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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×
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Self-citationRegulatory interactions between muscle and the immune system during muscle regeneration
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Cancer Metabolism Drives a Stromal Regenerative Response
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“…pro-inflammatory M1 to a regenerative M2 phenotype is facilitated by regulatory T-cells, which coordinate both the resolution of inflammation and activation of parenchymal progenitor cells to begin the process of tissue regeneration (Arnold et al., 2007; Burzyn et al., 2013; Kuswanto et al., 2016).”
BackgroundMatias, M. I., Yong, C. S. M., Foroushani, A. B. K., Goldsmith, C., Mongellaz, C., Sezgin, E., Levental, K. R., Talebi, A., Perrault, J., Riviere, A., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109911 · Cited by 124
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“As discussed, these tissue Treg cells have altered phenotypes, distinct TCR repertoires, and function differently than Treg cells from lymphoid organs (44, 55, 147, 148).”
BackgroundInsulin‐like growth factor‐1 stimulates regulatory T cells and suppresses autoimmune disease
Bilbao, D., Luciani, L., Jóhannesson, B., Piszczek, A., & Rosenthal, N. A. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201303376 · Cited by 121
“Given recent evidence of Treg (Burzyn et al , 2013), it is likely that local stimulation of Treg cell expansion by IGF-1 may contribute to its well-documented beneficial effects in tissue regeneration as well.”
Antigen-specific regulatory T-cell responses to intestinal microbiota
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“…in ECM, as well as tissue module suppression and inflammatory fibroblasts in the context of PCL. Communication between immune and tissue modules is an area of growing interest in tissue repair as demonstrated in immune-satellite signaling in muscle 55 and lymphatic-stem cell signaling in skin 56 .”
Droplet-based forward genetic screening of astrocyte–microglia cross-talk
Wheeler, M. A., Clark, I. C., Lee, H., Li, Z., Linnerbauer, M., Rone, J. M., Blain, M., Akl, C. F., Piester, G., Giovannoni, F., et al. (2023) · Science · doi:10.1126/science.abq4822 · Cited by 125
Cancer-Derived Exosomes as Effectors of Key Inflammation-Related Players
Othman, N., Jamal, R., & Abu, N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02103 · Cited by 121
Campbell, C., Dikiy, S., Bhattarai, S. K., Chinen, T., Matheis, F., Calafiore, M., Hoyos, B. E., Hanash, A. M., Mucida, D., Bucci, V., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.04.013 · Cited by 121
Recruitment and Expansion of Tregs Cells in the Tumor Environment—How to Target Them?
Cinier, J., Hubert, M., Besson, L., Roio, A. D., Rodriguez, C., Lombardi, V., Caux, C., & Ménétrier‐Caux, C. (2021) · Cancers · doi:10.3390/cancers13081850 · Cited by 125
“ST2, another member of the IL-1R family, is constitutively expressed by a subset of resident Tregs present in nonlymphoid tissues, such as adipose tissues [291], lung [292], gut [293], colon [294] and muscle [295,296].”
BackgroundMatta, B. M., Reichenbach, D. K., Zhang, X., Mathews, L. R., Koehn, B. H., Dwyer, G. K., Lott, J. M., Uhl, F. M., Pfeifer, D., Feser, C. J., et al. (2016) · Blood · doi:10.1182/blood-2015-12-684142 · Cited by 118
“Since then, reports of IL-33 contributing to Treg function and expansion in other models have grown considerably.(37,41,49) We now demonstrate that IL-33–driven Treg expansion is maintained post-TBI, consistent with Treg radiation resistance.”
