Circulating and Tissue-Resident CD4+ T Cells With Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function Is Altered During Inflammation
Open accessAbstract
Background & Aims Interactions between commensal microbes and the immune system are tightly regulated and maintain intestinal homeostasis, but little is known about these interactions in humans. We investigated responses of human CD4 + T cells to the intestinal microbiota. We measured the abundance of T cells in circulation and intestinal tissues that respond to intestinal microbes and determined their clonal diversity. We also assessed their functional phenotypes and effects on intestinal resident cell populations, and studied alterations in microbe-reactive T cells in patients with chronic intestinal inflammation. Methods We collected samples of peripheral blood mononuclear cells and intestinal tissues from healthy individuals (controls, n = 13−30) and patients with inflammatory bowel diseases (n = 119; 59 with ulcerative colitis and 60 with Crohn's disease). We used 2 independent assays (CD154 detection and carboxy-fluorescein succinimidyl ester dilution assays) and 9 intestinal bacterial species ( Escherichia coli, Lactobacillus acidophilus, Bifidobacterium animalis subsp lactis, Faecalibacterium prausnitzii, Bacteroides vulgatus, Roseburia intestinalis, Ruminococcus obeum, Salmonella typhimurium, and Clostridium difficile ) to quantify, expand, and characterize microbe-reactive CD4 + T cells. We sequenced T-cell receptor Vβ genes in expanded microbe-reactive T-cell lines to determine their clonal diversity. We examined the effects of microbe-reactive CD4 + T cells on intestinal stromal and epithelial cell lines. Cytokines, chemokines, and gene expression patterns were measured by flow cytometry and quantitative polymerase chain reaction. Results Circulating and gut-resident CD4 + T cells from controls responded to bacteria at frequencies of 40−4000 per million for each bacterial species tested. Microbiota-reactive CD4 + T cells were mainly of a memory phenotype, present in peripheral blood mononuclear cells and intestinal tissue, and had a diverse T-cell receptor Vβ repertoire. These cells were functionally heterogeneous, produced barrier-protective cytokines, and stimulated intestinal stromal and epithelial cells via interleukin 17A, interferon gamma, and tumor necrosis factor. In patients with inflammatory bowel diseases, microbiota-reactive CD4 + T cells were reduced in the blood compared with intestine; T-cell responses that we detected had an increased frequency of interleukin 17A production compared with responses of T cells from blood or intestinal tissues of controls. Conclusions In an analysis of peripheral blood mononuclear cells and intestinal tissues from patients with inflammatory bowel diseases vs controls, we found that reactivity to intestinal bacteria is a normal property of the human CD4 + T-cell repertoire, and does not necessarily indicate disrupted interactions between immune cells and the commensal microbiota. T-cell responses to commensals might support intestinal homeostasis, by producing barrier-protective cytokines and providing a large pool of T cells that react to pathogens.
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Gut-resident bacteria-reactive T cells produced more IFNγ, IL-17A and IL-2 and less IL-22, GMCSF and IL-4 than non-enteric microbiota-reactive T cells.
“Compared with non-enteric microbiota-reactive T cells, gut-resident bacteria-reactive T cells produced high amounts of IFNγ, IL-17A and IL-2, and low amounts of IL-22, GMCSF and IL-4 (ref. 112).”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [112]
In IBD, circulating and gut-resident microbiota-reactive CD4+ T cells secreted more IL-17A than those from healthy volunteers.
“In pathological circumstances of mucosal barrier dysfunction, such as IBD, circulating and gut-resident microbiota-reactive CD4+ T cells secreted increased levels of IL-17A compared with those from healthy volunteers112.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [112]
In healthy volunteers, enteric bacteria-reactive CD4+ T cells occurred at precursor frequencies of 40-500 per 10^6 circulating CD4+ T cells for almost all enteric bacteria tested.
“In a survey of healthy volunteers, enteric bacteria-reactive CD4+ T cells were present at precursor frequencies of 40–500 cells per 106 circulating CD4+ T cells for almost all enteric bacteria analysed112; the frequency of bacteria-reactive T cells in gut tissue was threefold to eightfold that in circulation.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [112]
Bacteria-reactive T cell frequency in gut tissue was threefold to eightfold higher than in circulation.
