The transcription factor Aiolos restrains the activation of intestinal intraepithelial lymphocytes.


Journal

Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354

Informations de publication

Date de publication:
04 Dec 2023
Historique:
received: 06 12 2022
accepted: 27 10 2023
medline: 5 12 2023
pubmed: 5 12 2023
entrez: 4 12 2023
Statut: aheadofprint

Résumé

Intestinal intraepithelial lymphocytes (IELs) exhibit prompt innate-like responses to microenvironmental cues and require strict control of effector functions. Here we showed that Aiolos, an Ikaros zinc-finger family member encoded by Ikzf3, acted as a regulator of IEL activation. Ikzf3

Identifiants

pubmed: 38049581
doi: 10.1038/s41590-023-01693-w
pii: 10.1038/s41590-023-01693-w
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIAID NIH HHS
ID : U19 AI142733
Pays : United States

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.

Références

Mayassi, T. & Jabri, B. Human intraepithelial lymphocytes. Mucosal Immunol. 11, 1281–1289 (2018).
pubmed: 29674648 pmcid: 6178824 doi: 10.1038/s41385-018-0016-5
Olivares-Villagomez, D. & Van Kaer, L. Intestinal intraepithelial lymphocytes: sentinels of the mucosal barrier. Trends Immunol. 39, 264–275 (2018).
pubmed: 29221933 doi: 10.1016/j.it.2017.11.003
Colonna, M. Innate lymphoid cells: diversity, plasticity, and unique functions in immunity. Immunity 48, 1104–1117 (2018).
pubmed: 29924976 pmcid: 6344351 doi: 10.1016/j.immuni.2018.05.013
Cheroutre, H., Lambolez, F. & Mucida, D. The light and dark sides of intestinal intraepithelial lymphocytes. Nat. Rev. Immunol. 11, 445–456 (2011).
pubmed: 21681197 pmcid: 3140792 doi: 10.1038/nri3007
McDonald, B. D., Jabri, B. & Bendelac, A. Diverse developmental pathways of intestinal intraepithelial lymphocytes. Nat. Rev. Immunol. 18, 514–525 (2018).
pubmed: 29717233 pmcid: 6063796 doi: 10.1038/s41577-018-0013-7
McFarland, A. P. et al. Multi-tissue single-cell analysis deconstructs the complex programs of mouse natural killer and type 1 innate lymphoid cells in tissues and circulation. Immunity 54, 1320–1337 (2021).
pubmed: 33945787 pmcid: 8312473 doi: 10.1016/j.immuni.2021.03.024
Van Acker, A. et al. A murine intestinal intraepithelial NKp46-negative innate lymphoid cell population characterized by group 1 properties. Cell Rep. 19, 1431–1443 (2017).
pubmed: 28514662 doi: 10.1016/j.celrep.2017.04.068
Mayassi, T., Barreiro, L. B., Rossjohn, J. & Jabri, B. A multilayered immune system through the lens of unconventional T cells. Nature 595, 501–510 (2021).
pubmed: 34290426 pmcid: 8514118 doi: 10.1038/s41586-021-03578-0
Hayday, A., Theodoridis, E., Ramsburg, E. & Shires, J. Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat. Immunol. 2, 997–1003 (2001).
pubmed: 11685222 doi: 10.1038/ni1101-997
Abadie, V., Discepolo, V. & Jabri, B. Intraepithelial lymphocytes in celiac disease immunopathology. Semin. Immunopathol. 34, 551–566 (2012).
pubmed: 22660791 doi: 10.1007/s00281-012-0316-x
Catalan-Serra, I., Sandvik, A. K., Bruland, T. & Andreu-Ballester, J. C. Gammadelta T cells in Crohn’s disease: a new player in the disease pathogenesis? J. Crohns Colitis 11, 1135–1145 (2017).
pubmed: 28333360 doi: 10.1093/ecco-jcc/jjx039
Atlasy, N. et al. Single cell transcriptomic analysis of the immune cell compartment in the human small intestine and in Celiac disease. Nat. Commun. 13, 4920 (2022).
pubmed: 35995787 pmcid: 9395525 doi: 10.1038/s41467-022-32691-5
Heizmann, B., Kastner, P. & Chan, S. The Ikaros family in lymphocyte development. Curr. Opin. Immunol. 51, 14–23 (2018).
pubmed: 29278858 doi: 10.1016/j.coi.2017.11.005
Koipally, J., Renold, A., Kim, J. & Georgopoulos, K. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 18, 3090–3100 (1999).
pubmed: 10357820 pmcid: 1171390 doi: 10.1093/emboj/18.11.3090
Zhang, J. et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 13, 86–94 (2011).
pubmed: 22080921 pmcid: 3868219 doi: 10.1038/ni.2150
Molnar, A. & Georgopoulos, K. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol. Cell Biol. 14, 8292–8303 (1994).
pubmed: 7969165 pmcid: 359368
Georgopoulos, K. et al. The Ikaros gene is required for the development of all lymphoid lineages. Cell 79, 143–156 (1994).
