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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The epidermal growth factor receptor ligand amphiregulin is 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.
“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]
The Results section (page unavailable) identifies amphiregulin as an EGFR ligand expressed by muscle Treg cells and reports that it enhances muscle-repair measures. The Discussion (page unavailable) mentions lung healing, but not as a finding about lung Treg cells; the paper does not establish the claimed role for tissue Tregs across lung, muscle, and brain. (LLM, conf=0.86)
Experimental — accuracy not yet measuredTreg 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.
“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]
The Discussion section (“How Might Treg Cells Influence Muscle Repair”; page not provided) says Treg cells regulate inflammatory myeloid cells and that Treg-produced amphiregulin may act on muscle satellite cells. The Results section identifies amphiregulin as a member of the EGF family. These findings concern repair of injured muscle, not protection from epithelial cell injury, so the claim extends the paper’s findings to a different tissue. (LLM, conf=0.86)
Experimental — accuracy not yet measuredTreg cell-derived amphiregulin (Areg) promotes repair after acute tissue injury.
“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]
The Results section (page unavailable) shows that muscle Treg cells express Areg and that administered Areg improved repair-related measures after acute muscle injury in mice. The claim extends this muscle-specific evidence to acute tissue injury generally; the experiment also tested administered Areg rather than directly establishing that Treg-derived Areg caused the repair. (LLM, conf=0.84)
Experimental — accuracy not yet measuredIn acute injury settings, Treg cell-derived Areg is independent of Treg cell-mediated immunosuppression and acts on tissue-resident mesenchymal cells and stem cells, not immune cells.
“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]
The Results section (page unavailable) reports that Areg enhanced muscle regeneration and, when Tregs were present, affected repair-related genes without significantly affecting immune-response genes. The Discussion says Areg may directly affect muscle satellite cells. These findings support a nonimmune route for muscle repair, but do not establish that Treg-derived Areg is independent of Treg-mediated immunosuppression or acts on mesenchymal cells and stem cells rather than any immune cells. (LLM, conf=0.86)
Experimental — accuracy not yet measuredTreg cells support tissue homeostasis and regeneration, ranging from regulating metabolic parameters in adipose tissue to potentiating tissue repair in skeletal muscles, lung tissue, or brain.
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Schmitz, J., Owyang, A. M., Oldham, E. R., Song, Y., Murphy, E., McClanahan, T. K., Zurawski, G., Moshrefi, M., Qin, J., Li, X., et al. (2005) · Immunity · doi:10.1016/j.immuni.2005.09.015 · Cited by 3,701 · cited 1× · see citing works
“…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).”
Regulatory T cells: mechanisms of differentiation and function
Josefowicz, S. Z., Lu, L.-F., & Rudensky, A. Y. (2012) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141623 · Cited by 2,866 · cited 7× · see citing works
“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).”
InfluentialFeuerer, M., Herrero, L., Cipolletta, D., Naaz, A., Wong, J., Nayer, A., Lee, J., Goldfine, A. B., Benoist, C., Shoelson, S., et al. (2009) · Nature Medicine · doi:10.1038/nm.2002 · Cited by 2,145 · cited 3× · see citing works
“However, expression of Egfr was undetectable in Treg cells from lymphoid (spleen, lymph node) or nonlymphoid (muscle, VAT) tissues in our microarray studies.”
Self-citationArnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K., & Chazaud, B. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070075 · Cited by 2,002 · cited 2× · see citing works
“As anticipated (Arnold et al., 2007), there was a rapid increase in CD11b+Gr1 myeloid mononuclear cells beginning before day 1, initially a proinflammatory Ly6chi population but switching to an anti-inflammatory Ly6clo population by day 4 (Figure 1A, top).”
Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice
Kim, J. M., Rasmussen, J. P., & Rudensky, A. Y. (2006) · Nature Immunology · doi:10.1038/ni1428 · Cited by 1,827 · cited 4× · see citing works
“) starting from the time of im Ctx injection and were analyzed 1 week later, a time chosen to avoid the multiorgan autoimmunity provoked by long-term ablation of Treg cells (Kim et al., 2007).”
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× · see citing works
“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
Monticelli (2011) · PubMed · doi:10.1031/ni.2131 · Cited by 1,286 · see citing works
Brochet, X., Lefranc, M., & Giudicelli, V. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn316 · Cited by 1,220 · cited 1× · see citing works
“Raw sequencing files were filtered for sequence quality, processed in automated fashion, and parsed using IMGT/V-QUEST (Brochet et al., 2008).”
PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells
Cipolletta, D., Feuerer, M., Li, A., Kamei, N., Lee, J., Shoelson, S. E., Benoist, C., & Mathis, D. (2012) · Nature · doi:10.1038/nature11132 · Cited by 1,143 · cited 2× · see citing works
“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
Tidball, J. G., & Villalta, S. A. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00735.2009 · Cited by 1,105 · cited 4× · see citing works
“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).”
InfluentialSelective Stimulation of T Cell Subsets with Antibody-Cytokine Immune Complexes
Boyman, O., Kovář, M., Rubinstein, M., Surh, C., & Sprent, J. (2006) · Science · doi:10.1126/science.1122927 · Cited by 940 · cited 1× · see citing works
“For the gain-of-function experiments, we made use of the published observation that complexes of recombinant IL-2 and a particular anti-IL-2 mAb (clone JES6-1A12) can preferentially expand Treg populations after injection into mice (Boyman et al., 2006).”
Skeletal muscle stem cells express anti-apoptotic ErbB receptors during activation from quiescence.
Golding, J. P., Calderbank, E. F., Partridge, T. A., & Beauchamp, J. (2007) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.10.019 · Cited by 801 · cited 2× · see citing works
“Most relevant in the current context, previous studies have suggested that Areg might act directly on muscle cells (Golding et al., 2007; Andrechek et al., 2002).”
