Cell type-specific molecular mechanisms and implications of necroptosis in inflammatory respiratory diseases
Ying Guo
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai, Shandong, China
Search for more papers by this authorJin Zhou
Key Laboratory of Spatiotemporal Single-Cell Technologies and Translational Medicine, Yantai, Shandong, China
Department of Endocrinology, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Search for more papers by this authorYaqi Wang
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Search for more papers by this authorXueliang Wu
Department of General Surgery, The First Affiliated Hospital of Hebei North University, Zhangjiakou, Hebei, China
Tumor Research Institute, The First Affiliated Hospital of Hebei North University, Zhangjiakou, Hebei, China
Search for more papers by this authorCorresponding Author
Yakui Mou
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai, Shandong, China
Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai, Shandong, China
Correspondence
Xicheng Song and Yakui Mou, Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai 264000, Shandong, China.
Email: [email protected] and [email protected]
Search for more papers by this authorCorresponding Author
Xicheng Song
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Key Laboratory of Spatiotemporal Single-Cell Technologies and Translational Medicine, Yantai, Shandong, China
Correspondence
Xicheng Song and Yakui Mou, Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai 264000, Shandong, China.
Email: [email protected] and [email protected]
Search for more papers by this authorYing Guo
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai, Shandong, China
Search for more papers by this authorJin Zhou
Key Laboratory of Spatiotemporal Single-Cell Technologies and Translational Medicine, Yantai, Shandong, China
Department of Endocrinology, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Search for more papers by this authorYaqi Wang
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Search for more papers by this authorXueliang Wu
Department of General Surgery, The First Affiliated Hospital of Hebei North University, Zhangjiakou, Hebei, China
Tumor Research Institute, The First Affiliated Hospital of Hebei North University, Zhangjiakou, Hebei, China
Search for more papers by this authorCorresponding Author
Yakui Mou
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Shandong Provincial Clinical Research Center for Otorhinolaryngologic Diseases, Yantai, Shandong, China
Yantai Key Laboratory of Otorhinolaryngologic Diseases, Yantai, Shandong, China
Correspondence
Xicheng Song and Yakui Mou, Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai 264000, Shandong, China.
Email: [email protected] and [email protected]
Search for more papers by this authorCorresponding Author
Xicheng Song
Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai, Shandong, China
Key Laboratory of Spatiotemporal Single-Cell Technologies and Translational Medicine, Yantai, Shandong, China
Correspondence
Xicheng Song and Yakui Mou, Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital of Qingdao University, Yantai 264000, Shandong, China.
Email: [email protected] and [email protected]
Search for more papers by this authorYing Guo and Jin Zhou contributed equally to this work.
This article is part of a series of reviews covering Mechanisms of programmed cell death appearing in Volume 321 of Immunological Reviews.
Summary
Necroptosis is generally considered as an inflammatory cell death form. The core regulators of necroptotic signaling are receptor-interacting serine–threonine protein kinases 1 (RIPK1) and RIPK3, and the executioner, mixed lineage kinase domain-like pseudokinase (MLKL). Evidence demonstrates that necroptosis contributes profoundly to inflammatory respiratory diseases that are common public health problem. Necroptosis occurs in nearly all pulmonary cell types in the settings of inflammatory respiratory diseases. The influence of necroptosis on cells varies depending upon the type of cells, tissues, organs, etc., which is an important factor to consider. Thus, in this review, we briefly summarize the current state of knowledge regarding the biology of necroptosis, and focus on the key molecular mechanisms that define the necroptosis status of specific cell types in inflammatory respiratory diseases. We also discuss the clinical potential of small molecular inhibitors of necroptosis in treating inflammatory respiratory diseases, and describe the pathological processes that engage cross talk between necroptosis and other cell death pathways in the context of respiratory inflammation. The rapid advancement of single-cell technologies will help understand the key mechanisms underlying cell type-specific necroptosis that are critical to effectively treat pathogenic lung infections and inflammatory respiratory diseases.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
REFERENCES
- 1Xi Y, Chen L, Tang J, Yu B, Shen W, Niu X. Amplifying "eat me signal" by immunogenic cell death for potentiating cancer immunotherapy. Immunol Rev. 2023.
- 2Li S, Wang A, Wu Y, et al. Targeted therapy for non-small-cell lung cancer: new insights into regulated cell death combined with immunotherapy. Immunol Rev. 2023.
- 3Li L, Li T, Qu X, Sun G, Fu Q, Han G. Stress/cell death pathways, neuroinflammation, and neuropathic pain. Immunol Rev. 2023.
- 4Degterev A, Hitomi J, Germscheid M, et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol. 2008; 4(5): 313-321.
- 5Degterev 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(2): 112-119.
- 6Zhou W, Yuan J. SnapShot: necroptosis. Cell. 2014; 158(2): 464.e461.
- 7Horne CR, Samson AL, Murphy JM. The web of death: the expanding complexity of necroptotic signaling. Trends Cell Biol. 2023; 33(2): 162-174.
- 8Daniels BP, Snyder AG, Olsen TM, et al. RIPK3 restricts viral pathogenesis via cell death-independent neuroinflammation. Cell. 2017; 169(2): 301-313.e311.
- 9Rickard JA, O'Donnell JA, Evans JM, et al. RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis. Cell. 2014; 157(5): 1175-1188.
- 10Sun L, Wang H, Wang Z, et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 2012; 148(1–2): 213-227.
- 11Vucur M, Ghallab A, Schneider AT, et al. Sublethal necroptosis signaling promotes inflammation and liver cancer. Immunity. 2023; 56(7): 1578-1595.e1578.
- 12Fritsch M, Günther SD, Schwarzer R, et al. Caspase-8 is the molecular switch for apoptosis, necroptosis and pyroptosis. Nature. 2019; 575(7784): 683-687.
