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TGFβ in the Context of an Inflammatory Cytokine Milieu Supports De Novo Differentiation of IL-17-Producing T Cells
Open accessAbstract
We describe de novo generation of IL-17-producing T cells from naive CD4 T cells, induced in cocultures of naive CD4 T cells and naturally occurring CD4+ CD25+ T cells (Treg) in the presence of TLR3, TLR4, or TLR9 stimuli. Treg can be substituted by TGFbeta1, which, together with the proinflammatory cytokine IL-6, supports the differentiation of IL-17-producing T cells, a process that is amplified by IL-1beta and TNFalpha. We could not detect a role for IL-23 in the differentiation of IL-17-producing T cells but confirmed its importance for their survival and expansion. Transcription factors GATA-3 and T-bet, as well as its target Hlx, are absent in IL-17-producing T cells, and they do not express the negative regulator for TGFbeta signaling, Smad7. Our data indicate that, in the presence of IL-6, TGFbeta1 subverts Th1 and Th2 differentiation for the generation of IL-17-producing T cells.
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“Here, we report that in addition to its key role in Th17 cell induction (3, 4), there is an absolute requirement for persistent IL-6 signaling to maintain the Th17 genetic program, and thus Th17 cells.”
From T H 17 cells require ongoing classic IL-6 receptor signaling to retain transcriptional and functional identity (2020) · cites this paper as [3]
In the citing paper
“IL-6 together with TGFβ induces Th17 cells (Fig. 2) (164).”
From IL-6 in inflammation, autoimmunity and cancer (2021) · cites this paper as [164]
In the citing paper
“The produced IL-6 further induces Th17 cell differentiation through STAT3 in the presence of TGFβ, IL-1β and IL-23, all of which are rich in inflammatory lesions and tumor microenvironments (164, 166, 169–171, 174, 175).”
From IL-6 in inflammation, autoimmunity and cancer (2021) · cites this paper as [164]
In the citing paper
“Th17 cells were established as an independent T helper cell subset with the discovery of signature cytokines IL-17A, IL-17F, and IL-22, lineage-specific differentiation factors, and dedicated or “master” transcription factors”
From TH17 cell heterogeneity and its role in tissue inflammation (2023) · cites this paper as [10]
In the citing paper
“In response to TGF-β in vitro as well as in vivo, many T cells co-express RORγt and Foxp3 (Veldhoen et al., 2006; Yang et al., 2008a).”
From Control of TH17/Treg Balance by Hypoxia-Inducible Factor 1 (2011) · cites this paper as Veldhoen et al., 2006
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Zheng, S. G., Wang, J., & Horwitz, D. A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.11.7112 · Cited by 363
Interleukin-6, a mental cytokine
Spooren, A., Kolmus, K., Laureys, G., Clinckers, R., De Keyser, J., Haegeman, G., & Gerlo, S. (2011) · Brain Research Reviews · doi:10.1016/j.brainresrev.2011.01.002 · Cited by 352
“IL-6 is crucial for the induction of Th17 cells (Bettelli et al., 2006; Veldhoen et al., 2006).”
BackgroundHeterogeneity of CD4+ memory T cells: Functional modules for tailored immunity
Sallusto, F., & Lanzavecchia, A. (2009) · European Journal of Immunology · doi:10.1002/eji.200939722 · Cited by 348
Hamada, S., Umemura, M., Shiono, T., Tanaka, K., Yahagi, A., Begum, M. D., Oshiro, K., Okamoto, Y., Watanabe, H., Kawakami, K., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.5.3456 · Cited by 364
Kimura, A., Naka, T., & Kishimoto, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705268104 · Cited by 363
T Helper Cell Differentiation, Heterogeneity, and PlasticityPreprint
Zhu, J. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a030338 · Cited by 374
“Together with IL-2-mediated STAT5 activation, TGF-β induces Treg differentiation; on the other hand, together with IL-6-mediated STAT3 activation, TGF-β induces Th17-cell differentiation (Bettelli et al. 2006; Veldhoen et al. 2006).”
