Neutrophils: importance in the systemic lupus erythematosus pathogenesis

封面

如何引用文章

全文:

开放存取 开放存取
受限制的访问 ##reader.subscriptionAccessGranted##
受限制的访问 订阅存取

详细

The review summarizes the modern scientific data concerning the neutrophils participation in the development of systemic lupus erythematosus (SLE) pathological processes. Acting as a link between innate and adaptive immunity, they play a fundamental role in the SLE immunopathogenesis. The review considers the phenotypic diversity and functions of these granulocytes. The features of changes in the qualitative and quantitative composition of their population in SLE are shown. The disease is characterized by impaired autophagy, phagocytosis, production of reactive oxygen species and neutrophil clearance. The process of formation of neutrophil extracellular traps (NETs) is of great importance. Тhe mathematical model aimed at studying its contribution to the process of SLE initiation is proposed. Changes in the functional properties of neutrophils, the NETs formation contribute to the development of thrombophilic conditions, endothelial dysfunction, damage to the vessels, kidneys, lungs, and skin. Therapeutic strategies that allow influencing the associated with the functioning of neutrophils processes have potential in terms of increasing the disease treatment effectiveness.

作者简介

E. Mozgovaya

Federal State Budgetary Institution “Research Institute of Clinical and Experimental Rheumatology named after A.B. Zborovsky”

编辑信件的主要联系方式.
Email: nauka@pebma.org
俄罗斯联邦, Volgograd, 400138

S. Bedina

Federal State Budgetary Institution “Research Institute of Clinical and Experimental Rheumatology named after A.B. Zborovsky”; Volgograd State Medical University

Email: nauka@pebma.org
俄罗斯联邦, Volgograd, 400138; Volgograd, 400131

A. Trofimenko

Federal State Budgetary Institution “Research Institute of Clinical and Experimental Rheumatology named after A.B. Zborovsky”

Email: nauka@pebma.org
俄罗斯联邦, Volgograd, 400138

S. Spitsina

Federal State Budgetary Institution “Research Institute of Clinical and Experimental Rheumatology named after A.B. Zborovsky”; Volgograd State Medical University

Email: nauka@pebma.org
俄罗斯联邦, Volgograd, 400138; Volgograd, 400131

M. Mamus

Federal State Budgetary Institution “Research Institute of Clinical and Experimental Rheumatology named after A.B. Zborovsky”

Email: nauka@pebma.org
俄罗斯联邦, Volgograd, 400138

I. Zborovskaya

Federal State Budgetary Institution “Research Institute of Clinical and Experimental Rheumatology named after A.B. Zborovsky”

