References

mimmun

Медицинская иммунология

Medical Immunology (Russia)

1563-06252313-741X

SPb RAACI

10.15789/1563-0625-AAN-2482

mimmun-2482

Research Article

ОБЗОРЫ

REVIEWS

Аутофагия, апоптоз, некроптоз, пироптоз и нетоз в патогенезе иммуновоспалительных ревматических заболеваний

Autophagy, apoptosis, necroptosis, pyroptosis and netosis in pathogenesis of immune-inflammatory rheumatic diseases

https://orcid.org/0000-0001-6246-4482

Саидов

М. З.

Saidov

M. Z.

Саидов Марат Зиявдинович – доктор медицинских наук, профессор, заведующий кафедрой патологической физиологии.

367000, Республика Дагестан, Махачкала, пл. Ленина, 1.

Тел.: 8 (988) 300-90-45

Marat Z. Saidov - PhD, MD (Medicine), Professor, Head, Department of Pathological Physiology.

367000, Republic of Dagestan, Makhachkala, Lenin Square, 1.

Phone: 7 (988) 300-90-45.

marat.saidov.55@mail.ru

Дагестанский государственный медицинский университетРоссияDagestan State Medical UniversityRussian Federation

2022

13072022

244659704

2022

Саидов М.З.

Saidov M.Z.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://www.mimmun.ru/mimmun/article/view/2482

При иммуновоспалительных ревматических заболеваниях организованными формами клеточного инфильтрата являются эктопические фолликулоподобные лимфоидные структуры и ГЗТ-гранулемы, неорганизованными формами — диффузный клеточный воспалительный инфильтрат. Неотъемлемым компонентом патогенетической динамики этих видов клеточного инфильтрата являются программируемые варианты гибели клеток, из которых наиболее значимыми являются аутофагия, апоптоз, некроптоз, пироптоз и нетоз. Существует тесная взаимосвязь между указанными формами клеточной гибели. Эта взаимосвязь сформировалась в процессе биологической эволюции, отличается выраженным консерватизмом и подчиняется общебиологическим закономерностям молекулярно-клеточных процессов в клетке. Высвобождающиеся в процессе гибели клеток «сигналы опасности» (DAMPs) индуцируют состояние аутореактивности, обусловленной в том числе модуляцией процессов гибели клеток с помощью PRR-рецепторов клеток врожденной иммунной системы. На основании анализа процесса эндоцитоза, сигнальных путей, адапторных молекул, транскрипционных факторов, свойственных каждой из указанных форм гибели клеток, представлена патогенетическая значимость изменений мембранных структур и молекулярных путей реализации программируемой клеточной гибели при иммуновоспалительных ревматических заболеваниях. В этом отношении фундаментальными являются мембран-ассоциированные клеточные процессы, формирование различных видов внутриклеточных инфламмасом, процессы кросс-презентации МНС-рестриктированных продуктов дезорганизации рыхлой волокнистой соединительной ткани и индукция аутореактивности врожденной и адаптивной иммунных систем. Причинно-следственные взаимоотношения молекулярных путей реализации указанных форм клеточной гибели позволяют идентифицировать целевые молекулярные мишени с целью модуляции продуктивного воспаления.

There are organized forms of cellular infiltrate observed in immune-inflammatory rheumatic diseases, i.e., ectopic follicle-like lymphoid structures and delayed-type response granulomas, whereas diffuse cellular inflammatory infiltrates represent non-organized forms. In these types of cellular infiltration, an integral pathogenetic link includes programmable cell death variants, with autophagy, apoptosis, necroptosis, pyroptosis and netosis being the most significant. There is a close relationship between these forms of cell death. This relationship occured in the process of biological evolution, being characterized by pronounced conservatism, and it follows general biological laws of molecular cellular processes. The “danger signals” (DAMPs) released during cell death induce a state of autoreactivity caused, e.g., by modulation of cell death processes using cellular PRR receptors of the innate immune system. When analyzing the processes of endocytosis, signaling pathways, adaptive molecules, transcription factors involved into these modes of cell death, we discuss pathogenetic role of changing membrane structures and molecular pathways of programmed cell death in immune-inflammatory rheumatic diseases. In this regard, there are fundamental membrane-associated cellular processes, genesis of various types of intracellular inflammasomes, cross-presentation of MHC-restricted products of disorganized loose fibrous connective tissue, and induction of innate and adaptive immune autoreactivity. Causal relationships of the molecular pathways for initiation of these forms of cell death, thus enabling identification of the molecular targets, in order to modulate productive inflammation.

воспалениеревматические болезниаутофагияапоптознекроптозпироптознетозаутореактивностьМНС I классаМНС II класса

inflammationrheumatic diseasesautophagyapoptosisMHC II class necroptosispyroptosisnetosisautoaggressionMHC I class

References1

Глебов Р.Н. Эндоцитоз и экзоцитоз. М.: Высшая школа, 1987, 91 с.

Glebov R.N. Endocytosis and exocytosis. Moscow: High School, 1987. 91 p.

Насонов Е.Л., Александрова Е.Н., Новиков А.А. Аутоиммунные ревматические заболевания - проблемы иммунопатологии и персонифицированной терапии // Вестник РАМН, 2015. Т. 70, № 2. С. 169-182.

Nasonov E.L., Alexandrova E.N., Novikov A.A. Autoimmune rheumatic diseases - problems of immunopathology and personalized treatment. Vestnik rossiiskoi akademii meditsinskikh nauk = Annals of the Russian Academy of Medical Sciences, 2015, Vol. 70, no. 2, pp. 169-182. (In Russ.)

Пинегин Б.В., Воробьева Н.В., Пащенков М.В., Черняк Б.В. Роль митохондриальных активных форм кислорода в активации врожденного иммунитета // Иммунология, 2018. Т. 39, № 4. С. 221-229.

Pinegin B.V., Vorobjeva N.V., Pashenkov M.V., Chernyak B.V. The role of mitochondrial reactive oxygen species in activation of innate immunity. Immunologiya = Immunologiya, 2018, Vol. 39, no. 4, pp. 221-229. (In Russ.)

Саидов М.З. Патогенетическое значение клеточного инфильтрата при иммуновоспалительных ревматических заболеваниях // Медицинская иммунология, 2021. Т. 23, № 6. С. 1239-1274. doi.:10.15789/1563-0625-PVO-2386.

Saidov M.Z. Pathogenetic value of cell infiltrate in immunoinflammatory rheumatic diseases. Meditsinskaya Immunologiya = Medical Immunology (Russia), 2021, Vol. 23, no. 6, pp. 1239-1274. (In Russ.) doi.:10.15789/1563-0625-PVO-2386.

Ярилин А.А., Никонова М.Ф., Ярилина А.А., Варфоломеева М.И., Григорьева Т.Ю. Апоптоз, роль в патологии и значимость его оценки при клинико-иммунологическом обследовании больных // Медицинская иммунология, 2000. Т. 2, № 1. С. 7-16.

Yarilin A.A., Nikonova M.F., Yarilina A.A., Varfolomeeva M.I., Grigorieva T.Yu. Apoptosis, imortance of its evaluation in immunopathological states. Meditsinskaya immunologiya = Medical Immunology (Russia), 2000, Vol. 2, no. 1, pp. 7-16. (In Russ.)

Abdulahad D.A., Westra J., Bijzet J., Limburg P.C., Wallenberg C.G., Bijl M. High mobility group box 1 (HMGB1) and anti-HMGB1 antibodies and their relation to disease characteristics in systemic lupus erythematosus. Arthritis Res. Ther., 2011, Vol. 13, no. 3, R71. doi:10.1186/ar3332.

Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., Sallusto F. Interleukins 1 в and 6 but not transforming growth factor-в are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol., 2007, Vol. 8, no. 9, pp. 942-949.

