Interleukin 23 receptor: Expression and regulation in immune cells.
Chronic inflammatory diseases
Gene regulation
Interleukin-23 (IL-23)
Interleukin-23 receptor (IL-23R)
Transcription factors
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
14 Oct 2023
14 Oct 2023
Historique:
revised:
11
10
2023
received:
31
05
2023
accepted:
12
10
2023
pubmed:
14
10
2023
medline:
14
10
2023
entrez:
14
10
2023
Statut:
aheadofprint
Résumé
The importance of IL-23 and its specific receptor, IL-23R, in the pathogenesis of several chronic inflammatory diseases has been established, but the underlying pathological mechanisms are not fully understood. This review focuses on IL-23R expression and regulation in immune cells.
Identifiants
pubmed: 37837262
doi: 10.1002/eji.202250348
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2250348Subventions
Organisme : Institut Pasteur
Organisme : Janssen Research and Development
Informations de copyright
© 2023 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.
Références
Oppmann, B., Lesley, R., Blom, B., Timans, J. C., Xu, Y., Hunte, B., Vega, F. et al., Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity. 2000. 13: 715-725.
Aggarwal, S., Ghilardi, N., Xie, M.-H., De Sauvage, F. J. and Gurney, A. L., Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17 *. J. Biol. Chem. 2003. 278: 1910-1914.
Cua, D. J., Sherlock, J., Chen, Y., Murphy, C. A., Joyce, B., Seymour, B., Lucian, L. et al., Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 2003. 421: 744-748.
Duerr, R. H., Taylor, K. D., Brant, S. R., Rioux, J. D., Silverberg, M. S., Daly, M. J., Steinhart, A. H. et al., A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science. 2006. 314: 1461-1463.
Wellcome Trust Case Control Consortium, Australo-Anglo-American Spondylitis Consortium (TASC), Burton, P. R., Clayton, D. G., Cardon, L. R., Craddock, N., Deloukas, P., Duncanson, A., Kwiatkowski, D. P. et al., Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat. Genet. 2007. 39: 1329-1337.
Cargill, M., Schrodi, S. J., Chang, M., Garcia, V. E., Brandon, R., Callis, K. P., Matsunami, N. et al., A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am. J. Hum. Genet. 2007. 80: 273-290.
Teng, M. W. L., Bowman, E. P., Mcelwee, J. J., Smyth, M. J., Casanova, J.-L., Cooper, A. M. and Cua, D. J., IL-12 and IL-23 cytokines: from discovery to targeted therapies for immune-mediated inflammatory diseases. Nat. Med. 2015. 21: 719-729.
Schinocca, C., Rizzo, C., Fasano, S., Grasso, G., La Barbera, L., Ciccia, F. et al., Role of the IL-23/IL-17 pathway in rheumatic diseases: an overview. Front. Immunol. 2021 [cited 2023 May 30];12. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2021.637829
Parham, C., Chirica, M., Timans, J., Vaisberg, E., Travis, M., Cheung, J., Pflanz, S. et al., A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 2002. 168: 5699-5708.
Rosine, N., Rowe, H., Koturan, S., Yahia-Cherbal, H., Leloup, C., Watad, A., Berenbaum, F. et al., Characterization of blood mucosal-associated invariant t cells in patients with axial spondyloarthritis and of resident mucosal-associated invariant t cells from the axial entheses of non-axial spondyloarthritis control patients. Arthritis Rheumatol. 2022. 74: 1786-1795.
Philippot, Q., Ogishi, M., Bohlen, J., Puchan, J., Arias, A. A., Nguyen, T., Martin-Fernandez, M. et al., Human IL-23 is essential for IFN-γ-dependent immunity to mycobacteria. Sci. Immunol. 2023. 8: eabq5204.
Trinchieri, G., Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol. 1995. 13: 251-276.
Sinigaglia, F., D'ambrosio, D., Panina-Bordignon, P. and Rogge, L., Regulation of the IL-12/IL-12R axis: a critical step in T-helper cell differentiation and effector function. Immunol. Rev. 1999. 170: 65-72.
Presky, D. H., Yang, H., Minetti, L. J., Chua, A. O., Nabavi, N., Wu, C.-Y., Gately, M. K. et al., A functional interleukin 12 receptor complex is composed of two β-type cytokine receptor subunits. Proc. Natl. Acad. Sci. 1996. 93: 14002-14007.
Schröder, J., Moll, J. M., Baran, P., Grötzinger, J., Scheller, J. and Floss, D. M., Non-canonical interleukin 23 receptor complex assembly. J. Biol. Chem. 2015. 290: 359-370.
Pastor-Fernández, G., Mariblanca, I. R. and Navarro, M. N., Decoding IL-23 signaling cascade for new therapeutic opportunities. Cells. 2020. 9: 2044.
