Spotlight on anifrolumab and its potential for the treatment of moderate-to-severe systemic lupus erythematosus: evidence to date

References

• Felten R, Scher F, Sibilia J, Chasset F, Arnaud L. Advances in the treatment of systemic lupus erythematosus: from back to the future, to the future and beyond. Jt Bone Spine Rev Rhum. 2018. doi:10.1016/j.jbspin.2018.09.004
   PubMed Web of Science ®Google Scholar
• Felten R, Sagez F, Gavand P-E, et al. 10 most important contemporary challenges in the management of SLE. Lupus Sci Med. 2019;6(1):e000303. doi:10.1136/lupus-2018-00030330729019
   PubMed Web of Science ®Google Scholar
• Felten R, Dervovic E, Chasset F, et al. The 2018 pipeline of targeted therapies under clinical development for systemic lupus erythematosus: a systematic review of trials. Autoimmun Rev. 2018;17(8):781–790. doi:10.1016/j.autrev.2018.02.01129885544
   PubMed Web of Science ®Google Scholar
• Chasset F, Arnaud L. Targeting interferons and their pathways in systemic lupus erythematosus. Autoimmun Rev. 2018;17(1):44–52. doi:10.1016/j.autrev.2017.11.00929108825
   PubMed Web of Science ®Google Scholar
• Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci. 1957;147(927):258–267.13465720
   PubMed Web of Science ®Google Scholar
• Lauwerys BR, Ducreux J, Houssiau FA. Type I interferon blockade in systemic lupus erythematosus: where do we stand? Rheumatol Oxf Engl. 2014;53(8):1369–1376. doi:10.1093/rheumatology/ket403
   PubMed Web of Science ®Google Scholar
• Steinberg AD, Baron S, Talal N. The pathogenesis of autoimmunity in New Zealand mice, I. Induction of antinucleic acid antibodies by polyinosinic-polycytidylic acid. Proc Natl Acad Sci U S A. 1969;63(4):1102–1107.5307809
   PubMed Web of Science ®Google Scholar
• Hooks JJ, Moutsopoulos HM, Geis SA, Stahl NI, Decker JL, Notkins AL. Immune interferon in the circulation of patients with autoimmune disease. N Engl J Med. 1979;301(1):5–8. doi:10.1056/NEJM197907053010102449915
   PubMed Web of Science ®Google Scholar
• Rönnblom LE. Autoimmunity after alpha-interferon therapy for malignant carcinoid tumors. Ann Intern Med. 1991;115(3):178. doi:10.7326/0003-4819-115-3-1782058872
   PubMed Web of Science ®Google Scholar
• 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. 2003;100(5):2610–2615. doi:10.1073/pnas.033767910012604793
   PubMed Web of Science ®Google Scholar
• Bennett L, Palucka AK, Arce E, et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med. 2003;197(6):711–723. doi:10.1084/jem.2002155312642603
   PubMed Web of Science ®Google Scholar
• Relle M, Weinmann-Menke J, Scorletti E, Cavagna L, Schwarting A. Genetics and novel aspects of therapies in systemic lupus erythematosus. Autoimmun Rev. 2015;14(11):1005–1018. doi:10.1016/j.autrev.2015.07.00326164648
   PubMed Web of Science ®Google Scholar
• Lausch E, Janecke A, Bros M, et al. Genetic deficiency of tartrate-resistant acid phosphatase associated with skeletal dysplasia, cerebral calcifications and autoimmunity. Nat Genet. 2011;43(2):132–137. doi:10.1038/ng.74921217752
   PubMed Web of Science ®Google Scholar
• Crow YJ. Type I interferonopathies: a novel set of inborn errors of immunity. Ann N Y Acad Sci. 2011;1238(1):91–98. doi:10.1111/j.1749-6632.2011.06220.x22129056
   PubMed Web of Science ®Google Scholar
• Hoffman RW, Merrill JT, Alarcón-Riquelme MME, et al. Gene expression and pharmacodynamic changes in 1,760 systemic lupus erythematosus patients from two phase III trials of BAFF blockade with tabalumab. Arthritis Rheumatol Hoboken NJ. 2017;69(3):643–654. doi:10.1002/art.39950
   PubMed Web of Science ®Google Scholar
• Yao Y, Higgs BW, Morehouse C, et al. Development of potential pharmacodynamic and diagnostic markers for anti-IFN-α monoclonal antibody trials in systemic lupus erythematosus. Hum Genomics Proteomics. 2009;2009. doi:10.4061/2009/374312
   PubMedGoogle Scholar
• Banchereau R, Hong S, Cantarel B, et al. Personalized immunomonitoring uncovers molecular networks that stratify lupus patients. Cell. 2016;165(3):551–565. doi:10.1016/j.cell.2016.03.00827040498
   PubMed Web of Science ®Google Scholar
