{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T04:09:24Z","timestamp":1779250164731,"version":"3.51.4"},"reference-count":90,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,2,26]],"date-time":"2024-02-26T00:00:00Z","timestamp":1708905600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>Pre-neutrophils, while developing in the bone marrow, transcribe the <jats:italic>Inhba<\/jats:italic> gene and synthesize Activin-A protein, which they store and release at the earliest stage of their activation in the periphery. However, the role of neutrophil-derived Activin-A is not completely understood.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>To address this issue, we developed a neutrophil-specific Activin-A-deficient animal model (<jats:italic>S100a8-Cre\/Inhba<\/jats:italic><jats:sup>fl\/fl<\/jats:sup> mice) and analyzed the immune response to Influenza A virus (IAV) infection. More specifically, evaluation of body weight and lung mechanics, molecular and cellular analyses of bronchoalveolar lavage fluids, flow cytometry and cell sorting of lung cells, as well as histopathological analysis of lung tissues, were performed in PBS-treated and IAV-infected transgenic animals.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>We found that neutrophil-specific Activin-A deficiency led to exacerbated pulmonary inflammation and widespread hemorrhagic histopathology in the lungs of IAV-infected animals that was associated with an exuberant production of neutrophil extracellular traps (NETs). Moreover, deletion of the Activin-A receptor ALK4\/ACVR1B in neutrophils exacerbated IAV-induced pathology as well, suggesting that neutrophils themselves are potential targets of Activin-A-mediated signaling. The pro-NETotic tendency of Activin-A-deficient neutrophils was further verified in the context of thioglycollate-induced peritonitis, a model characterized by robust peritoneal neutrophilia. Of importance, transcriptome analysis of Activin-A-deficient neutrophils revealed alterations consistent with a predisposition for NET release. <\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Collectively, our data demonstrate that Activin-A, secreted by neutrophils upon their activation in the periphery, acts as a feedback mechanism to moderate their pro-NETotic tendency and limit the collateral tissue damage caused by neutrophil excess activation during the inflammatory response.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fimmu.2024.1302489","type":"journal-article","created":{"date-parts":[[2024,2,26]],"date-time":"2024-02-26T04:47:39Z","timestamp":1708922859000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Neutrophil-derived Activin-A moderates their pro-NETotic activity and attenuates collateral tissue damage caused by Influenza A virus infection"],"prefix":"10.3389","volume":"15","author":[{"given":"Georgios","family":"Divolis","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Evgenia","family":"Synolaki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Athanasia","family":"Doulou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ariana","family":"Gavriil","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christina C.","family":"Giannouli","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anastasia","family":"Apostolidou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martyn L.","family":"Foster","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martin M.","family":"Matzuk","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Panagiotis","family":"Skendros","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ioanna-Evdokia","family":"Galani","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paschalis","family":"Sideras","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2024,2,26]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1038\/s41572-018-0002-y","article-title":"Influenza","volume":"4","author":"Krammer","year":"2018","journal-title":"Nat Rev Dis Primers"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1002\/jmv.26990","article-title":"A brief review of influenza virus infection","volume":"93","author":"Javanian","year":"2021","journal-title":"J Med Virol"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1000115","article-title":"H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice","volume":"4","author":"Perrone","year":"2008","journal-title":"PloS Pathog"},{"key":"B4","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1186\/1465-9921-9-57","article-title":"The role of neutrophils in the upper and lower respiratory tract during influenza virus infection of mice","volume":"9","author":"Tate","year":"2008","journal-title":"Respir