The gut microbiota promotes distal tissue regeneration via RORγ+ regulatory T cell emissaries
Open accessAbstract
Specific microbial signals induce the differentiation of a distinct pool of RORγ+ regulatory T (Treg) cells crucial for intestinal homeostasis. We discovered highly analogous populations of microbiota-dependent Treg cells that promoted tissue regeneration at extra-gut sites, notably acutely injured skeletal muscle and fatty liver. Inflammatory meditators elicited by tissue damage combined with MHC-class-II-dependent T cell activation to drive the accumulation of gut-derived RORγ+ Treg cells in injured muscle, wherein they regulated the dynamics and tenor of early inflammation and helped balance the proliferation vs. differentiation of local stem cells. Reining in IL-17A-producing T cells was a major mechanism underlying the rheostatic functions of RORγ+ Treg cells in compromised tissues. Our findings highlight the importance of gut-trained Treg cell emissaries in controlling the response to sterile injury of non-mucosal tissues.
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 gut microbiome regulates the activity of RORγ+ Treg cells, and dysregulation of these cells can lead to diseases such as colitis, food allergy, and colon cancer.
“In addition, the gut microbiome regulates the activity of retinoic acid receptor-related orphan receptor gamma-positive (RORγ+) Treg cells, dysregulation of which can lead to diseases such as colitis, food allergy, and colon cancer.622,701–704”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [704]
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
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458 · see citing works
Integrated analysis of multimodal single-cell data
Hao, Y., Hao, S., Andersen-Nissen, E., Mauck, W. M., Zheng, S., Butler, A., Lee, M. J., Wilk, A. J., Darby, C., Zagar, M., et al. (2020) · doi:10.1101/2020.10.12.335331 · Cited by 15,508 · see citing works
Metascape provides a biologist-oriented resource for the analysis of systems-level datasets
Zhou, Y., Zhou, B., Pache, L., Chang, M., Khodabakhshi, A. H., Tanaseichuk, O., Benner, C., & Chanda, S. K. (2019) · Nature Communications · doi:10.1038/s41467-019-09234-6 · Cited by 14,611 · see citing works
Integrating single-cell transcriptomic data across different conditions, technologies, and species
Butler, A., Hoffman, P., Smibert, P., Papalexi, E., & Satija, R. (2018) · Nature Biotechnology · doi:10.1038/nbt.4096 · Cited by 13,174 · see citing works
Trapnell, C., Roberts, A., Goff, L. A., Pertea, G. M., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., & Pachter, L. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.016 · Cited by 11,930 · see citing works
Enrichr: a comprehensive gene set enrichment analysis web server 2016 update
Kuleshov, M. V., Jones, M. R., Rouillard, A. D., Fernandez, N. F., Duan, Q., Wang, Z., Koplev, S., Jenkins, S. L., Jagodnik, K. M., Lachmann, A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw377 · Cited by 10,799 · see citing works
Fast, sensitive and accurate integration of single-cell data with Harmony
Korsunsky, I., Millard, N., Fan, J., Slowikowski, K., Zhang, F., Wei, K., Baglaenko, Y., Brenner, M., Loh, P.-R., & Raychaudhuri, S. (2019) · Nature Methods · doi:10.1038/s41592-019-0619-0 · Cited by 10,488 · see citing works
SCANPY: large-scale single-cell gene expression data analysis
Wolf, F. A., Angerer, P., & Theis, F. J. (2018) · Genome Biology · doi:10.1186/s13059-017-1382-0 · Cited by 8,881 · see citing works
Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L., & Kuchroo, V. K. (2006) · Nature · doi:10.1038/nature04753 · Cited by 6,992 · see citing works
Induction of Intestinal Th17 Cells by Segmented Filamentous Bacteria
Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., et al. (2009) · Cell · doi:10.1016/j.cell.2009.09.033 · Cited by 4,554 · see citing works
An Immunomodulatory Molecule of Symbiotic Bacteria Directs Maturation of the Host Immune System
Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., & Kasper, D. L. (2005) · Cell · doi:10.1016/j.cell.2005.05.007 · Cited by 2,910 · see citing works
Feuerer, 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 · see citing works
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 · see citing works
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 · see citing works
Regulatory T Cell-Derived Interleukin-10 Limits Inflammation at Environmental Interfaces
Rubtsov, Y. P., Rasmussen, J. P., Chi, E. Y., Fontenot, J., Castelli, L., Ye, X., Treuting, P., Siewe, L., Roers, A., Henderson, W. R., et al. (2008) · Immunity · doi:10.1016/j.immuni.2008.02.017 · Cited by 1,586 · see citing works
Gut-Residing Segmented Filamentous Bacteria Drive Autoimmune Arthritis via T Helper 17 Cells
Wu, H.-J., Ivanov, I. I., Darce, J., Hattori, K., Shima, T., Umesaki, Y., Littman, D. R., Benoist, C., & Mathis, D. (2010) · Immunity · doi:10.1016/j.immuni.2010.06.001 · Cited by 1,577 · see citing works
Self-citationWucherpfennig, K. W., & Strominger, J. L. (1995) · Cell · doi:10.1016/0092-8674(95)90348-8 · Cited by 1,545 · see citing works
Microbiota regulates immune defense against respiratory tract influenza A virus infection
Ichinohe, T., Pang, I. K., Kumamoto, Y., Peaper, D. R., Ho, J. H., Murray, T. S., & Iwasaki, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019378108 · Cited by 1,502 · see citing works
Microbiome-derived inosine modulates response to checkpoint inhibitor immunotherapy
Mager, L. F., Burkhard, R., Pett, N., Cooke, N. C. A., Brown, K., Ramay, H., Paik, S., Stagg, J., Groves, R. A., Gallo, M., et al. (2020) · Science · doi:10.1126/science.abc3421 · Cited by 1,407 · see citing works
A Special Population of Regulatory T Cells Potentiates Muscle Repair
Burzyn, D., Kuswanto, W., Kolodin, D., Shadrach, J. L., Cerletti, M., Jang, Y., Sefik, E., Tan, T. G., Wagers, A. J., Benoist, C., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.054 · Cited by 1,234 · see citing works
Self-citationLepper, C., Partridge, T. A., & Fan, C.-M. (2011) · Development · doi:10.1242/dev.067595 · Cited by 1,105 · 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
Eberl, G., Marmon, S., Sunshine, M. J., Rennert, P. D., Choi, Y., & Littman, D. R. (2003) · Nature Immunology · doi:10.1038/ni1022 · Cited by 986 · see citing works
Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration
Sambasivan, R., Yao, R., Kissenpfennig, A., Van Wittenberghe, L., Paldi, A., Gayraud-Morel, B., Guenou, H., Malissen, B., Tajbakhsh, S., & Galy, A. (2011) · Development · doi:10.1242/dev.067587 · Cited by 939 · 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-citationDiet-microbiota interactions and personalized nutrition
Kolodziejczyk, A. A., Zheng, D., & Elinav, E. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0256-8 · Cited by 879 · see citing works
The microbiota regulates type 2 immunity through RORγt <sup>+</sup> T cells
Ohnmacht, C., Park, J.-H., Cording, S., Wing, J. B., Atarashi, K., Obata, Y., Gaboriau-Routhiau, V., Marques, R., Dulauroy, S., Fedoseeva, M., et al. (2015) · Science · doi:10.1126/science.aac4263 · Cited by 863 · see citing works
mTORC1 controls the adaptive transition of quiescent stem cells from G0 to GAlert
Rodgers, J. T., King, K. Y., Brett, J. O., Cromie, M. J., Charville, G. W., Maguire, K. K., Brunson, C., Mastey, N., Liu, L., Tsai, C.-R., et al. (2014) · Nature · doi:10.1038/nature13255 · Cited by 776 · see citing works
Mining the Human Gut Microbiota for Immunomodulatory Organisms
