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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IL-23 is required to promote the production of effector molecules.
“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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Roy, D. G., Chen, J., Mamane, V. H., Ma, E. H., Muhire, B. M., Sheldon, R. D., Shorstova, T., Koning, R., Johnson, R. M., Esaulova, E., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.01.006 · Cited by 347 · see citing works
B and T Cells Driving Multiple Sclerosis: Identity, Mechanisms and Potential Triggers
van Langelaar, J., Rijvers, L., Smolders, J., & van Luijn, M. M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00760 · Cited by 328 · see citing works
“Such subsets are characterized by master transcription factors T-bet and RORγt (73, 74), of which the latter is involved in the coexpression of IL-17 and GM-CSF in mice but not in humans (75, 76).”
BackgroundEffector T Cells in Multiple SclerosisPreprint
Kaskow, B. J., & Baecher‐Allan, C. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029025 · Cited by 314 · see citing works
“The secretion of GM-CSF by Th17 cells may play a fundamental role in activating CNSmyeloid cells (microglia,macrophages, and dendritic cells) as GM-CSF-deficient Th17 cells are unable to induce EAE (El-Behi et al. 2011).”
BackgroundInfluentialRecent advances in the IL-17 cytokine family
Gaffen, S. L. (2011) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.07.006 · Cited by 283 · see citing works
“Recent findings indicate that GM-CSF is another Th17-derived cytokine that contributes to the inflammatory pathology of Th17 cells, based on data from EAE models [2,3].”
Hamilton, J. A. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190945 · Cited by 310 · see citing works
Colony stimulating factors and myeloid cell biology in health and disease
Hamilton, J. A., & Achuthan, A. (2013) · Trends in Immunology · doi:10.1016/j.it.2012.08.006 · Cited by 285 · see citing works
Mease, P. J., Rahman, P., Gottlieb, A. B., Kollmeier, A. P., Hsia, E. C., Xu, X. L., Sheng, S., Agarwal, P., Zhou, B., Zhuang, Y., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30263-4 · Cited by 358 · see citing works
The IL-1β phenomena in neuroinflammatory diseases
Mendiola, A. S., & Cardona, A. E. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1732-9 · Cited by 311 · see citing works
“Further EAE studies identified a critical role of IL1b and IL-23 in regulating the production of Th17-derived GM-CSF (transcribed from Csf2), a non-redundant cyto- kine required for T cells to become encephalitogenic (Codarri et al. 2011; El-Behi et al. 2011; Mufazalov et al. 2016).”
BackgroundPlasticity of Human CD4 T Cell Subsets
Geginat, J., Paroni, M., Maglie, S., Alfen, J. S., Kastirr, I., Gruarin, P., Simone, M. C. D., Pagani, M., & Abrignani, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00630 · Cited by 289 · see citing works
“A particular relevant cytokine in the pathogenesis of experimental autoimmunity is GM-CSF, which is induced by IL-1β, IL-23, and ROR-γt in mice (102, 129).”
BackgroundCao, Y., Goods, B. A., Raddassi, K., Nepom, G. T., Kwok, W. W., Love, J. C., & Hafler, D. A. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa8038 · Cited by 290 · see citing works
“Recently, it was shown that GM-CSF plays a pathogenic role in EAE pathology (14, 15).”
Role of Th17 cells in the pathogenesis of CNS inflammatory demyelination
Rostami, A. M., & Ćirić, B. (2013) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2013.03.002 · Cited by 275 · see citing works
“In a co-culture of purified CD4+ T cells and APCs of MOGimmunized mice IL-12Rβ1−/− APCs drove CD4+ T cells of both WT and IL-12Rβ1−/− mice toward Th2 lineage, whereas WT APCs induced Th1 lineage.”