Res"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1038\/nature07201","article-title":"Origin and physiological roles of inflammation","volume":"454","author":"Medzhitov","year":"2008","journal-title":"Nature"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1126\/sciimmunol.aat4579","article-title":"Neutrophils: New insights and open questions","volume":"3","author":"Ley","year":"2018","journal-title":"Sci Immunol"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1016\/j.immuni.2021.06.006","article-title":"The neutrophil","volume":"54","author":"Burn","year":"2021","journal-title":"Immunity"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2014.00448","article-title":"Granule protein processing and regulated secretion in neutrophils","volume":"5","author":"Sheshachalam","year":"2014","journal-title":"Front Immunol"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1126\/science.1092385","article-title":"Neutrophil extracellular traps kill bacteria","volume":"303","author":"Brinkmann","year":"2004","journal-title":"Science"},{"key":"B10","doi-asserted-by":"publisher","first-page":"1469","DOI":"10.3390\/cells10061469","article-title":"To trap a pathogen: neutrophil extracellular traps and their role in mucosal epithelial and skin diseases","volume":"10","author":"Dominguez-Diaz","year":"2021","journal-title":"Cells"},{"key":"B11","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1007\/s12016-020-08804-7","article-title":"A review of neutrophil extracellular traps (NETs) in disease: potential anti-NETs therapeutics","volume":"61","author":"Mutua","year":"2021","journal-title":"Clin Rev Allergy Immunol"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.0902497","article-title":"Neutrophils ameliorate lung injury and the development of severe disease during influenza infection","volume":"183","author":"Tate","year":"2009","journal-title":"J Immunol"},{"key":"B13","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/j.ajpath.2011.03.013","article-title":"Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis","volume":"179","author":"Narasaraju","year":"2011","journal-title":"Am J Pathol"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2101497118","article-title":"IgA potentiates NETosis in response to viral infection","volume":"118","author":"Stacey","year":"2021","journal-title":"Proc Natl Acad Sci USA"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jix475","article-title":"High level of neutrophil extracellular traps correlates with poor prognosis of severe influenza A infection","volume":"217","author":"Zhu","year":"2018","journal-title":"J Infect Dis"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1164\/rccm.201810-1869OC","article-title":"Extracellular DNA, neutrophil extracellular traps, and inflammasome activation in severe asthma","volume":"199","author":"Lachowicz-Scroggins","year":"2019","journal-title":"Am J Respir Crit Care Med"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1038\/s41590-019-0496-9","article-title":"Locally instructed CXCR4(hi) neutrophils trigger environment-driven allergic asthma through the release of neutrophil extracellular traps","volume":"20","author":"Radermecker","year":"2019","journal-title":"Nat Immunol"},{"key":"B18","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1002\/path.4359","article-title":"Neutrophil extracellular traps promote differentiation and function of fibroblasts","volume":"233","author":"Chrysanthopoulou","year":"2014","journal-title":"J Pathol"},{"key":"B19","doi-asserted-by":"publisher","first-page":"317","DOI":"10.3390\/life12020317","article-title":"Neutrophil extracellular traps in ANCA-associated vasculitis and interstitial lung disease: A scoping review","volume":"12","author":"D'alessandro","year":"2022","journal-title":"Life (Basel)"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.18632\/oncotarget.22744","article-title":"Neutrophil extracellular traps contribute to the pathogenesis of acid-aspiration-induced ALI\/ARDS","volume":"9","author":"Li","year":"2018","journal-title":"Oncotarget"},{"key":"B21","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1186\/s12931-022-02065-y","article-title":"Delayed neutrophil apoptosis may enhance NET formation in ARDS","volume":"23","author":"Song","year":"2022","journal-title":"Respir Res"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1172\/JCI141374","article-title":"Complement and tissue factor-enriched neutrophil extracellular traps are key drivers in COVID-19 immunothrombosis","volume":"130","author":"Skendros","year":"2020","journal-title":"J Clin Invest"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.821007","article-title":"On