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RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation
Abstract
Although the role of the T(H)1 and T(H)17 subsets of helper T cells as disease mediators in autoimmune neuroinflammation remains a subject of some debate, none of their signature cytokines are essential for disease development. Here we report that interleukin 23 (IL-23) and the transcription factor RORγt drove expression of the cytokine GM-CSF in helper T cells, whereas IL-12, interferon-γ (IFN-γ) and IL-27 acted as negative regulators. Autoreactive helper T cells specifically lacking GM-CSF failed to initiate neuroinflammation despite expression of IL-17A or IFN-γ, whereas GM-CSF secretion by Ifng(-/-)Il17a(-/-) helper T cells was sufficient to induce experimental autoimmune encephalomyelitis (EAE). During the disease effector phase, GM-CSF sustained neuroinflammation via myeloid cells that infiltrated the central nervous system. Thus, in contrast to all other known helper T cell-derived cytokines, GM-CSF serves a nonredundant function in the initiation of autoimmune inflammation regardless of helper T cell polarization.
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“Th2 cells regulate multiple non-immune tissue cells at mucosal sites”
From TH17 cell heterogeneity and its role in tissue inflammation (2023) · cites this paper as [25]
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“GM-CSF is essential for the development and progression of EAE. Mice deficient in GM-CSF are resistant to EAE induction, and blockade of GM-CSF in wild-type mice suppresses ongoing disease (McQualter et al., 2001; Codarri et al., 2011).”
From The Role of Iron Regulation in Immunometabolism and Immune-Related Disease (2019) · cites this paper as Codarri et al., 2011
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Cites
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
Ivanov, I. I., McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J., & Littman, D. R. (2006) · Cell · doi:10.1016/j.cell.2006.07.035 · Cited by 5,145
Harrington, L. E., Hatton, R. D., Mangan, P. R., Turner, H., Murphy, T. L., Murphy, K. M., & Weaver, C. T. (2005) · Nature Immunology · doi:10.1038/ni1254 · Cited by 4,742
A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17
Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y.-H., Wang, Y., Hood, L., Zhu, Z., Tian, Q., et al. (2005) · Nature Immunology · doi:10.1038/ni1261 · Cited by 4,265
IL-23 drives a pathogenic T cell population that induces autoimmune inflammation
Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T., Kastelein, R. A., & Cua, D. J. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20041257 · Cited by 4,099
Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M., & Stockinger, B. (2006) · Immunity · doi:10.1016/j.immuni.2006.01.001 · Cited by 3,605
Cua, D. J., Sherlock, J., Chen, Y., Murphy, C. A., Joyce, B., Seymour, B., Lucian, L., To, W., Kwan, S., Churakova, T., et al. (2003) · Nature · doi:10.1038/nature01355 · Cited by 2,906
Oppmann, B., Lesley, R., Blom, B., Timans, J. C., Xu, Y., Hunte, B., Vega, F., Yu, N., Wang, J., Singh, K. P., et al. (2000) · Immunity · doi:10.1016/s1074-7613(00)00070-4 · Cited by 2,819
IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells
Korn, T., Bettelli, E., Gao, W., Awasthi, A., Jäger, A., Strom, T. B., Oukka, M., & Kuchroo, V. K. (2007) · Nature · doi:10.1038/nature05970 · Cited by 1,896
Aggarwal, S., Ghilardi, N., Xie, M.-H., de Sauvage, F. J., & Gurney, A. L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m207577200 · Cited by 1,848
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Yu, X.-F., Liu, W., Chen, S., Cheng, X.-Q., Paez, P. A., Sun, T., Yuan, F., Wei, C.-Y., Landry, J. W., Poklepovic, A., et al. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001595 · Cited by 20
Tsai, Y.-W., Dong, J.-L., Jian, Y.-J., Fu, S., Chien, M., Liu, Y., Hsu, C.-Y., & Sytwu, H. (2021) · Microorganisms · doi:10.3390/microorganisms9091930 · Cited by 21
Zheng, R., Kong, M., Wang, S., He, B., & Xie, X. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.108702 · Cited by 21
Translating the biology of β common receptor-engaging cytokines into clinical medicine
Pant, H., Hercus, T. R., Tumes, D. J., Yip, K. H., Parker, M. W., Owczarek, C. M., Lopez, A. F., & Huston, D. P. (2022) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2022.09.030 · Cited by 21
