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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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“…an activation marker; CCR2, important for the recruitment of various leukocyte populations to injured muscle (Warren et al., 2005); and ST2 (encoded by Il1rl1), 1284 Cell 155, 1282–1295, December 5, 2013 ª2013 Elsevier Inc. which is the receptor for the ‘‘alarmin’’ IL-33 (Schmitz et al., 2005).”
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“A Unique Population of Treg Cells that Accumulates in Skeletal Muscle There is growing appreciation that the Treg compartment is heterogeneous, has multiple functions, and exerts influences exceeding the boundaries of the immune system (Josefowicz et al., 2012).”
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“However, expression of Egfr was undetectable in Treg cells from lymphoid (spleen, lymph node) or nonlymphoid (muscle, VAT) tissues in our microarray studies.”
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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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“Sample processing and data analysis were performed as previously described (Cipolletta et al., 2012).”
Self-citationRegulatory interactions between muscle and the immune system during muscle regeneration
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“Both ‘‘flavors’’ of myeloid cell are important for proper muscle repair, and any alteration in the tightly orchestrated scenario wherein each accumulates and functions at the site of injury can be detrimental (Tidball and Villalta, 2010).”
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The Immune System and Its Contribution to Variability in Regenerative Medicine
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Host macrophage response to injectable hydrogels derived from ECM and α-helical peptides
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NF-kB in Signaling Patterns and Its Temporal Dynamics Encode/Decode Human Diseases
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“For example, recruitment of Treg cells to injured skeletal muscle to promote tissue repair was found to bemediated by the growth factor amphiregulin and regulated by IL-18 and IL-33 (33).”
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Plasticity of the Muscle Stem Cell Microenvironment
Dinulović, I., Furrer, R., & Handschin, C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-69194-7_8 · Cited by 37
“An instrumental role of T regulatory cells in proper SC expansion and muscle regeneration, as well as in the M1 to M2 macrophage switch after injury has been described (88, 89).”
A Novel Hybrid Cytokine IL233 Mediates regeneration following Doxorubicin-Induced Nephrotoxic Injury
Sabapathy, V., Cheru, N. T., Corey, R., Mohammad, S., & Sharma, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-39886-9 · Cited by 36
Bhaskaran, N., Faddoul, F., da Silva, A. P., Jayaraman, S., Schneider, E., Mamileti, P., Weinberg, A., & Pandiyan, P. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.595936 · Cited by 35
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Tissue Resident Foxp3+ Regulatory T Cells: Sentinels and Saboteurs in Health and Disease
Lee, J., Kim, D., & Min, B. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.865593 · Cited by 38
“In vitro coculture with Treg cells induces enhanced proliferation and reduced myogenic differentiation of muscle satellite cells (106).”
BackgroundInfluentialRole of hormones in the pregnancy and sex‐specific outcomes to infections with respiratory viruses*
Cervantes, O., Talavera, I. C., Every, E., Coler, B. S., Li, M., Li, A., Li, H., & Waldorf, K. M. A. (2022) · Immunological Reviews · doi:10.1111/imr.13078 · Cited by 35
TREGking From Gut to Brain: The Control of Regulatory T Cells Along the Gut-Brain Axis
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“Transcriptome analysis of brain-infiltrated Tregs showed a profile similar to those of other tissue Tregs such as visceral adipose tissue and muscle (107, 108), with the expression of Il-10, amphiregulin (Areg), Klrg1, Pparg, and WNT signaling-related genes (22).”
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“Of note, the increased number of DAPI-stained nuclei seen in muscle injured by cardiotoxin (Figure 5A) has been reported by others to be related to inflammation, fibroblast infiltration, as well as an increase in the number of activated satellite cells that are proliferating within the injury site (29-32).”
Regulatory T Cells, a Viable Target Against Airway Allergic Inflammatory Responses in Asthma
Zhang, J., Zou, Y., Chen, L., Xu, Q., Wang, Y., Xie, M., Liu, X., Zhao, J., & Wang, C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.902318 · Cited by 33
Immunoengineering Biomaterials for Musculoskeletal Tissue Repair across Lifespan
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Tissue-Resident Lymphocytes in Solid Organ Transplantation
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“For example, VAT-resident Treg cells preserve insulin sensitivity, whereas Treg cells in the muscle promote tissue repair after injury.(63,64) Indeed, tissue repair appears to be a common function of several types of tissue-resident cells.”