Agostini L., Martinon E, Burns K., McDermott M.F., Hawkins P.N., Tschopp J. NALP3 forms an IL-1 в-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity, 2004, Vol. 20, no. 3, pp. 319-325.

Aichinger M., Wu J., Nedjic L.K. Macroautophagy substrates are loaded onto MHC class II of medullary thymic epithelial cells for central tolerance. J. Exp. Med., 2013, Vol. 210, no. 2, pp. 287-300.

Albert M.I., Sauter B., Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class-restricted CTLs. Nature, 1998, Vol. 392, pp. 86-89.

Albert M.L., Pearce S.F., Francisco L.M., Sauter B., Roy P., Silverstein R.L., Bhardwaj N. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med., 1998, Vol. 188, no. 7, pp. 1359-1368.

Alessandri C., Barbati C., Vacirca D., Piscopo P., Confaloni A., Sanchez M., Maselli A., Colasanti T., Conti F., Truglia S., Perl A., Valesini G., Malorni W., Ortona E., Pierdominici M. T lymphocytes from patients with systemic lupus erythematosus are resistant to induction of autophagy. FASEB J., 2012, Vol. 26, no. 11, pp. 4722-4732.

An N., Chen Y., Wang C., Yang C., Wu Z., Xue J., Ye L., Wang S., Liu H., Pan Q. Chloroquine autophagic inhibition rebalances Th17/Treg-mediated immunity and ameliorates systemic lupus erythematosus. Cell. Physiol. Biochem., 2017, Vol. 44, no. 1, pp. 412-422.

Apel F., Zychlinsky A., Kenny E.F. The role of neutrophil extracellular traps in rheumatic diseases. Nat. Rev. Rheumatol., 2018, Vol. 14, no. 8, pp. 467-475.

Baier A., Meineckel I., Gay S., Pap T. Apoptosis in rheumatoid arthritis. Curr. Opin. Rheumat., 2003, Vol. 15, no. 3, pp. 274-279.

Banchereau R., Cepika A.M., Banchereau J., Pascual V. Understanding human autoimmunity and autoinflammation through transcriptomics. Annu. Rev. Immunol., 2017, Vol. 35, pp. 337-370.

Baumann I., Kolowos W., Voll R.E., Manger B., Gaipl U., Neuhuber W., Kirchner T., Kalden J., Herrmann M. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum., 2002, Vol. 46, no. 1, pp. 191-201.

Beckley K.D., Wen H., Ting J.P. The Inflammasome NLRs in Immunity, Inflammation, and Associated Diseases. Annu. Rev. Immunol., 2011, Vol. 29, pp. 707-735.

Bengtsson A.A., Gullstrand B., Truedsson L., Sturfelt G. SLE serum induces classical caspase-dependent apoptosis independent of death receptors. Clin. Immunol., 2008, Vol. 126, no. 1, pp. 57-66.

Bennett L., Palucka A.K., Arce E., Cantrell V., Borvak J., Banchereau J., Pascual V. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med., 2003, Vol. 197, no. 6, pp. 711-723.

Berghe T.V., Vanlangenakker N., Parthoens E., Deckers W., Devos M., Festjens N., Guerin C.J., Brunk U.T., Declercq W., Vandenabeele P. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ., 2010, Vol. 17, no. 6, pp. 922-930.

Berghe T.V., Linkermann A., Jouan-Lanhouet S., Walczak H., Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol., 2014, Vol. 15, pp. 135-147.

Berthelot J.-M., Le Goff B., Neel A., Maugars Y., Hamidou M. NETosis: At the crossroads of rheumatoid arthritis, lupus, and vasculitis. Joint Bone Spine, 2017, Vol. 84, no. 3, pp. 255-262.

Bonnani A., Vaglio A., Bruschi M., Sinico R., Cavagna L., Moroni G., Franceschini F., Allegri L., Pratesi F., Migliorini P., Candiano G., Pesce G., Ravelli A., Puppo F., Martini A., Tincan A., Ghiggeri G. Multi-antibody composition in lupus nephritis: isotype and antigen specificity make the difference. Autoimmun. Rev., 2015, Vol. 14, no. 8, pp. 692-702.

Bortoluci K.R., Medzhitov R. Control of infection by pyroptosis and autophagy: role of TLR and NLR. Cell. Mol. Life Sci., 2010, Vol. 67, no. 10, pp. 1643-1651.

Brennan M.A., Cookson B.T. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol. Microbiol., 2000, Vol. 38, no. 1, pp. 31-40.

Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science, 2004, Vol. 303, pp. 1532-1535.

Broderick L., De Nardo D., Franklin B.S., Hoffman H.M., Latz E. The inflammasomes and autoinflammatory syndromes. Annu. Rev. Pathol., 2015, Vol. 10, pp. 395-424.

Cai P., Lu Z., Jiang T., Wang Z., Yang Y., Zheng L., Zhao J. Syndecan-4 involves in the pathogenesis of rheumatoid arthritis by regulating the inflammatory response and apoptosis of fibroblast-like synoviocytes. J. Cell. Physiol., 2020, Vol. 235, no. 2, pp. 1746-1758.

Caproni M., Torchia D., Cardinali C., Volpi W., Del B. E., D'Agata A., Fabbri P. Infiltrating cells, related cytokines and chemokine receptors in lesional skin of patients with dermatomyositis. Br. J. Dermatol., 2004, Vol. 151, no. 4, pp. 784-791.

Carlson J.A., Chen K.R. Cutaneous vasculitis update: small vessel neutrophilic vasculitis syndromes. Am. J. Dermatopathol., 2006, Vol. 28, no. 6, pp. 486-506.

Carmona-Rivera C., Kaplan M.J. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin. Immunopathol. 2013, Vol. 35, no. 4, pp. 455-463.

Carmona-Rivera C., Zhao W., Yalavarthi S., Kaplan M.J. Neutrophil extracellular traps induce endothelial dysfunction in systemic lupus erythematosus through the activation of matrix metalloproteinase-2. Ann. Rheum. Dis., 2015, Vol. 74, no. 7, pp. 1417-1424.

Chadha S., Behl T., Bungau S., Kumar A., Arora R., Gupta A., Uddin V., Zengin G., Aleya L., Setia D., Arora S. Mechanistic insights into the role of pyroptosis in rheumatoid arthritis. Curr. Res. Transl. Med., 2020, Vol. 68, no. 4, pp. 151-158.

Chen G.Y., Chen X., King S., Cavassani K.A., Cheng J., Zheng X., Cao H., Yu H., Qu J., Fang D., Wu W., Bai X., Lui J., Woodiga S., Chen C., Sun L., Hogaboam C., Kunkel S., Zheng P., Lui Y. Amelioration of sepsis by inhibiting sialidase-mediated disruption of the CD24-SiglecG interaction. Nat. Biotechnol., 2011, Vol. 29, no. 5, pp. 428-435.

Chen G.Y., Nunez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol., 2010, Vol. 10, no. 12, pp. 826-837.

Cho Y.S., Challa S., Moquin D., Genga R., Ray T., Guidford M., Chan F. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell, 2009, Vol. 137, no. 6, pp. 1112-1123.

Christofferson D.E., Li Y., Hitomi J., Zhou W., Upperman C., Zhu H., Gerber S.A., Gygi S., Yuan J. A novel role for RIP1 kinase in mediating TNFa production. Cell Death Dis., 2012, Vol. 3, no. 6, e320. doi:10.1038/cddis.2012.64.

Church L.D., Cook G.P., McDermott M.F. Primer: inflammasomes and interleukin 1p in inflammatory disorders. Nat. Clin. Pract. Rheumatol., 2008, Vol. 4, no. 1, pp. 34-42.

Colonna L., Lood C., Elkon K. B. Beyond apoptosis in lupus. Curr. Opin. Rheumatol., 2014, Vol. 26, no. 5, pp. 459-466.

Cookson B.T., Brennan M.A. Pro-inflammatory programmed cell death. Trends Microbiol., 2001, Vol. 9, no. 3, pp. 113-114.

