Single-cell analysis of skeletal muscle macrophages reveals age-associated functional subpopulations

Tissue-resident macrophages represent a group of highly responsive innate immune cells that acquire diverse functions by polarizing toward distinct subpopulations. The subpopulations of macrophages that reside in skeletal muscle (SKM) and their changes during aging are poorly characterized. By singl...

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Veröffentlicht in:	eLife Jg. 11
Hauptverfasser:	Krasniewski, Linda K, Chakraborty, Papiya, Cui, Chang-Yi, Mazan-Mamczarz, Krystyna, Dunn, Christopher, Piao, Yulan, Fan, Jinshui, Shi, Changyou, Wallace, Tonya, Nguyen, Cuong, Rathbun, Isabelle A, Munk, Rachel, Tsitsipatis, Dimitrios, De, Supriyo, Sen, Payel, Ferrucci, Luigi, Gorospe, Myriam
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	England eLife Sciences Publications Ltd 19.10.2022 eLife Sciences Publications, Ltd
Schlagworte:	Aging Animals Approximation Biomarkers - metabolism Cell adhesion & migration Cell Biology Cell growth Cytokines Flow cytometry Gene expression Genomics Inflammation Lyve1 Macrophages Macrophages - metabolism Male MHCII Mice Muscle, Skeletal - metabolism muscle-resident macrophages Musculoskeletal system Neutrophils Ontology Phagocytes Phagocytes - metabolism Proteins Senescence Single-Cell Analysis Skeletal muscle Transcriptome Transcriptomics mouse Lyve1 cell biology MHCII flow cytometry aging muscle-resident macrophages single-cell analysis
ISSN:	2050-084X, 2050-084X
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Abstract	Tissue-resident macrophages represent a group of highly responsive innate immune cells that acquire diverse functions by polarizing toward distinct subpopulations. The subpopulations of macrophages that reside in skeletal muscle (SKM) and their changes during aging are poorly characterized. By single-cell transcriptomic analysis with unsupervised clustering, we found 11 distinct macrophage clusters in male mouse SKM with enriched gene expression programs linked to reparative, proinflammatory, phagocytic, proliferative, and senescence-associated functions. Using a complementary classification, membrane markers LYVE1 and MHCII identified four macrophage subgroups: LYVE1−/MHCII hi (M1-like, classically activated), LYVE1+/MHCII lo (M2-like, alternatively activated), and two new subgroups, LYVE1+/MHCII hi and LYVE1−/MHCII lo . Notably, one new subgroup, LYVE1+/MHCII hi , had traits of both M2 and M1 macrophages, while the other new subgroup, LYVE1−/MHCII lo , displayed strong phagocytic capacity. Flow cytometric analysis validated the presence of the four macrophage subgroups in SKM and found that LYVE1− macrophages were more abundant than LYVE1+ macrophages in old SKM. A striking increase in proinflammatory markers ( S100a8 and S100a9 mRNAs) and senescence-related markers ( Gpnmb and Spp1 mRNAs) was evident in macrophage clusters from older mice. In sum, we have identified dynamically polarized SKM macrophages and propose that specific macrophage subpopulations contribute to the proinflammatory and senescent traits of old SKM.