GM-CSF producing autoreactive CD4+ T cells in type 1 diabetes
Knoop, J., Gavrisan, A., Kuehn, D., Reinhardt, J., Heinrich, M., Hippich, M., Eugster, A., Ockert, C., Ziegler, A., & Bonifacio, E. E. (2017) · Clinical Immunology · doi:10.1016/j.clim.2017.12.002 · Cited by 21
Interaction of RNA-binding protein HuR and miR-466i regulates GM-CSF expression
Chen, J., Adamiak, W., Huang, G., Atasoy, U., Rostami, A. M., & Yu, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-17371-5 · Cited by 22
Wu, X., Shen, H., Zhang, Y., Wang, C., Li, Q., Zhang, C., Zhuang, X., Li, C., Shi, Y., Xing, Y., et al. (2021) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.1c00763 · Cited by 22
IFN-γ protects from lethal IL-17 mediated viral encephalomyelitis independent of neutrophils
Savarin, C., Stohlman, S., Hinton, D., Ransohoff, R., Cua, D., & Bergmann, C. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-104 · Cited by 24
Lalle, G., Lautraite, R., Bouherrou, K., Plaschka, M., Pignata, A., Voisin, A., Twardowski, J., Perrin-Niquet, M., Stéphan, P., Durget, S., et al. (2024) · The Journal of Experimental Medicine · doi:10.1084/jem.20231348 · Cited by 21
“…immune responses to tumors (Borst et al., 2018), whereas granulocyte macrophage-colony stimulating factor (GM-CSF) – producing pathogenic TH17 cells emerge as the main drivers of MS and its murine model experimental autoimmune encephalomyelitis (EAE) (Codarri et al., 2011; Croxford et al., 2015).”
BackgroundOkamoto, M., Kuratani, A., Okuzaki, D., Kamiyama, N., Kobayashi, T., Sasai, M., & Yamamoto, M. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2401692121 · Cited by 20
Nowatzky, J., Manches, O., Khan, S. A., Godefroy, E., & Bhardwaj, N. (2018) · Journal of Autoimmunity · doi:10.1016/j.jaut.2018.05.005 · Cited by 20
SOCS3 Attenuates GM-CSF/IFN-γ-Mediated Inflammation During Spontaneous Spinal Cord Regeneration
Zhang, X., He, B., Li, H., Wang, Y., Zhou, Y., Wang, W., Song, T., Gu, X., Gu, X., Luo, Y., et al. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00493-8 · Cited by 20
“Therefore, GM-CSF promotes CNS inflammation via microglial activation.”
BackgroundInfluentialPD-1 Blockade Reverses Obesity-Mediated T Cell Priming Impairment
Le, C. T., Khuat, L. T., Caryotakis, S. E., Wang, M., Dunai, C., Nguyen, A. V., Vick, L. V., Stoffel, K. M., Blazar, B. R., Monjazeb, A. M., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.590568 · Cited by 19
Control of T cell effector functions by miRNAs
Inácio, D., Amado, T., Silva‐Santos, B., & Gomes, A. Q. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.04.011 · Cited by 19
Granulocyte-macrophage colony-stimulating factor as a mediator of autoimmunity in multiple sclerosis
Kostić, M. S., Živković, N., Cvetanović, A., & Stojanović, I. R. (2018) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2018.07.002 · Cited by 21
SRC3 is a co-factor for RORγt in Th17 differentiation but not thymocyte development
He, Z.-H., Zhang, J., Du, Q., Xu, J.-M., Gwack, Y., & Sun, Z.-M. (2018) · Journal of Immunology · doi:10.4049/jimmunol.1801187 · Cited by 18
Pilipović, I., Vujnović, I., Stojić-Vukanić, Z., Petrović, R., Kosec, D., Nacka-Aleksić, M., Jasnić, N., & Leposavić, G. (2019) · Immunologic research · doi:10.1007/s12026-019-09082-y · Cited by 19
Heras‐Garvin, A., Refolo, V., Reindl, M., Wenning, G. K., & Stefanova, N. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1714-y · Cited by 20
The many-sided contributions of NF-κB to T-cell biology in health and disease
Voisin, A., & Grinberg‐Bleyer, Y. (2020) · International review of cytology · doi:10.1016/bs.ircmb.2020.10.006 · Cited by 22
Fu, S.-H., Lin, M.-H., Yeh, L.-T., Wang, Y.-L., Chien, M.-W., Lin, S.-H., Chang, D., & Sytwu, H. (2014) · Gut · doi:10.1136/gutjnl-2013-306585 · Cited by 22
Lipid metabolism: a central modulator of RORγt-mediated Th17 cell differentiation
Kanno, T., Miyako, K., & Endo, Y. (2024) · International Immunology · doi:10.1093/intimm/dxae031 · Cited by 20
Walkenhorst, M., Sonner, J. K., Meurs, N., Engler, J. B., Bauer, S., Winschel, I., Woo, M. S., Raich, L., Winkler, I., Vieira, V., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-53657-9 · Cited by 21
“GM-CSF is the only so far identi fi ed in fl ammatory cytokine being indispensable for EAE induction in C57BL/6J mice 63 .”
