The DOI matches its Crossref record; 67 of the 68 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The chemokine system in diverse forms of macrophage activation and polarization
MANTOVANI, A., SICA, A., SOZZANI, S., ALLAVENA, P., VECCHI, A., & LOCATI, M. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.09.015 · Cited by 6,534 · cited 1×
“4), all of which are cytokines that typify a Th1 cytokine response (27).”
BackgroundFadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., & Henson, P. M. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1112 · Cited by 3,166 · cited 2×
“Furthermore, phagocytosis of apoptotic neutrophils by M1 macrophages increased production of the Th2 cytokine TGF-b by the macrophages, while reducing expression of the Th1 cytokines IL-1b and TNF-a, reflecting a shift toward an M2 phenotype (52).”
BackgroundCellular and Molecular Regulation of Muscle Regeneration
CHARGÉ, S. B. P., & Rudnicki, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00019.2003 · Cited by 2,691 · cited 1×
“The transition during myogenesis to a stage at which myogenin expression is elevated is developmentally important, because it represents the transition from a proliferative population of myogenic cells that is unable to undergo terminal differentiation to a population that has permanently withdrawn from the cell cycle…”
BackgroundArnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K., & Chazaud, B. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070075 · Cited by 2,002 · cited 3×
“These findings contrast with a previous report that showed that cocultures of muscle cells with macrophages that had been activated with the corticosteroid dexamethasone together with IL-10 caused no change in myoblast proliferation, but they increased myogenin expression (18).”
BackgroundResultInfluentialRegulatory interactions between muscle and the immune system during muscle regeneration
Tidball, J. G., & Villalta, S. A. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00735.2009 · Cited by 1,105 · cited 1×
“C hanges in muscle use or acute damage produce a rapid and highly structured inflammatory response that is dominated by successive waves of invasion of myeloid cells that can strongly influence both the magnitude of muscle damage and the rate at which repair occurs (1).”
BackgroundSelf-citationHeme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice
Lee, T.-S., & Chau, L.-Y. (2002) · Nature Medicine · doi:10.1038/nm0302-240 · Cited by 1,019 · cited 5×
“However, expression of heme oxygenase-1 (HMOX-1), which can be activated by CD163 ligation (37), was not increased at 4 d (Fig.”
BackgroundInfluentialHindlimb unloading rodent model: technical aspects
Morey, E. R., & Globus, R. K. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00969.2001 · Cited by 998
Cornelison, D., & Wold, B. J. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8721 · Cited by 934 · cited 1×
“withdraw from the cell cycle, and the expression of myogenin, also a transcription factor, increases (20, 21).”
BackgroundInterleukin-6 Is an Essential Regulator of Satellite Cell-Mediated Skeletal Muscle Hypertrophy
Serrano, A. L., Baeza-Raja, B., Perdiguero, E., Jardí, M., & Muñoz-Cánoves, P. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.011 · Cited by 873 · cited 1×
“However, the relationships between IL-6 and myoblast proliferation and differentiation are complex; IL-6 is well established as a muscle mitogen (25) that plays a significant role in muscle fiber growth (42), but it can also induce muscle wasting (43).”
BackgroundAtrophy of the soleus muscle by hindlimb unweighting
Thomason, D. B., & Booth, F. W. (1990) · Journal of Applied Physiology · doi:10.1152/jappl.1990.68.1.1 · Cited by 631 · cited 1×
“The soleus muscle is most rapidly affected and can lose 30 to 40% of its mass in 10 d through mechanisms that resemble those that occur in the muscles of patients subjected to prolonged bedrest (34).”
Background
Cited by
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
Microglial M1/M2 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
“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).”
BackgroundMuscle damage and inflammation during recovery from exercise.
Peake, J., Neubauer, O., Gatta, P. D. D., & Nosaka, K. (2016) · Journal of applied physiology · doi:10.1152/japplphysiol.00971.2016 · Cited by 740
“apoptosis and stimulate their proliferation, promote muscle regeneration and growth, as 373 well as the production of connective tissue (13, 23, 104).”
