User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Complementarity and redundancy of IL-22-producing innate lymphoid cells.

Primary tabs

download
  • Open access
  • PDF
  • 1.84 M
Rankin, Lucille C Girard-Madoux, Mathilde J H Seillet, Cyril Mielke, Lisa A Kerdiles, Yann Renauld, Jean-Christophe [UCL] Vivier, Eric

Intestinal T cells and group 3 innate lymphoid cells (ILC3 cells) control the composition of the microbiota and gut immune responses. Within the gut, ILC3 subsets coexist that either express or lack the natural cytoxicity receptor (NCR) NKp46. We identified here the transcriptional signature associated with the transcription factor T-bet-dependent differentiation of NCR(-) ILC3 cells into NCR(+) ILC3 cells. Contrary to the prevailing view, we found by conditional deletion of the key ILC3 genes Stat3, Il22, Tbx21 and Mcl1 that NCR(+) ILC3 cells were redundant for the control of mouse colonic infection with Citrobacter rodentium in the presence of T cells. However, NCR(+) ILC3 cells were essential for cecal homeostasis. Our data show that interplay between intestinal ILC3 cells and adaptive lymphocytes results in robust complementary failsafe mechanisms that ensure gut homeostasis.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2016
Language Anglais
Journal information "Nature Immunology" - Vol. 17, no.2, p. 179-186 (2015)
Peer reviewed yes
Publisher Nature Publishing Group (New York)
issn 1529-2908
e-issn 1529-2916
Publication status Publié
Affiliation UCL - SSS/DDUV - Institut de Duve
MESH Subject Animals ; Immunity, Innate ; Interleukins ; Lymphocyte Subsets ; Lymphocytes ; Male ; Mice ; Mice, Knockout ; Mice, Transgenic ; Myeloid Cell Leukemia Sequence 1 Protein ; Natural Cytotoxicity Triggering Receptor 1 ; Citrobacter rodentium ; Signal Transduction ; T-Box Domain Proteins ; Transcriptome ; Cluster Analysis ; Disease Models, Animal ; Enterobacteriaceae Infections ; Female ; Gene Expression Profiling ; Gene Expression Regulation ; Homeostasis
Links
  1. Dudakov Jarrod A., Hanash Alan M., van den Brink Marcel R.M., Interleukin-22: Immunobiology and Pathology, 10.1146/annurev-immunol-032414-112123
  2. Spits Hergen, Artis David, Colonna Marco, Diefenbach Andreas, Di Santo James P., Eberl Gerard, Koyasu Shigeo, Locksley Richard M., McKenzie Andrew N. J., Mebius Reina E., Powrie Fiona, Vivier Eric, Innate lymphoid cells — a proposal for uniform nomenclature, 10.1038/nri3365
  3. McKenzie Andrew N.J., Spits Hergen, Eberl Gerard, Innate Lymphoid Cells in Inflammation and Immunity, 10.1016/j.immuni.2014.09.006
  4. Diefenbach Andreas, Colonna Marco, Koyasu Shigeo, Development, Differentiation, and Diversity of Innate Lymphoid Cells, 10.1016/j.immuni.2014.09.005
  5. Montaldo Elisa, Juelke Kerstin, Romagnani Chiara, Group 3 innate lymphoid cells (ILC3s): Origin, differentiation, and plasticity in humans and mice : Highlights - (Mini-Review), 10.1002/eji.201545598
  6. Eberl Gérard, Di Santo James P, Vivier Eric, The brave new world of innate lymphoid cells, 10.1038/ni.3059
  7. Eberl G., Colonna M., Di Santo J. P., McKenzie A. N. J., Innate lymphoid cells: A new paradigm in immunology, 10.1126/science.aaa6566
  8. Mebius Reina E, Rennert Paul, Weissman Irving L, Developing Lymph Nodes Collect CD4 + CD3 − LTβ + Cells That Can Differentiate to APC, NK Cells, and Follicular Cells but Not T or B Cells, 10.1016/s1074-7613(00)80371-4
  9. Constantinides Michael G., Gudjonson Herman, McDonald Benjamin D., Ishizuka Isabel E., Verhoef Philip A., Dinner Aaron R., Bendelac Albert, PLZF expression maps the early stages of ILC1 lineage development, 10.1073/pnas.1423244112