- 13De Giovanni M, Chen H, Li X, Cyster JG. GPR35 and mediators from platelets and mast cells in neutrophil migration and inflammation. Immunol Rev. 2023; 317(1): 187-202.
- 14Newton K, Dixit VM, Kayagaki N. Dying cells fan the flames of inflammation. Science. 2021; 374(6571): 1076-1080.
- 15Hiemstra PS, McCray PB Jr, Bals R. The innate immune function of airway epithelial cells in inflammatory lung disease. Eur Respir J. 2015; 45(4): 1150-1162.
- 16Tang D, Kang R, Berghe TV, Vandenabeele P, Kroemer G. The molecular machinery of regulated cell death. Cell Res. 2019; 29(5): 347-364.
- 17Mompeán M, Li W, Li J, et al. The structure of the Necrosome RIPK1-RIPK3 Core, a human hetero-amyloid signaling complex. Cell. 2018; 173(5): 1244-1253.e1210.
- 18Hadian K, Stockwell BR. The therapeutic potential of targeting regulated non-apoptotic cell death. Nat Rev Drug Discov. 2023; 22: 723-742.
- 19Messaoud-Nacer Y, Culerier E, Rose S, et al. STING agonist diABZI induces PANoptosis and DNA mediated acute respiratory distress syndrome (ARDS). Cell Death Dis. 2022; 13(3): 269.
- 20Schneider AT, Gautheron J, Feoktistova M, et al. RIPK1 suppresses a TRAF2-dependent pathway to liver cancer. Cancer Cell. 2017; 31(1): 94-109.
- 21Annibaldi A, Wicky John S, Vanden Berghe T, et al. Ubiquitin-mediated regulation of RIPK1 kinase activity independent of IKK and MK2. Mol Cell. 2018; 69(4): 566-580.e565.
- 22Legarda D, Justus SJ, Ang RL, et al. CYLD proteolysis protects macrophages from TNF-mediated auto-necroptosis induced by LPS and licensed by type I IFN. Cell Rep. 2016; 15(11): 2449-2461.
- 23Ang RL, Chan M, Legarda D, et al. Immune dysregulation in SHARPIN-deficient mice is dependent on CYLD-mediated cell death. Proc Natl Acad Sci USA. 2021; 118(50): e2001602118.
- 24Lee EW, Kim JH, Ahn YH, et al. Ubiquitination and degradation of the FADD adaptor protein regulate death receptor-mediated apoptosis and necroptosis. Nat Commun. 2012; 3: 978.
- 25Newton K, Wickliffe KE, Dugger DL, et al. Cleavage of RIPK1 by caspase-8 is crucial for limiting apoptosis and necroptosis. Nature. 2019; 574(7778): 428-431.
- 26Füllsack S, Rosenthal A, Wajant H, Siegmund D. Redundant and receptor-specific activities of TRADD, RIPK1 and FADD in death receptor signaling. Cell Death Dis. 2019; 10(2): 122.
- 27Tenev T, Bianchi K, Darding M, et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol Cell. 2011; 43(3): 432-448.
- 28Vandenabeele P, Bultynck G, Savvides SN. Pore-forming proteins as drivers of membrane permeabilization in cell death pathways. Nat Rev Mol Cell Biol. 2023; 24(5): 312-333.
- 29Xie Y, Zhu S, Zhong M, et al. Inhibition of Aurora kinase a induces necroptosis in pancreatic carcinoma. Gastroenterology. 2017; 153(5): 1429-1443.e1425.
- 30Liu Z, Dagley LF, Shield-Artin K, et al. Oligomerization-driven MLKL ubiquitylation antagonizes necroptosis. EMBO J. 2021; 40(23):e103718.
- 31Guo R, Jia X, Ding Z, et al. Loss of MLKL ameliorates liver fibrosis by inhibiting hepatocyte necroptosis and hepatic stellate cell activation. Theranostics. 2022; 12(11): 5220-5236.
- 32Chen X, Li W, Ren J, et al. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res. 2014; 24(1): 105-121.
- 33Gitlin AD, Heger K, Schubert AF, et al. Integration of innate immune signalling by caspase-8 cleavage of N4BP1. Nature. 2020; 587(7833): 275-280.
- 34Speir M, Nowell CJ, Chen AA, et al. Ptpn6 inhibits caspase-8- and Ripk3/Mlkl-dependent inflammation. Nat Immunol. 2020; 21(1): 54-64.
- 35Newton K. RIPK1 and RIPK3: critical regulators of inflammation and cell death. Trends Cell Biol. 2015; 25(6): 347-353.
- 36Imanishi T, Unno M, Yoneda N, et al. RIPK1 blocks T cell senescence mediated by RIPK3 and caspase-8. Sci Adv. 2023; 9(4):eadd6097.
- 37Zhang T, Zhang Y, Cui M, et al. CaMKII is a RIP3 substrate mediating ischemia- and oxidative stress-induced myocardial necroptosis. Nat Med. 2016; 22(2): 175-182.
- 38Yuan G, Cao C, Cao D, et al. Receptor-interacting protein 3-phosphorylated Ca(2+) /calmodulin-dependent protein kinase II and mixed lineage kinase domain-like protein mediate intracerebral hemorrhage-induced neuronal necroptosis. J Neurochem. 2023; 164(1): 94-114.
- 39González-Juarbe N, Bradley KM, Shenoy AT, et al. Pore-forming toxin-mediated ion dysregulation leads to death receptor-independent necroptosis of lung epithelial cells during bacterial pneumonia. Cell Death Differ. 2017; 24(5): 917-928.
- 40Qu Y, Tang J, Wang H, et al. RIPK3 interactions with MLKL and CaMKII mediate oligodendrocytes death in the developing brain. Cell Death Dis. 2017; 8(2):e2629.
- 41He Y, Rofaani E, Huang X, et al. Generation of alveolar epithelium using reconstituted basement membrane and hiPSC-derived organoids. Adv Healthc Mater. 2022; 11(6):e2101972.