Bloch, Y., Bouchareychas, L., Merceron, R., Składanowska, K., Van Den Bossche, L., Detry, S., Govindarajan, S. et al., Structural activation of pro-inflammatory human cytokine IL-23 by cognate IL-23 receptor enables recruitment of the shared receptor IL-12Rβ1. Immunity. 2018. 48: 45-58. e6.
Zou, J., Presky, D. H., Wu, C.-Y. and Gubler, U., Differential associations between the cytoplasmic regions of the interleukin-12 receptor subunits beta1 and beta2 and JAK kinases. J. Biol. Chem. 1997. 272: 6073-6077.
Floss, D. M., Klöcker, T., Schröder, J., Lamertz, L., Mrotzek, S., Strobl, B., Hermanns, H. et al., Defining the functional binding sites of interleukin 12 receptor β1 and interleukin 23 receptor to Janus kinases. Mol. Biol. Cell. 2016. 27: 2301-2316.
Rogge, L., Barberis-Maino, L., Biffi, M., Passini, N., Presky, D. H., Gubler, U. and Sinigaglia, F., Selective expression of an interleukin-12 receptor component by human T helper 1 cells. J. Exp. Med. 1997. 185: 825-831.
Gollob, J. A., Murphy, E. A., Mahajan, S., Schnipper, C. P., Ritz, J. and Frank, D. A., Altered interleukin-12 responsiveness in Th1 and Th2 cells is associated with the differential activation of STAT5 and STAT1. Blood. 1998. 91: 1341-1354.
Lee, P. W., Smith, A. J., Yang, Y., Selhorst, A. J., Liu, Y., Racke, M. K. and Lovett-Racke, A. E., IL-23R-activated STAT3/STAT4 is essential for Th1/Th17-mediated CNS autoimmunity. JCI Insight. [cited 2020 Dec 21];2. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5621925/
Zhang, X.-Y., Zhang, H.-J., Zhang, Y., Fu, Y.-J., He, J., Zhu, L. P., Wang, S.-H. et al., Identification and expression analysis of alternatively spliced isoforms of human interleukin-23 receptor gene in normal lymphoid cells and selected tumor cells. Immunogenetics. 2006. 57: 934-943.
Kan, S.-H., Mancini, G. and Gallagher, G., Identification and characterization of multiple splice forms of the human interleukin-23 receptor alpha chain in mitogen-activated leukocytes. Genes Immun. 2008. 9: 631-639.
Zhang, W., Ferguson, J., Ng, S. M., Hui, K., Goh, G., Lin, A., Esplugues, E. et al., Effector CD4+ T cell expression signatures and immune-mediated disease associated genes. PLoS One. 2012. 7: e38510.
Floss, D. M., Moll, J. M. and Scheller, J., IL-12 and IL-23-Close relatives with structural homologies but distinct immunological functions. Cells. 2020. 9: 2184.
Leshinsky-Silver, E., Karban, A., Dalal, I., Eliakim, R., Shirin, H., Tzofi, T., Boaz, M. et al., Evaluation of the interleukin-23 receptor gene coding variant R381Q in pediatric and adult Crohn disease. J. Pediatr. Gastroenterol. Nutr. 2007. 45: 405-408.
Roberts, R. L., Gearry, R. B., Hollis-Moffatt, J. E., Miller, A. L., Reid, J., Abkevich, V., Timms, K. M. et al., IL23R R381Q and ATG16L1 T300A are strongly associated with Crohn's disease in a study of New Zealand Caucasians with inflammatory bowel disease. Am. J. Gastroenterol. 2007. 102: 2754-2761.
Silverberg, M. S., Cho, J. H., Rioux, J. D., Mcgovern, D. P. B., Wu, J., Annese, V., Achkar, J.-P. et al., Ulcerative colitis-risk loci on chromosomes 1p36 and 12q15 found by genome-wide association study. Nat. Genet. 2009. 41: 216-220.
Liu, Y., Helms, C., Liao, W., Zaba, L. C., Duan, S., Gardner, J., Wise, C. et al., A genome-wide association study of psoriasis and psoriatic arthritis identifies new disease loci. PLoS Genet. 2008. 4: e1000041.
Rahman, P., Inman, R. D., Gladman, D. D., Reeve, J. P., Peddle, L. and Maksymowych, W. P., Association of interleukin-23 receptor variants with ankylosing spondylitis. Arthritis Rheum. 2008. 58: 1020-1025.
Australo-Anglo-American Spondyloarthritis Consortium (TASC), Reveille, J. D., Sims, A. M., Danoy, P., Evans, D. M., Leo, P. et al., Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat. Genet. 2010. 42: 123-127.
Sarin, R., Wu, X. and Abraham, C., Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4+ and CD8+ human T-cell functional responses. Proc Natl Acad Sci USA. 2011. 108: 9560-9565.