pubmed: 7923373 doi: 10.1016/0092-8674(94)90407-3
Quintana, F. J. et al. Aiolos promotes T
pubmed: 22751139 pmcid: 3541018 doi: 10.1038/ni.2363
Morgan, B. et al. Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J. 16, 2004–2013 (1997).
pubmed: 9155026 pmcid: 1169803 doi: 10.1093/emboj/16.8.2004
Wang, J. H. et al. Aiolos regulates B cell activation and maturation to effector state. Immunity 9, 543–553 (1998).
pubmed: 9806640 doi: 10.1016/S1074-7613(00)80637-8
Qiu, J. et al. Tissue signals imprint Aiolos expression in ILC2s to modulate type 2 immunity. Mucosal Immunol. 14, 1306–1322 (2021).
pubmed: 34349237 pmcid: 8528704 doi: 10.1038/s41385-021-00431-5
Felton, J. M. et al. Aiolos regulates eosinophil migration into tissues. Mucosal Immunol. 14, 1271–1281 (2021).
pubmed: 34341502 pmcid: 8542574 doi: 10.1038/s41385-021-00416-4
Holmes, M. L. et al. Peripheral natural killer cell maturation depends on the transcription factor Aiolos. EMBO J. 33, 2721–2734 (2014).
pubmed: 25319415 pmcid: 4282578 doi: 10.15252/embj.201487900
Cella, M. et al. Subsets of ILC3-ILC1-like cells generate a diversity spectrum of innate lymphoid cells in human mucosal tissues. Nat. Immunol. 20, 980–991 (2019).
pubmed: 31209406 pmcid: 6685551 doi: 10.1038/s41590-019-0425-y
Mazzurana, L. et al. Suppression of Aiolos and Ikaros expression by lenalidomide reduces human ILC3-ILC1/NK cell transdifferentiation. Eur. J. Immunol. 49, 1344–1355 (2019).
pubmed: 31151137 doi: 10.1002/eji.201848075
Whang, M. I., Guerra, N. & Raulet, D. H. Costimulation of dendritic epidermal gammadelta T cells by a new NKG2D ligand expressed specifically in the skin. J. Immunol. 182, 4557–4564 (2009).
pubmed: 19342629 doi: 10.4049/jimmunol.0802439
Puddington, L., Olson, S. & Lefrancois, L. Interactions between stem cell factor and c-Kit are required for intestinal immune system homeostasis. Immunity 1, 733–739 (1994).
pubmed: 7534619 doi: 10.1016/S1074-7613(94)80015-4
Shui, J. W. et al. HVEM signalling at mucosal barriers provides host defence against pathogenic bacteria. Nature 488, 222–225 (2012).
pubmed: 22801499 pmcid: 3477500 doi: 10.1038/nature11242
Rezende, R. M. et al. gammadelta T cell-secreted XCL1 mediates anti-CD3-induced oral tolerance. J. Immunol. 203, 2621–2629 (2019).
pubmed: 31578268 doi: 10.4049/jimmunol.1900784
Zehn, D. et al. ‘Stem-like’ precursors are the fount to sustain persistent CD8
Wu, J. et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285, 730–732 (1999).
pubmed: 10426994 doi: 10.1126/science.285.5428.730
Lanier, L. L. DAP10- and DAP12-associated receptors in innate immunity. Immunol. Rev. 227, 150–160 (2009).
pubmed: 19120482 pmcid: 2794881 doi: 10.1111/j.1600-065X.2008.00720.x
Nixon, B. G. et al. Cytotoxic granzyme C-expressing ILC1s contribute to antitumor immunity and neonatal autoimmunity. Sci. Immunol. 7, eabi8642 (2022).
pubmed: 35394814 pmcid: 9233921 doi: 10.1126/sciimmunol.abi8642
Yomogida, K. et al. Hobit confers tissue-dependent programs to type 1 innate lymphoid cells. Proc. Natl Acad. Sci. USA 118, e2117965118 (2021).
Friedrich, C. et al. Effector differentiation downstream of lineage commitment in ILC1s is driven by Hobit across tissues. Nat. Immunol. 22, 1256–1267 (2021).
pubmed: 34462601 pmcid: 7611762 doi: 10.1038/s41590-021-01013-0
Gilfillan, S. et al. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat. Immunol. 3, 1150–1155 (2002).
Ma, L. J., Acero, L. F., Zal, T. & Schluns, K. S. Trans-presentation of IL-15 by intestinal epithelial cells drives development of CD8alphaalpha IELs. J. Immunol. 183, 1044–1054 (2009).
pubmed: 19553528 doi: 10.4049/jimmunol.0900420
Zhou, R., Wei, H., Sun, R. & Tian, Z. Recognition of double-stranded RNA by TLR3 induces severe small intestinal injury in mice. J. Immunol. 178, 4548–4556 (2007).
pubmed: 17372013 doi: 10.4049/jimmunol.178.7.4548
Lodolce, J. P. et al. T cell-independent interleukin 15rα signals are required for bystander proliferation. J. Exp. Med. 194, 1187–1194 (2001).
Zhou, R. et al. NKG2D recognition mediates Toll-like receptor 3 signaling-induced breakdown of epithelial homeostasis in the small intestines of mice. Proc. Natl Acad. Sci. USA 104, 7512–7515 (2007).
