МНЕНИЕ

Анализ экспрессии ИФН-стимулированных генов как инструмент для оптимизации терапии системной красной волчанки

Т. О. Наконечная1, И. А. Шагина2,3, М. Ю. Мышкин2,3, З. Ю. Мутовина4, Е. В. Рязанцева4, Д. М. Чудаков1,2, М. А. Турчанинова2,3, О. В. Британова2,3
Информация об авторах

1 Институт биоорганической химии имени М. М. Шемякина и Ю. А. Овчинникова Российской академии наук, Москва, Россия

2 Российский национальный исследовательский медицинский университет имени Н. И. Пирогова, Москва, Россия

3 ООО МайЛаборатори, Москва, Россия

4 Отделение ревматологиии Городской клинической больницы № 52 Депертамента здравоохранения Москвы, Москва, Россия

Для корреспонденции: Ольга Владимировна Британова
ул. Миклухо-Маклая, д. 16/10, 117997, г. Москва, Россия; moc.liamg@natirblo

Информация о статье

Финансирование: исследование выполнено на средства гранта Правительства Москвы (НИР № 2412-63/22-1 НИР от 13.05.2022), спонсор — АНО «Московский центр инновационных технологий в здравоохранении».

Вклад авторов: М. Ю. Мышкин — анализ литературы; З. Ю. Мутовина, И. А. Шагина — сбор данных в сфере ревматологии и медицины; Д. М. Чудаков — концепция, М. А. Турчанинова — анализ и интерпретация данных; О. В. Британова, Т. О. Наконечная — анализ литературы и подготовка рукописи.

