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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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Citations
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InfluentialInnate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus
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InfluentialCD36-mediated metabolic adaptation supports regulatory T cell survival and function in tumors
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InfluentialSelf-citationInnate lymphoid cells in the initiation, regulation and resolution of inflammation
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BackgroundControl of satellite cell function in muscle regeneration and its disruption in ageing
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MethodSelf-citationSkeletal Muscle as Potential Central Link between Sarcopenia and Immune Senescence
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“Increasingly, studies of these pathways have uncovered interactions with basal metabolism, mucosal homeostasis, and tissue repair (Burzyn et al., 2013b; 2013a; Cipolletta et al., 2012; Heredia et al., 2013; Molofsky et al., 2013; Qiu et al., 2014; Schiering et al., 2014; Wu et al., 2011).”
BackgroundHomeostatic control of regulatory T cell diversity
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BackgroundSingle-cell gene expression reveals a landscape of regulatory T cell phenotypes shaped by the TCR
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Self-citationTreg Heterogeneity, Function, and Homeostasis
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“The mechanisms of action may vary from tissue to tissue and include: amphiregulin (a growth factor) production, promotion of proliferation and differentiation of stem cells of different tissues, inhibition of neutrophil extravasation and monocyte activity and also the limitation of osteoclastogenesis (93, 94).”
BackgroundDisease tolerance and immunity in host protection against infection
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“For both TCR chains, LN Tregs showed few CDR3 repeats (Figure 3D, left pies); the slight increase over the near-zero we previously reported (Feuerer et al., 2009; Burzyn et al., 2013) most likely reflects the advanced age of the mice in our current study.”
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BackgroundMethodInfluentialPrinciples and therapeutic applications of adaptive immunity
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BackgroundInfluentialT Cells in Fibrosis and Fibrotic Diseases
Zhang, M., & Zhang, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01142 · Cited by 344
Tissue Stem Cells: Architects of Their Niches
Fuchs, E., & Blau, H. M. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.09.011 · Cited by 332
“Since the stem cells are responsible for the reparative phase of the response, there must be intricate immune-stem cell communication to ensure not only that the pathogen invasion is under control, but also that the inflammation is subsequently dampened in order to facilitate repair (Arnold et al., 2007; Burzyn et al.…”
BackgroundInfluentialSavage, P. A., Klawon, D. E. J., & Miller, C. H. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-100219-020937 · Cited by 321
The cAMP Pathway as Therapeutic Target in Autoimmune and Inflammatory Diseases
Raker, V., Becker, C., & Steinbrink, K. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00123 · Cited by 330
“Muscle Treg distinctly express the growth factor amphiregulin, which improves muscle repair by directly acting on muscle satellite cells (114).”
BackgroundMolecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease
Almada, A. E., & Wagers, A. J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.7 · Cited by 322
Self-citationCahill, T. J., Choudhury, R. P., & Riley, P. R. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.106 · Cited by 315
Immune Modulation of Stem Cells and Regeneration
Aurora, A. B., & Olson, E. N. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.06.009 · Cited by 322
Immune-mediated pathology in Duchenne muscular dystrophy
Rosenberg, A. S., Puig, M., Nagaraju, K., Hoffman, E. P., Villalta, S. A., Rao, V. A., Wakefield, L. M., & Woodcock, J. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa7322 · Cited by 320
Thome, J. J. C., Bickham, K. L., Ohmura, Y., Kubota, M., Matsuoka, N., Gordon, C., Granot, T., Griesemer, A., Lerner, H., Kato, T., et al. (2016) · Nature Medicine · doi:10.1038/nm.4008 · Cited by 305
Tim-3: An Emerging Target in the Cancer Immunotherapy Landscape
Anderson, A. C. (2014) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-14-0039 · Cited by 307
“For example, adipose tissue Tregs express the transcription regulator PPAR-g and regulate metabolism (22), and the Tregs that accumulate in muscle tissue after muscle injury express amphiregulin, which mediates repair of damaged tissue (23).”
BackgroundExercise‐induced muscle damage: What is it, what causes it and what are the nutritional solutions?
