INVITED REVIEW
A variety of death modes of neutrophils and their role in the etiology of autoimmune diseases
Yanhong Li,
Yinlan Wu,
Jingang Huang,
Xue Cao,
Qiyuan An,
Yun Peng,
Yi Zhao,
Yubin Luo,
Yanhong Li
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Search for more papers by this authorYinlan Wu
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Search for more papers by this authorJingang Huang
Medical Research Center, Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Guangdong-Hong Kong Joint Laboratory for RNA Medicine, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorXue Cao
Department of Rheumatology and Immunology, Henan Provincial People's Hospital, People's Hospital of Zhengzhou University, People's Hospital of Henan University, Zhengzhou, Henan, China
Search for more papers by this authorQiyuan An
School of Inspection and Biotechnology, Southern Medical University, Guangzhou, China
Search for more papers by this authorYun Peng
Department of Rheumatology and Clinical Immunology, School of Medicine, The First Affiliated Hospital of Xiamen University, Xiamen University, Xiamen, Fujian, China
Search for more papers by this authorYi Zhao
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Search for more papers by this authorCorresponding Author
Yubin Luo
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Institute of Immunology and Inflammation, Frontiers Science Center for Disease-Related Molecular Network, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Correspondence
Yubin Luo, Laboratory of Rheumatology and Immunology, Department of Rheumatology & Immunology, West China Hospital, Sichuan University, No. 37 Guoxue Alley, 610041 Chengdu, Sichuan, China.
Email: [email protected]
Search for more papers by this authorYanhong Li,
Yinlan Wu,
Jingang Huang,
Xue Cao,
Qiyuan An,
Yun Peng,
Yi Zhao,
Yubin Luo,
Yanhong Li
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Search for more papers by this authorYinlan Wu
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Search for more papers by this authorJingang Huang
Medical Research Center, Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Guangdong-Hong Kong Joint Laboratory for RNA Medicine, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China
Search for more papers by this authorXue Cao
Department of Rheumatology and Immunology, Henan Provincial People's Hospital, People's Hospital of Zhengzhou University, People's Hospital of Henan University, Zhengzhou, Henan, China
Search for more papers by this authorQiyuan An
School of Inspection and Biotechnology, Southern Medical University, Guangzhou, China
Search for more papers by this authorYun Peng
Department of Rheumatology and Clinical Immunology, School of Medicine, The First Affiliated Hospital of Xiamen University, Xiamen University, Xiamen, Fujian, China
Search for more papers by this authorYi Zhao
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Search for more papers by this authorCorresponding Author
Yubin Luo
Department of Rheumatology & Immunology, Laboratory of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Institute of Immunology and Inflammation, Frontiers Science Center for Disease-Related Molecular Network, West China Hospital, Sichuan University, Chengdu, Sichuan, China
Correspondence
Yubin Luo, Laboratory of Rheumatology and Immunology, Department of Rheumatology & Immunology, West China Hospital, Sichuan University, No. 37 Guoxue Alley, 610041 Chengdu, Sichuan, China.
Email: [email protected]
Search for more papers by this authorYanhong Li and Yinlan Wu contributed equally to this article.
This article is part of a series of reviews covering Mechanisms of programmed cell death appearing in Volume 321 of Immunological Reviews.
Summary
Neutrophils are important in the context of innate immunity and actively contribute to the progression of diverse autoimmune disorders. Distinct death mechanisms of neutrophils may exhibit specific and pivotal roles in autoimmune diseases and disease pathogenesis through the orchestration of immune homeostasis, the facilitation of autoantibody production, the induction of tissue and organ damage, and the incitement of pathological alterations. In recent years, more studies have provided in-depth examination of various neutrophil death modes, revealing nuances that challenge conventional understanding and underscoring their potential clinical utility in diagnosis and treatment. This review explores the multifaceted processes and characteristics of neutrophil death, with a focus on tailored investigations within various autoimmune diseases. It also highlights the potential interplay between neutrophil death and the landscape of autoimmune disorders. The review encapsulates the pertinent pathways implicated in various neutrophil death mechanisms across diverse autoimmune diseases while also charts possible avenues for future research.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
Open Research
DATA AVAILABILITY STATEMENT
There is no data included the revision manuscript.
REFERENCES
- 1Kennedy AD, DeLeo FR. Neutrophil apoptosis and the resolution of infection. Immunol Res. 2009; 43: 25-61.
- 2Kotzin JJ, Spencer SP, McCright SJ, et al. The long non-coding RNA Morrbid regulates Bim and short-lived myeloid cell lifespan. Nature. 2016; 537: 239-243.
- 3Kantari C, Pederzoli-Ribeil M, Witko-Sarsat V. The role of neutrophils and monocytes in innate immunity. Contrib Microbiol. 2008; 15: 118-146.
- 4Burn GL, Foti A, Marsman G, Patel DF, Zychlinsky A. The neutrophil. Immunity. 2021; 54: 1377-1391.
- 5Maianski NA, Maianski AN, Kuijpers TW, Roos D. Apoptosis of neutrophils. Acta Haematol. 2004; 111: 56-66.
- 6Mayadas TN, Cullere X, Lowell CA. The multifaceted functions of neutrophils. Annu Rev Pathol. 2014; 9: 181-218.
- 7Wigerblad G, Kaplan MJ. Neutrophil extracellular traps in systemic autoimmune and autoinflammatory diseases. Nat Rev Immunol. 2023; 23: 274-288.
- 8Thiam HR, Wong SL, Wagner DD, Waterman CM. Cellular mechanisms of NETosis. Annu Rev Cell Dev Biol. 2020; 36: 191-218.
- 9Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004; 303: 1532-1535.
- 10Sorvillo N, Cherpokova D, Martinod K, Wagner DD. Extracellular DNA NET-works with dire consequences for health. Circ Res. 2019; 125: 470-488.
- 11Hakkim A, Fürnrohr BG, Amann K, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA. 2010; 107: 9813-9818.
- 12Cao X, Li Y, Luo Y, et al. Transient receptor potential melastatin 2 regulates neutrophil extracellular traps formation and delays resolution of neutrophil-driven sterile inflammation. J Inflamm (Lond). 2023; 20: 7.
- 13Wong SL, Wagner DD. Peptidylarginine deiminase 4: a nuclear button triggering neutrophil extracellular traps in inflammatory diseases and aging. FASEB J. 2018; 32:fj201800691R.
- 14Thiam HR, Wong SL, Qiu R, et al. NETosis proceeds by cytoskeleton and endomembrane disassembly and PAD4-mediated chromatin decondensation and nuclear envelope rupture. Proc Natl Acad Sci USA. 2020; 117: 7326-7337.
- 15Hidalgo A, Libby P, Soehnlein O, Aramburu IV, Papayannopoulos V, Silvestre-Roig C. Neutrophil extracellular traps: from physiology to pathology. Cardiovasc Res. 2022; 118: 2737-2753.