Email: nauka@pebma.org
俄罗斯联邦, Volgograd, 400138

参考

  1. Беляева А.С., Ванько Л.В., Матвеева Н.К., Кречетова Л.В. Нейтрофильные гранулоциты как регуляторы иммунитета // Иммунология. 2016. Т. 37. № 2. С. 129–133. https://doi.org/10.18821/0206-4952-2016-37-2-129-133
  2. Богданов А.Н., Тыренко В.В., Щербак С.Г. Изменения системы крови при ревматических заболеваниях // Вестник Российской военно-медицинской академии. 2013. Т. 3. № 42. С. 173–179.
  3. Долгушин И.И. Нейтрофильные гранулоциты: новые лица старых знакомых // Бюллетень сибирской медицины. 2019. Т. 18. № 1. С. 30–37. https://doi.org/10.20538/1682-0363-2019-1-30–37
  4. Насонов Е.Л., Авдеева А.С., Решетняк Т.М., Алексанкин А.П., Рубцов Ю.П. Роль нетоза в патогенезе иммуновоспалительных ревматических заболеваний // Научно-практическая ревматология. 2023. Т. 61. № 5. С. 513–530. https://doi.org/10.47360/1995-4484-2023-513-530
  5. Насонов Е.Л., Решетняк Т.М., Соловьев С.К., Попкова Т.В. Системная красная волчанка и антифосфолипидный синдром: вчера, сегодня, завтра // Терапевтический архив. 2023. Т. 95. № 5. С. 365–374. https://doi.org/10.26442/00403660.2023.05.202246
  6. Решетняк Т.М., Нурбаева К.С., Пташник И.В. и др. Нетоз при волчаночном нефрите // Терапевтический архив. 2024. Т. 96. № 5. С. 453–458. https://doi.org/10.26442/00403660.2024.05.202699
  7. Смирнова Е.В., Краснова Т.Н., Проскурнина Е.В., Мухин Н.А. Роль дисфункции нейтрофилов в патогенезе системной красной волчанки // Терапевтический архив. 2017. Т. 89. № 12. C. 110–113. https://doi.org/10.17116/terarkh20178912110-113
  8. Смирнова Е.В., Проскурнина Е.В., Краснова Т.Н. Особенности функционального статуса нейтрофилов у больных волчаночным нефритом // Здоровье и образование в XXI в. 2017. Т. 19. № 12. http://dx.doi.org/10.26787/nydha-2226-7425-2017-19-12-277-280
  9. Тасибекова Г.Т., Калиев Э.А., Кожахметова А.Н. Особенности изменения гемотологических показателей крови при системной красной волчанке. Обзор литературы // Ғылым және Денсаулық сақтау. 2020. Т. 22. № 5. С. 57–67. https://doi.org/10.34689/SH.2020.22.5.005
  10. Федорова Е.В., Матвеева Н.К., Ванько Л.В. и др. Клинико-иммунологическая характеристика беременных женщин с системной красной волчанкой // Акушерство и гинекология. 2013. № 12. С. 46–51.
  11. Хаитов Р.М. Иммунология: структура и функции иммунной системы. ГЭОТАР-Медиа. М. 2019. 328 с.
  12. Accapezzato D., Caccavale R., Paroli M.P. et al. Advances in the Pathogenesis and Treatment of Systemic Lupus Erythematosus // Int. J. Mol. Sci. 2023. V. 24. № 7. P. 6578. https://doi.org/10.3390/ijms24076578
  13. Ambler W.G., Kaplan M.J. Vascular damage in systemic lupus erythematosus // Nat. Rev. Nephrol. 2024. V. 20. P. 251–265. https://doi.org/10.1038/s41581-023-00797-8
  14. Antiochos B., Trejo-Zambrano D., Fenaroli P. et al. The DNA sensors Aim2 and Ifi16 are SLE Autoantigens that bind neutrophil extracellular traps // Elife. 2022. V. 1. e72103. https://doi.org/10.7554/eLife.72103
  15. Apel F., Zychlinsky A., Kenny E.F. The role of neutrophil extracellular traps in rheumatic diseases // Nat. Rev. Rheumatol. 2018. V. 14. P. 467–475. https://doi.org/10.1038/s41584-018-0039-z.
  16. Banchereau R., Hong S., Cantarel B. et al. Personalized immunomonitoring uncovers molecular networks that stratify lupus patients // Cell. 2016. V. 165. № 3. P. 551–565. https://doi.org/10.1016/j.cell.2016.03.008
  17. Barrera-Vargas A., Gómez-Martín D., Carmona-Rivera C. et al. Differential ubiquitination in NETs regulates macrophage responses in systemic lupus erythematosus // Ann. Rheum. Dis. 2018. V. 77. № 6. P. 944–950. https://doi.org 10.1136/annrheumdis-2017-212617.
