PROSPECTS FOR PHARMACOTHERAPY OF SYSTEMIC LUPUS ERYTHEMATOSUS
https://doi.org/10.14412/1995-4484-2014-311-321
Abstract
The whole armory of the drugs used in rheumatology is employed to treat systemic lupus erythematosus (SLE); how- ever, most of them have not got regulatory authorities' approval and are used off-label for SLE. The successful use of a biological agent rituximab (anti-CD20 monoclonal antibodies) and the registration of belimumab (anti-BLyS mono- clonal antibodies) for the treatment of SLE have spurred the development of novel approaches to treating this disease.
About the Authors
E. L. Nasonov
Nasonova Research Institute of Rheumatology, Moscow, Russia
Russian Federation
Russian Federation
S. K. Solovyev
Nasonova Research Institute of Rheumatology, Moscow, Russia
Russian Federation
Russian Federation
References
1. Насонов ЕЛ, редактор. Системная красная волчанка. В кн.: Клинические рекомендации. Москва: ГЭОТАР-Медиа; 2010. С. 429–81. [Nasonov EL, editor. Systemic lupus erythe- matosus. In: Klinicheskie rekomendatsii [Clinical recommenda- tions]. Moscow: GEOTAR-Media; 2010. P. 429–81.]
2. Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med. 2008;358(9):929–39. DOI: 10.1056/NEJMra071297.
3. Murphy G, Lisnevskaia L, Isenberg D. Systemic lupus erythe- matosus and other autoimmune rheumatic diseases: chalenges to treatment. Lancet. 2013;382(9894):808–18. DOI: 10.1016/S0140-6736(13)60889-2. Epub 2013 Aug 23.
4. Stohl W. Future prospects in biologic therapy for systemic lupus erythematosus. Nat Rev Rheumatol. 2013;9(12):705–20. DOI: 10.1038/nrrheum.2013.136. Epub 2013 Sep 10.
5. Thanou A, Merrill JT. Treatment of systemic lupus erythemato- sus: new therapeutic avenues and blind alleys. Nat Rev Rheumatol. 2014;10(1):23–34. DOI: 10.1038/nrrheum.2013.145. Epub 2013 Oct 8.
6. Насонов ЕЛ, редактор. Генно-инженерные биологические препараты в лечении ревматоидного артрита. Москва: ИМА-ПРЕСС; 2013. С. 549. [Nasonov EL, editor. Genetically engineered biological biological preparations in treatment of rheumatoid arthritis. Moscow: IMA-PRESS; 2013. P. 549]
7. Насонов ЕЛ, редактор. Анти-В-клеточная терапия в ревматологии: фокус на ритуксимаб. Москва: ИМА- ПРЕСС; 2012. С. 119–52. [Nasonov EL, editor. Anti-В-cellular therapy in rheumatology: focus on ritukximab. Moscow: IMA- PRESS; 2013. P. 119–52.]
8. Sanz I, Lee FE. B cells as therapeutic targets in SLE. Nat Rev Rheumatol. 2010;6(6):326–37. DOI: 10.1038/nrrheum.2010.68. 9. Левицки А, Линдер С, Ван Волленховен РФ. Ритуксимаб в терапии системной красной волчнки. Научно-практическая ревматология. 2013;51(3):223–39. [Levitsky A, Linder S, Vollenhoven RF. Rituximab in the management of systemic lupus erythematosus. Nauchno-prakticheskaya revmatologiya = Rheumatology Science and Practice. 2013;51(3):223–39. (In Russ.)]. DOI: http://dx.doi.org/10.14412/1995-4484-2013-1494.
9. Цанян МЭ, Соловьев СК, Торгашина АВ и др. Эффективность терапии ритуксимабом у больных системной красной волчанкой при длительном динамическом наблюдении. Научно-практическая ревматология. 2014;52(2):159–68. [Tsanyan ME, Soloviev SK, Torgashina AV. Rituximab treatment efficacy in patients with sys- temic lupus erythematosus refractory to standard therapy in the long-term follow-up. Nauchno-prakticheskaya revmatologiya = Rheumatology Science and Practice. 2014;52(2):159–68. (In Russ.)]. DOI: http://dx.doi.org/10.14412/1995-4484-2014-159- 168.
10. Merrill JT, Neuwelt CM, Wallace DJ, et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythe- matosus: The randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum. 2010;62(1):222–33. DOI: 10.1002/art.27233.
11. Rovin BH, Furie R, Latinis K, et al.; LUNAR Investigator Group. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the lupus nephritis assessment with rituximab study. Arthritis Rheum. 2012;64(4):1215–26. DOI: 10.1002/art.34359. Epub 2012 Jan 9.
