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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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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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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MethodInfluentialMacrophages and fibroblasts during inflammation and tissue repair in models of organ regeneration
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BackgroundThe Complex Role of Regulatory T Cells in Immunity and Aging
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“, 2013) and regulatory T cells (Tregs; Burzyn et al., 2013) can influence muscle regeneration and fibrosis following acute injury or disease, we tested whether transgene expression affected numbers of eosinophils or Tregs in aging muscle.”
BackgroundResultInfluentialMacrophage Plasticity in Skeletal Muscle Repair
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“A previously unrecognized population of Tregs with amphiregulin-expressing was found accumulating in injured skeletal muscle (28) and inflamed colon of mice (31).”
BackgroundInfluentialRisk factors and disease mechanisms in myositis
Miller, F. W., Lamb, J. A., Schmidt, J., & Nagaraju, K. (2018) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2018.48 · Cited by 193
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“To further characterize the phenotype and function of VAT Tregs, we asked whether these cells also express ST2, one of the chains of the IL33R, because expression of this protein has recently been reported on Tregs resident in other tissues (11, 12).”
BackgroundCurrent Methods for Skeletal Muscle Tissue Repair and Regeneration
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BackgroundModulation of regulatory T cell function and stability by co-inhibitory receptors
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“PI3K catalyses phosphorylation of phosphatidylinositol 4,5-biphosphate (PtdIns(4,5)P2) to PtdIns(3,4,5)P3, which functions as a second messenger to activate AKT.”
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Immunomodulatory bioactive glasses for tissue regeneration
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Self-citationEpicardial YAP/TAZ orchestrate an immunosuppressive response following myocardial infarction
Ramjee, V., Li, D., Manderfield, L. J., Liu, F., Engleka, K. A., Aghajanian, H. K., Rodell, C. B., Lu, W. Y., Ho, V. C., Wang, T., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci88759 · Cited by 187
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“Emerging evidence shows that AREG plays a critical role in restoring tissue integrity after infection or inflammation [145–148] and induces tolerance by promoting the restoration of tissue integrity after damage associated with acute or chronic inflammation [149, 150].”
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
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“One is tempted to suggest that these Treg ST2(+) cells contribute to hepatic repair by expression of trophic factors such as Areg, as previously described in other tissues (36, 121).”
BackgroundZhang, B., Su, Y., Zhou, J., Zheng, Y., & Zhu, D. (2021) · Advanced Science · doi:10.1002/advs.202100446 · Cited by 181
Duchenne muscular dystrophy: disease mechanism and therapeutic strategies
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“A distinct population of regulatory T cells (Foxp3+ Treg) drives the transition to a pro-regenerative state and potentiates muscle regeneration and repair (Burzyn et al., 2013).”
BackgroundDivergent 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
“Muscle regeneration capacity is similarly attenuated in CD8+-deficient mice (Zhang et al., 2014) and with the depletion of Foxp3+ CD4+ regulatory T cells (Treg cells) (Burzyn et al., 2013).”
BackgroundRegulatory T cells in skin injury: At the crossroads of tolerance and tissue repair
Boothby, I. C., Cohen, J. N., & Rosenblum, M. D. (2020) · Science Immunology · doi:10.1126/sciimmunol.aaz9631 · Cited by 182
“85,98 Tregs accumulate in skin after either epidermal abrasion or full-thickness wounding, reaching their maximal levels ~1 week after injury.”
InfluentialRegulatory T cells produce profibrotic cytokines in the skin of patients with systemic sclerosis
MacDonald, K. G., Dawson, N. A. J., Huang, Q., Dunne, J. V., Levings, M. K., & Broady, R. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2014.12.1932 · Cited by 170
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Self-citationFoxp3+ regulatory T cells promote lung epithelial proliferation
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“regeneration prolongs the proinflammatory process and impairs muscle repair, while increased Treg activities improve muscle regeneration through the expression of Amphiregulin, which acts on MuSCs [39].”