BackgroundResultInfluentialSelf-citationT cell responses in the central nervous system
Korn, T., & Kallies, A. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.144 · Cited by 268 · see citing works
PI3K inhibitors in inflammation, autoimmunity and cancer
Stark, A., Sriskantharajah, S., Hessel, E., & Okkenhaug, K. (2015) · Current opinion in pharmacology (Print) · doi:10.1016/j.coph.2015.05.017 · Cited by 266 · see citing works
“EAE progression is mainly driven by Th17 mediated inflammation of the CNS leading to the destruction of myelin, with antigen presenting cells (APC) playing a key role in the amplification of inflammation [37].”
BackgroundMacrophage subsets and microglia in multiple sclerosis
Bogie, J. F. J., Stinissen, P., & Hendriks, J. J. A. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1310-2 · Cited by 279 · see citing works
Qin, H., Yeh, W.-I., Sarno, P. D., Holdbrooks, A. T., Liu, Y., Muldowney, M., Reynolds, S. L., Yanagisawa, L. L., Fox, T. H., Park, K., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1117218109 · Cited by 266 · see citing works
“Th1 cells in turn produce IFN-γ and GM-CSF, whereas Th17 cells produce GMCSF (32, 33), which will sustain the M1 phenotype, establishing a feed-forward regulatory loop for M1, Th1, and Th17 cells.”
BackgroundPKM2 promotes Th17 cell differentiation and autoimmune inflammation by fine-tuning STAT3 activation
Damasceno, L. E. A., Prado, D. D. S., Veras, F. P., Fonseca, M. M., Toller-Kawahisa, J. E., Rosa, M. H., Públio, G. A., Martins, T. V., Ramalho, F. S., Waisman, A., et al. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20190613 · Cited by 289 · see citing works
Targeting GM-CSF in inflammatory diseases
Wicks, I. P., & Roberts, A. W. (2015) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2015.161 · Cited by 261 · see citing works
Laoui, D., Keirsse, J., Morias, Y., van Overmeire, E., Geeraerts, X., Elkrim, Y., Kiss, M., Bolli, E., Lahmar, Q., Sichien, D., et al. (2016) · Nature Communications · doi:10.1038/ncomms13720 · Cited by 255 · see citing works
McGinley, A. M., Sutton, C. E., Edwards, S. C., Leane, C. M., DeCourcey, J., Teijeiro, A., Hamilton, J. A., Boon, L., Djouder, N., & Mills, K. H. G. (2020) · Immunity · doi:10.1016/j.immuni.2020.01.002 · Cited by 248 · see citing works
Peters, A., Lee, Y., & Kuchroo, V. K. (2011) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.08.007 · Cited by 232 · see citing works
IL-17 and Th17 Cells in Atherosclerosis
Taleb, S., Tedgui, A., & Mallat, Z. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.303567 · Cited by 263 · see citing works
Th17 Response and Inflammatory Autoimmune Diseases
Waite, J. C., & Skokos, D. (2011) · International Journal of Inflammation · doi:10.1155/2012/819467 · Cited by 239 · see citing works
“Although GM-CSF expression is not required for Th17 differentiation, a recent study showed that this cytokine is required for autoimmune neuroinflammation via myeloid cells (CD45hi, CD11b+) infiltrating the central nervous system during the effector phase of the response [30, 31].”
BackgroundInterleukin-17 in chronic inflammatory neurological diseases
Milovanovic, J., Arsenijevic, A., Stojanovic, B., Kanjevac, T., Arsenijevic, D., Radosavljevic, G., Milovanovic, M., & Arsenijevic, N. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00947 · Cited by 250 · see citing works
“Findings indicating that GM-CSF has the key role in the encephalitogenic potential of Th17 cells in mice (74, 170, 171), specifically, increased levels of GM-CSF in the cerebrospinal fluid and serum of active MS patients with the relapsing-remitting type of the disease and increased secretion of GM-CSF from T cells is…”
BackgroundInfluentialIL-17 and GM-CSF Expression Are Antagonistically Regulated by Human T Helper Cells
Noster, R., Riedel, R., Mashreghi, M., Radbruch, H., Harms, L., Haftmann, C., Chang, H., Radbruch, A., & Zielinski, C. E. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3008706 · Cited by 231 · see citing works
“Because TH cell subsets can traditionally be distinguished on the basis of their master transcription factors, we isolated in vivo primed TH1, TH2, and TH17 clones and also TH clones that produced GMCSF but were negative for IFN-g, IL-17, and IL-4 expression, and analyzed transcript levels of T-bet, GATA-3, and ROR-gt…”
BackgroundResultInfluentialExperimental Autoimmune Encephalomyelitis (EAE) as Animal Models of Multiple Sclerosis (MS)
Glatigny, S., & Bettelli, E. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a028977 · Cited by 247 · see citing works
“Interestingly, IL-23 was also shown to induce the expression of GM-CSF in CD4+ T cells (Codarri et al. 2011; El-Behi et al. 2011).”