Darrah E., Andrade F. NETs: the missing link between cell death and systemic autoimmune diseases? Front. Immunol., 2013, Vol. 3, 428. doi:10.3389/fimmu.2012.00428.

Degterev A., Hitomi J., Germscheid M., Chen I., Korkina O., Teng X., Abbott D., Cuny G., Yuan C., Wagner G., Hedrick S., Gerber S., Lugovskoy A., Yuan J. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol., 2008, Vol. 4, no. 5, pp. 313-321.

Degterev A., Huang Z., Boyce M., Li Y., Jagtap P., Mizushima N., Cuny G.D., Mitchison T.J., Moskowitz M.A., Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol., 2005, Vol. 1, no. 2, pp. 112-119.

Denny M.F., Chandaroy P., Killen P., Caricchio R., Lewis E., Richardson B., Lee K., Gavalchin J., Kaplan M. Accelerated macrophage apoptosis induces autoantibody formation and organ damage in systemic lupus erythematosus. J. Immunol., 2006, Vol. 176, no. 4, pp. 2095-2104.

Deretic V. Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol. Rev., 2011, Vol. 240, no. 1, pp. 92-104.

Deter R.L., de Duve C. Influence of glucagon, an inducer of cellular autophagy, on some physical properties of rat liver lysosomes. J. Cell Biol., 1967, Vol. 33, no. 2, pp. 437-449.

Díaz-Godínez C., Carrero J.C. The state of art of neutrophil extracellular traps in protozoan and helminthic infections. Biosci. Re., 2019, Vol. 39, no. 1, BSR20180916. doi:10.1042/bsr20180916.

Doitsh G., Galloway N.L.K., Geng X., Yang Z., Monroe K.M., Zepeda O., Hunt P., Hatano H., Sowinski S., Munoz-Arias I., Greene W.C. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature, 2014, Vol. 505, no. 7484, pp. 509-514.

Dondelinger Y., Aguileta M.A., Goossens V., Dubuisson C., Grootjans S., Dejardin E., Vandenabeele P., Bertrand M. RIPK3 contributes to TNFR1-mediated RIPK1 kinase- dependent apoptosis in conditions of cIAP1/2 depletion or TAK1 kinase inhibition. Cell Death Differ., 2013, Vol. 20, no. 10, pp. 1381-1392.

Doster R.S., Rogers L.M., Gaddy J.A., Aronoff D.M. Macrophage Extracellular Traps: A Scoping Review. J. Innate Immun., 2017, Vol. 10, no. 1, pp. 3-13.

Duvvuri B., Pachman L.M., Morgan G., Khojah A.M., Klein-Gitelman M., Curran M.L., Doty S., Lood C. Neutrophil extracellular traps in tissue and periphery in juvenile dermatomyositis. Arthritis Rheumatol., 2020, Vol. 72, no. 2, pp. 348-358.

Dwivedi N., Radic M. Citrullination of autoantigens implicates NETosis in the induction of autoimmunity. Annals Rheum. Dis., 2013, Vol. 73, no. 3, pp. 483-491.

Eigenbrod T., Park J.H., Harder J., Iwakura Y., Nunez G. Cutting edge: critical role for mesothelial cells in necrosis-induced inflammation through the recognition of IL-1 alpha released from dying cells. J. Immunol., 2008, Vol. 181, pp. 8194-8198.

Erwig L.P., Henson P.M. Immunological consequences of apoptotic cell phagocytosis. Am. J. Pathol., 2007, Vol. 171, no. 1, pp. 2-8.

Fan F.H., Dong L.G., Ren D., Xu Y., Dou J., Wang T., Sun L., Hou Y. Activation-induced necroptosis contributes to B-cell lymphopenia in active systemic lupus erythematosus. Cell Death Dis., 2014, Vol. 5, no. 9, e1416. doi: 10.1038/cddis.2014.375.

Fink S.L., Cookson B.T. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol., 2006, Vol. 8, no. 11, pp. 1812-1825.

Fitzpatrick A.M., Holguin F., Teague W.G., Brown L.A. Alveolar macrophage phagocytosis is impaired in children with poorly controlled asthma. J. Allergy Clin. Immunol., 2008, Vol. 121, no. 6, pp. 1372-1378.

Fu R., Guo C., Wang S., Huang Y., Jin O., Haoqiang H., Chen J., Xu B., Zhou M., Zhao J., Sung S., Wang H., Gaskin F., Yang N., Fu S. Podocyte activation of NLRP3 inflammasomes contributes to the development of proteinuria in lupus nephritis. Arthritis Rhematol., 2017, Vol. 69, no. 8, pp. 1636-1646.

Galluzzi L., Kepp O., Chan F.K.-M., Kroemer G. Necroptosis: Mechanisms and Relevance to Disease. Annu. Rev. Pathol., 2017, Vol. 12, no. 1, pp. 103-130.

Galluzzi L., Vitale I., Abrams J.M., Alnemri E.S., Baehrecke E.H., Blagosklonny M.V., Dawson T.M., Dawson V.L., El-Deiry W.S., Fulda S., Gottlieb E., Green D.R., Hengartner M.O., Kepp O., Knight R.A., Kumar S., Lipton S.A., Lu X., Madeo F., Malorni W, Mehlen P, Nunez G., Peter M.E., Piacentini M., Rubinsztein D.C., Shi Y., Simon H.-U., Vandenabeele P., White E., Yuan J., Zhivotovsky B., Melino G., Kroemer G. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ., 2012, Vol. 19, no. 1, pp. 107-120.

Galluzzi L., Vitale I., Aaronson S.A., Abrams J.M., Adam D., Agostinis P., Alnemri E.S., Altucci L., Amelio I., Andrews D.W., Annicchiarico-Petruzzelli M., Antonov A.V., Arama E., Baehrecke E.H., BarlevN.A., Bazan N.G., Bernassola F., Bertrand M.J.M., Bianchi K., Blagosklonny M.V., Blomgren K., Borner C., Boya P., Brenner C., Campanella M., Candi E., Carmona-Gutierrez D., Cecconi F., Chan F.K.-M., Chandel N.S., ChengE.H., Chipuk J.E., Cidlowski J.A., Ciechanover A., Cohen G.M., Conrad M., Cubillos-Ruiz J.R., Czabotar P.E., D'Angiolella V., Dawson T.M., Dawson V.L., de Laurenzi V., de Maria R., Debatin K.-M., DeBerardinis R.J., Deshmukh M., di Daniele N., di Virgilio F., Dixit V.M., Dixon S.J., Duckett C.S., Dynlacht B.D., El-Deiry W.S., Elrod J.W., Fimia G.M., Fulda S., Garda-Saez A.J., Garg A.D., Garrido C., Gavathiotis E., Golstein P, Gottlieb E., Green D.R., Greene L.A., Gronemeyer H., Gross A., Hajnoczky G., Hardwick J.M., Harris I.S., Hengartner M.O., Hetz C., Ichijo H., Jaattela M., Joseph B., Jost PJ., Juin P.P., Kaiser W.J., Karin M., Kaufmann T., Kepp O., Kimchi A., KitsisR.N., Klionsky D.J., KnightR.A., Kumar S., Lee S.W., Lemasters J.J., Levine B., Linkermann A., Lipton S.A., Lockshin R.A., Lopez-Otm C., Lowe S.W., Luedde T., Lugli E., MacFarlane M., Madeo F., Malewicz M., Malorni W., Manic G., Marine J.-C., Martin S.J., Martinou J.-C., Medema J.P., Mehlen P., Meier P., Melino S., Miao E.A., Molkentin J.D., Moll U.M., Munoz-Pinedo C., Nagata S., Nunez G., Oberst A., Oren M., Overholtzer M., Pagano M., Panaretakis T., Pasparakis M., Penninger J.M., Pereira D.M., Pervaiz S., Peter M.E., Piacentini M., Pinton P., Prehn J.H.M., Puthalakath H., Rabinovich G.A., Rehm M., Rizzuto R., Rodrigues C.M.P., Rubinsztein D.C., Rudel T., Ryan K.M., Sayan E., Scorrano L., Shao F., Shi Y., Silke J., Simon H.-U., Sistigu A., Stockwell B.R., Strasser A., Szabadkai G., Tait S.W.G., Tang D., Tavernarakis N., Thorburn A., Tsujimoto Y., Turk B., Berghe T.V., Vandenabeele P., Heiden M.G.V., Villunger A., Virgin H.W., Vousden K.H., Vucic D., Wagner E.F., Walczak H., Wallach D., Wang Y., Wells J.A., Wood W., Yuan J., Zakeri Z., Zhivotovsky B., Zitvogel L., Melino G., Kroemer G. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ., 2018, Vol. 25, no. 3, pp. 486-541.