  10. Klose Christoph S. N., Kiss Elina A., Schwierzeck Vera, Ebert Karolina, Hoyler Thomas, d’Hargues Yannick, Göppert Nathalie, Croxford Andrew L., Waisman Ari, Tanriver Yakup, Diefenbach Andreas, A T-bet gradient controls the fate and function of CCR6−RORγt+ innate lymphoid cells, 10.1038/nature11813
  11. Rankin Lucille C, Groom Joanna R, Chopin Michaël, Herold Marco J, Walker Jennifer A, Mielke Lisa A, McKenzie Andrew N J, Carotta Sebastian, Nutt Stephen L, Belz Gabrielle T, The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the Notch pathway, 10.1038/ni.2545
  12. Kirchberger Stefanie, Royston Daniel J., Boulard Olivier, Thornton Emily, Franchini Fanny, Szabady Rose L., Harrison Oliver, Powrie Fiona, Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model, 10.1084/jem.20122308
  13. Satoh-Takayama Naoko, Vosshenrich Christian A.J., Lesjean-Pottier Sarah, Sawa Shinichiro, Lochner Matthias, Rattis Frederique, Mention Jean-Jacques, Thiam Kader, Cerf-Bensussan Nadine, Mandelboim Ofer, Eberl Gerard, Di Santo James P., Microbial Flora Drives Interleukin 22 Production in Intestinal NKp46+ Cells that Provide Innate Mucosal Immune Defense, 10.1016/j.immuni.2008.11.001
  14. Cella Marina, Fuchs Anja, Vermi William, Facchetti Fabio, Otero Karel, Lennerz Jochen K. M., Doherty Jason M., Mills Jason C., Colonna Marco, A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity, 10.1038/nature07537
  15. Sonnenberg Gregory F., Fouser Lynette A., Artis David, Functional Biology of the IL-22-IL-22R Pathway in Regulating Immunity and Inflammation at Barrier Surfaces, Advances in Immunology (2010) ISBN:9780123813008 p.1-29, 10.1016/b978-0-12-381300-8.00001-0
  16. Zheng Yan, Valdez Patricia A, Danilenko Dimitry M, Hu Yan, Sa Susan M, Gong Qian, Abbas Alexander R, Modrusan Zora, Ghilardi Nico, de Sauvage Frederic J, Ouyang Wenjun, Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens, 10.1038/nm1720
  17. Satoh-Takayama Naoko, Serafini Nicolas, Verrier Thomas, Rekiki Abdessalem, Renauld Jean-Christophe, Frankel Gad, Di Santo James P., The Chemokine Receptor CXCR6 Controls the Functional Topography of Interleukin-22 Producing Intestinal Innate Lymphoid Cells, 10.1016/j.immuni.2014.10.007
  18. Artis David, Spits Hergen, The biology of innate lymphoid cells, 10.1038/nature14189
  19. Robinette Michelle L, Fuchs Anja, Cortez Victor S, Lee Jacob S, Wang Yaming, Durum Scott K, Gilfillan Susan, Colonna Marco, Shaw Laura, Yu Bingfei, Goldrath Ananda, Mostafavi Sara, Regev Aviv, Kim Edy Y, Dwyer Dan F, Brenner Michael B, Austen K Frank, Rhoads Andrew, Moodley Devapregasan, Yoshida Hideyuki, Mathis Diane, Benoist Christophe, Nabekura Tsukasa, Lam Viola, Lanier Lewis L, Brown Brian, Merad Miriam, Cremasco Viviana, Turley Shannon, Monach Paul, Dustin Michael L, Li Yuesheng, Shinton Susan A, Hardy Richard R, Shay Tal, Qi Yilin, Sylvia Katelyn, Kang Joonsoo, Fairfax Keke, Randolph Gwendalyn J, Robinette Michelle L, Fuchs Anja, Colonna Marco, Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets, 10.1038/ni.3094
  20. Sciumé Giuseppe, Hirahara Kiyoshi, Takahashi Hayato, Laurence Arian, Villarino Alejandro V., Singleton Kentner L., Spencer Sean P., Wilhelm Christoph, Poholek Amanda C., Vahedi Golnaz, Kanno Yuka, Belkaid Yasmine, O'Shea John J., Distinct requirements for T-bet in gut innate lymphoid cells, 10.1084/jem.20122097
  21. Guo Xiaohuan, Qiu Ju, Tu Tony, Yang Xuanming, Deng Liufu, Anders Robert A., Zhou Liang, Fu Yang-Xin, Induction of Innate Lymphoid Cell-Derived Interleukin-22 by the Transcription Factor STAT3 Mediates Protection against Intestinal Infection, 10.1016/j.immuni.2013.10.021