BackgroundInfluentialSchmidleithner, L., Thabet, Y., Schönfeld, E., Köhne, M., Sommer, D., Abdullah, Z., Sadlon, T. J., Osei-Sarpong, C., Subbaramaiah, K., Copperi, F., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.03.014 · Cited by 117
Savage, T. M., Fortson, K. T., de los Santos-Alexis, K., Oliveras-Alsina, A., Rouanne, M., Rae, S. S., Gamarra, J. R., Shayya, H., Kornberg, A., Cavero, R., et al. (2024) · Immunity · doi:10.1016/j.immuni.2024.01.009 · Cited by 120
Interleukin-33-induced expression of PIBF1 by decidual B cells protects against preterm labor
Huang, B., Faucette, A. N., Pawlitz, M. D., Pei, B., Goyert, J. W., Zhou, J., El-Hage, N. G., Deng, J., Lin, J., Yao, F., et al. (2016) · Nature Medicine · doi:10.1038/nm.4244 · Cited by 119
Dial, C. F., Tune, M. K., Doerschuk, C. M., & Mock, J. R. (2017) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2017-0019oc · Cited by 117
“Importantly, recent published studies by several groups have demonstrated a tissuespecific influence on the transcriptional prolife of Foxp3(1) Tregs (17, 18).”
BackgroundMethodInfluentialSommer, K., Wiendl, M., Müller, T. M., Heidbreder, K., Voskens, C., Neurath, M. F., & Zundler, S. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.643973 · Cited by 125
Metabolic regulation of macrophages during tissue repair: insights from skeletal muscle regeneration
Juban, G., & Chazaud, B. (2017) · FEBS Letters · doi:10.1002/1873-3468.12703 · Cited by 127
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Amphiregulin-producing γδ T cells are vital for safeguarding oral barrier immune homeostasis
Krishnan, S., Prise, I. E., Wemyss, K., Schenck, L. P., Bridgeman, H. M., McClure, F. A., Zangerle-Murray, T., O’Boyle, C., Barbera, T. A., Mahmood, F. A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1802320115 · Cited by 110
Immune modulation of hair follicle regeneration
Rahmani, W. M., Sinha, S., & Biernaskie, J. A. (2020) · npj Regenerative Medicine · doi:10.1038/s41536-020-0095-2 · Cited by 113
Interleukin-33 activates regulatory T cells to suppress innate γδ T cell responses in the lung
Faustino, L., Griffith, J. W., Rahimi, R. A., Nepal, K., Hamilos, D. L., Cho, J. L., Medoff, B. D., Moon, J. J., Vignali, D. A. A., & Luster, A. D. (2020) · Nature Immunology · doi:10.1038/s41590-020-0785-3 · Cited by 121
“ST2 + (GATA-3 + ) T reg cells in non-lymphoid tissues express helios and neuropilin-1 4, 11, 32 , two markers of thymus-derived T reg cells 33, 34 , and constitute a clonally expanded population after tissue injury with a TCR repertoire distinct from T reg cells in the spleen 4 .”
BackgroundInfluentialIL-33 dysregulates regulatory T cells and impairs established immunologic tolerance in the lungs
Chen, C., Kobayashi, T., Iijima, K., Hsu, F., & Kita, H. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.01.015 · Cited by 112
“For example, IL-33 promotes repair of chemically injured skeletal muscle injury, and the process appears to bemediated by a Treg cell subset producing amphiregulin.(50,52) Similarly, in the lungs of mice infected with the influenza virus, amphiregulin derived from ST2(1) IL-33– responsive Treg cells limits lung pathol…”
The 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
“, cardiotoxin-induced injury and cryo-injury) [99].”
BackgroundInfluentialInterleukin-2 and regulatory T cells in rheumatic diseases
Kolios, A. G. A., Tsokos, G. C., & Klatzmann, D. (2021) · Nature Reviews Rheumatology · doi:10.1038/s41584-021-00707-x · Cited by 116
“(89)Zrlabeled CEAtargeted IL-2 variant immunocytokine in patients with solid tumors: CEAmediated tumor accumulation and role of IL-2 receptorbinding.”