BackgroundTh17 Response in Uveitis: A Double-Edged Sword in Ocular Inflammation and Immune Regulation
Zong, Y., Tong, X., & Chong, W. P. (2025) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-025-09038-1 · Cited by 19
PI3K activity in dendritic cells exerts paradoxical effects during autoimmune inflammation
Datler, H., Vogel, A., Kerndl, M., Baumgartinger, C., Musiejovsky, L., Makivic, N., Frech, S., Niederreiter, B., Haider, T. T., Pühringer, M., et al. (2019) · Molecular Immunology · doi:10.1016/j.molimm.2019.03.015 · Cited by 19
Tristetraprolin Regulates TH17 Cell Function and Ameliorates DSS-Induced Colitis in Mice
Peng, H. C., Ning, H., Wang, Q., Lai, J., Wei, L., Stumpo, D. J., Blackshear, P. J., Fu, M., Hou, R., Hoft, D. F., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01952 · Cited by 19
LRRC4 functions as a neuron-protective role in experimental autoimmune encephalomyelitis
Zhang, Y., Li, D., Zeng, Q., Feng, J., Fu, H., Luo, Z., Xiao, B., Yang, H., & Wu, M. (2021) · Molecular Medicine · doi:10.1186/s10020-021-00304-4 · Cited by 19
“In contrast to Th1 and Th17 cells, Th2 cells secrete IL-4, -10, and -13 and induce strong antibody responses while inhibiting several functions of phagocytic cells (Codarri et al. 2011).”
BackgroundÁlvarez‐Sánchez, N., & Dunn, S. E. (2022) · Current topics in behavioral neurosciences · doi:10.1007/7854_2022_324 · Cited by 21
Li, J., Yang, P., Wu, Q., Li, H., Ding, Y., Hsu, H., Spalding, D. M., & Mountz, J. D. (2013) · Arthritis & Rheumatism · doi:10.1002/art.38057 · Cited by 20
Steeneck, C., Gege, C., Kinzel, O. D., Albers, M., Kleymann, G., Schlüter, T., Schulz, A., Xue, X., Cummings, M. D., Fourie, A. M., et al. (2020) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2020.127174 · Cited by 19
B cell depletion changes the immune cell profile in multiple sclerosis patients: One-year report
Lovett‐Racke, A. E., Yang, Y., Liu, Y., Gormley, M., Kraus, E. E., Graham, C., Wray, S. E., Racke, M. K., Álvarez, E., Bass, A. D.-D., et al. (2021) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2021.577676 · Cited by 20
“In addition, GM-CSF expressed by CD4 T cells has been identified as an essential molecule in encephalitogenic T cells in mice (Codarri et al., 2011; El-Behi et al., 2011).”
Ubiquitin Ligases and Deubiquitinating Enzymes in CD4+ T Cell Effector Fate Choice and Function
Layman, A. A. K., & Oliver, P. M. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502660 · Cited by 20
Alvarenga-Filho, H., Salles, M., Hygino, J., Ferreira, T. B., Sacramento, P. M., Monteiro, C., Vasconcelos, C., Alvarenga, R., & Bento, C. (2017) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2016.12.013 · Cited by 20
“These cytokines induce the release of large amounts of free radicals and matrix metalloproteinases (MMPs) by macrophages that migrate to the CNS of MS patients (Miossec, 2009; Behi et al., 2011; Codarri et al., 2011; Cravens et al., 2011; Rasouli et al., 2015).”
