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IL-10 Triggers Changes in Macrophage Phenotype That Promote Muscle Growth and Regeneration
Open accessAbstract
We examined the function of IL-10 in regulating changes in macrophage phenotype during muscle growth and regeneration following injury. Our findings showed that the Th1 cytokine response in inflamed muscle is characterized by high levels of expression of CD68, CCL-2, TNF-α, and IL-6 at 1 d postinjury. During transition to the Th2 cytokine response, expression of those transcripts declined, whereas CD163, IL-10, IL-10R1, and arginase-1 increased. Ablation of IL-10 amplified the Th1 response at 1 d postinjury, causing increases in IL-6 and CCL2, while preventing a subsequent increase in CD163 and arginase-1. Reductions in muscle fiber damage that normally occurred between 1 and 4 d postinjury did not occur in IL-10 mutants. In addition, muscle regeneration and growth were greatly slowed by loss of IL-10. Furthermore, myogenin expression increased in IL-10 mutant muscle at 1 d postinjury, suggesting that the mutation amplified the transition from the proliferative to the early differentiation stages of myogenesis. In vitro assays showed that stimulation of muscle cells with IL-10 had no effect on cell proliferation or expression of MyoD or myogenin. However, coculturing muscle cells with macrophages activated with IL-10 to the M2 phenotype increased myoblast proliferation without affecting MyoD or myogenin expression, showing that M2 macrophages promote the early, proliferative stage of myogenesis. Collectively, these data show that IL-10 plays a central role in regulating the switch of muscle macrophages from a M1 to M2 phenotype in injured muscle in vivo, and this transition is necessary for normal growth and regeneration of muscle.
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“In mouse skeletal muscle injury by chemical toxin or unloading/reloading, IL-4 mRNA, although detectable, does not rise above uninjured levels over the course of healing [73,74].”
From Macrophage phenotypes during tissue repair (2013) · cites this paper as [73]
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InfluentialMechanisms of cooperative cell-cell interactions in skeletal muscle regeneration
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“Previously, it was demonstrated that M2 promote the early, proliferative stage of myogenesis following sterile injury (37).”
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“It has been shown that the secretome associated with alternatively activated M2 macrophages is myogenic for skeletal muscle myoblasts.(42,43) Previously, we have shown that media conditioned by ECMtreated macrophages promoted myotube formation and sarcomeric myosin expression of C2C12 myoblasts.”
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BackgroundImmunological regulation of skeletal muscle adaptation to exercise
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“43,59,60 Therefore, stromal and myeloid cells may sense the temporary loss of structure in load-bearing hindlimb muscles, and other local deviations in regulated variables, and communicate such deviations to Tregs via enhanced IL-6 production.”
Regenerative Medicine Approaches for Age-Related Muscle Loss and Sarcopenia: A Mini-Review
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“Therefore, drugs that can deactivate the M1 phenotype and promote activation of the M2 phenotype can increase muscle repair and ameliorate the progression of muscular dystrophies (Kovalovskya et al., 2000; Mikita et al., 2011; Villalta et al., 2011b; Deng et al., 2012).”
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“IL-10 derived from M2-like 467 macrophages is well known to suppress the expression of inflammatory cytokines 468 released by M1-like macrophages (11) and was reported to play a role in the intestinal 469 recovery from POI in mice (48).”
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“Indeed, IL- 10 participates to the shift in macrophage phenotype (Deng et al., 2012) while pro- inflammatory macrophages robustly express TNFα.”
BackgroundMacrophage Involvement in Aging-Associated Skeletal Muscle Regeneration
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“At late repair stages, M1 macrophages tra sition to M2 crophag s thanks to antiinflammatory cytokines secreted by regulatory T lymphocytes (Treg cells) and by phagocytosed cell debris [18,117,118].”
