Programmed ‘disarming’ of the neutrophil proteome reduces the magnitude of inflammation

Jose M. Adrover; Alejandra Aroca-Crevillén; Georgiana Crainiciuc; Fernando Ostos; Yeny Rojas-Vega; Andrea Rubio-Ponce; Catia Cilloniz; Elena Bonzón-Kulichenko; Enrique Calvo; Daniel Rico; María A. Moro; Christian Weber; Ignacio Lizasoaín; Antoni Torres; Jesús Ruiz-Cabello; Jesús Vázquez; Andrés Hidalgo

doi:10.1038/s41590-019-0571-2

Programmed ‘disarming’ of the neutrophil proteome reduces the magnitude of inflammation

Jose M. Adrover, Alejandra Aroca-Crevillén, Georgiana Crainiciuc, Fernando Ostos, Yeny Rojas-Vega, Andrea Rubio-Ponce, Catia Cilloniz, Elena Bonzón-Kulichenko, Enrique Calvo, Daniel Rico, María A. Moro, Christian Weber, Ignacio Lizasoaín, Antoni Torres, Jesús Ruiz-Cabello, Jesús Vázquez, Andrés Hidalgo

Producción científica: Artículo Científico › Artículo original › revisión exhaustiva

218 Citas (Scopus)

Resumen

The antimicrobial functions of neutrophils are facilitated by a defensive armamentarium of proteins stored in granules, and by the formation of neutrophil extracellular traps (NETs). However, the toxic nature of these structures poses a threat to highly vascularized tissues, such as the lungs. Here, we identified a cell-intrinsic program that modified the neutrophil proteome in the circulation and caused the progressive loss of granule content and reduction of the NET-forming capacity. This program was driven by the receptor CXCR2 and by regulators of circadian cycles. As a consequence, lungs were protected from inflammatory injury at times of day or in mouse mutants in which granule content was low. Changes in the proteome, granule content and NET formation also occurred in human neutrophils, and correlated with the incidence and severity of respiratory distress in pneumonia patients. Our findings unveil a ‘disarming’ strategy of neutrophils that depletes protein stores to reduce the magnitude of inflammation.

Idioma original	Inglés estadounidense
Páginas (desde-hasta)	135-144
-	10
Publicación	Nature Immunology
Volumen	21
N.º	2
DOI	https://doi.org/10.1038/s41590-019-0571-2
Estado	Indizado - 1 feb. 2020
Publicado de forma externa	Sí

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Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.

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Adrover, J. M., Aroca-Crevillén, A., Crainiciuc, G., Ostos, F., Rojas-Vega, Y., Rubio-Ponce, A., Cilloniz, C., Bonzón-Kulichenko, E., Calvo, E., Rico, D., Moro, M. A., Weber, C., Lizasoaín, I., Torres, A., Ruiz-Cabello, J., Vázquez, J., & Hidalgo, A. (2020). Programmed ‘disarming’ of the neutrophil proteome reduces the magnitude of inflammation. Nature Immunology, 21(2), 135-144. https://doi.org/10.1038/s41590-019-0571-2

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title = "Programmed {\textquoteleft}disarming{\textquoteright} of the neutrophil proteome reduces the magnitude of inflammation",

abstract = "The antimicrobial functions of neutrophils are facilitated by a defensive armamentarium of proteins stored in granules, and by the formation of neutrophil extracellular traps (NETs). However, the toxic nature of these structures poses a threat to highly vascularized tissues, such as the lungs. Here, we identified a cell-intrinsic program that modified the neutrophil proteome in the circulation and caused the progressive loss of granule content and reduction of the NET-forming capacity. This program was driven by the receptor CXCR2 and by regulators of circadian cycles. As a consequence, lungs were protected from inflammatory injury at times of day or in mouse mutants in which granule content was low. Changes in the proteome, granule content and NET formation also occurred in human neutrophils, and correlated with the incidence and severity of respiratory distress in pneumonia patients. Our findings unveil a {\textquoteleft}disarming{\textquoteright} strategy of neutrophils that depletes protein stores to reduce the magnitude of inflammation.",