BackgroundLopatina, T., Favaro, E., Grange, C., Cedrino, M., Ranghino, A., Occhipinti, S., Fallo, S., Buffolo, F., Gaykalova, D. A., Zanone, M. M., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-36143-3 · Cited by 34
T cells and their function in the immune response to viruses
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CAR-Based Therapy for Autoimmune Diseases: A Novel Powerful Option
Műzes, G., & Sípos, F. (2023) · Cells · doi:10.3390/cells12111534 · Cited by 39
Rejuvenating stem cells to restore muscle regeneration in aging
Bengal, E., Perdiguero, E., Serrano, A. L., & Muñoz‐Cánoves, P. (2017) · F1000Research · doi:10.12688/f1000research.9846.1 · Cited by 30
Dwyer, G. K., & Turnquist, H. R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.611910 · Cited by 35
“org 12 after injury through secretion of Areg that supports muscle satellite cells (75, 76) and potentially limits the local generation of inflammatory Ly6C macrophages (75).”
BackgroundUnderstanding immunity: an alternative framework beyond defense and strength
Zach, M., & Greslehner, G. P. (2023) · Biology & Philosophy · doi:10.1007/s10539-023-09893-2 · Cited by 35
Louapre, C., Rosenzwajg, M., Golse, M., Roux, A., Pitoiset, F., Adda, L., Tchitchek, N., Papeix, C., Maillart, É., Ungureanu, A., et al. (2023) · Journal of Neurology · doi:10.1007/s00415-023-11690-6 · Cited by 33
Single‐cell profiling of muscle‐infiltrating T cells in idiopathic inflammatory myopathies
Argyriou, A., Horuluoglu, B., Galindo‐Feria, A. S., Boada, J. S. D., Sijbranda, M., Notarnicola, A., Dani, L., van Vollenhoven, A., Ramsköld, D., Nennesmo, I., et al. (2023) · EMBO Molecular Medicine · doi:10.15252/emmm.202217240 · Cited by 33
“In these models, Tregs are proposed to promote muscle repair through the growth factor amphiregulin (Burzyn et al , 2013).”
BackgroundBeyond FOXP3: a 20-year journey unravelling human regulatory T-cell heterogeneity
Nirmala, S. S., Kayani, K., Gliwiński, M., Hu, Y., Iwaszkiewicz‐Grześ, D., Piotrowska, M., Sakowska, J., Tomaszewicz, M., Morales, J. M. M., Lakshmi, K., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1321228 · Cited by 37
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“This regulatory role of Tregs is further supported by studies showing that their absence enhances pro-inflammatory macrophage activity and IFN-γ expression [88], leading to increased accumulation of CD8 + T cells and fibrotic collagen deposition at the injury site [89].”
Non-coding RNAs in skeletal muscle regeneration
Gonçalves, T. J. M., & Armand, A. (2017) · Non-coding RNA Research · doi:10.1016/j.ncrna.2017.03.003 · Cited by 33
“to accumulate in injured skeletal muscles [92,93].”
Mudgapalli, N., Nallasamy, P., Chava, H., Chava, S. P., Pathania, A. S., Gunda, V., Gorantla, S., Pandey, M. K., Gupta, S. C., & Challagundla, K. B. (2019) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2019.10.001 · Cited by 31
“These cells play crucial role in immune homeostasis and can regulate various inflammatory processes such as autoimmunity and tissue injury (Grindebacke et al., 2009; Burzyn et al., 2013).”
