CTLA-4-expressing ILC3s restrain interleukin-23-mediated inflammation.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
12 Jun 2024
Historique:
received: 18 04 2023
accepted: 07 05 2024
medline: 13 6 2024
pubmed: 13 6 2024
entrez: 12 6 2024
Statut: aheadofprint

Résumé

Interleukin (IL-)23 is a major mediator and therapeutic target in chronic inflammatory diseases that also elicits tissue protection in the intestine at homeostasis or following acute infection

Identifiants

pubmed: 38867048
doi: 10.1038/s41586-024-07537-3
pii: 10.1038/s41586-024-07537-3
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Investigateurs

David Artis (D)
Randy Longman (R)
Gregory F Sonnenberg (GF)
Ellen Scherl (E)
Robbyn Sockolow (R)
Dana Lukin (D)
Vinita Jacob (V)
Laura Sahyoun (L)
Michael Mintz (M)
Lasha Gogokhia (L)
Thomas Ciecierega (T)
Aliza Solomon (A)
Arielle Bergman (A)
Kimberley Chein (K)
Elliott Gordon (E)
Michelle Ramos (M)
Victoria Ribeiro de Godoy (VR)
Adriana Brcic-Susak (A)
Seun Oguntunmibi (S)
Dario Garone (D)
Caitlin Mason (C)