Hill, J., Feuerer, M., Tash, K., Haxhinasto, S., Perez, J., Melamed, R., Mathis, D., & Benoist, C. (2007) · Immunity · doi:10.1016/j.immuni.2007.09.010 · Cited by 671 · cited 4× · see citing works
“…population residing in nonlymphoid tissue, and dissimilarity to lymphoid-organ Treg cells, did not simply reflect a higher activation state in tissues, because few of the distinguishing transcripts were members of a previously determined Treg activation signature (Hill et al., 2007) (Figure 2C).”
InfluentialSelf-citationStructure and Function of Human Amphiregulin: A Member of the Epidermal Growth Factor Family
SHOYAB, M., Plowman, G. D., McDonald, V. L., Bradley, J. G., & Todaro, G. J. (1989) · Science · doi:10.1126/science.2466334 · Cited by 597 · cited 1× · see citing works
“Areg belongs to the epithelial growth factor (EGF) family and signals through the EGF receptor (EGFR) system (Shoyab et al., 1989).”
Highly Efficient, Functional Engraftment of Skeletal Muscle Stem Cells in Dystrophic Muscles
Cerletti, M., Jurga, S., Witczak, C. A., Hirshman, M. F., Shadrach, J. L., Goodyear, L. J., & Wagers, A. J. (2008) · Cell · doi:10.1016/j.cell.2008.05.049 · Cited by 472 · cited 3× · see citing works
“Clonal Myogenesis and Myogenic Differentiation Assays For the clonal assays, myofiber-associated cells were prepared from hind-limb muscles as described (Cerletti et al., 2008).”
Self-citationThe Epidermal Growth Factor Receptor System in Skin Repair and Inflammation
Pastore, S., Mascia, F., Mariani, V., & Girolomoni, G. (2007) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5701184 · Cited by 441 · cited 2× · see citing works
“, CCR1), and two well-known growth factors (platelet-derived growth factor [PDGF] and Amphiregulin [Areg]] (Pastore et al., 2008).”
Zaiss, D. M. W., van Loosdregt, J., Gorlani, A., Bekker, C. P. J., Gröne, A., Sibilia, M. C., Henegouwen, P. M. P. V. B. E., Roovers, R. C., Coffer, P. J., & Sijts, A. J. A. M. (2013) · Immunity · doi:10.1016/j.immuni.2012.09.023 · Cited by 418 · cited 1× · see citing works
“Interestingly, it was recently reported that Areg might also impact Treg cells directly and enhance their ability to suppress immune responses (Zaiss et al., 2013).”
Short-Term Calorie Restriction Enhances Skeletal Muscle Stem Cell Function
Cerletti, M., Jang, Y. C., Finley, L. W. S., Haigis, M. C., & Wagers, A. J. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.04.002 · Cited by 397 · cited 2× · see citing works
“, 2008), and their functionality was evaluated in clonal myogenesis assays, as described in (Cerletti et al., 2012) (Figure 4F).”
Self-citationCD4+CD25+ Regulatory T Cells Control the Severity of Viral Immunoinflammatory Lesions
Suvas, S., Azkur, A. K., Kim, B. S., Kumaraguru, U., & Rouse, B. T. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.7.4123 · Cited by 358 · see citing works
Complement C1q Activates Canonical Wnt Signaling and Promotes Aging-Related Phenotypes
Naito, A. T., Sumida, T., Nomura, S., Liu, M.-L., Higo, T., Nakagawa, A., Okada, K., Sakai, T., Hashimoto, A., Hara, Y., et al. (2012) · Cell · doi:10.1016/j.cell.2012.03.047 · Cited by 320 · cited 2× · see citing works
“However, in DTR mice, this drop did not occur or was greatly attenuated, again suggesting an ineffective and prolonged repair process, especially given the recent report that C1qa and related molecules strongly inhibit muscle regeneration (Naito et al., 2012).”
Vetrone, S., Montecino-Rodriguez, E., Kudryashova, E., Kramerova, I., Hoffman, E. P., Liu, S., Miceli, M., & Spencer, M. J. (2009) · Journal of Clinical Investigation · doi:10.1172/jci37662 · Cited by 297 · cited 2× · see citing works
“The genes encoding osteopontin (Spp1; 2.1-fold) and connective-tissue growth factor (Ctgf; 1.8-fold), both of which promote skeletal muscle fibrosis and mdx pathology (Morales et al., 2011; Vetrone et al., 2009), were upregulated in the absence of Tregs.”
InfluentialThe Molecular Regulation of Muscle Stem Cell FunctionPreprint
Rudnicki, M. A., Grand, F. L., McKinnell, I. W., & Kuang, S. (2008) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2008.73.064 · Cited by 261 · cited 1× · see citing works
“This series of events is controlled by the sequential activation and repression of specific transcription factors (Rudnicki et al., 2008).”
Beyer, M., Thabet, Y., Müller, R., Sadlon, T. J., Claßen, S., Lahl, K., Basu, S., Zhou, X., Bailey-Bucktrout, S. L., Krebs, W., et al. (2011) · Nature Immunology · doi:10.1038/ni.2084 · Cited by 212 · cited 1× · see citing works
“Included in the list of repressed genes is Satb1, which encodes a chromatin organizer that inhibits Treg suppressive activity (Beyer et al., 2011).”
Adaptation of TCR Repertoires to Self-Peptides in Regulatory and Nonregulatory CD4+ T Cells
Wong, J., Obst, R., Correia‐Neves, M., Losyev, G., Mathis, D. J., & Benoist, C. O. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.11.7032 · Cited by 183 · cited 1× · see citing works
“For RT-PCR analyses and single-cell TCR sequencing, published protocols (Wong et al., 2007; Baker et al., 2002) were followed with some modifications to the primer sets used.”