BackgroundDual Role of GM-CSF as a Pro-Inflammatory and a Regulatory Cytokine: Implications for Immune Therapy
Bhattacharya, P., Budnick, I., Singh, M., Thiruppathi, M., Alharshawi, K., Elshabrawy, H. A., Holterman, M., & Prabhakar, B. S. (2015) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2014.0149 · Cited by 264 · see citing works
Toll-like receptor 4 signaling in T cells promotes autoimmune inflammation
Reynolds, J., Martinez, G., Chung, Y., & Dong, C. (2012) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1120585109 · Cited by 237 · see citing works
“Recent work has shown that IL-23-driven production of GMCSF by Th17 cells is critical for the development of EAE (23, 24).”
BackgroundBroughton, S. E., Dhagat, U., Hercus, T. R., Nero, T. L., Grimbaldeston, M. A., Bonder, C. S., Lopez, A. F., & Parker, M. W. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01164.x · Cited by 230 · see citing works
“and adaptive immune responses to infection (6, 29, 30) and inflammatory diseases (9, 31), such as asthma (32–34), rheumatoid arthritis (35–37), multiple sclerosis (38, 39), and autoimmune glomerulonephritis (40, 41).”
BackgroundMicroRNA-21 promotes Th17 differentiation and mediates experimental autoimmune encephalomyelitis
Murugaiyan, G., da Cunha, A. P., Ajay, A. K., Joller, N., Garo, L. P., Kumaradevan, S., Yosef, N., Vaidya, V. S., & Weiner, H. L. (2015) · Journal of Clinical Investigation · doi:10.1172/jci74347 · Cited by 239 · see citing works
“In fact, Th1 cells that lack the ability to produce GM-CSF do not transfer EAE (42).”
Cardiac myosin-Th17 responses promote heart failure in human myocarditis
Myers, J. M., Cooper, L. T., Kem, D. C., Stavrakis, S., Kosanke, S. D., Shevach, E. M., Fairweather, D., Stoner, J. A., Cox, C. J., & Cunningham, M. W. (2016) · JCI Insight · doi:10.1172/jci.insight.85851 · Cited by 230 · see citing works
“Given that IL-23 promotes inflammation through GM-CSF secretion from Th17 cells (52, 53), we determined if IL-23, GM-CSF, and GM-CSF lymphocytes were elevated in myocarditis/DCM.”
The Th17 family: flexibility follows function
Basu, R., Hatton, R. D., & Weaver, C. T. (2013) · Immunological Reviews · doi:10.1111/imr.12035 · Cited by 229 · see citing works
“In the thymus, nTregs undergo demethylation of an upstream cis-regulatory element (Foxp3 CNS2) that is bound by Foxp3 in a Runx1- and Cbf-b-dependent manner to establish a positive feedback loop that stabilizes Foxp3 expression.”
BackgroundInfluentialPouring fuel on the fire: Th17 cells, the environment, and autoimmunity
Burkett, P. R., zu Hörste, G. M., & Kuchroo, V. K. (2015) · Journal of Clinical Investigation · doi:10.1172/jci78085 · Cited by 221 · see citing works
“Additionally, the IL-23R–mediated induction of the cytokine GM-CSF is required for the pathogenicity of Th17 cells, although by itself it is not sufficient to induce EAE in vivo (56, 57).”