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Delacher, M., Simon, M., Sanderink, L., Hotz-Wagenblatt, A., Wuttke, M., Schambeck, K., Schmidleithner, L., Bittner, S., Pant, A., Ritter, U., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.03.007 · Cited by 164
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“This signature was more highly represented in nonlymphoid-tissue Tregs than splenic Tregs, consistent with the fact that the pan-Treg gene set includes loci related to Treg activation (40) and that nonlymphoid-tissue Tregs tend to have an activated phenotype compared with lymphoid organ Tregs (3, 7, 9).”
Self-citationBrett, J. O., Arjona, M., Ikeda, M., Quarta, M., de Morrée, A., Egner, I. M., Perandini, L. A., Ishak, H. D., Goshayeshi, A., Benjamin, D. I., et al. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0190-0 · Cited by 162
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“Tregs also produce growth factors that can directly induce the proliferation and differentiation of the tissue-resident progenitors/stem cells (7, 8).”
BackgroundSkeletal 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
Rejuvenating Strategies for Stem Cell-Based Therapies in Aging
Neves, J., Sousa‐Victor, P., & Jasper, H. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.01.008 · Cited by 160
“…recently due to their ability to dampen inflammatory responses and promote tissue repair in the skeletal muscle, heart, skin, kidney, and brain (Burzyn et al., 2013; Gandolfo et al., 2009; Nosbaum et al., 2016; Raposo et al., 2014; Villalta et al., 2014; Wan et al., 2015; Weirather et al.,…”
Immune determinants of endometrial receptivity: a biological perspective
Robertson, S. A., Moldenhauer, L. M., Green, E. S., Care, A. S., & Hull, M. L. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.04.023 · Cited by 162
Mojumdar, K., Liang, F., Giordano, C., Lemaire, C. F., Danialou, G., Okazaki, T., Bourdon, J., Rafei, M., Galipeau, J., Divangahi, M., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201403967 · Cited by 156
“…the numbers of B or T cells within acutely injured muscles (Lu et al , 2011), we do not exclude a possible role for altered regulatory T-cell (Burzyn et al , 2013) or Th2-type T-lymphocyte responses (Traynor et al , 2000; Kim et al , 2001), which could in turn lead to the production of…”
Disease Tolerance as an Inherent Component of Immunity
Martins, R., Carlos, A. R., Braza, F., Thompson, J. A., Bastos-Amador, P., Ramos, S., & Soares, M. P. (2019) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042718-041739 · Cited by 151
Emerging Functions of IL-33 in Homeostasis and Immunity
Dwyer, G. K., D’Cruz, L. M., & Turnquist, H. R. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101320-124243 · Cited by 164
pH sensing at the intersection of tissue homeostasis and inflammation
Hajjar, S., & Zhou, X. (2023) · Trends in Immunology · doi:10.1016/j.it.2023.08.008 · Cited by 165
Roles of Regulatory T Cells in Tissue Pathophysiology and Metabolism
Campbell, C., & Rudensky, A. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2019.09.010 · Cited by 154
Durães, F. D. V., Lafont, A., Beibel, M., Martin, K., Darribat, K., Cuttat, R., Waldt, A., Naumann, U., Wieczorek, G., Gaulis, S., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.130651 · Cited by 156
Beta Cell Dedifferentiation Induced by IRE1α Deletion Prevents Type 1 Diabetes
Lee, H., Lee, Y.-S., Harenda, Q., Pietrzak, S., Oktay, H. Z., Schreiber, S., Liao, Y., Sonthalia, S., Ciecko, A. E., Chen, Y.-G., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.03.002 · Cited by 152
Santa, F. D., Vitiello, L., Torcinaro, A., & Ferraro, E. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7420 · Cited by 157
“…regeneration; neutrophils and M F are very abundant in damaged muscles, as observed in human biopsies and in mice (6, 93, 340, 342), whereas eosinophils (129) and lymphoid cells (CD4 + , CD8 + , and regulatory T cells/Treg) are rare although relevant for successful regeneration (29, 34, 367).”