BackgroundAnsari, M. A., Nadeem, A., Attia, S., Bakheet, S., Shahid, M., Rehman, M., Alanazi, M., Alhamed, A. S., Ibrahim, K. E., Albekairi, N., et al. (2022) · Immunobiology · doi:10.1016/j.imbio.2022.152245 · Cited by 17
Activation of mucosal immunity as a novel therapeutic strategy for combating brucellosis
Pascual, D. W., Goodwin, Z. I., Bhagyaraj, E., Hoffman, C. A., & Yang, X. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1018165 · Cited by 18
“Th17 cells have been reported to produce GM-CSF and IL-22 following RORγt activation (Liang et al., 2006; Zheng et al., 2007; Codarri et al., 2011; El-Behi et al., 2011).”
BackgroundNeuro-immune crosstalk in depressive symptoms of multiple sclerosis
Wang, C., Zhou, Y., & Feinstein, A. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106005 · Cited by 20
Induction of Passive EAE Using Myelin-Reactive CD4+ T Cells
McPherson, R. C., Cambrook, H., O’Connor, R. A., & Anderton, S. M. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1212-4_17 · Cited by 18
Huarte, E., Jun, S., Rynda‐Apple, A., Golden, S., Jackiw, L. O., Hoffman, C. A., Maddaloni, M., & Pascual, D. W. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501973 · Cited by 21
Singh, A. K., Novakova, L., Axelsson, M., Malmeström, C., Zetterberg, H., Lycke, J., & Cardell, S. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00260 · Cited by 19
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Wang, X., Richard, M. L., Li, P., Henry, B., Schutt, S. D., Yu, X., Fan, H., Zhang, W., Gilkeson, G. S., & Zhang, X. K. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000664 · Cited by 18
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Behi, M. E., Dai, H., Magalhaes, J. G., Hwang, D. H., Zhang, G., Rostami, A. M., & Ćirić, B. (2014) · European Journal of Immunology · doi:10.1002/eji.201344360 · Cited by 20
Aychek, T., & Jung, S. (2014) · Science · doi:10.1126/science.1252785 · Cited by 20
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Lai, S., Wu, X., Liu, Y., Liu, B., Wu, H., & Ma, K. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100928 · Cited by 18
“Conversely, IL-23 and ROR γ t can induce GM-CSF production in EAE mice (Codarri et al., 2011).”
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Benamar, M., Contini, P., Schmitz‐Abe, K., Lanzetta, O., Getachew, F., Bachelin, C., Leyva-Castillo, J. M., Wang, M., Öktelik, F. B., Perrot, O., et al. (2025) · Immunity · doi:10.1016/j.immuni.2025.09.007 · Cited by 17
Zhang, Y., Wei, Z., Dong, H. F., Zhou, J., Yuan, J., Ni, B., Wu, Y., Han, C., & Tian, Y. (2020) · RNA Biology · doi:10.1080/15476286.2020.1862567 · Cited by 17
“induce autoimmune neuroinflammation [67,68].”
Dopaminergic stimulation leads B-cell infiltration into the central nervous system upon autoimmunity
Prado, C. E., Osorio‐Barrios, F., Falcón, P., Espinoza, A., Sáez, J. J., Yuseff, M.-I., & Pacheco, R. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02338-1 · Cited by 17
“In contrast to IL-17 and IFNγ, GM-CSF is essential to promote EAE manifestation [57].”
BackgroundSTAT1 signaling protects self-reactive T cells from control by innate cells during neuroinflammation
Arbelaez, C. A., Palle, P., Charaix, J., & Bettelli, E. (2022) · JCI Insight · doi:10.1172/jci.insight.148222 · Cited by 18
“IL-23 is also important for the differentiation of pathogenic T cells producing GM-CSF (11, 12).”
