Interleukin-21 Receptor Blockade Inhibits Secondary Humoral Responses and Halts the Progression of Preestablished Disease in the (NZB X NZW)F1 Systemic Lupus Erythematosus Model

Arthritis and Rheumatology

Volumn 67, Issue 10, 2015, Pages 2723-2731

  Zhang, Ming ^a   Yu, Gang ^a   Chan, Brian ^a,b   Pearson, Joshua T ^c,d   Rathanaswami, Palaniswami ^b   Delaney, John ^c,d   Lim, Ai Ching ^c,d   Babcook, John ^a,b   Hsu, Hailing ^a   Gavin, Marc A ^c,d  

^a AMGEN INC   (United States)

^b Centre for Drug Research and Development   (Canada)

^c BENAROYA RESEARCH INSTITUTE   (United States)

^d AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING ANTIBODY; IMMUNOGLOBULIN G; INTERLEUKIN 21 RECEPTOR;

ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOIMMUNITY; B LYMPHOCYTE; BLOOD; DISEASE COURSE; DISEASE MODEL; DRUG EFFECTS; FEMALE; HUMORAL IMMUNITY; IMMUNOLOGY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MOUSE; NEW ZEALAND BLACK MOUSE; PATHOLOGY; SHEEP; T LYMPHOCYTE; TREATMENT OUTCOME;

ANIMALS; ANTIBODIES, BLOCKING; AUTOIMMUNITY; B-LYMPHOCYTES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED NZB; RECEPTORS, INTERLEUKIN-21; SHEEP; T-LYMPHOCYTES; TREATMENT OUTCOME;

EID: 84988844611     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/ART.39233     Document Type: Article

References (46)