- 42Hu Q, Zhang S, Yang Y, et al. Extracellular vesicles in the pathogenesis and treatment of acute lung injury. Mil Med Res. 2022; 9(1): 61.
- 43Barnes PJ, Burney PG, Silverman EK, et al. Chronic obstructive pulmonary disease. Nat Rev Dis Primers. 2015; 1: 15076.
- 44Van Eeckhoutte HP, Donovan C, Kim RY, et al. RIPK1 kinase-dependent inflammation and cell death contribute to the pathogenesis of COPD. Eur Respir J. 2023; 61(4): 2201506.
- 45Chen D, Gregory AD, Li X, et al. RIP3-dependent necroptosis contributes to the pathogenesis of chronic obstructive pulmonary disease. JCI Insight. 2021; 6(12): e144689.
- 46Tan HT, Hagner S, Ruchti F, et al. Tight junction, mucin, and inflammasome-related molecules are differentially expressed in eosinophilic, mixed, and neutrophilic experimental asthma in mice. Allergy. 2019; 74(2): 294-307.
- 47Kato K, Lillehoj EP, Kim KC. MUC1 regulates epithelial inflammation and apoptosis by PolyI:C through inhibition of toll/IL-1 receptor-domain-containing adapter-inducing IFN-β (TRIF) recruitment to toll-like receptor 3. Am J Respir Cell Mol Biol. 2014; 51(3): 446-454.
- 48Iverson E, Griswold K, Song D, et al. Membrane-tethered mucin 1 is stimulated by interferon and virus infection in multiple cell types and inhibits influenza A virus infection in human airway epithelium. MBio. 2022; 13(4):e0105522.
- 49Zhang H, Ji J, Liu Q, Xu S. MUC1 downregulation promotes TNF-α-induced necroptosis in human bronchial epithelial cells via regulation of the RIPK1/RIPK3 pathway. J Cell Physiol. 2019; 234(9): 15080-15088.
- 50Zhang H, Liu Q, Kong L, Xu S. Mucin 1 downregulation impairs the anti-necroptotic effects of glucocorticoids in human bronchial epithelial cells. Life Sci. 2019; 221: 168-177.
- 51Lyons JD, Mandal P, Otani S, et al. The RIPK3 scaffold regulates lung inflammation during Pseudomonas aeruginosa pneumonia. Am J Respir Cell Mol Biol. 2023; 68(2): 150-160.
- 52Tummers B, Mari L, Guy CS, et al. Caspase-8-dependent inflammatory responses are controlled by its adaptor, FADD, and necroptosis. Immunity. 2020; 52(6): 994-1006.e1008.
- 53Oikonomou N, Schuijs MJ, Chatzigiagkos A, et al. Airway epithelial cell necroptosis contributes to asthma exacerbation in a mouse model of house dust mite-induced allergic inflammation. Mucosal Immunol. 2021; 14(5): 1160-1171.
- 54Brower RG, Matthay MA, Morris A, Schoenfeld D, Thompson BT, Wheeler A. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N Engl J Med. 2000; 342(18): 1301-1308.
- 55Hao Q, Shetty S, Tucker TA, Idell S, Tang H. Interferon-γ preferentially promotes necroptosis of lung epithelial cells by upregulating MLKL. Cells. 2022; 11(3): 563.
- 56Karki R, Sharma BR, Tuladhar S, et al. Synergism of TNF-α and IFN-γ triggers inflammatory cell death, tissue damage, and mortality in SARS-CoV-2 infection and cytokine shock syndromes. Cell. 2021; 184(1): 149-168.e117.
- 57Li X, Zhang Z, Wang Z, Gutiérrez-Castrellón P, Shi H. Cell deaths: involvement in the pathogenesis and intervention therapy of COVID-19. Signal Transduct Target Ther. 2022; 7(1): 186.
- 58Hao S, Ning K, Kuz CA, et al. SARS-CoV-2 infection of polarized human airway epithelium induces necroptosis that causes airway epithelial barrier dysfunction. J Med Virol. 2023; 95(9):e29076.
- 59Li S, Zhang Y, Guan Z, et al. SARS-CoV-2 triggers inflammatory responses and cell death through caspase-8 activation. Signal Transduct Target Ther. 2020; 5(1): 235.
- 60Coultas JA, Smyth R, Openshaw PJ. Respiratory syncytial virus (RSV): a scourge from infancy to old age. Thorax. 2019; 74(10): 986-993.
- 61Milési C, Essouri S, Pouyau R, et al. High flow nasal cannula (HFNC) versus nasal continuous positive airway pressure (nCPAP) for the initial respiratory management of acute viral bronchiolitis in young infants: a multicenter randomized controlled trial (TRAMONTANE study). Intensive Care Med. 2017; 43(2): 209-216.
- 62Raita Y, Pérez-Losada M, Freishtat RJ, et al. Integrated omics endotyping of infants with respiratory syncytial virus bronchiolitis and risk of childhood asthma. Nat Commun. 2021; 12(1): 3601.
- 63Cheemarla NR, Uche IK, McBride K, Naidu S, Guerrero-Plata A. In utero tobacco smoke exposure alters lung inflammation, viral clearance, and CD8(+) T-cell responses in neonatal mice infected with respiratory syncytial virus. Am J Physiol Lung Cell Mol Physiol. 2019; 317(2): L212-l221.
- 64Simpson J, Loh Z, Ullah MA, et al. Respiratory syncytial virus infection promotes necroptosis and HMGB1 release by airway epithelial cells. Am J Respir Crit Care Med. 2020; 201(11): 1358-1371.
- 65Simpson J, Spann KM, Phipps S. MLKL regulates rapid cell death-independent HMGB1 release in RSV infected airway epithelial cells. Front Cell Dev Biol. 2022; 10:890389.