- 16Pilsczek FH, Salina D, Poon KK, et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol. 2010; 185: 7413-7425.
- 17Douda DN, Yip L, Khan MA, Grasemann H, Palaniyar N. Akt is essential to induce NADPH-dependent NETosis and to switch the neutrophil death to apoptosis. Blood. 2014; 123: 597-600.
- 18Azzouz D, Khan MA, Sweezey N, Palaniyar N. Two-in-one: UV radiation simultaneously induces apoptosis and NETosis. Cell Death Discov. 2018; 4: 51.
- 19Kaul A, Gordon C, Crow MK, et al. Systemic lupus erythematosus. Nat Rev Dis Primers. 2016; 2: 16039.
- 20Petretto A, Bruschi M, Pratesi F, et al. Neutrophil extracellular traps (NET) induced by different stimuli: a comparative proteomic analysis. PLoS One. 2019; 14:e0218946.
- 21Villanueva E, Yalavarthi S, Berthier CC, et al. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J Immunol. 2011; 187: 538-552.
- 22Garcia-Romo GS, 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; 3: 73ra20.
- 23Lande 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; 3: 73ra19.
- 24Guiducci C, Tripodo C, Gong M, et al. Autoimmune skin inflammation is dependent on plasmacytoid dendritic cell activation by nucleic acids via TLR7 and TLR9. J Exp Med. 2010; 207: 2931-2942.
- 25Denny MF, Yalavarthi S, Zhao W, et al. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J Immunol. 2010; 184: 3284-3297.
- 26Barrera-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; 77: 944-950.
- 27Zhan M, Wang Z, Bao H, et al. Antibodies against neutrophil extracellular traps (NETs) potentiate clinical performance of anti-double-stranded DNA antibodies in systemic lupus erythematosus. Clin Immunol. 2023; 249:109297.
- 28Hanata N, Ota M, Tsuchida Y, et al. Serum extracellular traps associate with the activation of myeloid cells in SLE patients with the low level of anti-DNA antibodies. Sci Rep. 2022; 12: 18397.
- 29Pieterse E, Hofstra J, Berden J, Herrmann M, Dieker J, van der Vlag J. Acetylated histones contribute to the immunostimulatory potential of neutrophil extracellular traps in systemic lupus erythematosus. Clin Exp Immunol. 2015; 179: 68-74.
- 30Wang H, Li T, Chen S, Gu Y, Ye S. Neutrophil extracellular trap mitochondrial DNA and its autoantibody in systemic lupus erythematosus and a proof-of-concept trial of metformin. Arthritis Rheumatol. 2015; 67: 3190-3200.
- 31Gestermann N, Di Domizio J, Lande R, et al. Netting neutrophils activate autoreactive B cells in lupus. J Immunol. 2018; 200: 3364-3371.
- 32Bertelli R, Schena F, Antonini F, et al. Neutrophil extracellular traps in systemic lupus erythematosus stimulate IgG2 production from B lymphocytes. Front Med. 2021; 8:635436.
- 33Carrillo-Vázquez DA, Jardón-Valadez E, Torres-Ruiz J, et al. Conformational changes in myeloperoxidase induced by ubiquitin and NETs containing free ISG15 from systemic lupus erythematosus patients promote a pro-inflammatory cytokine response in CD4(+) T cells. J Transl Med. 2020; 18: 429.
- 34Kahlenberg JM, Carmona-Rivera C, Smith CK, Kaplan MJ. Neutrophil extracellular trap-associated protein activation of the NLRP3 inflammasome is enhanced in lupus macrophages. J Immunol. 2013; 190: 1217-1226.
- 35Linhares-Lacerda L, Temerozo JR, Ribeiro-Alves M, et al. Neutrophil extracellular trap-enriched supernatants carry microRNAs able to modulate TNF-α production by macrophages. Sci Rep. 2020; 10: 2715.
- 36Frangou E, Chrysanthopoulou A, Mitsios A, et al. REDD1/autophagy pathway promotes thromboinflammation and fibrosis in human systemic lupus erythematosus (SLE) through NETs decorated with tissue factor (TF) and interleukin-17A (IL-17A). Ann Rheum Dis. 2019; 78: 238-248.
- 37Dieker J, Tel J, Pieterse E, et al. Circulating apoptotic microparticles in systemic lupus erythematosus patients drive the activation of dendritic cell subsets and prime neutrophils for NETosis. Arthritis Rheumatol. 2016; 68: 462-472.
- 38Chen SY, Wang CT, Chen CY, et al. Galectin-3 mediates NETosis and acts as an autoantigen in systemic lupus erythematosus-associated diffuse alveolar haemorrhage. Int J Mol Sci. 2023; 24:9493.
- 39Yang B, Huang X, Xu S, et al. Decreased miR-4512 levels in monocytes and macrophages of individuals with systemic lupus erythematosus contribute to innate immune activation and neutrsophil NETosis by targeting TLR4 and CXCL2. Front Immunol. 2021; 12:756825.
- 40Linge P, Arve S, Olsson LM, et al. NCF1-339 polymorphism is associated with altered formation of neutrophil extracellular traps, high serum interferon activity and antiphospholipid syndrome in systemic lupus erythematosus. Ann Rheum Dis. 2020; 79: 254-261.
- 41Lood C, Blanco LP, Purmalek MM, et al. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat Med. 2016; 22: 146-153.
- 42Carmona-Rivera C, Zhao W, Yalavarthi S, Kaplan MJ. Neutrophil extracellular traps induce endothelial dysfunction in systemic lupus erythematosus through the activation of matrix metalloproteinase-2. Ann Rheum Dis. 2015; 74: 1417-1424.
- 43Blanco LP, Wang X, Carlucci PM, et al. RNA externalized by neutrophil extracellular traps promotes inflammatory pathways in endothelial cells. Arthritis Rheumatol. 2021; 73: 2282-2292.
- 44Knight JS, Zhao W, Luo W, et al. Peptidylarginine deiminase inhibition is immunomodulatory and vasculoprotective in murine lupus. J Clin Invest. 2013; 123: 2981-2993.
- 45Knight JS, Subramanian V, O'Dell AA, et al. Peptidylarginine deiminase inhibition disrupts NET formation and protects against kidney, skin and vascular disease in lupus-prone MRL/lpr mice. Ann Rheum Dis. 2015; 74: 2199-2206.
- 46Lin H, Liu J, Li N, et al. NETosis promotes chronic inflammation and fibrosis in systemic lupus erythematosus and COVID-19. Clin Immunol. 2023; 254: 109687.
- 47Georgakis S, Gkirtzimanaki K, Papadaki G, et al. NETs decorated with bioactive IL-33 infiltrate inflamed tissues and induce IFN-α production in patients with SLE. JCI Insight. 2021; 6:e147671.
- 48Whittall-García LP, Torres-Ruiz J, Zentella-Dehesa A, et al. Neutrophil extracellular traps are a source of extracellular HMGB1 in lupus nephritis: associations with clinical and histopathological features. Lupus. 2019; 28: 1549-1557.