Gershov D., Kim S., Brot N., Elkon K.B. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med., 2000, Vol. 192, no. 9, pp. 1353-1364.

Granger V., Peyneau M., Chollet-Martin S., de Chaisemartin L. Neutrophil extracellular traps in autoimmunity and allergy: immune complexes at work. Front. Immunol., 2019, Vol. 10, no. 2824. doi: 10.3389/fimmu.2019.02824.

Gupta A.K., Giaglis S., Hasler P., Hahn S. Efficient neutrophil extracellular trap induction requires mobilization of both intracellular and extracellular calcium pools and is modulated by cyclosporine A. PLoS One, 2014, Vol. 9, no. 5, e97088. doi: 10.1371/journal.pone.0097088.

Gupta A.K., Joshi M.B., Philippova M., Erne P., Hasler P., Hahn S., Resink T.J. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett., 2010, Vol. 584, pp. 3193-3197.

Gutierrez K.D., Davis M.F., Daniels B.P., Olsen T.M., Ralli-Jain P., Tait S., Jr M., Oberst A. MLKL activation triggers NLRP3-mediated processing and release of IL-1 в independently of gasdermin-D. J. Immunol., 2017, Vol. 198, no. 5, pp. 2156-2164.

Harle G., Kowalski C., Dubrot J., Brighouse D., Clavel G., Pick R., Bessis N., Niven J., Scheiermann C., Gannage M., Hugues S. Macroautophagy in lymphatic endothelial cells inhibits T cell-mediated autoimmunity J. Exp. Med., 2021, Vol. 218, no. 6, e20201776. doi: 10.1084/jem.20201776.

He M.X., McLeod I.X., Jia W., He Y.W. Macroautophagy in T lymphocyte development and function. Front. Immunol., 2012, Vol. 3, 22. doi: 10.3389/fimmu.2012.00022.

Hodge S., Hodge G., Scicchitano R., Reynolds P.N., Holmes M. Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol. Cell Biol., 2003, Vol. 81, no. 4, pp. 289-296.

Hoffman H.M., Wanderer A. A. Inflammasome and IL-1 в-mediated disorders. Curr. Allergy Asthma Rep., 2010, Vol. 10, no. 4, pp. 229-235.

Honarpisheh M., Desai J., Marschner J. A., Weidenbusch M., Lech M., Vielhauer V., Hans-Joachim Anders, Mulay S. R. Regulated necrosis-related molecule mRNA expression in humans and mice and in murine acute tissue injury and systemic autoimmunity leading to progressive organ damage, and progressive fibrosis. Biosci. Rep., 2016, Vol. 36, no. 6, e00425. doi:10.1042/bsr20160336.

Jafari-Nakhjavani M.R., Abedi-Azar S., Nejati B. Correlation of plasma interleukin-18 concentration and severity of renal involvement and disease activity in systemic lupus erythematosus. J. Nephropathol., 2016, Vol. 5, no. 1, pp. 28-33.

Jariwala M.P., Laxer R.M. NETosis in Rheumatic Diseases. Curr. Rheumatol. Rep., 2021, Vol. 23, no. 2. doi:10.1007/s11926-020-00977-6.

Johansson U., Walther-Jallow L., Smed-Sorensen A., Spetz A.L. Triggering of dendritic cell responses after exposure to activated, but not resting, apoptotic PBMCs. J. Immunol., 2007, Vol. 179, no. 3, pp. 1711-1720.

Jung J.Y., Koh B.R., Kim H.A., Jeon J.Y., Suh C.H. Autoantibodies to C-reactive protein in incomplete lupus and systemic lupus erythematosus. J. Investig. Med., 2014, Vol. 62, no. 6, pp. 890-893.

Kessenbrock K., Krumbholz M., Schonermarck U., Back W, Gross W, Werb Z., Grone H., Brinkmann V, Jenne D. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med., 2009, Vol. 15, no. 6, pp. 623-625.

Kaczmarek А., Vandenabeele Р., Krysko D.V. Necroptosis: The release of damage-associated molecular patterns and its physiological relevance. Immunity, 2013, Vol. 38, no. 2, pp. 209-223.

Kahlenberg J. M., Carmona-Rivera C., Smith C.K., Kaplan M. Neutrophil extracellular trap-associated protein activation of the NLRP3 inflammasome is enhanced in lupus macrophages. J. Immunol., 2013, Vol. 190, no. 3, pp. 1217-1226.

Kalaaji M., Fenton K.A., Mortensen E.S., Olsen R., Sturfelt G., Alm P., Rekvig O. Glomerular apoptotic nucleosomes are central target structures for nephritogenic antibodies in human SLE nephritis. Kidney Int., 2007, Vol. 71, no. 7, pp. 664-672.

Kaplan M. J., Apoptosis in systemic lupus erythematosus. Clin. Immunol., 2004, Vol. 112, no. 3, pp. 210-218.

Kato M., Ospelt C., Gay R.E., Gay S., Klein K. Dual role of autophagy in stress-induced cell death in rheumatoid arthritis synovial fibroblasts. Arthritis Rheumatol., 2014, Vol. 66, no. 1, pp. 40-48.

Kaushik S., Massey A.C., Mizushima N., Cuervo A.M. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol. Biol. Cell, 2008, Vol. 19, no. 5, pp. 2179-2192.

Kayagaki N., Warming S., Lamkanfi M., Vande Walle L., Louie S., Dong J., Newton K., Qu Y., Liu J., Heldens S., Zang J., Lee W., Roose-Girma M., Dixit V. Non-canonical inflammasome activation targets caspase-11. Nature, 2011, Vol. 479, pp. 117-121.

Kerr J.F.R., Wyllie A.H., Currie A. R. Apoptosis: A Basic Biological Phenomenon with Wideranging Implications in Tissue Kinetics. Br. J. Cancer, 1972, Vol. 26, no. 4, pp. 239-257.

Kessenbrock K., Krumbholz M., Schonermarck U., Back W., Gross W.L., Werb Z., Grone H., Brinkmann V., Jenne D. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med., 2009, Vol. 15, no. 6, pp. 623-625.

Khandpur R., Carmona-Rivera C., Vivekanandan-Giri A., Gizinski A., Yalavarthi S., Knight J.S., Friday S., Li S., Patel R.M., Subramanian V., Thompson P., Chen P., Fox D.A., Pennathur S., Kaplan M.J. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci.Transl.l Med.,2013, Vol. 5, no. 178, 178ra40. doi:10.1126/scitranslmed.3005580.

Khoury M.K., Gupta K., Franco S.R., Liu B. Necroptosis in the pathophysiology of disease. Am. J. Pathol., 2020, Vol. 190, no. 2, pp. 272-285.

Kobayashi K., Kaneda K., Kasama T. Immunopathogenesis of delayed-type hypersensitivity. Microsc. Res. Tech., 2001, Vol. 53, no. 4, pp. 241-245.