  18. Bashant K.R., Aponte A.M., Randazzo D. et al. Proteomic, biomechanical and functional analyses define neutrophil heterogeneity in systemic lupus erythematosus // Ann. Rheum. Dis. 2021. V. 80. № 2. P. 209–218. https://doi.org/ 10.1136/annrheumdis-2020-218338
  19. Blanco L.P., Wang X., Carlucci P.M. et al. RNA Externalized by Neutrophil Extracellular Traps Promotes Inflammatory Pathways in Endothelial Cells // Arthritis Rheumatol. 2021. V. 73. № 12. P. 2282–2292. https://doi.org/10.1002/art.41796
  20. Boeltz S., Amini P., Anders H.J. et al. To NET or not to NET: current opinions and state of the science regarding the formation of neutrophil extracellular traps // Cel.l Death. Differ. 2019. V. 26. P. 395–408. https://doi.org/10.1038/s41418-018-0261-x
  21. Brostjan C., Oehler R. The role of neutrophil death in chronic inflammation and cancer // Cell. Death. Discov. 2020. V. 6. № 26. https://doi.org/10.1038/s41420-020-0255-6
  22. Budu-Grajdeanu P., Schugart R.C., Friedman A. et al. Mathematical framework for human SLE nephritis: disease dynamics and urine biomarkers // Theor Biol. Med. Model. 2010. V. 7. P. 14. https://doi.org/10.1186/1742-4682-7-14
  23. Capsoni F., Sarzi-Puttini P., Zanella A. Primary and secondary autoimmune neutropenia // Arthritis. Res. Ther. 2005. V. 7. № 5. P. 208–214. https://doi.org/10.1186/ar1803
  24. Chang H.H., Dwivedi N., Nicholas A.P., Ho I.C. The W620 Polymorphism in PTPN22 Disrupts Its Interaction With Peptidylarginine Deiminase Type 4 and Enhances Citrullination and NETosis // Arthritis Rheumatol. 2015. V. 67. № 9. P. 2323–2334. https://doi.org/10.1002/art.39215
  25. Chen Y.M., Tang K.T., Liu H.J. et al. tRF-His-GTG-1 enhances NETs formation and interferon-α production in lupus by extracellular vesicle // Cell. Commun Signal. 2024. V. 22. № 1. P. 354. https://doi.org/10.1186/s12964-024-01730-7
  26. Dąbrowska D., Jabłońska E., Iwaniuk A., Garley M. Many Ways – One Destination: Different Types of Neutrophils Death // Int. Rev. Immunol. 2019. V. 38. № 1. P. 18–32. https://doi.org/10.1080/08830185.2018.1540616
  27. De Bont C.M., Boelens W.C., Pruijn G.J.M. NETosis, complement, and coagulation: A triangular relationship // Cell. Mol. Immunol. 2019. V. 16. P. 19–27. https://doi.org/10.1038/s41423-018-0024-0
  28. De Bont C., Pruijn G.J.M. Citrulline is not a major determinant of autoantibody reactivity to neutrophil extracellular traps // Philos. Trans. R Soc. Lond B Biol Sci. 2023. V. 378. № 1890. P. 20220249. https://doi.org/10.1098/rstb.2022.0249
  29. Delabio Auer E., Bumiller-Bini Hoch V., Borges da Silva E. et al. Association of neutrophil extracellular trap levels with Raynaud’s phenomenon, glomerulonephritis and disease index score in SLE patients from Brazil // Immunobiology. 2024. V. 229. № 3. P. 152803. https://doi.org/10.1016/j.imbio.2024.152803
  30. Dömer D., Walther T., Möller S. et al. Neutrophil extracellular traps activate proinflammatory functions of human neutrophils // Frontiers in Immunoogy. 2021. V. 12. P. 636954. https://doi.org/10.3389/fimmu.2021.636954.
  31. Euler M., Hoffmann M.H. The double-edged role of neutrophil extracellular traps in inflammation // Biochemical Society Transactions. 2019. V. 47. № 6. P. 1921–1930. https://doi.org/10.1042/BST20190629
  32. Fayyaz A., Igoe A., Kurien B.T. et al. Haematological manifestations of lupus // Lupus. Sci. Med. 2015. V. 3. № 2(1). e000078. https://doi.org/ 10.1136/lupus-2014-000078
  33. Foret T., Dufrost V., du Mont L.S. et al. A new pro-thrombotic mechanism of neutrophil extracellular traps in antiphospholipid syndrome: Impact on activated protein C resistance // Rheumatology. 2022. V. 61. P. 2993–2998. https://doi.org/10.1093/rheumatology/keab853
  34. Fousert E., Toes R., Desai J. Neutrophil extracellular traps (NETs) take the central stage in driving autoimmune responses // Cells. 2020. V. 9. P. 915. https://doi.org/10.3390/cells9040915