- 49Jiang M, Shen N, Zhou H, et al. The enrichment of neutrophil extracellular traps impair the placentas of systemic lupus erythematosus through accumulating decidual NK cells. Sci Rep. 2021; 11: 6870.
- 50Tumurkhuu G, Laguna DE, Moore RE, et al. Neutrophils contribute to ER stress in lung epithelial cells in the pristane-induced diffuse alveolar hemorrhage mouse model. Front Immunol. 2022; 13:790043.
- 51Shin HD, Park BL, Kim LH, Lee HS, Kim TY, Bae SC. Common DNase I polymorphism associated with autoantibody production among systemic lupus erythematosus patients. Hum Mol Genet. 2004; 13: 2343-2350.
- 52Chauhan SK, Rai R, Singh VV, Rai M, Rai G. Differential clearance mechanisms, neutrophil extracellular trap degradation and phagocytosis, are operative in systemic lupus erythematosus patients with distinct autoantibody specificities. Immunol Lett. 2015; 168: 254-259.
- 53Leffler J, Martin M, Gullstrand B, et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol. 2012; 188: 3522-3531.
- 54Antiochos B, Trejo-Zambrano D, Fenaroli P, et al. The DNA sensors AIM2 and IFI16 are SLE autoantigens that bind neutrophil extracellular traps. Elife. 2022; 11:e72103.
- 55Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med. 2010; 207: 1853-1862.
- 56Hemmers S, Teijaro JR, Arandjelovic S, Mowen KA. PAD4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection. PLoS One. 2011; 6:e22043.
- 57Gordon RA, Herter JM, Rosetti F, et al. Lupus and proliferative nephritis are PAD4 independent in murine models. JCI Insight. 2017; 2:e92926.
- 58Macanovic M, Sinicropi D, Shak S, Baughman S, Thiru S, Lachmann PJ. The treatment of systemic lupus erythematosus (SLE) in NZB/W F1 hybrid mice; studies with recombinant murine DNase and with dexamethasone. Clin Exp Immunol. 1996; 106: 243-252.
- 59Davis JC Jr, Manzi S, Yarboro C, et al. Recombinant human Dnase I (rhDNase) in patients with lupus nephritis. Lupus. 1999; 8: 68-76.
- 60Jarrot PA, Tellier E, Plantureux L, et al. Neutrophil extracellular traps are associated with the pathogenesis of diffuse alveolar hemorrhage in murine lupus. J Autoimmun. 2019; 100: 120-130.
- 61Curran AM, Naik P, Giles JT, Darrah E. PAD enzymes in rheumatoid arthritis: pathogenic effectors and autoimmune targets. Nat Rev Rheumatol. 2020; 16: 301-315.
- 62Thanabalasuriar A, Scott BNV, Peiseler M, et al. Neutrophil extracellular traps confine Pseudomonas aeruginosa ocular biofilms and restrict brain invasion. Cell Host Microbe. 2019; 25: 526-536.e4.
- 63Lapponi MJ, Carestia A, Landoni VI, et al. Regulation of neutrophil extracellular trap formation by anti-inflammatory drugs. J Pharmacol Exp Ther. 2013; 345: 430-437.
- 64Tang TT, Lv LL, Pan MM, et al. Hydroxychloroquine attenuates renal ischemia/reperfusion injury by inhibiting cathepsin mediated NLRP3 inflammasome activation. Cell Death Dis. 2018; 9: 351.
- 65Zhang S, Zhang Q, Wang F, et al. Hydroxychloroquine inhibiting neutrophil extracellular trap formation alleviates hepatic ischemia/reperfusion injury by blocking TLR9 in mice. Clin Immunol. 2020; 216:108461.
- 66Bonegio RG, Lin JD, Beaudette-Zlatanova B, York MR, Menn-Josephy H, Yasuda K. Lupus-associated immune complexes activate human neutrophils in an FcγRIIA-dependent but TLR-independent response. J Immunol. 2019; 202: 675-683.
- 67Ivey AD, Matthew Fagan B, Murthy P, et al. Chloroquine reduces neutrophil extracellular trap (NET) formation through inhibition of peptidyl arginine deiminase 4 (PAD4). Clin Exp Immunol. 2023; 211: 239-247.
- 68Gupta AK, 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; 9:e97088.
- 69Kraaij T, Kamerling SWA, de Rooij ENM, et al. The NET-effect of combining rituximab with belimumab in severe systemic lupus erythematosus. J Autoimmun. 2018; 91: 45-54.
- 70van Dam LS, Osmani Z, Kamerling SWA, et al. A reverse translational study on the effect of rituximab, rituximab plus belimumab, or bortezomib on the humoral autoimmune response in SLE. Rheumatology (Oxford). 2020; 59: 2734-2745.
- 71Smith MH, Berman JR. What is rheumatoid arthritis? JAMA. 2022; 327: 1194.
- 72Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med. 2013; 5: 178ra40.
- 73Biasi D, Carletto A, Caramaschi P, et al. Neutrophils in rheumatoid inflammation. Recenti Prog Med. 2003; 94: 25-30.
- 74Grönwall C, Liljefors L, Bang H, et al. A comprehensive evaluation of the relationship between different IgG and IgA anti-modified protein autoantibodies in rheumatoid arthritis. Front Immunol. 2021; 12:627986.
- 75Makrygiannakis D, af Klint E, Lundberg IE, et al. Citrullination is an inflammation-dependent process. Ann Rheum Dis. 2006; 65: 1219-1222.
- 76Catrina A, Krishnamurthy A, Rethi B. Current view on the pathogenic role of anti-citrullinated protein antibodies in rheumatoid arthritis. RMD Open. 2021; 7:e001228.
- 77Krishnamurthy A, Joshua V, Haj Hensvold A, et al. Identification of a novel chemokine-dependent molecular mechanism underlying rheumatoid arthritis-associated autoantibody-mediated bone loss. Ann Rheum Dis. 2016; 75: 721-729.
- 78Kwon EJ, Ju JH. Impact of posttranslational modification in pathogenesis of rheumatoid arthritis: focusing on citrullination, carbamylation, and acetylation. Int J Mol Sci. 2021; 22:10576.
- 79Liu CL, Tangsombatvisit S, Rosenberg JM, et al. Specific post-translational histone modifications of neutrophil extracellular traps as immunogens and potential targets of lupus autoantibodies. Arthritis Res Ther. 2012; 14: R25.
- 80Bach M, Moon J, Moore R, Pan T, Nelson JL, Lood C. A neutrophil activation biomarker panel in prognosis and monitoring of patients with rheumatoid arthritis. Arthritis Rheumatol. 2020; 72: 47-56.
- 81Delbosc S, Alsac JM, Journe C, et al. Porphyromonas gingivalis participates in pathogenesis of human abdominal aortic aneurysm by neutrophil activation. Proof of concept in rats. PLoS One. 2011; 6:e18679.