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Abraham, C. & Cho, J. H. IL-23 and autoimmunity: new insights into the pathogenesis of inflammatory bowel disease. Annu. Rev. Med. 60, 97–110 (2009).
pubmed: 18976050 doi: 10.1146/annurev.med.60.051407.123757
Maloy, K. J. & Powrie, F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474, 298–306 (2011).
pubmed: 21677746 doi: 10.1038/nature10208
Maynard, C. L., Elson, C. O., Hatton, R. D. & Weaver, C. T. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489, 231–241 (2012).
pubmed: 22972296 pmcid: 4492337 doi: 10.1038/nature11551
Fragoulis, G. E., Siebert, S. & McInnes, I. B. Therapeutic targeting of IL-17 and IL-23 cytokines in immune-mediated diseases. Annu. Rev. Med. 67, 337–353 (2016).
pubmed: 26565676 doi: 10.1146/annurev-med-051914-021944
Bernink, J. H. et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat. Immunol. 14, 221–229 (2013).
pubmed: 23334791 doi: 10.1038/ni.2534
Takayama, T. et al. Imbalance of NKp44
pubmed: 20638936 doi: 10.1053/j.gastro.2010.05.040
Zhou, L. et al. Innate lymphoid cells support regulatory T cells in the intestine through interleukin-2. Nature 568, 405–409 (2019).
pubmed: 30944470 pmcid: 6481643 doi: 10.1038/s41586-019-1082-x
Oppmann, B. 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 13, 715–725 (2000).
pubmed: 11114383 doi: 10.1016/S1074-7613(00)00070-4
Neurath, M. F. IL-23: a master regulator in Crohn disease. Nat. Med. 13, 26–28 (2007).
pubmed: 17206128 doi: 10.1038/nm0107-26
Krueger, G. G. et al. A human interleukin-12/23 monoclonal antibody for the treatment of psoriasis. N. Engl. J. Med. 356, 580–592 (2007).
pubmed: 17287478 doi: 10.1056/NEJMoa062382
Lubberts, E. The IL-23-IL-17 axis in inflammatory arthritis. Nat. Rev. Rheumatol. 11, 415–429 (2015).
pubmed: 25907700 doi: 10.1038/nrrheum.2015.53
Cua, D. J. et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744–748 (2003).
pubmed: 12610626 doi: 10.1038/nature01355
Duerr, R. H. et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314, 1461–1463 (2006).
pubmed: 17068223 pmcid: 4410764 doi: 10.1126/science.1135245
The Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447, 661–678 (2007).
pmcid: 2719288 doi: 10.1038/nature05911
D’Haens, G. et al. Risankizumab as induction therapy for Crohn’s disease: results from the phase 3 ADVANCE and MOTIVATE induction trials. Lancet 399, 2015–2030 (2022).
pubmed: 35644154 doi: 10.1016/S0140-6736(22)00467-6
Feagan, B. G. et al. Ustekinumab as induction and maintenance therapy for Crohn’s disease. N. Engl. J. Med. 375, 1946–1960 (2016).
pubmed: 27959607 doi: 10.1056/NEJMoa1602773
Sands, B. E. et al. Ustekinumab as induction and maintenance therapy for ulcerative colitis. N. Engl. J. Med. 381, 1201–1214 (2019).
pubmed: 31553833 doi: 10.1056/NEJMoa1900750
Shih, V. F. et al. Homeostatic IL-23 receptor signaling limits Th17 response through IL-22-mediated containment of commensal microbiota. Proc. Natl Acad. Sci. USA 111, 13942–13947 (2014).
pubmed: 25201978 pmcid: 4183330 doi: 10.1073/pnas.1323852111
Mangan, P. R. et al. Transforming growth factor-β induces development of the T
pubmed: 16648837 doi: 10.1038/nature04754
Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282–289 (2008).
pubmed: 18264109 doi: 10.1038/nm1720
Sonnenberg, G. F., Monticelli, L. A., Elloso, M. M., Fouser, L. A. & Artis, D. CD4
pubmed: 21194981 doi: 10.1016/j.immuni.2010.12.009
Cox, J. H. et al. Opposing consequences of IL-23 signaling mediated by innate and adaptive cells in chemically induced colitis in mice. Mucosal Immunol. 5, 99–109 (2012).
pubmed: 22089030 doi: 10.1038/mi.2011.54
Izcue, A. et al. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 28, 559–570 (2008).
pubmed: 18400195 pmcid: 2292821 doi: 10.1016/j.immuni.2008.02.019
Martínez-Barricarte, R. et al. Human IFN-γ immunity to mycobacteria is governed by both IL-12 and IL-23. Sci. Immunol. 3, eaau6759 (2018).
pubmed: 30578351 doi: 10.1126/sciimmunol.aau6759
Mao, K. et al. Innate and adaptive lymphocytes sequentially shape the gut microbiota and lipid metabolism. Nature 554, 255–259 (2018).
pubmed: 29364878 doi: 10.1038/nature25437
Sawa, S. et al. RORγt
pubmed: 21336274 doi: 10.1038/ni.2002
Sonnenberg, G. F. & Artis, D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat. Med. 21, 698–708 (2015).
pubmed: 26121198 pmcid: 4869856 doi: 10.1038/nm.3892
Spits, H. et al. Innate lymphoid cells—a proposal for uniform nomenclature. Nat. Rev. Immunol. 13, 145–149 (2013).
pubmed: 23348417 doi: 10.1038/nri3365
Kerdiles, Y. M. et al. Foxo transcription factors control regulatory T cell development and function. Immunity 33, 890–904 (2010).
pubmed: 21167754 pmcid: 3034255 doi: 10.1016/j.immuni.2010.12.002
Hossain, D. M. et al. FoxP3 acts as a cotranscription factor with STAT3 in tumor-induced regulatory T cells. Immunity 39, 1057–1069 (2013).
pubmed: 24315995 doi: 10.1016/j.immuni.2013.11.005
Jacobse, J. et al. Interleukin-23 receptor signaling impairs the stability and function of colonic regulatory T cells. Cell Rep. 42, 112128 (2023).
pubmed: 36807140 pmcid: 10432575 doi: 10.1016/j.celrep.2023.112128
Kannan, A. K. et al. IL-23 induces regulatory T cell plasticity with implications for inflammatory skin diseases. Sci. Rep. 9, 17675 (2019).
pubmed: 31776355 pmcid: 6881359 doi: 10.1038/s41598-019-53240-z
Uhlig, H. H. et al. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 25, 309–318 (2006).
pubmed: 16919486 doi: 10.1016/j.immuni.2006.05.017
Ahern, P. P. et al. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33, 279–288 (2010).
pubmed: 20732640 pmcid: 3078329 doi: 10.1016/j.immuni.2010.08.010
Wing, K. et al. CTLA-4 control over Foxp3
pubmed: 18845758 doi: 10.1126/science.1160062
Walker, L. S. & Sansom, D. M. The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nat. Rev. Immunol. 11, 852–863 (2011).
pubmed: 22116087 doi: 10.1038/nri3108
Chang, T. T., Jabs, C., Sobel, R. A., Kuchroo, V. K. & Sharpe, A. H. Studies in B7-deficient mice reveal a critical role for B7 costimulation in both induction and effector phases of experimental autoimmune encephalomyelitis. J. Exp. Med. 190, 733–740 (1999).
pubmed: 10477557 pmcid: 2195617 doi: 10.1084/jem.190.5.733
Lenschow, D. J. et al. CD28/B7 regulation of Th1 and Th2 subsets in the development of autoimmune diabetes. Immunity 5, 285–293 (1996).
pubmed: 8808683 doi: 10.1016/S1074-7613(00)80323-4
Tekguc, M., Wing, J. B., Osaki, M., Long, J. & Sakaguchi, S. Treg-expressed CTLA-4 depletes CD80/CD86 by trogocytosis, releasing free PD-L1 on antigen-presenting cells. Proc. Natl Acad. Sci. USA 118, e2023739118 (2021).
pubmed: 34301886 pmcid: 8325248 doi: 10.1073/pnas.2023739118
Sugiura, D. et al. Restriction of PD-1 function by cis-PD-L1/CD80 interactions is required for optimal T cell responses. Science 364, 558–566 (2019).
pubmed: 31000591 doi: 10.1126/science.aav7062
Francisco, L. M. et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J. Exp. Med. 206, 3015–3029 (2009).
pubmed: 20008522 pmcid: 2806460 doi: 10.1084/jem.20090847
Keir, M. E. et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203, 883–895 (2006).
pubmed: 16606670 pmcid: 2118286 doi: 10.1084/jem.20051776
Lyu, M. et al. ILC3s select microbiota-specific regulatory T cells to establish tolerance in the gut. Nature 610, 744–751 (2022).
pubmed: 36071169 pmcid: 9613541 doi: 10.1038/s41586-022-05141-x
Paustian, A. M. S. et al. Continuous IL-23 stimulation drives ILC3 depletion in the upper GI tract and, in combination with TNFα, induces robust activation and a phenotypic switch of ILC3. PLoS ONE 12, e0182841 (2017).
pubmed: 28792532 pmcid: 5549730 doi: 10.1371/journal.pone.0182841
Jacquelot, N. et al. Immune checkpoints and innate lymphoid cells—new avenues for cancer immunotherapy. Cancers (Basel) 13, 5967 (2021).
pubmed: 34885076 doi: 10.3390/cancers13235967
Hepworth, M. R. et al. Immune tolerance. Group 3 innate lymphoid cells mediate intestinal selection of commensal bacteria-specific CD4
pubmed: 25908663 pmcid: 4449822 doi: 10.1126/science.aaa4812
Goc, J. et al. Dysregulation of ILC3s unleashes progression and immunotherapy resistance in colon cancer. Cell 184, 5015–5030.e5016 (2021).
pubmed: 34407392 pmcid: 8454863 doi: 10.1016/j.cell.2021.07.029
Kløverpris, H. N. et al. Innate lymphoid cells are depleted irreversibly during acute HIV-1 infection in the absence of viral suppression. Immunity 44, 391–405 (2016).
pubmed: 26850658 pmcid: 6836297 doi: 10.1016/j.immuni.2016.01.006
Page, D. B., Postow, M. A., Callahan, M. K., Allison, J. P. & Wolchok, J. D. Immune modulation in cancer with antibodies. Annu. Rev. Med. 65, 185–202 (2014).
pubmed: 24188664 doi: 10.1146/annurev-med-092012-112807
Lo, B. C. et al. Microbiota-dependent activation of CD4
pubmed: 38175892 doi: 10.1126/science.adh8342
Mombaerts, P. et al. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68, 869–877 (1992).
pubmed: 1547488 doi: 10.1016/0092-8674(92)90030-G
Kühn, R., Löhler, J., Rennick, D., Rajewsky, K. & Müller, W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263–274 (1993).
pubmed: 8402911 doi: 10.1016/0092-8674(93)80068-P
Awasthi, A. et al. Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J. Immunol. 182, 5904–5908 (2009).
pubmed: 19414740 doi: 10.4049/jimmunol.0900732
Lochner, M. et al. In vivo equilibrium of proinflammatory IL-17
pubmed: 18504307 pmcid: 2413035 doi: 10.1084/jem.20080034
Narni-Mancinelli, E. et al. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl Acad. Sci. USA 108, 18324–18329 (2011).
pubmed: 22021440 pmcid: 3215049 doi: 10.1073/pnas.1112064108
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018).
pubmed: 29608179 pmcid: 6700744 doi: 10.1038/nbt.4096