Kobayashi N., Karisola P., Pena-Cruz V., Dorfman D.M., Jinushi M., Umetsu S.E., Butte M.J., Nagumo H., Chernova I., Zhu B., Sharpe A.H., Ito S., Dranoff G., Kaplan G.G., Casasnovas J.M., Umetsu D.T., Dekruyff R.H., Freeman G. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity, 2007, Vol. 27, no. 6, pp. 927-940.

Kolly L., Busso N., Palmer G., Talabot-Ayer D., Chobaz V., So A. Expression and function of the NALP3 inflammasome in rheumatoid synovium. Immunology, 2010, Vol. 129, no. 2, pp. 178-185.

Kono H., Karmarkar D., Iwakura Y., Rock K.L. Identification of the cellular sensor that stimulates the inflammatory response to sterile cell death. J. Immunol., 2010, Vol. 184, no. 8, pp. 4470-4478.

Kovacs J.R., Li C., Yang Q., Li G., Garcia I.G., Ju S., Roodman D.G., Windle J.J., Zhang X., Lu B. Autophagy promotes T-cell survival through degradation of proteins of the cell death machinery. Cell Death Differ., 2012, Vol. 19, no. 1, pp. 144-152.

Krainer J., Siebenhandl S., Weinhausel A. Systemic autoinflammatory diseases. J. Autoimmun., 2020,102421. doi:10.1016/j.jaut.2020.102421.

Kril I., Havrylyuk A., Potomkina H., Chopyak V. Apoptosis and secondary necrosis of neutrophils and monocytes in the immunopathogenesis of rheumatoid arthritis: a cohort study. Rheumat.Int., 2020, Vol. 40, Iss. 9, pp. 1449-1454.

Kroemer G.R., Galluzzi L., Vandenabeele P., Abrams J., Alnermi E.S., Baehrecke E.H., Blagosklonny M.V., El-Deiry W.S., Golstein P., Green D.R., Hengartner M., Knight R.A., Kumar S., Lipton S.A., Malorni W., Nunez G., Peter M.E., Tschopp J., Yuan J., Piacentini M., Zhivotovsky B., Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ., 2009, Vol. 16, no. 1, pp. 3-11.

Krysko D.V., Denecker G., Festjens N., Gabriels S., Parthoens E., D'Herde K., Vandenabeele P. Macrophages use different internalization mechanisms to clear apoptotic and necrotic cells. Cell Death Differ., 2006, Vol. 13, no. 12, pp. 2011-2022.

Lamkanfi M., Sarkar A., Vande Walle L., Vitari A.C., Amer A.O., Wewers M.D., Tracey K.J., Kanneganti T.D., Dixit V.M. Inflammasome-dependent release of the alarmin HMGB1 in endotoxemia. J. Immunol., 2010, Vol. 185, no. 7, pp. 4385-4392.

Laster S.M., Wood J.G., Gooding L.R. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J. Immunol., 1988, Vol. 141, no. 8, pp. 2629-2634.

100

Lauber K., Bohn E., Kroober S.M., Xiao Y.J., Blumenthal S.G., Lindemann R.K., Marini P., Wiedig C., Zobywalski A., Baksh S., Xu Y., Autenrieth I., Schulze-Jsthoff K., Belka C., Stuhler G., Wesselborg S. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell, 2003, Vol. 113, no. 6, pp. 717-730.

101

Lawlor K.E., Khan N., Mildenhalletal A., Gerlic M., Croker B.A., Dcuz A.A., Hall C., Spall S.K., Anderton H., Masters S.L., Rashidi M., Wicks I.P., Alexander W.S., Mitsuuchi Y., Benetatos C.A., Condon S.M., Wong W.W.-L., Silke J., Vaux D.L., Vince J. RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat. Commun., 2015, Vol. 6, 6282. doi: 10.1038/ncomms7282.

102

Lee J.W., Epardaud M., Sun J., Becker J.E., Cheng A.C., Yonekura A, Heath J.K., Turley S.J. Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat. Immunol., 2007. Vol. 8, no. 2, pp. 181-190.

103

Leffler J., Gullstrand B., Jonsen A., Nilsson J.A., Martin M., Blom A.M., Bengtsson A. Degradation of neutrophil extracellular traps covaries with disease activity in patients with systemic lupus erythematosus. Arthritis Res Ther., 2013, Vol. 15, no. 4, R84. doi:10.1186/ar4264.

104

Levine B., Mizushima N., Herbert W. Virgin Autophagy in immunity and inflammation. Nature, 2011, Vol. 469, pp. 323-334.

105

Li J., McQuade T., Siemer A., Napetschnig J., Moriwaki K., Hsiao Y., Damko E., Moquin D., Walz T., McDermott A., Chan F., Wu H. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell, 2012, Vol. 150, no. 2, pp. 339-350.

106

Li W., Yang Q., Mao Z. Chaperone-mediated autophagy: machinery, regulation and biological consequences. Cell. Mol. Life Sci., 2011, Vol. 68, no. 5, pp. 749-763.

107

Li Y., Shen Y., Jin K., Wen Z., Cao W., Wu B., Wen R., Tian L., Berry G., Goronzy J., Weyand C.M. The DNA repair nuclease MRE11A functions as a mitochondrial protector and prevents T cell pyroptosis and tissue inflammation. Cell Metab., 2019, Vol. 30, no. 3, pp. 477-492.

108

Liberale L., Carbone F., Vecchie A., Diaz-Canestro C., Camici G., Montecucco F., Dallegri F., Bonaventura A. The pathophysiological role of neutrophil extracellular traps in inflammatory diseases. Thromb. Haemost., 2018, Vol. 118, no. 1, pp. 6-27.

109

Lin N.Y., Beyer C., Giessl A., Kireva T., Scholtysek C., Uderhardt S., Enrique L. Munoz E.L., Dees C., Distler A., Wirtz S., Kronke G., Spenser B., Distler O., Schett G., Distler J.H. Autophagy regulates TNFa-mediated joint destruction in experimental arthritis. Ann. Rheum. Dis., 2013, Vol. 72, no. 5, pp. 761-768.

110

Lleo, A., Selmi C., Invernizzi P., Podda M., Gershwin M. E. The consequences of apoptosis in autoimmunity. J. Autoimmun., 2008, Vol. 31, no. 3, pp. 257-262.

111

Lood С., Blanco L.P., Pumalike M.M., Carmona-Rivera C., de Ravin S., Smith C., Malech H., Ledbetter J., Elkon K., Kaplan M. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat. Med., 2016, Vol. 22, no. 2, pp. 146-153.

112

Lopalco G., Cantarini L., Vitale A., Iannone F., Anelli M. G., Andreozzi, L., Lapadula G., Galeazzi M., Rigante D. Interleukin-1 as a common denominator from autoinflammatory to autoimmune disorders: premises, perils, and perspectives. Mediators Inflamm., 2015, Vol. 2015, 194864. doi:10.1155/2015/194864

113

Ludemann J., Utecht B., Gross W.L. Anti-neutrophil cytoplasm antibodies in Wegener's granulomatosis recognize an elastinolytic enzyme. J. Exp. Med., 1990, Vol. 171, pp. 357-362.

114

Luo X.Y., Yuan J.L., Liuetal J. Increased macroautophagy in interferon-gamma-producing T cells from patients with newly diagnosed systemic lupus erythematosus. Chin. Med. J., 2018, Vol. 131, no. 13, pp. 1527-1532.

115

Maeda A., Fadeel B. Mitochondria released by cells undergoing TNF-a-induced necroptosis act as danger signals. Cell Death Dis., 2014, Vol. 5. no. 7, e1312. doi: 10.1038/cddis.2014.277.

116

Martin S.J., Henry C.M., Cullen S.P. A perspective on mammalian caspases as positive and negative regulators of inflammation. Mol. Cell, 2012, Vol. 46, no. 4, pp. 387-397.