12. Wofsy D. Recent progress in conventional and biologic therapy for systemic lupus erythematosus. Ann Rheum Dis. 2013;72 Suppl 2:ii66–8. DOI: 10.1136/annrheumdis-2012-202204. Epub 2012 Dec 19.
13. Tew GW, Rabbee N, Wolslegel K, et al. Baseline autoantibody profiles predict normalization of complement and anti-dsDNA autoantibody levels following Rituximab treatment in systemic lupus erythematosus. Lupus. 2010;19(2):146–57. DOI: 10.1177/0961203309350752. Epub 2009 Nov 27.
14. Murray E, Perry M. Off-label use of Rituximab in systemic lupus erythematosus: a systemic review. Clin Rheumatol. 2010;29(7):707–16. DOI: 10.1007/s10067-010-1387-5. Epub 2010 Feb 13.
15. Pepper R, Grifith M, Kirwan C, et al. Rituximab is an effective treatment for lupus nephritis and allows a reduction in mainte- nance steroids. Nephrol Dial Transplant. 2009;24(12):3717–23. DOI: 10.1093/ndt/gfp336. Epub 2009 Jul 17.
16. Ezeonyeji AN, Isenberg DA. Early treatment with rituximab in newly diagnosed systemic lupus erythematosus patients: a steroid-sparing regime. Rheumatology (Oxford). 2012;51(3):476–81. DOI: 10.1093/rheumatology/ker337. Epub 2011 Nov 16.
17. Gordon MB, Ashby D, Pepper RJ, et al. Prospective observa- tional single-centre cohort study to evaluate the effectiveness of treating lupus nephritis with rituximab and mycophenolate mofetil but no oral steroids. Ann Rheum Dis. 2013;72(8):1280–6. DOI: 10.1136/annrheumdis-2012-202844. Epub 2013 Jun 5.
18. Tedeschi B, Arnaud L, Hie M, et al. Successful treatment of combined proliferative and membranous lupus nephritis usind a full corticosteroid-free regimen. Ann Rheum Dis. 2012;73(2):474–5. DOI: 10.1136/annrheumdis-2013-204385.
19. Li EK, Tam LS, Zhu TY, et al. Is combination rituximab with cyclophosphamide better than Rituximab alone in the treatment of lupus nephritis? Rheumatology (Oxford). 2009;48(8):892–8. DOI: 10.1093/rheumatology/kep124. Epub 2009 May 28.
20. Chen H, Zheng W, Su J, et al. Low-dose rituximab therapy for refractory thrombocytopenia in patients with systemic lupus ery- thematosus – a prospective pilot study. Rheumatology (Oxford). 2011;50(9):1640–4. DOI: 10.1093/rheumatolofy/ker176.
21. Weidenbusch M, Rö mmele C, Schrö ttle A, Anders HJ. Beyond the LUNAR trial. Efficacy of rituximab in refractory lupus nephritis. Nephrol Dial Transplant. 2013;28(1):106–11. DOI: 10.1093/ndt/gfs285. Epub 2012 Jul 3.
22. Bertsias GK, Tektonidou M, Amoura Z, et al. Joint European League Against Rheumatism and European Renal Association- European Dialysis and Transplant Association (EULAR/ERA- EDTA) recommendations for the management of adult and pae- diatric lupus nephritis. Ann Rheum Dis. 2012;71(11):1771–82. DOI: 10.1136/annrheumdis-2012-201940. Epub 2012 Jul 31.
23. Hanh BH, McMahon MA, Wilkinson A, et al.; American College of Rheumatology. American College of Rheumatology duidlines for screening, treatment, and management of lupus nephritis. Arthritis Care Res (Hoboken). 2012;64(6):797–808. DOI: 10.1002/acr.21664.
24. Guerry MJ, Brogan P, Bruce IN, et al. Recommendations for the use of Rituximab in anti-neutrophile cytoplasm antibody-associ- ated vasculitis. Rheumatology (Oxford). 2011;51(4):634–43. DOI: 10.1093/rheumatolofy/ker150. Epub 2011 May 25.
25. Mysler EF. Efficacy and safety of ocrelizumab, a humanized antiCD20 antibody, in patients with active proliferative lupus nephritis (LN): results from the randomized, double-blind phase III BELONG study. Arthritis Rheum. 2010;62:S606–7.
26. Tedder TF, Inaoki M, Sato S. The CD19–CD21 complex regu- lates signal transduction thresholds governing humoral immunity and autoimmunity. Immunity. 1997;6(2):107–18. DOI: http://dx.doi.org/10.1016/S1074-7613(00)80418-5.