“In a survey of healthy volunteers, enteric bacteria-reactive CD4+ T cells were present at precursor frequencies of 40–500 cells per 106 circulating CD4+ T cells for almost all enteric bacteria analysed112; the frequency of bacteria-reactive T cells in gut tissue was threefold to eightfold that in circulation.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [112]
T cell responses against commensals are commonly found in healthy people.
“T cell responses against commensals are commonly detected in healthy individuals, suggesting that these cells participate in intestinal homeostasis by producing barrier-protective cytokines, and might constitute a sizeable pool of pathobiont-reactive T cells112.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [112]
Reactivity to intestinal bacteria seems to be a healthy property of both intestinal and systemic human CD4+ T cells, which may support homeostasis by providing a large pool of immune cells protective against pathogens.
“Reactivity to intestinal bacteria seems to be a 'healthy' property of both intestinal and systemic human CD4+ T cells, which may support homeostasis by providing a large pool of immune cells protective against pathogens.108”
From Interaction between microbiota and immunity in health and disease (2020) · cites this paper as [108]
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Cites
Robust enumeration of cell subsets from tissue expression profiles
Newman, A. M., Liu, C. L., Green, M. R., Gentles, A. J., Feng, W., Xu, Y., Hoang, C. D., Diehn, M., & Alizadeh, A. A. (2015) · Nature Methods · doi:10.1038/nmeth.3337 · Cited by 12,116 · see citing works
Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J.-P., & Ricciardi‐Castagnoli, P. (2001) · Nature Immunology · doi:10.1038/86373 · Cited by 2,554 · see citing works
Intestinal homeostasis and its breakdown in inflammatory bowel disease
Maloy, K. J., & Powrie, F. M. (2011) · Nature · doi:10.1038/nature10208 · Cited by 1,876 · see citing works
Self-citationPhenotypic and functional features of human Th17 cells
Annunziato, F., Cosmi, L., Santarlasci, V., Maggi, L., Liotta, F., Mazzinghi, B., Parente, E., Filì, L., Ferri, S., Frosali, F., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070663 · Cited by 1,861 · see citing works
The Microbiome in Inflammatory Bowel Disease: Current Status and the Future Ahead
Kostic, A. D., Xavier, R. J., & Gevers, D. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.02.009 · Cited by 1,789 · see citing works
The Biological Functions of T Helper 17 Cell Effector Cytokines in Inflammation
Ouyang, W., Kolls, J. K., & Zheng, Y. (2008) · Immunity · doi:10.1016/j.immuni.2008.03.004 · Cited by 1,698 · see citing works
Induction of Protective IgA by Intestinal Dendritic Cells Carrying Commensal Bacteria
Macpherson, A. J., & Uhr, T. (2004) · Science · doi:10.1126/science.1091334 · Cited by 1,584 · see citing works
Immunoglobulin A Coating Identifies Colitogenic Bacteria in Inflammatory Bowel Disease
Palm, N. W., de Zoete, M. R., Cullen, T. W., Barry, N. A., Stefanowski, J., Hao, L., Degnan, P. H., Hu, J., Peter, I., Zhang, W., et al. (2014) · Cell · doi:10.1016/j.cell.2014.08.006 · Cited by 1,286 · see citing works
Lymphocyte traffic control by chemokines
Moser, B., & Loetscher, P. (2001) · Nature Immunology · doi:10.1038/84219 · Cited by 1,235 · see citing works
Sonnenberg, G. F., Fouser, L. A., & Artis, D. (2011) · Nature Immunology · doi:10.1038/ni.2025 · Cited by 1,041 · see citing works
A very high level of crossreactivity is an essential feature of the T-cell receptor
Mason, D. (1998) · Immunology Today · doi:10.1016/s0167-5699(98)01299-7 · Cited by 950 · see citing works
