104
Views
0
CrossRef citations to date
0
Altmetric
Original Article

Double-filtration plasmapheresis reduces type I interferon bioavailability and inducing activity in systemic lupus erythematosus

, , , , , , , , ORCID Icon, & show all
Received 22 Apr 2024, Accepted 23 Jun 2024, Published online: 01 Jul 2024

References

  • Tsokos GC, Lo MS, Costa Reis P, et al. New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol. 2016;12(12):716–730. doi: 10.1038/nrrheum.2016.186.
  • Rönnblom L, Alm GV, Eloranta M-L. The type I interferon system in the development of lupus. Semin Immunol. 2011;23(2):113–121. doi: 10.1016/j.smim.2011.01.009.
  • Crow MK. Type I interferon in the pathogenesis of lupus. J Immunol. 2014;192(12):5459–5468. doi: 10.4049/jimmunol.1002795.
  • Crow MK, Olferiev M, Kirou KA. Targeting of type I interferon in systemic autoimmune diseases. Transl Res. 2015;165(2):296–305. doi: 10.1016/j.trsl.2014.10.005.
  • Crow MK. Pathogenesis of systemic lupus erythematosus: risks, mechanisms and therapeutic targets. Ann Rheum Dis. 2023;82(8):999–1014. [cited 2024 Jun 5]. Available from: https://ard.bmj.com/content/early/2023/02/14/ard-2022-223741
  • Tanaka Y, Kusuda M, Yamaguchi Y. Interferons and systemic lupus erythematosus: pathogenesis, clinical features, and treatments in interferon-driven disease. Mod Rheumatol. 2023;33(5):857–867. doi: 10.1093/mr/roac140.
  • Gallucci S, Meka S, Gamero AM. Abnormalities of the type I interferon signaling pathway in lupus autoimmunity. Cytokine. 2021;146:155633. doi: 10.1016/j.cyto.2021.155633.
  • Hooks JJ, Moutsopoulos HM, Geis SA, et al. Immune interferon in the circulation of patients with autoimmune disease. N Engl J Med. 1979;301(1):5–8. doi: 10.1056/NEJM197907053010102.
  • Ytterberg SR, Schnitzer TJ. Serum interferon levels in patients with systemic lupus erythematosus. Arthritis Rheum. 1982;25(4):401–406. doi: 10.1002/art.1780250407.
  • Preble OT, Black RJ, Friedman RM, et al. Systemic lupus erythematosus: presence in human serum of an unusual acid-labile leukocyte interferon. Science. 1982;216(4544):429–431. doi: 10.1126/science.6176024.
  • Kirou KA, Lee C, George S, et al. Activation of the interferon-alpha pathway identifies a subgroup of systemic lupus erythematosus patients with distinct serologic features and active disease. Arthritis Rheum. 2005;52(5):1491–1503. doi: 10.1002/art.21031.
  • Hua J, Kirou K, Lee C, et al. Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies. Arthritis Rheum. 2006;54(6):1906–1916. doi: 10.1002/art.21890.
  • Niewold TB, Adler JE, Glenn SB, et al. Age- and sex-related patterns of serum interferon-alpha activity in lupus families. Arthritis Rheum. 2008;58(7):2113–2119. doi: 10.1002/art.23619.
  • Mathian A, Weinberg A, Gallegos M, et al. IFN-alpha induces early lethal lupus in preautoimmune (New Zealand Black × New Zealand White) F1 but not in BALB/c mice. J Immunol. 2005;174(5):2499–2506. doi: 10.4049/jimmunol.174.5.2499.
  • Santiago-Raber M-L, Baccala R, Haraldsson KM, et al. Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice. J Exp Med. 2003;197(6):777–788. doi: 10.1084/jem.20021996.
  • Braun D, Geraldes P, Demengeot J. Type I Interferon controls the onset and severity of autoimmune manifestations in lpr mice. J Autoimmun. 2003;20(1):15–25. doi: 10.1016/s0896-8411(02)00109-9.
  • Kälkner KM, Rönnblom L, Karlsson Parra AK, et al. Antibodies against double-stranded DNA and development of polymyositis during treatment with interferon. Q J Med. 1998;91(6):393–399. doi: 10.1093/qjmed/91.6.393.
  • Ehrenstein MR, McSweeney E, Swane M, et al. Appearance of anti-DNA antibodies in patients treated with interferon-alpha. Arthritis Rheum. 1993;36(2):279–280. doi: 10.1002/art.1780360224.
  • Rönnblom LE, Alm GV, Oberg KE. Autoimmunity after alpha-interferon therapy for malignant carcinoid tumors. Ann Intern Med. 1991;115(3):178–183. doi: 10.7326/0003-4819-115-3-178.