117

Martinod K., Wiltsch T., Farley K., Gallant M., Remold-Odonnell E., Wagner D. Neutrophil elastasedeficient mice form neutrophil extracellular traps in an experimental model of deep vein thrombosis. J. Thromb. Haemost., 2016, Vol. 14, no. 3, pp. 551-558.

118

Masters S.L., Simon A., Aksentijevich I., Kastner D.L. Horror autoinflammaticus: the molecular pathophysiology of autoinflammatory disease. Annu. Rev. Immunol., 2009, Vol. 27, pp. 621-668.

119

Matzinger P. The danger model: a renewed sense of self. Science, 2002, Vol. 296, pp. 301-305.

120

Mayes M.D., Bossini-Castillo L., Gorlova O., Martin J.E., Zhou X., Chen W.V., Assassi S., Ying J., Tan F.K., Arnett F.C., Reveille J.D., Guerra S., Teruel M., Carmona F.D., Gregersen P.K., Lee A.T., Lopez-Isac E., Ochoa E., Carreira P., Simeon C.P., CastelM I., Gonzalez-Gay M.A., Spanish Scleroderma Group; Zhernakova A., Padyukov L., Alarcon-Riquelme M., Wijmenga C., Brown M., Beretta L., Riemekasten G., Witte T., Hunzelmann N., Kreuter A., Distler J.H.W., Voskuyl A.E., Schuerwegh A.J., Hesselstrand R., Nordin A., Airo P., Lunardi C., Shiels P., van Laar J.M., Herrick A., Worthington J., Denton C., Wigley F.M., Hummers L.K., Varga J., Hinchcliff M.E., Baron M., Hudson M., Pope J.E., Furst D.E., Khanna D., Phillips K., Schiopu E., Segal B.M., Molitor J.A., Silver R.M., Steen V.D., Simms R.W., Lafyatis R.A., Fessler B.J., Frech T.M., Alkassab F., Docherty P., Kaminska E., Khalidi N., Jones H.N., Markland J., Robinson D., Broen J., Radstake T.R.D.J., Fonseca C., Koeleman B.P., Martin J. Immunochip analysis identifies multiple susceptibility loci for systemic sclerosis. Am. J. Hum. Genet., 2014, Vol. 94, no. 1, pp. 47-61.

121

McGonagle D., McDermott M.F. A proposed classification of the immunological diseases. PLoS Med., 2006, Vol. 3, no. 8, e297. doi:10.1371/journal.pmed.0030297.

122

McLeod I.X., He Y. Roles of autophagy in lymphocytes: reflections and directions. Cell. Mol. Immunol., 2010, Vol. 7, no. 2, pp. 104-107.

123

Mcllroy D.J., Jarnicki A.G., Au G.G., Lott N., Smith D., Hansbro P., Balogh Z. Mitochondrial DNA neutrophil extra cellular traps are formed after trauma and subsequent surgery. J. Crit. Care, 2014, Vol. 29, no. 6, 1133.e1-e5. doi: 10.1016/j.jcrc.2014.07.013.

124

Mehrpour M., Esclatine A., Beau I., Codogno P. Overview of macroautophagy regulation in mammalian cells. Cell Res., 2010, Vol. 20, no. 7, pp. 748-762.

125

Metzler K.D., Goosmann C., Lubojemska A., Zychlinsky A., Papayannopoulos V. A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Rep., 2014, Vol. 8, no. 3, pp. 883-896.

126

Mijaljica D., Prescott M., Devenish R.J. Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy, 2011, Vol. 7, no. 7, pp. 673-682.

127

Mitchell J.S., Li N., Weinhold N., Forsti A., Ali M., van Duin M., Thorleifsson G., Johnson D.C., Chen B., Halvarsson B.-M., Gudbjartsson D.F., Kuiper R., Stephens O.W., Bertsch U., Broderick P., Campo C., Einsele H., Gregory W.A., Gullberg U., Henrion M., Hillengass J., Hoffmann P, Jackson G.H., Johnsson E., Joud M., Kristinsson S.Y., Lenhoff S., Lenive O., Mellqvist U.-H., Migliorini G., Nahi H., Nelander S., Nickel J., Nothen M.M., Rafnar T., Ross F.M., da Silva Filho M.I., Swaminathan B., Thomsen H., Turesson I., Vangsted A., Vogel U., Waage A., Walker B.A., Wihlborg A.-K., Broyl A., Davies F.E., Thorsteinsdottir U., Langer C., Hansson M., Kaiser M., Sonneveld P., Stefansson K., Morgan G.J., Goldschmidt H., Hemminki K., Nilsson B., Houlston R. Genome-wide association study identifies multiple susceptibility loci for multiple myeloma. Nat. Commun., 2016, Vol. 7, 12050. doi: 10.1038/ncomms12050.

128

Mizushima N. Autophagy: process and function. Genes Dev., 2007, Vol. 21, no. 22, pp. 2861-2873.

129

Mizushima N., Klionsky D.J. Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr., 2007, Vol. 27, pp. 19-40.

130

Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell, 2010, Vol. 140, no. 3, pp. 313-326.

131

Mocarski E.S., Upton J.W., Kaiser W.J. Viral infection and the evolution of caspase 8-regulated apoptotic and necrotic death pathways. Nat. Rev. Immunol., 2011, Vol. 12, no. 2, pp. 79-88.

132

Mohr W., Westerhellweg H., Wessinghage D. Polymorphonuclear granulocytes in rheumatic tissue destruction. III. An electron microscopic study of PMNs at the pannus-cartilage junction in rheumatoid arthritis. Ann. Rheum. Dis., 1981, Vol. 40, 396-399.

133

Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol., 2008, Vol. 8, no. 12, pp. 958-969.

134

Munoz L.E., Lauber K., Schiller M., Manfredi A.A., Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat. Rev. Rheumatol., 2010, Vol. 6, no. 5, pp. 280-289.

135

Munoz L., van Bavel C., Franz S., Berden J., Herrmann M., van der Vlag J. Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus, 2008, Vol. 17, no. 5, pp. 371-375.

136

Munz С. Autophagy and antigen presentation. Cell. Microbiol., 2006, Vol. 8, no. 6, pp. 891-898.

137

Munz C. Antigen processing via autophagy - not only for MHC class II presentation anymore? Curr. Opin. Immunol., 2010, Vol. 22, pp. 89-93.

138

Muruve D.A., Petrilli V., Zaiss A., White L., Clark S., Ross P., Parks R., Tschopp J. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature, 2008, Vol. 452, pp. 103-107.

139

Nagata S. Apoptosis and clearance of apoptotic cells. Annu. Rev. Immunol., 2018, Vol. 36, pp. 489-517.

140

Nagy G., Barcza M., Gonchoroff N., Phillips P.E., Perl A. Nitric oxide-dependent mitochondrial biogenesis generates Ca2+ signaling profile of lupus T cells. J. Immunol., 2004, Vol. 173, no. 6, pp. 3676-3683.

141

Ning X., Wang Y., Jingetal M. Apoptotic caspases suppress type I interferon production via the cleavage of cGAS, MAVS, and IRF3. Mol. Cell, Vol. 74, no. 1, pp. 19-31.

142

Oppenheim J.J., Yang D. Alarmins: chemotactic activators of immune responses. Curr. Opin. Immunol., 2005, Vol. 17, no. 4, pp. 359-365.

143

Panaretakis T., Kepp O., Brockmeier U., Tesniere A., Bjorklund A.C., Chapman D.C., Durchschlag M., Joza N., Pierron G., van Endert, P., Yuan J., Zitvogel L., Madeo F., Williams D., Kroemer G. Mechanisms of preapoptotic calreticulin exposure in immunogenic cell death. EMBO J., 2009, Vol. 28, no. 5, pp. 578-590.

144

Park S.Y., Jung M.Y., Kim H.J., Lee S.J., Kim S.Y., Lee B.H., Kwon T., Park R., Kim I. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ., 2008, Vol. 15, no. 1, pp. 192-201.