Статья получена: 24.06.2024 Статья принята к печати: 28.06.2024 Опубликовано online: 30.06.2024
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  1. Попкова Т. В, Панафидина Т. А., Герасимова Е. В., Лила А. М. Cистемная красная волчанка: диагностика, лечение, мониторинг для специалистов первичного звена: врачей-терапевтов, врачей общей практики. Методические рекомендации ФГБУ Научно-исследовательский институт ревматологии имени В. А. Насоновой. 2022.
  2. Tian J, Zhang D, Yao X, Huang Y, Lu, Q. Global epidemiology of systemic lupus erythematosus: a comprehensive systematic analysis and modelling study. Ann Rheum Dis. 2023; (82): 351–56.
  3. Izmirly PM, et al. Incidence rates of systemic lupus erythematosus in the USA: estimates from a meta-analysis of the Centers for Disease Control and Prevention national lupus registries. Lupus Sci Med. 2021; (8): e000614.
  4. Kaul A, Gordon C, Crow MK, et al. Systemic lupus erythematosus. Nat Rev Dis Primers. 2016; 2: 16039
  5. Kiriakidou M, Ching CL. Systemic Lupus Erythematosus. Ann Intern Med. 2020; (172): ITC81–ITC96.
  6. Fanouriakis A, Bertsias G. Changing paradigms in the treatment of systemic lupus erythematosus. Lupus Sci Med. 2019; (6): e000310.
  7. Durcan L, O’Dwyer T, Petri, M. Management strategies and future directions for systemic lupus erythematosus in adults. The Lancet. 2019; (393): 2332–43.
  8. Соловьев С. К., Асеева Е. А., Попкова Т. В., Лила А. М., Мазуров В. И., Насонов Е. Л. Системная красная волчанка: новые горизонты диагностики и терапии. Научно-практическая ревматология. 2020; 58 (1): 5–14.
  9. Jorge AM, Lu N, Zhang Y, Rai SK, Choi HK. Unchanging premature mortality trends in systemic lupus erythematosus: a general population-based study (1999–2014). Rheumatology. 2018; (57): 337–44.
  10. Gatto M, Zen M, Iaccarino L, Doria A. New therapeutic strategies in systemic lupus erythematosus management. Nat Rev Rheumatol. 2019; (15): 30–48.
  11. Dörner T, Furie R. Novel paradigms in systemic lupus erythematosus. The Lancet. 2019; (393): 2344–58.
  12. Nasonov EL, Avdeeva AS. Immunoinflammatory rheumatic diseases associated with type i interferon: new evidence. Rheumatology Science and Practice. 2019; (57): 452–61.
  13. Aringer M, et al. 2019 European League Against Rheumatism/ American College of Rheumatology classification criteria for systemic lupus erythematosus. Ann Rheum Dis. 2019; (78): 1151–9.
  14. Siegel CH, Sammaritano LR. Systemic Lupus Erythematosus. JAMA. 2024; (331): 1480.
  15. Yuan S, et al. Phenotypical changes and clinical significance of CD4+/CD8+ T cells in SLE. Lupus Sci Med. 2022; (9): e000660.
  16. Shan J, Jin H, Xu Y. T Cell Metabolism: A New Perspective on Th17/Treg Cell Imbalance in Systemic Lupus Erythematosus. Front Immunol. 2020; (11).
  17. Tsai Y-G, et al. Pathogenesis and novel therapeutics of regulatory T cell subsets and interleukin-2 therapy in systemic lupus erythematosus. Front Immunol. 2023; (14).
  18. Baechler EC, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proceedings of the National Academy of Sciences. 2003; (100): 2610–5.
  19. Kirou KA, et al. Coordinate overexpression of interferon-α– induced genes in systemic lupus erythematosus. Arthritis Rheum. 2004; (50): 3958–67.
  20. Londe AC, Fernandez-Ruiz R, Julio PR, Appenzeller S, Niewold TB. Type I Interferons in Autoimmunity: Implications in Clinical Phenotypes and Treatment Response. J Rheumatol. 2023; (50): 1103–13.
  21. Crow MK, Olferiev M, Kirou KA. Type I Interferons in Autoimmune Disease. Annual Review of Pathology: Mechanisms of Disease. 2019; (14): 369–93.
  22. Rönnblom L, Leonard D. Interferon pathway in SLE: one key to unlocking the mystery of the disease. Lupus Sci Med. 2019; (6): e000270.
  23. Fava A, et al. Integrated urine proteomics and renal single-cell genomics identify an IFN-γ response gradient in lupus nephritis. JCI Insight. 2020; (5)
  24. Viallard JF, et al. Th1 (IL-2, interferon-gamma (IFN-γ)) and Th2 (IL-10, IL-4) cytokine production by peripheral blood mononuclear cells (PBMC) from patients with systemic lupus erythematosus (SLE). Clin Exp Immunol. 2001; (115): 189–95.