Self-citationDC ablation in mice: promises, pitfalls, and challenges
Bennett, C. L., & Clausen, B. E. (2007) · Trends in Immunology · doi:10.1016/j.it.2007.08.011 · Cited by 181 · cited 1× · see citing works
“DTR-mediated in vivo ablation of a designated cell population is known to be apoptotic and noninflammatory (Bennett and Clausen, 2007).”
Chemokine receptor CCR2 involvement in skeletal muscle regeneration
Warren, G. L., Hulderman, T., Mishra, D., Gao, X., Millecchia, L., O’Farrell, L., Kuziel, W. A., & Simeonova, P. P. (2004) · The FASEB Journal · doi:10.1096/fj.04-2421fje · Cited by 167 · cited 4× · see citing works
“…muscle include those encoding KLRG1, 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…”
InfluentialCipolletta, D., Kolodin, D., Benoist, C. O., & Mathis, D. J. (2011) · Seminars in Immunology · doi:10.1016/j.smim.2011.06.002 · Cited by 124 · cited 1× · see citing works
“Perhaps the best-characterized example is a unique population of Treg cells residing in the visceral adipose tissue (VAT) and regulating metabolic indices (Feuerer et al., 2009; Cipolletta et al., 2011).”
Self-citationErbB2 Is Required for Muscle Spindle and Myoblast Cell Survival
Andrechek, E. R., Hardy, W. R., Girgis-Gabardo, A., Perry, R. L., Butler, R., Graham, F. L., Kahn, R., Rudnicki, M. A., & Muller, W. J. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.13.4714-4722.2002 · Cited by 123 · cited 1× · see citing works
“Most relevant in the current context, previous studies have suggested that Areg might act directly on muscle cells (Golding et al., 2007; Andrechek et al., 2002).”
CTGF/CCN‐2 over‐expression can directly induce features of skeletal muscle dystrophy
Morales, M. G., Cabello‐Verrugio, C., Santander, C., Cabrera, D., Goldschmeding, R., & Brandan, E. (2011) · The Journal of Pathology · doi:10.1002/path.2952 · Cited by 107 · cited 2× · see citing works
“The genes encoding osteopontin (Spp1; 2.1-fold) and connective-tissue growth factor (Ctgf; 1.8-fold), both of which promote skeletal muscle fibrosis and mdx pathology (Morales et al., 2011; Vetrone et al., 2009), were upregulated in the absence of Tregs.”
InfluentialShao, J., & Sheng, H. (2010) · Endocrinology · doi:10.1210/en.2010-0319 · Cited by 87 · cited 1× · see citing works
“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).”
Bosurgi, L., Manfredi, A., & Rovere-Querini, P. (2011) · Front. Immun. · doi:10.3389/fimmu.2011.00062 · Cited by 80 · cited 2× · see citing works
“In vitro experiments have shown that macrophages can directly influence muscle progenitors (Bosurgi et al., 2011); it is possible, then, that Treg cells act on satellite”
Skeletal Muscle Degenerative Diseases and Strategies for Therapeutic Muscle Repair
Tabebordbar, M., Wang, E. T., & Wagers, A. J. (2013) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-011811-132450 · Cited by 79 · cited 4× · see citing works
“It is driven largely by satellite cells, a pool of quiescent precursors closely associated with muscle fibers (Tabebordbar et al., 2013).”
InfluentialSelf-citationRestricted islet-cell reactive T cell repertoire of early pancreatic islet infiltrates in NOD mice
Baker, F. J., Lee, M., Chien, Y., & Davis, M. M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.142284899 · Cited by 75 · cited 1× · see citing works
“For RT-PCR analyses and single-cell TCR sequencing, published protocols (Wong et al., 2007; Baker et al., 2002) were followed with some modifications to the primer sets used.”
Horikawa, M., Higashiyama, S., Nomura, S., Kitamura, Y., Ishikawa, M., & Taniguchi, N. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)01213-2 · Cited by 44 · cited 1× · see citing works
“EGFR is expressed by a variety of cells, including muscle satellite cells and a myoblast cell line, in which it appears to have antiapoptotic/survival functions (Golding et al., 2007; Horikawa et al., 1999).”
Kohlhapp, F. J., & Zloza, A. (2014) · Springer eBooks · doi:10.1007/978-1-4614-6613-0_139-1 · Cited by 35 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Control of adaptive immunity by the innate immune system
Iwasaki, A., & Medzhitov, R. (2015) · Nature Immunology · doi:10.1038/ni.3123 · Cited by 2,160 · see citing works
Pathophysiology of Inflammatory Bowel Diseases
Chang, J. T. (2020) · New England Journal of Medicine · doi:10.1056/nejmra2002697 · Cited by 1,295 · see citing works
The far-reaching scope of neuroinflammation after traumatic brain injury
Simon, D. W., McGeachy, M. J., Bayır, H., Clark, R. S. B., Loane, D. J., & Kochanek, P. M. (2017) · Nature Reviews Neurology · doi:10.1038/nrneurol.2017.13 · Cited by 1,190 · see citing works
Interleukin-33 in health and disease
Liew, F. Y., Girard, J., & Turnquist, H. R. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.95 · Cited by 1,157 · see citing works
Regulatory T Cells and Human Disease
Sakaguchi, S., Mikami, N., Wing, J. B., Tanaka, A., Ichiyama, K., & Ohkura, N. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042718-041717 · Cited by 1,132 · see citing works
A Distinct Function of Regulatory T Cells in Tissue Protection
Arpaia, N., Green, J. A., Moltedo, B., Arvey, A., Hemmers, S., Yuan, S., Treuting, P. M., & Rudensky, A. Y. (2015) · Cell · doi:10.1016/j.cell.2015.08.021 · Cited by 991 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition)
Cossarizza, A., Chang, H., Radbruch, A., Acs, A., Adam, D., Adam‐Klages, S., Agace, W. W., Aghaeepour, N., Akdiş, M., Allez, M., et al. (2019) · European Journal of Immunology · doi:10.1002/eji.201970107 · Cited by 982 · see citing works
Individual intestinal symbionts induce a distinct population of RORγ <sup>+</sup> regulatory T cells
Sefik, E., Geva-Zatorsky, N., Oh, S., Konnikova, L., Zemmour, D., McGuire, A. M., Burzyn, D., Ortiz-Lopez, A., Lobera, M., Yang, J., et al. (2015) · Science · doi:10.1126/science.aaa9420 · Cited by 879 · see citing works
Self-citationMuscle damage and inflammation during recovery from exercise
Peake, J. M., Neubauer, O., Gatta, P. A. D., & Nosaka, K. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00971.2016 · Cited by 829 · see citing works
Promoting tissue regeneration by modulating the immune system
Julier, Z., Park, A. J., Briquez, P. S., & Martino, M. M. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.01.056 · Cited by 766 · see citing works
De Simone, M., Arrigoni, A., Rossetti, G., Gruarin, P., Ranzani, V., Politano, C., Bonnal, R. J. P., Provasi, E., Sarnicola, M. L., Panzeri, I., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.10.021 · Cited by 687 · see citing works
“…transcriptional signatures, because they can display functions beyond their well-established suppressive roles, such as metabolic modulation in adipose tissue (Cipolletta et al., 2012) or regulation of tissue repair in skeletal muscle (Burzyn et al., 2013) and in lung tissue (Arpaia et al., 2015).”