BackgroundYan, D., Yu, F., Chen, L., Yao, Q., Yan, C., Zhang, S., Wu, N., Gong, D., Sun, H., Fu, Y., et al. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.14.22 · Cited by 32
ICOS signaling limits regulatory T cell accumulation and function in visceral adipose tissue
Mittelsteadt, K. L., Hayes, E. T., & Campbell, D. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20201142 · Cited by 31
“For example, Areg+ TR expand in skeletal muscle and the lungs in response to injury and are required for proper tissue repair (Arpaia et al., 2015; Burzyn et al., 2013), whereas TR within hair follicles and skin are essential for hair generation and inhibiting fibrosis (Ali et al., 2017; Kalekar et…”
BackgroundMagenta, A., Florio, M. C., Ruggeri, M., & Furgiuele, S. (2021) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2021.5006 · Cited by 32
“Recently, it has been observed that Treg lymphocytes are able to polarize macrophages and activate satellite cells in ischemic tissue (113).”
BackgroundHippen, K. L., Hefazi, M., Larson, J. H., & Blazar, B. R. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.926550 · Cited by 32
Profiling the lymphoid-resident T cell pool reveals modulation by age and microbiota
Durand, A., Audemard‐Verger, A., Guichard, V., Mattiuz, R., Delpoux, A., Hamon, P., Bonilla, N., Rivière, M., Delon, J., Martin, B., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-02458-4 · Cited by 34
All for One and One for All: Regenerating Skeletal MusclePreprint
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An integrated transcription factor framework for Treg identity and diversity
Chowdhary, K., Léon, J., Ramanan, D., Mathis, D., & Benoist, C. O. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2411301121 · Cited by 31
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Macrophage depletion impairs neonatal tendon regeneration
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“During muscle regeneration, specific T cell 394 subpopulations (Th1, Th2 and Tregs) have been shown to induce or impede regenerative 395 healing (40-43).”
BackgroundNon-canonical inflammasome activation mediates the adjuvanticity of nanoparticles
Muñoz‐Wolf, N., Ward, R. W., Hearnden, C. H. A., Sharp, F. A., Geoghegan, J. A., O’Grady, K., McEntee, C. P., Shanahan, K. A., Guy, C., Bowie, A., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2022.100899 · Cited by 31
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“Recent reports demonstrate that CD4-positive regulatory T cells, known to be dysregulated in HIV (20), play a critical role in suppressing muscle inflammation and injury and facilitating muscle repair (21, 22).”
BackgroundDikiy, S., Ghelani, A. P., Levine, A. G., Martis, S., Giovanelli, P., Wang, Z.-M., Beroshvili, G., Pritykin, Y., Krishna, C., Huang, X. J., et al. (2025) · Nature Immunology · doi:10.1038/s41590-024-02075-6 · Cited by 36
Beyond canonical inflammasomes: emerging pathways in IL-1-mediated autoinflammatory disease
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“resolution of inflammatory responses and to promote tissue repair [32].”
BackgroundYi, G., Guo, S., Liu, W., Wang, H., Liu, R., Tsun, A., Jin, G. Y., & Li, B. (2018) · 中国科学通报：英文版 · doi:10.1016/j.scib.2018.05.028 · Cited by 29
One, No One, and One Hundred Thousand: T Regulatory Cells' Multiple Identities in Neuroimmunity
Sambucci, M., Gargano, F., Guerrera, G., Battistini, L., & Borsellino, G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02947 · Cited by 31
“In the muscle, Tregs participate to tissue repair through the secretion of amphiregulin, which facilitates the regeneration of muscle satellite cells (110); similarly, amphiregulin production by Treg cells helps contain the damage to lung tissue following infection (111).”
BackgroundTranscriptional regulation of Treg homeostasis and functional specification
Wang, K., & Fu, W. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03534-7 · Cited by 34
Engineering skeletal muscle: Building complexity to achieve functionality
Mihaly, E., Altamirano, D. E., TUFFAHA, S. H., & Grayson, W. L. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.04.016 · Cited by 30
Spath, S., Roan, F., Presnell, S., Höllbacher, B., & Ziegler, S. F. (2022) · iScience · doi:10.1016/j.isci.2022.104998 · Cited by 30
Sitzia, C., Farini, A., Jardim, L. S., Razini, P., Belicchi, M., Cassinelli, L., Villa, C., Erratico, S., Parolini, D., Bella, P., et al. (2016) · Molecular Therapy · doi:10.1038/mt.2016.163 · Cited by 29
Li, Y., Wei, Q., Ke, X., Xu, Y.-H., Xu, B., Zhang, K., Zhu, W., Lian, X., Liu, L., & Guo, Z. (2024) · Scientific Reports · doi:10.1038/s41598-024-75164-z · Cited by 34
“In acute muscle injury models, they mainly recruit macrophages and CD4 + Tregs cells to promote macrophage polarization and activate MUSC proliferation through CD8 + T cells 42,43 .”