Highlights of the advances in basic immunology in 2011
Liu, J., Liu, S., & Cao, X. (2012) · Cellular and Molecular Immunology · doi:10.1038/cmi.2012.12 · Cited by 18
Eylenstein, R., Weinfurtner, D., Härtle, S., Strohner, R., Böttcher, J., Augustin, M. A., Ostendorp, R., & Steidl, S. (2015) · mAbs · doi:10.1080/19420862.2015.1099774 · Cited by 17
René, O., Fauber, B. P., Barnard, A., Chapman, K. L., Deng, Y., Eidenschenk, C., Everett, C., Gobbi, A., Johnson, A. R., La, H., et al. (2016) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2016.07.081 · Cited by 17
Drohomyrecky, P. C., Doroshenko, E. R., Akkermann, R., Moshkova, M., Yi, T. J., Zhao, F. L., Ahn, J. J., McGaha, T. L., Pahan, K., & Dunn, S. E. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801200 · Cited by 18
“8B), and IL-12p70 and IL-1b were not detectable above background levels (data not shown).”
BackgroundInfluentialQin, S., Vodovotz, L., Zamora, R., Fitzpatrick, M., Kessinger, C., Kingsley, L., McMahon, D., DeSensi, R., Leader, J., Crothers, K., et al. (2020) · Journal of Acquired Immune Deficiency Syndromes · doi:10.1097/qai.0000000000002234 · Cited by 11
Modeling a complex disease: Multiple sclerosis—Update 2020
Regen, T., & Waisman, A. (2021) · Advances in immunology · doi:10.1016/bs.ai.2021.03.002 · Cited by 16
Rasouli, J., Casella, G., Ishikawa, L. L. W., Thomé, R., Boehm, A., Ertel, A., Melo‐Silva, C. R., Mari, E. R., Porazzi, P., Zhang, W., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.679498 · Cited by 17
Mair, F., & Becher, B. (2013) · European Journal of Immunology · doi:10.1002/eji.201343653 · Cited by 17
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Spath, S., & Becher, B. (2013) · European Journal of Immunology · doi:10.1002/eji.201344109 · Cited by 16
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Arellano, B., Hussain, R. Z., Zacharias, T., Yoon, J., David, C., Zein, S., Steinman, L., Forsthuber, T., Greenberg, B., Lambracht-Washington, D., et al. (2012) · Archives of Neurology · doi:10.1001/archneurol.2012.1300 · Cited by 16
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BackgroundLayman, A. A. K., Sprout, S. L., Phillips, D., & Oliver, P. M. (2017) · Scientific Reports · doi:10.1038/srep39649 · Cited by 17
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Oukka, M., & Bettelli, E. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2018.09.008 · Cited by 19
Li, Z., He, C., Zhang, J., Zhang, H., Wei, H., Wu, S., & Jiang, W. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1900916 · Cited by 16
SerpinB1 expression in Th17 cells depends on hypoxia-inducible factor 1-alpha
Hou, L., & Yuki, K. (2020) · International Immunopharmacology · doi:10.1016/j.intimp.2020.106826 · Cited by 16
Roles of CSF2 as a modulator of inflammation during retinal degeneration
Saita, K., Moriuchi, Y., Iwagawa, T., Aihara, M., Takai, Y., Uchida, K., & Watanabe, S. (2022) · Cytokine · doi:10.1016/j.cyto.2022.155996 · Cited by 15
ALCAM on human oligodendrocytes mediates CD4 T cell adhesion
Jamann, H., Desu, H. L., Cui, Q., Halaweh, A., Tastet, O., Klément, W., Zandee, S., Pernin, F., Mamane, V. H., Ouédraogo, O., et al. (2023) · Brain · doi:10.1093/brain/awad286 · Cited by 16
Islam, S. M. T., Curtis, A. D., Taslim, N., Wilkinson, D., & Mannie, M. (2014) · Journal of Immunology · doi:10.4049/jimmunol.1303223 · Cited by 17
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BackgroundHernández-Mir, G., & McGeachy, M. J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173655 · Cited by 16
So, J.-B., Silver, P., Jittayasothorn, Y., Mattapallil, M., Chan, C.-C., Horai, R., & Caspi, R. (2020) · Journal of Autoimmunity · doi:10.1016/j.jaut.2020.102507 · Cited by 18
Targeting IFN-λ Signaling Promotes Recovery from Central Nervous System Autoimmunity
Manivasagam, S., Williams, J. L., Vollmer, L. L., Bollman, B., Bartleson, J. M., Ai, S., Wu, G. F., & Klein, R. S. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2101041 · Cited by 16
GM-CSF production by CD4+ T cells in MS patients: Regulation by regulatory T cells and vitamin D
Peelen, E., Muris, A., Damoiseaux, J. G. M. C., Knippenberg, S. A. M., Broens, K., Smolders, J., Tervaert, J.-W. C., Hupperts, R., & Thewissen, M. M. (2015) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2015.02.007 · Cited by 16
“However, knockout models of IFN-γ and IL-17A, i.e. Th1 and Th17 cell signature cytokines, are still susceptible to EAE (Codarri et al., 2011; El-behi et al., 2010; Komiyama et al., 2006; Ferber et al., 1996).”
