IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration

Deng, Bo; Wehling-Henricks, Michelle; Villalta, S Armando; Wang, Ying; Tidball, James G

doi:10.4049/jimmunol.1103180

Cited by 472Muscle Physiology and DisordersCardiac Fibrosis and RemodelingWound Healing and Treatments

IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration

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Deng, Bo, Wehling-Henricks, Michelle, Villalta, S Armando, Wang, Ying, Tidball, James G·2012·The Journal of Immunology

DOI 10.4049/jimmunol.1103180PMC PMC3448810

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Abstract

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.
“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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Tumor Necrosis Factor-α and Basic Fibroblast Growth Factor Differentially Inhibit the Insulin-like Growth Factor-I Induced Expression of Myogenin in C2C12 Myoblasts
Layne, M. D., & Farmer, S. R. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4465 · Cited by 71 · see citing works
Cardiomyopathic features associated with muscular dystrophy are independent of dystrophin absence in cardiovasculature
Hainsey, T. A., Senapati, S., Kuhn, D. E., & Rafael, J. A. (2003) · Neuromuscular Disorders · doi:10.1016/s0960-8966(02)00286-9 · Cited by 69 · cited 1× · see citing works
“Muscle fibers experiencing membrane lesions were identified by IgG staining, as previously described (35).”
Method
Apoptosis of macrophages during the resolution of muscle inflammation
Tidball, J., & Pierre, B. S. S. (1996) · Journal of Leukocyte Biology · doi:10.1002/jlb.59.3.380 · Cited by 66 · cited 1× · see citing works
“The peak of apoptosis and phagocytosis of inflammatory cells occurs 2 d after the onset of muscle reloading (53), which coincides with an increase in M2 macrophage populations.”
Background
Expression and Neural Control of Myogenic Regulatory Factor Genes During Regeneration of Mouse Soleus
Launay, T., Armand, A., Charbonnier, F., Mira, J., Donsez, E., Gallien, C. L., & Chanoine, C. (2001) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540104900709 · Cited by 55 · cited 1× · see citing works
“Injection of cardiotoxin into soleus muscle increases MyoD expression at 2 d postinjury (39), and myogenin expression is elevated in muscle fibers at ∼1 d following the increase in MyoD (21).”
Background
Time course of the regenerative response in bupivacaine injured orbicularis oculi muscle
McLoon, L. K., NGUYEN, L. T. H., & Wirtschafter, J. D. (1998) · Cell and Tissue Research · doi:10.1007/s004410051195 · Cited by 45 · cited 1× · see citing works
“injury models show a similar time course in the increase in MyoD at ∼2 d postinjury, followed by the elevated expression of other, developmentally regulated transcripts (40).”
Background
C-Jun N-Terminal Kinase Mediates Tumor Necrosis Factor-α Suppression of Differentiation in Myoblasts
Strle, K., Broussard, S. R., McCusker, R. H., Shen, W. H., LeCleir, J. M., Johnson, R. W., Freund, G. G., Dantzer, R., & Kelley, K. W. (2006) · Endocrinology · doi:10.1210/en.2005-1541 · Cited by 44 · cited 1× · see citing works
“Application of TNF-a to muscle cells in vitro can greatly diminish myogenin expression (46–48) that can result from activation of c-Jun N-terminal kinase (49).”
Background
Effects of calcitonin gene-related peptide and interleukin 6 on myoblast differentiation
Okazaki, S., Kawai, H., Arii, Y., Yamaguchi, H., & Saito, S. (1996) · Cell Proliferation · doi:10.1046/j.1365-2184.1996.00996.x · Cited by 28 · cited 1× · see citing works
“Nevertheless, IL-6 treatment of myoblasts in vitro was reported to increase myogenin expression (44), and a recent investigation showed a strong, positive effect of IL-6 on myogenin expression in vivo (45).”
Background
Effects of calcitonin gene-related peptide and interleukin 6 on myoblast differentiation
Okazaki, S., Kawai, H., Arii, Y., et al. (1996) · Cell Proliferation · doi:10.1111/j.1365-2184.1996.tb00104.x · Cited by 21 · see citing works

Flagged first, then by citations

1 of the 68 references couldn’t be matched to a known paper.

