The IL-27 receptor has biphasic effects in crescentic glomerulonephritis mediated through Th1 responses

American Journal of Pathology

Volumn 178, Issue 2, 2011, Pages 580-590

  Summers, Shaun A ^a,b   Phoon, Richard K S ^a   Ooi, Joshua D ^a   Holdsworth, Stephen R ^a,b   Kitching, A Richard ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b MONASH MEDICAL CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 27; INTERLEUKIN 27 RECEPTOR ALPHA; INTERLEUKIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; GENE SILENCING; IMMUNE RESPONSE; IMMUNOREGULATION; KIDNEY INJURY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN FUNCTION; RAPIDLY PROGRESSIVE GLOMERULONEPHRITIS; RENAL PROTECTION; TH1 CELL; WILD TYPE;

EID: 79951844953     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.10.013     Document Type: Article

References (47)

1. Holdsworth SR, Kitching AR, Tipping PG: Th1 and Th2 T helper cell subsets affect patterns of injury and outcomes in glomerulonephritis. Kidney Int 1999, 55:1198-1216 (Pubitemid 29157116)
2. Huang XR, Tipping PG, Shuo L, Holdsworth SR: Th1 responsiveness to nephritogenic antigens determines susceptibility to crescentic glomerulonephritis in mice. Kidney Int 1997, 51:94-103 (Pubitemid 27064526)
3. Li S, Holdsworth SR, Tipping PG: Antibody independent crescentic glomerulonephritis in mu chain deficient mice. Kidney Int 1997, 51: 672-678 (Pubitemid 27157950)
4. Phoon RK, Kitching AR, Odobasic D, Jones LK, Semple TJ, Holdsworth SR: T-bet deficiency attenuates renal injury in experimental crescentic glomerulonephritis. J Am Soc Nephrol 2008, 19:477-485 (Pubitemid 351355391)
5. Kitching AR, Tipping PG, Holdsworth SR: IL-12 directs severe renal injury, crescent formation and Th1 responses in murine glomerulonephritis. Eur J Immunol 1999, 29:1-10 (Pubitemid 29043516)
6. Kitching AR, Tipping PG, Kurimoto M, Holdsworth SR: IL-18 has IL-12-independent effects in delayed-type hypersensitivity: studies in cell-mediated crescentic glomerulonephritis. J Immunol 2000, 165: 4649-4657
7. Kitching AR, Holdsworth SR, Tipping PG: IFN-γ mediates crescent formation and cell-mediated immune injury in murine glomerulonephritis. J Am Soc Nephrol 1999, 10:752-759 (Pubitemid 29149525)
8. Kitching AR, Tipping PG, Mutch DA, Huang XR, Holdsworth SR: Interleukin-4 deficiency enhances Th1 responses and crescentic glomerulonephritis in mice. Kidney Int 1998, 53:112-118 (Pubitemid 28066909)
9. Kitching AR, Tipping PG, Timoshanko JR, Holdsworth SR: Endogenous interleukin-10 regulates Th1 responses that induce crescentic glomerulonephritis. Kidney Int 2000, 57:518-525 (Pubitemid 30430643)
10. Kitching AR, Tipping PG, Huang XR, Mutch DA, Holdsworth SR: Interleukin-4 and interleukin-10 attenuate established crescentic glomerulonephritis in mice. Kidney Int 1997, 52:52-59 (Pubitemid 27321814)
11. Tipping PG, Kitching AR, Huang XR, Mutch DA, Holdsworth SR: Immune modulation with interleukin-4 and interleukin-10 prevents crescent formation and glomerular injury in experimental glomerulonephritis. Eur J Immunol 1997, 27:530-537 (Pubitemid 27085260)
12. Pflanz S, Timans JC, Cheung J, Rosales R, Kanzler H, Gilbert J, Hibbert L, Churakova T, Travis M, Vaisberg E, Blumenschein WM, Mattson JD, Wagner JL, To W, Zurawski S, McClanahan TK, Gorman DM, Bazan JF, de Waal Malefyt R, Rennick D, Kastelein RA: IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002, 16:779-790 (Pubitemid 34786477)
13. Sonobe Y, Yawata I, Kawanokuchi J, Takeuchi H, Mizuno T, Suzumura A: Production of IL-27 and other IL-12 family cytokines by microglia and their subpopulations. Brain Res 2005, 1040:202-207 (Pubitemid 40459635)
14. Chen Q, Ghilardi N, Wang H, Baker T, Xie MH, Gurney A, Grewal IS, de Sauvage FJ: Development of Th1-type immune responses requires the type I cytokine receptor TCCR. Nature 2000, 407:916-920