145

Pasparakis M., Vandenabeele P. Necroptosis and its role in inflammation. Nature, 2015, Vol. 517, no. 7534, pp. 311-320.

146

Pierdominici M., Vomero M., Barbati C., Colasanti T, Maselli A., Vacirca D., Giovannetti A., Malorni W., Ortona E. Role of autophagy in immunity and autoimmunity, with a special focus on systemic lupus erythematosus. FASEB J., 2012, Vol. 26, no. 4, pp. 1400-1412.

147

Pisetsky D.S., Erlandsson-Harris H., Andersson U. High-mobility group box protein 1 (HMGB1): an alarmin mediating the pathogenesis of rheumatic disease. Arthritis Res. Ther., 2008, Vol. 10, no. 3, 209. doi:10.1186/ar2440.

148

Pua H.H., He Y.W. Maintaining T lymphocyte homeostasis: another duty of autophagy. Autophagy, 2007, Vol. 3, no. 3, pp. 266-267.

149

Pua H.H., Guo J., Komatsu M., He Y.W. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J. Immunol., 2009, Vol. 182, no. 7, pp. 4046-4055.

150

Puri A.W., Broz P., Shen A., Monack D.M., Bogyo M. Caspase-1 activity is required to bypass macrophage apoptosis upon Salmonella infection. Nat. Chem. Biol., 2012, Vol. 8, no. 9, pp. 745-747.

151

Radic M. Clearance of apoptotic bodies, NETs, and Biofilm DNA: implications for autoimmunity. Front. Immunol., 2014, Vol. 5, 365. doi: 10.3389/fimmu.2014.00365.

152

Radic M., Herrmann M.J., van der Vlag J., Rekvig O.P. Regulatory and pathogenetic mechanisms of autoantibodies in SLE. Autoimmunity, 2011, Vol. 44, no. 5, pp. 349-356.

153

Ren Y., Tang J., Mok M.Y., Chan A.W., Wu A., Lau C.S. Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum., 2003, Vol. 48, no. 10, pp. 2888-2897.

154

Riedl S.J., Salvesen G.S. The apoptosome: signalling platform of cell death. Nat. Rev., 2007, Vol. 8, no. 5, pp. 405-413.

155

Rizzo C., Grasso G., Castaniti G., Ciccia F., Guggino G. Primary sjogren syndrome: focus on innate immune cells and inflammation. Vaccines, 2020, Vol. 8, no. 2, pp. 1-23.

156

Roberts T.L., Idris A., Dunn J.A., Kelly G.M., Burnton C.M., Hodgson S., Hardy L.L., Garceau V., Sweet M.J., Ross L.I., Hume A.D., Stacey J.K. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science, 2009, Vol. 323, no. 5917, pp. 1057-1060.

157

Robinson N., McComb S., Mulligan R., Dudani R., Krishnan L., Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica, serovar Typhimurium. Nat. Immunol., 2012, Vol. 13, no. 10, pp. 954-962.

158

Rock K.L., Kono H. The inflammatory response to cell death. Annu. Rev. Pathol., 2008, Vol. 3, pp. 99-126.

159

Rock K.L., Latz E., Ontiveros F., Kono H. The sterile inflammatory response. Annu. Rev. Immunol., 2010, Vol. 28, pp. 321-342.

160

Rubartelli A., Poggi A., Zocchi M.R. The selective engulfment of apoptotic bodies by dendritic cells is mediated by the alpha(v)beta3 integrin and requires intracellular and extracellular calcium. Eur. J. Immunol., 1997, Vol. 27, no. 8, pp. 1893-1900.

161

Sangaletti S., Tripodo C., Chiodoni C., Guarnotta C., Cappetti B., Casalini P., Piconese S., Parenza M., Guiducci C., Vitali C., Colombo M. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood, 2012, Vol. 120, no. 15, pp. 3007-3018.

162

Sarhan J., Liu B.C., Muendleinetal H.I. Constitutive interferon signaling maintains critical threshold of MLKL expression to license necroptosis. Cell Death Differ., 2019, Vol. 26, no. 2, pp. 332-347.

163

Schauer C., Janko C., Munoz L.E., Zhao Y., Kienhofer D., Frey B., Lell M., Manger B., Rech J., Naschberger E., Holmdahl R., Krenn V., Harrer T., Jeremic I., Bilyy R., Schett G., Hoffmann M., Herrmann M. Aggregated neutrophil extracellular traps limit inflammation by degrading cytokines and chemokines. Nat. Med., 2014, Vol. 20, no. 5, pp. 511-517.

164

Schmid D., Pypaert M. Munz C. Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity, 2007, Vol. 26, no. 1, pp. 79-92.

165

Schorn C., Janko C., Latzko M., Chaurio R., Schett G., Herrmann M. Monosodium urate crystals induce extracellular DNA traps in neutrophils, eosinophils, and basophils but not in mononuclear cells. Front. Immunol., 2012, Vol. 3, 277. doi: 10.3389/fimmu.2012.00277.

166

Sciorati C., Rigamonti E., Manfredi A.A., Rovere-Querini P. Cell death, clearance and immunity in the skeletal muscle. Cell Death Differ., 2016, Vol. 23, no. 6, pp. 927-937.

167

Shin M.S., Kang Y., Lee N., Wahl R., Kim S., Kang K., Lazova R., Kang I. Self double-stranded (ds)DNA induces IL-1 в production from human monocytes by activating NLRP3 inflammasome in the presence of anti-dsDNA antibodies. J. Immunol., 2013, Vol. 190, no. 4, pp. 1407-1415.

168

Shin M.S., Kang Y., Wahl E.R., Park H., Lasova R., Leng L., Mamula M., Krishnaswamy S., Bucala R., Kang I. Macrophage Migration Inhibitory Factor Regulates U1 Small Nuclear RNP Immune Complex-Mediated Activation of the NLRP3 Inflammasome. Arthritis Rhematol., 2019, Vol. 71, no. 1, pp. 109-120.

169

Siegert C., Daha M., Westedt M.L., van der Voort E., Breedveld F. IgG autoantibodies against C1q are correlated with nephritis, hypocomplementemia, and dsDNA antibodies in systemic lupus erythematosus. J. Rheumatol., 1991, Vol. 18, no. 2, pp. 230-234.

170

Silke J., Rickard J.A., Gerlic M. The diverse role of RIP kinases in necroptosis and inflammation. Nat. Immunol., 2015, Vol. 16, no. 7, pp. 689-697.

171

Spengler J., Lugonia B., Ytterberg A.J., Zubarev R.A., Creese A.J., Pearson M.J., Grant M.M., Milward M., Lundberg K., Buckley C.D., Filer A., Raza K., Cooper P.R., Chapple I.L., Scheel-Toellner D. Release of active peptidyl arginine deiminases by neutrophils can explain production of extracellular citrullinated autoantigens in rheumatoid arthritis synovial fluid. Arthritis Rheumatol., 2015, Vol. 67, no. 12, pp. 3135-3145.

172

Sutterwala F.S., Ogura Y., Szczepanik M., Lara-Tejero M., Lichtenberger G.S., Grant E. P., Bertin J., Coyle A.J., Galan J.E., Askenase P.W., Fravell R.A. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity, 2006, Vol. 24, no. 3, pp. 317-327.

173

Sutton C.E., Lalor S.J.., Sweeney C.M., Brereton C.F., Lavelle E.C., Mills K.H. Interleukin-1 and IL-23 induce innate IL-17 production from y§-T cells, amplifying 'lh17 responses and autoimmunity. Immunity, 2009, Vol. 31, no. 2, pp. 331-341.

174

Takeshige K., Baba M., Tsuboi S., Noda T., Ohsumi Y. Autophagy in yeast demonstrated with proteinasedeficient mutants and conditions for its induction. J. Cell Biol., 1992, Vol. 119, no. 2, pp. 301-311.