  22. Sathe Priyanka, Delconte Rebecca B., Souza-Fonseca-Guimaraes Fernando, Seillet Cyril, Chopin Michael, Vandenberg Cassandra J., Rankin Lucille C., Mielke Lisa A., Vikstrom Ingela, Kolesnik Tatiana B., Nicholson Sandra E., Vivier Eric, Smyth Mark J., Nutt Stephen L., Glaser Stefan P., Strasser Andreas, Belz Gabrielle T., Carotta Sebastian, Huntington Nicholas D., Innate immunodeficiency following genetic ablation of Mcl1 in natural killer cells, 10.1038/ncomms5539
  23. Qiu Ju, Guo Xiaohuan, Chen Zong-ming E., He Lei, Sonnenberg Gregory F., Artis David, Fu Yang-Xin, Zhou Liang, Group 3 Innate Lymphoid Cells Inhibit T-Cell-Mediated Intestinal Inflammation through Aryl Hydrocarbon Receptor Signaling and Regulation of Microflora, 10.1016/j.immuni.2013.08.002
  24. Guo Xiaohuan, Liang Yong, Zhang Yuan, Lasorella Anna, Kee Barbara L., Fu Yang-Xin, Innate Lymphoid Cells Control Early Colonization Resistance against Intestinal Pathogens through ID2-Dependent Regulation of the Microbiota, 10.1016/j.immuni.2015.03.012
  25. Basu Rajatava, O’Quinn Darrell B., Silberger Daniel J., Schoeb Trenton R., Fouser Lynette, Ouyang Wenjun, Hatton Robin D., Weaver Casey T., Th22 Cells Are an Important Source of IL-22 for Host Protection against Enteropathogenic Bacteria, 10.1016/j.immuni.2012.08.024
  26. Ahlfors Helena, Morrison Peter J., Duarte João H., Li Ying, Biro Judit, Tolaini Mauro, Di Meglio Paola, Potocnik Alexandre J., Stockinger Brigitta, IL-22 Fate Reporter Reveals Origin and Control of IL-22 Production in Homeostasis and Infection, 10.4049/jimmunol.1401244
  27. Vonarbourg Cedric, Mortha Arthur, Bui Viet L., Hernandez Pedro P., Kiss Elina A., Hoyler Thomas, Flach Melanie, Bengsch Bertram, Thimme Robert, Hölscher Christoph, Hönig Manfred, Pannicke Ulrich, Schwarz Klaus, Ware Carl F., Finke Daniela, Diefenbach Andreas, Regulated Expression of Nuclear Receptor RORγt Confers Distinct Functional Fates to NK Cell Receptor-Expressing RORγt+ Innate Lymphocytes, 10.1016/j.immuni.2010.10.017
  28. Dhiman R., Indramohan M., Barnes P. F., Nayak R. C., Paidipally P., Rao L. V. M., Vankayalapati R., IL-22 Produced by Human NK Cells Inhibits Growth of Mycobacterium tuberculosis by Enhancing Phagolysosomal Fusion, 10.4049/jimmunol.0902587
  29. Guo H., Topham D. J., Interleukin-22 (IL-22) Production by Pulmonary Natural Killer Cells and the Potential Role of IL-22 during Primary Influenza Virus Infection, 10.1128/jvi.00187-10
  30. Male V., Hughes T., McClory S., Colucci F., Caligiuri M. A., Moffett A., Immature NK Cells, Capable of Producing IL-22, Are Present in Human Uterine Mucosa, 10.4049/jimmunol.1001637
  31. Tang Q., Ahn Y.-O., Southern P., Blazar B. R., Miller J. S., Verneris M. R., Development of IL-22-producing NK lineage cells from umbilical cord blood hematopoietic stem cells in the absence of secondary lymphoid tissue, 10.1182/blood-2010-09-303081
  32. Xu X., Weiss I. D., H. Zhang H., Singh S. P., Wynn T. A., Wilson M. S., Farber J. M., Conventional NK Cells Can Produce IL-22 and Promote Host Defense in Klebsiella pneumoniae Pneumonia, 10.4049/jimmunol.1300039
  33. Macho-Fernandez E, Koroleva E P, Spencer C M, Tighe M, Torrado E, Cooper A M, Fu Y-X, Tumanov A V, Lymphotoxin beta receptor signaling limits mucosal damage through driving IL-23 production by epithelial cells, 10.1038/mi.2014.78
