Neutrophil "plucking" on megakaryocytes drives platelet production and boosts cardiovascular disease

Intravascular neutrophils and platelets collaborate in maintaining host integrity, but their interaction can also trigger thrombotic complications. We report here that cooperation between neutrophil and platelet lineages extends to the earliest stages of platelet formation by megakaryocytes in the b...

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Vydané v:	Immunity (Cambridge, Mass.) Ročník 55; číslo 12; s. 2285
Hlavní autori:	Petzold, Tobias, Zhang, Zhe, Ballesteros, Iván, Saleh, Inas, Polzin, Amin, Thienel, Manuela, Liu, Lulu, Ul Ain, Qurrat, Ehreiser, Vincent, Weber, Christian, Kilani, Badr, Mertsch, Pontus, Götschke, Jeremias, Cremer, Sophie, Fu, Wenwen, Lorenz, Michael, Ishikawa-Ankerhold, Hellen, Raatz, Elisabeth, El-Nemr, Shaza, Görlach, Agnes, Marhuenda, Esther, Stark, Konstantin, Pircher, Joachim, Stegner, David, Gieger, Christian, Schmidt-Supprian, Marc, Gaertner, Florian, Almendros, Isaac, Kelm, Malte, Schulz, Christian, Hidalgo, Andrés, Massberg, Steffen
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States 13.12.2022
Predmet:	Blood Platelets - physiology Cardiovascular Diseases Humans Megakaryocytes Myocardial Infarction Neutrophils Thrombopoiesis Thrombosis thromboinflammation thrombosis neutrophils thrombopoiesis mechanotransduction bone marrow
ISSN:	1097-4180, 1097-4180
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Abstract	Intravascular neutrophils and platelets collaborate in maintaining host integrity, but their interaction can also trigger thrombotic complications. We report here that cooperation between neutrophil and platelet lineages extends to the earliest stages of platelet formation by megakaryocytes in the bone marrow. Using intravital microscopy, we show that neutrophils "plucked" intravascular megakaryocyte extensions, termed proplatelets, to control platelet production. Following CXCR4-CXCL12-dependent migration towards perisinusoidal megakaryocytes, plucking neutrophils actively pulled on proplatelets and triggered myosin light chain and extracellular-signal-regulated kinase activation through reactive oxygen species. By these mechanisms, neutrophils accelerate proplatelet growth and facilitate continuous release of platelets in steady state. Following myocardial infarction, plucking neutrophils drove excessive release of young, reticulated platelets and boosted the risk of recurrent ischemia. Ablation of neutrophil plucking normalized thrombopoiesis and reduced recurrent thrombosis after myocardial infarction and thrombus burden in venous thrombosis. We establish neutrophil plucking as a target to reduce thromboischemic events.
AbstractList	Intravascular neutrophils and platelets collaborate in maintaining host integrity, but their interaction can also trigger thrombotic complications. We report here that cooperation between neutrophil and platelet lineages extends to the earliest stages of platelet formation by megakaryocytes in the bone marrow. Using intravital microscopy, we show that neutrophils "plucked" intravascular megakaryocyte extensions, termed proplatelets, to control platelet production. Following CXCR4-CXCL12-dependent migration towards perisinusoidal megakaryocytes, plucking neutrophils actively pulled on proplatelets and triggered myosin light chain and extracellular-signal-regulated kinase activation through reactive oxygen species. By these mechanisms, neutrophils accelerate proplatelet growth and facilitate continuous release of platelets in steady state. Following myocardial infarction, plucking neutrophils drove excessive release of young, reticulated platelets and boosted the risk of recurrent ischemia. Ablation of neutrophil plucking normalized thrombopoiesis and reduced recurrent thrombosis after myocardial infarction and thrombus burden in venous thrombosis. We establish neutrophil plucking as a target to reduce thromboischemic events.Intravascular neutrophils and platelets collaborate in maintaining host integrity, but their interaction can also trigger thrombotic complications. We report here that cooperation between neutrophil