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The encephalitogenicity of TH17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF
Open accessAbstract
Interleukin 17 (IL-17)-producing helper T cells (T(H)17 cells) require exposure to IL-23 to become encephalitogenic, but the mechanism by which IL-23 promotes their pathogenicity is not known. Here we found that IL-23 induced production of the cytokine granulocyte-macrophage colony-stimulating factor (GM-CSF) in T(H)17 cells and that GM-CSF had an essential role in their encephalitogenicity. Our findings identify a chief mechanism that underlies the important role of IL-23 in autoimmune diseases. IL-23 induced a positive feedback loop whereby GM-CSF secreted by T(H)17 cells stimulated the production of IL-23 by antigen-presenting cells. Such cross-regulation of IL-23 and GM-CSF explains the similar pattern of resistance to autoimmunity when either of the two cytokines is absent and identifies T(H)17 cells as a crucial source of GM-CSF in autoimmune inflammation.
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“and to promote the production of effector molecules (El-Behi et al., 2011).”
From Distinct characteristics of hippocampal pathogenic th17 cells in a mouse model of depression (2018) · cites this paper as El-Behi et al., 2011
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“Is it important to highlight that GM-CSF production in T lymphocytes is driven by IL-23, which is secreted by antigen presenting cells (APCs) (32), binds to IL-23R and enables GMCSF secretion by T cells (33–35), highlighting the importance of the iron/IL-17/IL-23/GM-CSF axis in the pathogenesis of autoimmune disorders.”
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BackgroundLithium Controls Central Nervous System Autoimmunity through Modulation of IFN-γ Signaling
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BackgroundMast cell inflammasome activity in the meninges regulates EAE disease severity
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“For example: GM-CSF derives from T cells and promotes dendritic cell recruitment [20, 21],”
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“However, studies by El-Behi et al.11 and Codarri et al.12 showed GM-CSF to be critical in the pathogenicity of Th17 cells during EAE.”
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CCAAT/Enhancer-binding protein β promotes pathogenesis of EAE
Simpson-Abelson, M. R., Hernández-Mir, G., Childs, E. E., Cruz, J. A., Poholek, A. C., Chattopadhyay, A., Gaffen, S. L., & McGeachy, M. J. (2017) · Cytokine · doi:10.1016/j.cyto.2017.01.005 · Cited by 44
He, Z.-H., Wang, F., Ma, J., Sen, S., Zhang, J., Gwack, Y., Zhou, Y., & Sun, Z.-M. (2016) · Journal of Immunology · doi:10.4049/jimmunol.1600548 · Cited by 38
“Conversely, effective prevention of Th17-mediated autoimmune diseases, such as multiple sclerosis and psoriasis, depends on inhibiting Th17 differentiation (4, 17, 18, 21, 47).”
BackgroundDopamine favors expansion of glucocorticoid-resistant IL-17-producing T cells in multiple sclerosis
Ferreira, T. B., Barros, P. O., Teixeira, B., Cassano, T., Centurião, N., Kasahara, T. M., Hygino, J., Vasconcelos, C. C. F., Filho, H. A., Alvarenga, R. M. P., et al. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.05.013 · Cited by 41
Computational modeling of heterogeneity and function of CD4+ T cells
Carbo, A., Hontecillas, R., Andrew, T., Eden, K. B., Mei, Y., Hoops, S., & Bassaganya-Riera, J. (2014) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2014.00031 · Cited by 43
“…provide a mechanisms through which Tregs cells reinforce the epithelial barrier (Lin et al., 2014), this same Th17 population can accumulate and produce additional mediators such as IFN γ or GM-CSF during gut inflammatory disorders (Ahern et al., 2010; Codarri et al., 2011; El-Behi et al., 2011).”