- 66Zhang Z, Zheng Y, Chen Y, et al. Gut fungi enhances immunosuppressive function of myeloid-derived suppressor cells by activating PKM2-dependent glycolysis to promote colorectal tumorigenesis. Exp Hematol Oncol. 2022; 11(1): 88.
- 67Huang D, Han Y, Tang T, et al. Dlk1 maintains adult mice long-term HSCs by activating notch signaling to restrict mitochondrial metabolism. Exp Hematol Oncol. 2023; 12(1): 11.
- 68Guo W, Gong Q, Zong X, et al. GPR109A controls neutrophil extracellular traps formation and improve early sepsis by regulating ROS/PAD4/Cit-H3 signal axis. Exp Hematol Oncol. 2023; 12(1): 15.
- 69Penkala IJ, Liberti DC, Pankin J, et al. Age-dependent alveolar epithelial plasticity orchestrates lung homeostasis and regeneration. Cell Stem Cell. 2021; 28(10): 1775-1789.e1775.
- 70Paris AJ, Hayer KE, Oved JH, et al. STAT3-BDNF-TrkB signalling promotes alveolar epithelial regeneration after lung injury. Nat Cell Biol. 2020; 22(10): 1197-1210.
- 71Liberti DC, Kremp MM, Liberti WA 3rd, et al. Alveolar epithelial cell fate is maintained in a spatially restricted manner to promote lung regeneration after acute injury. Cell Rep. 2021; 35(6):109092.
- 72Tamada N, Tojo K, Yazawa T, Goto T. Necrosis rather than apoptosis is the dominant form of alveolar epithelial cell death in lipopolysaccharide-induced experimental acute respiratory distress syndrome model. Shock. 2020; 54(1): 128-139.
- 73Guo J, Luo Y, Zuo J, Teng J, Shen B, Liu X. Echinacea polyphenols inhibit NLRP3-dependent Pyroptosis, apoptosis, and necroptosis via suppressing NO production during lipopolysaccharide-induced acute lung injury. J Agric Food Chem. 2023; 71(19): 7289-7298.
- 74Li H, Guan J, Chen J, et al. Necroptosis signaling and NLRP3 inflammasome cross-talking in epithelium facilitate Pseudomonas aeruginosa mediated lung injury. Biochim Biophys Acta Mol Basis Dis. 2023; 1869(3):166613.
- 75Muntaka S, Almuhanna Y, Jackson D, et al. Gamma interferon and interleukin-17A differentially influence the response of human macrophages and neutrophils to Pseudomonas aeruginosa infection. Infect Immun. 2019; 87(2): e00814-18.
- 76Zhan Y, Cao J, Ji L, et al. Impaired mitochondria of Tregs decreases OXPHOS-derived ATP in primary immune thrombocytopenia with positive plasma pathogens detected by metagenomic sequencing. Exp Hematol Oncol. 2022; 11(1): 48.
- 77Lee SH, Shin JH, Park MW, et al. Impairment of mitochondrial ATP synthesis induces RIPK3-dependent necroptosis in lung epithelial cells during lung injury by lung inflammation. Immune Netw. 2022; 22(2):e18.
- 78Liu F, Chen J, Hu W, et al. PTP1B inhibition improves mitochondrial dynamics to alleviate calcific aortic valve disease via regulating OPA1 homeostasis. JACC Basic Transl Sci. 2022; 7(7): 697-712.
- 79Lai Y, Lin P, Chen M, et al. Restoration of L-OPA1 alleviates acute ischemic stroke injury in rats via inhibiting neuronal apoptosis and preserving mitochondrial function. Redox Biol. 2020; 34:101503.
- 80Jiang HL, Yang HH, Liu YB, et al. L-OPA1 deficiency aggravates necroptosis of alveolar epithelial cells through impairing mitochondrial function during acute lung injury in mice. J Cell Physiol. 2022; 237(7): 3030-3043.
- 81Liu Q, Weng J, Li C, et al. Attenuation of PM(2.5)-induced alveolar epithelial cells and lung injury through regulation of mitochondrial fission and fusion. Part Fibre Toxicol. 2023; 20(1): 28.
- 82Arnold PK, Jackson BT, Paras KI, et al. A non-canonical tricarboxylic acid cycle underlies cellular identity. Nature. 2022; 603(7901): 477-481.
- 83Li Y, Li YC, Liu XT, et al. Blockage of citrate export prevents TCA cycle fragmentation via Irg1 inactivation. Cell Rep. 2022; 38(7):110391.
- 84Le A, Lane AN, Hamaker M, et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab. 2012; 15(1): 110-121.
- 85Yang Y, He J, Zhang B, et al. SLC25A1 promotes tumor growth and survival by reprogramming energy metabolism in colorectal cancer. Cell Death Dis. 2021; 12(12): 1108.
- 86Pouikli A, Maleszewska M, Parekh S, et al. Hypoxia promotes osteogenesis by facilitating acetyl-CoA-mediated mitochondrial-nuclear communication. EMBO J. 2022; 41(23):e111239.
- 87Yang HH, Jiang HL, Tao JH, et al. Mitochondrial citrate accumulation drives alveolar epithelial cell necroptosis in lipopolysaccharide-induced acute lung injury. Exp Mol Med. 2022; 54(11): 2077-2091.
- 88Du Z, Huang Z, Chen X, et al. Modified dendritic cell-derived exosomes activate both NK cells and T cells through the NKG2D/NKG2D-L pathway to kill CML cells with or without T315I mutation. Exp Hematol Oncol. 2022; 11(1): 36.
- 89Chen H, Li Y, Wu J, et al. RIPK3 collaborates with GSDMD to drive tissue injury in lethal polymicrobial sepsis. Cell Death Differ. 2020; 27(9): 2568-2585.
- 90Li ZG, Scott MJ, Brzóska T, et al. Lung epithelial cell-derived IL-25 negatively regulates LPS-induced exosome release from macrophages. Mil Med Res. 2018; 5(1): 24.