BackgroundInfluentialRegulation 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
Self-citationMacrophages in inflammation, repair and regeneration
Oishi, Y., & Manabe, I. (2018) · International Immunology · doi:10.1093/intimm/dxy054 · Cited by 770
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
“Consistently, the suppression of M2 macrophages in vivo leads to reduced myogenin expression and impaired fiber growth (86, 253).”
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 742
“removal of debris and fibrosis, for example in the mdx dystrophy model; IL-10 enhances macrophage promotion of satellite cell proliferation (131, 132).”
BackgroundMechanisms 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
Macrophage phenotypes during tissue repair
Novak, M. L., & Koh, T. J. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.1012512 · Cited by 658
“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].”
BackgroundFrailty 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
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 543
“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
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
“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-citationMonocytes 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
“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.”
BackgroundResultA 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 363
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 325
“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].”
BackgroundExercise-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 307
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
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 298
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 299
“Furthermore, myoblast proliferation is enhanced in coculture with macrophages preactivated with IL-10 to an M2 polarization (32).”
BackgroundInflammation induced loss of skeletal muscle
Londhe, P., & Guttridge, D. C. (2015) · Bone · doi:10.1016/j.bone.2015.03.015 · Cited by 276
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 268
“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.”
BackgroundInfluentialThe 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
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 256
“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 270
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
“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).”
BackgroundBiomimetic 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 250
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 257
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
“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].”
BackgroundMakita, N., Hizukuri, Y., Yamashiro, K., Murakawa, M., & Hayashi, Y. (2014) · International Immunology · doi:10.1093/intimm/dxu090 · Cited by 217
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
“The measurement of cross-section area was performed according to the published method with slight modification 54 .”
Wang, Y., Wehling‐Henricks, M., Samengo, G., & Tidball, J. G. (2015) · Aging Cell · doi:10.1111/acel.12350 · Cited by 205
“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).”
BackgroundResultMetabolic 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 206
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 211
“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].”
BackgroundFibro-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 205
“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].”
BackgroundRethinking Regenerative Medicine: A Macrophage-Centered Approach
Brown, B. N., Sicari, B. M., & Badylak, S. F. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00510 · Cited by 196
“J Biomed Mater Res A (2010) 94(4):1172–86.”
BackgroundMeteorin-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
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 187
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 172
“Interestingly, IL-10 itself can also promote the M1 to M2 transition (Deng et al. 2012).”
Perandini, L. A., Chimin, P., Lutkemeyer, D. D. S., & Câmara, N. O. S. (2018) · FEBS Journal · doi:10.1111/febs.14417 · Cited by 167
Panduro, M., Benoist, C. O., & Mathis, D. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800618115 · Cited by 164
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
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
“…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).”
BackgroundSanta, F. D., Vitiello, L., Torcinaro, A., & Ferraro, E. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7420 · Cited by 157
“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 155
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 149
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
“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).”
BackgroundMuire, P. J., Mangum, L. H., & Wenke, J. C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01056 · Cited by 152
“M2 macrophages express IL10 and transforming growth factor (TGFβ) and favor muscle repair by promoting myoblast differentiation, fusion and myotubule formation (32, 36).”
BackgroundThe Basis of Muscle Regeneration
Musarò, A. (2014) · Advances in Biology · doi:10.1155/2014/612471 · Cited by 149
“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 141
“[54] B.”
BackgroundShared signaling systems in myeloid cell-mediated muscle regeneration
Tidball, J. G., Dorshkind, K. A., & Wehling‐Henricks, M. (2014) · Development · doi:10.1242/dev.098285 · Cited by 151
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 140
Palma, A., Jarrah, A. S., Tieri, P., Cesareni, G., & Castiglione, F. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01659 · Cited by 122
Fukui, H., Xu, X., & Miwa, H. (2018) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm18071 · Cited by 128
“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.”
BackgroundRegenerative 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 130
“Furthermore, mouse myoblast 367 cell cultures supplemented with IL-10 and M2 macrophages resulted in enhanced myoblast 368 proliferation (Deng et al., 2012).”