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Tsai, H., & Wu, R. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1301079 · Cited by 17
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BackgroundSevere exacerbation of relapsing-remitting multiple sclerosis after G-CSF therapy
Rust, H. M., Kühle, J., Kappos, L., & Derfuss, T. J. (2016) · Neurology Neuroimmunology & Neuroinflammation · doi:10.1212/nxi.0000000000000215 · Cited by 16
“The closely related hematopoietic growth factor granulocyte-macrophage colony-stimulating factor (GM-CSF) has recently been implicated in the pathogenesis of MS.2–5 GM-CSF-deficient mice were resistant to the induction of experimental autoimmune encephalitis (EAE) and failed to sustain immune cell infiltrates in the C…”
Papatriantafyllou, M. (2011) · Nature reviews. Immunology · doi:10.1038/nri2996 · Cited by 17
RGC-32 Promotes Th17 Cell Differentiation and Enhances Experimental Autoimmune Encephalomyelitis
Rus, V., Nguyen, V. Q., Tatomir, A., Lees, J. R., Mekala, A. P., Boodhoo, D., Tegla, C., Luzina, I. G., Antony, P. A., Cudrici, C. D., et al. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1602158 · Cited by 16
“highly pathogenic potential (43, 44), were also significantly decreased in RGC-32 EAE mice (Fig.”
BackgroundLee, J.-H., Choi, J., Lee, W., Ko, K. R., & Kim, S. (2015) · Molecular Immunology · doi:10.1016/j.molimm.2015.09.028 · Cited by 16
Decoupling the role of RORγt in the differentiation and effector function of T H 17 cells
Zhong, X., Wu, H., Zhang, W., Gwack, Y., Shang, W., Lee, K. O., Isakov, N., He, Z., & Sun, Z. (2022) · Science Advances · doi:10.1126/sciadv.adc9221 · Cited by 16
“Differentiated TH17 cells are able to induce tissue inflammation involved in the pathogenesis of autoimmune diseases, including psoriasis, inflammatory bowel disease, and multiple sclerosis (2, 3, 14).”
BackgroundAlghibiwi, H. K., Ansari, M. A., Nadeem, A., Algonaiah, M. A., Attia, S. M., Bakheet, S. A., Albekairi, T. H., Almudimeegh, S., Alhamed, A. S., Shahid, M., et al. (2023) · Biomedicines · doi:10.3390/biomedicines11061511 · Cited by 16
“GM-CSF signaling was shown to be sufficient to initiate EAE and was produced by myeloid cells infiltrating the CNS sustained neuroinflammation [73].”