Research works printed but not linked: 4

[36]Mantovani A Sica A Sozzani S Allavena P Vecchi A Locati M 2004 The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol 25 677 686 15530839
[40]McLennan IS 1993 Resident macrophages (ED2- and ED3-positive) do not phagocytose degenerating rat skeletal muscle fibres Cell Tissue Res 272 193 196 8481952
[42]Yablonka-Reuveni Z Rivera AJ 1994 Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers Develop Biol 164 588 603 7913900 PMC4128087
[64]Lee TS Chau LY 2002 Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice Nature Med 8 240 246 11875494

Sorted by citations

Macrophages in Tissue Repair, Regeneration, and Fibrosis
Wynn, T. A., & Vannella, K. M. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.015 · Cited by 4,481 · see citing works
Microglial <scp>M1/M2</scp> polarization and metabolic states
Orihuela, R., McPherson, C. A., & Harry, G. J. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13139 · Cited by 2,070 · see citing works
“While the initial response of macrophages to injury has been known for some time, positive influences on tissue remodelling have been recognized more recently (Longbrake et al., 2007; Ruffell et al., 2009; Deng et al., 2012; Novak and Koh, 2013; Shechter and Schwartz, 2013; Shechter et al., 2013).”
Background
Muscle damage and inflammation during recovery from exercise
Peake, J. M., Neubauer, O., Gatta, P. A. D., & Nosaka, K. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00971.2016 · Cited by 829 · see citing works
“apoptosis and stimulate their proliferation, promote muscle regeneration and growth, as 373 well as the production of connective tissue (13, 23, 104).”
BackgroundInfluential
Satellite Cells and Skeletal Muscle Regeneration
Dumont, N. A., Bentzinger, C. F., Sincennes, M., & Rudnicki, M. A. (2015) · Comprehensive Physiology · doi:10.1002/cphy.c140068 · Cited by 719 · see citing works
Regulation of Muscle Growth and Regeneration by the Immune System
Tidball, J. G. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.150 · Cited by 740 · see citing works
Macrophages in inflammation, repair and regeneration
Oishi, Y., & Manabe, I. (2018) · International Immunology · doi:10.1093/intimm/dxy054 · Cited by 645 · see citing works
Macrophage heterogeneity in tissues: phenotypic diversity and functions
Gordon, S., Plüddemann, A., & Martínez, F. O. (2014) · Immunological Reviews · doi:10.1111/imr.12223 · Cited by 713 · see citing works
“removal of debris and fibrosis, for example in the mdx dystrophy model; IL-10 enhances macrophage promotion of satellite cell proliferation (131, 132).”
Background
Mechanisms of Organ Injury and Repair by Macrophages
Vannella, K. M., & Wynn, T. A. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034356 · Cited by 656 · see citing works
Macrophage phenotypes during tissue repair
Novak, M. L., & Koh, T. J. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.1012512 · Cited by 658 · see citing works
“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].”
Background
Frailty and sarcopenia: The potential role of an aged immune system
Wilson, D., Jackson, T., Sapey, E., & Lord, J. M. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.01.006 · Cited by 573 · see citing works
Endothelial Lactate Controls Muscle Regeneration from Ischemia by Inducing M2-like Macrophage Polarization
Zhang, J., Muri, J., Fitzgerald, G., Gorski, T., Giannì-Barrera, R., Masschelein, E., D’Hulst, G., Gilardoni, P. A., Turiel, G., Fan, Z., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.05.004 · Cited by 538 · see citing works
“This M1 to M2 repolarization is required for optimal muscle regeneration (Arnold et al., 2007; Deng et al., 2012; Tidball and Wehling-Henricks, 2007).”
B cell-derived GABA elicits IL-10+ macrophages to limit anti-tumour immunity
Zhang, B., Vogelzang, A., Miyajima, M., Sugiura, Y., Wu, Y., Chamoto, K., Nakano, R., Hatae, R., Menzies, R. J., Sonomura, K., et al. (2021) · Nature · doi:10.1038/s41586-021-04082-1 · Cited by 455 · see citing works
Cellular dynamics in the muscle satellite cell niche
Bentzinger, C. F., Wang, Y. X., Dumont, N. A., & Rudnicki, M. A. (2013) · The EMBO Reports · doi:10.1038/embor.2013.182 · Cited by 398 · see citing works
