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A Special Population of Regulatory T Cells Potentiates Muscle Repair
Open accessAbstract
Long recognized to be potent suppressors of immune responses, Foxp3(+)CD4(+) regulatory T (Treg) cells are being rediscovered as regulators of nonimmunological processes. We describe a phenotypically and functionally distinct population of Treg cells that rapidly accumulated in the acutely injured skeletal muscle of mice, just as invading myeloid-lineage cells switched from a proinflammatory to a proregenerative state. A Treg population of similar phenotype accumulated in muscles of genetically dystrophic mice. Punctual depletion of Treg cells during the repair process prolonged the proinflammatory infiltrate and impaired muscle repair, while treatments that increased or decreased Treg activities diminished or enhanced (respectively) muscle damage in a dystrophy model. Muscle Treg cells expressed the growth factor Amphiregulin, which acted directly on muscle satellite cells in vitro and improved muscle repair in vivo. Thus, Treg cells and their products may provide new therapeutic opportunities for wound repair and muscular dystrophies.
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“Several publications identified the epidermal growth factor receptor ligand amphiregulin as a key factor of tissue Treg cells to maintain homeostasis or induce tissue regeneration in a diverse set of tissues, including lung, muscle, and brain [447, 448].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [447]
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“Together, these studies suggest that Treg cells protect from epithelial cell injury by both interacting with immune cells to suppress inflammation and by producing epithelial growth factors that signal to non-immune cells.”
From Amphiregulin from regulatory T cells promotes liver fibrosis and insulin resistance in non-alcoholic steatohepatitis (2024) · cites this paper as [26]
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“Production of amphiregulin (Areg) by regulatory T (Treg) cells promotes repair after acute tissue injury.”
From Amphiregulin from regulatory T cells promotes liver fibrosis and insulin resistance in non-alcoholic steatohepatitis (2024) · cites this paper as [26]
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“In these settings, Treg cell-derived Areg is notably independent of Treg cell-mediated immunosuppression, and acts on tissue-resident mesenchymal cells and stem cells - not immune cells 25,26,28 .”
From Amphiregulin from regulatory T cells promotes liver fibrosis and insulin resistance in non-alcoholic steatohepatitis (2024) · cites this paper as [26]
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“They have been shown to support tissue homeostasis and regeneration, ranging from regulating metabolic parameters in the adipose tissue to potentiating tissue repair [444-446], e.g., in skeletal muscles [447], lung tissue [448], or brain [449].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [447]
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Cites
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InfluentialInnate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus
Monticelli, L. A., Sonnenberg, G. F., Abt, M. C., Alenghat, T., Ziegler, C. G. K., Doering, T. A., Angelosanto, J., Laidlaw, B. J., Yang, C. Y., Sathaliyawala, T., et al. (2011) · Nature Immunology · doi:10.1038/ni.2131 · Cited by 1,327 · cited 1×
“Areg is an EGF family member known to promote healing and regeneration of multiple tissues, for example intestinal mucosa and lung epithelium (Shao and Sheng, 2010; Monticelli et al., 2011).”
Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus
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Bonomo, A. C., Mariz, F. P., Riederer, I., Benjamim, C. F., Butler-Browne, G. S., Mouly, V., & Savino, W. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.573347 · Cited by 27
“Muscle T regs, characteristically express ST2 and produce amphiregulin (AREG), a pleiotropic molecule with diverse functions in tissue regeneration and immune suppression (Burzyn et al., 2013; Jin et al., 2018).”
BackgroundInfluentialB and T Cell Immunity in Tissues and Across the Ages
Booth, J. S., & Toapanta, F. R. (2021) · Vaccines · doi:10.3390/vaccines9010024 · Cited by 30
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“Indeed, one of the important characteristics that was found for tissue-resident ST2+ Tregs in skin and fat was the production of amphiregulin (22), which facilitated repair from muscle damage (37) and viral infection (38).”
BackgroundImmunomodulation of Myocardial Fibrosis
Sikking, M. A., Stroeks, S. L. V. M., Marelli‐Berg, F. M., Heymans, S. R. B., Ludewig, B., & Verdonschot, J. A. J. (2023) · JACC Basic to Translational Science · doi:10.1016/j.jacbts.2023.03.015 · Cited by 28
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“So far an association between regulatory T cells and muscle repair has been clearly demonstrated 82 and osteopontin seems to influence regulatory T cell numbers 34 .”
