Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammation

Summary: Herein, we demonstrate that extracellular vesicles (EVs) present in healthy human plasma regulate macrophage activation by triggering MERTK-dependent signaling in a growth arrest-specific 6 (GAS6)- and protein S (PROS1)-dependent manner. Moreover, EVs regulate oxidative burst and degranulat...

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Main Authors: Martina P. Fabiano, Alan M. Adamczyk, Olesia A. Gololobova, Ignacio G. Mazzitelli, María L. Leicaj, Tomás M. Grosso, Paula S. Pérez, Cora L. Alvarez, Julieta Schachter, Silvina Palmer, Florencia Sabbione, Fernando A. Erra Díaz, Analía S. Trevani, Manuel Varas-Godoy, Eugenio A. Carrera Silva, Kenneth W. Witwer, Matías Ostrowski
Format: Article
Language:English
Published: Elsevier 2025-08-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124725008678
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author Martina P. Fabiano
Alan M. Adamczyk
Olesia A. Gololobova
Ignacio G. Mazzitelli
María L. Leicaj
Tomás M. Grosso
Paula S. Pérez
Cora L. Alvarez
Julieta Schachter
Silvina Palmer
Florencia Sabbione
Fernando A. Erra Díaz
Analía S. Trevani
Manuel Varas-Godoy
Eugenio A. Carrera Silva
Kenneth W. Witwer
Matías Ostrowski
author_facet Martina P. Fabiano
Alan M. Adamczyk
Olesia A. Gololobova
Ignacio G. Mazzitelli
María L. Leicaj
Tomás M. Grosso
Paula S. Pérez
Cora L. Alvarez
Julieta Schachter
Silvina Palmer
Florencia Sabbione
Fernando A. Erra Díaz
Analía S. Trevani
Manuel Varas-Godoy
Eugenio A. Carrera Silva
Kenneth W. Witwer
Matías Ostrowski
author_sort Martina P. Fabiano
collection DOAJ
description Summary: Herein, we demonstrate that extracellular vesicles (EVs) present in healthy human plasma regulate macrophage activation by triggering MERTK-dependent signaling in a growth arrest-specific 6 (GAS6)- and protein S (PROS1)-dependent manner. Moreover, EVs regulate oxidative burst and degranulation in neutrophils and the PAMP-stimulated secretion of the pro-inflammatory cytokine interleukin (IL)-1β while enhancing the secretion of the anti-inflammatory cytokine transforming growth factor beta (TGF-β). Neutrophil regulation is mediated by the biochemical activity of the EV-exposed extracellular nucleotidases CD39 and CD73, which degrade inflammatory extracellular ATP into anti-inflammatory adenosine. In turn, adenosine modulates neutrophil oxidative burst by acting through the A2A receptor. Additionally, we demonstrate that the incubation of live neutrophils with EVs enhances their interaction with macrophages, resulting in the formation of neutrophil-macrophage conjugates and the modulation of the macrophage response to an inflammatory stimulus. In conclusion, we propose that EVs from plasma serve as homeostatic regulators of inflammation by acting on multiple immune cell populations through distinct regulatory mechanisms.