• Nikpour M, Dempsey AA, Urowitz MB, Gladman DD, Barnes DA. Association of a gene expression profile from whole blood with disease activity in systemic lupus erythaematosus. Ann Rheum Dis. 2008;67(8):1069–1075. doi:10.1136/ard.2007.07476518063674
   PubMed Web of Science ®Google Scholar
• Petri M, Singh S, Tesfasyone H, et al. Longitudinal expression of type I interferon responsive genes in systemic lupus erythematosus. Lupus. 2009;18(11):980–989. doi:10.1177/096120330910552919762399
   PubMed Web of Science ®Google Scholar
• Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol. 2014;14(1):36–49. doi:10.1038/nri358124362405
   PubMed Web of Science ®Google Scholar
• Wallace DJ, Furie RA, Tanaka Y, et al. Baricitinib for systemic lupus erythematosus: a double-blind, randomised, placebo-controlled, phase 2 trial. Lancet Lond Engl. 2018;392(10143):222–231. doi:10.1016/S0140-6736(18)31363-1
   PubMed Web of Science ®Google Scholar
• 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 Hoboken NJ. 2017;69(2):376–386. doi:10.1002/art.39962
   PubMed Web of Science ®Google Scholar
• Uzé G, Lutfalla G, Gresser I. Genetic transfer of a functional human interferon alpha receptor into mouse cells: cloning and expression of its cDNA. Cell. 1990;60(2):225–234.2153461
   PubMed Web of Science ®Google Scholar
• Novick D, Cohen B, Rubinstein M. The human interferon alpha/beta receptor: characterization and molecular cloning. Cell. 1994;77(3):391–400.8181059
   PubMed Web of Science ®Google Scholar
• Cohen B, Novick D, Barak S, Rubinstein M. Ligand-induced association of the type I interferon receptor components. Mol Cell Biol. 1995;15(8):4208–4214.7623815
   PubMed Web of Science ®Google Scholar
• Oganesyan V, Gao C, Shirinian L, Wu H, Dall’Acqua WF. Structural characterization of a human Fc fragment engineered for lack of effector functions. Acta Crystallogr D Biol Crystallogr. 2008;64(Pt 6):700–704. doi:10.1107/S090744490800787718560159
   PubMed Web of Science ®Google Scholar
• Peng L, Oganesyan V, Wu H, Dall’Acqua WF, Damschroder MM. Molecular basis for antagonistic activity of anifrolumab, an anti-interferon-α receptor 1 antibody. mAbs. 2015;7(2):428–439. doi:10.1080/19420862.2015.100781025606664
   PubMed Web of Science ®Google Scholar
• Lu J, Chuntharapai A, Beck J, et al. Structure-function study of the extracellular domain of the human IFN-alpha receptor (hIFNAR1) using blocking monoclonal antibodies: the role of domains 1 and 2. J Immunol Baltim Md 1950. 1998;160(4):1782–1788.
   Google Scholar
• Benoit P, Maguire D, Plavec I, Kocher H, Tovey M, Meyer F. A monoclonal antibody to recombinant human IFN-alpha receptor inhibits biologic activity of several species of human IFN-alpha, IFN-beta, and IFN-omega. Detection of heterogeneity of the cellular type I IFN receptor. J Immunol Baltim Md 1950. 1993;150(3):707–716.
   Google Scholar
• Riggs JM, Hanna RN, Rajan B, et al. Characterisation of anifrolumab, a fully human anti-interferon receptor antagonist antibody for the treatment of systemic lupus erythematosus. Lupus Sci Med. 2018;5(1):e000261. doi:10.1136/lupus-2018-00026129644082
   PubMed Web of Science ®Google Scholar
• Hall JC, Rosen A. Type I interferons: crucial participants in disease amplification in autoimmunity. Nat Rev Rheumatol. 2010;6(1):40–49. doi:10.1038/nrrheum.2009.23720046205
   PubMed Web of Science ®Google Scholar
• Liao AP, Salajegheh M, Morehouse C, et al. Human plasmacytoid dendritic cell accumulation amplifies their type 1 interferon production. Clin Immunol Orlando Fla. 2010;136(1):130–138. doi:10.1016/j.clim.2010.02.014
   PubMed Web of Science ®Google Scholar
• Brohawn P, Santiago L, Morehouse C, Higgs B, Illei G, Ranade K. Target modulation of a type I interferon gene signature and pharmacokinetics of anifrolumab in a phase IIb study of patients with moderate to severe systemic lupus erythematosus. ACR Meet Abstr. 2015 Available from: https://acrabstracts.org/abstract/target-modulation-of-a-type-i-interferon-gene-signature-and-pharmacokinetics-of-anifrolumab-in-a-phase-iib-study-of-patients-with-moderate-to-severe-systemic-lupus-erythematosus/. Accessed January 10, 2019.