Auteurs

Anees Ahmed (A)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA.

Ann M Joseph (AM)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA.

Jordan Zhou (J)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA.

Veronika Horn (V)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA.

Jazib Uddin (J)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA.

Mengze Lyu (M)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA.

Jeremy Goc (J)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA.

Robbyn E Sockolow (RE)

Department of Pediatrics, Division of Gastroenterology, Hepatology, & Nutrition, Weill Cornell Medicine, Cornell University, New York, NY, USA.

James B Wing (JB)

Laboratory of Experimental Immunology, World Premier International Immunology Frontier Research Center, Osaka University, Suita, Japan.
Laboratory of Human Single Cell Immunology, WPI IFReC, Osaka University, Suita, Japan.
Human Single Cell Immunology Team, Center for Infectious Disease Education and Research, Osaka University, Suita, Japan.

Eric Vivier (E)

Innate Pharma Research Laboratories, Innate Pharma, Marseille, France.
Aix Marseille University, CNRS, INSERM, CIML, Marseille, France.
APHM, Hôpital de la Timone, Marseille-Immunopôle, Marseille, France.
Paris Saclay Cancer Cluster, Villejuif, France.

Shimon Sakaguchi (S)

Laboratory of Experimental Immunology, World Premier International Immunology Frontier Research Center, Osaka University, Suita, Japan.
Department of Experimental Pathology, Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan.

Gregory F Sonnenberg (GF)

Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology & Hepatology, Weill Cornell Medicine, Cornell University, New York, NY, USA. gfsonnenberg@med.cornell.edu.
Department of Microbiology & Immunology, Weill Cornell Medicine, Cornell University, New York, NY, USA. gfsonnenberg@med.cornell.edu.
Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, Cornell University, New York, NY, USA. gfsonnenberg@med.cornell.edu.

Classifications MeSH