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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
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Targeting Regulatory T Cells to Treat Patients With Systemic Lupus Erythematosus
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“Previous studies have shown that Treg cells exhibiting a prorepair phenotype express high levels of the alarmin IL-33 receptor (ST2), proinflammatory cytokine receptor IL-18 (IL-18Rα or CD218α), and antiinflammatory cytokine IL-10 (13, 25).”
BackgroundOne microenvironment does not fit all: heterogeneity beyond cancer cells
Kim, I. S., & Zhang, X. H.-F. (2016) · Cancer and Metastasis Reviews · doi:10.1007/s10555-016-9643-z · Cited by 75
Graft IL-33 regulates infiltrating macrophages to protect against chronic rejection
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“Since then, secretion of the epidermal growth factor amphiregulin (Areg) by IL-33–stimulated ST2+ Tregs has been shown to support tissue repair after injury to the skeletal muscle and lung epithelium (31, 67, 68).”
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“Muscle Tregs possess high expression levels of amphiregulin (Areg), a member of the epidermal growth factor family whose receptor (epidermal growth factor receptor, EGFR) is expressed on immune cells and satellite cells (SCs) within the muscles.(4) Areg has recently been demonstrated to play a central role in orchestr…”
BackgroundMechanisms of T cell organotropism
Fu, H., Ward, E. J., & Marelli‐Berg, F. M. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2211-4 · Cited by 76
“range of tissues under homeostatic conditions, such as skin, gastrointestinal tract, lung, liver and adipose tissue [315–318].”
BackgroundVisceral adipose tissue Tregs and the cells that nurture them
Li, C., Spallanzani, R. G., & Mathis, D. J. (2020) · Immunological Reviews · doi:10.1111/imr.12850 · Cited by 73
Self-citationThe role of satellite and other functional cell types in muscle repair and regeneration
Chen, B., & Shan, T. (2019) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-019-09511-3 · Cited by 77
Regulatory T Cells in Chronic Heart Failure
Lu, Y., Xia, N., & Cheng, X. C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.732794 · Cited by 71
Exploring new perspectives in immunology
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Regulatory T cells as metabolic sensors
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Regulatory T cell is critical for interleukin-33-mediated neuroprotection against stroke
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The meninges host a distinct compartment of regulatory T cells that preserves brain homeostasis
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“Second, injection of an anti-CD25 mAb into the cisterna magna, a means to remove T regs that is less inflammatory ( 44 ) and is meninges-preferential ( 33 ), provoked meningeal changes very similar to those observed upon DT-mediated T reg depletion.”
Self-citationLegoux, F. P., Salou, M., & Lantz, O. J. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060725 · Cited by 69
Cutting Edge: c-Maf Is Required for Regulatory T Cells To Adopt RORγt+ and Follicular Phenotypes
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Leukocyte Heterogeneity in Adipose Tissue, Including in Obesity
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Regulation of regulatory T cells in cancer
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Inflammation during post-injury skeletal muscle regeneration.
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“The marked heterogeneity of Treg cells is further illustrated by the identification of populations of Treg cells in nonlymphoid tissues that can be characterized by differential chemokine receptor expression (Burzyn et al. 2013a, b).”
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“by muscle-specific Treg cells, enhancing the differentiation of muscle cell precursors and lowering the expression of proteins associated with fibrosis.(145) In conclusion, muscle-specific Treg cells play an important role once muscle damage has occurred.”
BackgroundInfluentialNair, V. S., Song, M. H., Ko, M., & Oh, K. I. (2016) · Molecules and Cells · doi:10.14348/molcells.2016.0276 · Cited by 67
“…lineage or tissue specific transcription factors like T-bet, ROR-t, Bcl6 and PPAR- to control the corresponding immune and non-immune responses (Burzyn et al., 2013; Chaudhry et al., 2009; Chung et al., 2011; Cipolletta et al., 2012; Koch et al., 2009; Linterman et al., 2011; Ohnmacht et al.,…”
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Self-citationDifferential roles of regulatory T cells in acute respiratory infections
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“Production of growth factors such as the EGFR ligand family molecule amphiregulin (AREG) has emerged as a mechanism of Treg-mediated tolerance, tissue protection, and possibly active repair, in multiple tissue types, including the lung (23, 28, 92–97).”
Functional heterogeneity of gut‐resident regulatory T cells
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“On the basis of previous reports (6, 12, 13), we anticipated that the elevated number of muscle Tregs in Ctxinjured TCR-tg mice, with their augmented expression of transcripts encoding reparative factors such as interleukin 10 and Areg, would enhance muscle repair.”
BackgroundInfluentialSelf-citationIkeno, Y., Ohara, D., Takeuchi, Y., Watanabe, H., Kondoh, G., Taura, K., Uemoto, S., & Hirota, K. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.584048 · Cited by 62
CD4 T-cells regulate angiogenesis and myogenesis
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“This discrepancy may be related to the finding that only a specific sub-population of Tregs secrete amphilregulin, which mediates these in vivo effects [62].”