  • Khamashta M, Merrill JT, Werth VP, et al. Sifalimumab, an anti-interferon-α monoclonal antibody, in moderate to severe systemic lupus erythematosus: a randomised, double-blind, placebo-controlled study. Ann Rheum Dis. 2016;75(11):1909–1916. doi: 10.1136/annrheumdis-2015-208562.
  • Furie R, Khamashta M, Merrill JT, et al. Anifrolumab, an anti-interferon-α receptor monoclonal antibody, in moderate-to-severe systemic lupus erythematosus. Arthritis Rheumatol. 2017;69:376–386. doi: 10.1002/art.39962.
  • Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140(6):805–820. doi: 10.1016/j.cell.2010.01.022.
  • Chen Q, Sun L, Chen ZJ. Regulation and function of the cGAS–STING pathway of cytosolic DNA sensing. Nat Immunol. 2016;17(10):1142–1149. doi: 10.1038/ni.3558.
  • Akira S, Takeda K. Toll-like receptor signalling. Nat Rev Immunol. 2004;4(7):499–511. doi: 10.1038/nri1391.
  • Ishikawa H, Barber GN. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature. 2008;455(7213):674–678. doi: 10.1038/nature07317.
  • Ablasser A, Goldeck M, Cavlar T, et al. cGAS produces a 2′-5′-linked cyclic dinucleotide second messenger that activates STING. Nature. 2013;498(7454):380–384. doi: 10.1038/nature12306.
  • Zhang X, Shi H, Wu J, et al. Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell. 2013;51(2):226–235. doi: 10.1016/j.molcel.2013.05.022.
  • Siegal FP, Kadowaki N, Shodell M, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science. 1999;284(5421):1835–1837. doi: 10.1126/science.284.5421.1835.
  • Cella M, Jarrossay D, Facchetti F, et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med. 1999;5(8):919–923. doi: 10.1038/11360.
  • Colonna M, Trinchieri G, Liu Y-J. Plasmacytoid dendritic cells in immunity. Nat Immunol. 2004;5(12):1219–1226. doi: 10.1038/ni1141.
  • Kwok S-K, Lee J-Y, Park S-H, et al. Dysfunctional interferon-alpha production by peripheral plasmacytoid dendritic cells upon Toll-like receptor-9 stimulation in patients with systemic lupus erythematosus. Arthritis Res Ther. 2008;10(2):R29. doi: 10.1186/ar2382.
  • Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11(5):373–384. doi: 10.1038/ni.1863.
  • Murayama G, Furusawa N, Chiba A, et al. Enhanced IFN-α production is associated with increased TLR7 retention in the lysosomes of palasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Res Ther. 2017;19(1):234. doi: 10.1186/s13075-017-1441-7.
  • Murayama G, Chiba A, Kuga T, et al. Inhibition of mTOR suppresses IFNα production and the STING pathway in monocytes from systemic lupus erythematosus patients. Rheumatology. 2020;59(10):2992–3002. doi: 10.1093/rheumatology/keaa060.
  • Gall A, Treuting P, Elkon KB, et al. Autoimmunity initiates in nonhematopoietic cells and progresses via lymphocytes in an interferon-dependent autoimmune disease. Immunity. 2012;36(1):120–131. doi: 10.1016/j.immuni.2011.11.018.
  • Ahn J, Gutman D, Saijo S, et al. STING manifests self DNA-dependent inflammatory disease. Proc Natl Acad Sci USA. 2012;109(47):19386–19391. doi: 10.1073/pnas.1215006109.
  • Liu Y, Jesus AA, Marrero B, et al. Activated STING in a vascular and pulmonary syndrome. N Engl J Med. 2014;371(6):507–518. doi: 10.1056/NEJMoa1312625.
  • Baum R, Sharma S, Carpenter S, et al. Cutting edge: AIM2 and endosomal TLRs differentially regulate arthritis and autoantibody production in DNase II-deficient mice. J Immunol. 2015;194(3):873–877. doi: 10.4049/jimmunol.1402573.
  • Hirano R, Namazuda K, Hirata N. Double filtration plasmapheresis: review of current clinical applications. Ther Apher Dial. 2021;25(2):145–151. doi: 10.1111/1744-9987.13548.
  • Mineshima M. Double filtration plasmapheresis: determination of the optimal albumin concentration in the supplementation fluid. Transfus Apher Sci. 2017;56(5):654–656. doi: 10.1016/j.transci.2017.08.009.