Regulation of Muscle Growth and Regeneration by the Immune System
Tidball, J. G. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.150 · Cited by 740 · see citing works
Macrophages in inflammation, repair and regeneration
Oishi, Y., & Manabe, I. (2018) · International Immunology · doi:10.1093/intimm/dxy054 · Cited by 645 · see citing works
Treg cell-based therapies: challenges and perspectives
Raffin, C., Vo, L. T., & Bluestone, J. A. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0232-6 · Cited by 728 · see citing works
Human FOXP3+ Regulatory T Cell Heterogeneity and Function in Autoimmunity and Cancer
Wing, J. B., Tanaka, A., & Sakaguchi, S. (2019) · Immunity · doi:10.1016/j.immuni.2019.01.020 · Cited by 726 · see citing works
Brain regulatory T cells suppress astrogliosis and potentiate neurological recovery
Ito, M., Komai, K., Mise-Omata, S., Iizuka-Koga, M., Noguchi, Y., Kondo, T., Sakai, R., Matsuo, K., Nakayama, T., Yoshie, O., et al. (2019) · Nature · doi:10.1038/s41586-018-0824-5 · Cited by 784 · see citing works
Regulatory T cells in autoimmune disease
Dominguez-Villar, M., & Hafler, D. A. (2018) · Nature Immunology · doi:10.1038/s41590-018-0120-4 · Cited by 713 · see citing works
Biomaterials: Foreign Bodies or Tuners for the Immune Response?
Mariani, E., Lisignoli, G., Borzì, R. M., & Pulsatelli, L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030636 · Cited by 706 · see citing works
Weirather, J., Hofmann, U., Beyersdorf, N., Ramos, G. C., Vogel, B., Frey, A., Ertl, G., Kerkau, T., & Frantz, S. (2014) · Circulation Research · doi:10.1161/circresaha.115.303895 · Cited by 705 · see citing works
Regulatory T Cells in Skin Facilitate Epithelial Stem Cell Differentiation
Ali, N., Zirak, B., Rodriguez, R. S., Pauli, M. L., Truong, H.-A., Lai, K., Ahn, R., Corbin, K., Lowe, M. M., Scharschmidt, T. C., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.002 · Cited by 680 · see citing works
“…would be preferentially expressed in skin Tregs when compared to Tregs found in SDLNs. Consistent with heightened activation of Tregs in tissues (Burzyn et al., 2013; Feuerer et al., 2009; Sanchez Rodriguez et al., 2014), differential expression analyses revealed increased abundance of genes…”
InfluentialCD36-mediated metabolic adaptation supports regulatory T cell survival and function in tumors
Wang, H., Franco, F., Tsui, Y.-C., Xie, X., Trefny, M. P., Zappasodi, R., Mohmood, S. R., Fernández-García, J., Tsai, C.-H., Schulze, I., et al. (2020) · Nature Immunology · doi:10.1038/s41590-019-0589-5 · Cited by 680 · see citing works
The multifaceted role of CD4+ T cells in CD8+ T cell memory
Laidlaw, B. J., Craft, J. E., & Kaech, S. M. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2015.10 · Cited by 657 · see citing works
AAV Vector Immunogenicity in Humans: A Long Journey to Successful Gene Transfer
Costa Verdera, H., Kuranda, K., & Mingozzi, F. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2019.12.010 · Cited by 641 · see citing works
Emerging Functions of Amphiregulin in Orchestrating Immunity, Inflammation, and Tissue Repair
Zaiss, D. M. W., Gause, W. C., Osborne, L. C., & Artis, D. (2015) · Immunity · doi:10.1016/j.immuni.2015.01.020 · Cited by 639 · see citing works
Interleukin-33 in tissue homeostasis, injury, and inflammation
Molofsky, A. B., Savage, A. K., & Locksley, R. M. (2015) · Immunity · doi:10.1016/j.immuni.2015.06.006 · Cited by 638 · see citing works
“, 2015) and in models of muscle damage (Burzyn et al., 2013), suggesting that damageinduced IL-33 might participate in these responses.”
InfluentialThe regulation of immune tolerance by FOXP3
Lu, L., Barbi, J., & Pan, F. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.75 · Cited by 580 · see citing works
T Helper Cell Cytokines Modulate Intestinal Stem Cell Renewal and Differentiation
Biton, M., Haber, A. L., Rogel, N., Burgin, G., Beyaz, S., Schnell, A., Ashenberg, O., Su, C., Smillie, C. S., Shekhar, K., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.008 · Cited by 580 · see citing works
“Among adaptive immune cells, recent studies have implicated T regulatory cells (Tregs) in tissue regeneration processes in the muscles and lungs (Arpaia et al., 2015; Burzyn et al., 2013), and T cytotoxic cells were shown to eliminate Lgr5+ ISCs via MHC class I (Agudo et al.”