175

Tanaka T., Warner B.M., Odani T., Ji Y., Mo Y.-Q., Nakamura H., Jang S.-I., Yin H., Michael D.G., Hirata N., Suizu F., Ishigaki S., Oliveira F.R., Motta A.C.F., Ribeiro-Silva A., Rocha E.M., Atsumi T., Noguchi M., Chiorini J.A. LAMP3 induces apoptosis and autoantigen release in Sjogren's syndrome patients. Sci. Rep., 2020, Vol. 10, no. 1, 15169. doi:10.1038/s41598-020-71669-5

176

Tang S., Zhang Y., Yin S .W., Gao X., Shi W., Wang Y., Huahg X., Wang L., Zou L., Zhao J., Huang Y., Shan L., Gounni A., Wu Y., Zhang J. Neutrophil extracellular trap formation is associated with autophagy-related signalling in ANCA-associated vasculitis. Clin. Exp. Immunol., 2015, Vol. 180, no. 3, pp. 408-418.

177

Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol., 2008, Vol. 9, no. 3, pp. 231-241.

178

Tillack K., Breiden P., Martin R., Sospedra M. T lymphocyte priming by neutrophil extracellular traps links innate and adaptive immune responses. J. Immunol., 2012, Vol. 188, no. 7, pp. 3150-3159.

179

Tsuchiya K. Switching from apoptosis to pyroptosis: gasdermin-elicited inflammation and antitumor immunity. International J. Mol. Sci., 2021, Vol. 22, no. 1, 426. doi:10.3390/ijms22010426.

180

Urban C.F., Reichard U., Brinkmann V., Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol., 2006, Vol. 8, no. 4, pp. 668-676.

181

Valesini G., Gerardi M.C., Iannuccelli C., Pacucci V., Pendolino M., Shoenfeld Y. Citrullination and autoimmunity. Autoimmun. Rev., 2015, Vol. 14, no. 6, pp. 490-497.

182

Vandanmagsar B., Youm Y.H., Ravussin A., Galgani J.E., Stadler K., Mynatt R.L., Ravussin E., Stephens J.M., Dixit V.D. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med., 2011, Vol. 17, no. 2. pp. 179-188.

183

Vande Walle L., Lamkanfi M. Pyroptosis. Curr. Biol., 2016, Vol. 26, no. 13, pp. R568-R572.

184

Vandivier R.W., Fadok V.A., Ogden C.A., Hoffmann P.R., Brain J.D., Accurso F.J. Impaired clearance of apoptotic cells from cystic fibrosis airways. Chest, 2002, Vol. 121, Iss. 3 Suppl., 89S. doi: 10.1378/chest.121.3_suppl.89S.

185

Voll R.E., Herrmann M., Roth E.A., Stach C. Kalden J.R., Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature, 1997, Vol. 390, no. 6658, pp. 350-351.

186

Wu M-Y., Lu J.-H. Autophagy and macrophage functions: inflammatory response and phagocytosis. Cells, 2020, Vol. 9, no. 1, 70. doi:10.3390/cells9010070.

187

Wu X., Li K., Yang H., Yang B., Lu X., Zhao L., Fei Y-Y., Chen H., Wang L., Li J., Peng L-Y., Zheng W-J., Hou Y., Jiang Y., Shi Q., Zhang W., Zhang F-C., Zhang J-M., Huang B., He W., Zhang X. Complement C1q synergizes with PTX3 in promoting NLRP3 inflammasome over-activation and pyroptosis in rheumatoid arthritis. J. Autoimmun., 2019, 102336. doi:10.1016/j.jaut.2019.102336.

188

Wu X., Ren G., Zhou R., Ge J., Chen F.-H. The role of Ca2+ in acid-sensing ion channel 1a-mediated chondrocyte pyroptosis in rat adjuvant arthritis. Laboratory Investigation, 2019, Vol. 99, no. 4, pp. 499-513.

189

Xie L., Xu J. Role of MiR-98 and its underlying mechanisms in systemic lupus erythematosus. The Journal of Rheumatology, 2018, Vol. 45, no. 10, pp. 1397-1405.

190

Xu J., Jiang Y., Wang J., Shi X., Liu Q., Liu Z., Fan J. Macrophage endocytosis of high-mobility group box 1 triggers pyroptosis. Cell Death Differ., 2014, Vol. 21, no. 8, pp. 1229-1239.

191

Xu Y., Jagannath C., Liu X-D., Sharafkhaneh A., Kolodziejska K., Eissa T. Toll-like Receptor 4 is a sensor for autophagy associated with innate immunity. Immunity, 2007, Vol. 27, no.1, pp. 135-144.

192

Yang F., He Y., Zhai Z., Sun E. Programmed cell death pathways in the pathogenesis of systemic lupus erythematosus. J. Immunol. Res., 2019, 3638562. doi:10.1155/2019/363856.

193

Yang Y., Jiang G., Zhang P., Fan J. Programmed cell death and its role in inflammation. Mil. Med. Res., 2015, Vol. 2, 12. doi:10.1186/s40779-015-0039-0.

194

Yao Z., Delorme-Axford E., Backues S.K., Klionsky D.J. Atg41/Icy2 regulates autophagosome formation. Autophagy, 2015, Vol. 11, pp. 2288-2299. doi: 10.1080/15548627.2015.1107692.

195

Ye X., Zhou X.-J., Zhang H. Exploring the role of autophagy-related gene 5 (ATG5) yields important insights into autophagy in autoimmune / autoinflammatory diseases. Front. Immunol., 2018, Vol. 9, 2334. doi: 10.3389/fimmu.2018.02334.

196

Yipp B.G., Kubes P. NETosis: how vital is it? Blood, 2013, Vol. 122, no. 16, pp. 2784-2794.

197

Zhang D.W., Shao J., Lin J., Zhang N., Lu B.J., Lin S.C., Dong M.Q., Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science, 2009, Vol. 325, pp. 332-336.

198

Zhang S., Lu X., Shu X., Tian X., Yang H., Yang W., Zhang Y., Wang G. Elevated plasma cfDNA may be associated with active lupus nephritis and partially attributed to abnormal regulation of neutrophil extracellular traps (NETs) in patients with systemic lupus erythematosus. Intern. Med., 2014, Vol. 53, no. 24, pp. 2763-2771.

199

Zhao J., Jitkaew S., Cai, Z., Choksi S., Li Q., Luo J., Liu, Z.G. Mixed lineage kinase domain-like is a key receptor interacting protein 3 down-stream component of TNF-induced necrosis. Proc. Natl. Acad. Sci. USA, 2012, Vol. 109, no. 14, pp. 5322-5327.

200

Zhou X.J., Lu X.L., Lv J.C., Yang H.Z., Qin L.X., Zhao M.H., Su Y., Li Z., Zhang H. Genetic association of PRDM1-ATG5 intergenic region and autophagy with systemic lupus erythematosus in a Chinese population. Ann. Rheum. Dis., 2011, Vol. 70, no. 7, pp. 1330-1337.

201

Zhu L., Wang H., Wu Y., He Z., Qin Y., Shen Q. The autophagy level is increased in the synovial tissues of patients with active rheumatoid arthritis and is correlated with disease severity. Mediators Inflamm., 2017, Vol. 2017, 7623145. doi: 10.1155/2017/7623145.

202

Zickert A., Palmblad K., Sundelin B., Chavan S., Tracey K., Bruchfeld A., Gunnarsson I. Renal expression and serum levels of high mobility group box 1 protein in lupus nephritis. Arthritis Res. Ther., 2012, Vol. 14, no. 1, R36. doi: 10.1186/ar3747.

203

Zoncu R., Efeyan A., Sabatini D.M. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell. Biol., 2011, Vol. 12, no. 1, pp. 21-35.

The authors declare that there are no conflicts of interest present.