AbstractList	Tissue-resident macrophages represent a group of highly responsive innate immune cells that acquire diverse functions by polarizing toward distinct subpopulations. The subpopulations of macrophages that reside in skeletal muscle (SKM) and their changes during aging are poorly characterized. By single-cell transcriptomic analysis with unsupervised clustering, we found 11 distinct macrophage clusters in male mouse SKM with enriched gene expression programs linked to reparative, proinflammatory, phagocytic, proliferative, and senescence-associated functions. Using a complementary classification, membrane markers LYVE1 and MHCII identified four macrophage subgroups: LYVE1−/MHCII hi (M1-like, classically activated), LYVE1+/MHCII lo (M2-like, alternatively activated), and two new subgroups, LYVE1+/MHCII hi and LYVE1−/MHCII lo . Notably, one new subgroup, LYVE1+/MHCII hi , had traits of both M2 and M1 macrophages, while the other new subgroup, LYVE1−/MHCII lo , displayed strong phagocytic capacity. Flow cytometric analysis validated the presence of the four macrophage subgroups in SKM and found that LYVE1− macrophages were more abundant than LYVE1+ macrophages in old SKM. A striking increase in proinflammatory markers ( S100a8 and S100a9 mRNAs) and senescence-related markers ( Gpnmb and Spp1 mRNAs) was evident in macrophage clusters from older mice. In sum, we have identified dynamically polarized SKM macrophages and propose that specific macrophage subpopulations contribute to the proinflammatory and senescent traits of old SKM. Tissue-resident macrophages represent a group of highly responsive innate immune cells that acquire diverse functions by polarizing toward distinct subpopulations. The subpopulations of macrophages that reside in skeletal muscle (SKM) and their changes during aging are poorly characterized. By single-cell transcriptomic analysis with unsupervised clustering, we found 11 distinct macrophage clusters in male mouse SKM with enriched gene expression programs linked to reparative, proinflammatory, phagocytic, proliferative, and senescence-associated functions. Using a complementary classification, membrane markers LYVE1 and MHCII identified four macrophage subgroups: LYVE1−/MHCIIhi (M1-like, classically activated), LYVE1+/MHCIIlo (M2-like, alternatively activated), and two new subgroups, LYVE1+/MHCIIhi and LYVE1−/MHCIIlo. Notably, one new subgroup, LYVE1+/MHCIIhi, had traits of both M2 and M1 macrophages, while the other new subgroup, LYVE1−/MHCIIlo, displayed strong phagocytic capacity. Flow cytometric analysis validated the presence of the four macrophage subgroups in SKM and found that LYVE1− macrophages were more abundant than LYVE1+ macrophages in old SKM. A striking increase in proinflammatory markers (S100a8 and S100a9 mRNAs) and senescence-related markers (Gpnmb and Spp1 mRNAs) was evident in macrophage clusters from older mice. In sum, we have identified dynamically polarized SKM macrophages and propose that specific macrophage subpopulations contribute to the proinflammatory and senescent traits of old SKM. Tissue-resident macrophages represent a group of highly responsive innate immune cells that acquire diverse functions by polarizing toward distinct subpopulations. The subpopulations of macrophages that reside in skeletal muscle (SKM) and their changes during aging are poorly characterized. By single-cell transcriptomic analysis with unsupervised clustering, we found 11 distinct macrophage clusters in male mouse SKM with enriched gene expression programs linked to reparative, proinflammatory, phagocytic, proliferative, and senescence-associated functions. Using a complementary classification, membrane markers LYVE1 and MHCII identified four macrophage subgroups: LYVE1-/MHCII (M1-like, classically activated), LYVE1+/MHCII (M2-like, alternatively activated), and two new subgroups, LYVE1+/MHCII and LYVE1-/MHCII . Notably, one new subgroup, LYVE1+/MHCII , had traits of both M2 and M1 macrophages, while the other new subgroup, LYVE1-/MHCII , displayed strong phagocytic capacity. Flow cytometric analysis validated the presence of the four macrophage subgroups in SKM and found that LYVE1- macrophages were more abundant than LYVE1+ macrophages in old SKM. A striking increase in proinflammatory markers ( and mRNAs) and senescence-related markers ( and mRNAs) was evident in macrophage clusters from older mice. In