Preparing the ground for tissue regeneration: from mechanism to therapy
Forbes, S. J., & Rosenthal, N. A. (2014) · Nature Medicine · doi:10.1038/nm.3653 · Cited by 585 · see citing works
A wave of regulatory T cells into neonatal skin mediates tolerance to commensal microbes
Scharschmidt, T. C., Vasquez, K. S., Truong, H.-A., Gearty, S. V., Pauli, M. L., Nosbaum, A., Gratz, I. K., Otto, M., Moon, J. J., Liese, J., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.10.016 · Cited by 586 · see citing works
“, 1959), where they stably reside (Burzyn et al., 2013; Cipolletta et al., 2012; Sanchez Rodriguez et al., 2014).”
Autoimmunity and organ damage in systemic lupus erythematosus
Tsokos, G. C. (2020) · Nature Immunology · doi:10.1038/s41590-020-0677-6 · Cited by 589 · see citing works
Regulatory T cells promote myelin regeneration in the central nervous system
Dombrowski, Y., O'Hagan, T., Dittmer, M., Penalva, R., Mayoral, S. R., Bankhead, P., Fleville, S., Eleftheriadis, G., Zhao, C., Naughton, M., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4528 · Cited by 533 · see citing works
Immunological landscape and immunotherapy of hepatocellular carcinoma
Prìeto, J., Melero, I., & Sangro, B. (2015) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2015.173 · Cited by 564 · see citing works
Panduro, M., Benoist, C., & Mathis, D. (2016) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095948 · Cited by 536 · see citing works
“For example, VAT Tregs produce large amounts of IL-10, and this cytokine has a strong in situ impact on their profile of gene expression (27), whereas colonic RORγt+Helioslo/− and pancreas Tregs display little if any IL-10 receptor (75).”
BackgroundInfluentialSelf-citationSano, T., Huang, W., Hall, J. A., Yang, Y., Chen, A., Gavzy, S. J., Lee, J.-Y., Ziel, J. W., Miraldi, E. R., Domingos, A. I., et al. (2015) · Cell · doi:10.1016/j.cell.2015.08.061 · Cited by 547 · see citing works
“Recent studies have shown that the tissue microenvironment confers distinct transcriptional and functional properties to otherwise similar lymphoid and myeloid cells (Burzyn et al., 2013; Cipolletta et al., 2012; Lavin et al., 2014; Lewis et al., 2011).”
Single-Cell Transcriptomics of Regulatory T Cells Reveals Trajectories of Tissue Adaptation
Miragaia, R. J., Gomes, T., Chomka, A., Jardine, L., Riedel, A., Hegazy, A. N., Whibley, N., Tucci, A., Chen, X., Lindeman, I., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.01.001 · Cited by 499 · see citing works
Monticelli, L. A., Osborne, L. C., Noti, M., Tran, S. V., Zaiss, D. M. W., & Artis, D. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1509070112 · Cited by 534 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531 · see citing works
Kuswanto, W. F., Burzyn, D., Panduro, M., Wang, K. K., Jang, Y. C., Wagers, A. J., Benoist, C. O., & Mathis, D. J. (2016) · Immunity · doi:10.1016/j.immuni.2016.01.009 · Cited by 509 · see citing works
“The ‘‘muscle homeostasis/function’’ and ‘‘muscle repair/regeneration’’ signatures were developed and validated in Burzyn et al. (2013), as were the Areg ‘‘up’’ and ‘‘down’’ signatures.”
InfluentialSelf-citationInnate lymphoid cells in the initiation, regulation and resolution of inflammation
Sonnenberg, G. F., & Artis, D. (2015) · Nature Medicine · doi:10.1038/nm.3892 · Cited by 503 · see citing works
Tissue-specific contribution of macrophages to wound healing
Minutti, C. M., Knipper, J. A., Allen, J. E., & Zaiss, D. M. W. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.08.006 · Cited by 472 · see citing works
“Amphiregulin can induce the differentiation of tissue precursor cells within wounds [67].”
BackgroundControl of satellite cell function in muscle regeneration and its disruption in ageing
Sousa-Victor, P., García-Prat, L., & Muñoz-Cánoves, P. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00421-2 · Cited by 476 · see citing works
Principles of regulatory T cell function
Dikiy, S., & Rudensky, A. Y. (2023) · Immunity · doi:10.1016/j.immuni.2023.01.004 · Cited by 450 · see citing works
Regulatory T cells generated early in life play a distinct role in maintaining self-tolerance
Yang, S., Fujikado, N., Kolodin, D., Benoist, C. O., & Mathis, D. J. (2015) · Science · doi:10.1126/science.aaa7017 · Cited by 444 · see citing works
“amplification and microarray hybridization were done as previously described (35, 36).”
MethodSelf-citationSkeletal Muscle as Potential Central Link between Sarcopenia and Immune Senescence
Nelke, C., Dziewas, R., Minnerup, J., Meuth, S. G., & Ruck, T. (2019) · eBioMedicine · doi:10.1016/j.ebiom.2019.10.034 · Cited by 437 · see citing works
“In part, reg and satellite cell interaction is mediated by amphiregulin, a rowth factor directly acting on satellite cells [61] .”
BackgroundMolofsky, A. B., Gool, F. V., Liang, H.-E., Dyken, S. J. V., Nussbaum, J. C., Lee, J., Bluestone, J. A., & Locksley, R. M. (2015) · Immunity · doi:10.1016/j.immuni.2015.05.019 · Cited by 433 · see citing works
“Increasingly, studies of these pathways have uncovered interactions with basal metabolism, mucosal homeostasis, and tissue repair (Burzyn et al., 2013b; 2013a; Cipolletta et al., 2012; Heredia et al., 2013; Molofsky et al., 2013; Qiu et al., 2014; Schiering et al., 2014; Wu et al., 2011).”