- 82Romero V, Fert-Bober J, Nigrovic PA, et al. Immune-mediated pore-forming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis. Sci Transl Med. 2013; 5: 209ra150.
- 83O'Neil LJ, Barrera-Vargas A, Sandoval-Heglund D, et al. Neutrophil-mediated carbamylation promotes articular damage in rheumatoid arthritis. Sci Adv. 2020; 6:eabd2688.
- 84Nakabo S, Ohmura K, Akizuki S, et al. Activated neutrophil carbamylates albumin via the release of myeloperoxidase and reactive oxygen species regardless of NETosis. Mod Rheumatol. 2020; 30: 345-349.
- 85Birkelund S, Bennike TB, Kastaniegaard K, et al. Proteomic analysis of synovial fluid from rheumatic arthritis and spondyloarthritis patients. Clin Proteomics. 2020; 17: 29.
- 86Spengler J, Lugonja B, Ytterberg AJ, et al. Release of active peptidyl arginine deiminases by neutrophils can explain production of extracellular citrullinated autoantigens in rheumatoid arthritis synovial fluid. Arthritis Rheumatol. 2015; 67: 3135-3145.
- 87Chapman EA, Lyon M, Simpson D, et al. Caught in a trap? Proteomic analysis of neutrophil extracellular traps in rheumatoid arthritis and systemic lupus erythematosus. Front Immunol. 2019; 10: 423.
- 88Pieterse 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; 77: 1790-1798.
- 89Knuckley B, Luo Y, Thompson PR. Profiling protein arginine deiminase 4 (PAD4): a novel screen to identify PAD4 inhibitors. Bioorg Med Chem. 2008; 16: 739-745.
- 90Foulquier C, Sebbag M, Clavel C, et al. Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation. Arthritis Rheum. 2007; 56: 3541-3553.
- 91Kinloch A, Lundberg K, Wait R, et al. Synovial fluid is a site of citrullination of autoantigens in inflammatory arthritis. Arthritis Rheum. 2008; 58: 2287-2295.
- 92Paoliello-Paschoalato AB, Marchi LF, de Andrade MF, Kabeya LM, Donadi EA, Lucisano-Valim YM. Fcγ and complement receptors and complement proteins in neutrophil activation in rheumatoid arthritis: contribution to pathogenesis and progression and modulation by natural products. Evid Based Complement Alternat Med. 2015; 2015:429878.
- 93Kilsgård O, Andersson P, Malmsten M, et al. Peptidylarginine deiminases present in the airways during tobacco smoking and inflammation can citrullinate the host defense peptide LL-37, resulting in altered activities. Am J Respir Cell Mol Biol. 2012; 46: 240-248.
- 94Dwivedi N, Upadhyay J, Neeli I, et al. Felty's syndrome autoantibodies bind to deiminated histones and neutrophil extracellular chromatin traps. Arthritis Rheum. 2012; 64: 982-992.
- 95Corsiero E, Bombardieri M, Carlotti E, et al. Single cell cloning and recombinant monoclonal antibodies generation from RA synovial B cells reveal frequent targeting of citrullinated histones of NETs. Ann Rheum Dis. 2016; 75: 1866-1875.
- 96Carmona-Rivera C, Carlucci PM, Moore E, et al. Synovial fibroblast-neutrophil interactions promote pathogenic adaptive immunity in rheumatoid arthritis. Sci Immunol. 2017; 2:eaag3358.
- 97Kenny EF, Herzig A, Krüger R, et al. Diverse stimuli engage different neutrophil extracellular trap pathways. Elife. 2017; 6:e24437.
- 98Rasheed Z. Hydroxyl radical damaged immunoglobulin G in patients with rheumatoid arthritis: biochemical and immunological studies. Clin Biochem. 2008; 41: 663-669.
- 99Abimannan T, Peroumal D, Parida JR, Barik PK, Padhan P, Devadas S. Oxidative stress modulates the cytokine response of differentiated Th17 and Th1 cells. Free Radic Biol Med. 2016; 99: 352-363.
- 100Knight JS, Luo W, O'Dell AA, et al. Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis. Circ Res. 2014; 114: 947-956.
- 101Koushik S, Joshi N, Nagaraju S, et al. PAD4: pathophysiology, current therapeutics and future perspective in rheumatoid arthritis. Expert Opin Ther Targets. 2017; 21: 433-447.
- 102Lewis HD, Liddle J, Coote JE, et al. Inhibition of PAD4 activity is sufficient to disrupt mouse and human NET formation. Nat Chem Biol. 2015; 11: 189-191.
- 103Li M, Lin C, Deng H, et al. A novel peptidylarginine deiminase 4 (PAD4) inhibitor BMS-P5 blocks formation of neutrophil extracellular traps and delays progression of multiple myeloma. Mol Cancer Ther. 2020; 19: 1530-1538.
- 104Watts RA, Hatemi G, Burns JC, Mohammad AJ. Global epidemiology of vasculitis. Nat Rev Rheumatol. 2022; 18: 22-34.
- 105Mayer-Hain S, Gebhardt K, Neufeld M, et al. Systemic activation of neutrophils by immune complexes is critical to IgA Vasculitis. J Immunol. 2022; 209: 1048-1058.
- 106Michailidou D, Kuley R, Wang T, et al. Neutrophil extracellular trap formation in anti-neutrophil cytoplasmic antibody-associated and large-vessel vasculitis. Clin Immunol. 2023; 249: 109274.
- 107Gill C, Sturman J, Ozbek L, et al. Cocaine-induced granulomatosis with polyangiitis – an under-recognized condition. Rheumatol Adv Pract. 2023; 7:rkad027.
- 108Takeuchi H, Kawasaki T, Shigematsu K, Kawamura K, Oka N. Neutrophil extracellular traps in neuropathy with anti-neutrophil cytoplasmic autoantibody-associated microscopic polyangiitis. Clin Rheumatol. 2017; 36: 913-917.
- 109Söderberg D, Segelmark M. Neutrophil extracellular traps in ANCA-associated vasculitis. Front Immunol. 2016; 7: 256.
- 110Pruchniak MP, Ostafin M, Wachowska M, et al. Neutrophil extracellular traps generation and degradation in patients with granulomatosis with polyangiitis and systemic lupus erythematosus. Autoimmunity. 2019; 52: 126-135.
- 111Grayson PC, Carmona-Rivera C, Xu L, et al. Neutrophil-related gene expression and low-density granulocytes associated with disease activity and response to treatment in antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol. 2015; 67: 1922-1932.
- 112Nakazawa D, Shida H, Tomaru U, et al. Enhanced formation and disordered regulation of NETs in myeloperoxidase-ANCA-associated microscopic polyangiitis. J Am Soc Nephrol. 2014; 25: 990-997.
