There is emerging evidence that platelets are major contributors to inflammatory processes through intimate associations with innate immune cells. Here, we report that activated platelets induce the formation of neutrophil extracellular traps (NETs) in transfusion-related acute lung injury (TRALI), which is the leading cause of death after transfusion therapy. NETs are composed of decondensed chromatin decorated with granular proteins that function to trap extracellular pathogens; their formation requires the activation of neutrophils and release of their DNA in a process that may or may not result in neutrophil death. In a mouse model of TRALI that is neutrophil and platelet dependent, NETs appeared in the lung microvasculature and NET components increased in the plasma. We detected NETs in the lungs and plasma of human TRALI and in the plasma of patients with acute lung injury. In the experimental TRALI model, targeting platelet activation with either aspirin or a glycoprotein IIb/IIIa inhibitor decreased NET formation and lung injury. We then directly targeted NET components with a histone blocking antibody and DNase1, both of which protected mice from TRALI. These data suggest that NETs contribute to lung endothelial injury and that targeting NET formation may be a promising new direction for the treatment of acute lung injury.
Axelle Caudrillier, Kai Kessenbrock, Brian M. Gilliss, John X. Nguyen, Marisa B. Marques, Marc Monestier, Pearl Toy, Zena Werb, Mark R. Looney
Title and authors | Publication | Year |
---|---|---|
CD39+CD9+ lung interstitial macrophages suppress IL-23/Th17-mediated neutrophilic asthma by inhibiting NETosis
Seunghan Han, Bomin Kim, Do Hyeon, Daeun Jeong, Jae-Sung Nam, Yoon Choi, Bo-Ram Kim, Sang Chul Park, Youn Chung, Sung Shin, June-Yong Lee, Jong Kyoung Kim, Jihye Park, Sei Lee, Tae-Bum Kim, Jae Cheon, Hyung-Ju Cho, Chang-Hoon Kim, Joo-Heon Yoon, Daehee Hwang, Ji-Hwan Ryu |
Nature communications | 2024 |
Pyroptotic Macrophage-Derived Microvesicles Accelerate Formation of Neutrophil Extracellular Traps via GSDMD-N-expressing Mitochondrial Transfer during Sepsis
Kuang L, Wu Y, Shu J, Yang J, Zhou H, Huang X |
International journal of biological sciences | 2024 |
IgG hexamers initiate acute lung injury
Simon Cleary, Yurim Seo, Jennifer Tian, Nicholas Kwaan, David Bulkley, Arthur Bentlage, Gestur Vidarsson, Éric Boilard, Rolf Spirig, James Zimring, Mark Looney |
Journal of Clinical Investigation | 2024 |
Neutrophil extracellular traps and their implications in airway inflammatory diseases
Xuan N, Zhao J, Kang Z, Cui W, Tian BP |
Frontiers in Medicine | 2024 |
A Narrative Review: The Role of NETs in Acute Respiratory Distress Syndrome/Acute Lung Injury
Zhou X, Jin J, Lv T, Song Y |
International journal of molecular sciences | 2024 |
IgG hexamers initiate acute lung injury
Cleary SJ, Seo Y, Tian JJ, Kwaan N, Bulkley DP, Bentlage AE, Vidarsson G, Boilard É, Spirig R, Zimring JC, Looney MR |
2024 | |
Neutrophil extracellular traps - a potential trigger for the development of thrombocytopenia during extracorporeal membrane oxygenation
Haus M, Foltan M, Philipp A, Mueller T, Gruber M, Lingel MP, Krenkel L, Lehle K |
Frontiers in immunology | 2024 |
Resveratrol Attenuates Rheumatoid Arthritis Induce Neutrophil Extracellular Traps via TLR-4 Mediated Inflammation in C57BL/6 Mice.