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Regulatory T Cells: Pathophysiological Roles and Clinical Applications
Sakai, R., Komai, K., Iizuka-Koga, M., Yoshimura, A., & Ito, M. (2019) · The Keio Journal of Medicine · doi:10.2302/kjm.2019-0003-oa · Cited by 25
New function of zebrafish regulatory T cells in organ regeneration
Kikuchi, K. (2019) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.10.001 · Cited by 25
Myeloid cell diversification during regenerative inflammation: Lessons from skeletal muscle
Patsalos, A., Tzerpos, P., Wei, X., & Nagy, L. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.005 · Cited by 28
“Interestingly, macrophages and Treg cells spatially colocalized in the regenerating areas of injured muscle and experimental Treg ablation, either systemically or locally to the injured muscle, led to (i) an increase of immune cellular infiltrate, (ii) a failure of the myeloid cell compartment to undergo the expected…”
BackgroundLayilin Anchors Regulatory T Cells in Skin
Mehta, P., Gouirand, V., Boda, D. P., Zhang, J., Gearty, S. V., Zirak, B., Lowe, M. M., Clancy, S., Boothby, I. C., Mahuron, K. M., et al. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2000970 · Cited by 27
Cellular and molecular modulation of rotator cuff muscle pathophysiology
Fu, C., Huang, A. H., Galatz, L. M., & Han, W. M. (2021) · Journal of Orthopaedic Research® · doi:10.1002/jor.25179 · Cited by 24
“further supports MuSC survival and differentiation, directly impacting the regeneration (Figure 1).(50) Collectively, the evidence unequivocally highlights the important roles of immune cells in coordinating muscle regeneration through both direct and indirect”
BackgroundPregnancy and Tumour: The Parallels and Differences in Regulatory T Cells
Muralidhara, P., Sood, V., Ashok, V. V., & Bansal, K. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.866937 · Cited by 25
Telomerase reverse transcriptase and neurodegenerative diseases
Yu, X., Liu, M., Zheng, C., Liu, Y., Wang, Z., & Wang, Z.-Y. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1165632 · Cited by 25
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“Apart from inflammation and innate immune responses, adaptive immune responses including anti-dystrophin T cells and Treg cells are also present in DMDpatients (9, 11) andmdxmice (6, 12, 13).”
InfluentialDysregulated Treg repair responses lead to chronic rejection after heart transplantation
Warunek, J., Fan, L., Zhang, X., Wang, S., Sanders, S. M., Li, T., Mathews, L. R., Dwyer, G. K., Wood, M. A., Traczek, S., et al. (2024) · Journal of Clinical Investigation · doi:10.1172/jci173593 · Cited by 25
“Treg secretion of Areg is instrumental to early tissue injury repair after muscle, lung, and neuronal injury (11–13 , 30 ).”
InfluentialPoupiot, J., Verdera, H. C., Hardet, R., Colella, P., Collaud, F., Bartolo, L., Davoust, J. M., Sanatine, P., Mingozzi, F., Richard, I., et al. (2019) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2019.08.012 · Cited by 27
Transcriptional control of macrophage inflammatory shift during skeletal muscle regeneration
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Warunek, J., Jin, R. M., Blair, S. J., Garis, M. R., Marzullo, B. J., & Wohlfert, E. A. (2021) · ImmunoHorizons · doi:10.4049/immunohorizons.2100080 · Cited by 24
Macrophage-stem cell crosstalk: regulation of the stem cell niche
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Research progress of neuroinflammation-related cells in traumatic brain injury: A review
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“Treg aid in repair of acutely injured skeletal muscle, possibly because they encourage MP to switch from classical to non-classical phenotypes [68].”
Heterogeneity and Stability in Foxp3+ Regulatory T Cells
Min, B. (2017) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2017.0027 · Cited by 24
“Besides integrin expression, Treg heterogeneity is also observed based on various chemokine receptor expression levels (Campbell and Koch 2011).”