Geva-Zatorsky, N., Sefik, E., Kua, L., Pasman, L., Tan, T. G., Ortiz-Lopez, A., Yanortsang, T. B., Yang, L., Jupp, R., Mathis, D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.01.022 · Cited by 762 · see citing works
Self-citationRegulation 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
Meng, F., Wang, K., Aoyama, T., Grivennikov, S. I., Paik, Y., Scholten, D., Cong, M., Iwaisako, K., Liu, X., Zhang, M., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.05.049 · Cited by 711 · 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
A weaning reaction to microbiota is required for resistance to immunopathologies in the adult
Al Nabhani, Z., Dulauroy, S., Marques, R., Cousu, C., Al Bounny, S., Déjardin, F., Sparwasser, T., Bérard, M., Cerf-Bensussan, N., & Eberl, G. (2019) · Immunity · doi:10.1016/j.immuni.2019.02.014 · Cited by 679 · see citing works
Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring
Kim, S., Kim, H., Yim, Y. S., Ha, S., Atarashi, K., Tan, T. G., Longman, R. S., Honda, K., Littman, D. R., Choi, G. B., et al. (2017) · Nature · doi:10.1038/nature23910 · Cited by 678 · see citing works
scRepertoire: An R-based toolkit for single-cell immune receptor analysis
Borcherding, N. C., Bormann, N. L., & Kraus, G. (2020) · F1000Research · doi:10.12688/f1000research.22139.1 · Cited by 612 · 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
Dietary antigens limit mucosal immunity by inducing regulatory T cells in the small intestine
Kim, K. S., Hong, S., Han, D., Yi, J., Jung, J., Yang, B., Lee, J. Y., Lee, M., & Surh, C. D. (2016) · Science · doi:10.1126/science.aac5560 · Cited by 541 · see citing works
Komatsu, N., Mariotti‐Ferrandiz, E., Wang, Y., MALISSEN, B., Waldmann, H., & Hori, S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811556106 · Cited by 523 · see citing works
An improved mouse model that rapidly develops fibrosis in non‐alcoholic steatohepatitis
Matsumoto, M., Hada, N., Sakamaki, Y., Uno, A., Shiga, T., Tanaka, C., Ito, T., Katsume, A., & Sudoh, M. (2013) · International Journal of Experimental Pathology · doi:10.1111/iep.12008 · Cited by 523 · 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
Self-citationc-MAF-dependent regulatory T cells mediate immunological tolerance to a gut pathobiont
Xu, M., Pokrovskii, M., Ding, Y., Yi, R., Au, C., Harrison, O. J., Galan, C., Belkaid, Y., Bonneau, R., & Littman, D. R. (2018) · Nature · doi:10.1038/nature25500 · Cited by 498 · see citing works
Gut microbiome, liver immunology, and liver diseases
Wang, R., Tang, R., Li, B., Ma, X., Schnabl, B., & Tilg, H. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-00592-6 · Cited by 466 · see citing works
Targeting the sphingosine-1-phosphate axis in cancer, inflammation and beyond
Kunkel, G. T., Maceyka, M. W., Milstien, S., & Spiegel, S. (2013) · Nature Reviews Drug Discovery · doi:10.1038/nrd4099 · Cited by 437 · see citing works
Yang, B.-H., Hagemann, S., Mamareli, P., Lauer, U., Hoffmann, U., Beckstette, M., Föhse, L., Prinz, I., Pezoldt, J., Suerbaum, S., et al. (2015) · Mucosal Immunology · doi:10.1038/mi.2015.74 · Cited by 435 · see citing works
Tomura, M., Yoshida, N., Tanaka, J., Karasawa, S., Miwa, Y., Miyawaki, A., & Kanagawa, O. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802278105 · Cited by 414 · see citing works
Gomes, A. L., Teijeiro, A., Burén, S., Tummala, K. S., Yilmaz, M., Waisman, A., Theurillat, J.-P., Perna, C., & Djouder, N. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.05.020 · Cited by 401 · see citing works
Isolation of skeletal muscle stem cells by fluorescence-activated cell sorting
Liu, L. A., Cheung, T. H., Charville, G. W., & Rando, T. A. (2015) · Nature Protocols · doi:10.1038/nprot.2015.110 · Cited by 396 · see citing works
Microbiota therapy acts via a regulatory T cell MyD88/RORγt pathway to suppress food allergy