“By contrast, inhibition of the transition from M1 to M2 macrophages in mice negative for IL-10 or the transcription factor C/EBP β resulted in reduced myogenin expression and fibre growth [47,48].”
Self-citation
Monocytes and macrophages in tissue repair: Implications for immunoregenerative biomaterial design
Ogle, M. E., Segar, C. E., Sridhar, S., & Botchwey, E. A. (2016) · Experimental Biology and Medicine · doi:10.1177/1535370216650293 · Cited by 378 · see citing works
“Blockade of M2 polarization by transgenic knockout of IL-10 causes an increased/sustained M1 response and poor regeneration in an injured muscle.(71) This phenotype switching in the muscle may be a key step in normal healing and may suggest that both polarization states are important for muscle repair.”
BackgroundResult
A Muscle Stem Cell Support Group: Coordinated Cellular Responses in Muscle Regeneration
Wosczyna, M. N., & Rando, T. A. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.06.018 · Cited by 353 · see citing works
Macrophage Plasticity and the Role of Inflammation in Skeletal Muscle Repair
Kharraz, Y., Guerra, J., Mann, C. J., Serrano, A. L., & Muñoz‐Cánoves, P. (2013) · Mediators of Inflammation · doi:10.1155/2013/491497 · Cited by 302 · see citing works
“ese cytokines have essential roles in promoting proper wound healing, by supporting myogenesis [50], enhancing angiogenesis, and stimulating the transient deposition of the ECM [51].”
Background
Exercise-dependent regulation of the tumour microenvironment
Koelwyn, G. J., Quail, D. F., Zhang, X., White, R. M., & Jones, L. W. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2017.78 · Cited by 299 · see citing works
Interleukin 6 as an Energy Allocator in Muscle Tissue
Kistner, T. M., Pedersen, B. K., & Lieberman, D. E. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00538-4 · Cited by 295 · see citing works
Temporal Dynamics and Heterogeneity of Cell Populations during Skeletal Muscle Regeneration
Oprescu, S. N., Yue, F., Qiu, J., Brito, L. F., & Kuang, S. (2020) · iScience · doi:10.1016/j.isci.2020.100993 · Cited by 288 · see citing works
Cross-talk between skeletal muscle and immune cells: muscle-derived mediators and metabolic implications
Pillon, N. J., Bilan, P. J., Fink, L. N., & Klip, A. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00553.2012 · Cited by 285 · see citing works
“Furthermore, myoblast proliferation is enhanced in coculture with macrophages preactivated with IL-10 to an M2 polarization (32).”
Background
Inflammation induced loss of skeletal muscle
Londhe, P., & Guttridge, D. C. (2015) · Bone · doi:10.1016/j.bone.2015.03.015 · Cited by 276 · see citing works
Angiogenic capacity of M1- and M2-polarized macrophages is determined by the levels of TIMP-1 complexed with their secreted proMMP-9
Zając, E., Schweighofer, B., Kupriyanova, T. A., Juncker‐Jensen, A., Minder, P., Quigley, J. P., & Deryugina, E. I. (2013) · Blood · doi:10.1182/blood-2013-05-501494 · Cited by 261 · see citing works
“Following 7-day incubation, M0macrophages were incubated for 24 hr either in the mixture of IFNγ and LPS to induce M1phenotype or with IL-4 to induce M2-phenotype.”
BackgroundInfluential
The promotion of a constructive macrophage phenotype by solubilized extracellular matrix
Sicari, B. M., Dziki, J. L., Siu, B. F., Medberry, C. J., Dearth, C. L., & Badylak, S. F. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.06.060 · Cited by 255 · see citing works
Regenerative Wound Healing: The Role of Interleukin-10
King, A., Balaji, S., Le, L. D., Crombleholme, T. M., & Keswani, S. G. (2013) · Advances in Wound Care · doi:10.1089/wound.2013.0461 · Cited by 250 · see citing works
“46 Studies in murine cardiac tissue have demonstrated that IL-10 plays an important role after injury in an induced cardiac hypertrophy model.”
Monocyte/macrophage interactions with myogenic precursor cells during skeletal muscle regeneration
Saclier, M., Cuvellier, S., Magnan, M., Mounier, R., & Chazaud, B. (2013) · FEBS Journal · doi:10.1111/febs.12166 · Cited by 248 · see citing works
The effects of obesity on skeletal muscle regeneration
Akhmedov, D., & Berdeaux, R. (2013) · Frontiers in Physiology · doi:10.3389/fphys.2013.00371 · Cited by 241 · see citing works
“During later stages of regeneration, TGF-β and IL-10 secreted by anti-inflammatory M2 macrophages promote myogenic differentiation (Arnold et al., 2007; Deng et al., 2012).”