BackgroundJudge, S. M., Howard, T. M., Ahn, B., Ferreira, L. F., & Judge, A. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062687 · Cited by 127
“limb immobilization as performed in the current study [48] as well as following hind limb suspension [42,64].”
BackgroundMethodMaurel, D. B., Jähn, K., & Lara-Castillo, N. (2017) · Biomedicines · doi:10.3390/biomedicines5040062 · Cited by 127
“A switch can occur between M1 and M2 macrophages during regeneration [107].”
BackgroundForum 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
“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…”
ResultEngineered 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 125
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
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. (2021) · Research · doi:10.34133/2021/4189516 · Cited by 116
“The anti-inflammatory IL-10 plays an essential role in the polarization of macrophages from proinflammation to anti-inflammation, which boosts muscle regeneration [76].”
BackgroundTemporal 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 112
“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].”
BackgroundThe Role of Innate and Adaptive Immune Cells in Skeletal Muscle Regeneration
Ziemkiewicz, N., Hilliard, G. M., Pullen, N., & Garg, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22063265 · Cited by 124
“The study also found that, without the induction of M2 macrophages, muscle regeneration was reduced, and muscle fiber growth was significantly slowed [100].”
ResultExtrinsic and intrinsic control of macrophage inflammatory responses
Cohen, H., & Mosser, D. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.0413236 · Cited by 106
“Early wound-associated macrophages typically release chemokines, lipid mediators, and a number of inflammatory cytokines, including (but not limited to) TNF- , IL-1 , IL-12, IL-18, and IL-23 [26, 32].”
Effect of exercise training on skeletal muscle cytokine expression in the elderly
Gatta, P. A. D., GARNHAM, A. P., Peake, J. M., & Cameron‐Smith, D. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.01.006 · Cited by 101
“Ablation of IL-10 prolongs the Th1/ pro-inflammatory response, suppresses the Th2 response, and subsequently delays muscle regeneration (Deng et al., 2012).”
BackgroundGrover, 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
Pagel, C. N., Wijesinghe, D. K. W., Esfandouni, N. T., & Mackie, E. J. (2013) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-013-0217-3 · Cited by 102
Ye, J., Xie, C., Wang, C., Huang, J., Yin, Z., Heng, B. C., Chen, X., & Shen, W. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.04.017 · Cited by 97
“IL-10 regulates the transition of macrophages from M1 to M2, which is necessary for regeneration of injured muscle [60].”
BackgroundMacrophage Polarization: Implications on Metabolic Diseases and the Role of Exercise
Silveira, L. S., Antunes, B. M., Minari, A. L. A., dos Santos, R. V. T., Neto, J. C. R., & Lira, F. S. (2016) · Critical Reviews in Eukaryotic Gene Expression · doi:10.1615/critreveukaryotgeneexpr.2016015920 · Cited by 96
Patsalos, A., Halász, L., Medina-Serpas, M. A., Berger, W. K., Dániel, B., Tzerpos, P., Kiss, M., Nagy, G., Fischer, C., Simándi, Z., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20210420 · Cited by 94
“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…”
BackgroundRegenerative inflammation: When immune cells help to re‐build tissues
Caballero‐Sánchez, N., Alonso‐Alonso, S., & Nagy, L. (2022) · FEBS Journal · doi:10.1111/febs.16693 · Cited by 100
“After the macrophage switch, the anti-inflammatory response associated with regenerative inflammation upregulates the expression IL-10 [129].”
BackgroundReparative T lymphocytes in organ injury
D’Alessio, F. R., Kurzhagen, J. T., & Rabb, H. (2019) · Journal of Clinical Investigation · doi:10.1172/jci124614 · Cited by 91
Searching for the link between inflammaging and sarcopenia
Wang, T. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101611 · Cited by 90
Acidosis differently modulates the inflammatory program in monocytes and macrophages
Riemann, A., Wußling, H., Loppnow, H., Fu, H., Reime, S., & Thews, O. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.10.017 · Cited by 89
Keratinocyte-Macrophage Crosstalk by the Nrf2/Ccl2/EGF Signaling Axis Orchestrates Tissue Repair
VILLARREAL-PONCE, A. P., Tiruneh, M. W., Lee, J., Guerrero‐Juarez, C. F., Kuhn, J. F., David, J. A., Dammeyer, K. L., Kell, R. M., Kwong, J., Rabbani, P. S., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108417 · Cited by 91
“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).”