the origin of neutrophil extracellular traps in COVID-19","volume":"13","author":"Pastorek","year":"2022","journal-title":"Front Immunol"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1165\/ajrcmb.25.1.4396","article-title":"Activation of the TGF-beta\/activin-Smad2 pathway during allergic airway inflammation","volume":"25","author":"Rosendahl","year":"2001","journal-title":"Am J Respir Cell Mol Biol"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1164\/rccm.201105-0784OC","article-title":"Activin-A overexpression in the murine lung causes pathology that simulates acute respiratory distress syndrome","volume":"185","author":"Apostolou","year":"2012","journal-title":"Am J Respir Crit Care Med"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1007\/s00281-013-0365-9","article-title":"Activin, neutrophils, and inflammation: just coincidence","volume":"35","author":"Sideras","year":"2013","journal-title":"Semin Immunopathol"},{"key":"B27","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1186\/1471-2334-14-253","article-title":"Serum activin A and B, and follistatin in critically ill patients with influenza A(H1N1) infection","volume":"14","author":"Linko","year":"2014","journal-title":"BMC Infect Dis"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jiab108","article-title":"The Activin\/Follistatin axis is severely deregulated in COVID-19 and independently associated with in-hospital mortality","volume":"223","author":"Synolaki","year":"2021","journal-title":"J Infect Dis"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1007\/s00408-021-00470-6","article-title":"Progranulin and Activin A concentrations are elevated in serum from patients with acute exacerbations of idiopathic pulmonary fibrosis","volume":"199","author":"Xie","year":"2021","journal-title":"Lung"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a022053","article-title":"Signaling receptors for TGF-beta family members","volume":"8","author":"Heldin","year":"2016","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"B31","doi-asserted-by":"publisher","first-page":"487","DOI":"10.3390\/biom10030487","article-title":"TGF-beta signaling","volume":"10","author":"Tzavlaki","year":"2020","journal-title":"Biomolecules"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1016\/j.mce.2004.07.010","article-title":"Activin A and follistatin in systemic inflammation","volume":"225","author":"Jones","year":"2004","journal-title":"Mol Cell Endocrinol"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a021881","article-title":"Activins and Inhibins: roles in development, physiology, and disease","volume":"8","author":"Namwanje","year":"2016","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1084\/jem.176.5.1449","article-title":"Activin A\/erythroid differentiation factor is induced during human monocyte activation","volume":"176","author":"Eramaa","year":"1992","journal-title":"J Exp Med"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1189\/jlb.72.2.347","article-title":"Potent induction of activin A secretion from monocytes and bone marrow stromal fibroblasts by cognate interaction with activated T cells","volume":"72","author":"Abe","year":"2002","journal-title":"J Leukoc Biol"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1016\/j.neulet.2006.11.065","article-title":"Microglial cells and peritoneal macrophages release activin A upon stimulation with Toll-like receptor agonists","volume":"413","author":"Ebert","year":"2007","journal-title":"Neurosci Lett"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1182\/blood-2010-09-306993","article-title":"Activin A skews macrophage polarization by promoting a proinflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers","volume":"117","author":"Sierra-Filardi","year":"2011","journal-title":"Blood"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1182\/blood-2007-03-080994","article-title":"Activin-A: a novel dendritic cell-derived cytokine that potently attenuates CD40 ligand-specific cytokine and chemokine production","volume":"111","author":"Robson","year":"2008","journal-title":"Blood"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.177.10.6787","article-title":"Activin A functions as a Th2 cytokine in the promotion of the alternative activation of macrophages","volume":"177","author":"Ogawa","year":"2006","journal-title":"J Immunol"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1189\/jlb.1007710","article-title":"A dual role of activin A in regulating immunoglobulin production of B cells","volume":"83","author":"Ogawa","year":"2008","journal-title":"J Leukoc Biol"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1016\/j.yexcr.2018.11.013","article-title":"Activin