- 91Jiao Y, Zhang T, Zhang C, et al. Exosomal miR-30d-5p of neutrophils induces M1 macrophage polarization and primes macrophage pyroptosis in sepsis-related acute lung injury. Crit Care. 2021; 25(1): 356.
- 92Jiang K, Yang J, Guo S, Zhao G, Wu H, Deng G. Peripheral circulating exosome-mediated delivery of miR-155 as a novel mechanism for acute lung inflammation. Mol Ther. 2019; 27(10): 1758-1771.
- 93Gong T, Zhang X, Peng Z, et al. Macrophage-derived exosomal aminopeptidase N aggravates sepsis-induced acute lung injury by regulating necroptosis of lung epithelial cell. Commun Biol. 2022; 5(1): 543.
- 94Carnino JM, Lee H, He X, Groot M, Jin Y. Extracellular vesicle-cargo miR-185-5p reflects type II alveolar cell death after oxidative stress. Cell Death Dis. 2020; 6: 82.
- 95Richeldi L, Azuma A, Cottin V, et al. Trial of a preferential phosphodiesterase 4B inhibitor for idiopathic pulmonary fibrosis. N Engl J Med. 2022; 386(23): 2178-2187.
- 96King TE Jr, Bradford WZ, Castro-Bernardini S, et al. A phase 3 trial of pirfenidone in patients with idiopathic pulmonary fibrosis. N Engl J Med. 2014; 370(22): 2083-2092.
- 97Lee JM, Yoshida M, Kim MS, et al. Involvement of alveolar epithelial cell necroptosis in idiopathic pulmonary fibrosis pathogenesis. Am J Respir Cell Mol Biol. 2018; 59(2): 215-224.
- 98Chen H, Xia Z, Qing B, et al. Analysis of necroptosis-related prognostic genes and immune infiltration in idiopathic pulmonary fibrosis. Front Immunol. 2023; 14:1119139.
- 99Takezaki A, Tsukumo SI, Setoguchi Y, et al. A homozygous SFTPA1 mutation drives necroptosis of type II alveolar epithelial cells in patients with idiopathic pulmonary fibrosis. J Exp Med. 2019; 216(12): 2724-2735.
- 100Zhang L, Yang Y, Lin W, Shao F, Gao Y, He J. Complement-related molecular classification and a gene signature for lung adenocarcinoma. Exp Hematol Oncol. 2023; 12(1): 22.
- 101Bui TO, Angeli E, El Bouchtaoui M, et al. Metastatic clear-cell renal cell carcinoma: a frequent NOTCH1 mutation predictive of response to anti-NOTCH1 CB-103 treatment. Exp Hematol Oncol. 2023; 12(1): 46.
- 102Ding Z, Zhong R, Yang Y, et al. Systems pharmacology reveals the mechanism of activity of Ge-gen-Qin-Lian decoction against LPS-induced acute lung injury: a novel strategy for exploring active components and effective mechanism of TCM formulae. Pharmacol Res. 2020; 156:104759.
- 103Cui Y, Wang X, Lin F, et al. MiR-29a-3p improves acute lung injury by reducing alveolar epithelial cell PANoptosis. Aging Dis. 2022; 13(3): 899-909.
- 104Zhang H, Zhang X, Ling C, et al. EGFR-TNFR1 pathway in endothelial cell facilitates acute lung injury by NF-κB/MAPK-mediated inflammation and RIP3-dependent necroptosis. Int Immunopharmacol. 2023; 117:109902.
- 105Yu X, Mao M, Liu X, et al. A cytosolic heat shock protein 90 and co-chaperone p23 complex activates RIPK3/MLKL during necroptosis of endothelial cells in acute respiratory distress syndrome. J Mol Med (Berl). 2020; 98(4): 569-583.
- 106Spinella PC, Tucci M, Fergusson DA, et al. Effect of fresh vs standard-issue red blood cell transfusions on multiple organ dysfunction syndrome in critically ill pediatric patients: a randomized clinical trial. JAMA. 2019; 322(22): 2179-2190.
- 107Qing DY, Conegliano D, Shashaty MG, et al. Red blood cells induce necroptosis of lung endothelial cells and increase susceptibility to lung inflammation. Am J Respir Crit Care Med. 2014; 190(11): 1243-1254.
- 108Wang H, Liu F, Chen X, et al. Outcome differences between PD-1/PD-L1 inhibitors-based monotherapy and combination treatments in NSCLC with brain metastases. Exp Hematol Oncol. 2023; 12(1): 56.
- 109Xia L, Zhang C, Lv N, et al. AdMSC-derived exosomes alleviate acute lung injury via transferring mitochondrial component to improve homeostasis of alveolar macrophages. Theranostics. 2022; 12(6): 2928-2947.
- 110Feng Z, Zhou J, Liu Y, et al. Epithelium- and endothelium-derived exosomes regulate the alveolar macrophages by targeting RGS1 mediated calcium signaling-dependent immune response. Cell Death Differ. 2021; 28(7): 2238-2256.
- 111Pouwels SD, Zijlstra GJ, van der Toorn M, et al. Cigarette smoke-induced necroptosis and DAMP release trigger neutrophilic airway inflammation in mice. Am J Physiol Lung Cell Mol Physiol. 2016; 310(4): L377-L386.
- 112Lu Z, Van Eeckhoutte HP, Liu G, et al. Necroptosis signaling promotes inflammation, airway remodeling, and emphysema in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2021; 204(6): 667-681.
- 113Wang Y, Wang XK, Wu PP, Wang Y, Ren LY, Xu AH. Necroptosis mediates cigarette smoke-induced inflammatory responses in macrophages. Int J Chron Obstruct Pulmon Dis. 2020; 15: 1093-1101.