BackgroundNeutrophils Mediate Blood–Spinal Cord Barrier Disruption in Demyelinating Neuroinflammatory Diseases
Aubé, B., Lévesque, S. A., Paré, A., Chamma, É., Kébir, H., Gorina, R., Lécuyer, M., Alvarez, J. I., Koninck, Y. D., Engelhardt, B., et al. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400401 · Cited by 229 · see citing works
Fructose and hepatic insulin resistance
Softic, S., Stanhope, K. L., Boucher, J., Divanovic, S., Lanaspa, M. A., Johnson, R. J., & Kahn, C. R. (2020) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408363.2019.1711360 · Cited by 255 · see citing works
“helper cell polarization and promote skewing of naive CD4þ T cells into Th17 subset [101,102].”
BackgroundCD 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
“El-Behi M, et al. The encephalitogenicity of T(H) 17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF.”
BackgroundInfluentialILC3 GM-CSF production and mobilisation orchestrate acute intestinal inflammation
Pearson, C., Thornton, E., McKenzie, B., Schaupp, A., Huskens, N., Griseri, T., West, N., Tung, S., Seddon, B., Uhlig, H., et al. (2016) · eLife · doi:10.7554/elife.10066 · Cited by 218 · see citing works
Th17 cell development: from the cradle to the grave
Zuniga, L. A., JAIN, R. K., Haines, C., & Cua, D. J. (2013) · Immunological Reviews · doi:10.1111/imr.12036 · Cited by 218 · see citing works
“This work was followed by two important studies that identified GM-CSF as an essential factor induced by IL-23 to regulate pathogenic function of Th17 cells (45, 46).”
BackgroundCholesterol Accumulation in Dendritic Cells Links the Inflammasome to Acquired Immunity
Westerterp, M., Gautier, E. L., Ganda, A., Molusky, M. M., Wang, W., Fotakis, P., Wang, N., Randolph, G. J., D'Agati, V. D., Yvan-Charvet, L., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.04.005 · Cited by 218 · see citing works
“Previous studies have suggested that GMCSF induces the secretion of these cytokines by DCs (Codarri et al., 2011; El-Behi et al., 2011; Sonderegger et al., 2008), linking GM-CSF signaling with autoimmunity.”
BackgroundInfluentialvan Langelaar, J., de Vries, R. M. V. D. V., Janssen, M., Wierenga‐Wolf, A. F., Spilt, I. M., Siepman, T. A. M., Dankers, W., Verjans, G. M. G. M., de Vries, H. E., Lubberts, E., et al. (2018) · Brain · doi:10.1093/brain/awy069 · Cited by 224 · see citing works
“Th17 polyfunctionality is differently regulated between species, as reflected by the antagonistic regulation of IL-17 and GM-CSF expression in human compared to murine T helper cells (El-Behi et al., 2011; Noster et al., 2014; Paterka et al., 2016).”
BackgroundRoles of GM-CSF in the Pathogenesis of Autoimmune Diseases: An Update
Lotfi, N., Thomé, R., Rezaei, N., Zhang, G., Rezaei, A., Rostami, A. M., & Esmaeil, N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01265 · Cited by 229 · see citing works
“It was later shown that GM-CSF secreted by Th17 cells is the main cytokine contributing to encephalitogenicity (62).”
BackgroundSelf-citationImmunological mechanisms and therapeutic targets of fatty liver diseases
Wang, H., Mehal, W. Z., Nagy, L. E., & Rotman, Y. (2020) · Cellular and Molecular Immunology · doi:10.1038/s41423-020-00579-3 · Cited by 222 · see citing works
Helminth Immunomodulation in Autoimmune Disease
Smallwood, T., Giacomin, P., Loukas, A., Mulvenna, J., Clark, R. J., & Miles, J. J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00453 · Cited by 208 · see citing works
Gut Microbiota, Immunity, and Disease: A Complex Relationship
Kosiewicz, M. M., Zirnheld, A. L., & Alard, P. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00180 · Cited by 205 · see citing works
“…appears to induce Th17 or RORγt+ T cells to produce GM-CSF that is required for disease induction; this was demonstrated in experiments showing that GM-CSF-producing IL-17-deficient T cells, but not GM-CSF-deficient Th17 cells, were able to induce EAE (Codarri et al., 2011; El-Behi et al., 2011).”