A regulates activities of peripheral blood natural killer cells of mouse in an autocrine and paracrine manner","volume":"374","author":"Ma","year":"2019","journal-title":"Exp Cell Res"},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1016\/j.jaci.2009.06.022","article-title":"Activin and transforming growth factor-beta signaling pathways are activated after allergen challenge in mild asthma","volume":"124","author":"Kariyawasam","year":"2009","journal-title":"J Allergy Clin Immunol"},{"key":"B43","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1016\/j.immuni.2018.02.002","article-title":"Developmental analysis of bone marrow neutrophils reveals populations specialized in expansion, trafficking, and effector functions","volume":"48","author":"Evrard","year":"2018","journal-title":"Immunity"},{"key":"B44","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1677\/joe.0.1820069","article-title":"Characterisation of the rapid release of activin A following acute lipopolysaccharide challenge in the ewe","volume":"182","author":"Jones","year":"2004","journal-title":"J Endocrinol"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0705971104","article-title":"Activin A is a critical component of the inflammatory response, and its binding protein, follistatin, reduces mortality in endotoxemia","volume":"104","author":"Jones","year":"2007","journal-title":"Proc Natl Acad Sci USA"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1152\/ajpregu.00478.2011","article-title":"Acute regulation of activin A and its binding protein, follistatin, in serum and tissues following lipopolysaccharide treatment of adult male mice","volume":"303","author":"Wu","year":"2012","journal-title":"Am J Physiol Regul Integr Comp Physiol"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1038\/icb.2011.12","article-title":"Tumour necrosis factor-alpha stimulates human neutrophils to release preformed activin A","volume":"89","author":"Chen","year":"2011","journal-title":"Immunol Cell Biol"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2004.10.010","article-title":"JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells","volume":"119","author":"Passegue","year":"2004","journal-title":"Cell"},{"key":"B49","doi-asserted-by":"publisher","DOI":"10.1210\/me.2007-0146","article-title":"Intraovarian activins are required for female fertility","volume":"21","author":"Pangas","year":"2007","journal-title":"Mol Endocrinol"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.1002\/dvg.22352","article-title":"Generation of a conditional mouse model to target Acvr1b disruption in adult tissues","volume":"51","author":"Ripoche","year":"2013","journal-title":"Genesis"},{"key":"B51","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1002\/dvg.20335","article-title":"A global double-fluorescent Cre reporter mouse","volume":"45","author":"Muzumdar","year":"2007","journal-title":"Genesis"},{"key":"B52","doi-asserted-by":"publisher","first-page":"eabn4395","DOI":"10.1126\/scisignal.abn4395","article-title":"Coordinated activation of TGF-beta and BMP pathways promotes autophagy and limits liver injury after acetaminophen intoxication","volume":"15","author":"Stavropoulos","year":"2022","journal-title":"Sci Signal"},{"key":"B53","doi-asserted-by":"publisher","first-page":"875-90.e876","DOI":"10.1016\/j.immuni.2017.04.025","article-title":"Interferon-lambda Mediates Non-redundant Front-Line Antiviral Protection against Influenza Virus Infection without Compromising Host Fitness","volume":"46","author":"Galani","year":"2017","journal-title":"Immunity"},{"key":"B54","doi-asserted-by":"publisher","first-page":"101151","DOI":"10.1016\/j.xpro.2022.101151","article-title":"Protocol for influenza A virus infection of mice and viral load determination","volume":"3","author":"Galani","year":"2022","journal-title":"STAR Protoc"},{"key":"B55","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1016\/j.cell.2013.06.013","article-title":"A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection","volume":"154","author":"Brandes","year":"2013","journal-title":"Cell"},{"key":"B56","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0041460","article-title":"Activation of the canonical bone morphogenetic protein (BMP) pathway during lung morphogenesis and adult lung tissue repair","volume":"7","author":"Sountoulidis","year":"2012","journal-title":"PloS One"},{"key":"B57","doi-asserted-by":"publisher","first-page":"fcz028","DOI":"10.1093\/braincomms\/fcz028","article-title":"Activation of both transforming growth factor-beta and bone morphogenetic protein signalling pathways upon traumatic brain injury restrains