27. Herbst R, Wang Y, Gallagher S, et al. B-cell depletion in vitro and in vivo with an afucosylated anti-CD19 antibody. J Pharmacol Exp Ther. 2010;335(1):213–22. DOI: 10.1124/jpet.110.168062. Epub 2010 Jul 6.
28. Cardarelli PM, Rao-Naik C, Chen S, et al. A nonfucosylated human antibody to CD19 with potent B-cell depletive activity for therapy of B-cell malignancies. Cancer Immunol Immunother. 2010;59(2):257–65. DOI: 10.1007/s00262-009-0746-z.
29. Carnahan J, Stein R, Qu Z, et al. Epratuzumab, a CD22-target- ing recombinant humanized antibody with a different mode of action from rituximab. Mol Immunol. 2007;44(6):1331–41. DOI: http://dx.doi.org/10.1016/j.molimm.2006.05.007. Epub 2006 Jun 30.
30. Traczewski P, Rudnicka L. Treatment of systemic lupus erythe- matosus with epratuzumab. Br J Clin Pharmacol. 2011;71(2):175–82. DOI: 10.1111/j.1365-2125.2010.03767.x.
31. Sieger N, Fleischer SJ, Mei HE, et al. CD22 ligation inhibits downstream B-cell receptor signaling ava Ca2+ flux upon activa- tion. Arthritis Rheum. 2013;65(3):770–9. DOI: 10.1002/art.37818.
32. Wallace DJ, Kalunian K, Petri MA, et al. Efficacy and safety of epratuzumab in patients with moderate/severe active systemic lupus erythematosus: results from EMBLEM, a phase IIb, ran- domised, double-blind, placebo-controlled, multicentre study. Ann Rheum Dis. 2014;73(1):183–90. DOI: 10.1136/annrheumdis-2012-202760. Epub 2013 Jan 12.
33. Wallace DJ, Gordon C, Strand V, et al. Efficacy and safety of epratuzumab in patients with moderate/severe flaring systemic lupus erythematosus: results from two randomized, double-blind, placebo-controlled, multicentre studies (ALLEVIATE) and fol- low-up. Rheumatology (Oxford). 2013;52(7):1313–22. DOI: 10.1093/rheumatology/ket129. Epub 2013 Mar 28.
34. FDA approves Benlysta to treat lupus. [Last accessed on 2011 Mar 28]. Available from: http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncemen ts/ucm246489.htm
35. European Medicines Agency. Benlysta: belimumab. (cited August 8, 2011). Available from: www.ema.ruropa.eu/ema/index/jsp?curl=pages/medicines/huma n/medicines.002015/human_med_001466.jsp&mid=WC0bac058 001d124
36. Merrill JT. Ending the 50-year drought of FDA drug approval for SLE. Bull NYU Hosp Joint Dis. 2011;69(3):238–42.
37. Stohl W, Hilbert DM. The discovery and development of beli- mumab: the anti-BlyS-lupus connection. Nature Biotechnol. 2012;30(1):69–77. DOI: 10.1038/nbt.2076.
38. Насонов ЕЛ, Решетняк ТМ, Денисов ЛН и др. Белимумаб: прогресс в лечении системной красной волчанки. Научно- практическая ревматология. 2012;51(5):13–9. [Nasonov EL, Reshetnyak TM, Denisov LN, et al. Belimumab: advances in drug therapy for systemic lupus erythematosus. Nauchno-prak- ticheskaya revmatologiya = Rheumatology Science and Practice. 2012;51(5):13–9. (In Russ.)]. DOI: http://dx.doi.org/10.14412/1995-4484-2012-1174.
39. Furie R, Stohl W, Ginzler EM, et al. Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with sys- temic lupus erythematosus. Arthritis Res Ther. 2008;10(5):R109. DOI: 10.1186/ar2506. Epub 2008 Sep 11.
40. Wallace DJ, Stohl W, Ginzler EM, et al. A phase II, randomized, double-blind, placebo-controlled, dose-ranging study of beli- mumab in patients with active systemic lupus erythematosus. Arthritis Rheum. 2009;61(9):1168–78. DOI: 10.1002/art.24699.
41. Navarra SV, Guzman RM, Gallacher AE, et al.; BLISS-52 Study Group. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet. 2011;377(9767):721–731. DOI: 10.1016/S0140-6736(10)61354-2. Epub 2011 Feb 4.
42. Furie, R, Petri M, Zamani E, et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 2011;63(12):3918–30.
43. DOI: 10.1002/art.30613.
44. Ginzler EM, Wallace DJ, Merrill JT, et al. Disease control and safety of belimumab plus standart therapy over 7 years in patients with systemic lupus erythematosus. J Rheumatology. 2014;41(2):300–9. DOI: 10.3899/jrheum.121368. Epub 2013 Nov 1.