15. Yoshida H, Hamano S, Senaldi G, Covey T, Faggioni R, Mu S, Xia M, Wakeham AC, Nishina H, Potter J, Saris CJ, Mak TW: WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection. Immunity 2001, 15:569-578 (Pubitemid 33016442)
16. Kamiya S, Owaki T, Morishima N, Fukai F, Mizuguchi J, Yoshimoto T: An indispensable role for STAT1 in IL-27-induced T-bet expression but not proliferation of naive CD4+ T cells. J Immunol 2004, 173: 3871-3877 (Pubitemid 39280750)
17. Takeda A, Hamano S, Yamanaka A, Hanada T, Ishibashi T, Mak TW, Yoshimura A, Yoshida H: Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment. J Immunol 2003, 170:4886-4890 (Pubitemid 36554716)
18. Owaki T, Asakawa M, Morishima N, Hata K, Fukai F, Matsui M, Mizuguchi J, Yoshimoto T: A role for IL-27 in early regulation of Th1 differentiation. J Immunol 2005, 175:2191-2200 (Pubitemid 41113825)
19. Artis D, Villarino A, Silverman M, He W, Thornton EM, Mu S, Summer S, Covey TM, Huang E, Yoshida H, Koretzky G, Goldschmidt M, Wu GD, de Sauvage F, Miller HR, Saris CJ, Scott P, Hunter CA: The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity. J Immunol 2004, 173:5626-5634 (Pubitemid 39392150)
20. Bancroft AJ, Humphreys NE, Worthington JJ, Yoshida H, Grencis RK: WSX-1: a key role in induction of chronic intestinal nematode infection. J Immunol 2004, 172:7635-7641 (Pubitemid 38747628)
21. Hamano S, Himeno K, Miyazaki Y, Ishii K, Yamanaka A, Takeda A, Zhang M, Hisaeda H, Mak TW, Yoshimura A, Yoshida H: WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production. Immunity 2003, 19:657-667 (Pubitemid 37490791)
22. Villarino A, Hibbert L, Lieberman L, Wilson E, Mak T, Yoshida H, Kastelein RA, Saris C, Hunter CA: The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection. Immunity 2003, 19: 645-655 (Pubitemid 37490790)
23. Rosas LE, Satoskar AA, Roth KM, Keiser TL, Barbi J, Hunter C, de Sauvage FJ, Satoskar AR: Interleukin-27R (WSX-1/T-cell cytokine receptor) gene-deficient mice display enhanced resistance to leishmania donovani infection but develop severe liver immunopathology. Am J Pathol 2006, 168:158-169 (Pubitemid 43062569)
24. Yamanaka A, Hamano S, Miyazaki Y, Ishii K, Takeda A, Mak TW, Himeno K, Yoshimura A, Yoshida H: Hyperproduction of proinflammatory cytokines by WSX-1-deficient NKT cells in concanavalin A-induced hepatitis. J Immunol 2004, 172:3590-3596 (Pubitemid 38337940)
25. Batten M, Li J, Yi S, Kljavin NM, Danilenko DM, Lucas S, Lee J, de Sauvage FJ, Ghilardi N: Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat Immunol 2006, 7:929-936 (Pubitemid 44263906)
26. Shimizu S, Sugiyama N, Masutani K, Sadanaga A, Miyazaki Y, Inoue Y, Akahoshi M, Katafuchi R, Hirakata H, Harada M, Hamano S, Nakashima H, Yoshida H: Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1). J Immunol 2005, 175:7185-7192 (Pubitemid 41713412)
27. Sugiyama N, Nakashima H, Yoshimura T, Sadanaga A, Shimizu S, Masutani K, Igawa T, Akahoshi M, Miyake K, Takeda A, Yoshimura A, Hamano S, Yoshida H: Amelioration of human lupus-like phenotypes in MRL/lpr mice by overexpression of interleukin 27 receptor α (WSX- 1). Ann Rheum Dis 2008, 67:1461-1467
28. Edgtton KL, Gow RM, Kelly DJ, Carmeliet P, Kitching AR: Plasmin is not protective in experimental renal interstitial fibrosis. Kidney Int 2004, 66:68-76 (Pubitemid 38870083)
29. Li M, O'Sullivan KM, Jones LK, Lo C, Semple T, Kumanogoh A, Kikutani H, Holdsworth SR, Kitching AR: Endogenous CD100 promotes glomerular injury and macrophage recruitment in experimental crescentic glomerulonephritis. Immunology 2009, 128:114-122
30. Timoshanko JR, Sedgwick JD, Holdsworth SR, Tipping PG: Intrinsic renal cells are the major source of tumor necrosis factor contributing to renal injury in murine crescentic glomerulonephritis. J Am Soc Nephrol 2003, 14:1785-1793 (Pubitemid 36750474)