Owens, D. J., Twist, C., Cobley, J. N., Howatson, G., & Close, G. L. (2018) · European Journal of Sport Science · doi:10.1080/17461391.2018.1505957 · Cited by 309
“…of immune cell types infiltrate the damaged tissue, including mast cells, neutrophils, T regulatory lymphocytes, eosinophils and CD8 T lymphocytes (Burzyn et al., 2013; Castiglioni et al., 2015; Cote, Tremblay, Duchesne, & Lapoite, 2008; Heredia et al., 2013; Zhang et al., 2014) to carry out…”
BackgroundRegulatory T cells in the treatment of disease
Sharabi, A., Tsokos, M., Ding, Y., Malek, T. R., Klatzmann, D., & Tsokos, G. C. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.148 · Cited by 301
Tissue regulatory T cells: regulatory chameleons
Muñoz-Rojas, A. R., & Mathis, D. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-021-00519-w · Cited by 281
Self-citationChronic Critical Illness and the Persistent Inflammation, Immunosuppression, and Catabolism Syndrome
Hawkins, R. B., Raymond, S. L., Stortz, J. A., Horiguchi, H., Brakenridge, S. C., Gardner, A. K., Efron, P. A., Bihorac, A., Segal, M. S., Moore, F. A., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01511 · Cited by 304
The Mechanisms of T Cell Selection in the Thymus
Takaba, H., & Takayanagi, H. (2017) · Trends in Immunology · doi:10.1016/j.it.2017.07.010 · Cited by 345
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
“…production of oncostatin M, underscoring the interdependence of various cellular responses (Christov et al., 2007; Latroche et al., 2017; Arnold et al., 2007; Burzyn et al., 2013; Hardy et al., 2016; Heredia et al., 2013; Joe et al., 2010; Segawa et al., 2008; Tidball and Wehling-Henricks, 2007).”
BackgroundDelacher, M., Imbusch, C. D., Hotz-Wagenblatt, A., Mallm, J.-P., Bauer, K., Simon, M., Riegel, D., Rendeiro, A. F., Bittner, S., Sanderink, L., et al. (2020) · Immunity · doi:10.1016/j.immuni.2019.12.002 · Cited by 261
Genome-wide DNA-methylation landscape defines specialization of regulatory T cells in tissues
Delacher, M., Imbusch, C. D., Weichenhan, D., Breiling, A., Hotz-Wagenblatt, A., Träger, U., Hofer, A.-C., Kägebein, D., Wang, Q., Frauhammer, F., et al. (2017) · Nature Immunology · doi:10.1038/ni.3799 · Cited by 282
Metabolic control of regulatory T cell development and function
Zeng, H., & Chi, H. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.08.003 · Cited by 282
Function of a Foxp3 cis -Element in Protecting Regulatory T Cell Identity
Li, X., Liang, Y., Leblanc, M., Benner, C. W., & Zheng, Y. (2014) · Cell · doi:10.1016/j.cell.2014.07.030 · Cited by 277
Beyond Host Defense: Emerging Functions of the Immune System in Regulating Complex Tissue Physiology
Rankin, L. C., & Artis, D. (2018) · Cell · doi:10.1016/j.cell.2018.03.013 · Cited by 275
Immune Cells and Immunotherapy for Cardiac Injury and Repair
Rurik, J. G., Aghajanian, H. K., & Epstein, J. A. (2021) · Circulation Research · doi:10.1161/circresaha.121.318005 · Cited by 275
Impaired Epidermal to Dendritic T Cell Signaling Slows Wound Repair in Aged Skin
Keyes, B. E., Liu, S., Asare, A., Naik, S., Levorse, J., Polak, L., Lu, C. P., Nikolova, M., Pasolli, H. A., & Fuchs, E. (2016) · Cell · doi:10.1016/j.cell.2016.10.052 · Cited by 266
Zebrafish Regulatory T Cells Mediate Organ-Specific Regenerative Programs
Hui, S. P., Sheng, D. Z., Sugimoto, K., González-Rajal, Á., Nakagawa, S., Hesselson, D., & Kikuchi, K. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.11.010 · Cited by 272
Allen, J. E., & Sutherland, T. E. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.06.003 · Cited by 279
Emerging Functions of Regulatory T Cells in Tissue Homeostasis
Sharma, A., & Rudra, D. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00883 · Cited by 273
Scharschmidt, T. C., Vasquez, K. S., Pauli, M. L., Leitner, E. G., Chu, K., Truong, H.-A., Lowe, M. M., Sanchez Rodriguez, R., Ali, N., Laszik, Z. G., et al. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.03.001 · Cited by 258
“Treg cells in barrier tissues, such as the skin and the intestine, are known to play an important role in promoting tolerance to commensal-derived antigens (Burzyn et al., 2013a; Scharschmidt et al., 2015).”