sum, we have identified dynamically polarized SKM macrophages and propose that specific macrophage subpopulations contribute to the proinflammatory and senescent traits of old SKM. Tissue-resident macrophages represent a group of highly responsive innate immune cells that acquire diverse functions by polarizing toward distinct subpopulations. The subpopulations of macrophages that reside in skeletal muscle (SKM) and their changes during aging are poorly characterized. By single-cell transcriptomic analysis with unsupervised clustering, we found 11 distinct macrophage clusters in male mouse SKM with enriched gene expression programs linked to reparative, proinflammatory, phagocytic, proliferative, and senescence-associated functions. Using a complementary classification, membrane markers LYVE1 and MHCII identified four macrophage subgroups: LYVE1-/MHCIIhi (M1-like, classically activated), LYVE1+/MHCIIlo (M2-like, alternatively activated), and two new subgroups, LYVE1+/MHCIIhi and LYVE1-/MHCIIlo. Notably, one new subgroup, LYVE1+/MHCIIhi, had traits of both M2 and M1 macrophages, while the other new subgroup, LYVE1-/MHCIIlo, displayed strong phagocytic capacity. Flow cytometric analysis validated the presence of the four macrophage subgroups in SKM and found that LYVE1- macrophages were more abundant than LYVE1+ macrophages in old SKM. A striking increase in proinflammatory markers (S100a8 and S100a9 mRNAs) and senescence-related markers (Gpnmb and Spp1 mRNAs) was evident in macrophage clusters from older mice. In sum, we have identified dynamically polarized SKM macrophages and propose that specific macrophage subpopulations contribute to the proinflammatory and senescent traits of old SKM.Tissue-resident macrophages represent a group of highly responsive innate immune cells that acquire diverse functions by polarizing toward distinct subpopulations. The subpopulations of macrophages that reside in skeletal muscle (SKM) and their changes during aging are poorly characterized. By single-cell transcriptomic analysis with unsupervised clustering, we found 11 distinct macrophage clusters in male mouse SKM with enriched gene expression programs linked to reparative, proinflammatory, phagocytic, proliferative, and senescence-associated functions. Using a complementary classification, membrane markers LYVE1 and MHCII identified four macrophage subgroups: LYVE1-/MHCIIhi (M1-like, classically activated), LYVE1+/MHCIIlo (M2-like, alternatively activated), and two new subgroups, LYVE1+/MHCIIhi and LYVE1-/MHCIIlo. Notably, one new subgroup, LYVE1+/MHCIIhi, had traits of both M2 and M1 macrophages, while the other new subgroup, LYVE1-/MHCIIlo, displayed strong phagocytic capacity. Flow cytometric analysis validated the presence of the four macrophage subgroups in SKM and found that LYVE1- macrophages were more abundant than LYVE1+ macrophages in old SKM. A striking increase in proinflammatory markers (S100a8 and S100a9 mRNAs) and senescence-related markers (Gpnmb and Spp1 mRNAs) was evident in macrophage clusters from older mice. In sum, we have identified dynamically polarized SKM macrophages and propose that specific macrophage subpopulations contribute to the proinflammatory and senescent traits of old SKM.
Author	Fan, Jinshui Cui, Chang-Yi Mazan-Mamczarz, Krystyna Rathbun, Isabelle A Gorospe, Myriam Nguyen, Cuong De, Supriyo Sen, Payel Chakraborty, Papiya Shi, Changyou Piao, Yulan Krasniewski, Linda K Wallace, Tonya Tsitsipatis, Dimitrios Dunn, Christopher Ferrucci, Luigi Munk, Rachel
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Keywords	mouse Lyve1 cell biology MHCII flow cytometry aging muscle-resident macrophages single-cell analysis
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SubjectTerms	Aging Animals Approximation Biomarkers - metabolism Cell adhesion & migration Cell Biology Cell growth Cytokines Flow cytometry Gene expression Genomics Inflammation Lyve1 Macrophages Macrophages - metabolism Male MHCII Mice Muscle, Skeletal - metabolism muscle-resident macrophages Musculoskeletal system Neutrophils Ontology Phagocytes Phagocytes - metabolism Proteins Senescence Single-Cell Analysis Skeletal muscle Transcriptome Transcriptomics
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Title	Single-cell analysis of skeletal muscle macrophages reveals age-associated functional subpopulations
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