- 113Schreiber A, Rousselle A, Becker JU, von Mässenhausen A, Linkermann A, Kettritz R. Necroptosis controls NET generation and mediates complement activation, endothelial damage, and autoimmune vasculitis. Proc Natl Acad Sci USA. 2017; 114: E9618-E9625.
- 114Sha LL, Wang H, Wang C, Peng HY, Chen M, Zhao MH. Autophagy is induced by anti-neutrophil cytoplasmic Abs and promotes neutrophil extracellular traps formation. Innate Immun. 2016; 22: 658-665.
- 115Tang S, Zhang Y, Yin SW, et al. Neutrophil extracellular trap formation is associated with autophagy-related signalling in ANCA-associated vasculitis. Clin Exp Immunol. 2015; 180: 408-418.
- 116Remijsen Q, Vanden Berghe T, Wirawan E, et al. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res. 2011; 21: 290-304.
- 117Hayden H, Ibrahim N, Klopf J, et al. ELISA detection of MPO-DNA complexes in human plasma is error-prone and yields limited information on neutrophil extracellular traps formed in vivo. PLoS One. 2021; 16:e0250265.
- 118Kessenbrock K, Krumbholz M, Schönermarck U, et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med. 2009; 15: 623-625.
- 119Sangaletti S, Tripodo C, Chiodoni C, et al. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood. 2012; 120: 3007-3018.
- 120Falk RJ, Terrell RS, Charles LA, Jennette JC. Anti-neutrophil cytoplasmic autoantibodies induce neutrophils to degranulate and produce oxygen radicals in vitro. Proc Natl Acad Sci USA. 1990; 87: 4115-4119.
- 121Al-Moujahed A, Tian B, Efstathiou NE, et al. Receptor interacting protein kinase 3 (RIP3) regulates iPSCs generation through modulating cell cycle progression genes. Stem Cell Res. 2019; 35:101387.
- 122Korkmaz B, Horwitz MS, Jenne DE, Gauthier F. Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol Rev. 2010; 62: 726-759.
- 123Kumar SV, Kulkarni OP, Mulay SR, et al. Neutrophil extracellular trap-related extracellular histones cause vascular necrosis in severe GN. J Am Soc Nephrol. 2015; 26: 2399-2413.
- 124Pieterse E, Rother N, Garsen M, et al. Neutrophil extracellular traps drive endothelial-to-mesenchymal transition. Arterioscler Thromb Vasc Biol. 2017; 37: 1371-1379.
- 125Lin F, Wang N, Zhang TC. The role of endothelial-mesenchymal transition in development and pathological process. IUBMB Life. 2012; 64: 717-723.
- 126Jiang D, Muschhammer J, Qi Y, et al. Suppression of neutrophil-mediated tissue damage – a novel skill of mesenchymal stem cells. Stem Cells. 2016; 34: 2393-2406.
- 127Invernizzi P, Mackay IR. Autoimmune liver diseases. World J Gastroenterol. 2008; 14: 3290-3291.
- 128Eksteen B, Afford SC, Wigmore SJ, Holt AP, Adams DH. Immune-mediated liver injury. Semin Liver Dis. 2007; 27: 351-366.
- 129Mieli-Vergani G, Vergani D. Autoimmune hepatitis. Nat Rev Gastroenterol Hepatol. 2011; 8: 320-329.
- 130Kerkar N, Vergani D. De novo autoimmune hepatitis – is this different in adults compared to children? J Autoimmun. 2018; 95: 26-33.
- 131Invernizzi P, Selmi C, Ranftler C, Podda M, Wesierska-Gadek J. Antinuclear antibodies in primary biliary cirrhosis. Semin Liver Dis. 2005; 25: 298-310.
- 132Domerecka W, Homa-Mlak I, Mlak R, et al. Indicator of inflammation and NETosis-low-density granulocytes as a biomarker of autoimmune hepatitis. J Clin Med. 2022; 11:2174.
- 133Apel F, Andreeva L, Knackstedt LS, et al. The cytosolic DNA sensor cGAS recognizes neutrophil extracellular traps. Sci Signal. 2021; 14:eaax7942.
- 134Rawat A, Bhattad S, Singh S. Chronic granulomatous disease. Indian J Pediatr. 2016; 83: 345-353.
- 135Ravindran M, Khan MA, Palaniyar N. Neutrophil extracellular trap formation: physiology, pathology, and pharmacology. Biomolecules. 2019; 9: 365.
- 136Selmi C, Bowlus CL, Gershwin ME, Coppel RL. Primary biliary cirrhosis. Lancet. 2011; 377: 1600-1609.
- 137Kaplan MM, Gershwin ME. Primary biliary cirrhosis. N Engl J Med. 2005; 353: 1261-1273.
- 138Carstens PO, Schmidt J. Diagnosis, pathogenesis and treatment of myositis: recent advances. Clin Exp Immunol. 2014; 175: 349-358.
- 139Schmidt J. Current classification and management of inflammatory myopathies. J Neuromuscul Dis. 2018; 5: 109-129.
- 140Moon SJ, Jung SM, Baek IW, Park KS, Kim KJ. Molecular signature of neutrophil extracellular trap mediating disease module in idiopathic inflammatory myopathy. J Autoimmun. 2023; 138:103063.
- 141Zhang S, Shu X, Tian X, Chen F, Lu X, Wang G. Enhanced formation and impaired degradation of neutrophil extracellular traps in dermatomyositis and polymyositis: a potential contributor to interstitial lung disease complications. Clin Exp Immunol. 2014; 177: 134-141.
- 142Peng Y, Zhang S, Zhao Y, Liu Y, Yan B. Neutrophil extracellular traps may contribute to interstitial lung disease associated with anti-MDA5 autoantibody positive dermatomyositis. Clin Rheumatol. 2018; 37: 107-115.
- 143Zhang S, Jia X, Zhang Q, et al. Neutrophil extracellular traps activate lung fibroblast to induce polymyositis-related interstitial lung diseases via TLR9-miR-7-Smad2 pathway. J Cell Mol Med. 2020; 24: 1658-1669.
- 144Zhang S, Shu X, Tian X, Chen F, Lu X, Wang G. Enhanced formation and impaired degradation of neutrophil extracellular traps in dermatomyositis and polymyositis: a potential contributor to interstitial lung disease complications. Clin Exp Immunol. 2014; 177(1): 134-141.
- 145Ma W, Zhu J, Bai L, Zhao P, Li F, Zhang S. The role of neutrophil extracellular traps and proinflammatory damage-associated molecular patterns in idiopathic inflammatory myopathies. Clin Exp Immunol. 2023; 213: 202-208.
- 146Duvvuri B, Pachman LM, Morgan G, et al. Neutrophil extracellular traps in tissue and periphery in juvenile dermatomyositis. Arthritis Rheumatol. 2020; 72: 348-358.
- 147Troyanov Y, Targoff IN, Tremblay JL, Goulet JR, Raymond Y, Senécal JL. Novel classification of idiopathic inflammatory myopathies based on overlap syndrome features and autoantibodies: analysis of 100 French Canadian patients. Medicine. 2005; 84: 231-249.