Chen Z, Xiao G, Ao J |
2024 | |
Neutrophils in physiology and pathology
Aroca-Crevillén A, Vicanolo T, Ovadia S, Hidalgo A |
Annual review of pathology | 2024 |
Platelets in Alcohol-Associated Liver Disease: Interaction With Neutrophils
Wang J, Wang X, Peng H, Dong Z, Liangpunsakul S, Zuo L, Wang H |
Cellular and Molecular Gastroenterology and Hepatology | 2024 |
Acute pulmonary injury in hematology patients supported with pathogen-reduced and conventional platelet components
Wheeler AP, Snyder EL, Refaai M, Cohn CS, Poisson J, Fontaine M, Sehl M, Nooka AK, Uhl L, Spinella PC, Fenelus M, Liles D, Coyle T, Becker J, Jeng M, Gehrie EA, Spencer BR, Young P, Johnson A, O\u2019Brien JJ, Schiller GJ, Roback JD, Malynn E, Jackups R, Avecilla ST, Liu K, Bentow S, Varrone J, Benjamin RJ, Corash LM |
Blood Advances | 2024 |
Pathogenic role and clinical significance of neutrophils and neutrophil extracellular traps in idiopathic inflammatory myopathies
Liu R, Liu H, Yang L, Li C, Yin G, Xie Q |
Clinical and Experimental Medicine | 2024 |
Cathepsin C from extracellular histone-induced M1 alveolar macrophages promotes NETosis during lung ischemia-reperfusion injury
Yu J, Fu Y, Gao J, Zhang Q, Zhang N, Zhang Z, Jiang X, Chen C, Wen Z |
Redox Biology | 2024 |
The role of P-selectin/PSGL-1 in regulating NETs as a novel mechanism in cerebral ischemic injury
Li X, Ma Y, Wang D |
Frontiers in neurology | 2024 |
A Razor’s Edge: Vascular Responses to Acute Inflammatory Lung Injury/Acute Respiratory Distress Syndrome
Price DR, Garcia JG |
Annual Review of Physiology | 2024 |
PAI-1 Deficiency Promotes NET-mediated Pyroptosis and Ferroptosis during Pseudomonas Aeruginosa-induced Acute Lung Injury by Regulating the PI3K/MAPK/AKT Axis.
Aji N, Wang L, Wang S, Pan T, Song J, Chen C, Wang L, Feng N, Tang X, Song Y |
Inflammation | 2024 |
The incidence, risk factors, and prognosis of acute kidney injury in patients after cardiac surgery
Wang XD, Bao R, Lan Y, Zhao ZZ, Yang XY, Wang YY, Quan ZY, Wang JF, Bian JJ |
Frontiers in Cardiovascular Medicine | 2024 |
Neutrophil extracellular traps - an a-list-actor in a variety of diseases.
Wang N, Shi XL, Li D, Li BB, Liu P, Luo H |
Annals of Hematology | 2024 |
Nuclear Factor Erythroid 2-Related Factor 2 Intervenes the Release of Neutrophil Extracellular Traps during Lipopolysaccharide-Induced Acute Lung Injury in Mice.
Lu J, Xiong G, Li H, Zhang D, Zhang X |
Mediators of inflammation | 2024 |
Pulmonary Injury as a Complication of Urinary Tract Infection in Pregnancy.
Hafez W, Al Shareef J, Alyoussef A, Ghanem M, Abazid RR, Yadav A, Rashid A, Sayfoo FM, Venkataramani S, Restrepo PO, Elkott MM, Lakshman VS, Arief T, Mohammed AG, Abdulaal F, Hossam Y |
International journal of MCH and AIDS | 2024 |
Mast cell extracellular trap formation underlies vascular and neural injury and hyperalgesia in sickle cell disease.