  25. Yang B-C, Wang Y-S, Lin L-C, Liu M-F. Induction of Apoptosis and Cytokine Gene Expression in T‐ell Lines by Sera of Patients with Systemic Lupus Erythematosus. Scand J Immunol. 1997; (45): 96–102.
  26. Greene JA, DeVecchio JL, Gould MP, Auletta JJ, Heinzel FP. In vivo and In vitro Regulation of Type I IFN Synthesis by Synergistic Effects of CD40 and Type II IFN. The Journal of Immunology. 2006; (176): 5995–6003.
  27. Weihua X, Ling W, Kalvakolanu D. Regulation of interferonα/β-stimulated gene expression through the gamma-activated transcriptional element. Antiviral Res. 1990; (40): 145–53.
  28. Tan EM, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982; (25): 1271–7.
  29. Hochberg MC. Updating the American college of rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997; (40): 1725.
  30. Schoggins JW. Interferon-Stimulated Genes: What Do They All Do? Annu Rev Virol. 2019; (6): 567–84.
  31. Reizis B. Plasmacytoid Dendritic Cells: Development, Regulation, and Function. Immunity. 2019; (50): 37–50.
  32. Baccala R, et al. Essential requirement for IRF8 and SLC15A4 implicates plasmacytoid dendritic cells in the pathogenesis of lupus. Proceedings of the National Academy of Sciences. 2013; (110): 2940–5.
  33. Sisirak V, et al. Genetic evidence for the role of plasmacytoid dendritic cells in systemic lupus erythematosus. Journal of Experimental Medicine. 2014; (211): 1969–76.
  34. Crowl JT, Gray EE, Pestal K, Volkman HE, Stetson DB. Intracellular Nucleic Acid Detection in Autoimmunity. Annu Rev Immunol. 2017; (35): 313–36.
  35. Schlee M, Hartmann G. Discriminating self from non-self in nucleic acid sensing. Nat Rev Immunol. 2016; (16): 566–80.
  36. Kono DH, Baccala R, Theofilopoulos AN. TLRs and interferons: a central paradigm in autoimmunity. Curr Opin Immunol. 2013; (25): 720–27.
  37. Mathian A, et al. Ultrasensitive serum interferon-α quantification during SLE remission identifies patients at risk for relapse. Ann Rheum Dis. 2019; (78): 1669–76.
  38. Miyamoto, Takayuki et al. Assessment of type I interferon signatures in undifferentiated inflammatory diseases: A Japanese multicenter experience. Frontiers in immunology, 2022; (13): 905960.
  39. Kim H, et al. Development of a Validated Interferon Score Using NanoString Technology. Journal of Interferon & Cytokine Research. 2018; (38): 171–85.
  40. Суспицын Е. Н., Раупов Р. К., Кучинкская Е. М. & Костик М. М. Анализ профиля экспрессии интерферон-зависимых генов для дифференциальной диагностики заболеваний иммунной системы (обзор литературы). Клиническая Лабораторная Диагностика. 2021; 279–84.
  41. Raupov R, Suspitsin E, Preobrazhenskaya EV, Kostik M. Interferon type I signature associated with skin disease in juvenile dermatomyositis. Front Med (Lausanne). 2024; (11).
  42. Suspitsin EN, Raupov RK, Kuchinskaya EM, Kostik MM. Analysis of interferon type I signature for differential diagnosis of diseases of the immune system (review of literature). Russian Clinical Laboratory Diagnostics. 2021; (66): 279–84.
  43. Васин А. В., Плотникова М. А., Клотченко С. А., Гюлиханданова Н. Е., Ложков А. А., авторы; ФГАОУ ВО «СпбПУ», патентообладатель. Многопараметрическая диагностическая тест-система для количественного определения уровня мрнк генов rig-1, ifit-1, ifih-1 человека. Патент «RU 2782428».
  44. Banchereau R, et al. Personalized Immunomonitoring Uncovers Molecular Networks that Stratify Lupus Patients. Cell. 2016; (165): 551–65.
  45. Chiche L; et al. Modular Transcriptional Repertoire Analyses of Adults With Systemic Lupus Erythematosus Reveal Distinct Type I and Type II Interferon Signatures. Arthritis & Rheumatolog. 2014; (66): 1583–95.
  46. Petri M, et al. Association between changes in gene signatures expression and disease activity among patients with systemic lupus erythematosus. BMC Med Genomics. 2019; (12): 4.
  47. Weckerle CE, et al. Network analysis of associations between serum interferon-α activity, autoantibodies, and clinical features in systemic lupus erythematosus. Arthritis Rheum. 2011; (63): 1044–53.
  48. Feng X, et al. Association of increased interferon-inducible gene expression with disease activity and lupus nephritis in patients with systemic lupus erythematosus. Arthritis Rheum. 2006; (54): 2951–62.