- 148Allenbach Y, Benveniste O. Usefulness of autoantibodies for the diagnosis of autoimmune myopathies. Rev Neurol. 2013; 169: 656-662.
- 149Benveniste O, Stenzel W, Allenbach Y. Advances in serological diagnostics of inflammatory myopathies. Curr Opin Neurol. 2016; 29: 662-673.
- 150Mariampillai K, Granger B, Amelin D, et al. Development of a new classification system for idiopathic inflammatory myopathies based on clinical manifestations and myositis-specific autoantibodies. JAMA Neurol. 2018; 75: 1528-1537.
- 151Seto N, Torres-Ruiz JJ, Carmona-Rivera C, et al. Neutrophil dysregulation is pathogenic in idiopathic inflammatory myopathies. JCI Insight. 2020; 5:e134189.
- 152Lawrence SM, Corriden R, Nizet V. How neutrophils meet their end. Trends Immunol. 2020; 41: 531-544.
- 153Stenberg A, Sehlin J, Oldenborg PA. Neutrophil apoptosis is associated with loss of signal regulatory protein alpha (SIRPα) from the cell surface. J Leukoc Biol. 2013; 93: 403-412.
- 154Noseykina EM, Schepetkin IA, Atochin DN. Molecular mechanisms for regulation of neutrophil apoptosis under normal and pathological conditions. J Evol Biochem Physiol. 2021; 57: 429-450.
- 155Krysko DV, Vanden Berghe T, Parthoens E, D'Herde K, Vandenabeele P. Methods for distinguishing apoptotic from necrotic cells and measuring their clearance. Methods Enzymol. 2008; 442: 307-341.
- 156Jorgensen I, Rayamajhi M, Miao EA. Programmed cell death as a defence against infection. Nat Rev Immunol. 2017; 17: 151-164.
- 157Krüger K, Mooren FC. Exercise-induced leukocyte apoptosis. Exerc Immunol Rev. 2014; 20: 117-134.
- 158Thieblemont N, Wright HL, Edwards SW, Witko-Sarsat V. Human neutrophils in auto-immunity. Semin Immunol. 2016; 28: 159-173.
- 159Fox S, Leitch AE, Duffin R, Haslett C, Rossi AG. Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J Innate Immun. 2010; 2: 216-227.
- 160Gabelloni ML, Trevani AS, Sabatté J, Geffner J. Mechanisms regulating neutrophil survival and cell death. Semin Immunopathol. 2013; 35: 423-437.
- 161Milot E, Filep JG. Regulation of neutrophil survival/apoptosis by Mcl-1. ScientificWorldJournal. 2011; 11: 1948-1962.
- 162Dąbrowska D, Jabłońska E, Iwaniuk A, Garley M. Many ways-one destination: different types of neutrophils death. Int Rev Immunol. 2019; 38: 18-32.
- 163Akgul C, Moulding DA, Edwards SW. Molecular control of neutrophil apoptosis. FEBS Lett. 2001; 487: 318-322.
- 164Filep JG, Ariel A. Neutrophil heterogeneity and fate in inflamed tissues: implications for the resolution of inflammation. Am J Physiol Cell Physiol. 2020; 319: C510-C532.
- 165Pérez-Figueroa E, Álvarez-Carrasco P, Ortega E, Maldonado-Bernal C. Neutrophils: many ways to die. Front Immunol. 2021; 12:631821.
- 166Griffiths HR, Gao D, Pararasa C. Redox regulation in metabolic programming and inflammation. Redox Biol. 2017; 12: 50-57.
- 167Martin KR, Ohayon D, Witko-Sarsat V. Promoting apoptosis of neutrophils and phagocytosis by macrophages: novel strategies in the resolution of inflammation. Swiss Med Wkly. 2015; 145:w14056.
- 168Bao L, Dou G, Tian R, et al. Engineered neutrophil apoptotic bodies ameliorate myocardial infarction by promoting macrophage efferocytosis and inflammation resolution. Bioact Mater. 2022; 9: 183-197.
- 169Courtney PA, Crockard AD, Williamson K, Irvine AE, Kennedy RJ, Bell AL. Increased apoptotic peripheral blood neutrophils in systemic lupus erythematosus: relations with disease activity, antibodies to double stranded DNA, and neutropenia. Ann Rheum Dis. 1999; 58: 309-314.
- 170Midgley A, McLaren Z, Moots RJ, Edwards SW, Beresford MW. The role of neutrophil apoptosis in juvenile-onset systemic lupus erythematosus. Arthritis Rheum. 2009; 60: 2390-2401.
- 171Midgley A, Thorbinson C, Beresford MW. Expression of toll-like receptors and their detection of nuclear self-antigen leading to immune activation in JSLE. Rheumatology (Oxford). 2012; 51: 824-832.
- 172Hu S, Yang X. Cellular inhibitor of apoptosis 1 and 2 are ubiquitin ligases for the apoptosis inducer Smac/DIABLO. J Biol Chem. 2003; 278: 10055-10060.
- 173Ren Y, Tang J, Mok MY, Chan AW, Wu A, Lau CS. Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum. 2003; 48: 2888-2897.
- 174Mikołajczyk TP, Skiba D, Batko B, et al. Characterization of the impairment of the uptake of apoptotic polymorphonuclear cells by monocyte subpopulations in systemic lupus erythematosus. Lupus. 2014; 23: 1358-1369.
- 175Cairns AP, Crockard AD, McConnell JR, Courtney PA, Bell AL. Reduced expression of CD44 on monocytes and neutrophils in systemic lupus erythematosus: relations with apoptotic neutrophils and disease activity. Ann Rheum Dis. 2001; 60: 950-955.
- 176Chiewchengchol D, Midgley A, Sodsai P, et al. The protective effect of GM-CSF on serum-induced neutrophil apoptosis in juvenile systemic lupus erythematosus patients. Clin Rheumatol. 2015; 34: 85-91.
- 177Midgley A, Mayer K, Edwards SW, Beresford MW. Differential expression of factors involved in the intrinsic and extrinsic apoptotic pathways in juvenile systemic lupus erythematosus. Lupus. 2011; 20: 71-79.
- 178Abeler-Dörner L, Rieger CC, Berger B, et al. Interferon-α abrogates the suppressive effect of apoptotic cells on dendritic cells in an in vitro model of systemic lupus erythematosus pathogenesis. J Rheumatol. 2013; 40: 1683-1696.
- 179Ballantine L, Midgley A, Harris D, Richards E, Burgess S, Beresford MW. Increased soluble phagocytic receptors sMer, sTyro3 and sAxl and reduced phagocytosis in juvenile-onset systemic lupus erythematosus. Pediatr Rheumatol Online J. 2015; 13: 10.