BackgroundRegulatory T cells in autoimmune kidney diseases and transplantation
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Leukocyte HMGB1 Is Required for Vessel Remodeling in Regenerating Muscles
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“also reported lower numbers of CD209-positive HBCs in PE placental tissues, but they did not distinguish between onsets of PE (96) Cytokines are important coordinators that likely promote phenotypic and functional changes of immune cells in inflammation (90, 97).”
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“Additionally, IL-10 ablation could cause a delay in pro-to anti-macrophage transition and reduce muscle fiber repair (Villalta et al., 2011; Deng et al., 2012).”
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“We also found a slight increase of IL-10 mRNA level in MAYV infected RAG/ mice, which is a cytokine involved in macrophage-induced muscle regeneration (Deng et al., 2012).”
BackgroundDehydrated Human Amnion Chorion Membrane as Treatment for Pediatric Burns
Ahuja, N., Jin, R. M., Powers, C., Billi, A., & Bass, K. D. (2019) · Advances in Wound Care · doi:10.1089/wound.2019.0983 · Cited by 45
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“Macrophage phenotype switching requires IL-10 and therefore the loss of IL-10 prolongs inflammation and impairs muscle regeneration [104,105].”
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“In this study, the mRNA level of anti-inflammatory M2 molecules, including IL-10, CD163, CD206, and Arg-1, was significantly upregulated by FGF21 treatment and, most notably, IL-10 itself has been identified to promote M1/M2 transition (Deng et al., 2012), suggesting a shift from M1 proinflammatory phenotype to M2 ant…”
BackgroundThe Role of Mitochondria in Mediation of Skeletal Muscle Repair
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“In the following hours to days, blood monocytes are recruited and differentiated into tissue macrophages, replacing neutrophils [43,44].”
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“Some studies have shown an increase in M2 CD163+ in synovial biopsies and inflamed colon of the patients with AS, and CD163 synovial over-expression has been shown to be correlated with disease (28, 29); in this context, IL-10 can alter the phenotype of macrophages from M1 to M2 (30).”
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“In the muscle, a major mode by which Tregs may affect macrophage polarization during regeneration is through the production of IL-10 (10, 16).”
BackgroundInfluentialPatsalos, A., Tzerpos, P., Halász, L., Nagy, G., Pap, A., Giannakis, N., Lyroni, K., Koliaraki, V., Pintye, É., Dezsö, B., et al. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1900553 · Cited by 40
“Evaluation of gene expression data from Bach1 KO muscleinfiltrating MFs revealed dysregulation of numerous genes (Il6, Il10, Dusp1, Slc40a1, Cebpb, Gdf3, Igf1, Pparg, and Spp1), known to be involved in muscle regeneration and MF phenotypeswitching pathways (13, 15, 18, 19, 21, 41, 53) (Fig.”
BackgroundMethodBoulanger‐Piette, A., Hamoudi, D., Marcadet, L., Morin, F., Argaw, A., Ward, L. M., & Frenette, J. (2018) · Current Osteoporosis Reports · doi:10.1007/s11914-018-0468-2 · Cited by 37
Macrophages in Skeletal Muscle Dystrophies, An Entangled Partner
Théret, M., Saclier, M., Messina, G., & Rossi, F. M. V. (2021) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-210737 · Cited by 41
“Interleukin 10 (IL-10) is required for macrophages to acquire a pro-regenerative function [80, 81].”
Macrophages at the Crossroad of Meta-Inflammation and Inflammaging
Qu, L., Matz, A., Karlinsey, K. S., Cao, Z., Vella, A. T., & Zhou, B. (2022) · Genes · doi:10.3390/genes13112074 · Cited by 42
“IL10 was reported to promote the phenotypic transition of macrophages to increase muscle fiber repair [81], and IL6 favors muscle regeneration in mice [82].”