BackgroundImmunology Guides Skeletal Muscle Regeneration
Sass, F. A., Fuchs, M. A., Pumberger, M., Geißler, S., Duda, G. N., Perka, C., & Schmidt‐Bleek, K. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19030835 · Cited by 89
“Research is therefore currently focussing on the possibility of using an artificially induced cell population or phenotypic switch in M1 to M2 macrophages to enhance regeneration in muscle [122,124].”
BackgroundSarcopenic obesity: Myokines as potential diagnostic biomarkers and therapeutic targets?
Guo, A., Li, K., & Xiao, Q. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111022 · Cited by 83
Heat stroke activates a stress-induced cytokine response in skeletal muscle.
Welc, S. S., Clanton, T., Dineen, S., & Leon, L. (2013) · Journal of applied physiology · doi:10.1152/japplphysiol.00636.2013 · Cited by 78
“Specifically, the presence of TNF- and IL-10 during recovery from injury is critical for normal muscle repair (11, 64).”
Gertz, M. L., Chin, C. R., Tomoiaga, D., MacKay, M. J., Chang, C., Butler, D., Afshinnekoo, E., Bezdan, D., Schmidt, M. A., Mozsary, C., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108429 · Cited by 84
“Important mediators include growth factors (fibroblast growth factor [FGF] basic, granulocyte colony stimulating factor [GCSF], granulocyte macrophage colony stimulating factor [GM-CSF]) (Nagaraju et al., 1998; Kuwabara et al., 2001; Park et al., 2007; Yun et al., 2010; Charoenlarp et al., 2017), which are associated…”
BackgroundInfluentialExercise conditioning in old mice improves skeletal muscle regeneration
Joanisse, S., Nederveen, J. P., Baker, J. M., Snijders, T., Iacono, C., & Parise, G. (2016) · The FASEB Journal · doi:10.1096/fj.201600143rr · Cited by 83
Human endothelial cells secrete neurotropic factors to direct axonal growth of peripheral nerves
Grasman, J. M., & Kaplan, D. L. (2017) · Scientific Reports · doi:10.1038/s41598-017-04460-8 · Cited by 81
Kang, H., Zhang, J., Wang, B., Liu, M., Zhao, J. L., Yang, M., & Li, Y. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.3841 · Cited by 81
“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
Dort, J., Orfi, Z., Fabre, P., Molina, T., Conte, T. C., Greffard, K., Pellerito, O., Bilodeau, J., & Dumont, N. A. (2021) · Nature Communications · doi:10.1038/s41467-021-26516-0 · Cited by 81
Eosinophil-Derived IL-10 Supports Chronic Nematode Infection
Huang, L., Gebreselassie, N. G., Gagliardo, L. F., Ruyechan, M. C., Lee, N. A., Lee, J. J., & Appleton, J. A. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400852 · Cited by 80
“By regulating macrophage phenotype, IL-10 promotes muscle regeneration and growth (60).”