Interleukin-33 Promotes Serotonin Release from Enterochromaffin Cells for Intestinal Homeostasis
Chen, Z., Luo, J., Li, J., Kim, G., Stewart, A., Urban, J. F., Huang, Y., Chen, S., Wu, L., Chesler, A. T., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.10.014 · Cited by 162
“However, since recent findings indicate that IL-33 plays critical roles in tissue repair (Burzyn et al., 2013; Gadani et al., 2015) and pain sensation (Han et al., 2013; Zarpelon et al., 2016), it is possible that IL-33 controls intestinal physiology and pathophysiology in a type 2…”
Immunobiology of Inherited Muscular Dystrophies
Tidball, J. G., Welc, S. S., & Wehling‐Henricks, M. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170052 · Cited by 170
“Furthermore, reductions in their numbers by antibody depletion of CD25 + cells from mdx mice increased muscle fiber damage, reflected by higher levels of serum CK (42), and increased muscle inflammation and IFN γ expression (344).”
Red alert: labile heme is an alarmin
Soares, M. P., & Bozza, M. T. (2016) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.11.006 · Cited by 148
“Upon migration, tissue resident TREG preserve the functional integrity of damaged tissues [32-34] via a mechanism involving the expression of molecules that act directly on parenchyma cells [34] and/or that polarize tissue-resident Mø towards tissue repair [32].”
BackgroundCellular senescence impact on immune cell fate and function
Vicente, R., Mausset-Bonnefont, A.-L., Jorgensen, C., Louis-Plence, P., & Brondello, J.-M. (2016) · Aging Cell · doi:10.1111/acel.12455 · Cited by 151
“Finally, recent data from Burzyn et al. (2013) revealed a surprising and novel function for Tregs.”
BackgroundRegulatory T cells and skeletal muscle regeneration
Schiaffino, S., Pereira, M. G., Ciciliot, S., & Rovere, P. Q. (2016) · FEBS Journal · doi:10.1111/febs.13827 · Cited by 159
Activation of immunosuppressive network in the aging process
Salminen, A. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.100998 · Cited by 155
Wang, Y. X., Feige, P., Brun, C. E., Hekmatnejad, B., Dumont, N. A., Renaud, J., Faulkes, S., Guindon, D. E., & Rudnicki, M. A. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.01.002 · Cited by 151
“Alternatively, amphiregulin is secreted by Foxp3expressing regulatory T-cells during regeneration, depletion of these cells in mdx mice causes accelerated muscle degeneration and increased fibrosis (Burzyn et al., 2013).”
BackgroundThe central role of IL-33/IL-1RL1 pathway in asthma: From pathogenesis to intervention
Jayalatha, A. K. S., Hesse, L., Ketelaar, M. E., Koppelman, G. H., & Nawijn, M. C. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107847 · Cited by 150
Tissue-specific Tregs in cancer metastasis: opportunities for precision immunotherapy
Huppert, L. A., Green, M. D., Kim, L., Chow, C., Leyfman, Y., DAUD, A. I., & Lee, J. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00742-4 · Cited by 150
Therapeutic induction of antigen-specific immune tolerance
Kenison, J. E., Stevens, N. A., & Quintana, F. J. (2023) · Nature reviews. Immunology · doi:10.1038/s41577-023-00970-x · Cited by 162
“In addition, tissue-resident T reg cells in the skin 41 , muscle 42 , visceral adipose tissue 43,44 and mucosal tissues, such as intestine 45,46 and lungs 39 , display specialized phenotypes and functions, as recently reviewed 47,48 .”