BackgroundMacroscale biomaterials strategies for local immunomodulation
Dellacherie, M. O., Seo, B. R., & Mooney, D. J. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0106-3 · Cited by 262
Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy
Villalta, S. A., Rosenthal, W. L., Martinez, L., Kaur, A., Sparwasser, T. D., Tidball, J. G., Margeta, M., Spencer, M. J., & Bluestone, J. A. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009925 · Cited by 267
“In summary, our studies and those reported recently by other investigators (26) reveal the therapeutic potential of targeting Tregs in muscular dystrophy and other muscle disorders.”
BackgroundResultInfluentialHBEGF + macrophages in rheumatoid arthritis induce fibroblast invasiveness
Kuo, D. C., Ding, J., Cohn, I. S., Zhang, F., Wei, K., Rao, D. A., Rozo, C. T., Sokhi, U. K., Shanaj, S., Oliver, D. J., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aau8587 · Cited by 251
“” Although leukocytederived growth factors have emerged as critical components in tissue homeostasis and repair (1, 59), our data uncovered a pathologic correlate.”
BackgroundT Regulatory Cells and Priming the Suppressive Tumor Microenvironment
Paluskievicz, C., Cao, X., Abdi, R., Zheng, P., Liu, Y., & Bromberg, J. S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02453 · Cited by 257
“For example, skeletal muscle Treg home to injured muscle in acute and chronic injury, and repair myocytes through a series of events including activation, proliferation, differentiation, migration, and formation of myofibers (143).”
BackgroundBilski, J., Pierzchalski, P., Szczepanik, M., Bonior, J., & Zoladz, J. A. (2022) · Cells · doi:10.3390/cells11010160 · Cited by 271
“Proper regeneration of skeletal muscle requires local expansion of a particular population of CD4+ CD25+ Foxp3+ regulatory T (Treg) cells [106], which is depleted in older mice [107].”
BackgroundTwo to Tango: Dialog between Immunity and Stem Cells in Health and Disease
Naik, S., Larsen, S. B., Cowley, C. J., & Fuchs, E. V. (2018) · Cell · doi:10.1016/j.cell.2018.08.071 · Cited by 246
Sawant, D. V., & Vignali, D. A. A. (2014) · Immunological Reviews · doi:10.1111/imr.12173 · Cited by 255
“Muscle-resident Tregs exhibit a distinct transcriptional profile characterized by expression of the antiinflammatory cytokine IL-10, chemokine receptor CCR1, and growth factors, namely, platederived growth factor (PDGF) and amphiregulin (Areg), that likely aid in their healing and regenerative capabilities (18).”
BackgroundHirata, Y., Furuhashi, K., Ishii, H., Li, H. W., Pinho, S., Ding, L., Robson, S. C., Frenette, P. S., & Fujisaki, J. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.01.017 · Cited by 262
“For example, specific subsets of Tregs in the visceral adipose tissue control glucose tolerance and insulin resistance (Cipolletta et al., 2012; Bapat et al., 2015), muscle Tregs potentiate muscle repair (Burzyn et al., 2013), and lung Tregs prevent tissue damage (Arpaia et al., 2015).”
BackgroundInfluentialCD4 T-Cell Subsets and the Pathophysiology of Inflammatory Bowel Disease
Gómez-Bris, R., Saéz, Á., Herrero‐Fernández, B., Rius, C., Sánchez-Martinez, H., & González, J. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032696 · Cited by 265
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
“As previously demonstrated, Treg cells promote muscle repair, accumulating in both acutely and chronically injured skeletal muscles (Burzyn et al., 2013; Castiglioni et al., 2015; Panduro et al., 2018).”
TIM-3 as a Target for Cancer Immunotherapy and Mechanisms of Action
Du, W., Yang, M., Turner, A., Xu, C., Ferris, R. L., Huang, J., Kane, L., & Lu, B. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18030645 · Cited by 242
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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