BackgroundHuynh, T., Reed, C. L., Blackwell, Z., Phelps, P., Pinzon‐Herrera, L., Almodóvar, J., Zaharoff, D. A., & Wolchok, J. C. (2023) · Scientific Reports · doi:10.1038/s41598-023-27981-x · Cited by 39
The extraocular muscle stem cell niche is resistant to ageing and disease
Formicola, L., Marazzi, G., & Sassoon, D. A. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00328 · Cited by 42
“, 2003) showed that wild-type EOMs and mdx limb muscles highly express specific genes involved in muscle regeneration and fibrosis, such as interleukin-10 receptor beta (IL10Rβ), connective tissue growth factor (Ctgf), follistatin-like 1 (Fstl-1) and TGFβ-induced protein (TGFβi; Porter et al., 2003; Serrano et al., 20…”
BackgroundInflammatory response during slow‐ and fast‐twitch muscle regeneration
Zimowska, M., Kasprzycka, P., Bocian, K., Delaney, K., Jung, P., Kuchcinska, K., Kaczmarska, K., Gladysz, D., Stremińska, W., & Ciemerych, M. (2017) · Muscle and Nerve · doi:10.1002/mus.25246 · Cited by 32
“It is also known to support muscle repair by impacting myoblast proliferation.(17,81,82) Thus, accurate and time-controlled changes in the level of IL-10 may be necessary for proper skeletal muscle regeneration.”
BackgroundChronic infection stunts macrophage heterogeneity and disrupts immune-mediated myogenesis
Jin, R. M., Warunek, J., & Wohlfert, E. A. (2018) · JCI Insight · doi:10.1172/jci.insight.121549 · Cited by 37
Delineating the relationship between immune system aging and myogenesis in muscle repair
Tobin, S. W., Alibhai, F. J., Wlodarek, L., Yeganeh, A., Millar, S., Wu, J., Li, S., Weisel, R. D., & Li, R. (2021) · Aging Cell · doi:10.1111/acel.13312 · Cited by 40
TAM kinase signaling is indispensable for proper skeletal muscle regeneration in mice
Al-Zaeed, N., Budai, Z., Szondy, Z., & Sarang, Z. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03892-5 · Cited by 36
“In addition to inflammatory macrophages and SCs, efficient muscle repair also requires the migration and proliferation of fibroblasts in order to produce new temporary extracellular matrix components.”
BackgroundInfluentialLi, W., Xu, Z., Zou, B., Yang, D., Lu, Y., Zhang, X., Zhang, C., Li, Y., & Zhu, C. (2024) · Fundamental Research · doi:10.1016/j.fmre.2023.12.015 · Cited by 37
“Moreover, IL-10 switches muscle macrophages from an M1 pro-inflammatory phenotype to an M2 muscle regeneration-promoting phenotype, a shift necessary for proper muscle growth and regeneration [47] .”
Cappellari, O., Mantuano, P., & Luca, A. D. (2020) · Cells · doi:10.3390/cells9071659 · Cited by 36
Lu, Z., Wang, Z., Zhang, X., & Ning, K. (2024) · Biomolecules · doi:10.3390/biom14101205 · Cited by 47
“The recovery of the damaged muscle plays an important regulatory role [152].”
BackgroundPlasticity of the Muscle Stem Cell Microenvironment
Dinulović, I., Furrer, R., & Handschin, C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-69194-7_8 · Cited by 37
Immunomodulation of Biomaterials by Controlling Macrophage Polarization
Yang, H., Park, H. C., Quan, H., & Kim, Y. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-0445-3_12 · Cited by 37
Reidy, P. T., Yonemura, N. M., Madsen, J. H., McKenzie, A. I., Mahmassani, Z. S., Rondina, M. T., Lin, Y. K., Kaput, K. L., & Drummond, M. J. (2019) · Acta Physiologica · doi:10.1111/apha.13251 · Cited by 35
Brant, J. O., Boatwright, J. L., Davenport, R., Sandoval, A. G. W., Maden, M., & Barbazuk, W. B. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216228 · Cited by 36
Bone Marrow Plasma Cells Modulate Local Myeloid-Lineage Differentiation via IL-10
Meng, L., de Almeida, L. N., Clauder, A., Lindemann, T., Luther, J., Link, C., Hofmann, K., Kulkarni, U., Wong, D. M., David, J., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01183 · Cited by 38
“Moreover, IL-10 seems also to play a critical role in regulating the switch of muscle macrophages from an M1 to an M2 phenotype in injured muscles in vivo (49).”