Abdel-Gadir, A., Victor, E. S., Gerber, G. K., Rivas, M. N., Wang, S., Harb, H., Wang, L., Li, N., Crestani, E., Spielman, S. C., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0461-z · Cited by 392 · see citing works
<i>Nebulosa</i> recovers single-cell gene expression signals by kernel density estimation
Alquicira-Hernandez, J., & Powell, J. E. (2021) · Bioinformatics · doi:10.1093/bioinformatics/btab003 · Cited by 381 · 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
Self-citationNext maSigPro: updating maSigPro bioconductor package for RNA-seq time series
Nueda, M. J., Tarazona, S., & Conesa, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu333 · Cited by 348 · see citing works
scRepertoire: An R-based toolkit for single-cell immune receptor analysis
Borcherding, N. C., Bormann, N. L., & Kraus, G. (2020) · F1000Research · doi:10.12688/f1000research.22139.2 · Cited by 348 · see citing works
TNF-α regulates myogenesis and muscle regeneration by activating p38 MAPK
Chen, S., Jin, B., & Li, Y.-P. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00486.2006 · Cited by 301 · 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
Developmental plasticity allows outside-in immune responses by resident memory T cells
Fonseca, R., Beura, L. K., Quarnstrom, C. F., Ghoneim, H. E., Fan, Y., Zebley, C. C., Scott, M. C., Fares-Frederickson, N. J., Wijeyesinghe, S., Thompson, E. A., et al. (2020) · Nature Immunology · doi:10.1038/s41590-020-0607-7 · Cited by 286 · 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-citationNovel antigen-presenting cell imparts Treg-dependent tolerance to gut microbiota
Akagbosu, B., Tayyebi, Z., Shibu, G., Paucar Iza, Y. A., Deep, D., Parisotto, Y. F., Fisher, L., Pasolli, H. A., Thevin, V., Elmentaite, R., et al. (2022) · Nature · doi:10.1038/s41586-022-05309-5 · Cited by 273 · see citing works
Huang, H., Kim, H. J., Chang, E.-J., Lee, Z. H., Hwang, S. J., Kim, H.-M., Lee, Y.-K., & Kim, H. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2009.74 · Cited by 272 · see citing works
Lu, H., Huang, D., Ransohoff, R. M., & Zhou, L. (2011) · The FASEB Journal · doi:10.1096/fj.10-178939 · Cited by 255 · see citing works
The role of interleukin-17 in tumor development and progression
Zhao, J., Chen, X., Herjan, T., & Li, X. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190297 · Cited by 253 · see citing works
Differentiation of regulatory Foxp3 + T cells in the thymic cortex
Liston, A., Nutsch, K., Farr, A. G., Lund, J. M., Rasmussen, J. P., Koni, P. A., & Rudensky, A. Y. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801506105 · Cited by 240 · see citing works
Pianta, A., Arvikar, S. L., Strle, K., Drouin, E. E., Wang, Q., Costello, C. E., & Steere, A. C. (2017) · Journal of Clinical Investigation · doi:10.1172/jci93450 · Cited by 239 · see citing works
TCR Transgenic Mice Reveal Stepwise, Multi-site Acquisition of the Distinctive Fat-Treg Phenotype
Li, C., DiSpirito, J. R., Zemmour, D., Spallanzani, R. G., Kuswanto, W., Benoist, C., & Mathis, D. (2018) · Cell · doi:10.1016/j.cell.2018.05.004 · Cited by 231 · see citing works
Self-citationXia, N., Lu, Y., Gu, M., Li, N., Liu, M., Jiao, J., Zhu, Z., Li, J., Li, D., Tang, T., et al. (2020) · Circulation · doi:10.1161/circulationaha.120.046789 · Cited by 229 · see citing works
Wu, L., Chen, X., Zhao, J., Martin, B. N., Zepp, J. A., Ko, J. S., Gu, C., Cai, G., Ouyang, W., Sen, G. C., et al. (2015) · The Journal of Experimental Medicine · doi:10.1084/jem.20150204 · Cited by 221 · see citing works
Act1 mediates IL-17-induced EAE pathogenesis selectively in NG2+ glial cells
Kang, Z., Wang, C., Zepp, J., Wu, L., Sun, K., Zhao, J., Chandrasekharan, U., DiCorleto, P. E., Trapp, B. D., Ransohoff, R. M., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3505 · Cited by 218 · see citing works