1. Spolski R, Leonard WJ. Interleukin-21: A double-edged sword with therapeutic potential. Nat Rev Drug Discov 2014;13:379-95.
2. Moens L, Tangye SG. Cytokine-mediated regulation of plasma cell generation: IL-21 takes center stage. Front Immunol 2014; 5:65.
3. Kuchen S, Robbins R, Sims GP, Sheng C, Phillips TM, Lipsky PE, et al. Essential role of IL-21 in B cell activation, expansion, and plasma cell generation during CD41 T cell-B cell collaboration. J Immunol 2007;179:5886-96.
4. Rankin AL, Guay H, Herber D, Bertino SA, Duzanski TA, Carrier Y, et al. IL-21 receptor is required for the systemic accumulation of activated B and T lymphocytes in MRL/MpJ-Faslpr/lpr/J mice. J Immunol 2012;188:1656-67.
5. Elsaesser H, Sauer K, Brooks DG. IL-21 is required to control chronic viral infection. Science 2009;324:1569-72.
6. Kotlarz D, Zietara N, Milner JD, Klein C. Human IL-21 and IL-21R deficiencies: Two novel entities of primary immunodeficiency. Curr Opin Pediatr 2014;26:704-12.
7. Sarra M, Pallone F, Macdonald TT, Monteleone G. Targeting interleukin-21 in immune-mediated pathologies. Curr Drug Targets 2010;11:645-9.
8. Bubier JA, Bennett SM, Sproule TJ, Lyons BL, Olland S, Young DA, et al. Treatment of BXSB-Yaa mice with IL-21R-Fc fusion protein minimally attenuates systemic lupus erythematosus. Ann NY AcadSci 2007;1110:590-601.
9. Bubier JA, Sproule TJ, Foreman O, Spolski R, Shaffer DJ, Morse HC III, et al. A critical role for IL-21 receptor signaling in the pathogenesis of systemic lupus erythematosus in BXSB-Yaa mice. Proc Natl Acad Sci U S A 2009;106:1518-23.
10. Herber D, Brown TP, Liang S, Young DA, Collins M, Dunussi-Joannopoulos K. IL-21 has a pathogenic role in a lupus-prone mouse model and its blockade with IL-21R.Fc reduces disease progression. J Immunol 2007;178:3822-30.
11. Jang E, Cho SH, Park H, Paik DJ, Kim JM, Youn J. A positive feedback loop of IL-21 signaling provoked by homeostatic CD41CD252 T cell expansion is essential for the development of arthritis in autoimmune K/BxN mice. J Immunol 2009;182: 4649-56.
12. Wen L, Hanvanich M, Werner-Favre C, Brouwers N, Perrin LH, Zubler RH. Limiting dilution assay for human B cells based on their activation by mutant EL4 thymoma cells: Total and antimalaria responder B cell frequencies. Eur J Immunol 1987;17: 887-92.
13. Babcook JS, Leslie KB, Olsen OA, Salmon RA, Schrader JW. A novel strategy for generating monoclonal antibodies from single, isolated lymphocytes producing antibodies of defined specificities. Proc Natl Acad Sci U S A 1996;93:7843-8.
14. Ozaki K, Spolski R, Feng CG, Qi CF, Cheng J, Sher A, et al. A critical role for IL-21 in regulating immunoglobulin production. Science 2002;298:1630-4.
15. Wofsy D, Chiang NY, Greenspan JS, Ermak TH. Treatment of murine lupus with monoclonal antibody to L3T4. I. Effects on the distribution and function of lymphocyte subsets and on the histopathology of autoimmune disease. J Autoimmun 1988;1:415-31.
16. Abe J, Ueha S, Suzuki J, Tokano Y, Matsushima K, Ishikawa S. Increased Foxp31 CD41 regulatory T cells with intact suppressive activity but altered cellular localization in murine lupus. Am J Pathol 2008;173:1682-92.
17. Korn T, Bettelli E, Gao W, Awasthi A, Jager A, Strom TB, et al. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 2007;448:484-7.
18. Fantini MC, Rizzo A, Fina D, Caruso R, Becker C, Neurath MF, et al. IL-21 regulates experimental colitis by modulating the balance between Treg and Th17 cells. Eur J Immunol 2007;37: 3155-63.
19. Pene J, Gauchat JF, Lecart S, Drouet E, Guglielmi P, Boulay V, et al. IL-21 is a switch factor for the production of IgG1 and IgG3 by human B cells. J Immunol 2004;172:5154-7.
20. Otani M, Kuroki A, Kikuchi S, Kihara M, Nakata J, Ito K, et al. Sialylation determines the nephritogenicity of IgG3 cryoglobulins. J Am Soc Nephrol 2012;23:1869-78.
21. Erausquin C, Merino R, Izui S, Fernandez-Sueiro L, Saez F, Fernandez F, et al. Therapeutic effect of early thymic irradiation in (NZB X NZW)F1 mice, associated with a selective decrease in the levels of IgG3 and gp70-anti-gp70 immune complexes. Cell Immunol 1995;161:207-12.
22. Sthoeger ZM, Zinger H, Mozes E. Beneficial effects of the antioestrogen tamoxifen on systemic lupus erythematosus of (NZB X NZW)F1 female mice are associated with specific reduction of IgG3 autoantibodies. Ann Rheum Dis 2003;62:341-6.
