Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regeneration

Skeletal muscle is one of the most abundant tissues of the human body and is responsible for the generation of movement. Muscle injuries can lead to severe disability. Skeletal muscle is characterized by an important regeneration capacity, which is possible due to the interaction between the myoblas...

Full description

Bibliographic Details
Main Authors: Jiram Torres-Ruiz, Beatriz Alcalá-Carmona, Ricardo Alejandre-Aguilar, Diana Gómez-Martín
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2023.1113214/full
_version_ 1797894278495600640
author Jiram Torres-Ruiz
Beatriz Alcalá-Carmona
Beatriz Alcalá-Carmona
Ricardo Alejandre-Aguilar
Diana Gómez-Martín
author_facet Jiram Torres-Ruiz
Beatriz Alcalá-Carmona
Beatriz Alcalá-Carmona
Ricardo Alejandre-Aguilar
Diana Gómez-Martín
author_sort Jiram Torres-Ruiz
collection DOAJ
description Skeletal muscle is one of the most abundant tissues of the human body and is responsible for the generation of movement. Muscle injuries can lead to severe disability. Skeletal muscle is characterized by an important regeneration capacity, which is possible due to the interaction between the myoblasts and immune cells. Neutrophils are fundamental as inducers of muscle damage and as promoters of the initial inflammatory response which eventually allows the muscle repair. The main functions of the neutrophils are phagocytosis, respiratory burst, degranulation, and the production of neutrophil extracellular traps (NETs). An overactivation of neutrophils after muscle injuries may lead to an expansion of the initial damage and can hamper the successful muscle repair. The importance of neutrophils as inducers of muscle damage extends beyond acute muscle injury and recently, neutrophils have become more relevant as part of the immunopathogenesis of chronic muscle diseases like idiopathic inflammatory myopathies (IIM). This heterogeneous group of systemic autoimmune diseases is characterized by the presence of muscle inflammation with a variable amount of extramuscular features. In IIM, neutrophils have been found to have a role as biomarkers of disease activity, and their expansion in peripheral blood is related to certain clinical features like interstitial lung disease (ILD) and cancer. On the other hand, low density granulocytes (LDG) are a distinctive subtype of neutrophils characterized by an enhanced production of NETs. These cells along with the NETs have also been related to disease activity and certain clinical features like ILD, vasculopathy, calcinosis, dermatosis, and cutaneous ulcers. The role of NETs in the immunopathogenesis of IIM is supported by an enhanced production and deficient degradation of NETs that have been observed in patients with dermatomyositis and anti-synthetase syndrome. Finally, new interest has arisen in the study of other phenotypes of LDG with a phenotype corresponding to myeloid-derived suppressor cells, which were also found to be expanded in patients with IIM and were related to disease activity. In this review, we discuss the role of neutrophils as both orchestrators of muscle repair and inducers of muscle damage, focusing on the immunopathogenesis of IIM.
first_indexed 2024-04-10T07:07:31Z
format Article
id doaj.art-a98c92fa124944779e7091f2cdff2006
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-04-10T07:07:31Z
publishDate 2023-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-a98c92fa124944779e7091f2cdff20062023-02-27T06:36:46ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-02-011410.3389/fimmu.2023.11132141113214Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regenerationJiram Torres-Ruiz0Beatriz Alcalá-Carmona1Beatriz Alcalá-Carmona2Ricardo Alejandre-Aguilar3Diana Gómez-Martín4Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, MexicoDepartment of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, MexicoLaboratory of Entomology, Department of Parasitology, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoLaboratory of Entomology, Department of Parasitology, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico City, MexicoDepartment of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, MexicoSkeletal muscle is one of the most abundant tissues of the human body and is responsible for the generation of movement. Muscle injuries can lead to severe disability. Skeletal muscle is characterized by an important regeneration capacity, which is possible due to the interaction between the myoblasts and immune cells. Neutrophils are fundamental as inducers of muscle damage and as promoters of the initial inflammatory response which eventually allows the muscle repair. The main functions of the neutrophils are phagocytosis, respiratory burst, degranulation, and the production of neutrophil extracellular traps (NETs). An overactivation of neutrophils after muscle injuries may lead to an expansion of the initial damage and can hamper the successful muscle repair. The importance of neutrophils as inducers of muscle damage extends beyond acute muscle injury and recently, neutrophils have become more relevant as part of the immunopathogenesis of chronic muscle diseases like idiopathic inflammatory myopathies (IIM). This heterogeneous group of systemic autoimmune diseases is characterized by the presence of muscle inflammation with a variable amount of extramuscular features. In IIM, neutrophils have been found to have a role as biomarkers of disease activity, and their expansion in peripheral blood is related to certain clinical features like interstitial lung disease (ILD) and cancer. On the other hand, low density granulocytes (LDG) are a distinctive subtype of neutrophils characterized by an enhanced production of NETs. These cells along with the NETs have also been related to disease activity and certain clinical features like ILD, vasculopathy, calcinosis, dermatosis, and cutaneous ulcers. The role of NETs in the immunopathogenesis of IIM is supported by an enhanced production and deficient degradation of NETs that have been observed in patients with dermatomyositis and anti-synthetase syndrome. Finally, new interest has arisen in the study of other phenotypes of LDG with a phenotype corresponding to myeloid-derived suppressor cells, which were also found to be expanded in patients with IIM and were related to disease activity. In this review, we discuss the role of neutrophils as both orchestrators of muscle repair and inducers of muscle damage, focusing on the immunopathogenesis of IIM.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1113214/fullmuscle regenerationneutrophilsneutrophil extracellular trapslow density granulocytesmyositis
spellingShingle Jiram Torres-Ruiz
Beatriz Alcalá-Carmona
Beatriz Alcalá-Carmona
Ricardo Alejandre-Aguilar
Diana Gómez-Martín
Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regeneration
Frontiers in Immunology
muscle regeneration
neutrophils
neutrophil extracellular traps
low density granulocytes
myositis
title Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regeneration
title_full Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regeneration
title_fullStr Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regeneration
title_full_unstemmed Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regeneration
title_short Inflammatory myopathies and beyond: The dual role of neutrophils in muscle damage and regeneration
title_sort inflammatory myopathies and beyond the dual role of neutrophils in muscle damage and regeneration
topic muscle regeneration
neutrophils
neutrophil extracellular traps
low density granulocytes
myositis
url https://www.frontiersin.org/articles/10.3389/fimmu.2023.1113214/full
work_keys_str_mv AT jiramtorresruiz inflammatorymyopathiesandbeyondthedualroleofneutrophilsinmuscledamageandregeneration
AT beatrizalcalacarmona inflammatorymyopathiesandbeyondthedualroleofneutrophilsinmuscledamageandregeneration
AT beatrizalcalacarmona inflammatorymyopathiesandbeyondthedualroleofneutrophilsinmuscledamageandregeneration
AT ricardoalejandreaguilar inflammatorymyopathiesandbeyondthedualroleofneutrophilsinmuscledamageandregeneration
AT dianagomezmartin inflammatorymyopathiesandbeyondthedualroleofneutrophilsinmuscledamageandregeneration