Duchmann, R., Kaiser, I., Hermann, E., Mayet, W.-J., Ewe, K., & BÜSCHENFELDE, K.-H. M. Z. (1995) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.1995.tb03836.x · Cited by 938 · see citing works
Pathogen-induced human TH17 cells produce IFN-γ or IL-10 and are regulated by IL-1β
Zielinski, C. E., Mele, F., Aschenbrenner, D., Jarrossay, D., Ronchi, F., Gattorno, M., Monticelli, S., Lanzavecchia, A., & Sallusto, F. (2012) · Nature · doi:10.1038/nature10957 · Cited by 919 · see citing works
Human memory T cells: generation, compartmentalization and homeostasis
Farber, D. L., Yudanin, N. A., & Restifo, N. P. (2014) · Nature Reviews Immunology · doi:10.1038/nri3567 · Cited by 897 · see citing works
Memory T Cell Subsets, Migration Patterns, and Tissue Residence
Mueller, S. N., Gebhardt, T., Carbone, F., & Heath, W. R. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095954 · Cited by 842 · see citing works
The microbiome in infectious disease and inflammation
Honda, K., & Littman, D. R. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-074937 · Cited by 791 · see citing works
Interleukin-23-Independent IL-17 Production Regulates Intestinal Epithelial Permeability
Lee, J. S., Tato, C. M., Joyce-Shaikh, B., Gulen, M. F., Cayatte, C., Chen, Y., Blumenschein, W. M., Judo, M., Ayanoglu, G., McClanahan, T. K., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.09.003 · Cited by 760 · see citing works
Phenotype and function of human T lymphocyte subsets: Consensus and issues
Appay, V., van Lier, R. A. W., Sallusto, F., & Roederer, M. (2008) · Cytometry Part A · doi:10.1002/cyto.a.20643 · Cited by 729 · see citing works
Vβ-Specific Stimulation of Human T Cells by Staphylococcal Toxins
Kappler, J. W., Kotzin, B. L., Herron, L. R., Gelfand, E. W., Bigler, R. D., Boylston, A. W., Carrel, S., Posnett, D. N., Choi, Y., & Marrack, P. (1989) · Science · doi:10.1126/science.2524876 · Cited by 696 · see citing works
IL-23–responsive innate lymphoid cells are increased in inflammatory bowel disease
Geremia, A., Arancibia-Cárcamo, C. V., Fleming, M. P. P., Rust, N. A., Singh, B., Mortensen, N., Travis, S. P. L., & Powrie, F. M. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20101712 · Cited by 640 · see citing works
Self-citationRole of the Commensal Microbiota in Normal and Pathogenic Host Immune Responses
Littman, D. R., & Pamer, E. G. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.10.004 · Cited by 548 · see citing works
Linking T-cell receptor sequence to functional phenotype at the single-cell level
Han, A. S., Glanville, J., Hansmann, L., & Davis, M. M. (2014) · Nature Biotechnology · doi:10.1038/nbt.2938 · Cited by 534 · see citing works
Development of intestinal microbiota in infants and its impact on health
Matamoros, S., Guen, C. G., Vacon, F. L., Potel, G., & de la Cochetière, M.-F. (2013) · Trends in Microbiology · doi:10.1016/j.tim.2012.12.001 · Cited by 533 · see citing works
Direct access to CD4+ T cells specific for defined antigens according to CD154 expression
Frentsch, M., Arbach, O., Kirchhoff, D., Moewes, B., Worm, M., Rothe, M., Scheffold, A., & Thiel, A. (2005) · Nature Medicine · doi:10.1038/nm1292 · Cited by 475 · see citing works
Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation
Kleinschek, M. A., Boniface, K., Sadekova, S., Grein, J., Murphy, E. E., Turner, S. P., Raskin, L., Desai, B., Faubion, W. A., de Waal Malefyt, R., et al. (2009) · Journal of Experimental Medicine · doi:10.1084/jem.20081712 · Cited by 460 · see citing works
Virus-specific CD4(+) memory-phenotype T cells are abundant in unexposed adults
Su, L. F., Kidd, B. A., Han, A., Kotzin, J. J., & Davis, M. M. (2013) · Immunity · doi:10.1016/j.immuni.2012.10.021 · Cited by 429 · see citing works
Gradel, K. O., Nielsen, H. L., Schønheyder, H. C., Ejlertsen, T., Kristensen, B., & Nielsen, H. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.04.001 · Cited by 424 · see citing works