BackgroundEstrellas, K. M., Chung, L., Cheu, L. A., Sadtler, K., Majumdar, S., Mula, J., Wolf, M. T., Elisseeff, J. H., & Wagner, K. R. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.004417 · Cited by 26
“Switching from the M1 to M2 subtype is closely associated with the release of the cytokine IL-10 from FoxP3 regulatory T cells, eventually leading to the induction of cytokine-related genes, such as Il4 and Fizz1, which are associated not only with immune-related functions but also myogenesis (29, 30).”
BackgroundLi, N., Chen, Y., Wang, Q., Liu, X., Han, C., Qu, C., Guan, X., Zou, W., Wang, X., Li, A., et al. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04481-5 · Cited by 26
“The interleukin-10 (IL-10) secreted by CD4 + regulatory T cells (Treg cells) can promote the transformation of macrophages into M2 type and can also secrete amphiregulin to directly act on myogenic cells, increasing their differentiation ability [91].”
Kostrzewa‐Nowak, D., & Nowak, R. (2018) · Biochemia Medica · doi:10.11613/bm.2018.030707 · Cited by 23
“Additionally, Treg cells have recently been identified in the muscles where they promote muscle tissue repair through secretion of the growth factor amphiregulin (25).”
BackgroundeATP/P2X7R Axis: An Orchestrated Pathway Triggering Inflammasome Activation in Muscle Diseases
Panicucci, C., Raffaghello, L., Bruzzone, S., Baratto, S., Principi, E., Minetti, C., Gazzerro, E., & Bruno, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21175963 · Cited by 28
“Tregs modulate the myeloid population from a pro- to an anti-inflammatory phenotype and actively promote muscle repair, directly acting on satellite cells, via Areg secretion [75].”
BackgroundTissue Nutrient Environments and Their Effect on Regulatory T Cell Biology
Blagih, J., Hennequart, M., & Zani, F. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.637960 · Cited by 25
Interactions between islets and regulatory immune cells in health and type 1 diabetes
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“Complicating our understanding of ILCs further, several ‘regulatory’ populations of ILCs have been described, including regulatory NKlike cells that have cytokine profiles distinct from those of conventional NK cells [82–84], ILCregs which produce IL10 and TGF-β and are defined byDNA-binding protein inhibitor ID3 expr…”
BackgroundInfluentialRaffaghello, L., Principi, E., Baratto, S., Panicucci, C., Pintus, S., Antonini, F., Zotto, G. D., Benzi, A., Bruzzone, S., Scudieri, P., et al. (2022) · Pharmaceuticals · doi:10.3390/ph15010089 · Cited by 24
“On one side, they suppress type 1 inflammation by secreting IL-10; on the other side, Treg may also have direct effects on muscle growth and regeneration through secretion of amphiregulin, an epidermal growth factor family member whose receptors are expressed on muscle satellite cells that are critical for muscle rege…”
BackgroundModulation of the Activity of Stem and Progenitor Cells by Immune Cells
Alshoubaki, Y. K., Nayer, B., Das, S., & Martino, M. M. (2022) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szab022 · Cited by 25
Regulatory T-Cell Differentiation and Their Function in Immune Regulation
Piccioni, M., Chen, Z., Tsun, A., & Li, B. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-94-017-9487-9_4 · Cited by 24
Hung, L., Oniskey, T. K., Sen, D., Krummel, M. F., Vaughan, A. E., Cohen, N. A., & Herbert, D. R. (2018) · American Journal Of Pathology · doi:10.1016/j.ajpath.2018.01.020 · Cited by 23
Differential gene expression in human tissue resident regulatory T cells from lung, colon, and blood
Niedzielska, M., Israelsson, E., Angermann, B., Sidders, B. S., Clausen, M., Catley, M. C., Malhotra, R., & Dumont, C. (2018) · Oncotarget · doi:10.18632/oncotarget.26322 · Cited by 23
“For instance Treg cells may reduce bone loss [31], regulate metabolic system [25, 32], potentiate muscle repair [28], and protect against lung injury [33].”
BackgroundMijnheer, G., & van Wijk, F. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00940 · Cited by 24
“Tissue resident Treg also show a considerable oligoclonality regarding their TCR repertoire, supporting the notion that tissue Treg and Treg from the site of autoimmune inflammation share typical features (115, 116) (Figure 1).”