BackgroundThe essential role of t cells in multiple sclerosis: A reappraisal
Constantinescu, C. S., & Gran, B. (2014) · Biomedical Journal · doi:10.4103/2319-4170.128746 · Cited by 36
Th1 not Th17 cells drive spontaneous MS-like disease despite a functional regulatory T cell response
Lowther, D. E., Chong, D. L. W., Ascough, S., Ettorre, A., Ingram, R. J., Boyton, R. J., & Altmann, D. M. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1159-9 · Cited by 40
Dong, W., & Zhu, P. (2012) · Autoimmunity Reviews · doi:10.1016/j.autrev.2012.02.019 · Cited by 35
The Dynamic Duo–Inflammatory M1 macrophages and Th17 cells in Rheumatic Diseases
Li, J. (2013) · Journal of Orthopedics & Rheumatology · doi:10.13188/2334-2846.1000002 · Cited by 37
“Therefore, the co-existence of IL-23 producing M1 macrophages and GM-CSF producing Th1/17 T cells forms a positive interactive inflammatory positive feedback circuit that is associated with the highest levels of inflammation in autoimmune disease including RA [12], multiple sclerosis (MS) [11], and possibly, Systemic…”
BackgroundImmunopathogenesis and distinct role of Th17 in periodontitis: A review
Kini, V. V., Mohanty, I. R., Telang, G., & Vyas, N. (2022) · Journal of Oral Biosciences · doi:10.1016/j.job.2022.04.005 · Cited by 40
TH Cells and Cytokines in Encephalitogenic Disorders
Krishnarajah, S., & Becher, B. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.822919 · Cited by 49
Nanjappa, S. G., McDermott, A. J., Fites, J. S., Galles, K., Wüthrich, M., Deepe, G. S., & Klein, B. S. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006356 · Cited by 42
Increased CD8+ T cell responses to apoptotic T cell-associated antigens in multiple sclerosis
Lolli, F., Martini, H., Citro, A., Franceschini, D., Portaccio, E., Amato, M. P., Mechelli, R., Annibali, V., Sidney, J., Sette, A., et al. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-94 · Cited by 36
“; licensee BioMed Central Ltd Commons Attribution License (http://creativec reproduction in any medium, provided the or IL-17 produced by CD4 or CD8 T cells specific to myelin proteins (likely in response to IL-23 and granulocyte monocyte-colony stimulating factor, GM-CSF) plays a preponderant role in the autoimmune d…”
BackgroundGuo, X., Higgs, B., Bay-Jensen, A., Wu, Y.-L., Karsdal, M., Kuziora, M., Godwood, A., Close, D., Ryan, P. C., Roskos, L., et al. (2018) · Rheumatology · doi:10.1093/rheumatology/kex383 · Cited by 37
Liu, Y., Gibson, S. A., Benveniste, E. N., & Qin, H. (2015) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.2016015517 · Cited by 43
Novel immune cell phenotypes in spondyloarthritis pathogenesis
Mauro, D., Simone, D., Bucci, L., & Ciccia, F. (2021) · Seminars in Immunopathology · doi:10.1007/s00281-021-00837-0 · Cited by 47
“One feature of pathogenicity described so far is the co-expression of inflammatory cytokines such as IFN-γ and GM-CSF [45].”
BackgroundTranscriptional regulation of CD4+ TH cells that mediate tissue inflammation
Loo, T. T., Gao, Y., & Lazarevic, V. (2018) · Journal of Leukocyte Biology · doi:10.1002/jlb.1ri0418-152rr · Cited by 43
Li, X., Li, Z., Han, J., Zhang, F., Liu, S., Zhu, L. D., Wang, Z., Zhang, G., & Zhang, Y. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01807 · Cited by 41
“org August 2018 | Volume 9 | Article 1807 (5, 6).”
Self-citationCytokine Regulation in Human CD4 T Cells by the Aryl Hydrocarbon Receptor and Gq-Coupled Receptors
McAleer, J. P., Fan, J., Roar, B., Primerano, D. A., & Denvir, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-29262-4 · Cited by 37
BATF-dependent IL-7RhiGM-CSF+ T cells control intestinal graft-versus-host disease
Ullrich, E., Abendroth, B., Rothamer, J., Huber, C., Büttner-Herold, M., Buchele, V., Vogler, T., Longerich, T., Zundler, S., Völkl, S., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci89242 · Cited by 36
Dohlman, T. H., Ding, J. X., Dana, R., & Chauhan, S. K. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.16-20789 · Cited by 38
Targeting Th17 Effector Cytokines for the Treatment of Autoimmune Diseases
Yamagata, T., Skepner, J. E., & Yang, J. (2015) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-015-0362-x · Cited by 37
“Recent studies reported that GM-CSF is critical for the pathogenicity of Th17 cells (Codarri et al. 2011; El-Behi et al. 2011).”
Harnessing the Therapeutic Potential of Th17 Cells
Byström, J., Taher, T. E. I., Muhyaddin, M. S., Clanchy, F. I. L., Mangat, P., Jawad, A. S., Williams, R. O., & Mageed, R. A. (2015) · Mediators of Inflammation · doi:10.1155/2015/205156 · Cited by 41
The role of Th17-associated cytokines in the pathogenesis of experimental autoimmune uveitis (EAU)
Sun, D., Liang, D., Kaplan, H. J., & Shao, H. (2015) · Cytokine · doi:10.1016/j.cyto.2014.12.017 · Cited by 36
“IL-23 induced production of the cytokine GM-CSF in Th17 cells, and GM-CSF had an essential role in their encephalitogenicity [77].”
