Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype

Skeletal muscle regeneration is a complex process involving crosstalk between immune cells and myogenic precursor cells, i.e., satellite cells. In this scenario, macrophage recruitment in damaged muscles is a mandatory step for tissue repair since pro-inflammatory M1 macrophages promote the activati...

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Autores principales:	Paulina Roux-Biejat, Marco Coazzoli, Pasquale Marrazzo, Silvia Zecchini, Ilaria Di Renzo, Cecilia Prata, Alessandra Napoli, Claudia Moscheni, Matteo Giovarelli, Maria Cristina Barbalace, Elisabetta Catalani, Maria Teresa Bassi, Clara De Palma, Davide Cervia, Marco Malaguti, Silvana Hrelia, Emilio Clementi, Cristiana Perrotta
Formato:	article
Lenguaje:	EN
Publicado:	MDPI AG 2021
Materias:	acid sphingomyelinase muscle regeneration macrophage phenotype inflammation Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/16971eb7aebc4553b086140f94e3f576
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spelling	oai:doaj.org-article:16971eb7aebc4553b086140f94e3f5762021-11-25T17:10:32ZAcid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype10.3390/cells101130282073-4409https://doaj.org/article/16971eb7aebc4553b086140f94e3f5762021-11-01T00:00:00Zhttps://www.mdpi.com/2073-4409/10/11/3028https://doaj.org/toc/2073-4409Skeletal muscle regeneration is a complex process involving crosstalk between immune cells and myogenic precursor cells, i.e., satellite cells. In this scenario, macrophage recruitment in damaged muscles is a mandatory step for tissue repair since pro-inflammatory M1 macrophages promote the activation of satellite cells, stimulating their proliferation and then, after switching into anti-inflammatory M2 macrophages, they prompt satellite cells’ differentiation into myotubes and resolve inflammation. Here, we show that acid sphingomyelinase (ASMase), a key enzyme in sphingolipid metabolism, is activated after skeletal muscle injury induced in vivo by the injection of cardiotoxin. ASMase ablation shortens the early phases of skeletal muscle regeneration without affecting satellite cell behavior. Of interest, ASMase regulates the balance between M1 and M2 macrophages in the injured muscles so that the absence of the enzyme reduces inflammation. The analysis of macrophage populations indicates that these events depend on the altered polarization of M1 macrophages towards an M2 phenotype. Our results unravel a novel role of ASMase in regulating immune response during muscle regeneration/repair and suggest ASMase as a supplemental therapeutic target in conditions of redundant inflammation that impairs muscle recovery.Paulina Roux-BiejatMarco CoazzoliPasquale MarrazzoSilvia ZecchiniIlaria Di RenzoCecilia PrataAlessandra NapoliClaudia MoscheniMatteo GiovarelliMaria Cristina BarbalaceElisabetta CatalaniMaria Teresa BassiClara De PalmaDavide CerviaMarco MalagutiSilvana HreliaEmilio ClementiCristiana PerrottaMDPI AGarticleacid sphingomyelinasemuscle regenerationmacrophage phenotypeinflammationBiology (General)QH301-705.5ENCells, Vol 10, Iss 3028, p 3028 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	acid sphingomyelinase muscle regeneration macrophage phenotype inflammation Biology (General) QH301-705.5
spellingShingle	acid sphingomyelinase muscle regeneration macrophage phenotype inflammation Biology (General) QH301-705.5 Paulina Roux-Biejat Marco Coazzoli Pasquale Marrazzo Silvia Zecchini Ilaria Di Renzo Cecilia Prata Alessandra Napoli Claudia Moscheni Matteo Giovarelli Maria Cristina Barbalace Elisabetta Catalani Maria Teresa Bassi Clara De Palma Davide Cervia Marco Malaguti Silvana Hrelia Emilio Clementi Cristiana Perrotta Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype
description	Skeletal muscle regeneration is a complex process involving crosstalk between immune cells and myogenic precursor cells, i.e., satellite cells. In this scenario, macrophage recruitment in damaged muscles is a mandatory step for tissue repair since pro-inflammatory M1 macrophages promote the activation of satellite cells, stimulating their proliferation and then, after switching into anti-inflammatory M2 macrophages, they prompt satellite cells’ differentiation into myotubes and resolve inflammation. Here, we show that acid sphingomyelinase (ASMase), a key enzyme in sphingolipid metabolism, is activated after skeletal muscle injury induced in vivo by the injection of cardiotoxin. ASMase ablation shortens the early phases of skeletal muscle regeneration without affecting satellite cell behavior. Of interest, ASMase regulates the balance between M1 and M2 macrophages in the injured muscles so that the absence of the enzyme reduces inflammation. The analysis of macrophage populations indicates that these events depend on the altered polarization of M1 macrophages towards an M2 phenotype. Our results unravel a novel role of ASMase in regulating immune response during muscle regeneration/repair and suggest ASMase as a supplemental therapeutic target in conditions of redundant inflammation that impairs muscle recovery.
format	article
author	Paulina Roux-Biejat Marco Coazzoli Pasquale Marrazzo Silvia Zecchini Ilaria Di Renzo Cecilia Prata Alessandra Napoli Claudia Moscheni Matteo Giovarelli Maria Cristina Barbalace Elisabetta Catalani Maria Teresa Bassi Clara De Palma Davide Cervia Marco Malaguti Silvana Hrelia Emilio Clementi Cristiana Perrotta
author_facet	Paulina Roux-Biejat Marco Coazzoli Pasquale Marrazzo Silvia Zecchini Ilaria Di Renzo Cecilia Prata Alessandra Napoli Claudia Moscheni Matteo Giovarelli Maria Cristina Barbalace Elisabetta Catalani Maria Teresa Bassi Clara De Palma Davide Cervia Marco Malaguti Silvana Hrelia Emilio Clementi Cristiana Perrotta
author_sort	Paulina Roux-Biejat
title	Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype
title_short	Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype
title_full	Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype
title_fullStr	Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype
title_full_unstemmed	Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype
title_sort	acid sphingomyelinase controls early phases of skeletal muscle regeneration by shaping the macrophage phenotype
publisher	MDPI AG
publishDate	2021
url	https://doaj.org/article/16971eb7aebc4553b086140f94e3f576
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Acid Sphingomyelinase Controls Early Phases of Skeletal Muscle Regeneration by Shaping the Macrophage Phenotype

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