Endogenous interferon-γ is required for efficient skeletal muscle regeneration
Cheng, M., Nguyen, M.-H., Fantuzzi, G., & Koh, T. J. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00568.2007 · Cited by 214 · see citing works
Girgenrath, M., Weng, S., Kostek, C. A., Browning, B., Wang, M., Brown, S. A. N., Winkles, J. A., Michaelson, J. S., Allaire, N., Schneider, P., et al. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601441 · Cited by 213 · see citing works
Intestinal Microbiota of Mice Influences Resistance to Staphylococcus aureus Pneumonia
Gauguet, S., D'Ortona, S., Ahnger-Pier, K., Duan, B., Surana, N. K., Lu, R., Cywes-Bentley, C., Gadjeva, M., Shan, Q., Priebe, G. P., et al. (2015) · Infection and Immunity · doi:10.1128/iai.00037-15 · Cited by 208 · see citing works
Endoscopic photoconversion reveals unexpectedly broad leukocyte trafficking to and from the gut
Morton, A. M., Sefik, E., Upadhyay, R., Weissleder, R., Benoist, C. O., & Mathis, D. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1405634111 · Cited by 200 · see citing works
Self-citationLi, F., Hao, X., Chen, Y., Bai, L., Gao, X., Lian, Z., Wei, H., Sun, R., & Tian, Z. (2017) · Nature Communications · doi:10.1038/ncomms13839 · Cited by 191 · see citing works
T Cell-Mediated Autoimmune Disease Due to Low-Affinity Crossreactivity to Common Microbial Peptides
Harkiolaki, M., Holmes, S. L., Svendsen, P., Gregersen, J. W., Jensen, L. T., McMahon, R. M., Friese, M. A., van Boxel, G., Etzensperger, R., Tzartos, J. S., et al. (2009) · Immunity · doi:10.1016/j.immuni.2009.01.009 · Cited by 190 · see citing works
Neumann, C., Blume, J., Roy, U., Teh, P. P., Vasanthakumar, A., Beller, A. V., Liao, Y., Heinrich, F., Arenzana, T. L., Hackney, J. A., et al. (2019) · Nature Immunology · doi:10.1038/s41590-019-0316-2 · Cited by 179 · see citing works
The Transcription Factor c-Maf Controls Touch Receptor Development and Function
Wende, H., Lechner, S. G., Chéret, C., Bourane, S., Sheean, M. E., Pattyn, A., Reuter, K., Munier, F. L., Carroll, P., Lewin, G. R., et al. (2012) · Science · doi:10.1126/science.1214314 · Cited by 176 · see citing works
Szymula, A., Rosenthal, J., Szczerba, B. M., Bagavant, H., Fu, S. M., & Deshmukh, U. S. (2014) · Clinical Immunology · doi:10.1016/j.clim.2014.02.004 · Cited by 166 · see citing works
Molecular diversification of regulatory T cells in nonlymphoid tissues
DiSpirito, J. R., Zemmour, D., Ramanan, D., Cho, J., Žilionis, R., Klein, A. M., Benoist, C. O., & Mathis, D. J. (2018) · Science Immunology · doi:10.1126/sciimmunol.aat5861 · Cited by 163 · see citing works
Self-citationGut CD4+ T cell phenotypes are a continuum molded by microbes, not by TH archetypes
Kiner, E., Willie, E., Vijaykumar, B., Chowdhary, K., Schmutz, H., Chandler, J. S., Schnell, A., Thakore, P. I., Gros, G. S. L., Mostafavi, S., et al. (2021) · Nature Immunology · doi:10.1038/s41590-020-00836-7 · Cited by 163 · see citing works
Self-citationPanduro, M., Benoist, C. O., & Mathis, D. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800618115 · Cited by 157 · see citing works
Self-citationGiannakis, N., Sansbury, B. E., Patsalos, A., Hays, T. T., Riley, C. O., Han, X., Spite, M. R., & Nagy, L. (2019) · Nature Immunology · doi:10.1038/s41590-019-0356-7 · Cited by 157 · see citing works
Mathur, A. N., Zirak, B., Boothby, I. C., Tan, M., Cohen, J. N., Mauro, T., Mehta, P., Lowe, M. M., Abbas, A. K., Ali, N., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.02.013 · Cited by 149 · see citing works
Pulmonary Th17 Antifungal Immunity Is Regulated by the Gut Microbiome