Zeng, M. Y., Cisalpino, D., Varadarajan, S., Hellman, J., Warren, H. S., Cascalho, M., Inohara, N., & Núñez, G. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.006 · Cited by 417 · see citing works
Smith, A. M., Rahman, F. Z., Hayee, B., Graham, S. J., Marks, D. J., Sewell, G. W., Palmer, C. D., Wilde, J. I., Foxwell, B. M. J., Gloger, I., et al. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20091233 · Cited by 399 · see citing works
Acute Gastrointestinal Infection Induces Long-Lived Microbiota-Specific T Cell Responses
Hand, T. W., dos Santos, L. M., Bouladoux, N. J., Molloy, M. J., Pagán, A. J., Pepper, M., Maynard, C. L., Elson, C. O., & Belkaid, Y. (2012) · Science · doi:10.1126/science.1220961 · Cited by 393 · see citing works
Cong, Y., Brandwein, S. L., McCabe, R. P., Lazenby, A., Birkenmeier, E. H., Sundberg, J. P., & Elson, C. O. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.187.6.855 · Cited by 383 · see citing works
Targeting Th17 cells in autoimmune diseases
Yang, J., Sundrud, M. S., Skepner, J. E., & Yamagata, T. (2014) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2014.07.006 · Cited by 348 · see citing works
Differential Roles for Interleukin-23 and Interleukin-17 in Intestinal Immunoregulation
Maxwell, J. R., Zhang, Y., Brown, W. A., Smith, C. L., Byrne, F. R., Fiorino, M., Stevens, E., Bigler, J., Davis, J. A., Rottman, J. B., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.08.019 · Cited by 342 · see citing works
Heterogeneity of Human CD4 <sup>+</sup> T Cells Against Microbes
Sallusto, F. (2016) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112056 · Cited by 336 · see citing works
A live-cell assay to detect antigen-specific CD4+ T cells with diverse cytokine profiles
Chattopadhyay, P. K., Yu, J., & Roederer, M. (2005) · Nature Medicine · doi:10.1038/nm1293 · Cited by 321 · see citing works
Picco, M. F. (2010) · Yearbook of Gastroenterology · doi:10.1016/s0739-5930(09)79399-7 · Cited by 316 · see citing works
Functional heterogeneity of human memory CD4 + T cell clones primed by pathogens or vaccines
Becattini, S., Latorre, D., Mele, F., Foglierini, M., Gregorio, C. D., Cassotta, A., Fernandez, B., Kelderman, S., Schumacher, T. N., Corti, D., et al. (2014) · Science · doi:10.1126/science.1260668 · Cited by 314 · see citing works
New targets for mucosal healing and therapy in inflammatory bowel diseases
Neurath, M. F. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.73 · Cited by 309 · see citing works
Cultivable bacterial diversity from the human colon
Duncan, S. H., Louis, P., & Flint, H. J. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02129.x · Cited by 279 · see citing works
Duchmann, R., May, E., Heike, M., Knolle, P. A., Neurath, M. F., & BÜSCHENFELDE, K.-H. M. Z. (1999) · Gut · doi:10.1136/gut.44.6.812 · Cited by 258 · see citing works
Th17 Cytokines and the Gut Mucosal Barrier
Blaschitz, C., & Raffatellu, M. (2010) · Journal of Clinical Immunology · doi:10.1007/s10875-010-9368-7 · Cited by 247 · see citing works
CD 4+ T‐cell subsets in intestinal inflammation
Shale, M., Schiering, C., & Powrie, F. M. (2013) · Immunological Reviews · doi:10.1111/imr.12039 · Cited by 222 · see citing works
Self-citationBacher, P., Schink, C., Teutschbein, J., Kniemeyer, O., Assenmacher, M., Brakhage, A. A., & Scheffold, A. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202221 · Cited by 173 · see citing works
Globig, A.-M., Hennecke, N., Martin, B., Seidl, M., Ruf, G., Hasselblatt, P., Thimme, R., & Bengsch, B. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000210 · Cited by 127 · see citing works
The mucosal firewalls against commensal intestinal microbes