- 114Guo Z, Yang H, Zhang JR, Zeng W, Hu X. Leptin receptor signaling sustains metabolic fitness of alveolar macrophages to attenuate pulmonary inflammation. Sci Adv. 2022; 8(28):eabo3064.
- 115Du XK, Ge WY, Jing R, Pan LH. Necroptosis in pulmonary macrophages mediates lipopolysaccharide-induced lung inflammatory injury by activating ZBP-1. Int Immunopharmacol. 2019; 77:105944.
- 116Guo C, Fu R, Zhou M, et al. Pathogenesis of lupus nephritis: RIP3 dependent necroptosis and NLRP3 inflammasome activation. J Autoimmun. 2019; 103:102286.
- 117Chen J, Wang S, Fu R, et al. RIP3 dependent NLRP3 inflammasome activation is implicated in acute lung injury in mice. J Transl Med. 2018; 16(1): 233.
- 118Du J, Liu Y, Lan G, et al. PTRF-IL33-ZBP1 signaling mediating macrophage necroptosis contributes to HDM-induced airway inflammation. Cell Death Dis. 2023; 14(7): 432.
- 119Lin J, Kumari S, Kim C, et al. RIPK1 counteracts ZBP1-mediated necroptosis to inhibit inflammation. Nature. 2016; 540(7631): 124-128.
- 120Bedient L, Pokharel SM, Chiok KR, et al. Lytic cell death mechanisms in human respiratory syncytial virus-infected macrophages: roles of Pyroptosis and necroptosis. Viruses. 2020; 12(9): 932.
- 121Santos LD, Antunes KH, Muraro SP, et al. TNF-mediated alveolar macrophage necroptosis drives disease pathogenesis during respiratory syncytial virus infection. Eur Respir J. 2021; 57(6): 2003764.
- 122Herold S, Becker C, Ridge KM, Budinger GR. Influenza virus-induced lung injury: pathogenesis and implications for treatment. Eur Respir J. 2015; 45(5): 1463-1478.
- 123Ackermann M, Verleden SE, Kuehnel M, et al. Pulmonary vascular Endothelialitis, thrombosis, and angiogenesis in Covid-19. N Engl J Med. 2020; 383(2): 120-128.
- 124Wang J, Li X, Wang Y, Li Y, Shi F, Diao H. Osteopontin aggravates acute lung injury in influenza virus infection by promoting macrophages necroptosis. Cell Death Dis. 2022; 8(1): 97.
- 125Zhao H, Chen Q, Huang H, et al. Osteopontin mediates necroptosis in lung injury after transplantation of ischaemic renal allografts in rats. Br J Anaesth. 2019; 123(4): 519-530.
- 126Richeldi L, Mariani M, Losi M, et al. Triggering receptor expressed on myeloid cells: role in the diagnosis of lung infections. Eur Respir J. 2004; 24(2): 247-250.
- 127Zhong WJ, Zhang J, Duan JX, et al. TREM-1 triggers necroptosis of macrophages through mTOR-dependent mitochondrial fission during acute lung injury. J Transl Med. 2023; 21(1): 179.
- 128González-Juarbe N, Gilley RP, Hinojosa CA, et al. Pore-forming toxins induce macrophage necroptosis during acute bacterial pneumonia. PLoS Pathog. 2015; 11(12):e1005337.
- 129Reyes LF, Restrepo MI, Hinojosa CA, et al. Severe pneumococcal pneumonia causes acute cardiac toxicity and subsequent cardiac remodeling. Am J Respir Crit Care Med. 2017; 196(5): 609-620.
- 130Weindel CG, Martinez EL, Zhao X, et al. Mitochondrial ROS promotes susceptibility to infection via gasdermin D-mediated necroptosis. Cell. 2022; 185(17): 3214-3231.e3223.
- 131Huang HR, Cho SJ, Harris RM, et al. RIPK3 activates MLKL-mediated necroptosis and Inflammasome signaling during streptococcus infection. Am J Respir Cell Mol Biol. 2021; 64(5): 579-591.
- 132Jia N, Li G, Wang X, et al. Staphylococcal superantigen-like protein 10 induces necroptosis through TNFR1 activation of RIPK3-dependent signal pathways. Commun Biol. 2022; 5(1): 813.
- 133Gonzalez-Juarbe N, Riegler AN, Jureka AS, et al. Influenza-induced oxidative stress sensitizes lung cells to bacterial-toxin-mediated necroptosis. Cell Rep. 2020; 32(8):108062.
- 134Park SS, Gonzalez-Juarbe N, Riegler AN, et al. Streptococcus pneumoniae binds to host GAPDH on dying lung epithelial cells worsening secondary infection following influenza. Cell Rep. 2021; 35(11):109267.
- 135Kita H. Eosinophils: multifaceted biological properties and roles in health and disease. Immunol Rev. 2011; 242(1): 161-177.
- 136Jackson DJ, Pavord ID. Living without eosinophils: evidence from mouse and man. Eur Respir J. 2023; 61(1): 2201217.
- 137Guyatt A, John C, Williams AT, et al. Mendelian randomisation of eosinophils and other cell types in relation to lung function and disease. Thorax. 2023; 78(5): 496-503.
- 138Kole TM, Vanden Berghe E, Kraft M, et al. Predictors and associations of the persistent airflow limitation phenotype in asthma: a post-hoc analysis of the ATLANTIS study. Lancet Respir Med. 2023; 11(1): 55-64.
- 139He A, Chen J, Guan J, et al. Selective eosinophil necroptosis contributes to airway inflammation and remodeling in asthma. Allergy. 2022; 77(11): 3456-3459.
- 140Werder RB, Ullah MA, Rahman MM, et al. Targeting the P2Y(13) receptor suppresses IL-33 and HMGB1 release and ameliorates experimental asthma. Am J Respir Crit Care Med. 2022; 205(3): 300-312.
- 141Badi YE, Salcman B, Taylor A, et al. IL1RAP expression and the enrichment of IL-33 activation signatures in severe neutrophilic asthma. Allergy. 2023; 78(1): 156-167.