Argueta DA, Tran H, Goel Y, Nguyen A, Nguyen J, Kiven SB, Chen C, Abdulla F, Vercellotti GM, Belcher JD, Gupta K |
Life science alliance | 2024 |
Crossing epigenetic frontiers: the intersection of novel histone modifications and diseases
Yao W, Hu X, Wang X |
Signal Transduction and Targeted Therapy | 2024 |
Neutrophil-fibroblast crosstalk drives immunofibrosis in Crohn’s disease through IFNα pathway
Gavriilidis E, Divolis G, Natsi AM, Kafalis N, Kogias D, Antoniadou C, Synolaki E, Pavlos E, Koutsi MA, Didaskalou S, Papadimitriou E, Tsironidou V, Gavriil A, Papadopoulos V, Agelopoulos M, Tsilingiris D, Koffa M, Giatromanolaki A, Kouklakis G, Ritis K, Skendros P |
Frontiers in Immunology | 2024 |
Neutrophil Extracellular Traps Affect Human Inner Ear Vascular Permeability
Sekulic M, Giaglis S, Chatelain N, Bodmer D, Petkovic V |
International Journal of Molecular Sciences | 2024 |
A Predictive Model for Disseminated Intravascular Coagulopathy in Sepsis: An Observational Study.
Fu Y, He Y, Zheng C, Zeng J, Ou H |
International journal of general medicine | 2024 |
SKAP1 Expression in Cancer Cells Enhances Colon Tumor Growth and Impairs Cytotoxic Immunity by Promoting Neutrophil Extracellular Trap Formation via the NFATc1/CXCL8 Axis.
Gao J, Liu J, Lu J, Zhang X, Zhang W, Li Q, Cai J, Li M, Gan Y, Tang Y, Wu S |
Advanced science (Weinheim, Baden-Wurttemberg, Germany) | 2024 |
Thromboinflammation is associated with clinical outcome after ST-elevation myocardial infarction
Benkhoff M, Alde K, Ehreiser V, Dahlmanns J, Metzen D, Haurand JM, Duse DA, Jung C, Kelm M, Petzold T, Polzin A |
Blood Advances | 2024 |
Atomic Force Microscopy and Scanning Ion-Conductance Microscopy for Investigation of Biomechanical Characteristics of Neutrophils
Shvedov M, Sherstyukova E, Kandrashina S, Inozemtsev V, Sergunova V |
Cells | 2024 |
Glycyrrhizin inhibits LPS-induced neutrophil-like release of NETs.
Shen Z, Gu J, Jiang B, Long H, Li Z, Chen C, Pei Z, Xia F |
American journal of translational research | 2024 |
Fostamatinib for Hospitalized Adults With COVID-19 and Hypoxemia: A Randomized Clinical Trial
Collins SP, Shotwell MS, Strich JR, Gibbs KW, de Wit M, Files DC, Harkins M, Hudock K, Merck LH, Moskowitz A, Apodaca KD, Barksdale A, Safdar B, Javaheri A, Sturek JM, Schrager H, Iovine NM, Tiffany B, Douglas I, Levitt J, Ginde AA, Hager DN, Shapiro N, Duggal A, Khan A, Lanspa M, Chen P, Gentile N, Harris E, Gong M, Sellers S, Goodwin AJ, Tidswell MA, Filbin M, Desai N, Gutiérrez F, Estrada V, Burgos J, Boyles T, Paño-Pardo JR, Hussen N, Rosenberg Y, Troendle J, Bernard GR, Bistran-Hall AJ, Walsh K, Casey JD, DeClercq J, Joly MM, Pulley J, Rice TW, Schildcrout JS, Wang L, Semler MW, Self WH |
JAMA Network Open | 2024 |
Malondialdehyde-specific natural IgM inhibit NETosis triggered by culprit site–derived extracellular vesicles from myocardial infarction patients
Ondracek AS, Afonyushkin T, Aszlan A, Taqi S, Koller T, Artner T, Porsch F, Resch U, Sharma S, Scherz T, Spittler A, Haertinger M, Hofbauer TM, Ozsvar-Kozma M, Seidl V, Beitzke D, Krueger M, Testori C, Lang IM, Binder CJ |
European Heart Journal | 2024 |