Macpherson, A. J., Slack, E. M. C., Geuking, M. B., & McCoy, K. D. (2009) · Seminars in Immunopathology · doi:10.1007/s00281-009-0174-3 · Cited by 114 · see citing works
Expression and kinetics of cytokines determined by intracellular staining using flow cytometry
Winkler, B., Schlenke, P., & Seyfarth, M. (1999) · Journal of Immunological Methods · doi:10.1016/s0022-1759(98)00200-2 · Cited by 106 · see citing works
Proteome-wide analysis of HIV-specific naive and memory CD4+ T cells in unexposed blood donors
Campion, S. L., Brodie, T. M., Fischer, W., Korber, B. T., Rossetti, A., Goonetilleke, N., McMichael, A. J., & Sallusto, F. (2014) · Journal of Experimental Medicine · doi:10.1084/jem.20130555 · Cited by 84 · see citing works
Self-citationEffector and memory T cell responses to commensal bacteria
Belkaid, Y., Bouladoux, N. J., & Hand, T. W. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.03.003 · Cited by 80 · see citing works
Characteristics and Functional Capacities of Human Cord Blood Granulocytes and Monocytes
Maródi, L., Leijh, P. C. J., & van Furth, R. (1984) · Pediatric Research · doi:10.1203/00006450-198411000-00014 · Cited by 80 · see citing works
CCR9 antagonism: potential in the treatment of Inflammatory Bowel Disease
Keshav, S., & Wendt, E. (2015) · Clinical and Experimental Gastroenterology · doi:10.2147/ceg.s48305 · Cited by 72 · see citing works
Self-citationImmunological consequences of intragenus conservation of Mycobacterium tuberculosis T-cell epitopes
Arlehamn, C. S. L., Paul, S., Mele, F., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1416537112 · Cited by 67 · see citing works
Pathogenesis of Crohn’s disease: Bug or no bug
Boscá-Watts, M. M. (2015) · World Journal of Gastrointestinal Pathophysiology · doi:10.4291/wjgp.v6.i1.1 · Cited by 44 · see citing works
Black, G. F., Weir, R. E., Chaguluka, S. D., Warndorff, D. K., Crampin, A. C., Mwaungulu, L., Sichali, L., Floyd, S., Bliss, L., Jarman, E., et al. (2003) · Clinical and Vaccine Immunology · doi:10.1128/cdli.10.4.602-611.2003 · Cited by 40 · see citing works
Sohlberg, E., Saghafian‐Hedengren, S., Bremme, K. A., et al. (2011) · Immunology · doi:10.1111/j.1365-2567.2011.03407.x · Cited by 37 · see citing works
Bächer, P., & Scheffold, A. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.04.005 · Cited by 37 · see citing works
OMIP‐018: Chemokine receptor expression on human T helper cells
Brodie, T., Brenna, E., & Sallusto, F. (2013) · Cytometry Part A · doi:10.1002/cyto.a.22278 · Cited by 32 · see citing works
Ergin, A., Syrbe, U., Scheer, R., Thiel, A., Adam, T., Büssow, K., Duchmann, R., Zeitz, M., & Sieper, J. (2011) · Journal of Clinical Immunology · doi:10.1007/s10875-011-9575-x · Cited by 28 · see citing works
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- [5]Frentsch M. Arbach O. Kirchhoff D. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression Nat Med 11 2005 1118 1124 16186818
- [7]Newman A.M. Liu C.L. Green M.R. Robust enumeration of cell subsets from tissue expression profiles Nat Methods 12 2015 453 457 25822800 PMC4739640
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Zheng, D., Liwinski, T., & Elinav, E. (2020) · Cell Research · doi:10.1038/s41422-020-0332-7 · Cited by 3,947 · 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
Britton, G. J., Contijoch, E. J., Mogno, I., Vennaro, O. H., Llewellyn, S. R., Ng, R., Li, Z., Mortha, A., Merad, M., Das, A., et al. (2019) · Immunity · doi:10.1016/j.immuni.2018.12.015 · Cited by 549 · see citing works
Human Anti-fungal Th17 Immunity and Pathology Rely on Cross-Reactivity against Candida albicans
Bacher, P., Hohnstein, T., Beerbaum, E., Röcker, M., Blango, M. G., Kaufmann, S., Röhmel, J., Eschenhagen, P., Grehn, C., Seidel, K., et al. (2019) · Cell · doi:10.1016/j.cell.2019.01.041 · Cited by 473 · see citing works