BackgroundSorensen, J. R., Kaluhiokalani, J. P., Hafen, P. S., Deyhle, M. R., Parcell, A. C., & Hyldahl, R. D. (2019) · The FASEB Journal · doi:10.1096/fj.201900519r · Cited by 37
“Indeed, the results from our cell culture experiments as well as other studies support the idea that anti-inflammatory macrophages promote proliferation and differentiation of satellite cell populations (11, 36), likelydue to the important source of cytokines and other secreted factors that immune cells produce (6, 37…”
ResultLoss of HDAC11 accelerates skeletal muscle regeneration in mice
Núñez‐Álvarez, Y., Hurtado, E., Muñoz, M., García‐Tuñón, I., Rech, G. E., Pluvinet, R., Sumoy, L., Pendás, A. M., Peinado, M. A., & Suelves, M. (2020) · FEBS Journal · doi:10.1111/febs.15468 · Cited by 34
Targeting Tumor-Associated Macrophages in the Pediatric Sarcoma Tumor Microenvironment
Koo, J., Hayashi, M., Verneris, M. R., & Lee‐Sherick, A. B. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.581107 · Cited by 34
Kawashima, M., Kawanishi, N., Tominaga, T., Suzuki, K., Miyazaki, A., Nagata, I., Miyoshi, M., Miyakawa, M., Sakuraya, T., Sonomura, T., et al. (2021) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01069.2020 · Cited by 36
Time-dependent gene expression analysis after mouse skeletal muscle contusion
Xiao, W., Liu, Y., Luo, B., Zhao, L.-L., Liu, X., Zeng, Z., & Chen, P. (2016) · Journal of Sport and Health Science · doi:10.1016/j.jshs.2016.01.017 · Cited by 35
“Moreover, we studied the antiinflammatory cytokine (IL-10) which plays a central role in regulating the switch of muscle macrophages from M1 to M2 phenotype in injured muscle.(32) The study showed that ablation of IL-10 prevented a subsequent increase in CD163 postinjury.”
BackgroundMethodThe Functions and Mechanisms of Low-Level Laser Therapy in Tendon Repair (Review)
Lyu, K., Liu, X., Jiang, L., Chen, Y., Lu, J., Zhu, B., Liu, X., Li, Y., Wang, D., & Li, S. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.808374 · Cited by 34
“In terms of anti-inflammation, LLLT mainly reduces the expression of the NF-KB gene and COX-2 activity to release a large number of anti-inflammatory factors, so as to achieve the goal of tendon repair (Pires et al., 2011; Deng et al., 2012; Rodrigues et al., 2014; Fortuna et al., 2018).”