McAleer, J. P., Nguyen, N. L. H., Chen, K., Kumar, P., Ricks, D. M., Binnie, M., Armentrout, R., Pociask, D. A., Hein, A., Yu, A. C., et al. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502566 · Cited by 126 · see citing works
A Gut Microbial Mimic that Hijacks Diabetogenic Autoreactivity to Suppress Colitis
Nanjundappa, R. H., Ronchi, F., Wang, J., Clemente‐Casares, X., Yamanouchi, J., Umeshappa, C. S., Yang, Y., Blanco, J., Bassolas-Molina, H., Salas, A., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.022 · Cited by 116 · see citing works
Skeletal muscle regeneration with robotic actuation–mediated clearance of neutrophils
Seo, B. R., Payne, C. J., McNamara, S. L., Freedman, B. R., Kwee, B. J., Nam, S., de Lázaro, I., Darnell, M., Alvarez, J. T., Dellacherie, M. O., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abe8868 · Cited by 111 · see citing works
IL-17R-EGFR axis links wound healing to tumorigenesis in Lrig1+ stem cells
Chen, X., Cai, G., Liu, C., Zhao, J., Gu, C., Wu, L., Hamilton, T. A., Zhang, C.-J., Ko, J., Zhu, L., et al. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20171849 · Cited by 106 · see citing works
FOS licenses early events in stem cell activation driving skeletal muscle regeneration
Almada, A. E., Horwitz, N., Price, F. D., Gonzalez, A. E., Ko, M. Y., Bölükbaşı, Ö. V., Messemer, K. A., Chen, S., Sinha, M., Rubin, L. L., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108656 · Cited by 95 · see citing works
Londhe, P., & Davie, J. K. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05397-11 · Cited by 86 · see citing works
Gut Microbial Antigenic Mimicry in Autoimmunity
Garabatos, N., & Santamaría, P. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.873607 · Cited by 74 · see citing works
Heterogeneity of Satellite Cells Implicates DELTA1/NOTCH2 Signaling in Self-Renewal
Yartseva, V., Goldstein, L. D., Rodman, J., Kates, L., Chen, M. Z., Chen, Y.-J. J., Foreman, O., Siebel, C. W., Modrusan, Z. D., Peterson, A. S., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.100 · Cited by 71 · see citing works
Pratama, A., Schnell, A., Mathis, D. J., & Benoist, C. O. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190428 · Cited by 70 · see citing works
Self-citationIL-17A–Induced PLET1 Expression Contributes to Tissue Repair and Colon Tumorigenesis
Zepp, J. A., Zhao, J., Liu, C., Bulek, K., Wu, L., Chen, X., Hao, Y., Wang, Z., Wang, X., Ouyang, W., et al. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601540 · Cited by 69 · see citing works
Kocić, J., Santibanez, J. F., Krstić, J., Mojsilović, S. B., Djordjević, I. O., Trivanović, D. I., Ilić, V. L., & Bugarski, D. S. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.01.001 · Cited by 66 · see citing works
Cho, J., Kuswanto, W. F., Benoist, C. O., & Mathis, D. J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1914848116 · Cited by 62 · see citing works
Self-citationLondhe, P., & Davie, J. K. (2013) · Science Signaling · doi:10.1126/scisignal.2004633 · Cited by 52 · see citing works
Neuronal, stromal, and T-regulatory cell crosstalk in murine skeletal muscle
Wang, K., Yaghi, O., Spallanzani, R. G., Chen, X., Zemmour, D., Lai, N. Y., Chiu, I. M., Benoist, C. O., & Mathis, D. J. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1922559117 · Cited by 52 · see citing works
Self-citationAtaide, M. A., Knöpper, K., de Casas, P. C., Ugur, M., Eickhoff, S., Zou, M., Shaikh, H., Trivedi, A., Grafen, A., Yang, T., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.07.019 · Cited by 51 · see citing works
PPARγ marks splenic precursors of multiple nonlymphoid-tissue Treg compartments
Li, C., Muñoz-Rojas, A. R., Wang, G., Mann, A. O., Benoist, C. O., & Mathis, D. J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2025197118 · Cited by 50 · see citing works
Self-citationIL-17A–producing γδT cells promote muscle regeneration in a microbiota-dependent manner