BackgroundLiu, Z., Hu, X., Liang, Y., Yu, J., Li, H., Shokhirev, M. N., & Zheng, Y. (2022) · Nature Immunology · doi:10.1038/s41590-022-01244-9 · Cited by 117
Il-10 producing T and B cells in allergy
Boonpiyathad, T., Satitsuksanoa, P., Akdiş, M., & Akdiş, C. A. (2019) · Seminars in Immunology · doi:10.1016/j.smim.2019.101326 · Cited by 109
Local administration of regulatory T cells promotes tissue healing
Nayer, B., Tan, J. L., Alshoubaki, Y. K., Lu, Y., Legrand, J. M. D., Lau, S., Hu, N., Park, A. J., Wang, X., Amann‐Zalcenstein, D., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51353-2 · Cited by 117
“Indeed, endogenous Tregs that accumulate within injured tissues have been shown to play a key role in facilitating repair or regeneration in multiple tissues and organs, such as muscle 8,9 , skin 10 , heart 11,12 , central nervous system 13 , and lung 14 .”
InfluentialTissue Immunometabolism: Development, Physiology, and Pathobiology
Man, K., Kutyavin, V. I., & Chawla, A. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.08.016 · Cited by 108
“The resident immune cell population of WAT includes a variety of innate and adaptive immune cells, including macrophages, eosinophils, group 2 innate lymphoid cells (ILC2s), and conventional and regulatory T (Tregs) cells (Mathis, 2013; Odegaard and Chawla, 2013).”
BackgroundInfluentialThe kinase DYRK1A reciprocally regulates the differentiation of Th17 and regulatory T cells
Khor, B., Gagnon, J. D., Goel, G., Roche, M. I., Conway, K. L., Tran, K. A., Aldrich, L. N., Sundberg, T. B., Paterson, A. M., Mordecai, S., et al. (2015) · eLife · doi:10.7554/elife.05920 · Cited by 108
“Gene signatures overlaid were previously reported and χ2 analyses were performed as previously reported (Hill et al., 2007; Zheng et al., 2009; Darce et al., 2012; Burzyn et al., 2013; Roychoudhuri et al., 2013; Joller et al., 2014).”
MethodRegulatory T Cell DNA Methyltransferase Inhibition Accelerates Resolution of Lung Inflammation
Singer, B. D., Mock, J. R., Aggarwal, N. R., Garibaldi, B. T., Sidhaye, V. K., Florez, M. A., Chau, E. P., Gibbs, K. W., Mandke, P., Tripathi, A., et al. (2014) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2014-0327oc · Cited by 105
“Tregs also promote repair in other tissue damage models and in clinical scenarios (6, 7).”
BackgroundT Regulatory Cells Support Plasma Cell Populations in the Bone Marrow
Zaretsky, A. G., Konradt, C., Dépis, F., Wing, J. B., Goenka, R., Gómez, D., Silver, J. S., Cho, S., Wolf, A. I., Quinn, W. J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.01.067 · Cited by 113
“Treg cells in non-lymphoid tissues have unique transcriptional profiles and functions associated with individual tissues (Burzyn et al., 2013a, 2013b; Feuerer et al., 2010).”
BackgroundSelf-citation‘Repair’ Treg Cells in Tissue Injury
Zhang, C., Li, L., Feng, K., Fan, D., Xue, W., & Lü, J. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000484295 · Cited by 111
Regulatory T Cell Development in the Thymus
Owen, D. L., Sjaastad, L. E., & Farrar, M. A. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1900662 · Cited by 111
Ohkura, N., Yasumizu, Y., Kitagawa, Y., Tanaka, A., Nakamura, Y., Motooka, D., Nakamura, S., Okada, Y., & Sakaguchi, S. (2020) · Immunity · doi:10.1016/j.immuni.2020.04.006 · Cited by 112
Shanley, L. C., Mahon, O. R., Kelly, D. J., & Dunne, A. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.02.023 · Cited by 110
Immunomodulatory effects of mesenchymal stem cells in peripheral nerve injury
Li, X., Guan, Y., Li, C., Zhang, T., Meng, F., Zhang, J., Li, J., Chen, S., Wang, Q., Wang, Y., et al. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02690-2 · Cited by 111
“T cells can regulate nerve regeneration through a variety of mechanisms, including the secretion of cytokines, release of growth factors, or direct interaction with cells [72].”