  49. Wither J, et al. Presence of an interferon signature in individuals who are anti-nuclear antibody positive lacking a systemic autoimmune rheumatic disease diagnosis. Arthritis Res Ther. 2017; (19): 41.
  50. Hua J, Kirou K, Lee C, Crow MK. Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti–RNA binding protein autoantibodies. Arthritis Rheum. 2006; (54): 1906–16.
  51. Kennedy WP, et al. Association of the interferon signature metric with serological disease manifestations but not global activity scores in multiple cohorts of patients with SLE. Lupus Sci Med. 2015; (2): e000080–e000080.
  52. Bradford HF, 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): 100894.
  53. Bastard P, et al. Autoantibodies against type I IFNs in patients with life-threatening COVID-19. Science. 2020; (370).
  54. Sarkar MK, et al. Photosensitivity and type I IFN responses in cutaneous lupus are driven by epidermal-derived interferon kappa. Ann Rheum Dis. 2018; (77): 1653–64.
  55. Braunstein I, Klein R, Okawa J, Werth VP. The interferonregulated gene signature is elevated in subacute cutaneous lupus erythematosus and discoid lupus erythematosus and correlates with the cutaneous lupus area and severity index score. British Journal of Dermatology. 2012; (166): 971–5.
  56. Toukap AN, et al. Identification of distinct gene expression profiles in the synovium of patients with systemic lupus erythematosus. Arthritis Rheum. 2007; (56): 1579–88.
  57. Castellano G, et al. Local synthesis of interferon-alpha in lupus nephritis is associated with type I interferons signature and LMP7 induction in renal tubular epithelial cells. Arthritis Res Ther. 2015; (17): 72.
  58. Shiozawa S, Kuroki Y, Kim M, Hirohata S, Ogino T. Interferonalpha in lupus psychosis. Arthritis Rheum. 1992; (35): 417–22.
  59. Arnaud L, et al. Burden of systemic lupus erythematosus in clinical practice: baseline data from the SLE Prospective Observational Cohort Study (SPOCS) by interferon gene signature. Lupus Sci Med. 2023; (10): e001032.
  60. Paredes JL, Niewold TB. Type I interferon antagonists in clinical development for lupus. Expert Opin Investig Drugs. 2020; (29): 1025–41.
  61. Chaichian Y, Strand V. Interferon-directed therapies for the treatment of systemic lupus erythematosus: a critical update. Clin Rheumatol. 2021; (40): 3027–37.
  62. Goulden B, Isenberg D. Anti-IFNαR Mabs for the treatment of systemic lupus erythematosus. Expert Opin Biol Ther. 2021; (21): 519–28.
  63. Peng L, Oganesyan V, Wu H, Dall’Acqua WF, Damschroder MM. Molecular basis for antagonistic activity of anifrolumab, an antiinterferon–α receptor 1 antibody. Mabs. 2015; (7): 428–39.
  64. Riggs JM, 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): e000261.
  65. Насонов Е. Л., Попкова Т. В., Лила А. М. Белимумаб в лечении системной красной волчанки: 20 лет фундаментальных исследований, 10 лет клинической практики. Научнопрактическая ревматология. 2021; 59 (4): 367–83.
  66. Casey KA, et al. Type I interferon receptor blockade with anifrolumab corrects innate and adaptive immune perturbations of SLE. Lupus Sci Med. 2018; (5): e000286.
  67. Lub-de Hooge, M. N. Soluble TRAIL concentrations are raised in patients with systemic lupus erythematosus. Ann Rheum Dis. 2005; (64): 854–8.
  68. Tanaka A, et al. Serum progranulin levels are elevated in patients with systemic lupus erythematosus, reflecting disease activity. Arthritis Res Ther. 2012; (14): R244.
  69. Bauer JW, et al. Interferon-regulated chemokines as biomarkers of systemic lupus erythematosus disease activity: A validation study. Arthritis Rheum. 2009; (60): 3098–107.
  70. Sjöstrand M, et al. The Expression of BAFF Is Controlled by IRF Transcription Factors. The Journal of Immunology. 2016; (196): 91–96.
  71. Jacobi AM, et al. Effect of long-term belimumab treatment on b cells in systemic lupus erythematosus: Extension of a phase II, double-blind, placebo‐controlled, dose-ranging study. Arthritis Rheum. 2010; (62): 201–10.
  72. Furie RA, et al. Type I interferon inhibitor anifrolumab in active systemic lupus erythematosus (TULIP-1): a randomised, controlled, phase 3 trial. Lancet Rheumatol. 2019; (1): e208–e219.
  73. Loncharich MF, Robertson I. Anifrolumab in systemic lupus erythematosus. Drugs of Today. 2023; (59): 53–61.