45. Furie RA, Petri MA, Wallace DJ, et al. Novel evidence-based systemic lupus erythematosus responder index. Arthritis Rheum.
46. ;61(9):1143–51. DOI: 10.1002/art.24698.
47. Furie RA, Leon G, Thomas M, et al. A phase 2, randomized, placebo-controlled clinical trial of blisibimod, an inhibitor of B cell activating factor, in patients with moderate-to-severe sys- temic lupus erythematosus, the PEARL-SC study. Arthritis Rheum. 2014 Apr 19. DOI: 10.1136/annrheumdis-2013-205144.
48. Genovese MC, Bojin S, Biagini IM, et al. Tabalumab in rheuma- toid arthritis patients with an inadequate response to methotrex- ate and naive to biologic therapy: a phase II, randomized, place- bo-controlled trial. Arthritis Rheum. 2013;65(4):880–9. DOI: 10.1002/art.37820.
49. Genovese MC, Fleischmann RM, Greenwald M, et al. Tabalumab, an anti-BAFF monoclonal antibody, in patients with active rheumatoid arthritis with an inadequate response to TNF inhibitors. Ann Rheum Dis. 2013 Sep 1;72(9):1461–8. DOI: http://dx.doi.org/10.1136/annrheumdis-2012-202775.
50. Dall'Era M, Chakravarty E, Wallace D, et al. Reduced B lym- phocyte and immunoglobulin levels after atacicept treatment in patients with systemic lupus erythematosus: results of a multicen- ter, phase Ib, double-blind, placebo-controlled, dose-escalating trial. Arthritis Rheum. 2007;56(12):4142–50. DOI: http://dx.doi.org/10.1002/art.23047.
51. Ginzler EM, Wax S, Rajeswaran A, et al. Atacicept in combina- tion with MMF and corticosteroids in lupus nephritis: results of a prematurely terminated trial. Arthritis Res Ther. 2012;14(1):R33. DOI: 10.1186/ar3738.
52. Baechler EC, Batliwalla FM, Karypis G, et al. Interferon- inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA. 2003;100(5):2610–5. DOI: http://dx.doi.org/10.1073/pnas.0337679100. Epub 2003 Feb 25.
53. Bennett L, Palucka AK, Arce E. et al. Interferon and granu- lopoiesis signatures in systemic lupus erythematosus blood. J Exp Med. 2003;197(6):711–23. DOI: http://dx.doi.org/10.1084/jem.20021553.
54. Kirou KA, Lee C, George S, et al. Activation of the interferon-α pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum. 2005;52(5):1491–503. DOI: http://dx.doi.org/10.1002/art.21031.
55. Peterson KS, Huang JF, Zhu J, et al. Characterization of hetero- geneity in the molecular pathogenesis of lupus nephritis from transcriptional profiles of laser-captured glomeruli. J Clin Invest. 2004;113(12):1722–33. DOI: http://dx.doi.org/10.1172/JCI200419139.
56. Nzeusseu Toukap A, Galant C, Theate I, et al. Identification of distinct gene expression profiles in the synovium of patients with systemic lupus erythematosus. Arthritis Rheum. 2007;56(5):1579–88. DOI: http://dx.doi.org/10.1002/art.22578.
57. Rö nnblom LE, Alm GV, Oberg KE. Possible induction of sys- temic lupus erythematosus by interferon-α treatment in a patient with a malignant carcinoid tumor. J Intern Med. 1990;227(3):207–10. DOI: http://dx.doi.org/10.1111/j.1365- 2796.1990.tb00144.x.
58. Niewold TB, Swedler WI. Systemic lupus erythematosus arising during interferon-α therapy for cryoglobulinemic vasculitis asso- ciated with hepatitis C. Clin Rheumatol. 2005;24(2):178–81. DOI: http://dx.doi.org/10.1007/s10067-004-1024-2. Epub 2004 Nov 24.
59. Thacker SG, Zhao W, Smith CK, et al. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum. 2012;64(9):2975–85. DOI: 10.1002/art.34504.
60. Denny MF, Thacker S, Mehta H, et al. Interferon-α promotes abnormal vasculogenesis in lupus: a potential pathway for prema- ture atherosclerosis. Blood. 2007;110(8):2907–915. DOI: http://dx.doi.org/10.1182/blood-2007-05-089086. Epub 2007 Jul 16.
61. Somers EC, Zhao W, Lewis EE, et al. Type I interferons are asso- ciated with subclinical markers of cardiovascular disease in a cohort of systemic lupus erythematosus patients. PLoS ONE. 2012;7(5):e37000. DOI: 10.1371/journal.pone.0037000. Epub 2012 May 14.