Pidasheva, S., Trifari, S., Phillips, A., Hackney, J. A., Ma, Y., Smith, A., Sohn, S. J. et al., Functional studies on the IBD susceptibility gene IL23R implicate reduced receptor function in the protective genetic variant R381Q. PLoS One. 2011. 6: e25038.
Di Meglio, P., Di Cesare, A., Laggner, U., Chu, C.-C., Napolitano, L., Villanova, F., Tosi, I. et al., The IL23R R381Q gene variant protects against immune-mediated diseases by impairing IL-23-induced Th17 effector response in humans. PLoS One. 2011. 6: e17160.
Coffre, M., Roumier, M., Rybczynska, M., Sechet, E., Law, H. K. W., Gossec, L., Dougados, M. et al., Combinatorial control of Th17 and Th1 cell functions by genetic variations in genes associated with the interleukin-23 signaling pathway in spondyloarthritis. Arthritis Rheum. 2013. 65: 1510-1521.
Sivanesan, D., Beauchamp, C., Quinou, C., Lee, J., Lesage, S., Chemtob, S., Rioux, J. D. et al., IL23R (interleukin 23 receptor) variants protective against inflammatory bowel diseases (IBD) display loss of function due to impaired protein stability and intracellular trafficking *. J. Biol. Chem. 2016. 291: 8673-8685.
Bauquet, A. T., Jin, H., Paterson, A. M., Mitsdoerffer, M., Ho, I.-C., Sharpe, A. H. and Kuchroo, V. K., Costimulatory molecule ICOS plays a critical role in the development of TH-17 and follicular T-helper cells by regulating c-Maf expression and IL-21 production. Nat. Immunol. 2009. 10: 167-175.
Wines, B. D., Yap, M. L., Powell, M. S., Tan, P. S., Ko, K. K., Orlowski, E. and Hogarth, P. M., Distinctive expression of interleukin-23 receptor subunits on human Th17 and γδ T cells. Immunol. Cell Biol. 2017. 95: 272-279.
Chen, Z., Tato, C. M., Muul, L., Laurence, A. and O'shea, J. J., Distinct regulation of interleukin-17 in human T helper lymphocytes. Arthritis Rheum. 2007. 56: 2936-2946.
Li, H., Hsu, H.-C., Wu, Q., Yang, P., Li, J., Luo, B., Oukka, M. et al., IL-23 promotes TCR-mediated negative selection of thymocytes through the upregulation of IL-23 receptor and RORγt. Nat. Commun. 2014. 5: 4259.
Tan, Z. Y., Bealgey, K. W., Fang, Y., Gong, Y. M. and Bao, S., Interleukin-23: Immunological roles and clinical implications. Int. J. Biochem. Cell Biol. 2009. 41: 733-735.
Ivanov, I. I., Mckenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J. et al., RORγt directs the differentiation program of proinflammatory Th17 Cells. Cell. 2006. 126: 1121-1133.
Lee, Y., Awasthi, A., Yosef, N., Quintana, F. J., Xiao, S., Peters, A., Wu, C. et al., Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 2012. 13: 991-999.
Jain, R., Chen, Y., Kanno, Y., Joyce-Shaikh, B., Vahedi, G., Hirahara, K., Blumenschein, W. M. et al., Interleukin-23-induced transcription factor blimp-1 promotes pathogenicity of T helper 17 cells. Immunity. 2016. 44: 131-142.
Komuczki, J., Tuzlak, S., Friebel, E., Hartwig, T., Spath, S., Rosenstiel, P., Waisman, A. et al., Fate-mapping of GM-CSF expression identifies a discrete subset of inflammation-driving T helper cells regulated by cytokines IL-23 and IL-1β. Immunity. 2019. 50: 1289-1304. e6.
Razawy, W., Asmawidjaja, P. S., Mus, A. M., Salioska, N., Davelaar, N., Kops, N., Oukka, M. et al., CD4+ CCR6+ T cells, but not γδ T cells, are important for the IL-23R-dependent progression of antigen-induced inflammatory arthritis in mice. Eur. J. Immunol. 2020. 50: 245-255.
Pawlak, M., Detomaso, D., Schnell, A., Meyer Zu Horste, G., Lee, Y., Nyman, J., Dionne, D. et al., Induction of a colitogenic phenotype in Th1-like cells depends on interleukin-23 receptor signaling. Immunity. 2022. 55: 1663-1679. e6.
Whitley, S. K., Li, M., Kashem, S. W., Hirai, T., Igyártó, B. Z., Knizner, K., Ho, J. et al., Local IL-23 is required for proliferation and retention of skin-resident memory TH17 cells. Sci. Immunol. 2022. 7: eabq3254.
Hong, H., Gao, M., Wu, Q., Yang, P., Liu, S., Li, H., Burrows, P. D. et al., IL-23 promotes a coordinated B cell germinal center program for class-switch recombination to IgG2b in BXD2 Mice. J. Immunol. 2020. 205: 346-358.