BackgroundTh17 cell promotes apoptosis of IL-23R+ neurons in experimental autoimmune encephalomyelitis
Sonar, S. A., Meitei, H. T., Karmakar, S., Mishra, A., Inamdar, S., Lenka, N., & Lal, G. (2024) · Clinical Immunology · doi:10.1016/j.clim.2024.109898 · Cited by 15
Kassem, S., Gaud, G., Bernard, I., Benamar, M., Dejean, A. S., Liblau, R., Fournié, G. J., Colacios, C., MALISSEN, B., & Saoudi, A. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006185 · Cited by 15
Serre, L., Girard, M., Ramadan, A., Menut, P., Rouquié, N., Lucca, L. E., Mahiddine, K., Léobon, B., Mars, L. T., & Guerder, S. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1700667 · Cited by 15
Uyttenhove, C., Gaignage, M., Donckers, D., Nasr, Z., Cheou, P., Snick, J. V., D'Auria, L., & van Pesch, V. (2018) · European Journal of Immunology · doi:10.1002/eji.201847580 · Cited by 11
Piper, C., Hainstock, E., Yin-Yuan, C., Chen, Y., Khatun, A., Kasmani, M. Y., Evans, J., Miller, J. A., Gorski, J., Cui, W., et al. (2022) · Blood Advances · doi:10.1182/bloodadvances.2021006084 · Cited by 14
Li, D., Li, J.-Y., Liu, H., Zhai, L.-N., Hu, W.-L., Xia, N., Tang, T., Jiao, J., Lv, B.-J., Nie, S., et al. (2022) · The FASEB Journal · doi:10.1096/fj.202101576r · Cited by 13
Valaperti, A., Nishii, M., Germano, D., Liu, P. P., & Eriksson, U. (2013) · Vaccine · doi:10.1016/j.vaccine.2013.07.084 · Cited by 15
Kuo, P., Brown, D. A., Scofield, B. A., Paraiso, H. C., Wang, P., Yu, I.-C. I., & Yen, J.-H. J. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.03.010 · Cited by 16
“Several T cell subsets, including CD4 + T cell lineages of Th1 and Th17, CD8 + T cells, and IL-17producting γδT cells, are essential for the pathogenesis of EAE (Camara et al., 2013; Codarri et al., 2011; Grifka-Walk et al., 2015; Jager et al., 2009; McWilliams et al., 2015; Paul et al., 2015).”
BackgroundWang, S.-H., Serr, I., Digigow, R. G., Metzler, B., Surnov, A., Gottwick, C., Alsamman, M., Krzikalla, D., Heine, M., Zahlten, M., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1542380 · Cited by 15
Alomar, H. A., Ansari, M. A., Nadeem, A., Attia, S. M., Bakheet, S. A., Al‐Mazroua, H. A., Hussein, M. H., Alqarni, S. A., & Ahmad, S. F. (2023) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2023.578069 · Cited by 15
TREM-2 Drives Development of Multiple Sclerosis by Promoting Pathogenic Th17 Polarization
Qu, S., Hu, S., Xu, H., Wu, Y., Ming, S., Zhan, X., Wang, C., & Huang, X. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-023-01094-x · Cited by 14
GM-CSF distinctly impacts human monocytes and macrophages via ERK1/2-dependent pathways
Farzam‐kia, N., Moratalla, A. C., Lemaître, F., Levert, A., Cal, S. D., Margarido, C., Solorio, Y. C., & Arbour, N. (2023) · Immunology Letters · doi:10.1016/j.imlet.2023.07.009 · Cited by 14
Immunoregulatory Effects of Interferon-β in Suppression of Th17 cells
Pennell, L. M., & Fish, E. N. (2013) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2013.0088 · Cited by 14
Inflammation‐associated genes: risks and benefits to Foxp3+ regulatory T‐cell function
O’Connor, R. A., & Anderton, S. M. (2015) · Immunology · doi:10.1111/imm.12507 · Cited by 15
Adaptive Immune Responses in CNS Autoimmune Disease: Mechanisms and Therapeutic Opportunities
McPherson, R. C., & Anderton, S. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9453-9 · Cited by 14
Stojić-Vukanić, Z., Pilipović, I., Vujnović, I., Nacka-Aleksić, M., Petrović, R., Arsenović-Ranin, N., Dimitrijević, M., & Leposavić, G. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166498 · Cited by 15
Cytokines as Mediators of Neuroinflammation in Experimental Autoimmune Encephalomyelitis
Gogoleva, V. S., Атретханы, К.-С. Н., Drutskaya, M. S., Mufazalov, I. A., Kruglov, A., & Nedospasov, S. A. (2018) · Biochemistry (Moscow) · doi:10.1134/s0006297918090110 · Cited by 13
Th17 cells: from gut homeostasis to CNS pathogenesis
Buckner, J. H., & Harrison, O. J. (2022) · Trends in Immunology · doi:10.1016/j.it.2022.01.005 · Cited by 14
Murray, M. P., Crosby, C., Marcovecchio, P. M., Hartmann, N., Chandra, S., Zhao, M., Khurana, A., Zahner, S., Clausen, B., Coleman, F., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2021.110209 · Cited by 8
“Further, IL-23 has been shown to stimulate GM-CSF production by CD4+ Th17 cells, although it is not known if this is true for iNKT cells (Codarri et al., 2011; El-Behi et al., 2011; Rothchild et al., 2014).”