62. Morimoto AM, Flesher DT, Yang J, et al. Association of endoge- nous anti-interferon-α autoantibodies with decreased interferon- pathway and disease activity in patients with systemic lupus ery- thematosus. Arthritis Rheum. 2011;63(8):2407–15. DOI: http://dx.doi.org/10.1002/art.30399.
63. Yao Y, Richman L, Higgs BW, et al. Neutralization of interferon- α/β-inducible genes and downstream effect in a phase I trial of an anti-interferon-α monoclonal antibody in systemic lupus ery- thematosus. Arthritis Rheum. 2009;60(6):1785–96. DOI: http://dx.doi.org/10.1002/art.24557.
64. Merrill JT, Wallace DJ, Petri M, et al. Safety profile and clinical activity of sifalimumab, a fully human anti-interferon α mono- clonal antibody, in systemic lupus erythematosus: a phase I, muticentre, double-blind randomised study. Ann Rheum Dis. 2011;70(11):1905–13. DOI: http://dx.doi.org/10.1136/ard.2010.144485.
65. Petri M, Wallace DJ, Spindler A, et al. Sifalimumab, a human anti-interferon-α monoclonal antibody, in systemic lupus erythe- matosus: a phase I randomized, controlled, dose-escalation study. Arthritis Rheum. 2013;65(4):1011–21. DOI: 10.1002/art.37824.
66. Tcherepanova I, Curtis M, Sale M, et al. Results of a randomized placebo controlled phase IA study of AGS-009, a humanized anti-interferon-α monoclonal antibody in subjects with systemic lupus erythematosus. Ann Rheum Dis. 2012;71 Suppl 3:536.
67. McBride JM, Jiang J, Abbas AR , et al. Safety and pharmacody- namics of rontalizumab in patients with systemic lupus erythe- matosus: results of a phase I, placebo-controlled, double-blind, dose-escalation study. Arthritis Rheum. 2012;64(11):3666–76. DOI: 10.1002/art.34632.
68. Kalunian K. Efficacy and safety of rontalizumab (anti-interferon α) in SLE subjects with restricted immunosuppressant use: results of a randomized, double-blind placebo-controlled phase 2 study. Arthritis Rheum. 2012;64:S1111.
69. Santiago-Raber ML, Baccala R, Haraldsson KM, et al. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J Exp Med. 2003;197:777–88. DOI: http://dx.doi.org/10.1084/jem.20021996.
70. Agrawal, H. et al. Deficiency of type I IFN receptor in lupus- prone New Zealand Mixed 2328 mice decreases dendritic cell numbers and activation and protects from disease. J Immunol. 2009; 183, 6021–6029. DOI: http://dx.doi.org/10.4049/jim- munol.0803872.
71. Goronzy JJ, Weyand CM. T-cell co-stimulatory pathways in autoimmunity. Arthritis Res Ther. 2008;10 Suppl 1:S3. DOI: http://dx.doi.org/10.1186/ar2414.
72. Yamada A, Salama AD, Sayegh MH. The role of novel T cell costimulatory pathways in autoimmunity and transplantation. J Am Soc Nephrol. 2002;13(2):559–75.
73. Finck BK, Linsley PS, Wofsy D. Treatment of murine lupus with CTLA4Ig. Science. 1994;265(5176):1225–7. DOI: http://dx.doi.org/10.1126/science.7520604.
74. Merrill JT, Burgos-Vargas R, Westhovens R, et al. The efficacy and safety of abatacept in patients with non-life-threatening manifestations of systemic lupus erythematosus: results of a twelve-month, multicenter, exploratory, phase IIb, randomized, double-blind, placebo-controlled trial. Arthritis Rheum. 2010;62(10):3077–87. DOI: http://dx.doi.org/10.1002/art.27601.
75. Furie R. Efficacy and safety of abatacept over 12 months in
76. patients with lupus nephritis: results from a multicenter, random- ized, double-blind, placebo-controlled phase II/III study. Arthritis Rheum. 2011;63:S962–3.
77. Wofsy D, Hillson JL, Diamond B. Abatacept for lupus nephritis: alternative definitions of complete response support conflicting conclusions. Arthritis Rheum. 2012;64(11):3660–5. DOI: http://dx.doi.org/10.1002/art.34624.
78. Daikh DI, Wofsy D. Cutting edge: reversal of murine lupus nephritis with CTLA-4Ig and cyclophosphamide. J Immunol. 2001;166(5):2913–6. DOI: http://dx.doi.org/10.4049/jim- munol.166.5.2913.
79. Desai-Mehta A, Lu L, Ramsey-Goldman R, Datta K. Hyperexpression of CD40 ligand by B and T cells in human lupus and its role in pathogenic autoantibody production. J Clin Invest. 1996;97(9):2063–73. DOI: http://dx.doi.org/10.1172/JCI118643.