Lin, M.-H., Yeh, L., Chen, S., Chiou, H.-Y. C., Chu, C., Yen, L. B., Lin, K., Chang, D., & Sytwu, H. (2014) · Clinical Immunology · doi:10.1016/j.clim.2014.02.006 · Cited by 34
NF-κB Activation in T Helper 17 Cell Differentiation
Park, S., Cho, G., & Park, S. (2014) · Immune Network · doi:10.4110/in.2014.14.1.14 · Cited by 37
“The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF.”
Vitamin B5 rewires Th17 cell metabolism via impeding PKM2 nuclear translocation
Chen, C., Zhang, W., Zhou, T., Liu, Q., Han, C., Huang, Z., Chen, S., Mei, Q., Zhang, C., Zhang, K., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111741 · Cited by 50
Imitola, J., Rasouli, J., Watanabe, F., Mahajan, K., Sharan, A. D., Ćirić, B., Zhang, G., & Rostami, A. M. (2017) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2017.12.017 · Cited by 38
Self-citationMedium-dose estrogen ameliorates experimental autoimmune encephalomyelitis in ovariectomized mice
Haghmorad, D., Salehipour, Z., Nosratabadi, R., Rastin, M., Kokhaei, P., Mahmoudi, M., Amini, A., & Mahmoudi, M. (2016) · Journal of Immunotoxicology · doi:10.1080/1547691x.2016.1223768 · Cited by 35
Defining the functional states of Th17 cells
Lee, Y., & Kuchroo, V. K. (2015) · F1000Research · doi:10.12688/f1000research.6116.1 · Cited by 32
Verinaud, L., Lopes, S. C., Prado, I., Zanucoli, F., da Costa, T. A., Gangi, R. D., Issayama, L. K., Carvalho, A. C., Bonfanti, A., Niederauer, G. F., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125409 · Cited by 35
“It is known that following MOG-immunization, encephalitogenic T cells migrate towards the CNS after 10 days, where they promote inflammation [10, 41, 42].”
BackgroundHuang, G., Wang, Y., Vogel, P., & Chi, H. (2015) · Science Signaling · doi:10.1126/scisignal.aaa2147 · Cited by 37
“In particular, GM-CSF produced by TH17 cells is a key stimulator of the encephalitogenic program (5, 6).”
Mangalam, A. K., Luo, N., Luckey, D. H., Papke, L. M., Hubbard, A., Wussow, A., Smart, M. K., Giri, S., Rodriguez, M., & David, C. S. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302008 · Cited by 39
“GM-CSF are more encephalitogenic than single IL-17 or GMCSF cells (33).”
BackgroundThe tyrosine phosphatase SHP-1 dampens murine Th17 development
Mauldin, I. S., Tung, K. S. K., & Lorenz, U. M. (2012) · Blood · doi:10.1182/blood-2011-09-377069 · Cited by 36
Nur, S., Sparber, F., Lemberg, C., Guiducci, E., Schweizer, T. A., Zwicky, P., Becher, B., & LeibundGut‐Landmann, S. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1008115 · Cited by 38
“and acanthosis [19] and that IL-23 can drive GM-CSF production, which is essential for the induction of EAE [16,17].”
BackgroundWei, Y., Chen, S., Sun, D., Li, X., Wei, R., Li, X., & Nian, H. (2019) · The FASEB Journal · doi:10.1096/fj.201901446r · Cited by 36
“KEY WORDS: IL-23 • pathogenic Th17 cells • IL-23R • GM-CSF • IL-22 T helper (Th)17 cells are critically involved in the pathogenesis of various autoimmune disorders, including uveitis and its animal model, experimental autoimmune uveitis (EAU) (1–3).”
BackgroundInfluentialMangalam, A. K., Rattan, R., Suhail, H., Singh, J., Hoda, M. N., Deshpande, M., Fulzele, S., Đenić, A., Shridhar, V., Kumar, A., et al. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501549 · Cited by 34
“Our data are in agreement with recent studies showing the key pathological role of GM-CSF for both Th1- and Th17-mediated demyelinating disease (33, 45, 46).”