BackgroundMolecular control of regulatory T cell development and function
Kitagawa, Y., & Sakaguchi, S. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.10.002 · Cited by 112
Regulatory T cells use arginase 2 to enhance their metabolic fitness in tissues
Lowe, M. M., Boothby, I. C., Clancy, S., Ahn, R. S., Liao, W. J., Nguyen, D. N., Schumann, K., Marson, A., Mahuron, K. M., Kingsbury, G. A., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.129756 · Cited by 109
Zhou, S., Zhang, W., Cai, G., Ding, Y., Wei, C., Li, S., Yu, Y., Qin, J., Liu, D., Zhang, H., et al. (2020) · Cell Research · doi:10.1038/s41422-020-00393-6 · Cited by 105
The Xenobiotic Transporter Mdr1 Enforces T Cell Homeostasis in the Presence of Intestinal Bile Acids
Cao, W., Kayama, H., Chen, M. L., Delmas, A., Sun, A., Kim, S. Y., Rangarajan, E. S., McKevitt, K., Beck, A. P., Jackson, C. B., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.11.012 · Cited by 102
“These findings in Teff cells are consistent with the specialized functions acquired by Foxp3 Tregs in several non-lymphoid tissues, including visceral adipose tissue, lung, skeletal muscle, and colon (Arpaia et al., 2015; Burzyn et al., 2013; Cipolletta et al., 2012; Schiering et al., 2014).”
ResultGlucocorticoids Shape Macrophage Phenotype for Tissue Repair
Desgeorges, T., Caratti, G., Mounier, R., Tuckermann, J. P., & Chazaud, B. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01591 · Cited by 109
“Tregs secrete the growth factor amphiregulin that stimulates MuSC expansion and differentiation (25).”
The Role of an IL-10/Hyaluronan Axis in Dermal Wound Healing
Singampalli, K. L., Balaji, S., Wang, X., Parikh, U. M., Kaul, A., Gilley, J., Birla, R. K., Bollyky, P. L., & Keswani, S. G. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00636 · Cited by 110
Reparative and Maladaptive Inflammation in Tendon Healing
Arvind, V., & Huang, A. H. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.719047 · Cited by 107
Loreti, M., & Sacco, A. (2022) · npj Regenerative Medicine · doi:10.1038/s41536-022-00204-z · Cited by 111
Crosstalk Between Skeletal Muscle and Immune System: Which Roles Do IL-6 and Glutamine Play?
Rogeri, P. S., Gasparini, S. O., Martins, G. L., Costa, L. K. F., Araujo, C. C., Lugaresi, R., Kopfler, M., & Lancha, A. H. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.582258 · Cited by 108
The untwining of immunosenescence and aging
Xu, W., Wong, G. C. L., Hwang, Y. Y., & Larbi, A. (2020) · Seminars in Immunopathology · doi:10.1007/s00281-020-00824-x · Cited by 105
“This observation can be reversed by treatment with IL-33 which induces an increased Treg population and an associated enhancement of muscle repair [31, 32].”
BackgroundWhiteside, S. K., Grant, F. M., Győri, D., Conti, A. G., Imianowski, C. J., Kuo, P., Nasrallah, R., Sadiyah, F., Lira, S. A., Tacke, F., et al. (2021) · Immunology · doi:10.1111/imm.13337 · Cited by 96
Traxinger, B. R., Richert-Spuhler, L. E., & Lund, J. M. (2021) · Mucosal Immunology · doi:10.1038/s41385-021-00471-x · Cited by 105
Kulkarni, O. P., Lichtnekert, J., Anders, H., & Mulay, S. R. (2016) · Mediators of Inflammation · doi:10.1155/2016/2856213 · Cited by 108
Molecular mechanisms underlying Th1-like Treg generation and function
Kitz, A., & Dominguez‐Villar, M. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2569-y · Cited by 100
“Similarly, other studies have identified roles for Treg cells in muscle repair [119, 120], regulation of skin homeostasis, and prevention of skin infections [121].”