80. Koshy M, Berger D, Crow MK. Increased expression of CD40 ligand on systemic lupus erythematosus lymphocytes. J Clin Invest. 1996;98(3):826–37. DOI: http://dx.doi.org/10.1172/JCI118855.
81. Mohan C, Shi Y, Laman JD, Datta SK. Interaction between CD40 and its ligand gp39 in the development of murine lupus nephritis. J Immunol. 1995;154(3):1470–80.
82. Early GS, Zhao W, Burns CM. Anti-CD40 ligand antibody treat- ment prevents the development of lupus-like nephritis in a subset of New Zealand Black X New Zealand White mice. J Immunol. 1996;157(7):3159–64.
83. Russell JQ, Mooney T, Cohen PL, et al. Anti-CD40L accelerates renal disease and adenopathy in MRL-lpr mice in parallel with decreased thymocyte apoptosis. J Immunol. 1998;161(2):729–39.
84. Kalunian KC, Davis JC Jr, Merrill JT, et al. Treatment of sys- temic lupus erythematosus by inhibition of T cell costimulation with anti-CD154. Arthritis Rheum. 2002;46(12):3251–8. DOI: http://dx.doi.org/10.1002/art.10681.
85. Boumpas DT, Furie R, Manzi D, et al.; BG9588 Lupus Nephritis Trial Group. A short course of BG9588 (anti-CD40 ligand anti- body) improves serologic activity and decreases hematuria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum. 2003;48(3):719–27. DOI: http://dx.doi.org/10.1002/art.10856.
86. Jones SA, Richards PJ, Scheller J, Rose-John S. IL-6 transsig- naling: the in vivo consequences. J Interferon Cytokine Res. 2005;25(5):241–53. DOI: http://dx.doi.org/10.1089/jir.2005.25.241.
87. Mihara M, Hashizume M, Yoshida H, et al. IL6/IL-6 receptor system and its role in physiological and pathological conditions. Clin Sci (Lond). 2012;122(4):143–59. DOI: 10.1042/CS20110340.
88. Tackey E, Lipsky PE, Illei GG. Rationale for interleukin-6 blockade in systemic lupus erythematosus. Lupus. 2004;13(5):339–43. DOI: http://dx.doi.org/10.1191/0961203304lu1023oa.
89. Linker-Israeli M, Deans RJ, Wallace DJ, et al. Elevated levels of endogenous IL-6 in systemic lupus erythematosus: a putative role in pathogenesis. J Immunol. 1991;147(1):117–23.
90. Peterson E, Robertson AD, Emlen W. Serum and urinary inter- leukin-6 in systemic lupus erythematosus. Lupus. 1996;5(6):571–5. DOI: http://dx.doi.org/10.1177/096120339600500603.
91. Grondal G, Gunnarsson I, Ronnelid J, et al. Cytokine produc- tion, serum levels and disease activity in systemic lupus erythe- matosus. Clin Exp Rheumatol. 2000;18(5):565–70.
92. Peterson E, Robertson AD, Emlen W. Serum and urinary inter- leukin-6 in systemic lupus erythematosus. Lupus. 1996;5(6):571–5. DOI: http://dx.doi.org/10.1177/096120339600500603.
93. Grondal G, Gunnarsson I, Ronnelid J, et al. Cytokine production, serum levels and disease activity in systemic lupus erythe-
94. matosus. Clin Exp Rheumatol. 2000;18(5):565–70.
95. Iwano M, Dohi K, Hirata E, et al. Urinary levels of IL-6 in patients with active lupus nephritis. Clinical Nephrology. 1993;40(1):16–21.
96. Malide D, Russo P, Bendayan M. Presence of tumor necrosis factor alpha and interleukin-6 in renal mesangial cells of lupus nephritis patients. Human Pathology. 1995;26(5):558–64. DOI: http://dx.doi.org/10.1016/0046-8177(95)90253-8.
97. Herrera-Esparza R, Barbosa-Cisneros O, Villalobos-Hurtado R, Avalos-DТaz E. Renal expression of IL-6 and TNFα genes in lupus nephritis. Lupus. 1998;7(3):154–8. DOI: http://dx.doi.org/10.1191/096120398678919949.
98. Tsai GY, Wu TH, Yu CL, et al. Increased excretions of β2- microglobulin, IL-6, and IL-8 and decreased excretion of Tamm-Horsfall glycoprotein in urine of patients with active lupus nephritis. Nephron. 2000;85(3):207–14. DOI: http://dx.doi.org/10.3109/03009749609069992.