BackgroundAutophagy in muscle regeneration: potential therapies for myopathies
Chen, W., Chen, Y., Liu, Y., & Wang, X. (2022) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.13000 · Cited by 80
Slivka, P. F., Dearth, C. L., Keane, T. J., Meng, F. W., Medberry, C. J., Riggio, R. T., Reing, J. E., & Badylak, S. F. (2014) · Biomaterials Science · doi:10.1039/c4bm00189c · Cited by 77
Reidy, P. T., McKenzie, A. I., Mahmassani, Z. S., Petrocelli, J. J., Nelson, D. B., Lindsay, C. C., Gardner, J. E., Morrow, V. R., Keefe, A., Huffaker, T. B., et al. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00422.2018 · Cited by 80
Stem Cell and Macrophage Roles in Skeletal Muscle Regenerative Medicine
Scala, P., Rehak, L., Giudice, V., Ciaglia, E., Puca, A. A., Selleri, C., Porta, G. D., & Maffulli, N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910867 · Cited by 77
“C2C12 After differentiation induction, TNF-α expression increases [80] Murine myoblasts Myoblast migration stimulation [82] Murine myoblasts Myoblast migration induction [83] C2C12 Inhibition of myoblast differentiation into myotubes [81] C2C12, Primary myoblasts Inhibition of myoblast differentiation [86] C2C12 Reduc…”
BackgroundInfluentialEffector molecules released by Th1 but not Th17 cells drive an M1 response in microglia
Prajeeth, C. K., Löhr, K., Floess, S., Zimmermann, J., Ulrich, R., Gudi, V., Beineke, A., Baumgärtner, W., Müller, M., Huehn, J., et al. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.01.001 · Cited by 76
Intrinsic Gastrointestinal Macrophages: Their Phenotype and Role in Gastrointestinal Motility
Cipriani, G., Gibbons, S. J., Kashyap, P., & Farrugia, G. (2016) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2016.01.003 · Cited by 77
Liu, X., Liu, Y., Zhao, L.-L., Zeng, Z., Xiao, W., & Chen, P. (2017) · Cell Biology International · doi:10.1002/cbin.10705 · Cited by 62
Naji, A., Muzembo, B. A., Yagyu, K.-I., Baba, N., Deschaseaux, F., Sensebé, L., & Suganuma, N. (2016) · Scientific Reports · doi:10.1038/srep26162 · Cited by 73
Dziki, J. L., Sicari, B. M., Wolf, M. T., Cramer, M. C., & Badylak, S. F. (2016) · Tissue Engineering Part A · doi:10.1089/ten.tea.2016.0340 · Cited by 72
“13 Specifically, paracrine factors secreted by M1 macrophages prompt local progenitor cells to enter the cell cycle and proliferate, thus facilitating an expansion of readily available cells with myogenic potential present at the site of injury.”
Klimczak, A., Kozłowska, U., & Kurpisz, M. K. (2018) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-018-0509-7 · Cited by 72
“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
Chang, M., Cai, Y., Gao, Z., Chen, X., Liu, B., Zhang, C., Yu, W., Cao, Q., Shen, Y., Yao, X., et al. (2023) · Journal of Neurology · doi:10.1007/s00415-023-11796-x · Cited by 68
“Some in vitro experiments have demonstrated that cytokines produced by M2 macrophages, such as interleukin-4 and interleukin-10, improve myogenic cell differentiation in vitro and increase the expression of Myog required for MuSCs differentiation [39].”
Ma, L., Dong, F., Zaid, M., Kumar, A., & Zha, X. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.413245 · Cited by 68
“Interestingly, IL-10 itself can also significantly promoteM1 toM2 transition (30).”
BackgroundGarton, T. P., Keep, R. F., Hua, Y., & Xi, G. (2017) · Translational Stroke Research · doi:10.1007/s12975-017-0535-5 · Cited by 68
Human dental pulp pluripotent-like stem cells promote wound healing and muscle regeneration
Martínez‐Sarrà, E., Montori, S., Gil-Recio, C., Núñez-Toldrà, R., Costamagna, D., Rotini, A., Atari, M., Luttun, A., & Sampaolesi, M. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0621-3 · Cited by 68
“Indeed, several reports have shown that IL-10 is primarily involved in the M2 transition and promotes muscle regeneration after acute and chronic injury [60, 61].”
Yu, B., Qin, S., Hu, B.-L., Qin, Q.-Y., Jiang, H., & Luo, W. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.109110 · Cited by 67
Human and mouse skeletal muscle stem and progenitor cells in health and disease
Mierzejewski, B., Archacka, K., Grabowska, I., Florkowska, A., Ciemerych, M. A., & Brzóska, E. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.01.004 · Cited by 70
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