   Google Scholar
• Tummala R, Rouse T, Berglind A, Santiago L. Safety, tolerability and pharmacokinetics of subcutaneous and intravenous anifrolumab in healthy volunteers. Lupus Sci Med. 2018;5(1):e000252. doi:10.1136/lupus-2017-00025229644080
   PubMed Web of Science ®Google Scholar
• Tanaka Y, Takeuchi T, Okada M, et al. Safety and tolerability of anifrolumab, a monoclonal antibody targeting type I interferon receptor, in Japanese patients with systemic lupus erythematosus: a multicenter, phase 2, open-label study. Mod Rheumatol. 2019;(ja):1–18. doi:10.1080/14397595.2019.1583833
   PubMed Web of Science ®Google Scholar
• Update on TULIP 1 phase III trial for anifrolumab in systemic lupus erythematosus. Available from: https://www.astrazeneca.com/media-centre/press-releases/2018/update-on-tulip-1-phase-iii-trial-for-anifrolumab-in-systemic-lupus-erythematosus-31082018.html. Accessed 110, 2019.
   Google Scholar
• Mahieu MA, Strand V, Simon LS, Lipsky PE, Ramsey-Goldman R. A critical review of clinical trials in systemic lupus erythematosus. Lupus. 2016;25(10):1122–1140. doi:10.1177/096120331665249227497257
   PubMed Web of Science ®Google Scholar
• 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)61354-221296403
   PubMed Web of Science ®Google Scholar
• Furie R, Petri M, Zamani O, 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):3918–3930. doi:10.1002/art.3061322127708
   PubMed Web of Science ®Google Scholar
• Touma Z, Gladman DD. Current and future therapies for SLE: obstacles and recommendations for the development of novel treatments. Lupus Sci Med. 2017;4(1):e000239. doi:10.1136/lupus-2017-00023929344386
   PubMed Web of Science ®Google Scholar
• Merrill JT, Wallace DJ, Petri M, et al. Safety profile and clinical activity of sifalimumab, a fully human anti-interferon α monoclonal antibody, in systemic lupus erythematosus: a phase I, multicentre, double-blind randomised study. Ann Rheum Dis. 2011;70(11):1905–1913. doi:10.1136/ard.2010.14448521798883
   PubMed Web of Science ®Google Scholar
• Ducreux J, Houssiau FA, Vandepapelière P, et al. Interferon α kinoid induces neutralizing anti-interferon α antibodies that decrease the expression of interferon-induced and B cell activation associated transcripts: analysis of extended follow-up data from the interferon α kinoid phase I/II study. Rheumatol Oxf Engl. 2016;55(10):1901–1905. doi:10.1093/rheumatology/kew262
   PubMedGoogle Scholar
• van Vollenhoven RF, Hahn BH, Tsokos GC, et al. Efficacy and safety of ustekinumab, an IL-12 and IL-23 inhibitor, in patients with active systemic lupus erythematosus: results of a multicentre, double-blind, phase 2, randomised, controlled study. Lancet Lond Engl. 2018;392(10155):1330–1339. doi:10.1016/S0140-6736(18)32167-6
   PubMed Web of Science ®Google Scholar
• Yao Y, Higgs BW, Richman L, White B, Jallal B. Use of type I interferon-inducible mRNAs as pharmacodynamic markers and potential diagnostic markers in trials with sifalimumab, an anti-IFNα antibody, in systemic lupus erythematosus. Arthritis Res Ther. 2010;12(Suppl 1):S6. doi:10.1186/ar288720392292
   PubMed Web of Science ®Google Scholar
• 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-2015-20856227009916
   PubMed Web of Science ®Google Scholar
• Merrill JT, Furie R, Werth VP, et al. Anifrolumab effects on rash and arthritis: impact of the type I interferon gene signature in the phase IIb MUSE study in patients with systemic lupus erythematosus. Lupus Sci Med. 2018;5(1):e000284. doi:10.1136/lupus-2018-00028430588322
   PubMed Web of Science ®Google Scholar
• Albrecht J, Taylor L, Berlin JA, et al. The CLASI (Cutaneous lupus erythematosus disease area and severity index): an outcome instrument for cutaneous lupus erythematosus. J Invest Dermatol. 2005;125(5):889–894. doi:10.1111/j.0022-202X.2005.23889.x16297185
   PubMed Web of Science ®Google Scholar