Cayrol, C. (2021) · Cells · doi:10.3390/cells11010107 · Cited by 104
Inflammation in tissue engineering: The Janus between engraftment and rejection
Crupi, A., Costa, A., Tarnok, A., Melzer, S., & Teodori, L. (2015) · European Journal of Immunology · doi:10.1002/eji.201545818 · Cited by 108
Therapeutic Potential of Regulatory T Cells in Preeclampsia—Opportunities and Challenges
Robertson, S. A., Green, E. S., Care, A. S., Moldenhauer, L. M., Prins, J. R., Hull, M. L., Barry, S. C., & Dekker, G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00478 · Cited by 100
“Like pTreg, tTregs can also be induced to proliferate and acquire greater suppressive function by antigen contact in the periphery (51, 55, 56).”
Mechanisms Underlying Mait Cell Ability to Promote Skin Wound Repair
du Halgouet, A., Darbois, A., Alkobtawi, M., Mestdagh, M., Alphonse, A., Prémel, V., Yvorra, T., Colombeau, L., Rodriguez, R., Zaiss, D. M. W., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.12.004 · Cited by 102
Hurtgen, B. J., Ward, C. L., Garg, K., Pollot, B. E., Goldman, S. M., McKinley, T. O., Wenke, J. C., & Corona, B. T. (2016) · PubMed Central · Cited by 97
Inflammatory adaptation in barrier tissues
Niec, R. E., Rudensky, A. Y., & Fuchs, E. V. (2021) · Cell · doi:10.1016/j.cell.2021.05.036 · Cited by 100
Regulatory T Cells in Post-stroke Immune Homeostasis
Liesz, A., & Kleinschnitz, C. (2016) · Translational Stroke Research · doi:10.1007/s12975-016-0465-7 · Cited by 97
“Treg cells in muscle that promote muscle regeneration [9].”
Poss, K. D., & Tanaka, E. M. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.07.007 · Cited by 97
Intrinsic immunomodulatory hydrogels for chronic inflammation
Qian, Y., Ding, J., Zhao, R., Song, Y., Yoo, J., Moon, H., Koo, S., Kim, J. S., & Shen, J. (2024) · Chemical Society Reviews · doi:10.1039/d4cs00450g · Cited by 100
Regulatory T Cells Promote Apelin-Mediated Sprouting Angiogenesis in Type 2 Diabetes
Leung, O. M., Li, J., Li, X., Chan, V. W., Yang, Y., Ku, M., Ji, L., Sun, H., Waldmann, H., Tian, X. Y., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.019 · Cited by 99
“Emerging evidence demonstrates that they accumulate in injured tissues and promote wound healing and regeneration of multiple organ systems, including heart muscle (Weirather et al., 2014), skeletal muscle (Burzyn et al., 2013), skin (Ali et al., 2017), and central nervous (Dombrowski et al., 2017).”
BackgroundRevilla, S. A., Kranenburg, O., & Coffer, P. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.903564 · Cited by 104
“eTreg cells not only dampen immune responses but also promote the regeneration and repair of injured tissue or stimulate stem cell differentiation (91, 92).”
BackgroundRegulatory T cell transfer ameliorates lymphedema and promotes lymphatic vessel function
Gousopoulos, E., Proulx, S. T., Bachmann, S. B., Scholl, J., Dionyssiou, D. D., Demiri, E. C., Halin, C., Dieterich, L. C., & Detmar, M. J. (2016) · JCI Insight · doi:10.1172/jci.insight.89081 · Cited by 97
Regulatory T cells in skeletal muscle repair and regeneration: recent insights
Wu, J., Ren, B., Wang, D., & Lin, H. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05142-8 · Cited by 101
“found better myogenicity in Aregtreated myogenic cells and speculated that it may function to promote muscle repair and regeneration through myogenic differentiation [8, 94].”
BackgroundInfluentialZhao, X., Yang, W., Yu, T., Yu, Y., Cui, X., Zhou, Z., Yang, H., Yu, Y., Bilotta, A. J., Yao, S., et al. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.09.006 · Cited by 94
Banerjee, H., & Kane, L. (2018) · F1000Research · doi:10.12688/f1000research.13446.1 · Cited by 91
The therapeutic potential of regulatory T cells for the treatment of autoimmune disease
Bluestone, J. A., Trotta, E., & Xu, D. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1037282 · Cited by 96
“Recent studies have focused on Tregs in non-lymphoid tissues, including intestinal mucosa [30], visceral adipose tissue (VAT) [31], muscle [32,33], lung [34] and skin [27].”