BackgroundWilde, J. M., Gumucio, J. P., Grekin, J. A., Sarver, D. C., Noah, A. C., Ruehlmann, D. G., Davis, M. E., Bedi, A., & Mendias, C. L. (2016) · Journal of Shoulder and Elbow Surgery · doi:10.1016/j.jse.2016.01.035 · Cited by 34
“IL-1β and IL-6 are potent proinflammatory cytokines known to direct atrophy and collagen production,(1,12) and IL10 is an anti-inflammatory gene that can protect against atrophy and fibrosis in skeletal muscle tissue.(9) In the current study, inhibition of p38 MAPK was effective at reducing the expression of IL-1β and…”
BackgroundBiomimetic Scaffolds for Skeletal Muscle Regeneration
Mulbauer, G. D., & Matthew, H. W. T. (2019) · Discoveries · doi:10.15190/d.2019.3 · Cited by 34
Magnolol Attenuates Cisplatin-Induced Muscle Wasting by M2c Macrophage Activation
Lee, C., Jeong, H., Lee, H., Hong, M., Park, S.-Y., & Bae, H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00077 · Cited by 37
Wang, Y., Wang, K., Bao, Y., Zhang, T., Ainiwaer, D., Xiong, X., Wang, G., & Sun, Z. (2022) · Tissue and Cell · doi:10.1016/j.tice.2022.101812 · Cited by 35
CDDO-Me Redirects Activation of Breast Tumor Associated Macrophages
Ball, M. S., Shipman, E. P., Kim, H. J., Liby, K. T., & Pioli, P. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149600 · Cited by 34
“Previous work has demonstrated that CD163 is upregulated by IL-10 [48] and that IL-10 induces M2 activation of macrophages [49].”
BackgroundHonkisz-Orzechowska, E., Łażewska, D., Baran, G., & Kieć‐Kononowicz, K. (2024) · Molecules · doi:10.3390/molecules29061258 · Cited by 35
“Because placental inflammation contributes to abnormal embryonic heart development [80], preterm delivery or pregnancy loss [81], the outcomes above could indicate a crucial role for RvD2 on placental function and, therefore, offspring health.”
BackgroundMarzetti, E., Lozanoska‐Ochser, B., Calvani, R., Landi, F., Coelho‐Júnior, H. J., & Picca, A. (2024) · Biomolecules · doi:10.3390/biom14040415 · Cited by 36
Rybalko, V. Y., Hsieh, P.-L., Ricles, L., Chung, E., Farrar, R., & Suggs, L. (2017) · Regenerative medicine · doi:10.2217/rme-2016-0094 · Cited by 32
Barroso, M. V., Cattani‐Cavalieri, I., de Brito‐Gitirana, L., Fautrel, A., Lagente, V., Schmidt, M., Pôrto, L. C., Romana‐Souza, B., Valença, S. S., & Lanzetti, M. (2017) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2017.08.026 · Cited by 35
Metadata
- Authors
- Deng, B., Wehling-Henricks, M., Villalta, S. A., Wang, Y., & Tidball, J. G.
- Affiliations
- University of California, Los Angeles (US)
- Department of Integrative Biology and Physiology, University of California , Los Angeles, Los Angeles, CA 90095
- Corresponding author
- Deng, Bo
- Wang, Ying
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-10-01
- Volume
- 189
- Issue
- 7
- Pages
- 3669-3680
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC3448810
- OpenAlex
- W2153554828
- Cited by
- 472
- References
- 68
- Citations by year
- 2026: 24 · 2025: 25 · 2024: 26 · 2023: 33 · 2022: 43 · 2021: 40 · 2020: 41 · 2019: 44 · 2018: 32 · 2017: 43 · 2016: 43 · 2015: 28 · 2014: 27 · 2013: 22 · 2012: 1
- FWCI
- 9.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Muscular Dystrophy Association (157881)
- National Institutes of Health (R01 AR/AG054451)
- National Institute on Aging (R01 AR/AG054451)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR047855, R01AR054451, R01AR047721)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Keywords
- IL-10, muscle regeneration, muscle growth, macrophage polarization, M2 macrophages, M1 macrophages, Th1/Th2 shift, muscle damage, myogenesis, myoblast proliferation, arginase-1, CD163, myogenin, MyoD, MCP-1, TNF-α, interleukin-6
- MeSH terms
- Animals, Female, Macrophages, Mice, Inbred C57BL, Regeneration, Up-Regulation, Immunophenotyping, Cytokines, Interleukin-10, Mice, Knockout, Th1 Cells, Th2 Cells, Muscle, Skeletal, Cell Enlargement, Cell Proliferation, Mice, Mice, 129 Strain
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