BackgroundImmunotherapy targeting plasma ASM is protective in a mouse model of Alzheimer’s disease
Choi, B. J., Park, M. H., Park, K. H., Han, W. H., Yoon, H. J., Jung, H. Y., Hong, J. Y., Chowdhury, M. R., Kim, K. Y., Lee, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37316-z · Cited by 14
Stojić-Vukanić, Z., Nacka-Aleksić, M., Pilipović, I., Vujnović, I., Blagojević, V., Kosec, D. J., Dimitrijević, M., & Leposavić, G. (2015) · Immunity & Ageing · doi:10.1186/s12979-015-0044-x · Cited by 15
“The expression of the cytokines (IL-1β and IL-23/p19) driving GM-CSF + IL-17 + IFN-γ + cell differentiation in mice was also augmented in aged rat spinal cord mononuclear cells.”
BackgroundInfluentialHassan, A., Wlodarczyk, M. F., Benamar, M., Bassot, E., Salvioni, A., Kassem, S., Berry, A., Saoudi, A., & Blanchard, N. (2020) · mBio · doi:10.1128/mbio.03394-19 · Cited by 14
Ahmad, S. F., Ansari, M. A., Nadeem, A., Bakheet, S. A., AL-Ayadhi, L. Y., Alsaad, A. M. S., Assiri, M. A., Al‐Mazroua, H. A., & Attia, S. M. (2020) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2020.577430 · Cited by 14
Autoimmunity beyond Th17: GM-CSF producing T cells
Zielinski, C. E. (2014) · Cell Cycle · doi:10.4161/15384101.2014.946377 · Cited by 14
Ewanchuk, B. W., Allan, E. R. O., Warren, A. L., Ramachandran, R., & Yates, R. M. (2017) · The FASEB Journal · doi:10.1096/fj.201700552r · Cited by 13
Harsini, S., & Rezaei, N. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-818006-8.00001-3 · Cited by 13
Metadata
- Authors
- Codarri, L., Gyülvészi, G., Tosevski, V., Hesske, L., Fontana, A., Magnenat, L., Suter, T., & Becher, B.
- Affiliations
- University Hospital Zurich (CH)
- University of Zurich (CH)
- Merck Serono S.A. (Switzerland) (CH)
- Corresponding author
- Becher, Burkhard
- Venue
- Nature Immunology
- Published
- 2011-04-24
- Volume
- 12
- Issue
- 6
- Pages
- 560-567
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- OpenAlex
- W2157837362
- Cited by
- 1,191
- References
- 44
- Citations by year
- 2026: 31 · 2025: 48 · 2024: 60 · 2023: 53 · 2022: 61 · 2021: 73 · 2020: 85 · 2019: 83 · 2018: 72 · 2017: 99 · 2016: 96 · 2015: 117 · 2014: 103 · 2013: 98 · 2012: 82
- FWCI
- 70.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- RORγt, GM-CSF, experimental autoimmune encephalomyelitis, T helper cells, IL-23, autoimmune neuroinflammation, Th1 cells, Th17 cells, myeloid cell infiltration, IL-12, interferon-gamma, IL-27, cytokine regulation
- MeSH terms
- Animals, Cells, Cultured, Encephalomyelitis, Autoimmune, Experimental, Female, Flow Cytometry, Glycoproteins, T-Lymphocytes, Helper-Inducer, Interferon-gamma, Interleukins, Male, Mice, Inbred C57BL, Mice, Inbred Strains, Mice, Transgenic, Peptide Fragments, Granulocyte-Macrophage Colony-Stimulating Factor, Mice, Knockout, Th1 Cells, Interleukin-12, Interleukin-17, Mice, Interleukin-23, Nuclear Receptor Subfamily 1, Group F, Member 3, Th17 Cells, Myelin-Oligodendrocyte Glycoprotein
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