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
“Depletion of these cells delays muscle repair and prolongs inflammation [96 – 98].”
BackgroundListon, A., Pasciuto, E., Fitzgerald, D. C., & Yshii, L. (2023) · Nature reviews. Immunology · doi:10.1038/s41577-023-00960-z · Cited by 95
Panahi, M., Papanikolaou, A., Torabi, A., Zhang, J., Khan, H. R., Vazir, A., Hasham, M. G., Cleland, J. G. F., Rosenthal, N. A., Harding, S. E., et al. (2018) · Cardiovascular Research · doi:10.1093/cvr/cvy145 · Cited by 89
Reparative 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
Human FOXP 3+ T regulatory cell heterogeneity
Mohr, A., Malhotra, R., Mayer, G., Gorochov, G., & Miyara, M. (2018) · Clinical & Translational Immunology · doi:10.1002/cti2.1005 · Cited by 88
“In the tissues, GATA-3 Treg cells can promote tissue regeneration especially in the muscles.(38,39) Such tissue Treg cells bear the IL-33 receptor ST2.”
BackgroundAntigen presentation safeguards the integrity of the hematopoietic stem cell pool
Hernández-Malmierca, P., Vonficht, D., Schnell, A., Uckelmann, H. J., Bollhagen, A., Mahmoud, M. A. A., Landua, S.-L., van der Salm, E., Trautmann, C. L., Raffel, S., et al. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.04.007 · Cited by 83
Hyldahl, R. D., Olson, T., Welling, T., Groscost, L., & Parcell, A. C. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00485 · Cited by 94
“Interestingly, a recent study showed that skeletal muscle T-cell infiltration enhances satellite cell activity and improves muscle regeneration in mice (Burzyn et al., 2013), which, taken together with our data, suggests a potential role for IP-10 as a mediator of satellite cell activity and muscle regeneration.”
BackgroundTranscriptional and epigenetic networks of helper T and innate lymphoid cells
Shih, H., Sciumè, G., Poholek, A. C., Vahedi, G., Hirahara, K., Villarino, A. V., Bonelli, M. M., Bosselut, R., Kanno, Y., Muljo, S. A., et al. (2014) · Immunological Reviews · doi:10.1111/imr.12208 · Cited by 91
“For example, there are fat- and muscle-resident Treg cells (70, 71).”
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
“Tregs contain the number of myeloid cells and promote their switch from a pro- to an anti-inflammatory phenotype [31,121].”
BackgroundMacrophage function in the elderly and impact on injury repair and cancer
Duong, L., Radley‐Crabb, H. G., Lee, B. R., Dye, D. E., Pixley, F. J., Grounds, M. D., Nelson, D. J., & Jackaman, C. (2021) · Immunity & Ageing · doi:10.1186/s12979-021-00215-2 · Cited by 93
Skin autonomous antibody production regulates host–microbiota interactions
Gribonika, I., Band, V. I., Chi, L., Pérez‐Chaparro, P. J., Link, V. M., Ansaldo, E., Oguz, C., Bousbaine, D., Fischbach, M. A., & Belkaid, Y. (2024) · Nature · doi:10.1038/s41586-024-08376-y · Cited by 88
Epigenetic reprogramming of immune cells in injury, repair, and resolution
Placek, K., Schultze, J. L., & Aschenbrenner, A. C. (2019) · Journal of Clinical Investigation · doi:10.1172/jci124619 · Cited by 86
“Tregs can also directly affect wound healing by producing growth factors such as amphiregulin (141), which promotes tissue regeneration.”