- 180Wright HL, Lyon M, Chapman EA, Moots RJ, Edwards SW. Rheumatoid arthritis synovial fluid neutrophils drive inflammation through production of chemokines, reactive oxygen species, and neutrophil extracellular traps. Front Immunol. 2020; 11:584116.
- 181Wright HL, Chikura B, Bucknall RC, Moots RJ, Edwards SW. Changes in expression of membrane TNF, NF-{kappa}B activation and neutrophil apoptosis during active and resolved inflammation. Ann Rheum Dis. 2011; 70: 537-543.
- 182Wright HL, Bucknall RC, Moots RJ, Edwards SW. Analysis of SF and plasma cytokines provides insights into the mechanisms of inflammatory arthritis and may predict response to therapy. Rheumatology (Oxford). 2012; 51: 451-459.
- 183Cross A, Moots RJ, Edwards SW. The dual effects of TNFalpha on neutrophil apoptosis are mediated via differential effects on expression of Mcl-1 and Bfl-1. Blood. 2008; 111: 878-884.
- 184Cross A, Barnes T, Bucknall RC, Edwards SW, Moots RJ. Neutrophil apoptosis in rheumatoid arthritis is regulated by local oxygen tensions within joints. J Leukoc Biol. 2006; 80: 521-528.
- 185Walmsley SR, Print C, Farahi N, et al. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J Exp Med. 2005; 201: 105-115.
- 186Elks PM, van Eeden FJ, Dixon G, et al. Activation of hypoxia-inducible factor-1α (Hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model. Blood. 2011; 118: 712-722.
- 187Kaplan MJ. Role of neutrophils in systemic autoimmune diseases. Arthritis Res Ther. 2013; 15: 219.
- 188Hu J, Huang Z, Yu M, Zhang P, Xia Z, Gao C. Caspase-8 activation in neutrophils facilitates autoimmune kidney vasculitis through regulating CD4(+) effector memory T cells. Front Immunol. 2022; 13: 1038134.
- 189Kallenberg CG. Dying neutrophils in ANCA-associated vasculitis: good or bad guys? Kidney Int. 2002; 61: 758-759.
- 190Harper L, Cockwell P, Adu D, Savage CO. Neutrophil priming and apoptosis in anti-neutrophil cytoplasmic autoantibody-associated vasculitis. Kidney Int. 2001; 59: 1729-1738.
- 191Witko-Sarsat V, Daniel S, Noël LH, Mouthon L. Neutrophils and B lymphocytes in ANCA-associated vasculitis. APMIS Suppl. 2009; 127: 27-31.
- 192Durant S, Pederzoli M, Lepelletier Y, et al. Apoptosis-induced proteinase 3 membrane expression is independent from degranulation. J Leukoc Biol. 2004; 75: 87-98.
- 193Kantari C, Pederzoli-Ribeil M, Amir-Moazami O, et al. Proteinase 3, the Wegener autoantigen, is externalized during neutrophil apoptosis: evidence for a functional association with phospholipid scramblase 1 and interference with macrophage phagocytosis. Blood. 2007; 110: 4086-4095.
- 194Tacnet-Delorme P, Gabillet J, Chatfield S, Thieblemont N, Frachet P, Witko-Sarsat V. Proteinase 3 interferes with C1q-mediated clearance of apoptotic cells. Front Immunol. 2018; 9: 818.
- 195Witko-Sarsat V, Thieblemont N. Granulomatosis with polyangiitis (Wegener granulomatosis): a proteinase-3 driven disease? Joint Bone Spine. 2018; 85: 185-189.
- 196Wang LY, Wang RX, Wang C, et al. Inhibitor of apoptosis proteins antagonist SM164 ameliorates experimental MPO-ANCA-associated vasculitis via enhancing fatty acid oxidation in neutrophils. Rheumatology (Oxford). 2023; 62: 2563-2573.
- 197Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010; 221: 3-12.
- 198Bhattacharya A, Wei Q, Shin JN, et al. Autophagy is required for neutrophil-mediated inflammation. Cell Rep. 2015; 12: 1731-1739.
- 199Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004; 15: 1101-1111.
- 200Bakema JE, Ganzevles SH, Fluitsma DM, et al. Targeting FcαRI on polymorphonuclear cells induces tumor cell killing through autophagy. J Immunol. 2011; 187: 726-732.
- 201Shatz O, Elazar Z. Autophagy in a nutshell. FEBS Lett. 2023. doi:10.1002/1873-3468.14679. Advance online publication.
- 202Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011; 147: 728-741.
- 203Zhao YG, Chen Y, Miao G, et al. The ER-localized transmembrane protein EPG-3/VMP1 regulates SERCA activity to control ER-isolation membrane contacts for autophagosome formation. Mol Cell. 2017; 67: 974-989.e6.
- 204Matoba K, Kotani T, Tsutsumi A, et al. Atg9 is a lipid scramblase that mediates autophagosomal membrane expansion. Nat Struct Mol Biol. 2020; 27: 1185-1193.
- 205Rožman S, Yousefi S, Oberson K, Kaufmann T, Benarafa C, Simon HU. The generation of neutrophils in the bone marrow is controlled by autophagy. Cell Death Differ. 2015; 22: 445-456.
- 206Levine B, Kroemer G. Biological functions of autophagy genes: a disease perspective. Cell. 2019; 176: 11-42.
- 207Li X, He S, Ma B. Autophagy and autophagy-related proteins in cancer. Mol Cancer. 2020; 19: 12.
- 208Reggiori F, Ungermann C. Autophagosome maturation and fusion. J Mol Biol. 2017; 429: 486-496.
- 209Tian X, Teng J, Chen J. New insights regarding SNARE proteins in autophagosome-lysosome fusion. Autophagy. 2021; 17: 2680-2688.
- 210Lőrincz P, Juhász G. Autophagosome-lysosome fusion. J Mol Biol. 2020; 432: 2462-2482.
- 211Delgado MA, Elmaoued RA, Davis AS, Kyei G, Deretic V. Toll-like receptors control autophagy. EMBO J. 2008; 27: 1110-1121.
- 212Mitroulis I, Kourtzelis I, Kambas K, et al. Regulation of the autophagic machinery in human neutrophils. Eur J Immunol. 2010; 40: 1461-1472.
- 213Podestà MA, Faravelli I, Ponticelli C. Autophagy in lupus nephritis: a delicate balance between regulation and disease. Autoimmun Rev. 2022; 21:103132.
- 214Maugeri N, Capobianco A, Rovere-Querini P, et al. Platelet microparticles sustain autophagy-associated activation of neutrophils in systemic sclerosis. Sci Transl Med. 2018; 10:eaao3089.
- 215Maugeri N, Campana L, Gavina M, et al. Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps. J Thromb Haemost. 2014; 12: 2074-2088.
- 216Mao C, Xu X, Ding Y, Xu N. Optimization of BCG therapy targeting neutrophil extracellular traps, autophagy, and miRNAs in bladder cancer: implications for personalized medicine. Front Med. 2021; 8:735590.