23. Jacob CO, van der Meide PH, McDevitt HO. In vivo treatment of (NZB X NZW)F1 lupus-like nephritis with monoclonal antibody to g interferon. J Exp Med 1987;166:798-803.
24. Nakajima A, Hirose S, Yagita H, Okumura K. Roles of IL-4 and IL-12 in the development of lupus in NZB/W F1 mice. J Immunol 1997;158:1466-72.
25. Hu YL, Metz DP, Chung J, Siu G, Zhang M. B7RP-1 blockade ameliorates autoimmunity through regulation of follicular helper T cells. J Immunol 2009;182:1421-8.
26. Daikh DI, Wofsy D. Reversal of murine lupus nephritis with CTLA4Ig and cyclophosphamide. J Immunol 2001;166:2913-6.
27. Wofsy D, Seaman WE. Reversal of advanced murine lupus in NZB/NZW F1 mice by treatment with monoclonal antibody to L3T4. J Immunol 1987;138:3247-53.
28. Adelman NE, Watling DL, McDevitt HO. Treatment of (NZB X NZW)F1 disease with anti-I-A monoclonal antibodies. J Exp Med 1983;158:1350-5.
29. Strengell M, Matikainen S, Siren J, Lehtonen A, Foster D, Julkunen I, et al. IL-21 in synergy with IL-15 or IL-18 enhances IFN-g production in human NK and T cells. J Immunol 2003;170:5464-9.
30. Sarra M, Caruso R, Cupi ML, Monteleone I, Stolfi C, Campione E, et al. IL-21 promotes skin recruitment of CD41 cells and drives IFN-g-dependent epidermal hyperplasia. J Immunol 2011;186: 5435-42.
31. Okamoto A, Fujio K, Tsuno NH, Takahashi K, Yamamoto K. Kidney-infiltrating CD41 T-cell clones promote nephritis in lupus-prone mice. Kidney Int 2012;82:969-79.
32. Odegard JM, DiPlacido LD, Greenwald L, Kashgarian M, Kono DH, Dong C, et al. ICOS controls effector function but not trafficking receptor expression of kidney-infiltrating effector T cells in murine lupus. J Immunol 2009;182:4076-84.
33. Clynes R, Dumitru C, Ravetch JV. Uncoupling of immune complex formation and kidney damage in autoimmune glomerulone-phritis. Science 1998;279:1052-4.
34. Rozzo SJ, Allard JD, Choubey D, Vyse TJ, Izui S, Peltz G, et al. Evidence for an interferon-inducible gene, Ifi202, in the susceptibility to systemic lupus. Immunity 2001;15:435-43.
35. Choubey D. Interferon-inducible Ifi200-family genes as modifiers of lupus susceptibility. Immunol Lett 2012;147:10-7.
36. Potula HH, Morel L. Genetic variation at a Yin-Yang 1 response site regulates the transcription of cyclin-dependent kinase inhibitor p18INK4C transcript in lupus-prone mice. J Immunol 2012; 188:4992-5002.
37. Perry DJ, Yin Y, Telarico T, Baker HV, Dozmorov I, Perl A, et al. Murine lupus susceptibility locus Sle1c2 mediates CD41 T cell activation and maps to estrogen-related receptor g. J Immunol 2012;189:793-803.
38. Qi ZM, Wang J, Sun ZR, Ma FM, Zhang QR, Hirose S, et al. Polymorphism of the mouse gene for the interleukin 10 receptor a chain (Il10ra) and its association with the autoimmune phenotype. Immunogenetics 2005;57:697-702.
39. Pau E, Loh C, Minty GE, Chang NH, Wither JE. Identification of a lupus-susceptibility locus leading to impaired clearance of apoptotic debris on New Zealand Black chromosome 13. Genes Immun 2013;14:154-61.
40. Zeumer L, Sang A, Niu H, Morel L. Murine lupus susceptibility locus Sle2 activates DNA-reactive B cells through two sub-loci with distinct phenotypes. Genes Immun 2011;12:199-207.
41. Cuda CM, Zeumer L, Sobel ES, Croker BP, Morel L. Murine lupus susceptibility locus Sle1a requires the expression of two sub-loci to induce inflammatory T cells. Genes Immun 2010;11: 542-53.
42. Scalapino KJ, Tang Q, Bluestone JA, Bonyhadi ML, Daikh DI. Suppression of disease in New Zealand Black/New Zealand White lupus-prone mice by adoptive transfer of ex vivo expanded regulatory T cells. J Immunol 2006;177:1451-9.
43. Hayashi T, Hasegawa K, Adachi C. Elimination of CD41CD251 T cell accelerates the development of glomerulonephritis during the preactive phase in autoimmune-prone female NZB 3 NZW F mice. Int J Exp Pathol 2005;86:289-96.
44. Altman A, Theofilopoulos AN, Weiner R, Katz DH, Dixon FJ. Analysis of T cell function in autoimmune murine strains: Defects in production and responsiveness to interleukin 2. J Exp Med 1981;154:791-808.
45. Huang FP, Stott DI. Restoration of an early, progressive defect in responsiveness to T-cell activation in lupus mice by exogenous IL-2. Autoimmunity 1993;15:19-29.
46. Chevalier N, Thorburn AN, Macia L, Tan J, Juglair L, Yagita H, et al. Inflammation and lymphopenia trigger autoimmunity by suppression of IL-2-controlled regulatory T cell and increase of IL-21-mediated effector T cell expansion. J Immunol 2014; 193:4845-58.