionary and therapeutic implications. Nat. Rev. Immunol. 2010, 10:328-343.
46. Sweet R.A., Christensen S.R., Harris M.L., Shupe J., Sutherland J.L., Shlomchik M.J. A new site-directed transgenic rheumatoid factor mouse model demonstrates extrafollicular class switch and plasmablast formation. Autoimmunity 2010, 43:607-618.
47. Takai T., Ono M., Hikida M., Ohmori H., Ravetch J.V. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature 1996, 379:346-349.
48. Valente A.J., Clark R.A., Siddesha J.M., Siebenlist U., Chandrasekar B. CIKS (Act1 or TRAF3IP2) mediates Angiotensin-II-induced Interleukin-18 expression, and Nox2-dependent cardiomyocyte hypertrophy. J. Mol. Cell. Cardiol. 2012, 53:113-124.
49. Vielhauer V., Stavrakis G., Mayadas T.N. Renal cell-expressed TNF receptor 2, not receptor 1, is essential for the development of glomerulonephritis. J. Clin. Invest. 2005, 115:1199-1209.
50. Zhang Z., Kyttaris V.C., Tsokos G.C. The role of IL-23/IL-17 axis in lupus nephritis. J. Immunol. 2009, 183:3160-3169.
51. Ziolkowska M., Koc A., Luszczykiewicz G., Ksiezopolska-Pietrzak K., Klimczak E., Chwalinska-Sadowska H., Maslinski W. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J. Immunol. 2000, 164:2832-2838.