BackgroundHomeostatic control of regulatory T cell diversity
Liston, A., & Gray, D. H. D. (2014) · Nature reviews. Immunology · doi:10.1038/nri3605 · Cited by 428 · see citing works
Cutting Edge: Regulatory T Cells Facilitate Cutaneous Wound Healing
Nosbaum, A., Prevel, N., Truong, H.-A., Mehta, P., Ettinger, M., Scharschmidt, T. C., Ali, N. H., Pauli, M. L., Abbas, A. K., & Rosenblum, M. D. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502139 · Cited by 418 · see citing works
“The EGFR ligand, AREG, is expressed by Tregs, where it enhances muscle and lung tissue repair after injury (4, 5).”
BackgroundSingle-cell gene expression reveals a landscape of regulatory T cell phenotypes shaped by the TCR
Zemmour, D., Zilionis, R., Kiner, E., Klein, A. M., Mathis, D., & Benoist, C. (2018) · Nature Immunology · doi:10.1038/s41590-018-0051-0 · Cited by 384 · see citing works
Self-citationTreg Heterogeneity, Function, and Homeostasis
Shevyrev, D., & Tereshchenko, V. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.03100 · Cited by 404 · see citing works
“The mechanisms of action may vary from tissue to tissue and include: amphiregulin (a growth factor) production, promotion of proliferation and differentiation of stem cells of different tissues, inhibition of neutrophil extravasation and monocyte activity and also the limitation of osteoclastogenesis (93, 94).”
BackgroundDisease tolerance and immunity in host protection against infection
Soares, M. P., Teixeira, L., & Moita, L. F. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2016.136 · Cited by 376 · see citing works
Bao, H., Cao, J., Chen, M., Min, C., Chen, W., Chen, X., Chen, Y., Chen, Y., Chen, Y., Chen, Z., et al. (2023) · Science China Life Sciences · doi:10.1007/s11427-023-2305-0 · Cited by 389 · see citing works
Regulatory T cells in allergic diseases
Rivas, M. N., & Chatila, T. A. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2016.06.003 · Cited by 378 · see citing works
IL-17-producing γδ T cells enhance bone regeneration
Ono, T., Okamoto, K., Nakashima, T., Nitta, T., Hori, S., Iwakura, Y., & Takayanagi, H. (2016) · Nature Communications · doi:10.1038/ncomms10928 · Cited by 371 · see citing works
Kolodin, D., van Panhuys, N., Li, C., Magnuson, A. M., Cipolletta, D., Miller, C. M., Wagers, A., Germain, R. N., Benoist, C., & Mathis, D. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.03.005 · Cited by 365 · see citing works
“For both TCR chains, LN Tregs showed few CDR3 repeats (Figure 3D, left pies); the slight increase over the near-zero we previously reported (Feuerer et al., 2009; Burzyn et al., 2013) most likely reflects the advanced age of the mice in our current study.”
Self-citationChronic Adaptations to Eccentric Training: A Systematic Review
Douglas, J. M., Pearson, S. N., Ross, A., & McGuigan, M. R. (2016) · Sports Medicine · doi:10.1007/s40279-016-0628-4 · Cited by 385 · see citing works
“IP-10 within skeletal muscle is postulated to recruit T lymphocytes [87, 88], and T-cell infiltration has been found to enhance satellite cell activation and muscle regeneration in mice [89].”
BackgroundIntricacies of TGF-β signaling in Treg and Th17 cell biology
Wang, J., Zhao, X., & Wan, Y. Y. (2023) · Cellular and Molecular Immunology · doi:10.1038/s41423-023-01036-7 · Cited by 377 · see citing works
Hallmarks of Tissue-Resident Lymphocytes
Fan, X., & Rudensky, A. Y. (2016) · Cell · doi:10.1016/j.cell.2016.02.048 · Cited by 352 · see citing works
“Tissue Treg cells are an important source of Areg (Burzyn et al., 2013), and mice in which Treg cells lack Areg exhibit impaired pulmonary function and exacerbated tissue pathology during influenza infection (Arpaia et al.”
BackgroundInfluentialOhkura, N., & Sakaguchi, S. (2020) · Cell Research · doi:10.1038/s41422-020-0324-7 · Cited by 356 · see citing works
A Muscle Stem Cell Support Group: Coordinated Cellular Responses in Muscle Regeneration
Wosczyna, M. N., & Rando, T. A. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.06.018 · Cited by 353 · see citing works
Regulatory T-Cells: Potential Regulator of Tissue Repair and Regeneration
Li, J., Tan, J. L., Martino, M. M., & Lui, K. O. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00585 · Cited by 345 · see citing works
“Overall, studies investigating the role of Treg during tissue regeneration have been largely based on the use of Foxp3DTR mouse model (17, 18, 22, 25, 57, 77, 90).”
BackgroundMethodInfluentialPrinciples and therapeutic applications of adaptive immunity
Chi, H., Pepper, M., & Thomas, P. G. (2024) · Cell · doi:10.1016/j.cell.2024.03.037 · Cited by 363 · see citing works
Skeletal muscle regeneration is modulated by inflammation
Yang, W.-J., & Hu, P. (2018) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2018.01.002 · Cited by 303 · see citing works
“The number of Tregs is low at the early stage of muscle regeneration [68], while the number increases dramatically at the late stage of muscle regeneration accompanied with the decrease of cell number of other subtypes of T cells [80].”