  35. Fresneda A.M., McLaren Z., Wright H.L. Neutrophils in the pathogenesis of rheumatoid arthritis and systemic lupus erythematosus: same foe different M.O. // Frontiers in Imunoogy. 2021. V. 12. P. 649693. https://doi.org/10.3389/fimmu.2021.649693
  36. Gao X., He J., Sun X., Li F. Dynamically modeling the effective range of IL-2 dosage in the treatment of systemic lupus erythematosus // iScience. 2022. V. 25. № 9. P. 104911. https://doi.org/10.1016/j.isci.2022.104911
  37. Garcia-Romo G.S., Caielli S., Vega B. et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus // Sci. Transl. Med. 2011. V. 3. № 73. 73ra20. https://doi.org/10.1126/scitranslmed.3001201
  38. Gestermann N., Di Domizio J., Lande R. et al. Netting neutrophils activate autoreactive B cells in lupus // J. Immunol. 2018. V. 200. № 10. P. 3364–3371. https://doi.org/10.4049/jimmunol.1700778
  39. Goel R.R., Nakabo S., Dizon B.L.P. et al. Lupus-like autoimmunity and increased interferon response in patients with STAT3-deficient hyper-IgE syndrome // J. Allergy Clin. Immunol. 2021. V. 147. P. 746–749. https://doi.org/10.1016/j.jaci.2020.07.024.
  40. Grecian R., Whyte M.K. B., Walmsley S.R. The role of neutrophils in cancer // Br. Med. Bull. 2018. V. 128. № 1. P. 5–14. https://doi.org/10.1093/bmb/ldy029
  41. Haidar Ahmad A., Melbouci D., Decker P. Polymorphonuclear neutrophils in rheumatoid arthritis and systemic lupus erythematosus: more complicated than anticipated // Immuno. 2022. V. 2. P. 85–103. https://doi.org/10.3390/immuno2010007
  42. Hao W., Rovin B.H., Friedman A. Mathematical model of renal interstitial fibrosis // Proc. Natl. Acad. Sci. USA. 2014. V. 111. № 39. P. 14193–14198. https://doi.org/10.1073/pnas.1413970111
  43. Henning S., Reimers T., Abdulahad W. et al. Low density granulocytes and neutrophil extracellular trap formation are increased in incomplete systemic lupus erythematosus // Rheumatology (Oxford), keae300. 2024. https://doi.org/10.1093/rheumatology/keae300.
  44. Herrero-Cervera A., Soehnlein O., Kenne E. Neutrophils in chronic inflammatory diseases // Cell. Mol. Immunol. 2022. V. 19. № 2. P. 177–191. https://doi.org/10.1038/s41423-021-00832-3
  45. Hom G., Graham R.R., Modrek B. et al. Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX // N. Engl. J. Med. 2008. V. 358. P. 900–909. https://doi.org/10.1056/NEJMoa0707865
  46. Huang J., Mao T., Zhang J. et al. Decreased DNase1L3 secretion and associated antibodies induce impaired degradation of NETs in patients with sporadic SLE // Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 2024. V. 40. № 1. P. 43–50.
  47. Jacob C.O., Eisenstein M., Dinauer M.C. et al. Lupus-associated causal mutation in neutrophil cytosolic factor 2 (NCF2) brings unique insights to the structure and function of NADPH oxidase // Proc. Natl. Acad. Sci. USA. 2012. V. 109. P. E59–E67. https://doi.org/ 10.1073/pnas.1113251108
  48. Java A., Apicelli A.J., Liszewski M.K. et al. The complement system in COVID-19: friend and foe? // JCI. Insight. 2020. V. 6. № 5(15). e140711. https://doi.org/10.1172/jci.insight.140711
  49. Java A., Kim A.H.J. The Role of Complement in Autoimmune Disease-Associated Thrombotic Microangiopathy and the Potential for Therapeutics // The Journal of Rheumatology. 2023. V. 50. № 6. P. 730–740. https://doi.org/10.3899/jrheum.220752
  50. Jog N.R., Wagner C.A., Aberle T. et al. Neutrophils isolated from systemic lupus erythematosus patients exhibit a distinct functional phenotype // Front Immunol. 2024. V. 15. 1339250. https://doi.org/ 10.3389/fimmu.2024.1339250
  51. Kahlenberg J.M., Carmona-Rivera C., Smith C.K., Kaplan M.J. Neutrophil extracellular trap-associated protein activation of the NLRP3 inflammasome is enhanced in lupus macrophages // J. Immunol. 2013. V. 190. P. 1217–1226. https://doi.org/10.4049/jimmunol.1202388