BackgroundNext steps in regulatory T cells: Biology and clinical application
Zou, C., Li, P., Li, B., Sparwasser, T. D., & Yuan, J. (2026) · Cell · doi:10.1016/j.cell.2025.11.035 · Cited by 29
Mempel, T. R., & Marangoni, F. (2019) · Immunological Reviews · doi:10.1111/imr.12761 · Cited by 30
Targeting ST2 expressing activated regulatory T cells in Kras-mutant lung cancer
Kim, B. S., Clinton, J., Wang, Q., & Chang, S. H. (2019) · OncoImmunology · doi:10.1080/2162402x.2019.1682380 · Cited by 29
Amphiregulin Aggravates Glomerulonephritis via Recruitment and Activation of Myeloid Cells
Melderis, S., Hagenstein, J., Warkotsch, M. T., Dang, J., Herrnstadt, G. R., Niehus, C. B., Neumann, K., Panzer, U., Berasain, C., Avila, M. A., et al. (2020) · Journal of the American Society of Nephrology · doi:10.1681/asn.2019111215 · Cited by 29
Trolese, M. C., Scarpa, C., Melfi, V., Fabbrizio, P., Sironi, F. M., Rossi, M., Bendotti, C., & Nardo, G. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.04.018 · Cited by 27
“Intriguingly, our analysis revealed that the immunosuppressive capability of MCP1-recruited Tregs [125] dampened the in ammation within the damaged tissue, sustaining the switch of M1 phagocytic macrophages towards the M2 pro-regenerative phenotype [88,126,127].”
Amphiregulin mediates non-cell-autonomous effect of senescence on reprogramming
von Joest, M., Chen, C., Douché, T., Chantrel, J., Chiche, A., Gianetto, Q. G., Matondo, M., & Li, H. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111074 · Cited by 31
Riaz, F., Wei, P. Y., & Pan, F. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.949603 · Cited by 31
Low-dose IL-2 shapes a tolerogenic gut microbiota that improves autoimmunity and gut inflammation
Tchitchek, N., Tchoumba, O. F. N., Pires, G., Dandou, S., Campagne, J., Churlaud, G., Fourcade, G., Hoffmann, T. W., Strozzi, F., Gaal, C., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.159406 · Cited by 29
“Tregs also have important roles in tissue regeneration (6), including in the intestine.”
Immunosenescence is a therapeutic target for frailty in older adults: a narrative review
Jia, H., Huang, W., Liu, C., Tang, S., Zhang, J., Chen, C., Tian, Y., & Zhong, W. (2022) · Annals of Translational Medicine · doi:10.21037/atm-22-4405 · Cited by 29
“Another study showed that a certain proportion of regulatory T cells promote muscle repair by regulating amphiregulin, the growth factor targeting muscle stem cells (53).”
BackgroundA Treg-specific long noncoding RNA maintains immune-metabolic homeostasis in aging liver
Ding, C., Yu, Z., Sefik, E., Zhou, J., Kaffe, E., Wang, G., Li, B., Flavell, R. A., Hu, W., Ye, Y., et al. (2023) · Nature Aging · doi:10.1038/s43587-023-00428-8 · Cited by 29
“There are several examples of tissue-specific adaptation of T reg cells that endow these T reg cells with better potential to maintain tissue homeostasis 50,51 .”
Self-citationDavies, O. G., Liu, Y., Player, D. J., Martin, N. R. W., Grover, L. M., & Lewis, M. P. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00194 · Cited by 29
“We will also place this in context with the current understanding of the sequential series of events leading to the formation of HO to better understand this debilitating phenomenon.”