BackgroundDavoli-Ferreira, M., de Lima, K. A., Fonseca, M. M., Guimarães, R. M., Gomes, F. I. F., Cavallini, M. C. M., de Quadros, A. U., Kusuda, R., Cunha, F. Q., Alves-Filho, J. C., et al. (2020) · Pain · doi:10.1097/j.pain.0000000000001879 · Cited by 91
“For the expansion of Tregs, we used the protocol described by Burzyn et al.(7) Briefly, we incubated 2.”
MethodResultInfluentialThe Role of IL-33-Dependent Inflammation in the Tumor Microenvironment
Wasmer, M.-H., & Krebs, P. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00682 · Cited by 84
CAR-T cell therapy: developments, challenges and expanded applications from cancer to autoimmunity
Kong, Y., Li, J., Zhao, X., Wu, Y., & Chen, L. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1519671 · Cited by 96
Natural and modified IL-2 for the treatment of cancer and autoimmune diseases
Mizui, M. (2018) · Clinical Immunology · doi:10.1016/j.clim.2018.11.002 · Cited by 84
IL-33 Signaling Alters Regulatory T Cell Diversity in Support of Tumor Development
Li, A., Herbst, R. H., Canner, D. A., Schenkel, J. M., Smith, O. C. G., Kim, J. Y., Hillman, M., Bhutkar, A. J., Cuoco, M. S., Rappazzo, C. G., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.120 · Cited by 83
“Klrg1 and Areg expression have been associated with Treg differentiation and tissue repair, respectively (Arpaia et al., 2015; Burzyn et al., 2013; Cheng et al., 2012).”
BackgroundShime, H., Odanaka, M., Tsuiji, M., Matoba, T., Imai, M., Yasumizu, Y., Uraki, R., Minohara, K., Watanabe, M., Bonito, A. J., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2000372117 · Cited by 85
“We next analyzed the gene expression of Treg cells from VAT, muscle, and brain using the database (18, 19, 22).”
BackgroundMethodBrain-resident regulatory T cells and their role in health and disease
Liston, A., Dooley, J., & Yshii, L. (2022) · Immunology Letters · doi:10.1016/j.imlet.2022.06.005 · Cited by 89
Treg cell therapy: How cell heterogeneity can make the difference
Giganti, G., Atif, M., Mohseni, Y., Mastronicola, D., Grageda, N., Povoleri, G. A., Miyara, M., & Scottà, C. (2021) · European Journal of Immunology · doi:10.1002/eji.201948131 · Cited by 82
Immune-Epithelial Cross Talk in Regeneration and Repair
Guenin‐Macé, L., Konieczny, P., & Naik, S. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101721-062818 · Cited by 85
“Indeed, Treg-derived AREG limits inflammation in muscle repair (75).”
BackgroundLangston, P. K., Sun, Y., Ryback, B. A., Mueller, A. L., Spiegelman, B. M., Benoist, C. O., & Mathis, D. J. (2023) · Science Immunology · doi:10.1126/sciimmunol.adi5377 · Cited by 82
“Given their reported roles in controlling inflammation and potentiating tissue regeneration after injury ( 11 ), we addressed the role of T regs in exercise-induced changes in muscle properties and exercise capacity.”
BackgroundMethodResultInfluentialSelf-citationEmerging role of immune cells as drivers of pulmonary fibrosis
Mutsaers, S. E., Miles, T., Prêle, C. M., & Hoyne, G. F. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108562 · Cited by 89
Pathological conditions re-shape physiological Tregs into pathological Tregs
Yang, W. Y., Shao, Y., Lopez‐Pastrana, J., Mai, J., Wang, H., & Yang, X. (2015) · Burns & Trauma · doi:10.1186/s41038-015-0001-0 · Cited by 82
“This report not only revealed a new function of Tregs in modulating tissue repair but also proposed a new pathway for Treg generation [20]; 2) whether there are tissue-resident Tregs, in other words, whether tissue physiological environment modulates Tregs’ genotypes and phenotypes; 3) how do Tregs maintain their own…”
BackgroundImmune‐ and non‐immune‐mediated roles of regulatory T‐cells during wound healing
Zaiss, D. M. W., Minutti, C. M., & Knipper, J. A. (2019) · Immunology · doi:10.1111/imm.13057 · Cited by 84
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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