Background
Biomimetic scaffolds for regeneration of volumetric muscle loss in skeletal muscle injuries
Grasman, J. M., Zayas, M. J., Page, R. L., & Pins, G. D. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.07.038 · Cited by 245 · see citing works
Fibro–Adipogenic Progenitors Cross-Talk in Skeletal Muscle: The Social Network
Biferali, B., Proietti, D., Mozzetta, C., & Madaro, L. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01074 · Cited by 244 · see citing works
Targeting the Shift from M1 to M2 Macrophages in Experimental Autoimmune Encephalomyelitis Mice Treated with Fasudil
Liu, C., Lǐ, Y., Yu, J., Ling, F., Hou, S., Liu, Y., Guo, M., Xie, Y., Meng, J., Zhang, H., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054841 · Cited by 233 · see citing works
“Classically activated macrophages, which are induced by a combination of IFN-c and LPS/ TNF-a, have anti-microbial and cytotoxic properties, whereas alternatively activated macrophages are anti-inflammatory or reparative [20,21].”
Background
IL-10 enhances the phenotype of M2 macrophages induced by IL-4 and confers the ability to increase eosinophil migration
Makita, N., Hizukuri, Y., Yamashiro, K., Murakawa, M., & Hayashi, Y. (2014) · International Immunology · doi:10.1093/intimm/dxu090 · Cited by 217 · see citing works
Lnc-mg is a long non-coding RNA that promotes myogenesis
Zhu, M., Liu, J., Xiao, J., Li, Y., Cai, M., Shen, H., Chen, X., Ma, Y., Hu, S., Wang, Z., et al. (2017) · Nature Communications · doi:10.1038/ncomms14718 · Cited by 210 · see citing works
“The measurement of cross-section area was performed according to the published method with slight modiﬁcation 54 .”
Increases of M2a macrophages and fibrosis in aging muscle are influenced by bone marrow aging and negatively regulated by muscle‐derived nitric oxide
Wang, Y., Wehling‐Henricks, M., Samengo, G., & Tidball, J. G. (2015) · Aging Cell · doi:10.1111/acel.12350 · Cited by 205 · see citing works
“However, during skeletal muscle inflammation, IL-10 is required for their activation to the M2a phenotype, which is characterized by elevated expression of CD163 and arginase (Villalta et al., 2011; Deng et al., 2012).”
BackgroundResult
Metabolic phenotype of skeletal muscle in early critical illness
Puthucheary, Z., Astin, R., McPhail, M. J. W., Saeed, S. M. B., Pasha, Y., Bear, D. E., Constantin, D., Velloso, C. P., Manning, S., Calvert, L. D., et al. (2018) · Thorax · doi:10.1136/thoraxjnl-2017-211073 · Cited by 200 · see citing works
Macrophages Are Key Regulators of Stem Cells during Skeletal Muscle Regeneration and Diseases
Dort, J., Fabre, P., Molina, T., & Dumont, N. A. (2019) · Stem Cells International · doi:10.1155/2019/4761427 · Cited by 196 · see citing works
“To determine the role of IL-10 in vivo, the regenerative capacity of IL-10null mice was investigated after hind limb muscle unloading and reloading [117].”
Background
Fibro-adipogenic progenitors in skeletal muscle homeostasis, regeneration and diseases
Molina, T., Fabre, P., & Dumont, N. A. (2021) · Open Biology · doi:10.1098/rsob.210110 · Cited by 193 · see citing works
“This cytokine is a central effector that triggers the change in macrophage subsets toward their anti-inflammatory phenotype, which in turn secrete factors that promote the differentiation and fusion of myogenic cells [13,14,58].”
Background
Rethinking Regenerative Medicine: A Macrophage-Centered Approach
Brown, B., Sicari, B. M., & Badylak, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00510 · Cited by 185 · see citing works
“J Biomed Mater Res A (2010) 94(4):1172–86.”
Background
Meteorin-like facilitates skeletal muscle repair through a Stat3/IGF-1 mechanism
Baht, G., Bareja, A., Lee, D. E., Rao, R. R., Huang, R., Huebner, J., Bartlett, D. B., Hart, C., Gibson, J. R., Lanza, I., et al. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0184-y · Cited by 168 · see citing works
Divergent Roles of Inflammation in Skeletal Muscle Recovery From Injury
Howard, E. E., Pasiakos, S. M., Blesso, C. N., Fussell, M. A., & Rodriguez, N. R. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00087 · Cited by 176 · see citing works
Vitamin D Treatment Attenuates Neuroinflammation and Dopaminergic Neurodegeneration in an Animal Model of Parkinson’s Disease, Shifting M1 to M2 Microglia Responses