99. Hirohata S, Miyamoto T. Elevated levels of interleukin-6 in cere- brospinal fluid from patients with systemic lupus erythematosus and central nervous system involvement. Arthritis Rheum. 1990;33(5):644–9. DOI: http://dx.doi.org/10.1002/art.1780330506.
100. Hagiwara E, Gourley MF, Lee S, Klinman DM. Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin-10: interferon-α-secreting cells in the peripheral blood. Arthritis Rheum. 1996;39(3):379–85. DOI: http://dx.doi.org/10.1002/art.1780390305.
101. Swaak G, van den Brink HG, Aarden LA. Cytokine production (IL-6 and TNFα) in whole blood cell cultures of patients with systemic lupus erythematosus. Scand J Rheumatol. 1996;25(4):233–8. DOI: http://dx.doi.org/10.3109/03009749609069992.
102. Klashman DJ, Martin RA, Martinez-Maza O, Stevens RH.
103. In vitro regulation of B cell differentiation by interleukin-6 and soluble CD23 in systemic lupus erythematosus B cell subpopula- tions and antigen-induced normal B cells. Arthritis Rheum. 1991;34(3):276–86. DOI: http://dx.doi.org/10.1002/art.1780340305.
104. Kitani A, Hara M, Hirose T, et al. Autostimulatory effects of IL- 6 on excessive B cell differentiation in patients with systemic lupus erythematosus: analysis of IL-6 production and IL-6R expression. Clin Exp Immunol. 1992;88(1):75–83. DOI: http://dx.doi.org/10.1111/j.1365-2249.1992.tb03042.x.
105. Suzuki H, Yasukawa K, Saito T, et al. Serum soluble interleukin- 6 receptor in MRL/lpr mice is elevated with age and mediates the interleukin-6 signal. Eur J Immunol. 1993;23(5):1078–82. DOI: http://dx.doi.org/10.1002/eji.1830230515.
106. Tang B, Matsuda T, Akira S, et al. Age-associated increase in interleukin 6 in MRL/lpr mice. Int Immunol. 1991;31(3):273–8. DOI: http://dx.doi.org/10.1093/intimm/3.3.273.
107. Alarcon-Riquelme ME, Moller G, Fernandez C. Age-dependent responsiveness to interleukin-6 in B lymphocytes from a systemic lupus erythematosus-prone (NZB x NZW)F1 hybrid. Clin Immunol Immunopath. 1992;62(3):264–9. DOI: http://dx.doi.org/10.1016/0090-1229(92)90101-S.
108. Mihara M, Fukui H, Koishihara Y, et al. Immunologic abnor- mality in NZB/W F1 mice. Thymus-independent expansion of B cells responding to interleukin-6. Clin Exp Immunol. 1990;82(3):533–7. DOI: http://dx.doi.org/10.1111/j.1365- 2249.1990.tb05485.x.
109. Mihara M, Ohsug Y. Possible role of IL-6 in pathogenesis of immune complex-mediated glomerulonephritis in NZB/W F1 mice: induction of IgG class anti-DNA autoantibody production. Intern. Arch Allergy Appl Immunol. 1990;93(1):89–92. DOI: http://dx.doi.org/10.1159/000235285.
110. Ryffel B, Car BD, Gunn H, et al. Interleukin-6 exacerbates glomerulonephritis in (NZBxNZW)F1 mice. Am J Pathol. 1994;144(5):927–37.
111. Finck BK, Chan B, Wofsy D. Interleukin 6 promotes murine lupus in NZB/NZW F1 mice. J Clin Inves. 1994;94(2):585–91. DOI: http://dx.doi.org/10.1172/JCI117373.
112. Mihara M, Takagi N, Takeda Y, Ohsugi Y. IL-6 receptor blockage inhibits the onset of autoimmune kidney disease in NZB/WF1 mice. Clin Exp Immunol. 1998;112(3):397–402. DOI: http://dx.doi.org/10.1046/j.1365-2249.1998.00612.x.
113. Liang B, Gardner DB, Griswold DE, et al. Anti-interleukin-6 monoclonal antibody inhibits autoimmune responses in a murine model of systemic lupus erythematosus. Immunology. 2006;119(3):296–305. DOI: http://dx.doi.org/10.1111/j.1365- 2567.2006.02433.x.
114. Pflegerl P, Vesely P, Hantusch B, et al. Epidermal loss of JunB leads to a SLE phenotype due to hyper IL-6 signaling. Proc Nat Acad Sci USA. 2009;106(48):20423–8. DOI: http://dx.doi.org/10.1073/pnas.0910371106.
115. Illei GG, Shirota Y, Yarboro CH, et al. Tocilizumab in systemic lupus erythematosus: data on safety, preliminary efficacy, and impact on circulating plasma cells from an open-label phase I dosage-escalation study. Arthritis Rheum. 2010;62(2):542–52. DOI: http://dx.doi.org/10.1002/art.27221.