BackgroundAndreas, N., Potthast, M., Geiselhöringer, A.-L., Garg, G., de Jong, R., Riewaldt, J., Rußkamp, D., Riemann, M., Girard, J., Blank, S., et al. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801530 · Cited by 24
The Nr4a family regulates intrahepatic Treg proliferation and liver fibrosis in MASLD models
Aki, D., Hayakawa, T., Srirat, T., Shichino, S., Ito, M., Saitoh, S.-I., Mise-Omata, S., & Yoshimura, A. (2024) · Journal of Clinical Investigation · doi:10.1172/jci175305 · Cited by 22
“We found high expression of Areg , Il1rl1 , and Ikzf2 in the 1_1 cluster and these genes are feature of Tregs that function in tissue repair upon muscle injury (34).”
FAPs orchestrate homeostasis of muscle physiology and pathophysiology
Yin, K., Zhang, C., Deng, Z., Wei, X., Xiang, T., Yang, C. H., Chen, C., Chen, Y., & Luo, F. (2024) · The FASEB Journal · doi:10.1096/fj.202400381r · Cited by 22
“54 Ablation of Treg cells limits muscle repair 53 (Table 1).”
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Melderis, S., Warkotsch, M. T., Dang, J., Hagenstein, J., Ehnold, L.-I., Herrnstadt, G. R., Niehus, C. B., Feindt, F. C., Kylies, D., Puelles, V. G., et al. (2022) · Journal of Autoimmunity · doi:10.1016/j.jaut.2022.102829 · Cited by 22
Saba, J. B., & Turnquist, H. R. (2023) · Transplantation · doi:10.1097/tp.0000000000004447 · Cited by 22
“ST2 Treg are responsive to IL-33 in injured muscles and contribute to regeneration by secreting Areg, which acts on satellite cells to support their differentiation.(19) Experiments with ST2-deficient Treg revealed similarly impaired accumulation of Treg in injured muscle, resulting in delayed muscle repair and regene…”
BackgroundShin, D. S., Ratnapriya, S., Cashin, C. N., Kuhn, L. F., Rahimi, R. A., Anthony, R. M., & Moon, J. J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112839 · Cited by 24
Guglielmi, V., Cheli, M., Tonin, P., & Vattemi, G. N. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25052742 · Cited by 21
“Studies have demonstrated that Tregs are able to control local immune responses during regeneration after skeletal muscle injury [182,183].”
BackgroundInflammation et régénération musculaire
Dufresne, S. S., Frenette, J., & Dumont, N. A. (2016) · médecine/sciences · doi:10.1051/medsci/20163206022 · Cited by 25
“Différentes études ont montré que les lymphocytes Treg favorisent la conversion des macrophages vers le phénotype anti-inflammatoire, qu’ils stimulent la prolifération des cellules satellites à la suite d’une blessure stérile et promeuvent la régénération musculaire (Figure 2) [29, 30].”
BackgroundDittmer, M., Young, A., O’Hagan, T., Eleftheriadis, G., Bankhead, P., Dombrowski, Y., Medina, R. J., & Fitzgerald, D. C. (2018) · Molecular Brain · doi:10.1186/s13041-018-0367-6 · Cited by 21
Regulatory T cells were recruited by CCL3 to promote cryo-injured muscle repair
Zhang, C., Qiao, Y., Huang, L. J., Li, F., Zhang, Z., Yü, P., Shen, Z., Lian, J., Li, F., Zhao, L., et al. (2018) · Immunology Letters · doi:10.1016/j.imlet.2018.10.004 · Cited by 21
The SINE Compound KPT-350 Blocks Dystrophic Pathologies in DMD Zebrafish and Mice
Hightower, R. M., Reid, A. L., Gibbs, D. E., Wang, Y., Widrick, J. J., Kunkel, L. M., Kastenschmidt, J. M., Villalta, S. A., van Groen, T., Chang, H., et al. (2019) · Molecular Therapy · doi:10.1016/j.ymthe.2019.08.016 · Cited by 22
Treg regulation of the epithelial stem cell lineage
Cho, I., Lui, P. P., & Ali, N. (2020) · Journal of Immunology and Regenerative Medicine · doi:10.1016/j.regen.2020.100028 · Cited by 21
The ST2+ Treg/amphiregulin axis protects from immune-mediated hepatitis