Calvello, R., Cianciulli, A., Nicolardi, G., Nuccio, F. D., Giannotti, L., Salvatore, R., Porro, C., Trotta, T., Panaro, M. A., & Lofrumento, D. D. (2016) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-016-9720-7 · Cited by 170 · see citing works
“Interestingly, IL-10 itself can also promote the M1 to M2 transition (Deng et al. 2012).”
Chronic inflammation in skeletal muscle impairs satellite cells function during regeneration: can physical exercise restore the satellite cell niche?
Perandini, L. A., Chimin, P., Lutkemeyer, D. D. S., & Câmara, N. O. S. (2018) · FEBS Journal · doi:10.1111/febs.14417 · Cited by 160 · see citing works
T reg cells limit IFN-γ production to control macrophage accrual and phenotype during skeletal muscle regeneration
Panduro, M., Benoist, C. O., & Mathis, D. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800618115 · Cited by 157 · see citing works
Skeletal muscle regeneration and impact of aging and nutrition
Domingues-Faria, C., Vasson, M.-P., Goncalves-Mendes, N., Boirie, Y., & Walrand, S. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2015.12.004 · Cited by 157 · see citing works
Pharmacological blockage of fibro/adipogenic progenitor expansion and suppression of regenerative fibrogenesis is associated with impaired skeletal muscle regeneration
Fiore, D., Judson, R. N., Low, M., Lee, S., Erica, Z., Hopkins, C. I., Xu, P., Lenzi, A., Rossi, F. M. V., & Lemos, D. R. (2016) · Stem Cell Research · doi:10.1016/j.scr.2016.06.007 · Cited by 156 · see citing works
“…and IL6 present obvious candidates as they are both highly expressed in FAPs and have established roles in regulating satellite cells and muscle regeneration (Joe et al., 2010; Lemos et al., 2012; Zhang et al., 2013; Serrano et al., 2008; Strle et al., 2007; Deng et al., 2012; Judson et al., 2013).”
Background
The Role of Metabolic Remodeling in Macrophage Polarization and Its Effect on Skeletal Muscle Regeneration
Santa, F. D., Vitiello, L., Torcinaro, A., & Ferraro, E. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7420 · Cited by 154 · see citing works
“As described in mice, after the phagocytic phase, an M1-to-M2 switch occurs, with M2 inhibiting M1 and reducing pro-inﬂammatory cytokines-mediated MPCs proliferation while stimulating their differentiation (70).”
An Overview About the Biology of Skeletal Muscle Satellite Cells
Forcina, L., Miano, C., Pelosi, L., & Musarò, A. (2019) · Current Genomics · doi:10.2174/1389202920666190116094736 · Cited by 151 · see citing works
Incorporation of macrophages into engineered skeletal muscle enables enhanced muscle regeneration
Juhas, M. E., Abutaleb, N. O., Wang, J. T., Ye, J., Shaikh, Z., Sriworarat, C., Qian, Y., & Bursac, N. (2018) · Nature Biomedical Engineering · doi:10.1038/s41551-018-0290-2 · Cited by 148 · see citing works
Interleukin-33 treatment reduces secondary injury and improves functional recovery after contusion spinal cord injury
Pomeshchik, Y., Kidin, I., Korhonen, P., Savchenko, E., Jaronen, M., Lehtonen, Š., Wojciechowski, S., Kanninen, K. M., Koıstınaho, J., & Malm, T. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.08.002 · Cited by 143 · see citing works
“For instance, IL-10, which we found to be elevated by IL-33 treatment in the spleen after SCI, is one of the cytokines mainly responsible for M2 polarization (Deng et al., 2012).”
Background
Satellite Cells and Skeletal Muscle Regeneration
Dumont, N. A., Bentzinger, C. F., Sincennes, M., & Rudnicki, M. A. (2015) · Comprehensive physiology · doi:10.1002/j.2040-4603.2015.tb00646.x · Cited by 143 · see citing works
“Consistently, the suppression of M2 macrophages in vivo leads to reduced myogenin expression and impaired fiber growth (86, 253).”
Time Course of Immune Response and Immunomodulation During Normal and Delayed Healing of Musculoskeletal Wounds
Muire, P. J., Mangum, L. H., & Wenke, J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01056 · Cited by 134 · see citing works
“M2 macrophages express IL10 and transforming growth factor (TGFβ) and favor muscle repair by promoting myoblast differentiation, fusion and myotubule formation (32, 36).”
Background
The Basis of Muscle Regeneration
Musarò, A. (2014) · Advances in Biology · doi:10.1155/2014/612471 · Cited by 138 · see citing works