BackgroundHuang, Q., Liu, X., Zhang, Y., Huang, J., Li, D., & Li, B. (2020) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2019.11.011 · Cited by 30
Song, Y., Li, M., Lei, S., Lü, H., Lv, Q., Liu, M., Wang, G., Wang, Z., Fu, X., & Wang, L. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121630 · Cited by 28
The Role of Muscle Stem Cells in Regeneration and Recovery after Denervation: A Review
Wong, A., & Pomerantz, J. H. (2019) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000005370 · Cited by 28
Discovery of surrogate agonists for visceral fat Treg cells that modulate metabolic indices in vivo
Fernandes, R. A., Li, C., Wang, G., Yang, X., Savvides, C. S., Glassman, C. R., Dong, S., Luxenberg, E., Sibener, L. V., Birnbaum, M. E., et al. (2020) · eLife · doi:10.7554/elife.58463 · Cited by 29
“Single-cell TCR sequencing analysis Foxp3CD4 TCRb Fat1562/A-PE Treg cells from VAT or pooled Spl/LN of 16–20 week-old Foxp3-GFP mice were first sorted in bulk before resorting as individual cells using a MoFlo (Beckman Coulter) into wells of 96-well PCR plates containing the reverse transcriptase reaction mix, and cDN…”
MethodSelf-citationFOXP3 + regulatory T cells and age‐related diseases
Deng, B., Zhang, W., Zhu, Y., Li, Y., Li, D., & Li, B. (2021) · FEBS Journal · doi:10.1111/febs.15743 · Cited by 31
Probiotics in Intestinal Mucosal Healing: A New Therapy or an Old Friend?
Filidou, E., & Kolios, G. C. (2021) · Pharmaceuticals · doi:10.3390/ph14111181 · Cited by 31
“Experimental studies from various organs in mice have shown that the depletion of Tregs deteriorates the clinical outcome by increasing the inflammation and inhibiting wound healing [99,100].”
BackgroundMetabolic regulation of stress erythropoiesis, outstanding questions, and possible paradigms
Ruan, B., & Paulson, R. F. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2022.1063294 · Cited by 30
“One of the better characterized regeneration systems is muscle regeneration, where satellite cells resident in the muscle are activated by inflammatory signals expressed by macrophages and infiltrating monocytes (Burzyn et al., 2013; Tidball, 2017; Scaramozza et al., 2019; Theret et al., 2019; Theret et al., 2022).”
BackgroundModulation of plasmacytoid dendritic cells response in inflammation and autoimmunity
Kioon, M. D. A., Laurent, P., Chaudhary, V., Du, Y., Crow, M. K., & Barrat, F. J. (2024) · Immunological Reviews · doi:10.1111/imr.13331 · Cited by 30
Tolerance induction to human stem cell transplants with extension to their differentiated progeny
Lui, K. O., Howie, D., Ng, S., Liu, S., Chien, K. R., & Waldmann, H. (2014) · Nature Communications · doi:10.1038/ncomms6629 · Cited by 28
Regulatory T cells: balancing protection versus pathology
Rakebrandt, N., Lambert, K., & Joller, N. (2016) · Swiss Medical Weekly · doi:10.4414/smw.2016.14343 · Cited by 30
Haskett, S. J., Ding, J. B., Zhang, W., Thai, A., Cullen, P. F., Xu, S., Petersen, B., Kuznetsov, G., Jandreski, L., Hamann, S., et al. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600407 · Cited by 29
“Similarly, LGT eTregs showed a clear expression of the canonical Treg signature (27), as well as shared the expression of many genes specific to other tissue-resident Tregs, such as visceral adipose tissue (VAT) (28) and muscle Tregs (29) (Fig.”
BackgroundImmune Regulation of Tissue Repair and Regeneration via miRNAs—New Therapeutic Target
Piotto, C., Julier, Z., & Martino, M. M. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00098 · Cited by 28
“Treg accumulation in muscle coincides with the switch from pro- to anti-inflammatory macrophages (Burzyn et al., 2013) and IL-33 has been reported to be crucial for Tregs accumulation in muscle (Kuswanto et al.”