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spelling doaj-art-6b6f16921e694ba9bb5a89aaa49e84592025-08-20T02:52:37ZengElsevierCell Reports2211-12472025-08-0144811609610.1016/j.celrep.2025.116096Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammationMartina P. Fabiano0Alan M. Adamczyk1Olesia A. Gololobova2Ignacio G. Mazzitelli3María L. Leicaj4Tomás M. Grosso5Paula S. Pérez6Cora L. Alvarez7Julieta Schachter8Silvina Palmer9Florencia Sabbione10Fernando A. Erra Díaz11Analía S. Trevani12Manuel Varas-Godoy13Eugenio A. Carrera Silva14Kenneth W. Witwer15Matías Ostrowski16Instituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, Argentina; Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, ArgentinaInstituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, Argentina; Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, ArgentinaDepartment of Comparative and Molecular Pathobiology, Johns Hopkins University School of Medicine, Baltimore, MD, USAInstituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, Argentina; Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, ArgentinaInstituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, ArgentinaInstituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, ArgentinaInstituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, ArgentinaInstituto de Química y Físico-Química Biológicas “Prof. Alejandro C. Paladini,” Universidad de Buenos Aires (UBA), CONICET, Buenos Aires, ArgentinaInstituto de Química y Físico-Química Biológicas “Prof. Alejandro C. Paladini,” Universidad de Buenos Aires (UBA), CONICET, Buenos Aires, ArgentinaServicio de Hematología, Hospital Británico, Buenos Aires, ArgentinaLaboratorio de inmunidad innata, Instituto de Medicina Experimental (IMEX)—CONICET, Academia Nacional de Medicina (ANM), Buenos Aires, Argentina; Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, ArgentinaInstituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, Argentina; Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, ArgentinaLaboratorio de inmunidad innata, Instituto de Medicina Experimental (IMEX)—CONICET, Academia Nacional de Medicina (ANM), Buenos Aires, Argentina; Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, ArgentinaCancer Cell Biology Lab, CEBICEM, Facultad de Ciencias, Universidad San Sebastián, Santiago, Chile; Centro Ciencia & Vida, Fundación Ciencia & Vida, Santiago, ChileLaboratorio de Trombosis Experimental e Inmunobiología de la Inflamación, IMEX, CONICET, ANM, Ciudad de Buenos Aires, ArgentinaDepartment of Comparative and Molecular Pathobiology, Johns Hopkins University School of Medicine, Baltimore, MD, USA; The Richman Family Precision Medicine Center of Excellence in Alzheimer’s Disease, Johns Hopkins University School of Medicine, Baltimore, MD, USA; Corresponding authorInstituto de Investigaciones Biomédicas en Retrovirus y SIDA (INBIRS), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Facultad de Medicina, Universidad de Buenos Aires (UBA), Buenos Aires, Argentina; Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina; Corresponding authorSummary: Herein, we demonstrate that extracellular vesicles (EVs) present in healthy human plasma regulate macrophage activation by triggering MERTK-dependent signaling in a growth arrest-specific 6 (GAS6)- and protein S (PROS1)-dependent manner. Moreover, EVs regulate oxidative burst and degranulation in neutrophils and the PAMP-stimulated secretion of the pro-inflammatory cytokine interleukin (IL)-1β while enhancing the secretion of the anti-inflammatory cytokine transforming growth factor beta (TGF-β). Neutrophil regulation is mediated by the biochemical activity of the EV-exposed extracellular nucleotidases CD39 and CD73, which degrade inflammatory extracellular ATP into anti-inflammatory adenosine. In turn, adenosine modulates neutrophil oxidative burst by acting through the A2A receptor. Additionally, we demonstrate that the incubation of live neutrophils with EVs enhances their interaction with macrophages, resulting in the formation of neutrophil-macrophage conjugates and the modulation of the macrophage response to an inflammatory stimulus. In conclusion, we propose that EVs from plasma serve as homeostatic regulators of inflammation by acting on multiple immune cell populations through distinct regulatory mechanisms.http://www.sciencedirect.com/science/article/pii/S2211124725008678CP: Immunology
spellingShingle Martina P. Fabiano
Alan M. Adamczyk
Olesia A. Gololobova
Ignacio G. Mazzitelli
María L. Leicaj
Tomás M. Grosso
Paula S. Pérez
Cora L. Alvarez
Julieta Schachter
Silvina Palmer
Florencia Sabbione
Fernando A. Erra Díaz
Analía S. Trevani
Manuel Varas-Godoy
Eugenio A. Carrera Silva
Kenneth W. Witwer
Matías Ostrowski
Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammation
Cell Reports
CP: Immunology
title Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammation
title_full Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammation
title_fullStr Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammation
title_full_unstemmed Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammation
title_short Plasma extracellular vesicle surface-located GAS6/PROS1 and CD39/CD73 attenuate inflammation
title_sort plasma extracellular vesicle surface located gas6 pros1 and cd39 cd73 attenuate inflammation
topic CP: Immunology
url http://www.sciencedirect.com/science/article/pii/S2211124725008678
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