BackgroundInfluentialSheng, W., Yang, F., Zhou, Y., Yang, H., Low, P. Y., Kemeny, D. M., Tan, P., Moh, A., Kaplan, M. H., Zhang, Y., et al. (2014) · Cell Research · doi:10.1038/cr.2014.154 · Cited by 203 · see citing works
Pivotal Roles of GM‐CSF in Autoimmunity and Inflammation
Shiomi, A., & Usui, T. (2015) · Mediators of Inflammation · doi:10.1155/2015/568543 · Cited by 200 · see citing works
Cytokines IL-17 and IL-22 in the host response to infection
Valeri, M., & Raffatellu, M. (2016) · Pathogens and Disease · doi:10.1093/femspd/ftw111 · Cited by 202 · see citing works
“2011 ) and a regulatory subset that produces IL-10 (Esplugues et al.”
BackgroundKomuczki, J., Tuzlak, S., Friebel, E., Hartwig, T., Spath, S., Rosenstiel, P., Waisman, A., Opitz, L., Oukka, M., Schreiner, B., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.04.006 · Cited by 201 · see citing works
Multiple sclerosis: Neuroimmune crosstalk and therapeutic targeting
Charabati, M., Wheeler, M. A., Weiner, H. L., & Quintana, F. J. (2023) · Cell · doi:10.1016/j.cell.2023.03.008 · Cited by 229 · see citing works
Regulation of the T Cell Response by CD39
Takenaka, M. C., Robson, S. C., & Quintana, F. J. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.04.009 · Cited by 203 · see citing works
“GM-CSF, for example, is expressed by pathogenic Th17 cells (74, 75).”
BackgroundGriseri, T., McKenzie, B. S., Schiering, C., & Powrie, F. M. (2012) · Immunity · doi:10.1016/j.immuni.2012.08.025 · Cited by 197 · see citing works
“Indeed, GM-CSF enhances IL-23 production by antigen-presenting cells in vitro (El-Behi et al., 2011).”
BackgroundThe Common Cytokine Receptor γ Chain Family of CytokinesPreprint
Lin, J., & Leonard, W. J. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028449 · Cited by 210 · see citing works
“…TGF-β (McGeachy et al. 2007), whereas pathogenic Th17 cells are generated when proinflammatory IL-23 is additionally present, thereby inhibiting Th17 cells from producing IL-10 and up-regulating granulocyte macrophage colony-stimulating factor (GM-CSF) (Codarri et al. 2011; El-Behi et al. 2011).”
BackgroundMyeloid Colony-Stimulating Factors as Regulators of Macrophage Polarization
Hamilton, T. A., Zhao, C., Pavicic, P. G., & Datta, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00554 · Cited by 194 · see citing works
“Particularly, T-cell derived GM-CSF was recently shown to be critical for disease phenotype in experimental autoimmune encephalomyelitis, generated by IL-23 action on Th17 cells (60, 61).”
BackgroundCurrent concepts of severe asthma.