Mann, A. O., Hanna, B. S., Muñoz-Rojas, A. R., Sandrock, I., Prinz, I., Benoist, C. O., & Mathis, D. J. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20211504 · Cited by 45 · see citing works
Self-citationHarnessing the microbiota for therapeutic purposes
Liwinski, T., & Elinav, E. (2019) · American Journal of Transplantation · doi:10.1111/ajt.15753 · Cited by 39 · see citing works
Sphingosine-1-phosphate receptor 2 restrains egress of γδ T cells from the skin
Laidlaw, B. J., Gray, E. E., Zhang, Y., Ramírez‐Valle, F., & Cyster, J. G. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190114 · Cited by 38 · see citing works
Pro, S. C., Arlehamn, C. S. L., Dhanda, S. K., Carpenter, C., Lindvall, M., Faruqi, A. A., Santee, C. A., Renz, H., Sidney, J., Peters, B., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0196551 · Cited by 32 · see citing works
Aguilar, C. A., Shcherbina, A., Ricke, D. O., Pop, R., Carrigan, C. T., Gifford, C. A., Urso, M. L., Kottke, M. A., & Meissner, A. (2015) · Scientific Reports · doi:10.1038/srep13885 · Cited by 25 · see citing works
Hardy, C. L., Bhathal, P. S., Snibson, K. J., et al. (1997) · Immunology · doi:10.1111/j.1365-2567.1997.00412.x · Cited by 18 · see citing works
Giannakis, N., Sansbury, B. E., Patsalos, A., et al. (2019) · Nature Immunology · doi:10.1038/s41590-019-0401-6 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
Loh, J. S., Mak, W. Q., Tan, L. K. S., Ng, C. X., Chan, H. H., Yeow, S. H., Foo, J. B., Ong, Y. S., How, C. W., & Khaw, K. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01743-1 · Cited by 1,193 · see citing works
Regulatory T cells in the face of the intestinal microbiota
Ramanan, D., Pratama, A., Zhu, Y., Venezia, O., Sassone-Corsi, M., Chowdhary, K., Galván-Peña, S., Sefik, E., Brown, C., Gélineau, A., et al. (2023) · Nature Reviews Immunology · doi:10.1038/s41577-023-00890-w · Cited by 126 · see citing works
Self-citationRegulatory T cells safeguard liver health during metabolic-associated steatohepatitis
Hanna, B. S., Langston, P. K., Marin-Rodero, M., Ramirez, R. N., Wan, M., Benoist, C., & Mathis, D. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2536314123 · Cited by 1 · see citing works
“Both reparative clusters expressed diagnostic Areg (encoding amphiregulin) and Il1rl1 (specifying the IL - 33 receptor, ST2) transcripts and were enriched for an established reparative - Treg signature ( SI Appendix , Table S1) (25).”
Self-citation
- Authors
- Hanna, B. S., Wang, G., Galván-Peña, S., Mann, A. O., Ramirez, R. N., Muñoz-Rojas, A. R., Smith, K., Wan, M., Benoist, C., & Mathis, D.
- Affiliations
- Brigham and Women's Hospital (US)
- Pfizer (United States) (US)
- Corresponding author
- Mathis, Diane
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2023-04
- Volume
- 56
- Issue
- 4
- Pages
- 829-846.e8
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC10101925
- OpenAlex
- W4321503800
- Cited by
- 126
- References
- 105
- Citations by year
- 2026: 33 · 2025: 44 · 2024: 30 · 2023: 19
- FWCI
- 13.75
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 417 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Pfizer
- Deutsche Forschungsgemeinschaft (HA 8510/1)
- National Institutes of Health
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR070334)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
- Keywords
- gut microbiota, tissue regeneration, skeletal muscle injury, sterile inflammation, IL-17A, MHC class II, T cell activation, stem cell proliferation and differentiation, intestinal homeostasis
- MeSH terms
- Gastrointestinal Microbiome, Animals, Mice, Inbred C57BL, T-Lymphocytes, Regulatory, Mice, Nuclear Receptor Subfamily 1, Group F, Member 3, Microbiota
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