BackgroundCharacterization of the interleukin-17 isoforms and receptors in lesional psoriatic skin
Johansen, C., Usher, P. A., Kjellerup, R. B., Lundsgaard, D., Iversen, L., & Kragballe, K. (2009) · British Journal of Dermatology · doi:10.1111/j.1365-2133.2008.08902.x · Cited by 352
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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 356
Alcorn, J. F., Crowe, C. R., & Kolls, J. K. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135926 · Cited by 357
Oxidative stress and inflammatory response in dermal toxicity of single-walled carbon nanotubes
Murray, A. R., Kisin, E. R., Leonard, S. S., Young, S., Kommineni, C., Kagan, V. E., Castranova, V., & Shvedova, A. A. (2008) · Toxicology · doi:10.1016/j.tox.2008.12.023 · Cited by 344
The Function and Role of the Th17/Treg Cell Balance in Inflammatory Bowel Disease
Yan, J., Luo, M., Chen, Z., & He, B. (2020) · Journal of Immunology Research · doi:10.1155/2020/8813558 · Cited by 365
Teitelbaum, D. H., & Coran, A. G. (2006) · CRC Press eBooks · doi:10.1201/b13237-67 · Cited by 341
Hovhannisyan, Z., Treatman, J. D., Littman, D. R., & Mayer, L. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.12.002 · Cited by 345
Differential regulation of interleukin 17 and interferon production in inflammatory bowel disease
Rovedatti, L., Kudo, T., Biancheri, P., Sarra, M., Knowles, C. H., Rampton, D. S., Corazza, G. R., Monteleone, G., Sabatino, A. D., & MacDonald, T. T. (2009) · Gut · doi:10.1136/gut.2009.182170 · Cited by 350
Contribution of IL-17–producing γδ T cells to the efficacy of anticancer chemotherapy
Ma, Y., Aymeric, L., Locher, C., Mattarollo, S. R., Delahaye, N. F., Pereira, P., Boucontet, L., Apétoh, L., Ghiringhelli, F., Casares, N., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20100269 · Cited by 356
Monin, L., & Gaffen, S. L. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028522 · Cited by 350
“…is a combination of IL-1b, IL-6, transforming growth factor b (TGF-b), and IL-21 for initial commitment (Bettelli et al. 2006; Mangan et al. 2006; Veldhoen et al. 2006; Zhou et al. 2007) and IL-23 for full acquisition of their pathogenic capacity (Cua et al. 2003; Awasthi et al. 2009; McGeachy…”
BackgroundNistala, K., Moncrieffe, H., Newton, K. R., Varsani, H., Hunter, P., & Wedderburn, L. R. (2008) · Arthritis & Rheumatism · doi:10.1002/art.23291 · Cited by 332
IL-27 Blocks RORc Expression to Inhibit Lineage Commitment of Th17 Cells
Diveu, C., McGeachy, M. J., Boniface, K., Stumhofer, J. S., Sathe, M., Joyce-Shaikh, B., Chen, Y., Tato, C. M., McClanahan, T. K., Malefyt, R. D. W., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0801162 · Cited by 346
Kreymborg, K., Etzensperger, R., Dumoutier, L., Haak, S., Rebollo, A., Buch, T., Heppner, F. L., Renauld, J., & Becher, B. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.12.8098 · Cited by 339
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Streptococcus pneumoniae: virulence factors and variation
Mitchell, A. M., & Mitchell, T. J. (2010) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2010.03183.x · Cited by 348
Selection of Self-Reactive T Cells in the Thymus
Stritesky, G. L., Jameson, S. C., & Hogquist, K. A. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-075035 · Cited by 350
IL-17 and Th17 cells in tuberculosis
Torrado, E., & Cooper, A. M. (2010) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2010.10.004 · Cited by 343
“TGF-b induces expression of foxp3 but further signaling by STAT-3-activating cytokines such as IL-6 promotes Th17 differentiation [24,25,84].”
BackgroundInterleukin-6: from an inflammatory marker to a target for inflammatory diseases
Rincón, M. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.07.003 · Cited by 339
Metadata
- Authors
- Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M., & Stockinger, B.
- Affiliations
- National Institute for Medical Research (GB)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Stockinger, Brigitta
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2006-02
- Volume
- 24
- Issue
- 2
- Pages
- 179-189
- ISSN
- 1074-7613 (ISSN-L)
- OpenAlex
- W2112866067
- Cited by
- 3,605
- References
- 70
- Citations by year
- 2026: 41 · 2025: 54 · 2024: 71 · 2023: 91 · 2022: 110 · 2021: 149 · 2020: 113 · 2019: 114 · 2018: 122 · 2017: 158 · 2016: 138 · 2015: 172 · 2014: 182 · 2013: 219 · 2012: 246
- FWCI
- 126.40
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (AI30663, R01AI030663)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- IL-17-producing T cells, TGF-β1, Th17 cell differentiation, regulatory T cells, interleukin-6, TLR3, TLR4, TLR9, IL-1β, TNF-α, IL-23, GATA3, T-bet, Smad7, Th1/Th2 differentiation, naive CD4+ T cells, inflammatory cytokines
- MeSH terms
- Animals, Cell Differentiation, Cells, Cultured, Dendritic Cells, Membrane Glycoproteins, Mice, Inbred C57BL, Mice, Transgenic, T-Lymphocytes, CD4-Positive T-Lymphocytes, Lymphocyte Subsets, Cytokines, Transforming Growth Factor beta, Receptors, Interleukin-1, Mice, Knockout, Th1 Cells, Th2 Cells, Interleukin-17, T-Lymphocytes, Regulatory, Mice, Smad7 Protein, Transforming Growth Factor beta1
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