BackgroundResultTissue resident regulatory T cells: novel therapeutic targets for human disease
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“Regulatory T cells are required for efficient muscle regeneration, likely by promoting macrophage phenotype switching and through the activation of satellite cells (38).”
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Immune-Mediated Repair: A Matter of Plasticity
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“AREG produced by IL1RL1 + T reg cells has been shown to be an important effector molecule for tissue repair ( 25 , 26 ).”
InfluentialImmune Modulation of Cardiac Repair and Regeneration: The Art of Mending Broken Hearts
Zlatanova, I., Pinto, C., & Silvestre, J. (2016) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2016.00040 · Cited by 66
“These muscle regulatory T cells express the growth factor amphiregulin, which acts directly on muscle satellite cells in vitro and improves muscle repair in vivo (64).”
BackgroundZEB1 protects skeletal muscle from damage and is required for its regeneration
Siles, L., Ninfali, C., Cortés, M., Darling, D. S., & Postigo, A. A. (2019) · Nature Communications · doi:10.1038/s41467-019-08983-8 · Cited by 61
Super-Treg: Toward a New Era of Adoptive Treg Therapy Enabled by Genetic Modifications
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Control of tissue‐localized immune responses by human regulatory T cells
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Selective recruitment of non-classical monocytes promotes skeletal muscle repair
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“Foxp3+ regulatory T cells are crucial to the healing of damaged skeletal muscle [54], and increasing their recruitment via”
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“We used this same gating and sorting to collect Vg6+ T cells from the lungs of 5-week-old Aire+/+ or Aire / mice. cDNA was prepared as described (Burzyn et al., 2013).”
Self-citationTissue regulatory T cells and neural repair
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The Immune System in Duchenne Muscular Dystrophy Pathogenesis
Tripodi, L., Villa, C., Molinaro, D., Torrente, Y., & Farini, A. (2021) · Biomedicines · doi:10.3390/biomedicines9101447 · Cited by 63
“In DMD, the abnormal regulation of regenerative processes leads to the rising of inflammation, the activation of the immune system and the consequent invasion of cytotoxic T-lymphocytes, neutrophils and macrophages that promot muscle damage [2,11] and cardiac dysfunctions [12–14] (Figure 1B).”
BackgroundEpigenetic Control of Regulatory T Cell Stability and Function: Implications for Translation
Joudi, A. M., Flores, C. P. R., & Singer, B. D. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.861607 · Cited by 61
The IL-1 family in tumorigenesis and antitumor immunity
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Treg specialization and functions beyond immune suppression
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“In vivo, the muscle Tregs were closely associated with the satellite cells [50].”
Challenges in tendon–bone healing: emphasizing inflammatory modulation mechanisms and treatment
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Age-associated inflammation and implications for skeletal muscle responses to exercise
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The Role of T Lymphocytes in Skeletal Muscle Repair From Traumatic and Contraction-Induced Injury
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New insights into the mechanisms of Treg function
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Myocardial Milieu Favors Local Differentiation of Regulatory T Cells
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Mechanisms of exTreg induction
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Mechanisms of cooperative cell-cell interactions in skeletal muscle regeneration
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“Tregs activated by the IL-33/ST2 axis express amphiregulin (Areg), and Areg directly stimulates EGFR on MuSCs to improve muscle repair [73].”
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“In this case, the increased frequency of Tregs not only helps to suppress inflammation, as would be expected, but also produce factors, such as amphiregulin, which enhance muscle regeneration and repair [34].”
Regulatory T Cells Promote Myositis and Muscle Damage in Toxoplasma gondii Infection
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Skeletal muscle antagonizes antiviral CD8 + T cell exhaustion
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“Previous studies have shown that naïve mice have detectable T cells within their skeletal muscle under steady-state conditions (31), supporting the idea that naïve CD8+ T cells may survive in the skeletal muscle microenvironment.”
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Writ large: Genomic dissection of the effect of cellular environment on immune response
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Regulatory T cells promote innate inflammation after skin barrier breach via TGF-β activation
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“Significant interactions included gene pathways identified to be involved in tissue-specific Treg function, including Notch-Jag and Egfr-Areg (23 , 24).”
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“As T cells can be an integral to cell functions, including macrophages, during regeneration (Burzyn et al., 2013; Nishimura et al., 2009; Zhang et al., 2014; Sadtler et al., 2016), we also assessed T cell accumulation within ANAs.”
BackgroundTargeting Inflammation in Rotator Cuff Tendon Degeneration and Repair
Abraham, A. C., Shah, S. A., & Thomopoulos, S. (2017) · Techniques in Shoulder & Elbow Surgery · doi:10.1097/bte.0000000000000124 · Cited by 53
“Skeletal muscle specific regulatory T cells were found to mediate tissue repair processes following injury by reducing late stage inflammation and secreting the growth factor amphiregulin, which acts directly on satellite cells.(54) Studies like these shed light on the phenotypic heterogeneity within immune cell popul…”
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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