Exercise and the Regulation of Inflammatory Responses
Allen, J. M., Sun, Y., & Woods, J. A. (2015) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2015.07.003 · Cited by 154
“, Amphiregulin) that regulate myocyte regeneration.(28)”
Inflammation and immunity in organ regeneration
Mescher, A. L., Neff, A. W., & King, M. W. (2016) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2016.02.015 · Cited by 145
“…recent work from different groups has revealed unique populations of Tregs capable of stimulating repair directly, at least in part through the production of amphiregulin, an epidermal growth factor family member, in both skeletal muscle (Burzyn et al., 2013) and lung (Arpaia et al., 2015).”
BackgroundNeuropeptide regulation of non-redundant ILC2 responses at barrier surfaces
Tsou, A. M., Yano, H., Parkhurst, C. N., Mahlakõiv, T., Chu, C., Zhang, W., He, Z., Jarick, K. J., Zhong, C., Putzel, G., et al. (2022) · Nature · doi:10.1038/s41586-022-05297-6 · Cited by 146
Tjärnlund, A., Tang, Q., Wick, C., Dastmalchi, M., Mann, H. F., Studýnková, J. T., Chura, R., Gullick, N., Salerno, R., Rönnelid, J., et al. (2017) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2017-211751 · Cited by 143
Epigenetic mechanisms regulating T-cell responses
Schmidl, C., Delacher, M., Huehn, J., & Feuerer, M. (2018) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2018.07.014 · Cited by 153
Regulatory T cells in skin are uniquely poised to suppress profibrotic immune responses
Kalekar, L. A., Cohen, J. N., Prevel, N., Sandoval, P. M., Mathur, A. N., Moreau, J. M., Lowe, M. M., Nosbaum, A., Wolters, P. J., Haemel, A. K., et al. (2019) · Science Immunology · doi:10.1126/sciimmunol.aaw2910 · Cited by 143
“In addition, these Tregs play major roles in mediating tissue-specific functions, such as muscle regeneration (13), lipid and glucose metabolism (14), hair follicle cycling (11), and epidermal repair (15).”
Regulatory T cell identity: formation and maintenance
Li, X., & Zheng, Y. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.04.006 · Cited by 150
Rashedi, I., Gómez-Aristizábal, A., Wang, X., Viswanathan, S., & Keating, A. (2016) · Stem Cells · doi:10.1002/stem.2485 · Cited by 142
Vasanthakumar, A., Liao, Y., Teh, P. P., Pascutti, M. F., Oja, A. E., Garnham, A. L., Gloury, R., Tempany, J. C., Sidwell, T., Cuadrado, E., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.068 · Cited by 144
Skeletal muscle stem cells in comfort and stress
Evano, B., & Tajbakhsh, S. (2018) · npj Regenerative Medicine · doi:10.1038/s41536-018-0062-3 · Cited by 144
“Notably, regulatory T cells (Treg) produce Amphiregulin that was reported to improve the regeneration process by acting on myogenic cells.(159) The inflammatory cytokine Prostaglandin E2 (PGE2) was also shown to stimulate satellite cell proliferation and enhance muscle regeneration by promoting the cAMP/phosphoCREB pa…”
BackgroundKo, J. H., Kim, H. J., Jeong, H. J., Lee, H. J., & Oh, J. Y. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.062 · Cited by 132
Li, J., Yang, Y., Tam, R. C. Y., Chan, V. W., Lan, H. Y., Hori, S., Zhou, B., & Lui, K. O. (2019) · Theranostics · doi:10.7150/thno.32734 · Cited by 137
Epigenetic and transcriptional control of Foxp3+ regulatory T cells
Huehn, J., & Beyer, M. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.02.002 · Cited by 136
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
The gut microbiota promotes distal tissue regeneration via RORγ+ regulatory T cell emissaries
Hanna, B. S., Wang, G., Galván-Peña, S., Mann, A. O., Ramirez, R. N., Muñoz-Rojas, A. R., Smith, K., Wan, M., Benoist, C., & Mathis, D. (2023) · Immunity · doi:10.1016/j.immuni.2023.01.033 · Cited by 126
Self-citation
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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