Wachtendorf, S., Jonin, F., Ochel, A., Heinrich, F., Westendorf, A. M., Tiegs, G., & Neumann, K. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1351405 · Cited by 21
Biomaterial-Based Regenerative Strategies for Volumetric Muscle Loss: Challenges and Solutions
Cai, C. W., Grey, J. A., Hubmacher, D., & Han, W. M. (2024) · Advances in Wound Care · doi:10.1089/wound.2024.0079 · Cited by 23
“35 – 37 In addition, VML induces sustained anti-in fl ammatory M2-like macrophages that promote fi brosis, possibly through elevated TGF-b levels, signaling an increase in fi bro/adipogenic progenitor (FAP) fi brogenesis 36 and inhibiting MuSC differentiation, 38 further dysregulating the regeneration…”
The dual role of tissue regulatory T cells in tissue repair: return to homeostasis or fibrosis
Zhang, P., Wang, J., Miao, J., & Zhu, P. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1560578 · Cited by 24
Zhang, Q., Yu, J. L., Chen, Q., Yan, H., Du, H., & Luo, W. (2021) · Molecular Medicine Reports · doi:10.3892/mmr.2021.12287 · Cited by 23
Regulatory T cells-centered regulatory networks of skeletal muscle inflammation and regeneration
Chen, Z., Lan, H., Liao, Z., Huang, J.-W., Jian, X., Hu, J., & Liao, H. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00847-x · Cited by 23
“In the acute muscle injury model injected with cardiotoxin (CTX) in mice, compared with spleen, CCR2, KLRD1(an activation marker), Amphiregulin (Areg) and IL1RL1(encode ST2 receptor) were highly expressed by Treg cells [11], and Treg cells found in chronic muscle injury models of mdx mice also fell into this category…”
BackgroundInfluentialCilia‐Mediated Insulin/Akt and ST2/JNK Signaling Pathways Regulate the Recovery of Muscle Injury
Yamakawa, D., Tsuboi, J., Kasahara, K., Matsuda, C., Nishimura, Y., Kodama, T., Katayama, N., Watanabe, M., & Inagaki, M. (2022) · Advanced Science · doi:10.1002/advs.202202632 · Cited by 21
Harb, H., & Chatila, T. A. (2023) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000887 · Cited by 21
“Treg cells are recruited into the lung after tissue injury to induce repair via an Amphiregulin/IL-18 mechanism [36,37].”
BackgroundDirect IL-6 Signals Maximize Protective Secondary CD4 T Cell Responses against Influenza
Strutt, T. M., McKinstry, K. K., Kuang, Y., Finn, C. M., Hwang, J. H., Dhume, K., Sell, S., & Swain, S. L. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600033 · Cited by 21
“IL-6 could signal memory CD4 T cells directly or it could exert indirect IL-6–dependent positive effects on the 2 ̊ CD4 T cell effector response by signaling other adaptive or innate immune populations, including APCs or Foxp3 regulatory T cells (Tregs) (41).”
BackgroundMeinicke, H., Bremser, A., Brack, M., Akéus, P., Pearson, C. F., Bullers, S. J., Hoffmeyer, K., Stemmler, M. P., Quiding‐Järbrink, M., & Ízcue, A. (2017) · Immunology · doi:10.1111/imm.12750 · Cited by 21
Expression profiling of disease progression in canine model of Duchenne muscular dystrophy
Brinkmeyer‐Langford, C., Chu, C. P., Balog-Alvarez, C. J., Yu, X., Cai, J. J., Nabity, M. B., & Kornegay, J. N. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194485 · Cited by 22
Martín‐Cruz, L., Benito‐Villalvilla, C., Sirvent, S., Angelina, A., & Palomares, Ó. (2024) · International Archives of Allergy and Immunology · doi:10.1159/000536335 · Cited by 21
Human CD8+ T Cells in Asthma: Possible Pathways and Roles for NK-Like Subtypes
Lourenço, O. M., Fonseca, A. M., & Taborda‐Barata, L. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00638 · Cited by 20
“Importantly, amphiregulinproducing CD4+Foxp3+ Tregs have been described in damaged tissues, namely muscles in murine models (67).”