  • Connelly-Smith L, Alquist CR, Aqui NA, et al. Guidelines on the use of therapeutic apheresis in clinical practice – evidence-based approach from the Writing Committee of the American Society for Apheresis: the ninth special issue. J Clin Apher. 2023;38(2):77–278. doi: 10.1002/jca.22043.
  • Jones JV, Cumming RH, Bucknall RC, et al. Plasmapheresis in the management of acute systemic lupus erythematosus? Lancet. 1976;1(7962):709–711. doi: 10.1016/s0140-6736(76)93088-9.
  • Yamaji K, Kim Y-J, Tsuda H, et al. Long-term clinical outcomes of synchronized therapy with plasmapheresis and intravenous cyclophosphamide pulse therapy in the treatment of steroid-resistant lupus nephritis. Ther Apher Dial. 2008;12(4):298–305. doi: 10.1111/j.1744-9987.2008.00591.x.
  • Li M, Wang Y, Qiu Q, et al. Therapeutic effect of double-filtration plasmapheresis combined with methylprednisolone to treat diffuse proliferative lupus nephritis: therapeutic effect of DFPP in diffuse proliferative LN. J Clin Apher. 2016;31(4):375–380. doi: 10.1002/jca.21408.
  • Al-Adhoubi NK, Bystrom J. Systemic lupus erythematosus and diffuse alveolar hemorrhage, etiology and novel treatment strategies. Lupus. 2020;29(4):355–363. doi: 10.1177/0961203320903798.
  • Furuichi K, Wada T. Apheresis for kidney disease. Contrib Nephrol. 2018;196:188–193. doi: 10.1159/000485721.
  • Kronbichler A, Brezina B, Quintana LF, et al. Efficacy of plasma exchange and immunoadsorption in systemic lupus erythematosus and antiphospholipid syndrome: a systematic review. Autoimmun Rev. 2016;15(1):38–49. doi: 10.1016/j.autrev.2015.08.010.
  • Jones JV, Cumming RH, Bacon PA, et al. Evidence for a therapeutic effect of plasmapheresis in patients with systemic lupus erythematosus. Q J Med. 1979;48(192):555–576.
  • Krapf F, Manger B, Koch B, et al. The estimation of circulating immune complexes, C3d, and anti-ds-DNA-antibody serum levels in the monitoring of therapeutic plasmapheresis in a patient with systemic lupus erythematosus. A case report. Clin Exp Rheumatol. 1985;3:159–162.
  • Kato Y, Park J, Takamatsu H, et al. Apoptosis-derived membrane vesicles drive the cGAS–STING pathway and enhance type I IFN production in systemic lupus erythematosus. Ann Rheum Dis. 2018;77(10):1507–1515. doi: 10.1136/annrheumdis-2018-212988.
  • Tug S, Helmig S, Menke J, et al. Correlation between cell free DNA levels and medical evaluation of disease progression in systemic lupus erythematosus patients. Cell Immunol. 2014;292(1–2):32–39. doi: 10.1016/j.cellimm.2014.08.002.
  • Båve U, Magnusson M, Eloranta ML, et al. FcγRIIa is expressed on natural IFN-α-producing cells (plasmacytoid dendritic cells) and is required for the IFN-α production induced by apoptotic cells combined with lupus IgG 1. J Immunol. 2003;171(6):3296–3302. doi: 10.4049/jimmunol.171.6.3296.
  • Vallin H, Perers A, Alm GV, et al. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-α inducer in systemic lupus erythematosus. J Immunol. 1999;163(11):6306–6313. doi: 10.4049/jimmunol.163.11.6306.
  • Lood C, Blanco LP, Purmalek MM, et al. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat Med. 2016;22(2):146–153. doi: 10.1038/nm.4027.
  • Emlen W, Ansari R, Burdick G. DNA-anti-DNA immune complexes. Antibody protection of a discrete DNA fragment from DNase digestion in vitro. J Clin Invest. 1984;74(1):185–190. doi: 10.1172/JCI111400.
  • Hartl J, Serpas L, Wang Y, et al. Autoantibody-mediated impairment of DNASE1L3 activity in sporadic systemic lupus erythematosus. J Exp Med. 2021;218(5):e20201138. doi: 10.1084/jem.20201138.
  • Heil F, Hemmi H, Hochrein H, et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science. 2004;303(5663):1526–1529. doi: 10.1126/science.1093620.
  • Tanaka Y, Tago F, Yamakawa N, et al. A new therapeutic target for systemic lupus erythematosus: the current landscape for drug development of a toll-like receptor 7/8 antagonist through academia-industry-government collaboration. Immunol Med. 2024;47(1):24–29. doi: 10.1080/25785826.2023.2264023.