Human immune diversity: from evolution to modernity
Liston, A., Humblet-Baron, S., Duffy, D., & Goris, A. (2021) · Nature Immunology · doi:10.1038/s41590-021-01058-1 · Cited by 187 · see citing works
Mishima, Y., Oka, A., Liu, B., Herzog, J. W., Eun, C. S., Fan, T.-J., Bulik-Sullivan, E., Carroll, I. M., Hansen, J. J., Chen, L., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci93820 · Cited by 166 · see citing works
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Thomas, A. M., Fidelle, M., Routy, B., Kroemer, G., Wargo, J. A., Segata, N., & Zitvogel, L. (2023) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-023-00785-8 · Cited by 141 · see citing works
Ma, W., Song, J., Wang, H., Shi, F., Zhou, N., Jiang, J., Xu, Y., Zhang, L., Yang, L., & Zhou, M. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.04.006 · Cited by 134 · see citing works
Cline-Smith, A., Axelbaum, A., Shashkova, E., Chakraborty, M., Sanford, J., Panesar, P., Peterson, M., Cox, L., Baldan, A., Veis, D., et al. (2020) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.3966 · Cited by 108 · see citing works
Cassotta, A., Goldstein, J. D., Durini, G., Jarrossay, D., Baggi Menozzi, F., Venditti, M., Russo, A., Falcone, M., Lanzavecchia, A., Gagliardi, M. C., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202048630 · Cited by 23 · see citing works
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- Authors
- Hegazy, A. N., West, N. R., Stubbington, M. J. T., Wendt, E., Suijker, K. I. M., Datsi, A., This, S., Danne, C., Campion, S., Duncan, S. H., Owens, B. M. J., Uhlig, H. H., McMichael, A., Bergthaler, A., Teichmann, S. A., Keshav, S., & Powrie, F.
- Affiliations
- John Radcliffe Hospital (GB)
- European Bioinformatics Institute (GB)
- University of Oxford (GB)
- University of Aberdeen (GB)
- Austrian Academy of Sciences (AT)
- Corresponding author
- Powrie, Fiona
- ORCID
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2017-11
- Volume
- 153
- Issue
- 5
- Pages
- 1320-1337.e16
- ISSN
- 0016-5085 (ISSN-L)
- PMC
- PMC5687320
- OpenAlex
- W2744280559
- Cited by
- 338
- References
- 57
- Citations by year
- 2026: 21 · 2025: 38 · 2024: 40 · 2023: 42 · 2022: 46 · 2021: 50 · 2020: 41 · 2019: 37 · 2018: 21 · 2017: 1
- FWCI
- 11.17
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Gastroenterology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
- HAL (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- Cancer Research Institute
- Eli Lilly and Company
- Pfizer
- Gilead Sciences
- Leona M. and Harry B. Helmsley Charitable Trust
- Wellcome Trust (102974/Z/13/Z, 095688/Z/11/Z)
- National Institute for Health and Care Research (NIHR-RP-R3-12-026)
- Vifor Pharma
- Mitsubishi Tanabe Pharma Corporation
- Dr. Falk Pharma
- Goddard Space Flight Center
- Allergan
- Medical Research Council (MC_UU_00008/7)
- National Institute of Allergy and Infectious Diseases (UM1AI100645)
- UCB Pharma
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- CD4+ T cells, gut microbiota, commensal bacteria, inflammatory bowel disease, ulcerative colitis, Crohn's disease, T cell receptor V beta repertoire, memory T cells, intestinal homeostasis, IL-17A, interferon-gamma, TNF-α, intestinal epithelial cells, intestinal stromal cells
- MeSH terms
- Gastrointestinal Microbiome, Bacteria, Cell Line, Colitis, Ulcerative, Crohn Disease, Humans, Immunologic Memory, Intestines, Phenotype, CD4-Positive T-Lymphocytes, Case-Control Studies, Receptors, Antigen, T-Cell, alpha-beta, CD4 Lymphocyte Count, Immunity, Mucosal, Interleukin-17, Host-Pathogen Interactions, Th17 Cells
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 ›
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