“and regeneration [73].”
Immune Cells and Inflammation in Diabetic Nephropathy
Zheng, Z., & Zheng, F. (2015) · Journal of Diabetes Research · doi:10.1155/2016/1841690 · Cited by 136 · see citing works
“[54] B.”
Background
Shared signaling systems in myeloid cell-mediated muscle regeneration
Tidball, J., Dorshkind, K., & Wehling-Henricks, M. (2014) · Development · doi:10.1242/dev.098285 · Cited by 130 · see citing works
The Muscle Stem Cell Niche in Health and Disease
Mashinchian, O., Pisconti, A., Moal, E. L., & Bentzinger, C. F. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.08.003 · Cited by 127 · see citing works
Role of Gut Microbiota-Gut Hormone Axis in the Pathophysiology of Functional Gastrointestinal Disorders
Fukui, H., Xu, X., & Miwa, H. (2018) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm18071 · Cited by 128 · see citing works
“On the other hand, Th2 cytokines including IL-10 may inhibit the expression of the above cytokines, thus accelerating of GI motility.(152,154) In IBS, it is still unclear whether these cytokines simply show this pattern of interaction.”
Background
Gene regulatory network modeling of macrophage differentiation corroborates the continuum hypothesis of polarization states
Palma, A., Jarrah, A. S., Tieri, P., Cesareni, G., & Castiglione, F. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01659 · Cited by 122 · see citing works
Regenerative function of immune system: Modulation of muscle stem cells
Saini, J., McPhee, J. S., Al-Dabbagh, S., Stewart, C. E., & Al‐Shanti, N. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.03.006 · Cited by 129 · see citing works
“Furthermore, mouse myoblast 367 cell cultures supplemented with IL-10 and M2 macrophages resulted in enhanced myoblast 368 proliferation (Deng et al., 2012).”
Background
Loss of the Inducible Hsp70 Delays the Inflammatory Response to Skeletal Muscle Injury and Severely Impairs Muscle Regeneration
Judge, S. M., Howard, T. M., Ahn, B., Ferreira, L. F., & Judge, A. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062687 · Cited by 125 · see citing works
“limb immobilization as performed in the current study [48] as well as following hind limb suspension [42,64].”
BackgroundMethod
Muscle–Bone Crosstalk: Emerging Opportunities for Novel Therapeutic Approaches to Treat Musculoskeletal Pathologies
Maurel, D. B., Jähn, K., & Lara-Castillo, N. (2017) · Biomedicines · doi:10.3390/biomedicines5040062 · Cited by 122 · see citing works
“A switch can occur between M1 and M2 macrophages during regeneration [107].”
Background
Forum on bone and skeletal muscle interactions: Summary of the proceedings of an ASBMR workshop
Bonewald, L. F., Kiel, D. P., Clemens, T. L., Esser, K. A., ORWOLL, E. S., O’Keefe, R. J., & Fielding, R. A. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1980 · Cited by 119 · see citing works
“A specialized phenotype of macrophages can have positive effects on muscle growth, in contrast to the consistently negative effects of osteoclasts on bone mass.((48,49)) The M2 macrophage phenotype that predominates in injured muscle promotes muscle regeneration and supports satellite cell function, unlike M1 proinfla…”
Result
Engineered skeletal muscles for disease modeling and drug discovery
Wang, J., Khodabukus, A., Rao, L., VanDusen, K. W., Abutaleb, N. O., & Bursac, N. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2019.119416 · Cited by 117 · see citing works
Matrix-bound nanovesicles recapitulate extracellular matrix effects on macrophage phenotype
Huleihel, L., Bartolacci, J. G., Dziki, J. L., Vorobyov, T., Arnold, B., Scarritt, M. E., Pineda Molina, C., LoPresti, S. T., Brown, B. N., Naranjo, J. D., et al. (2017) · Tissue Engineering Part A · doi:10.1089/ten.tea.2017.0102 · Cited by 116 · see citing works
The Dynamic Inflammatory Tissue Microenvironment: Signality and Disease Therapy by Biomaterials
Mata, R., Yao, Y., Cao, W., Ding, J., Zhou, T., Zhai, Z., & Gao, C.-Y. (2021) · Research · doi:10.34133/2021/4189516 · Cited by 112 · see citing works
“The anti-inflammatory IL-10 plays an essential role in the polarization of macrophages from proinflammation to anti-inflammation, which boosts muscle regeneration [76].”
Background
Temporal changes in macrophage phenotype after peripheral nerve injury