  52. Kubota T. An Emerging Role for Anti-DNA Antibodies in Systemic Lupus Erythematosus // Int J. Mol. Sci. 2023. V. 24. № 22. P. 16499. https://doi.org/10.3390/ijms242216499
  53. Lambers W.M., Westra J., Bootsma H., de Leeuw K. From incomplete to complete systemic lupus erythematosus: a review of the predictive serological immune markers // Semin. Arthritis. Rheum. 2021. V. 51. P. 43–48. https://doi.org/10.1016/j.semarthrit.2020.11.006
  54. Lande R., Ganguly D., Facchinetti V. et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus // Sci. Transl. Med. 2011. V. 3. 73ra19. https://doi.org/10.1126/scitranslmed.3001180
  55. Li D., Matta B., Song S. et al. IRF5 genetic risk variants drive myeloid-specific IRF5 hyperactivation and presymptomatic SLE // JCI Insight. 2020. V. 5. e124020. https://doi.org/10.1172/jci.insight.124020
  56. Li H.Y., Huang L.F., Huang X.R. et al. Endoplasmic Reticulum Stress in Systemic Lupus Erythematosus and Lupus Nephritis: Potential Therapeutic Target // J. Immunol. Res. 2023. P. 7625817. https://doi.org/10.1155/2023/7625817
  57. Li M., Weng L., Yu D. et al. Increased formation of neutrophil extracellular traps induced by autophagy and identification of autophagy-related biomarkers in systemic lupus erythematosus // Exp. Dermatol. 2024. V. 33. № 1. e14881. https://doi.org/10.1111/exd.14881
  58. Lin H., Liu J., Li N. et al. NETosis promotes chronic inflammation and fibrosis in systemic lupus erythematosus and COVID-19 // Clin. Immunol. 2023. V. 254. P. 109687. https://doi.org/10.1016/j.clim.2023.109687
  59. Liu Y., Kaplan M.J. Neutrophils in the Pathogenesis of Rheumatic Diseases: Fueling the Fire // Clin. Rev. Allergy. Immunol. 2021. V. 60. № 1. P. 1–16. https://doi.org/10.1007/s12016-020-08816-3
  60. Ma S., Jiang W., Zhang X., Liu W. Insights into the pathogenic role of neutrophils in systemic lupus erythematosus // Cur.r Opin. Rheumatol. 2023. V. 35. № 2. P. 82–88. https://doi.org/10.1097/ BOR.0000000000000912
  61. Manz M.G., Boettcher S. Emergency granulopoiesis // Nat. Rev. Immunol. 2014. V. 14. P. 302–314. https://doi.org/10.1038/nri3660
  62. Melbouci D., Ahmad A.H., Decker P. Neutrophil extracellular traps (NET): not only antimicrobial but also modulators of innate and adaptive immunities in inflammatory autoimmune diseases // RMD Open. 2023. V. 9. № 3. e003104. https://doi.org/10.1136/rmdopen-2023-003104
  63. Mistry P., Nakabo S., O’Neil L. et al. Transcriptomic, epigenetic, and functional analyses implicate neutrophil diversity in the pathogenesis of systemic lupus erythematosus // Proc. Natl. Acad. Sci. U S A. 2019. V. 116. № 50. P. 25222–25228. https://doi.org/ 10.1073/pnas.1908576116
  64. Moadab F., Sohrabi S., Wang X. et al. Subcellular location of L1 retrotransposon-encoded ORF1p, reverse transcription products, and DNA sensors in lupus granulocytes // Mob. DNA. 2024. V. 15. № 1. P. 14. https://doi.org/10.1186/s13100-024-00324-x
  65. Odqvist L., Jevnikar Z., Riise R. et al. Genetic variations in A20 DUB domain provide a genetic link to citrullination and neutrophil extracellular traps in systemic lupus erythematosus // Ann. Rheum. Dis. 2019. V. 78. P. 1363–1370. https://doi.org/10.1136/annrheumdis-2019-215434
  66. Ogawa H., Yokota S., Hosoi Y. et al. Methylprednisolone pulse-enhanced neutrophil extracellular trap formation in mice with imiquimod-induced lupus-like disease, resulting in ischaemia of the femoral head cartilage // Lupus. Sci. Med. 2023. V. 10. № 2. e001042. https://doi.org/10.1136/lupus-2023-00104