  34. Sonnenberg G. F., Monticelli L. A., Alenghat T., Fung T. C., Hutnick N. A., Kunisawa J., Shibata N., Grunberg S., Sinha R., Zahm A. M., Tardif M. R., Sathaliyawala T., Kubota M., Farber D. L., Collman R. G., Shaked A., Fouser L. A., Weiner D. B., Tessier P. A., Friedman J. R., Kiyono H., Bushman F. D., Chang K.-M., Artis D., Innate Lymphoid Cells Promote Anatomical Containment of Lymphoid-Resident Commensal Bacteria, 10.1126/science.1222551
  35. Sonnenberg Gregory F., Monticelli Laurel A., Elloso M. Merle, Fouser Lynette A., Artis David, CD4+ Lymphoid Tissue-Inducer Cells Promote Innate Immunity in the Gut, 10.1016/j.immuni.2010.12.009
  36. Hepworth Matthew R., Monticelli Laurel A., Fung Thomas C., Ziegler Carly G. K., Grunberg Stephanie, Sinha Rohini, Mantegazza Adriana R., Ma Hak-Ling, Crawford Alison, Angelosanto Jill M., Wherry E. John, Koni Pandelakis A., Bushman Frederic D., Elson Charles O., Eberl Gérard, Artis David, Sonnenberg Gregory F., Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria, 10.1038/nature12240
  37. Gasteiger Georg, Rudensky Alexander Y., Interactions between innate and adaptive lymphocytes, 10.1038/nri3726
  38. Wiles Siouxsie, Clare Simon, Harker James, Huett Alan, Young Douglas, Dougan Gordon, Frankel Gad, Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium, 10.1111/j.1462-5822.2004.00414.x
  39. SMITH H. F., FISHER R. E., EVERETT M. L., THOMAS A. D., RANDAL BOLLINGER R., PARKER W., Comparative anatomy and phylogenetic distribution of the mammalian cecal appendix, 10.1111/j.1420-9101.2009.01809.x
  40. Frisch M., Pedersen B. V, Andersson R. E, Appendicitis, mesenteric lymphadenitis, and subsequent risk of ulcerative colitis: cohort studies in Sweden and Denmark, 10.1136/bmj.b716
  41. Alonzi T., Maritano D., Gorgoni B., Rizzuto G., Libert C., Poli V., Essential Role of STAT3 in the Control of the Acute-Phase Response as Revealed by Inducible Gene Activation in the Liver, 10.1128/mcb.21.5.1621-1632.2001
  42. Eberl Matthias, Jomaa Hassan, Hayday Adrian C., Integrated immune responses to infection - cross-talk between human gammadelta T cells and dendritic cells, 10.1111/j.1365-2567.2004.01921.x
  43. Nieuwenhuis E. E. S., Neurath M. F., Corazza N., Iijima H., Trgovcich J., Wirtz S., Glickman J., Bailey D., Yoshida M., Galle P. R., Kronenberg M., Birkenbach M., Blumberg R. S., Disruption of T helper 2-immune responses in Epstein-Barr virus-induced gene 3-deficient mice, 10.1073/pnas.252648899
  44. Narni-Mancinelli E., Chaix J., Fenis A., Kerdiles Y. M., Yessaad N., Reynders A., Gregoire C., Luche H., Ugolini S., Tomasello E., Walzer T., Vivier E., Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor, 10.1073/pnas.1112064108
  45. Thakur Chitra, Lu Yongju, Sun Jiaying, Yu Miaomiao, Chen Bailing, Chen Fei, Increased expression of mdig predicts poorer survival of the breast cancer patients, 10.1016/j.gene.2013.11.031
  46. Liao Y., Smyth G. K., Shi W., featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, 10.1093/bioinformatics/btt656
  47. Ritchie Matthew E., Phipson Belinda, Wu Di, Hu Yifang, Law Charity W., Shi Wei, Smyth Gordon K., limma powers differential expression analyses for RNA-sequencing and microarray studies, 10.1093/nar/gkv007
  48. Smyth G.K., Stat. Appl. Genet. Mol. Biol., 3, 3 (2004)
  49. McCarthy D. J., Smyth G. K., Testing significance relative to a fold-change threshold is a TREAT, 10.1093/bioinformatics/btp053
  50. Yu Z., Biotechniques, 36, 808 (2004)
Bibliographic reference Rankin, Lucille C ; Girard-Madoux, Mathilde J H ; Seillet, Cyril ; Mielke, Lisa A ; Kerdiles, Yann ; et. al. Complementarity and redundancy of IL-22-producing innate lymphoid cells.. In: Nature Immunology, Vol. 17, no.2, p. 179-186 (2015)
Permanent URL http://hdl.handle.net/2078.1/184352