Yang, B.-H., Hagemann, S., Mamareli, P., Lauer, U., Hoffmann, U., Beckstette, M., Föhse, L. et al., Foxp3(+) T cells expressing RORγt represent a stable regulatory T-cell effector lineage with enhanced suppressive capacity during intestinal inflammation. Mucosal Immunol. 2016. 9: 444-457.
Jacobse, J., Brown, R. E., Li, J., Pilat, J. M., Pham, L., Short, S. P., Peek, C. T. et al., Interleukin-23 receptor signaling impairs the stability and function of colonic regulatory T cells. Cell Rep. 2023. 42: 112128.
Wei, Y.-L., Han, A., Glanville, J., Fang, F., Zuniga, L. A., Lee, J. S., Cua, D. J. et al., A highly focused antigen receptor repertoire characterizes γδ T cells that are poised to make IL-17 rapidly in naive animals. Front. Immunol. 2015 [cited 2023 Mar 16];6. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2015.00118
Sefik, E., Geva-Zatorsky, N., Oh, S., Konnikova, L., Zemmour, D., Mcguire, A. M., Burzyn, D. et al., Individual intestinal symbionts induce a distinct population of RORγ+ regulatory T cells. Science. 2015. 349: 993-997.
Izcue, A., Hue, S., Buonocore, S., Arancibia-Cárcamo, C. V., Ahern, P. P., Iwakura, Y., Maloy, K. J. et al., Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity. 2008. 28: 559-570.
Wu, C., Chen, Z., Xiao, S., Thalhamer, T., Madi, A., Han, T. and Kuchroo, V., SGK1 governs the reciprocal development of Th17 and regulatory T cells. Cell Rep. 2018. 22: 653-665.
Kannan, A. K., Su, Z., Gauvin, D. M., Paulsboe, S. E., Duggan, R., Lasko, L. M., Honore, P. et al., IL-23 induces regulatory T cell plasticity with implications for inflammatory skin diseases. Sci. Rep. 2019. 9: 17675.
Dong, S., Maiella, S., Xhaard, A., Pang, Y., Wenandy, L., Larghero, J., Becavin, C. et al., Multiparameter single-cell profiling of human CD4+FOXP3+ regulatory T-cell populations in homeostatic conditions and during graft-versus-host disease. Blood. 2013. 122: 1802-1812.
Alfen, J. S., Larghi, P., Facciotti, F., Gagliani, N., Bosotti, R., Paroni, M., Maglie, S. et al., Intestinal IFN-γ-producing type 1 regulatory T cells coexpress CCR5 and programmed cell death protein 1 and downregulate IL-10 in the inflamed guts of patients with inflammatory bowel disease. J. Allergy Clin. Immunol. 2018. 142: 1537-1547. e8.
Curtis, M. M., Way, S. S. and Wilson, C. B., IL-23 promotes the production of IL-17 by antigen-specific CD8 T cells in the absence of IL-12 and type-I interferons. J. Immunol. 2009. 183: 381-387.
Chognard, G., Bellemare, L., Pelletier, A.-N., Dominguez-Punaro, M. C., Beauchamp, C., Guyon, M.-J., Charron, G. et al., The dichotomous pattern of IL-12R and IL-23R expression elucidates the role of IL-12 and IL-23 in inflammation. PLoS One. 2014. 9: e89092.
Shen, H., Zhang, W., Abraham, C. and Cho, J. H., Age and CD161 expression contribute to inter-individual variation in interleukin-23 response in CD8+ memory human T cells. PLoS One. 2013. 8: e57746.
Steel, K. J. A., Srenathan, U., Ridley, M., Durham, L. E., Wu, S. Y., Ryan, S. E., Hughes, C. D. et al., Polyfunctional, proinflammatory, tissue-resident memory phenotype and function of synovial interleukin-17A+CD8+ T cells in psoriatic arthritis. Arthritis Rheumatol. 2020. 72: 435-447.
Ball, J. A., Clear, A., Aries, J., Charrot, S., Besley, C., Mee, M., Stagg, A. et al., Retinoic acid-responsive CD8 effector T cells are selectively increased in IL-23-rich tissue in gastrointestinal GVHD. Blood. 2021. 137: 702-717.
Ben Youssef, G., Tourret, M., Salou, M., Ghazarian, L., Houdouin, V., Mondot, S., Mburu, Y. et al., Ontogeny of human mucosal-associated invariant T cells and related T cell subsets. J. Exp. Med. 2018. 215: 459-479.
Wang, H., Kjer-Nielsen, L., Shi, M., D'souza, C., Pediongco, T. J., Cao, H., Kostenko, L. et al., IL-23 costimulates antigen-specific MAIT cell activation and enables vaccination against bacterial infection. Sci. Immunol. 2019. 4: eaaw0402.