and platelet lineages extends to the earliest stages of platelet formation by megakaryocytes in the bone marrow. Using intravital microscopy, we show that neutrophils "plucked" intravascular megakaryocyte extensions, termed proplatelets, to control platelet production. Following CXCR4-CXCL12-dependent migration towards perisinusoidal megakaryocytes, plucking neutrophils actively pulled on proplatelets and triggered myosin light chain and extracellular-signal-regulated kinase activation through reactive oxygen species. By these mechanisms, neutrophils accelerate proplatelet growth and facilitate continuous release of platelets in steady state. Following myocardial infarction, plucking neutrophils drove excessive release of young, reticulated platelets and boosted the risk of recurrent ischemia. Ablation of neutrophil plucking normalized thrombopoiesis and reduced recurrent thrombosis after myocardial infarction and thrombus burden in venous thrombosis. We establish neutrophil plucking as a target to reduce thromboischemic events. Intravascular neutrophils and platelets collaborate in maintaining host integrity, but their interaction can also trigger thrombotic complications. We report here that cooperation between neutrophil and platelet lineages extends to the earliest stages of platelet formation by megakaryocytes in the bone marrow. Using intravital microscopy, we show that neutrophils "plucked" intravascular megakaryocyte extensions, termed proplatelets, to control platelet production. Following CXCR4-CXCL12-dependent migration towards perisinusoidal megakaryocytes, plucking neutrophils actively pulled on proplatelets and triggered myosin light chain and extracellular-signal-regulated kinase activation through reactive oxygen species. By these mechanisms, neutrophils accelerate proplatelet growth and facilitate continuous release of platelets in steady state. Following myocardial infarction, plucking neutrophils drove excessive release of young, reticulated platelets and boosted the risk of recurrent ischemia. Ablation of neutrophil plucking normalized thrombopoiesis and reduced recurrent thrombosis after myocardial infarction and thrombus burden in venous thrombosis. We establish neutrophil plucking as a target to reduce thromboischemic events.
Author	Mertsch, Pontus Pircher, Joachim Stegner, David Ballesteros, Iván Zhang, Zhe Lorenz, Michael Kelm, Malte Fu, Wenwen Raatz, Elisabeth Weber, Christian Cremer, Sophie Almendros, Isaac Massberg, Steffen Görlach, Agnes Gieger, Christian Stark, Konstantin Marhuenda, Esther Thienel, Manuela Petzold, Tobias Götschke, Jeremias Ehreiser, Vincent Kilani, Badr Hidalgo, Andrés Polzin, Amin Schmidt-Supprian, Marc Ishikawa-Ankerhold, Hellen Schulz, Christian El-Nemr, Shaza Gaertner, Florian Ul Ain, Qurrat Saleh, Inas Liu, Lulu
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Vascular Biology and Therapeutics Program and Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06510, USA – sequence: 32 givenname: Steffen surname: Massberg fullname: Massberg, Steffen email: steffen.massberg@med.uni-muenchen.de organization: Medizinische Klinik und Poliklinik I, Klinikum der Universität München, Ludwig-Maximilians- University Munich, 81377 Munich, Germany; Partner site Munich Heart Alliance, DZHK (German Centre for Cardiovascular Research), 80802 Munich, Germany; Institute of Surgical Research at the Walter-Brendel-Centre of Experimental Medicine, Klinikum der Universität München, Ludwig-Maximilians- University Munich, 81377 Munich, Germany. Electronic address: steffen.massberg@med.uni-muenchen.de
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Snippet	Intravascular neutrophils and platelets collaborate in maintaining host integrity, but their interaction can also trigger thrombotic complications. We report...
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SubjectTerms	Blood Platelets - physiology Cardiovascular Diseases Humans Megakaryocytes Myocardial Infarction Neutrophils Thrombopoiesis Thrombosis
Title	Neutrophil "plucking" on megakaryocytes drives platelet production and boosts cardiovascular disease
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