BackgroundFlint, T. R., Jones, J. O., Ferrer, M., Colucci, F., & Janowitz, T. (2018) · Seminars in Oncology · doi:10.1053/j.seminoncol.2018.03.005 · Cited by 19
Lindzen, M., Ghosh, S., Noronha, A., Garcia, D. D., Nataraj, N. B., Leitner, O., Carvalho, S., Zmora, E., Sapoznik, S., Bahar‐Shany, K., et al. (2021) · Oncogene · doi:10.1038/s41388-021-01784-8 · Cited by 20
“[10], it promotes restoration of tissue integrity following damage associated with inflammation [11, 12].”
BackgroundInfluentialPetrof, B. J. (2021) · The Journal of Physiology · doi:10.1113/jp281673 · Cited by 23
“Many cell types are involved in the regulation of MP plasticity, including other inflammatory cells (e.g. lymphocytes, including CD4+ regulatory T cells) and structural cells, such as fibroadipogenic progenitors, fibroblasts, endothelial and myogenic cells (Burzyn et al. 2013; Tidball, 2017).”
BackgroundFatty Acid Metabolism and T Cells in Multiple Sclerosis
Pompura, S. L., Hafler, D. A., & Dominguez‐Villar, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.869197 · Cited by 22
Kidney Bioengineering for Transplantation
Ibi, Y., & Nishinakamura, R. (2023) · Transplantation · doi:10.1097/tp.0000000000004526 · Cited by 20
“Treg are associated with transplantation and tissue repair through the secretion of immunosuppressive factors such as interleukin-10 and transforming growth factor-β, as well as tissue-specific growth factors that mobilize stem cells and promote tissue repair.(97,98) To date, Treg therapy has been shown to be safe in…”
BackgroundLi, Q.-H., Zhao, Q., Yang, W., Jiang, A., Ren, C., & Meng, Y. (2024) · Journal of Inflammation Research · doi:10.2147/jir.s459263 · Cited by 20
“168,169 Intravenous immunoglobulin, prednisolone, and TNF inhibitors, initially developed for other autoinflammatory or specific autoimmune diseases, 61,170–172 have been investigated in patients with URSA and recurrent implantation failure.”
BackgroundThe Regulatory T Cell: Jack-Of-All-Trades
Vasanthakumar, A., & Kallies, A. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.10.002 · Cited by 21
“who found that Treg cells recruited to injured skeletal muscles produced high amounts of this factor [8].”
BackgroundLymphocytes at the Heart of Wound Healing
Silva, V. M. D. S., Frantz, S., & Ramos, G. C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-57613-8_11 · Cited by 22
Shi, D.-D., Gu, R.-C., Song, Y.-F., Ding, M.-C., Huang, T., Guo, M.-X., Xiao, J.-W., Huang, W.-H., & Liao, H. (2017) · Inflammation · doi:10.1007/s10753-017-0678-2 · Cited by 19
Petkov, S., Starodubova, E. S., Latanova, A. A., Kilpeläinen, A., Latyshev, O., Svirskis, Š., Wahrén, B., Chiodi, F., Gordeychuk, I. V., & Isaguliants, M. G. (2018) · PLoS ONE · doi:10.1371/journal.pone.0197902 · Cited by 20
Regulatory T cells in ischemic cardiovascular injury and repair
Zhuang, R., & Feinberg, M. W. (2020) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2020.08.004 · Cited by 20
Maguire, G. (2017) · World Journal of Stem Cells · doi:10.4252/wjsc.v9.i11.187 · Cited by 23
Metabolic regulation of regulatory T cells: mechanisms, heterogeneity, and implications in disease
Getachew, F., Hu, J., & Benamar, M. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1729690 · Cited by 22
Fu, H., Sun, Y., Shao, Y., Saredy, J., Cueto, R., Liu, L., Drummer, C., Johnson, C., Xu, K., Lu, Y., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.595813 · Cited by 20
Moving to the Outskirts: Interplay Between Regulatory T Cells and Peripheral Tissues
Brull, A. E., Panetti, C., & Joller, N. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.864628 · Cited by 20
Myocardial-Treg Crosstalk: How to Tame a Wolf
Weiß, E., Ramos, G. C., & Delgobo, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.914033 · Cited by 19
Han, S. M., Park, E. S., Park, J., Nahmgoong, H., Choi, Y. H., Oh, J., Yim, K. M., Lee, W. T., Lee, Y. K., Jeon, Y. G., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-44181-3 · Cited by 23
“For instance, in muscle and intestine, several immune cells such as macrophages, innate lymphoid cells (ILCs), T helper cells, and Regulatory T (Treg) cells mediate stem cell proliferation and differentiation through secreting epidermal growth factor (EGF) family 53,72 .”