- 217An Q, Yan W, Zhao Y, Yu K. Enhanced neutrophil autophagy and increased concentrations of IL-6, IL-8, IL-10 and MCP-1 in rheumatoid arthritis. Int Immunopharmacol. 2018; 65: 119-128.
- 218Degterev A, Huang Z, Boyce M, et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol. 2005; 1: 112-119.
- 219Pasparakis M, Vandenabeele P. Necroptosis and its role in inflammation. Nature. 2015; 517: 311-320.
- 220Zhang DW, Shao J, Lin J, et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science. 2009; 325: 332-336.
- 221Lentini G, Famà A, De Gaetano GV, et al. Caspase-8 inhibition improves the outcome of bacterial infections in mice by promoting neutrophil activation. Cell Rep Med. 2023; 4:101098.
- 222Wang X, He Z, Liu H, Yousefi S, Simon HU. Neutrophil necroptosis is triggered by ligation of adhesion molecules following GM-CSF priming. J Immunol. 2016; 197: 4090-4100.
- 223Dondelinger Y, Jouan-Lanhouet S, Divert T, et al. NF-κB-independent role of IKKα/IKKβ in preventing RIPK1 kinase-dependent apoptotic and necroptotic cell death during TNF signaling. Mol Cell. 2015; 60: 63-76.
- 224Sun L, Wang H, Wang Z, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012; 148: 213-227.
- 225Wang X, Gessier F, Perozzo R, et al. RIPK3-MLKL-mediated neutrophil death requires concurrent activation of fibroblast activation protein-α. J Immunol. 2020; 205: 1653-1663.
- 226Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012; 149: 1060-1072.
- 227Kim R, Taylor D, Vonderheide RH, Gabrilovich DI. Ferroptosis of immune cells in the tumor microenvironment. Trends Pharmacol Sci. 2023; 44: 542-552.
- 228Xie Y, Hou W, Song X, et al. Ferroptosis: process and function. Cell Death Differ. 2016; 23: 369-379.
- 229Peng Q, Peng G, Wu L, et al. Photo-reduction enables catalyst regeneration in Fenton reaction on an Fe(2)O(3)-decorated TiO(2) nanotube-based photocatalyst. Dalton Trans. 2020; 49: 6730-6737.
- 230Kim R, Hashimoto A, Markosyan N, et al. Ferroptosis of tumour neutrophils causes immune suppression in cancer. Nature. 2022; 612: 338-346.
- 231Li P, Jiang M, Li K, et al. Glutathione peroxidase 4-regulated neutrophil ferroptosis induces systemic autoimmunity. Nat Immunol. 2021; 22: 1107-1117.
- 232Ying Y, Padanilam BJ. Regulation of necrotic cell death: p53, PARP1 and cyclophilin D-overlapping pathways of regulated necrosis? Cell Mol Life Sci. 2016; 73: 2309-2324.
- 233Syntichaki P, Tavernarakis N. Death by necrosis. Uncontrollable catastrophe, or is there order behind the chaos? EMBO Rep. 2002; 3: 604-609.
- 234Vanlangenakker N, Vanden Berghe T, Krysko DV, Festjens N, Vandenabeele P. Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med. 2008; 8: 207-220.
- 235Galluzzi L, Bravo-San Pedro JM, Vitale I, et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 2015; 22: 58-73.
- 236Festjens N, Vanden Berghe T, Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta. 2006; 1757: 1371-1387.
- 237Fulda S. Cross talk between cell death regulation and metabolism. Methods Enzymol. 2014; 542: 81-90.
- 238Bano D, Young KW, Guerin CJ, et al. Cleavage of the plasma membrane Na+/Ca2+ exchanger in excitotoxicity. Cell. 2005; 120: 275-285.
- 239Vandenabeele P, Declercq W, Vanden Berghe T. Necrotic cell death and ‘necrostatins’: now we can control cellular explosion. Trends Biochem Sci. 2008; 33: 352-355.
- 240Ricci MS, Zong WX. Chemotherapeutic approaches for targeting cell death pathways. Oncologist. 2006; 11: 342-357.
- 241Li M, Carpio DF, Zheng Y, et al. An essential role of the NF-kappa B/toll-like receptor pathway in induction of inflammatory and tissue-repair gene expression by necrotic cells. J Immunol. 2001; 166: 7128-7135.
- 242Smith CK, Kaplan MJ. The role of neutrophils in the pathogenesis of systemic lupus erythematosus. Curr Opin Rheumatol. 2015; 27: 448-453.
- 243Feierl E, Smolen JS, Karonitsch T, et al. Engulfed cell remnants, and not cells undergoing apoptosis, constitute the LE-cell phenomenon. Autoimmunity. 2007; 40: 315-321.
- 244Singhal A, Kumar S. Neutrophil and remnant clearance in immunity and inflammation. Immunology. 2022; 165: 22-43.
- 245Mankan AK, Dau T, Jenne D, Hornung V. The NLRP3/ASC/Caspase-1 axis regulates IL-1β processing in neutrophils. Eur J Immunol. 2012; 42: 710-715.
- 246Jorgensen I, Miao EA. Pyroptotic cell death defends against intracellular pathogens. Immunol Rev. 2015; 265: 130-142.
- 247Cho JS, Guo Y, Ramos RI, et al. Neutrophil-derived IL-1β is sufficient for abscess formation in immunity against Staphylococcus aureus in mice. PLoS Pathog. 2012; 8:e1003047.
- 248Sollberger G. Approaching neutrophil pyroptosis. J Mol Biol. 2022; 434:167335.
- 249He WT, Wan H, Hu L, et al. Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 2015; 25: 1285-1298.
- 250Sborgi L, Rühl S, Mulvihill E, et al. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 2016; 35: 1766-1778.
- 251Shi J, Zhao Y, Wang K, et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature. 2015; 526: 660-665.
- 252Zhang Z, Jin L, Liu L, Zhou M, Zhang X, Zhang L. The intricate relationship between autoimmunity disease and neutrophils death patterns: a love-hate story. Apoptosis. 2023; 28: 1259-1284.
- 253Yi YS. Role of inflammasomes in inflammatory autoimmune rheumatic diseases. Korean J Physiol Pharmacol. 2018; 22: 1-15.
- 254Tan AL, Marzo-Ortega H, O'Connor P, Fraser A, Emery P, McGonagle D. Efficacy of anakinra in active ankylosing spondylitis: a clinical and magnetic resonance imaging study. Ann Rheum Dis. 2004; 63: 1041-1045.
- 255Huang W, Jiao J, Liu J, et al. MFG-E8 accelerates wound healing in diabetes by regulating “NLRP3 inflammasome-neutrophil extracellular traps” axis. Cell Death Discov. 2020; 6: 84.
- 256Hu Q, Shi H, Zeng T, et al. Increased neutrophil extracellular traps activate NLRP3 and inflammatory macrophages in adult-onset Still's disease. Arthritis Res Ther. 2019; 21: 9.
Citing Literature