author = "Adrover, \{Jose M.\} and Alejandra Aroca-Crevill{\'e}n and Georgiana Crainiciuc and Fernando Ostos and Yeny Rojas-Vega and Andrea Rubio-Ponce and Catia Cilloniz and Elena Bonz{\'o}n-Kulichenko and Enrique Calvo and Daniel Rico and Moro, \{Mar{\'i}a A.\} and Christian Weber and Ignacio Lizasoa{\'i}n and Antoni Torres and Jes{\'u}s Ruiz-Cabello and Jes{\'u}s V{\'a}zquez and Andr{\'e}s Hidalgo",

note = "Publisher Copyright: {\textcopyright} 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.",

year = "2020",

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doi = "10.1038/s41590-019-0571-2",

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Adrover, JM, Aroca-Crevillén, A, Crainiciuc, G, Ostos, F, Rojas-Vega, Y, Rubio-Ponce, A, Cilloniz, C, Bonzón-Kulichenko, E, Calvo, E, Rico, D, Moro, MA, Weber, C, Lizasoaín, I, Torres, A, Ruiz-Cabello, J, Vázquez, J & Hidalgo, A 2020, 'Programmed ‘disarming’ of the neutrophil proteome reduces the magnitude of inflammation', Nature Immunology, vol. 21, n.º 2, pp. 135-144. https://doi.org/10.1038/s41590-019-0571-2

TY - JOUR

T1 - Programmed ‘disarming’ of the neutrophil proteome reduces the magnitude of inflammation

AU - Adrover, Jose M.

AU - Aroca-Crevillén, Alejandra

AU - Crainiciuc, Georgiana

AU - Ostos, Fernando

AU - Rojas-Vega, Yeny

AU - Rubio-Ponce, Andrea

AU - Cilloniz, Catia

AU - Bonzón-Kulichenko, Elena

AU - Calvo, Enrique

AU - Rico, Daniel

AU - Moro, María A.

AU - Weber, Christian

AU - Lizasoaín, Ignacio

AU - Torres, Antoni

AU - Ruiz-Cabello, Jesús

AU - Vázquez, Jesús

AU - Hidalgo, Andrés

PY - 2020/2/1

Y1 - 2020/2/1

N2 - The antimicrobial functions of neutrophils are facilitated by a defensive armamentarium of proteins stored in granules, and by the formation of neutrophil extracellular traps (NETs). However, the toxic nature of these structures poses a threat to highly vascularized tissues, such as the lungs. Here, we identified a cell-intrinsic program that modified the neutrophil proteome in the circulation and caused the progressive loss of granule content and reduction of the NET-forming capacity. This program was driven by the receptor CXCR2 and by regulators of circadian cycles. As a consequence, lungs were protected from inflammatory injury at times of day or in mouse mutants in which granule content was low. Changes in the proteome, granule content and NET formation also occurred in human neutrophils, and correlated with the incidence and severity of respiratory distress in pneumonia patients. Our findings unveil a ‘disarming’ strategy of neutrophils that depletes protein stores to reduce the magnitude of inflammation.

AB - The antimicrobial functions of neutrophils are facilitated by a defensive armamentarium of proteins stored in granules, and by the formation of neutrophil extracellular traps (NETs). However, the toxic nature of these structures poses a threat to highly vascularized tissues, such as the lungs. Here, we identified a cell-intrinsic program that modified the neutrophil proteome in the circulation and caused the progressive loss of granule content and reduction of the NET-forming capacity. This program was driven by the receptor CXCR2 and by regulators of circadian cycles. As a consequence, lungs were protected from inflammatory injury at times of day or in mouse mutants in which granule content was low. Changes in the proteome, granule content and NET formation also occurred in human neutrophils, and correlated with the incidence and severity of respiratory distress in pneumonia patients. Our findings unveil a ‘disarming’ strategy of neutrophils that depletes protein stores to reduce the magnitude of inflammation.

UR - https://www.scopus.com/pages/publications/85077898671

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DO - 10.1038/s41590-019-0571-2

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AN - SCOPUS:85077898671

SN - 1529-2908

VL - 21

SP - 135

EP - 144

JO - Nature Immunology

JF - Nature Immunology

IS - 2

ER -

Programmed ‘disarming’ of the neutrophil proteome reduces the magnitude of inflammation

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