pro-inflammatory and boosts tissue reparatory responses of reactive astrocytes and microglia","volume":"1","author":"Divolis","year":"2019","journal-title":"Brain Commun"},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal Biochem"},{"key":"B59","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.180.11.7368","article-title":"C5a and TNF-alpha up-regulate the expression of tissue factor in intra-alveolar neutrophils of patients with the acute respiratory distress syndrome","volume":"180","author":"Kambas","year":"2008","journal-title":"J Immunol"},{"key":"B60","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.951232","article-title":"A gene expression map of host immune response in human brucellosis","volume":"13","author":"Mitroulis","year":"2022","journal-title":"Front Immunol"},{"key":"B61","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gky379","article-title":"The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update","volume":"46","author":"Afgan","year":"2018","journal-title":"Nucleic Acids Res"},{"key":"B62","doi-asserted-by":"publisher","first-page":"590","DOI":"10.3390\/biomedicines10030590","article-title":"Functional enrichment analysis of regulatory elements","volume":"10","author":"Garcia-Moreno","year":"2022","journal-title":"Biomedicines"},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkac1000","article-title":"The STRING database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest","volume":"51","author":"Szklarczyk","year":"2023","journal-title":"Nucleic Acids Res"},{"key":"B64","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0506580102","article-title":"Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles","volume":"102","author":"Subramanian","year":"2005","journal-title":"Proc Natl Acad Sci USA"},{"key":"B65","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.jim.2014.05.009","article-title":"Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice","volume":"408","author":"Abram","year":"2014","journal-title":"J Immunol Methods"},{"key":"B66","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajpath.2017.09.014","article-title":"The role of extracellular histones in influenza virus pathogenesis","volume":"188","author":"Ashar","year":"2018","journal-title":"Am J Pathol"},{"key":"B67","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1038\/cr.2010.150","article-title":"Neutrophil extracellular trap cell death requires both autophagy and superoxide generation","volume":"21","author":"Remijsen","year":"2011","journal-title":"Cell Res"},{"key":"B68","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1182\/blood-2013-09-526707","article-title":"Akt is essential to induce NADPH-dependent NETosis and to switch the neutrophil death to apoptosis","volume":"123","author":"Douda","year":"2014","journal-title":"Blood"},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1189\/jlb.4A0615-261RR","article-title":"Neutrophil extracellular traps release induced by Leishmania: role of PI3Kgamma, ERK, PI3Ksigma, PKC, and [Ca2+]","volume":"100","author":"Desouza-Vieira","year":"2016","journal-title":"J Leukoc Biol"},{"key":"B70","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0029318","article-title":"Neutrophil extracellular trap formation is associated with IL-1beta and autophagy-related signaling in gout","volume":"6","author":"Mitroulis","year":"2011","journal-title":"PloS One"},{"key":"B71","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2018.00109","article-title":"Autophagy in neutrophils: from granulopoiesis to neutrophil extracellular traps","volume":"6","author":"Skendros","year":"2018","journal-title":"Front Cell Dev Biol"},{"key":"B72","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0157454","article-title":"Neutrophil extracellular trap formation is independent of de novo gene expression","volume":"11","author":"Sollberger","year":"2016","journal-title":"PloS One"},{"key":"B73","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1909546117","article-title":"NETosis proceeds by cytoskeleton and endomembrane disassembly and PAD4-mediated chromatin decondensation and nuclear envelope rupture","volume":"117","author":"Thiam","year":"2020","journal-title":"Proc Natl Acad Sci USA"},{"key":"B74","doi-asserted-by":"publisher","DOI":"10.1182\/blood.2021013565","article-title":"Formation of neutrophil extracellular traps requires actin cytoskeleton rearrangements","volume":"139","author":"Sprenkeler","year":"2022","journal-title":"Blood"},{"key":"B75","doi-asserted-by":"publisher","DOI":"10.1038\/nm.3642","article-title":"Lung regeneration: mechanisms, applications and emerging stem cell populations","volume":"20","author":"Kotton","year":"2014","journal-title":"Nat