- 142Shlomovitz I, Erlich Z, Speir M, et al. Necroptosis directly induces the release of full-length biologically active IL-33 in vitro and in an inflammatory disease model. FEBS J. 2019; 286(3): 507-522.
- 143Chen L, Wang G, Qiao X, et al. Downregulated miR-524-5p participates in the tumor microenvironment of Ameloblastoma by targeting the Interleukin-33 (IL-33)/suppression of Tumorigenicity 2 (ST2) Axis. Med Sci Monit. 2020; 26:e921863.
- 144Li W, Terada Y, Tyurina YY, et al. Necroptosis triggers spatially restricted neutrophil-mediated vascular damage during lung ischemia reperfusion injury. Proc Natl Acad Sci USA. 2022; 119(10):e2111537119.
- 145Chen Y, Hu H, Tan S, et al. The role of neutrophil extracellular traps in cancer progression, metastasis and therapy. Exp Hematol Oncol. 2022; 11(1): 99.
- 146Wang J, Luan Y, Fan EK, et al. TBK1/IKKε negatively regulate LPS-induced neutrophil necroptosis and lung inflammation. Shock. 2021; 55(3): 338-348.
- 147Ghimire L, Paudel S, Jin L, Baral P, Cai S, Jeyaseelan S. NLRP6 negatively regulates pulmonary host defense in gram-positive bacterial infection through modulating neutrophil recruitment and function. PLoS Pathog. 2018; 14(9):e1007308.
- 148Kitur K, Parker D, Nieto P, et al. Toxin-induced necroptosis is a major mechanism of Staphylococcus aureus lung damage. PLoS Pathog. 2015; 11(4):e1004820.
- 149Zhou Y, Niu C, Ma B, et al. Inhibiting PSMα-induced neutrophil necroptosis protects mice with MRSA pneumonia by blocking the agr system. Cell Death Dis. 2018; 9(3): 362.
- 150Paudel S, Ghimire L, Jin L, Baral P, Cai S, Jeyaseelan S. NLRC4 suppresses IL-17A-mediated neutrophil-dependent host defense through upregulation of IL-18 and induction of necroptosis during gram-positive pneumonia. Mucosal Immunol. 2019; 12(1): 247-257.
- 151Wang X, O'Brien ME, Yu J, et al. Prolonged cold ischemia induces necroptotic cell death in ischemia-reperfusion injury and contributes to primary graft dysfunction after lung transplantation. Am J Respir Cell Mol Biol. 2019; 61(2): 244-256.
- 152Kanou T, Ohsumi A, Kim H, et al. Inhibition of regulated necrosis attenuates receptor-interacting protein kinase 1-mediated ischemia-reperfusion injury after lung transplantation. J Heart Lung Transplant. 2018; 37(10): 1261-1270.
- 153Dong L, Liang F, Lou Z, et al. Necrostatin-1 alleviates lung ischemia-reperfusion injury via inhibiting necroptosis and apoptosis of lung epithelial cells. Cells. 2022; 11(19): 3139.
- 154Bolognese AC, Yang WL, Hansen LW, et al. Inhibition of necroptosis attenuates lung injury and improves survival in neonatal sepsis. Surgery. 2018; 164: 110-116.
- 155Tao H, Zhao H, Ge D, et al. Necroptosis in pulmonary macrophages promotes silica-induced inflammation and interstitial fibrosis in mice. Toxicol Lett. 2022; 355: 150-159.
- 156Zhang X, Han Q, Hou R, et al. Targeting receptor-interacting protein kinase 1 by novel Benzothiazole derivatives: treatment of acute lung injury through the necroptosis pathway. J Med Chem. 2023; 66(7): 5261-5278.
- 157Li S, Zhang Y, Guan Z, et al. SARS-CoV-2 Z-RNA activates the ZBP1-RIPK3 pathway to promote virus-induced inflammatory responses. Cell Res. 2023; 33(3): 201-214.
- 158Cui YR, Qu F, Zhong WJ, et al. Beneficial effects of aloperine on inflammation and oxidative stress by suppressing necroptosis in lipopolysaccharide-induced acute lung injury mouse model. Phytomedicine. 2022; 100:154074.
- 159Huang D, Chen P, Huang G, et al. Salt-inducible kinases inhibitor HG-9-91-01 targets RIPK3 kinase activity to alleviate necroptosis-mediated inflammatory injury. Cell Death Dis. 2022; 13(2): 188.
- 160Rübbelke M, Fiegen D, Bauer M, et al. Locking mixed-lineage kinase domain-like protein in its auto-inhibited state prevents necroptosis. Proc Natl Acad Sci USA. 2020; 117(52): 33272-33281.
- 161Ueda S, Chen-Yoshikawa TF, Tanaka S, et al. Protective effect of necrosulfonamide on rat pulmonary ischemia-reperfusion injury via inhibition of necroptosis. J Thorac Cardiovasc Surg. 2022; 163(2): e113-e122.
- 162Racanelli AC, Choi AMK. The Saga of necroptosis in chronic obstructive pulmonary disease continues. Am J Respir Crit Care Med. 2021; 204(6): 622-624.
- 163Mizumura K, Cloonan SM, Nakahira K, et al. Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD. J Clin Invest. 2014; 124(9): 3987-4003.
- 164Wang Y, Liu J, Zhou JS, et al. MTOR suppresses cigarette smoke-induced epithelial cell death and airway inflammation in chronic obstructive pulmonary disease. J Immunol. 2018; 200(8): 2571-2580.
- 165Rogers NM, Thomson AW, Isenberg JS. Activation of parenchymal CD47 promotes renal ischemia-reperfusion injury. J Am Soc Nephrol. 2012; 23(9): 1538-1550.