Tomlinson, J. E., Žygelytė, E., Grenier, J. K., Edwards, M. G., & Cheetham, J. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1219-0 · Cited by 110 · see citing works
“There is increasing evidence that pro-inflammatory macrophages, which often predominate in early stages of tissue injury and repair [64, 65, 68, 69], are essential for the initiation of angiogenesis and attraction and proliferation of precursor cells required for repair [68–71].”
Background
The Role of Innate and Adaptive Immune Cells in Skeletal Muscle Regeneration
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Result
Extrinsic and intrinsic control of macrophage inflammatory responses
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“Ablation of IL-10 prolongs the Th1/ pro-inflammatory response, suppresses the Th2 response, and subsequently delays muscle regeneration (Deng et al., 2012).”
Background
Diabetic and idiopathic gastroparesis is associated with loss of <scp>CD</scp>206‐positive macrophages in the gastric antrum
Grover, M., Bernard, C. E., Pasricha, P. J., Parkman, H. P., Gibbons, S. J., Tonascia, J., Koch, K. L., McCallum, R. W., Sarosiek, I., Hasler, W. L., et al. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.13018 · Cited by 98 · see citing works
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Background
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“During the regeneration phase, Ly6Clow repair MFs secrete cytokines and growth factors such as insulin-like growth factor 1 (IGF-1), GDF-3, IL-10, and TGF-β that act in a paracrine and/or autocrine manner and can contribute to the repair cell milieu (Fadok et al., 1998; Lu et al., 2011; Deng et al., 2012; Tonkin et al…”
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“Although EpSCs in the basal epidermis have a prominent role in wound repair, their regenerative capacity is influenced by regulatory networks mediated by local immune responses, which are often altered by disease (Chen et al., 2015; Deng et al., 2012; Godwin et al., 2013; Naik et al., 2018).”
Background
Immunology Guides Skeletal Muscle Regeneration
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BackgroundInfluential
Exercise conditioning in old mice improves skeletal muscle regeneration
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“IL-10 IL-10 itself can also promote M1 to M2 transition (41).”
Resolvin-D2 targets myogenic cells and improves muscle regeneration in Duchenne muscular dystrophy
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Eosinophil-Derived IL-10 Supports Chronic Nematode Infection
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“By regulating macrophage phenotype, IL-10 promotes muscle regeneration and growth (60).”
Background
Autophagy in muscle regeneration: potential therapies for myopathies
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BackgroundInfluential
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“Therefore, M2 macrophages and anti-inflammatory cytokines IL-4 and IL-10 reduce inflammation and contribute to satellite cell differentiation, thus promoting myogenic differentiation (Deng et al. 2012).”
Duchenne muscular dystrophy: pathogenesis and promising therapies
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ABCA1 Protein Enhances Toll-like Receptor 4 (TLR4)-stimulated Interleukin-10 (IL-10) Secretion through Protein Kinase A (PKA) Activation
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“Interestingly, IL-10 itself can also significantly promoteM1 toM2 transition (30).”
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Regulatory interactions between muscle and the immune system during muscle regeneration
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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
ORCID: Deng, Bo
Villalta, S Armando
Wang, Ying
Tidball, James G
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
DOI: 10.4049/jimmunol.1103180
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
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
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 › Rehabilitation › 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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IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration

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