Leng, T., Akther, H. D., Hackstein, C.-P., Powell, K., King, T., Friedrich, M., Christoforidou, Z. et al., TCR and inflammatory signals tune human MAIT cells to exert specific tissue repair and effector functions. Cell Rep. 2019. 28: 3077-3091. e5.
Salou, M., Legoux, F., Gilet, J., Darbois, A., Du Halgouet, A., Alonso, R., Richer, W. et al., A common transcriptomic program acquired in the thymus defines tissue residency of MAIT and NKT subsets. J. Exp. Med. 2019. 216: 133-151.
Chen, L., He, Z., Slinger, E., Bongers, G., Lapenda, T. L., Pacer, M. E., Jiao, J. et al., IL-23 activates innate lymphoid cells to promote neonatal intestinal pathology. Mucosal Immunol. 2015. 8: 390-402.
Beckstette, M., Lu, C.-W., Herppich, S., Diem, E. C., Ntalli, A., Ochel, A., Kruse, F. et al., Profiling of epigenetic marker regions in murine ILCs under homeostatic and inflammatory conditions. J. Exp. Med. 2022. 219: e20210663.
Garner, L. C., Amini, A., Fitzpatrick, M. E. B., Lett, M. J., Hess, G. F., Filipowicz Sinnreich, M., Provine, N. M. et al., Single-cell analysis of human MAIT cell transcriptional, functional and clonal diversity. Nat. Immunol. 2023. 24: 1565-1578.
Slichter, C. K., Mcdavid, A., Miller, H. W., Finak, G., Seymour, B. J., Mcnevin, J. P., Diaz, G. et al., Distinct activation thresholds of human conventional and innate-like memory T cells. JCI Insight. 2016 Jun 2 [cited 2023 May 25];1. Available from: https://insight.jci.org/articles/view/86292
Constantinides, M. G., Link, V. M., Tamoutounour, S., Wong, A. C., Perez-Chaparro, P. J., Han, S.-J., Chen, Y. E. et al., MAIT cells are imprinted by the microbiota in early life and promote tissue repair. Science. 2019. 366: eaax6624.
Meermeier, E. W., Zheng, C. L., Tran, J. G., Soma, S., Worley, A. H., Weiss, D. I., Modlin, R. L. et al., Human lung-resident mucosal-associated invariant T cells are abundant, express antimicrobial proteins, and are cytokine responsive. Commun. Biol. 2022. 5: 1-13.
Raychaudhuri, S. K., Abria, C., Mitra, A. and Raychaudhuri, S. P., Functional significance of MAIT cells in psoriatic arthritis. Cytokine. 2020. 125: 154855.
Petermann, F., Rothhammer, V., Claussen, M. C., Haas, J. D., Blanco, L. R., Heink, S., Prinz, I. et al., γδ T cells enhance autoimmunity by restraining regulatory T cell responses via an interleukin-23-dependent mechanism. Immunity. 2010. 33: 351-363.
Moens, E., Brouwer, M., Dimova, T., Goldman, M., Willems, F. and Vermijlen, D., IL-23R and TCR signaling drives the generation of neonatal Vγ9Vδ2 T cells expressing high levels of cytotoxic mediators and producing IFN-γ and IL-17. J. Leukocyte Biol. 2011. 89: 743-752.
Awasthi, A., Riol-Blanco, L., JäGer, A., Korn, T., Pot, C., Galileos, G., Bettelli, E. et al., Cutting edge: IL-23 receptor GFP reporter mice reveal distinct populations of IL-17-producing cells. J. Immunol. 2009. 182: 5904-5908.
Lockhart, E., Green, A. M. and Flynn, J. L., IL-17 Production is dominated by γδ T cells rather than CD4 T cells during mycobacterium tuberculosis infection1. J. Immunol. 2006. 177: 4662-4669.
Sutton, C. E., Lalor, S. J., Sweeney, C. M., Brereton, C. F., Lavelle, E. C. and Mills, K. H. G., Interleukin-1 and IL-23 induce innate IL-17 production from γδ T cells, amplifying Th17 responses and autoimmunity. Immunity. 2009. 31: 331-341.
Liang, D., Zuo, A., Shao, H., Born, W. K., O'brien, R. L., Kaplan, H. J. and Sun, D., IL-23 receptor expression on γδ T cells correlates with their enhancing or suppressive effects on autoreactive T cells in experimental autoimmune uveitis. J. Immunol. 2013. 191: 1118-1125.
Cai, Y., Xue, F., Fleming, C., Yang, J., Ding, C., Ma, Y., Liu, M. et al., Differential developmental requirement and peripheral regulation for dermal Vγ4 and Vγ6T17 cells in health and inflammation. Nat. Commun. 2014. 5: 3986.
Riol-Blanco, L., Lazarevic, V., Awasthi, A., Mitsdoerffer, M., Wilson, B. S., Croxford, A. et al., IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. JI. 2010. 184: 1710-1720.