BackgroundMethodResultTbet or Continued RORγt Expression Is Not Required for Th17-Associated Immunopathology
Brucklacher-Waldert, V., Ferreira, C., Innocentin, S., Kamdar, S., Withers, D. R., Kullberg, M. C., & Veldhoen, M. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600137 · Cited by 30
“Because GM-CSF has been shown to be necessary for the development of EAE (46, 59, 60), the alteration of T cell populations producing GM-CSF/TNF in combination with IL-17 or IFN-g may not significantly impact on immunopathology.”
BackgroundThe Role of IL-23 in the Development of Inflammatory Diseases
García‐Domínguez, M. (2025) · Biology · doi:10.3390/biology14040347 · Cited by 27
“…experimental autoimmune encephalomyelitis (EAE), the most commonly used experimental model for human inflammatory demyelinating disease, including MS [99], IL-23 stimulates myelin-reactive T cells to produce both IFN-γ and IL-17, contributing to the generation of encephalitogenic Th17 cells [100].”
Autoimmunity as a target for chimeric immune receptor therapy: A new vision to therapeutic potential
Haddadi, M. H., Hajizadeh‐Saffar, E., Maharlooei, M. K., Basiri, M., Negahdari, B., & Baharvand, H. (2019) · Blood Reviews · doi:10.1016/j.blre.2019.100645 · Cited by 34
Deleterious versus protective autoimmunity in multiple sclerosis
Kostić, M. S., Stojanović, I. R., Marjanović, G., Živković, N., & Cvetanović, A. (2015) · Cellular Immunology · doi:10.1016/j.cellimm.2015.04.006 · Cited by 30
Oral zinc aspartate treats experimental autoimmune encephalomyelitis
Schubert, C., Guttek, K., Grüngreiff, K., Thielitz, A., Bühling, F., Reinhold, A., Brocke, S., & Reinhold, D. (2014) · BioMetals · doi:10.1007/s10534-014-9786-8 · Cited by 33
“Key pathogenic roles in this process were attributed to the Th1 cytokine IFN-c, the Th17 cytokine IL-17 and GM-CSF (Codarri et al. 2011; El-Behi et al. 2011).”
BackgroundInfluentialJiao, Z., Bedoui, S., Brady, J. L., Walter, A., Chopin, M., Carrington, E. M., Sutherland, R. M., Nutt, S. L., Zhang, Y., Ko, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091126 · Cited by 32
“Several recent publications suggest that GM-CSF derived from Th17 cells is critical for inflammation and pathology [50–52].”
Background
Metadata
- Authors
- El-Behi, M., Ciric, B., Dai, H., Yan, Y., Cullimore, M., Safavi, F., Zhang, G.-X., Dittel, B. N., & Rostami, A.
- Affiliations
- Thomas Jefferson University (US)
- Versiti Blood Center of Wisconsin (US)
- Corresponding author
- Rostami, Abdolmohamad
- ORCID
- Venue
- Nature Immunology
- Published
- 2011-04-24
- Volume
- 12
- Issue
- 6
- Pages
- 568-575
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC3116521
- OpenAlex
- W2084388036
- Cited by
- 1,071
- References
- 44
- Citations by year
- 2026: 25 · 2025: 38 · 2024: 38 · 2023: 58 · 2022: 62 · 2021: 72 · 2020: 82 · 2019: 71 · 2018: 74 · 2017: 96 · 2016: 82 · 2015: 108 · 2014: 91 · 2013: 80 · 2012: 73
- FWCI
- 37.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Multiple Sclerosis Society
- Mary E. Groff Surgical and Medical Research and Education Charitable Trust
- National Institute of Neurological Disorders and Stroke (R01NS046782)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Keywords
- Th17 cells, experimental autoimmune encephalomyelitis, IL-23, GM-CSF, interleukin-1, encephalitogenicity, autoimmune disease, antigen-presenting cells, positive feedback loop, T helper cells
- MeSH terms
- Animals, Antibodies, Cells, Cultured, Encephalomyelitis, Autoimmune, Experimental, Female, Flow Cytometry, Glycoproteins, Interleukin-1, Mice, Inbred C57BL, Mice, Transgenic, Peptide Fragments, CD4-Positive T-Lymphocytes, Granulocyte-Macrophage Colony-Stimulating Factor, Transforming Growth Factor beta, Mice, Knockout, Th1 Cells, Coculture Techniques, CD11c Antigen, Mice, Interleukin-1beta, Interleukin-23, Nuclear Receptor Subfamily 1, Group F, Member 3, Th17 Cells, Myelin-Oligodendrocyte Glycoprotein
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