Med"},{"key":"B76","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.semcdb.2019.11.006","article-title":"Lung regeneration: a tale of mice and men","volume":"100","author":"Basil","year":"2020","journal-title":"Semin Cell Dev Biol"},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.1016\/j.jaci.2010.12.1103","article-title":"Eosinophil and neutrophil extracellular DNA traps in human allergic asthmatic airways","volume":"127","author":"Dworski","year":"2011","journal-title":"J Allergy Clin Immunol"},{"key":"B78","doi-asserted-by":"publisher","DOI":"10.1136\/annrheumdis-2018-213181","article-title":"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)","volume":"78","author":"Frangou","year":"2019","journal-title":"Ann Rheum Dis"},{"key":"B79","doi-asserted-by":"publisher","DOI":"10.1136\/annrheumdis-2021-221409","article-title":"Deletion of activin A in mesenchymal but not myeloid cells ameliorates disease severity in experimental arthritis","volume":"81","author":"Waltereit-Kracke","year":"2022","journal-title":"Ann Rheum Dis"},{"key":"B80","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1616942114","article-title":"Activin-A co-opts IRF4 and AhR signaling to induce human regulatory T cells that restrain asthmatic responses","volume":"114","author":"Tousa","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"key":"B81","doi-asserted-by":"publisher","DOI":"10.1038\/labinvest.2014.97","article-title":"Activin A balance regulates epithelial invasiveness and tumorigenesis","volume":"94","author":"Le Bras","year":"2014","journal-title":"Lab Invest"},{"key":"B82","doi-asserted-by":"publisher","DOI":"10.1101\/gr.197566.115","article-title":"nanoCAGE reveals 5' UTR features that define specific modes of translation of functionally related MTOR-sensitive mRNAs","volume":"26","author":"Gandin","year":"2016","journal-title":"Genome Res"},{"key":"B83","doi-asserted-by":"publisher","first-page":"41749","DOI":"10.1038\/srep41749","article-title":"Transcriptional firing helps to drive NETosis","volume":"7","author":"Khan","year":"2017","journal-title":"Sci Rep"},{"key":"B84","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2017.01.022","article-title":"Autophagy and neurodegeneration: pathogenic mechanisms and therapeutic opportunities","volume":"93","author":"Menzies","year":"2017","journal-title":"Neuron"},{"key":"B85","doi-asserted-by":"publisher","first-page":"287","DOI":"10.3390\/ijms21010287","article-title":"Neutrophil Metabolic Shift during their Lifecycle: Impact on their Survival and Activation","volume":"21","author":"Injarabian","year":"2019","journal-title":"Int J Mol Sci"},{"key":"B86","doi-asserted-by":"publisher","DOI":"10.1002\/bab.2104","article-title":"The interplay of ROS and the PI3K\/Akt pathway in autophagy regulation","volume":"69","author":"Kma","year":"2022","journal-title":"Biotechnol Appl Biochem"},{"key":"B87","doi-asserted-by":"publisher","first-page":"2045894020966547","DOI":"10.1177\/2045894020966547","article-title":"Circulating markers of angiogenesis and endotheliopathy in COVID-19","volume":"10","author":"Pine","year":"2020","journal-title":"Pulm Circ"},{"key":"B88","doi-asserted-by":"publisher","first-page":"106604","DOI":"10.1016\/j.dib.2020.106604","article-title":"RNA-Seq transcriptome data of human cells infected with influenza A\/Puerto Rico\/8\/1934 (H1N1) virus","volume":"33","author":"Zhuravlev","year":"2020","journal-title":"Data Brief"},{"key":"B89","doi-asserted-by":"publisher","DOI":"10.1093\/bfgp\/elad025","article-title":"Integrating single-cell RNA sequencing data to genome-wide association analysis data identifies significant cell types in influenza A virus infection and COVID-19","author":"Zou","year":"2023","journal-title":"Brief Funct Genomics"},{"key":"B90","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1186\/s12920-020-0672-7","article-title":"Pathway mapping of leukocyte transcriptome in influenza patients reveals distinct pathogenic mechanisms associated with progression to severe infection","volume":"13","author":"Zerbib","year":"2020","journal-title":"BMC Med Genomics"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2024.1302489\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,26]],"date-time":"2024-02-26T04:47:42Z","timestamp":1708922862000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2024.1302489\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,2,26]]},"references-count":90,"alternative-id":["10.3389\/fimmu.2024.1302489"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2024.1302489","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,26]]},"article-number":"1302489"}}