Cuthbert, R. J., Watad, A., Fragkakis, E. M., Dunsmuir, R., Loughenbury, P., Khan, A., Millner, P. A. et al., Evidence that tissue resident human enthesis γδT-cells can produce IL-17A independently of IL-23R transcript expression. Ann. Rheum. Dis. 2019. 78: 1559-1565.
Venken, K., Jacques, P., Mortier, C., Labadia, M. E., Decruy, T., Coudenys, J., Hoyt, K. et al., RORγt inhibition selectively targets IL-17 producing iNKT and γδ-T cells enriched in Spondyloarthritis patients. Nat. Commun. 2019. 10: 9.
Zhang, L., Yan, J., Yang, B., Zhang, G., Wang, M., Dong, S., Liu, W. et al., IL-23 activated γδ T cells affect Th17 cells and regulatory T cells by secreting IL-21 in children with primary nephrotic syndrome. Scand. J. Immunol. 2018. 87: 36-45.
Edwards, S. C., Sutton, C. E., Ladell, K., Grant, E. J., Mclaren, J. E., Roche, F., Dash, P. et al., A population of proinflammatory T cells coexpresses αβ and γδ T cell receptors in mice and humans. J. Exp. Med. 2020. 217: e20190834.
Rachitskaya, A. V., Hansen, A. M., Horai, R., Li, Z., Villasmil, R., Luger, D., Nussenblatt, R. B. et al., Cutting edge: NKT cells constitutively express IL-23 receptor and RORγt and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J. Immunol. 2008. 180: 5167-5171.
Van De Wetering, D., De Paus, R. A., Van Dissel, J. T. and Van De Vosse, E., IL-23 modulates CD56+/CD3- NK cell and CD56+/CD3+ NK-like T cell function differentially from IL-12. Int. Immunol. 2009. 21: 145-153.
Buonocore, S., Ahern, P. P., Uhlig, H. H., Ivanov, I. I., Littman, D. R., Maloy, K. J. and Powrie, F., Innate lymphoid cells drive IL-23 dependent innate intestinal pathology. Nature. 2010. 464: 1371-1375.
Bauché, D., Joyce-Shaikh, B., Fong, J., Villarino, A. V., Ku, K. S., Jain, R., Lee, Y.-C. et al., IL-23 and IL-2 activation of STAT5 is required for optimal IL-22 production in ILC3s during colitis. Sci. Immunol. 2020. 5: eaav1080.
Eken, A., Singh, A. K., Treuting, P. M. and Oukka, M., IL-23R+ innate lymphoid cells induce colitis via interleukin-22-dependent mechanism. Mucosal Immunol. 2014. 7: 143-154.
Blijdorp, I. C. J., Menegatti, S., Van Mens, L. J. J., Van De Sande, M. G. H., Chen, S., Hreggvidsdottir, H. S., Noordenbos, T. et al., Expansion of interleukin-22- and granulocyte-macrophage colony-stimulating factor-expressing, but not interleukin-17A-expressing, group 3 innate lymphoid cells in the inflamed joints of patients with spondyloarthritis. Arthritis Rheumatol. 2019. 71: 392-402.
Bernink, J. H., Ohne, Y., Teunissen, M. B. M., Wang, J., Wu, J., Krabbendam, L., Guntermann, C. et al., c-Kit-positive ILC2s exhibit an ILC3-like signature that may contribute to IL-17-mediated pathologies. Nat. Immunol. 2019. 20: 992-1003.
Croft, C. A., Thaller, A., Marie, S., Doisne, J.-M., Surace, L., Yang, R., Puel, A. et al., Notch, RORC and IL-23 signals cooperate to promote multi-lineage human innate lymphoid cell differentiation. Nat. Commun. 2022. 13: 4344.
Ziblat, A., Nuñez, S. Y., Raffo Iraolagoitia, X. L., Spallanzani, R. G., Torres, N. I., Sierra, J. M., Secchiari, F. et al., Interleukin (IL)-23 stimulates IFN-γ secretion by CD56bright natural killer cells and enhances IL-18-driven dendritic cells activation. Front. Immunol. 2018. 8: 1959.
Cocco, C., Canale, S., Frasson, C., Di Carlo, E., Ognio, E., Ribatti, D., Prigione, I. et al., Interleukin-23 acts as antitumor agent on childhood B-acute lymphoblastic leukemia cells. Blood. 2010. 116: 3887-3898.
Cutrona, G., Tripodo, C., Matis, S., Recchia, A. G., Massucco, C., Fabbi, M., Colombo, M. et al., Microenvironmental regulation of the IL-23R/IL-23 axis overrides chronic lymphocytic leukemia indolence. Sci. Transl. Med. 2018. 10: eaal1571.
Cocco, C., Morandi, F. and Airoldi, I., Interleukin-27 and interleukin-23 modulate human plasma cell functions. J Leukoc Biol. 2011. 89: 729-734.