Ray, A., Raundhal, M., Oriss, T., Ray, P., & Wenzel, S. (2016) · Journal of Clinical Investigation · doi:10.1172/jci84144 · Cited by 191 · see citing works
Akdiş, M., Palomares, Ó., van de Veen, W., van Splunter, M. E., & Akdiş, C. A. (2012) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2012.05.003 · Cited by 191 · see citing works
Cutting Edge: The Pathogenicity of IFN-γ–Producing Th17 Cells Is Independent of T-bet
Duhen, R., Glatigny, S., Arbelaez, C. A., Blair, T. C., Oukka, M., & Bettelli, E. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1203172 · Cited by 169 · see citing works
Bandukwala, H. S., Gagnon, J. D., Togher, S., Greenbaum, J., Lamperti, E. D., Parr, N. J., Molesworth, A. M. H., Smithers, N. N., Lee, K. C., Witherington, J. J., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1212264109 · Cited by 182 · see citing works
“One explanation stems from the fact that this adoptive transfer model has a strong requirement for the cytokine GM-CSF (11, 14) in addition to the well-established proinflammatory cytokines, IFN-γ and IL-17 (20, 21).”
BackgroundResultModeling the heterogeneity of multiple sclerosis in animals
Simmons, S. B., Pierson, E. R., Lee, S. Y., & Goverman, J. M. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.04.006 · Cited by 176 · see citing works
Defining the human T helper 17 cell phenotype
Annunziato, F., Cosmi, L., Liotta, F., Maggi, E., & Romagnani, S. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.05.004 · Cited by 191 · see citing works
Griseri, T., Arnold, I., Pearson, C., Krausgruber, T., Schiering, C., Franchini, F., Schulthess, J., McKenzie, B., Crocker, P., & Powrie, F. (2015) · Immunity · doi:10.1016/j.immuni.2015.07.008 · Cited by 183 · see citing works
“More recently it was shown that IL-23 stimulated Th17 cells to produce GM-CSF, which was pathogenic in EAE although its functional role was not established (El-Behi et al., 2011).”
BackgroundT‐cell trafficking in the central nervous system
Sallusto, F., Impellizzieri, D., Basso, C., Laroni, A., Uccelli, A., Lanzavecchia, A., & Engelhardt, B. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01140.x · Cited by 186 · see citing works
“showed that GM-CSF, which is induced in Th17 cells by IL-23, is the critical pathogenetic factor required in the effector phase of EAE (35, 36).”
BackgroundMechanisms regulating regional localization of inflammation during CNS autoimmunity
Pierson, E. R., Simmons, S. B., Castelli, L., & Goverman, J. M. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01126.x · Cited by 176 · see citing works
“Although RORγt was implicated as an important transcription factor for GM-CSF expression, the presence of RORγt was not essential for GM-CSF production under certain conditions (particularly in vitro) (52, 53).”
BackgroundResultIL ‐17: overview and role in oral immunity and microbiome
Abusleme, L., & Moutsopoulos, N. M. (2016) · Oral Diseases · doi:10.1111/odi.12598 · Cited by 185 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript pathogenic Th17 is dependent on IL-1 and IL-23 and is required for pathogenicity (Codarri et al., 2011, El-Behi et al., 2011).”
Lin, C., Bradstreet, T. R., Schwarzkopf, E. A., Sim, J. E., Carrero, J. A., Chou, C., Cook, L. E., Egawa, T., Taneja, R., MURPHY, K. M. M., et al. (2014) · Nature Communications · doi:10.1038/ncomms4551 · Cited by 179 · see citing works
Chong, W. P., Mattapallil, M. J., Raychaudhuri, K., Bing, S. J., Wu, S., Zhong, Y., Wang, W., Chen, Z., Silver, P. B., Jittayasothorn, Y., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.06.022 · Cited by 183 · see citing works
Human Th17 Cells Express High Levels of Enzymatically Active Dipeptidylpeptidase IV (CD26)
Bengsch, B., Seigel, B., Flecken, T., Wolanski, J., Blum, H., & Thimme, R. (2012) · Journal of Immunology · doi:10.4049/jimmunol.1103801 · Cited by 177 · see citing works
“Indeed, neutralization of IL-17 was inefficient in avoiding Th17-cell mediated disease (29), and several studies suggest that other cytokines produced by Th17 cells, such as GM-CSF, may be more critically involved in inflammation compared with IL-17 (30, 31).”
Background
- 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 › Pathology and Forensic Medicine › 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
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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