BackgroundWang, Y., Welc, S. S., Wehling‐Henricks, M., Kong, Y., Thomas, C., Montecino‐Rodriguez, E., Dorshkind, K. A., & Tidball, J. G. (2022) · Aging Cell · doi:10.1111/acel.13690 · Cited by 26
“For example, immune cells that include CD8+ cytotoxic T-cells (Zhang et al., 2014) and regulatory T-cells (Burzyn et al., 2013; Wang et al., 2015) are also present in skeletal muscle where they can influence myogenesis; the functions of those cells could also be affected in mice receiving heterochronic bone marrow tra…”
BackgroundRegulatory T cells in allergic inflammation
Benamar, M., Chen, Q., Martínez‐Blanco, M., & Chatila, T. A. (2023) · Seminars in Immunology · doi:10.1016/j.smim.2023.101847 · Cited by 31
Yaghi, O., Hanna, B. S., Langston, P. K., Michelson, D. A., Jayewickreme, T., Marin-Rodero, M., Benoist, C. O., & Mathis, D. J. (2023) · Nature Immunology · doi:10.1038/s41590-023-01669-w · Cited by 25
“…with i.p. injection of ketamine:xylazine in combination (10 mg kg −1 :2 mg kg −1 ) and subsequently were injected with 0.03 ml Naja mossambica CTX (0.03 mg ml −1 ; Sigma-Aldrich) i.m. in one or more hindlimb muscles (tibialis anterior, gastrocnemius and quadriceps), as previously described 18 .”
BackgroundMethodInfluentialSelf-citationFragile Treg cells: Traitors in immune homeostasis?
Song, X., Chen, R., Li, J., Zhu, Y., Jiao, J., Liu, H., Chen, Z., & Geng, J. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107297 · Cited by 29
Harnessing immunomodulation to combat sarcopenia: current insights and possible approaches
Zhang, N., Zhai, L., Wong, R. M. Y., Cui, C., Law, S. W., Chow, S. K., Goodman, S. B., & Cheung, W. (2024) · Immunity & Ageing · doi:10.1186/s12979-024-00458-9 · Cited by 32
“T cells emerge as important contributors to the modulation of muscle during damage or injury based on clinical and pre-clinical studies [26–28].”
BackgroundRecirculating regulatory T cells mediate thymic regeneration through amphiregulin following damage
Lemarquis, A. L., Kousa, A. I., Argyropoulos, K. V., Jahn, L., Gipson, B., Pierce, J., Serrano-Marin, L., Victor, K., Kanno, Y., Girotra, N. N., et al. (2025) · Immunity · doi:10.1016/j.immuni.2025.01.006 · Cited by 27
Regulatory T cell and endothelial cell crosstalk
Piao, W., Lee, Z. L., Zapas, G., Wu, L., Jewell, C. M., Abdi, R., & Bromberg, J. S. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-025-01149-2 · Cited by 33
“Owing to the low levels of CD62L and CCR7, eT reg cells circulate and can be retained in nonlymphoid peripheral tissues such as visceral adipose tissue 178,179 , intestine 58,180 , lung 181 , muscle 182 and skin 165 .”
Peeling back the layers of immunogenicity in Cas9-based genomic medicine
Stigzelius, V., Cavallo, A. L., Chandode, R. K., & Nitsch, R. (2025) · Molecular Therapy · doi:10.1016/j.ymthe.2025.06.045 · Cited by 30
The emerging role of tissue regulatory T cells in tissue repair and regeneration
Raheem, A., Khan, I., Ahmad, I., Wajid, A., Alshahrani, M. Y., Alzahrani, F. M., Alzahrani, K. J., Qadeer, A., Liao, I., & Chen, C. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1640113 · Cited by 28
“Interestingly, autocrine EGFR signaling in Tregs has been primarily described in skin wound healing (117), but emerging evidence suggests similar mechanisms operate in lung and muscle repair (11, 20).”
InfluentialEnvironmental control of lineage plasticity and stem cell memory
Gola, A., & Fuchs, E. V. (2021) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.12.015 · Cited by 27
The engine initiating tissue regeneration: does a common mechanism exist during evolution?
Liu, Y., Lou, W. P.-K., & Fei, J. (2021) · Cell Regeneration · doi:10.1186/s13619-020-00073-1 · Cited by 27
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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