Leitner, M., Heck, S., Nguyen, K., Nguyen, P. Q., Harfoush, S., Rosenkranz, E., Bals, R. et al., Allergic airway inflammation induces upregulation of the expression of IL-23R by macrophages and not in CD3 + T cells and CD11c+F4/80- dendritic cells of the lung. Cell Tissue Res. 2022. 389: 85-98.
Schmiedel, B. J., Singh, D., Madrigal, A., Valdovino-Gonzalez, A. G., White, B. M., Zapardiel-Gonzalo, J., Ha, B. et al., Impact of genetic polymorphisms on human immune cell gene expression. Cell. 2018. 175: 1701-1715. e16.
Uhlén, M., Fagerberg, L., Hallström, B. M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, Å. et al., Proteomics. Tissue-based map of the human proteome. Science. 2015. 347: 1260419.
Sun, R. and Abraham, C., IL23 promotes antimicrobial pathways in human macrophages, which are reduced with the IBD-protective IL23R R381Q variant. Cell Mol Gastroenterol Hepatol. 2020. 10: 673-697.
Sun, R., Hedl, M. and Abraham, C., IL23 induces IL23R recycling and amplifies innate receptor-induced signalling and cytokines in human macrophages, and the IBD-protective IL23R R381Q variant modulates these outcomes. Gut. 2020. 69: 264-273.
Wang, C., Liu, T., Wang, Z., Li, W., Zhao, Q., Mi, Z. et al., IL-23/IL23R promote macrophage pyroptosis and Th1/Th17 cell differentiation in mycobacterial infection. J. Invest. Dermatol. 2023 May 12 [cited 2023 May 19];0(0). Available from: https://www.jidonline.org/article/S0022-202X(23)02062-6/fulltext
Bao, S., Zheng, J., Li, N., Huang, C., Chen, M., Cheng, Q., Li, Q. et al., Role of interleukin-23 in monocyte-derived dendritic cells of HBV-related acute-on-chronic liver failure and its correlation with the severity of liver damage. Clin. Res. Hepatol. Gastroenterol. 2017. 41: 147-155.
Belladonna, M. L., Renauld, J.-C., Bianchi, R., Vacca, C., Fallarino, F., Orabona, C., Fioretti, M. C. et al., IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells1. J. Immunol. 2002. 168: 5448-5454.
Li, Y., Zhu, L., Chu, Z., Yang, T., Sun, H.-X., Yang, F., Wang, W. et al., Characterization and biological significance of IL-23-induced neutrophil polarization. Cell Mol Immunol. 2018. 15: 518-530.
Yadav, B., Specht, C. A., Lee, C. K., Pokrovskii, M., Huh, J. R., Littman, D. R. and Levitz, S. M., Lung eosinophils elicited during allergic and acute aspergillosis express RORγt and IL-23R but do not require IL-23 for IL-17 production. PLoS Pathog. 2021. 17: e1009891.
Glasmacher, E., Agrawal, S., Chang, A. B., Murphy, T. L., Zeng, W., Vander Lugt, B., Khan, A. A. et al., A genomic regulatory element that directs assembly and function of immune-specific AP-1-IRF complexes. Science. 2012. 338: 975-980.
Li, P., Spolski, R., Liao, W., Wang, L., Murphy, T. L., Murphy, K. M. and Leonard, W. J., BATF-JUN is critical for IRF4-mediated transcription in T cells. Nature. 2012. 490: 543-546.
Ciofani, M., Madar, A., Galan, C., Sellars, M., Mace, K., Pauli, F., Agarwal, A. et al., A validated regulatory network for Th17 cell specification. Cell. 2012. 151: 289-303.
Pham, D., Moseley, C. E., Gao, M., Savic, D., Winstead, C. J., Sun, M., Kee, B. L. et al., Batf pioneers the reorganization of chromatin in developing effector T cells via Ets1-dependent recruitment of Ctcf. Cell Rep. 2019. 29: 1203-1220. e7.
Hall, J. A., Pokrovskii, M., Kroehling, L., Kim, Bo-R, Kim, S. Y., Wu, L., Lee, J.-Y. et al., Transcription factor RORα enforces stability of the Th17 cell effector program by binding to a Rorc cis-regulatory element. Immunity. 2022. 55: 2027-2043. e9.
Xiao, S., Yosef, N., Yang, J., Wang, Y., Zhou, L., Zhu, C., Wu, C. et al., Small-molecule RORγt antagonists inhibit T helper 17 cell transcriptional network by divergent mechanisms. Immunity. 2014. 40: 477-489.
Gocke, A. R., Cravens, P. D., Ben, L.-H., Hussain, R. Z., Northrop, S. C., Racke, M. K. and Lovett-Racke, A. E., T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J. Immunol. 2007. 178: 1341-1348.