  67. Olsson L.M., Johansson A.C., Gullstrand B. et al. A single nucleotide polymorphism in the NCF1 gene leading to reduced oxidative burst is associated with systemic lupus erythematosus // Ann. Rheum. Dis. 2017. V. 76. P. 1607–1613. https://doi.org/10.1136/annrheumdis-2017-211287
  68. Palanichamy A., Bauer J.W., Yalavarthi S. et al. Neutrophil mediated IFN activation in the bone marrow alters B cell development in human and murine SLE // J. Immunol. 2014. V. 192. № 3. P. 906–918. https://doi.org/10.4049/jimmunol.1302112
  69. Patiño-Trives A.M., Pérez-Sánchez C., Pérez-Sánchez L. et al. Anti-dsDNA Antibodies Increase the Cardiovascular Risk in Systemic Lupus Erythematosus Promoting a Distinctive Immune and Vascular Activation // Arteriosclerosis, Thrombosis, and Vascular Biology. 2021. V. 41. № 9. P. 2417–2430. https://doi.org/10.1161/ATVBAHA.121.315928
  70. Pieterse E., Rother N., Yanginlar C. et al. Cleaved N-terminal histone tails distinguish between NADPH oxidase (NOX)-dependent and NOX-independent pathways of neutrophil extracellular trap formation // Ann Rheum Dis. 2018. V. 77. № 12. P. 1790–1798. https://doi.org/10.1136/annrheumdis-2018-213223
  71. Pillay J., den Braber I., Vrisekoop N. et al. In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days // Blood. 2010. V. 116. P. 625–627. https://doi.org/10.1182/blood-2010-01-259028
  72. Poli C., Augusto J.F., Dauvé J. et al. IL-26 confers proinflammatory properties to extracellular DNA // J Immunol. 2017. V. 198. № 9. P. 3650–3661.
  73. Psarras A., Wittmann M., Vital E.M. Emerging concepts of type I interferons in SLE pathogenesis and therapy // Nat. Rev. Rheumatol. 2022. V. 18. № 10. P. 575–590. https://doi.org/10.1038/s41584-022-00826-z
  74. Puga I., Cols M., Barra C.M. et al. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen // Nat. Immunol. 2012. V. 13. P. 170–80. https://doi.org/10.1038/ni.2194
  75. Rahman S., Sagar D., Hanna R.N. et al. Low-density granulocytes activate T cells and demonstrate a non-suppressive role in systemic lupus erythematosus // Ann. Rheum. Dis. 2019. V. 78. P. 957–966. https://doi.org/10.1136/annrheumdis-2018-214620
  76. Rosales C. Neutrophils at the crossroads of innate and adaptive immunity // J. Leukoc Biol. 2020. V. 108. № 1. P. 377–396. https://doi.org/10.1002/ JLB.4MIR0220-574RR
  77. Rysenga C.E., May-Zhang L., Zahavi M. et al. Taxifolin inhibits NETosis through activation of Nrf2 and provides protective effects in models of lupus and antiphospholipid syndrome // Rheumatology (Oxford). 2024. V. 63. № 7. P. 2006–2015. https://doi.org/10.1093/rheumatology/kead547
  78. Safi R., Al-Hage J., Abbas O. et al. Investigating the presence of neutrophil extracellular traps in cutaneous lesions of different subtypes of lupus erythematosus // Exp. Dermatol. 2019. V. 28. № 11. P. 1348–1352. https://doi.org/10.1111/exd.14040
  79. Santiworakul C., Saisorn W., Siripen N. et al. Interleukin-8 and neutrophil extracellular traps in children with lupus nephritis and vitamin C deficiency // Pediatr Nephrol. 2024. V. 39. № 4. P. 1135–1142. https://doi.org/10.1007/s00467-023-06189-1
  80. Smith C.K., Kaplan M.J. The role of neutrophils in the pathogenesis of systemic lupus erythematosus // Current Opinion in Rheumatology. 2015. V. 27. № 5. P. 448–453. https://doi.org/10.1097/BOR.0000000000000197
  81. Starkebaum G., Price T.H., Lee M.Y. et al. Autoimmune neutropenia in systemic lupus erythematosus // Arthritis Rheum. 1978. V. 21. P. 504–512. https://doi.org/10.1002/art.1780210503
  82. Stojkov D., Gigon L., Peng S. et al. Physiological and pathophysiological roles of metabolic pathways for NET formation and other neutrophil functions // Frontiers in Immunology. 2022. V. 13. P. 826515. https://doi.org/10.3389/fimmu.2022.826515.826515