Longhi, M. P. et al. Dendritic cells require a systemic type I interferon response to mature and induce CD4
pubmed: 19564349 pmcid: 2715098 doi: 10.1084/jem.20090247
Chassaing, B., Aitken, J. D., Malleshappa, M. & Vijay-Kumar, M. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 104, 152511–152514 (2014).
doi: 10.1002/0471142735.im1525s104
Maekawa, Y. et al. Notch2 integrates signaling by the transcription factors RBP-J and CREB1 to promote T cell cytotoxicity. Nat. Immunol. 9, 1140–1147 (2008).
pubmed: 18724371 doi: 10.1038/ni.1649
Hahm, K. et al. Helios, a T cell-restricted Ikaros family member that quantitatively associates with Ikaros at centromeric heterochromatin. Genes Dev. 12, 782–796 (1998).
pubmed: 9512513 pmcid: 316626 doi: 10.1101/gad.12.6.782
Schjerven, H. et al. Selective regulation of lymphopoiesis and leukemogenesis by individual zinc fingers of Ikaros. Nat. Immunol. 14, 1073–1083 (2013).
pubmed: 24013668 pmcid: 3800053 doi: 10.1038/ni.2707
Hollenhorst, P. C., Shah, A. A., Hopkins, C. & Graves, B. J. Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 21, 1882–1894 (2007).
pubmed: 17652178 pmcid: 1935027 doi: 10.1101/gad.1561707
Ma, S. et al. Ikaros and Aiolos inhibit pre-B-cell proliferation by directly suppressing c-Myc expression. Mol. Cell Biol. 30, 4149–4158 (2010).
pubmed: 20566697 pmcid: 2937562 doi: 10.1128/MCB.00224-10
Bjorklund, C. C. et al. Rate of CRL4(CRBN) substrate Ikaros and Aiolos degradation underlies differential activity of lenalidomide and pomalidomide in multiple myeloma cells by regulation of c-Myc and IRF4. Blood Cancer J. 5, e354 (2015).
pubmed: 26430725 pmcid: 4635186 doi: 10.1038/bcj.2015.66
Peloquin, J. M. et al. Characterization of candidate genes in inflammatory bowel disease-associated risk loci. JCI Insight 1, e87899 (2016).
pubmed: 27668286 pmcid: 5033062 doi: 10.1172/jci.insight.87899
Katerndahl, C. D. S. et al. Antagonism of B cell enhancer networks by STAT5 drives leukemia and poor patient survival. Nat. Immunol. 18, 694–704 (2017).
pubmed: 28369050 pmcid: 5540372 doi: 10.1038/ni.3716
Heizmann, B. et al. Ikaros antagonizes DNA binding by STAT5 in pre-B cells. PLoS ONE 15, e0242211 (2020).
pubmed: 33180866 pmcid: 7660478 doi: 10.1371/journal.pone.0242211
Read, K. A. et al. Aiolos represses CD4
pubmed: 36964178 pmcid: 10039023 doi: 10.1038/s41467-023-37420-0
Abadie, V. et al. IL-15, gluten and HLA-DQ8 drive tissue destruction in coeliac disease. Nature 578, 600–604 (2020).
pubmed: 32051586 pmcid: 7047598 doi: 10.1038/s41586-020-2003-8
Lefrancois, L. & Lycke, N. Isolation of mouse small intestinal intraepithelial lymphocytes, Peyer’s patch, and lamina propria cells. Curr. Protoc. Immunol. 3, 19 (2001).
Buenrostro, J. D. et al. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).

Auteurs

Kentaro Yomogida (K)

Department of Pediatrics, University of Colorado Anschutz Medical Campus, Denver, CO, USA.
Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Tihana Trsan (T)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Raki Sudan (R)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Patrick F Rodrigues (PF)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Alina Ulezko Antonova (A)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Harshad Ingle (H)

Department of Medicine, Division of Infectious Diseases, Washington University School of Medicine, St. Louis, MO, USA.

Blanda Di Luccia (BD)

Department of Microbiology and Immunology, Stanford University, Stanford, CA, USA.

Patrick L Collins (PL)

Department of Microbial Infection and Immunity, Pelotonia Institute for Immuno-Oncology, The Ohio State University, Columbus, OH, USA.

Marina Cella (M)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Susan Gilfillan (S)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.

Megan T Baldridge (MT)

Department of Medicine, Division of Infectious Diseases, Washington University School of Medicine, St. Louis, MO, USA.

Eugene M Oltz (EM)

Department of Microbial Infection and Immunity, Pelotonia Institute for Immuno-Oncology, The Ohio State University, Columbus, OH, USA.

Marco Colonna (M)

Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA. mcolonna@wustl.edu.

Classifications MeSH