31. Timoshanko JR, Kitching AR, Iwakura Y, Holdsworth SR, Tipping PG: Contributions of IL-1β and IL-1α to crescentic glomerulonephritis in mice. J Am Soc Nephrol 2004, 15:910-918 (Pubitemid 38375310)
32. Tipping PG, Huang XR, Qi M, Van GY, Tang WW: Crescentic glomerulonephritis in CD4- and CD8-deficient mice: requirement for CD4 but not CD8 cells. Am J Pathol 1998, 152:1541-1548 (Pubitemid 28275012)
33. Batten M, Ghilardi N: The biology and therapeutic potential of interleukin 27. J Mol Med 2007, 85:661-672 (Pubitemid 47063520)
34. Morishima N, Owaki T, Asakawa M, Kamiya S, Mizuguchi J, Yoshimoto T: Augmentation of effector CD8+ T cell generation with enhanced granzyme B expression by IL-27. J Immunol 2005, 175: 1686-1693 (Pubitemid 41023072)
35. Li S, Holdsworth SR, Tipping PG: MHC class I pathway is not required for the development of crescentic glomerulonephritis in mice. Clin Exp Immunol 2000, 122:453-458 (Pubitemid 32002206)
36. Timoshanko JR, Holdsworth SR, Kitching AR, Tipping PG: IFN-γ production by intrinsic renal cells and bone marrow-derived cells is required for full expression of crescentic glomerulonephritis in mice. J Immunol 2002, 168:4135-4141 (Pubitemid 34298422)
37. Holscher C, Holscher A, Ruckerl D, Yoshimoto T, Yoshida H, Mak T, Saris C, Ehlers S: The IL-27 receptor chain WSX-1 differentially regulates antibacterial immunity and survival during experimental tuberculosis. J Immunol 2005, 174:3534-3544 (Pubitemid 40354062)
38. Fitzgerald DC, Ciric B, Touil T, Harle H, Grammatikopolou J, Das Sarma J, Gran B, Zhang GX, Rostami A: Suppressive effect of IL-27 on encephalitogenic Th17 cells and the effector phase of experimental autoimmune encephalomyelitis. J Immunol 2007, 179:3268-3275
39. Batten M, Kljavin NM, Li J, Walter MJ, de Sauvage FJ, Ghilardi N: Cutting edge: IL-27 is a potent inducer of IL-10 but not FoxP3 in murine T cells. J Immunol 2008, 180:2752-2756
40. Stumhofer JS, Silver JS, Laurence A, Porrett PM, Harris TH, Turka LA, Ernst M, Saris CJ, O'Shea JJ, Hunter CA: Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat Immunol 2007, 8:1363-1371 (Pubitemid 350131173)
41. Korn T, Bettelli E, Gao W, Awasthi A, Jager A, Strom TB, Oukka M, Kuchroo VK: IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007, 448:484-487 (Pubitemid 47123515)
42. Summers SA, Steinmetz OM, Li M, Kausman JY, Semple T, Edgtton KL, Borza DB, Braley H, Holdsworth SR, Kitching AR: Th1 and Th17 cells induce proliferative glomerulonephritis. J Am Soc Nephrol 2009, 20:2518-2524
43. Paust HJ, Turner JE, Steinmetz OM, Peters A, Heymann F, Holscher C, Wolf G, Kurts C, Mittrucker HW, Stahl RA, Panzer U: The IL-23/ Th17 axis contributes to renal injury in experimental glomerulonephritis. J Am Soc Nephrol 2009, 20:969-979
44. Villarino AV, Larkin J III, Saris CJ, Caton AJ, Lucas S, Wong T, de Sauvage FJ, Hunter CA: Positive and negative regulation of the IL-27 receptor during lymphoid cell activation. J Immunol 2005, 174:7684-7691 (Pubitemid 40806273)
45. O'Connor RA, Anderton SM: Multi-faceted control of autoaggression: foxp3+ regulatory T cells in murine models of organ-specific autoimmune disease. Cell Immunol 2008, 251:8-18
46. Bunnag S, Allanach K, Jhangri GS, Sis B, Einecke G, Mengel M, Mueller TF, Halloran PF: FOXP3 expression in human kidney transplant biopsies is associated with rejection and time post transplant but not with favorable outcomes. Am J Transplant 2008, 8:1423-1433 (Pubitemid 351989494)
47. Kitching AR, Kong YZ, Huang XR, Davenport P, Edgtton KL, Carmeliet P, Holdsworth SR, Tipping PG: Plasminogen activator inhibitor-1 is a significant determinant of renal injury in experimental crescentic glomerulonephritis. J Am Soc Nephrol 2003, 14:1487-1495 (Pubitemid 36687050)