  • Idborg H, Oke V. Cytokines as biomarkers in systemic lupus erythematosus: value for diagnosis and drug therapy. Int J Mol Sci. 2021;22(21):11327. doi: 10.3390/ijms222111327.
  • Caielli S, Wan Z, Pascual V. Systemic lupus erythematosus pathogenesis: interferon and beyond. Annu Rev Immunol. 2023;41(1):533–560. doi: 10.1146/annurev-immunol-101921-042422.
  • Möckel T, Basta F, Weinmann-Menke J, et al. B cell activating factor (BAFF): structure, functions, autoimmunity and clinical implications in systemic lupus erythematosus (SLE). Autoimmun Rev. 2021;20(2):102736. doi: 10.1016/j.autrev.2020.102736.
  • Navarra SV, Guzmán RM, Gallacher AE, et al. 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.
  • Zhang F, Bae S-C, Bass D, et al. A pivotal phase III, randomised, placebo-controlled study of belimumab in patients with systemic lupus erythematosus located in China, Japan and South Korea. Ann Rheum Dis. 2018;77(3):355–363. doi: 10.1136/annrheumdis-2017-211631.
  • Oke V, Gunnarsson I, Dorschner J, et al. High levels of circulating interferons type I, type II and type III associate with distinct clinical features of active systemic lupus erythematosus. Arthritis Res Ther. 2019;21(1):107. doi: 10.1186/s13075-019-1878-y.
  • Gies V, Bekaddour N, Dieudonné Y, et al. Beyond anti-viral effects of chloroquine/hydroxychloroquine. Front Immunol. 2020;11:1409. doi: 10.3389/fimmu.2020.01409.
  • Fujio K. Functional genome analysis for immune cells provides clues for stratification of systemic lupus erythematosus. Biomolecules. 2023;13(4):591. doi: 10.3390/biom13040591.
  • Northcott M, Gearing LJ, Nim HT, et al. Glucocorticoid gene signatures in systemic lupus erythematosus and the effects of type I interferon: a cross-sectional and in-vitro study. Lancet Rheumatol. 2021;3(5):e357–e370. doi: 10.1016/S2665-9913(21)00006-0.
  • Northcott M, Jones S, Koelmeyer R, et al. Type 1 interferon status in systemic lupus erythematosus: a longitudinal analysis. Lupus Sci Med. 2022;9(1):e000625. doi: 10.1136/lupus-2021-000625.
  • Casey KA, Guo X, Smith MA, et al. Type I interferon receptor blockade with anifrolumab corrects innate and adaptive immune perturbations of SLE. Lupus Sci Med. 2018;5(1):e000286. doi: 10.1136/lupus-2018-000286.
  • Dall’era MC, Cardarelli PM, Preston BT, et al. Type I interferon correlates with serological and clinical manifestations of SLE. Ann Rheum Dis. 2005;64(12):1692–1697. doi: 10.1136/ard.2004.033753.
  • Lin SL, Aw E, Zhang Y, et al. Interferon-alpha plays an important role in glial-mediated symptoms of neuropsychiatric systemic lupus erythematosus. J Immunol. 2023;210(1_Supplement):63.19–63.19. doi: 10.4049/jimmunol.210.Supp.63.19.
  • Stull D, O’Quinn S, Williams B, et al. Causal cascade of direct and indirect effects of anifrolumab on patient-reported outcomes: structural equation modelling of two phase 3 trials. Rheumatology. 2022;61(12):4731–4740. doi: 10.1093/rheumatology/keac138.
  • Morand EF, Furie R, Tanaka Y, et al. Trial of anifrolumab in active systemic lupus erythematosus. N Engl J Med. 2020;382(3):211–221. doi: 10.1056/nejmoa1912196.
  • Vital EM, Merrill JT, Morand EF, et al. Anifrolumab efficacy and safety by type I interferon gene signature and clinical subgroups in patients with SLE: post hoc analysis of pooled data from two phase III trials. Ann Rheum Dis. 2022;81(7):951–961. doi: 10.1136/annrheumdis-2021-221425.
  • Bradford HF, Haljasmägi L, Menon M, et al. Inactive disease in patients with lupus is linked to autoantibodies to type I interferons that normalize blood IFNα and B cell subsets. Cell Rep Med. 2023;4(1):100894. doi: 10.1016/j.xcrm.2022.100894.
  • Tanaka Y. Viewpoint on anifrolumab in patients with systemic lupus erythematosus and a high unmet need in clinical practice. RMD Open. 2023;9(3):e003270. doi: 10.1136/rmdopen-2023-003270.