Krausgruber, T., Schiering, C., Adelmann, K., Harrison, O. J., Chomka, A., Pearson, C., Ahern, P. P. et al., T-bet is a key modulator of IL-23-driven pathogenic CD4 + T cell responses in the intestine. Nat. Commun. 2016. 7: 11627.
Gökmen, M. R., Dong, R., Kanhere, A., Powell, N., Perucha, E., Jackson, I., Howard, J. K. et al., Genome-wide regulatory analysis reveals that T-bet controls Th17 lineage differentiation through direct suppression of IRF4. J. Immunol. 2013. 191: 5925-5932.
Moon, Y.-M., Lee, S.-Y., Kwok, S.-K., Lee, S. H., Kim, D., Kim, W. K., Her, Y.-M. et al., The Fos-related antigen 1-JUNB/activator protein 1 transcription complex, a downstream target of signal transducer and activator of transcription 3, induces T helper 17 differentiation and promotes experimental autoimmune arthritis. Front. Immunol. 2017. 8: 1793.
Shetty, A., Tripathi, S. K., Junttila, S., Buchacher, T., Biradar, R., Bhosale, S. D., Envall, T. et al., A systematic comparison of FOSL1, FOSL2 and BATF-mediated transcriptional regulation during early human Th17 differentiation. Nucleic. Acids. Res. 2022. 50: 4938-4958.
Ghoreschi, K., Laurence, A., Yang, X.-P., Tato, C. M., Mcgeachy, M. J., Konkel, J. E., Ramos, H. L. et al., Generation of pathogenic Th17 cells in the absence of TGF-β Signaling. Nature. 2010. 467: 967-971.
Newcomb, D. C., Cephus, J. Y., Boswell, M. G., Fahrenholz, J. M., Langley, E. W., Feldman, A. S., Zhou, W. et al., Estrogen and progesterone decrease let-7f microRNA expression and increase IL-23/IL-23 receptor signaling and IL-17A production in patients with severe asthma. J. Allergy Clin. Immunol. 2015. 136: 1025-1034. e11.
Fuseini, H., Cephus, J.-Y., Wu, P., Davis, J. B., Contreras, D. C., Gandhi, V. D., Rathmell, J. C. et al., ERα signaling increased IL-17A production in Th17 cells by upregulating IL-23R expression, mitochondrial respiration, and proliferation. Front. Immunol. 2019. 10: 2740.
Angelou, C. C., Wells, A. C., Vijayaraghavan, J., Dougan, C. E., Lawlor, R., Iverson, E., Lazarevic, V. et al., Differentiation of pathogenic Th17 cells is negatively regulated by Let-7 MicroRNAs in a mouse model of multiple sclerosis. Front. Immunol. 2019. 10: 3125.
Wang, L., Wang, E., Wang, Y., Mines, R., Xiang, K., Sun, Z., Zhou, G. et al., miR-34a is a microRNA safeguard for Citrobacter-induced inflammatory colon oncogenesis. eLife. 2018. 7: e39479.
Matis, S., Grazia Recchia, A., Colombo, M., Cardillo, M., Fabbi, M., Todoerti, K., Bossio, S. et al., MiR-146b-5p regulates IL-23 receptor complex expression in chronic lymphocytic leukemia cells. Blood Adv. 2022. 6: 5593-5612.
Hasan, Z., Koizumi, S.-I., Sasaki, D., Yamada, H., Arakaki, N., Fujihara, Y., Okitsu, S. et al., JunB is essential for IL-23-dependent pathogenicity of Th17 cells. Nat. Commun. 2017. 8: 15628.
Carr, T. M., Wheaton, J. D., Houtz, G. M. and Ciofani, M., JunB promotes Th17 cell identity and restrains alternative CD4+ T-cell programs during inflammation. Nat. Commun. 2017. 8: 301.
Dang, E. V., Barbi, J., Yang, H.-Y., Jinasena, D., Yu, H., Zheng, Y., Bordman, Z. et al., Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell. 2011. 146: 772-784.
Meyer Zu Horste, G., Wu, C., Wang, C., Cong, L., Pawlak, M., Lee, Y., Elyaman, W. et al., RBPJ controls development of pathogenic Th17 cells by regulating IL-23 receptor expression. Cell Rep. 2016. 16: 392-404.
Ando, N., Nakamura, Y., Aoki, R., Ishimaru, K., Ogawa, H., Okumura, Ko, Shibata, S. et al., Circadian gene clock regulates psoriasis-like skin inflammation in mice. J. Invest. Dermatol. 2015. 135: 3001-3008.
Snyder, K. J., Choe, H. K., Gao, Y., Sell, N. E., Braunreiter, K. M., Zitzer, N. C., Neidemire-Colley, L. et al., Inhibition of bromodomain and extra terminal (BET) domain activity modulates the IL-23R/IL-17 axis and suppresses acute graft-versus-host disease. Front. Oncol. 2021. 11: 760789.