- 166Raina A, Horn ET, Benza RL. The pathophysiology of endothelin in complications after solid organ transplantation: a potential novel therapeutic role for endothelin receptor antagonists. Transplantation. 2012; 94(9): 885-893.
- 167Zhao H, Ning J, Lemaire A, et al. Necroptosis and parthanatos are involved in remote lung injury after receiving ischemic renal allografts in rats. Kidney Int. 2015; 87(4): 738-748.
- 168Xu C, Wu J, Wu Y, et al. TNF-α-dependent neuronal necroptosis regulated in Alzheimer's disease by coordination of RIPK1-p62 complex with autophagic UVRAG. Theranostics. 2021; 11(19): 9452-9469.
- 169Woznicki JA, Saini N, Flood P, et al. TNF-α synergises with IFN-γ to induce caspase-8-JAK1/2-STAT1-dependent death of intestinal epithelial cells. Cell Death Dis. 2021; 12(10): 864.
- 170Li M, Liu Y, Xu C, et al. Ubiquitin-binding domain in ABIN1 is critical for regulating cell death and inflammation during development. Cell Death Differ. 2022; 29(10): 2034-2045.
- 171Otani T, Matsuda M, Mizokami A, et al. Osteocalcin triggers Fas/FasL-mediated necroptosis in adipocytes via activation of p300. Cell Death Dis. 2018; 9(12): 1194.
- 172Park SY, Park HH, Park SY, et al. Reduction in MLKL-mediated endosomal trafficking enhances the TRAIL-DR4/5 signal to increase cancer cell death. Cell Death Dis. 2020; 11(9): 744.
- 173Zhang T, Yin C, Boyd DF, et al. Influenza virus Z-RNAs induce ZBP1-mediated necroptosis. Cell. 2020; 180(6): 1115-1129.e1113.
- 174Koehler H, Cotsmire S, Zhang T, et al. Vaccinia virus E3 prevents sensing of Z-RNA to block ZBP1-dependent necroptosis. Cell Host Microbe. 2021; 29(8): 1266-1276.e1265.
- 175Jiao H, Wachsmuth L, Kumari S, et al. Z-nucleic-acid sensing triggers ZBP1-dependent necroptosis and inflammation. Nature. 2020; 580(7803): 391-395.
- 176Takemura R, Takaki H, Okada S, et al. PolyI:C-induced, TLR3/RIP3-dependent necroptosis backs up immune effector-mediated tumor elimination in vivo. Cancer Immunol Res. 2015; 3(8): 902-914.
- 177Zhan Y, Xu D, Tian Y, et al. Novel role of macrophage TXNIP-mediated CYLD-NRF2-OASL1 axis in stress-induced liver inflammation and cell death. JHEP Rep. 2022; 4(9):100532.
- 178Li Z, Scott MJ, Fan EK, et al. Tissue damage negatively regulates LPS-induced macrophage necroptosis. Cell Death Differ. 2016; 23(9): 1428-1447.
- 179McComb S, Cessford E, Alturki NA, et al. Type-I interferon signaling through ISGF3 complex is required for sustained Rip3 activation and necroptosis in macrophages. Proc Natl Acad Sci USA. 2014; 111(31): E3206-E3213.
- 180Martin-Sanchez D, Fontecha-Barriuso M, Carrasco S, et al. TWEAK and RIPK1 mediate a second wave of cell death during AKI. Proc Natl Acad Sci USA. 2018; 115(16): 4182-4187.
- 181Vandenabeele P, Grootjans S, Callewaert N, Takahashi N. Necrostatin-1 blocks both RIPK1 and IDO: consequences for the study of cell death in experimental disease models. Cell Death Differ. 2013; 20(2): 185-187.
- 182Liu L, Liang L, Yang C, Zhou Y, Chen Y. Extracellular vesicles of Fusobacterium nucleatum compromise intestinal barrier through targeting RIPK1-mediated cell death pathway. Gut Microbes. 2021; 13(1): 1-20.
- 183Linkermann A, Bräsen JH, Himmerkus N, et al. Rip1 (receptor-interacting protein kinase 1) mediates necroptosis and contributes to renal ischemia/reperfusion injury. Kidney Int. 2012; 81(8): 751-761.
- 184Seifert L, Werba G, Tiwari S, et al. The necrosome promotes pancreatic oncogenesis via CXCL1 and Mincle-induced immune suppression. Nature. 2016; 532(7598): 245-249.
- 185Lee SA, Chang LC, Jung W, et al. OASL phase condensation induces amyloid-like fibrillation of RIPK3 to promote virus-induced necroptosis. Nat Cell Biol. 2023; 25(1): 92-107.
- 186Rodriguez DA, Quarato G, Liedmann S, et al. Caspase-8 and FADD prevent spontaneous ZBP1 expression and necroptosis. Proc Natl Acad Sci USA. 2022; 119(41):e2207240119.
- 187Li X, Li F, Zhang X, et al. Caspase-8 auto-cleavage regulates programmed cell death and collaborates with RIPK3/MLKL to prevent lymphopenia. Cell Death Differ. 2022; 29(8): 1500-1512.
- 188Sun H, Lu J, Liu L, Yang CY, Wang S. Potent and selective small-molecule inhibitors of cIAP1/2 proteins reveal that the binding of Smac mimetics to XIAP BIR3 is not required for their effective induction of cell death in tumor cells. ACS Chem Biol. 2014; 9(4): 994-1002.
- 189Peng Y, Sun H, Lu J, et al. Bivalent Smac mimetics with a diazabicyclic core as highly potent antagonists of XIAP and cIAP1/2 and novel anticancer agents. J Med Chem. 2012; 55(1): 106-114.
- 190Schworer SA, Smirnova II, Kurbatova I, et al. Toll-like receptor-mediated down-regulation of the deubiquitinase cylindromatosis (CYLD) protects macrophages from necroptosis in wild-derived mice. J Biol Chem. 2014; 289(20): 14422-14433.