BackgroundInfluentialT Cells in Fibrosis and Fibrotic Diseases
Zhang, M., & Zhang, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01142 · Cited by 333 · see citing works
Tissue Stem Cells: Architects of Their Niches
Fuchs, E., & Blau, H. M. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.09.011 · Cited by 332 · see citing works
“Since the stem cells are responsible for the reparative phase of the response, there must be intricate immune-stem cell communication to ensure not only that the pathogen invasion is under control, but also that the inflammation is subsequently dampened in order to facilitate repair (Arnold et al., 2007; Burzyn et al.…”
BackgroundInfluentialSavage, P. A., Klawon, D. E. J., & Miller, C. H. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-100219-020937 · Cited by 321 · see citing works
The cAMP Pathway as Therapeutic Target in Autoimmune and Inflammatory Diseases
Raker, V., Becker, C., & Steinbrink, K. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00123 · Cited by 321 · see citing works
“Muscle Treg distinctly express the growth factor amphiregulin, which improves muscle repair by directly acting on muscle satellite cells (114).”
BackgroundMolecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease
Almada, A. E., & Wagers, A. J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.7 · Cited by 314 · see citing works
Self-citationCahill, T. J., Choudhury, R. P., & Riley, P. R. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.106 · Cited by 309 · see citing works
Immune Modulation of Stem Cells and Regeneration
Aurora, A., & Olson, E. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.06.009 · Cited by 293 · see citing works
Immune-mediated pathology in Duchenne muscular dystrophy
Rosenberg, A. S., Puig, M., Nagaraju, K., Hoffman, E. P., Villalta, S. A., Rao, V. A., Wakefield, L. M., & Woodcock, J. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa7322 · Cited by 306 · see citing works
Thome, J. J. C., Bickham, K. L., Ohmura, Y., Kubota, M., Matsuoka, N., Gordon, C., Granot, T., Griesemer, A., Lerner, H., Kato, T., et al. (2016) · Nature Medicine · doi:10.1038/nm.4008 · Cited by 305 · see citing works
Tim-3: An Emerging Target in the Cancer Immunotherapy Landscape
Anderson, A. C. (2014) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-14-0039 · Cited by 302 · see citing works
“For example, adipose tissue Tregs express the transcription regulator PPAR-g and regulate metabolism (22), and the Tregs that accumulate in muscle tissue after muscle injury express amphiregulin, which mediates repair of damaged tissue (23).”
BackgroundExercise‐induced muscle damage: What is it, what causes it and what are the nutritional solutions?
Owens, D. J., Twist, C., Cobley, J. N., Howatson, G., & Close, G. L. (2018) · European Journal of Sport Science · doi:10.1080/17461391.2018.1505957 · Cited by 309 · see citing works
“…of immune cell types infiltrate the damaged tissue, including mast cells, neutrophils, T regulatory lymphocytes, eosinophils and CD8 T lymphocytes (Burzyn et al., 2013; Castiglioni et al., 2015; Cote, Tremblay, Duchesne, & Lapoite, 2008; Heredia et al., 2013; Zhang et al., 2014) to carry out…”
BackgroundRegulatory T cells in the treatment of disease
Sharabi, A., Tsokos, M., Ding, Y., Malek, T. R., Klatzmann, D., & Tsokos, G. C. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.148 · Cited by 297 · see citing works
Tissue regulatory T cells: regulatory chameleons
Muñoz-Rojas, A. R., & Mathis, D. (2021) · Nature Reviews Immunology · doi:10.1038/s41577-021-00519-w · Cited by 281 · see citing works
Self-citationChronic Critical Illness and the Persistent Inflammation, Immunosuppression, and Catabolism Syndrome
Hawkins, R. B., Raymond, S. L., Stortz, J. A., Horiguchi, H., Brakenridge, S. C., Gardner, A. K., Efron, P. A., Bihorac, A., Segal, M. S., Moore, F. A., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01511 · Cited by 293 · see citing works
The Mechanisms of T Cell Selection in the Thymus
Takaba, H., & Takayanagi, H. (2017) · Trends in Immunology · doi:10.1016/j.it.2017.07.010 · Cited by 292 · see citing works
Temporal Dynamics and Heterogeneity of Cell Populations during Skeletal Muscle Regeneration
Oprescu, S. N., Yue, F., Qiu, J., Brito, L. F., & Kuang, S. (2020) · iScience · doi:10.1016/j.isci.2020.100993 · Cited by 288 · see citing works
“…production of oncostatin M, underscoring the interdependence of various cellular responses (Christov et al., 2007; Latroche et al., 2017; Arnold et al., 2007; Burzyn et al., 2013; Hardy et al., 2016; Heredia et al., 2013; Joe et al., 2010; Segawa et al., 2008; Tidball and Wehling-Henricks, 2007).”