116. Garcia-Hernandez FJ, Gonzalez-Leon R, Castillo-Palma MJ, et al. Tocilizumab for treating refractory haemolytic anaemia in a patient with systemic lupus erythematosus. Rheumatology (Oxford). 2012;51(10):1918–9. DOI: http://dx.doi.org/10.1093/rheumatology/kes072. Epub 2012 Apr 17.
117. Kamata Y, Minota S. Successful treatment of massive intractable pericardial effusion in a patient with systemic lupus erythemato- sus with tocilizumab. BMJ Case Rep. 2012 Dec 21;2012. pii: bcr2012007834. DOI: http://dx.doi.org/10.1136/bcr-2012- 007834.
118. Jacob CO, McDevitt HO. Tumour necrosis factor-α in murine autoimmune «lupus» nephritis. Nature. 1988;331(6154):356–8. DOI: http://dx.doi.org/10.1038/331356a0.
119. Gordon C, Ranges GE, Greenspan JS, Wofsy D. Chronic thera- py with recombinant tumor necrosis factor-α in autoimmune NZB/NZW F1 mice. Clin Immunol Immunopathol. 1989;52(3):421–34. DOI: http://dx.doi.org/10.1016/0090- 1229(89)90157-8.
120. Kontoyiannis D, Kollias G. Accelerated autoimmunity and lupus nephritis in NZB mice with an engineered heterozygous deficiency in tumor necrosis factor. Eur J Immunol. 2000;30(7):2038–47. DOI: http://dx.doi.org/10.1002/1521- 4141(200007)30:7%3C2038::AID-IMMU2038%3E3.0.CO;2-K.
121. Jacob N, et al. Accelerated pathological and clinical nephritis in systemic lupus erythematosus-prone New Zealand Mixed 2328 mice doubly deficient in TNF receptor 1 and TNF receptor 2 via a Th17-associated pathway. J Immunol. 2009;182(4):2532–41. DOI: http://dx.doi.org/10.4049/jim- munol.0802948.
122. Studnicka-Benke A, Steiner G, Petera P, Smolen JS. Tumour necrosis factor α and its soluble receptors parallel clinical dis- ease and autoimmune activity in systemic lupus erythematosus. Br J Rheumatol. 1996;35(11):1067–74. DOI: http://dx.doi.org/10.1093/rheumatology/35.11.1067.
123. Zhu LJ, Landolt-Marticorena C, Li T, et al. Altered expression of TNF-α signaling pathway proteins in systemic lupus erythemato- sus. J Rheumatol. 2010;37(8):1658–66. DOI: http://dx.doi.org/10.3899/jrheum.091123.
124. Soforno E, Baumgartner M, Francis L, et al. Induction of sys- temic lupus erythematosus with tumor necrosis factor blockers. J Rheumatol. 2010;37(1):204–5. DOI: http://dx.doi.org/10.3899/jrheum.081312.
125. Aringer M, Graninger WB, Steiner G, Smolen JS. Safety and efficacy of tumor necrosis factor α blockade in systemic lupus erythematosus: an open-label study. Arthritis Rheum. 2004;50(10):3161–9. DOI: http://dx.doi.org/10.1002/art.20576.
126. Uppal SS, Hayat SJ, Raghupathy R. Efficacy and safety of inflix- imab in active SLE: a pilot study. Lupus. 2009;18(8):690–7. http://dx.doi.org/10.1177/0961203309102557.
127. Matsumura R, Umemiya K, Sugiyama T, et al. Anti-tumor necrosis factor therapy in patients with difficult-to-treat lupus nephritis: a prospective series of nine patients. Clin Exp Rheumatol. 2009;27(3):416–21.
128. Aringer M, Houssiau F, Gordon C, et al. Adverse events and effi- cacy of TNF-α blockade with infliximab in patients with sys- temic lupus erythematosus: long-term follow-up of 13 patients. Rheumatology (Oxford). 2009;48(11):1451–4. DOI: http://dx.doi.org/10.1093/rheumatology/kep270.
129. Runkel L, Stacey J. Lupus clinical development: will belimum- ab`s approval catalase a new paradigm for SLE drug develop- ment? Expert Opin Biol Ther. 2014;14(4):491–501. DOI: http://dx.doi.org/10.1517/14712598.2014.884065.
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Nasonov E.L., Solovyev S.K. PROSPECTS FOR PHARMACOTHERAPY OF SYSTEMIC LUPUS ERYTHEMATOSUS. Rheumatology Science and Practice. 2014;52(3):311-321. (In Russ.) https://doi.org/10.14412/1995-4484-2014-311-321
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