BackgroundImmune-cell-mediated tissue engineering strategies for peripheral nerve injury and regeneration
Zhao, X., Deng, H., Feng, Y., Wang, Y., Yao, X., Ma, Y., Zhang, L., Jie, J., Yang, P., & Yang, Y. (2024) · Journal of Materials Chemistry B · doi:10.1039/d3tb02557h · Cited by 20
A comprehensive review of the roles of T-cell immunity in preeclampsia
Xu, P., Oluchi-Amaka, I. C., Kwak-Kim, J. Y.-H., & Yang, X. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1476123 · Cited by 20
Cardiac stem cell aging and heart failure
Cesselli, D., Aleksova, A., Mazzega, E., Caragnano, A., & Beltrami, A. P. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.01.013 · Cited by 20
Deyhle, M. R., Hafen, P. S., Parmley, J., Preece, C. N., Robison, M., Sorensen, J. R., Jackson, B., Eggett, D. L., Hancock, C. R., & Hyldahl, R. D. (2018) · Physiological Reports · doi:10.14814/phy2.13689 · Cited by 19
Therapeutic Potential of Mesenchymal Stem Cells in Immune-Mediated Diseases
Eljarrah, A., Gergues, M., Pobiarzyn, P. W., Sandiford, O. A., & Rameshwar, P. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-31206-0_5 · Cited by 19
Role of IL-18 induced Amphiregulin expression on virus induced ocular lesions
Varanasi, S. K., Rajasagi, N. K., Jaggi, U., & Rouse, B. T. (2018) · Mucosal Immunology · doi:10.1038/s41385-018-0058-8 · Cited by 19
de Kivit, S., Mensink, M., Kostidis, S., Derks, R. J. E., Zaal, E. A., Heijink, M., Verleng, L. J., de Vries, E., Schrama, E., Blomberg, N., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114681 · Cited by 23
Role of regulatory T cells in inflammatory liver diseases
Yang, L., & Zheng, S. G. (2025) · Autoimmunity Reviews · doi:10.1016/j.autrev.2025.103806 · Cited by 17
Metadata
- Authors
- Burzyn, D., Kuswanto, W., Kolodin, D., Shadrach, J. L., Cerletti, M., Jang, Y., Sefik, E., Tan, T. G., Wagers, A. J., Benoist, C., & Mathis, D.
- Affiliations
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Mathis, Diane
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 155
- Issue
- 6
- Pages
- 1282-1295
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3894749
- OpenAlex
- W2151328705
- Cited by
- 1,234
- References
- 35
- Citations by year
- 2026: 98 · 2025: 96 · 2024: 101 · 2023: 103 · 2022: 112 · 2021: 117 · 2020: 106 · 2019: 111 · 2018: 112 · 2017: 100 · 2016: 73 · 2015: 62 · 2014: 41 · 2013: 1
- FWCI
- 26.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health
- Harvard Stem Cell Institute
- National Institute on Aging (R01AG033053)
- National Heart, Lung, and Blood Institute (U01HL100402)
- National Institute of Allergy and Infectious Diseases (R37AI051530)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK036836, R01DK092541)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Keywords
- regulatory T cells, Foxp3, muscle repair, skeletal muscle injury, muscle regeneration, muscular dystrophy, amphiregulin, satellite cells, myeloid cells, Treg depletion, wound healing
- MeSH terms
- Animals, Glycoproteins, Lymphoid Tissue, Mice, Inbred C57BL, Muscular Dystrophies, Receptors, Antigen, T-Cell, Regeneration, Muscle, Skeletal, Intercellular Signaling Peptides and Proteins, T-Lymphocytes, Regulatory, Mice, Transcriptome, EGF Family of Proteins, Amphiregulin
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