BackgroundDelacher, M., Imbusch, C. D., Hotz-Wagenblatt, A., Mallm, J.-P., Bauer, K., Simon, M., Riegel, D., Rendeiro, A. F., Bittner, S., Sanderink, L., et al. (2020) · Immunity · doi:10.1016/j.immuni.2019.12.002 · Cited by 261 · see citing works
Genome-wide DNA-methylation landscape defines specialization of regulatory T cells in tissues
Delacher, M., Imbusch, C. D., Weichenhan, D., Breiling, A., Hotz-Wagenblatt, A., Träger, U., Hofer, A.-C., Kägebein, D., Wang, Q., Frauhammer, F., et al. (2017) · Nature Immunology · doi:10.1038/ni.3799 · Cited by 282 · see citing works
Metabolic control of regulatory T cell development and function
Zeng, H., & Chi, H. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.08.003 · Cited by 275 · see citing works
Function of a Foxp3 cis -Element in Protecting Regulatory T Cell Identity
Li, X., Liang, Y., Leblanc, M., Benner, C. W., & Zheng, Y. (2014) · Cell · doi:10.1016/j.cell.2014.07.030 · Cited by 268 · see citing works
Beyond Host Defense: Emerging Functions of the Immune System in Regulating Complex Tissue Physiology
Rankin, L. C., & Artis, D. (2018) · Cell · doi:10.1016/j.cell.2018.03.013 · Cited by 271 · see citing works
Immune Cells and Immunotherapy for Cardiac Injury and Repair
Rurik, J. G., Aghajanian, H. K., & Epstein, J. A. (2021) · Circulation Research · doi:10.1161/circresaha.121.318005 · Cited by 270 · see citing works
Impaired Epidermal to Dendritic T Cell Signaling Slows Wound Repair in Aged Skin
Keyes, B. E., Liu, S., Asare, A., Naik, S., Levorse, J., Polak, L., Lu, C. P., Nikolova, M., Pasolli, H. A., & Fuchs, E. (2016) · Cell · doi:10.1016/j.cell.2016.10.052 · Cited by 266 · see citing works
Zebrafish Regulatory T Cells Mediate Organ-Specific Regenerative Programs
Hui, S. P., Sheng, D. Z., Sugimoto, K., González-Rajal, Á., Nakagawa, S., Hesselson, D., & Kikuchi, K. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.11.010 · Cited by 269 · see citing works
Allen, J. E., & Sutherland, T. E. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.06.003 · Cited by 260 · see citing works
Emerging Functions of Regulatory T Cells in Tissue Homeostasis
Sharma, A., & Rudra, D. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00883 · Cited by 263 · see citing works
Scharschmidt, T. C., Vasquez, K. S., Pauli, M. L., Leitner, E. G., Chu, K., Truong, H.-A., Lowe, M. M., Sanchez Rodriguez, R., Ali, N., Laszik, Z. G., et al. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.03.001 · Cited by 258 · see citing works
“Treg cells in barrier tissues, such as the skin and the intestine, are known to play an important role in promoting tolerance to commensal-derived antigens (Burzyn et al., 2013a; Scharschmidt et al., 2015).”
BackgroundMacroscale biomaterials strategies for local immunomodulation
Dellacherie, M. O., Seo, B. R., & Mooney, D. J. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0106-3 · Cited by 259 · see citing works
Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy
Villalta, S. A., Rosenthal, W. L., Martinez, L., Kaur, A., Sparwasser, T. D., Tidball, J. G., Margeta, M., Spencer, M. J., & Bluestone, J. A. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009925 · Cited by 253 · see citing works
“In summary, our studies and those reported recently by other investigators (26) reveal the therapeutic potential of targeting Tregs in muscular dystrophy and other muscle disorders.”
BackgroundResultInfluentialHBEGF+ macrophages in rheumatoid arthritis induce fibroblast invasiveness
Kuo, D., Ding, J., Cohn, I., Zhang, F., Wei, K., Rao, D. A., Rozo, C., Sokhi, U. K., Shanaj, S., Oliver, D., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aau8587 · Cited by 231 · see citing works
“” Although leukocytederived growth factors have emerged as critical components in tissue homeostasis and repair (1, 59), our data uncovered a pathologic correlate.”
BackgroundT Regulatory Cells and Priming the Suppressive Tumor Microenvironment
Paluskievicz, C., Cao, X., Abdi, R., Zheng, P., Liu, Y., & Bromberg, J. S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02453 · Cited by 252 · see citing works
“For example, skeletal muscle Treg home to injured muscle in acute and chronic injury, and repair myocytes through a series of events including activation, proliferation, differentiation, migration, and formation of myofibers (143).”
BackgroundBilski, J., Pierzchalski, P., Szczepanik, M., Bonior, J., & Zoladz, J. A. (2022) · Cells · doi:10.3390/cells11010160 · Cited by 262 · see citing works
“Proper regeneration of skeletal muscle requires local expansion of a particular population of CD4+ CD25+ Foxp3+ regulatory T (Treg) cells [106], which is depleted in older mice [107].”
BackgroundTwo to Tango: Dialog between Immunity and Stem Cells in Health and Disease
Naik, S., Larsen, S. B., Cowley, C. J., & Fuchs, E. V. (2018) · Cell · doi:10.1016/j.cell.2018.08.071 · Cited by 249 · see citing works
Sawant, D. V., & Vignali, D. A. A. (2014) · Immunological Reviews · doi:10.1111/imr.12173 · Cited by 248 · see citing works
“Muscle-resident Tregs exhibit a distinct transcriptional profile characterized by expression of the antiinflammatory cytokine IL-10, chemokine receptor CCR1, and growth factors, namely, platederived growth factor (PDGF) and amphiregulin (Areg), that likely aid in their healing and regenerative capabilities (18).”
BackgroundHirata, Y., Furuhashi, K., Ishii, H., Li, H. W., Pinho, S., Ding, L., Robson, S. C., Frenette, P. S., & Fujisaki, J. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.01.017 · Cited by 249 · see citing works
“For example, specific subsets of Tregs in the visceral adipose tissue control glucose tolerance and insulin resistance (Cipolletta et al., 2012; Bapat et al., 2015), muscle Tregs potentiate muscle repair (Burzyn et al., 2013), and lung Tregs prevent tissue damage (Arpaia et al., 2015).”
BackgroundInfluentialCD4 T-Cell Subsets and the Pathophysiology of Inflammatory Bowel Disease
Gómez-Bris, R., Saéz, Á., Herrero‐Fernández, B., Rius, C., Sánchez-Martinez, H., & González, J. M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032696 · Cited by 255 · see citing works
Fibro–Adipogenic Progenitors Cross-Talk in Skeletal Muscle: The Social Network
Biferali, B., Proietti, D., Mozzetta, C., & Madaro, L. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01074 · Cited by 244 · see citing works
“As previously demonstrated, Treg cells promote muscle repair, accumulating in both acutely and chronically injured skeletal muscles (Burzyn et al., 2013; Castiglioni et al., 2015; Panduro et al., 2018).”
TIM-3 as a Target for Cancer Immunotherapy and Mechanisms of Action
Du, W., Yang, M., Turner, A., Xu, C., Ferris, R. L., Huang, J., Kane, L., & Lu, B. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18030645 · Cited by 237 · see citing works
- 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 › Rehabilitation › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