  83. Sukhikh G.T., Safronova V.G., Vanko L.V. et al. Phagocyte activity in the peripheral blood of pregnant women with systemic lupus erythematosus and in the cord blood of their newborns // Int. J. Rheum Dis. 2017. V. 20. № 5. P. 597–608. https://doi.org/10.1111/1756-185X.13085
  84. Sule G., Abuaita B.H., Steffes P.A. et al. Endoplasmic reticulum stress sensor IRE1α propels neutrophil hyperactivity in lupus // The Journal of Clinical Investigation. 2021. V. 131. № 7. P. 2021. e137866. https://doi.org/10.1172/JCI137866
  85. Suvandjieva V., Tsacheva I., Santos M. et al. Modelling the Impact of NETosis During the Initial Stage of Systemic Lupus Erythematosus // Bull Math Biol. 2024. V. 86. № 6. P. 66. https://doi.org/10.1007/s11538-024-01291-3
  86. Szekanecz Z., McInnes I.B., Schett G. et al. Autoinflammation and autoimmunity across rheumatic and musculoskeletal diseases // Nat. Rev. Rheumatol. 2021. V. 17. № 10. P. 585–595. https://doi.org/10.1038/s41584-021-00652-9
  87. Thimmappa P.Y., Nair A.S., D’silva S. et al. Neutrophils display distinct post-translational modifications in response to varied pathological stimuli // International Immunopharmacology. 2024. V. 132. P. 111950. https://doi.org/10.1016/j.intimp.2024.111950
  88. Trofimenko A.S., Mozgovaya E.E., Bedina S.A., Spasov A.A. Ambiguities in neutrophil extracellular traps. Ongoing concepts and potential biomarkers for rheumatoid arthritis: A narrative review // Current Rheumatology Reviews. 2021. V. 17. № 3. P. 283–293. https://doi.org/10.2174/1573397116666201221113100
  89. Van Damme K.F.A., Hertens P., Martens A. et al. Protein citrullination and NET formation do not contribute to the pathology of A20/TNFAIP3 mutant mice // Sci Rep. 2023. V. 13. № 1. P. 17992. https://doi.org/10.1038/s41598-023-45324-8
  90. Van der Linden M., van den Hoogen L.L., Westerlaken G.H.A. et al. Neutrophil extracellular trap release is associated with antinuclear antibodies in systemic lupus erythematosus and anti-phospholipid syndrome // Rheumatology (Oxford). 2018. V. 57. № 7. P. 1228–1234. https://doi.org/10.1093/rheumatology/key067.
  91. Wang T., Rathee A., Pemberton P.A., Lood C. Exogenous serpin B1 restricts immune complex-mediated NET formation via inhibition of a chymotrypsin-like protease and enhances microbial phagocytosis // J. Biol. Chem. 2024. V. 300. № 8. P. 107533. https://doi.org/10.1016/j.jbc.2024.107533
  92. Wigerblad G., Cao Q., Brooks S. et al. Single-cell analysis reveals the range of transcriptional States of circulating human neutrophils // J. Immunol. 2022. V. 209. P. 772–782. https://doi.org/10.4049/jimmunol.2200154
  93. Wigerblad G., Kaplan M.J. Neutrophil extracellular traps in systemic autoimmune and autoinflammatory diseases // Nat. Rev. Immunol. 2023. V. 23. P. 274–288. https://doi.org/10.1038/s41577-022-00787-0
  94. Yamamoto T. Role of neutrophils in cutaneous lupus erythematosus // J. Dermatol. 2024. V. 51. № 2. P. 180—184. https://doi.org/10.1111/1346-8138.17036
  95. Yamasaki K., Niho Y., Yanase T. Granulopoiesis in systemic lupus erythematosus // Arthritis Rheum. 1983. V. 26. № 516–521. https://doi.org/10.1002/art.1780260410
  96. Yazdani A., Bahrami F., Pourgholaminejad A. et al. A biological and a mathematical model of SLE treated by mesenchymal stem cells covering all the stages of the disease // Theor Biosci. 2023. V. 142. № 2. P. 167–179 https://doi.org/10.1007/s12064-023-00390-4
  97. Zuo Y., Navaz S., Tsodikov A. et al. Anti-neutrophil extracellular trap antibodies in antiphospholipid antibody-positive patients: Results from the Antiphospholipid Syndrome Alliance for Clinical Trials and International Networking clinical database and repository // Arthritis Rheumatol. 2023. V. 75. P. 1407–1414. https://doi.org/10.1002/art.42489

补充文件

附件文件
动作
1. JATS XML

版权所有 © Russian Academy of Sciences, 2025