Commensal-specific T cell plasticity promotes rapid tissue adaptation to injury

Science

Volumn 363, Issue 6422, 2019, Pages

  Harrison, Oliver J ^a   Linehan, Jonathan L ^a,f   Shih, Han Yu ^b   Bouladoux, Nicolas ^a   Han, Seong Ji ^a   Smelkinson, Margery ^a   Sen, Shurjo K ^c   Byrd, Allyson L ^a   Enamorado, Michel ^a   Yao, Chen ^b   Tamoutounour, Samira ^a   Van Laethem, Francois ^d,g   Hurabielle, Charlotte ^a,e   Collins, Nicholas ^a   Paun, Andrea ^a   Salcedo, Rosalba ^d   O’Shea, John J ^b   Belkaid, Yasmine ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e SAINT LOUIS HOSPITAL   (France)

^f GENENTECH INC   (United States)

^g INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALARMIN; INTERLEUKIN 13; INTERLEUKIN 18; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTOME;

ADAPTATION; ANTIGEN; CELL; ENVIRONMENTAL STRESS; IMMUNITY; INJURY; PLASTICITY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL FUNCTION; CELL PLASTICITY; CELLULAR IMMUNITY; COMMENSAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EX VIVO STUDY; FLOW CYTOMETRY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PARABIOSIS; PRIORITY JOURNAL; RNA SEQUENCE; STAPHYLOCOCCUS EPIDERMIDIS; T LYMPHOCYTE; TISSUE INJURY; TISSUE REPAIR; WOUND HEALING;

EID: 85058113593     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aat6280     Document Type: Article

References (57)

1. Y. Cong, T. Feng, K. Fujihashi, T. R. Schoeb, C. O. Elson, A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl. Acad. Sci. U.S.A. 106, 19256–19261 (2009). doi: 10.1073/pnas.0812681106; pmid: 19889972
2. T. W. Hand et al., Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 337, 1553–1556 (2012). doi: 10.1126/science.1220961; pmid: 22923434
3. Y. Yang et al., Focused specificity of intestinal TH17 cells towards commensal bacterial antigens. Nature 510, 152–156 (2014). doi: 10.1038/nature13279; pmid: 24739972
4. S. Naik et al., Commensal-dendritic-cell interaction specifies a unique protective skin immune signature. Nature 520, 104–108 (2015). doi: 10.1038/nature14052; pmid: 25539086
5. Y. Belkaid, O. J. Harrison, Homeostatic Immunity and the Microbiota. Immunity 46, 562–576 (2017). doi: 10.1016/ j.immuni.2017.04.008; pmid: 28423337
6. J. L. Linehan et al., Non-classical Immunity Controls Microbiota Impact on Skin Immunity and Tissue Repair. Cell 172, 784–796. e18 (2018). doi: 10.1016/j.cell.2017.12.033; pmid: 29358051
7. T. C. Scharschmidt et al., A Wave of Regulatory T Cells into Neonatal Skin Mediates Tolerance to Commensal Microbes. Immunity 43, 1011–1021 (2015). doi: 10.1016/ j.immuni.2015.10.016; pmid: 26588783
8. V. K. Ridaura et al., Contextual control of skin immunity and inflammation by Corynebacterium. J. Exp. Med. 215, 785–799 (2018). doi: 10.1084/jem.20171079; pmid: 29382696
9. J. M. Schenkel, D. Masopust, Tissue-resident memory T cells. Immunity 41, 886–897 (2014). doi: 10.1016/ j.immuni.2014.12.007; pmid: 25526304
10. D. E. Wright, A. J. Wagers, A. P. Gulati, F. L. Johnson, I. L. Weissman, Physiological migration of hematopoietic stem and progenitor cells. Science 294, 1933–1936 (2001). doi: 10.1126/science.1064081; pmid: 11729320
11. J. M. Kim, J. P. Rasmussen, A. Y. Rudensky, Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8, 191–197 (2007). doi: 10.1038/ni1428; pmid: 17136045
12. + regulatory T cell fate during inflammation in mice. J. Clin. Invest. 121, 4503–4515 (2011). doi: 10.1172/JCI57456; pmid: 21965331
13. M. Delacher et al., Genome-wide DNA-methylation landscape defines specialization of regulatory T cells in tissues. Nat. Immunol. 18, 1160–1172 (2017). doi: 10.1038/ni.3799; pmid: 28783152
14. Y. Wang, M. A. Su, Y. Y. Wan, An essential role of the transcription factor GATA-3 for the function of regulatory T cells. Immunity 35, 337–348 (2011). doi: 10.1016/ j.immuni.2011.08.012; pmid: 21924928
15. D. Rudra et al., Transcription factor Foxp3 and its protein partners form a complex regulatory network. Nat. Immunol. 13, 1010–1019 (2012). doi: 10.1038/ni.2402; pmid: 22922362
16. H. Y. Shih et al., Developmental Acquisition of Regulomes Underlies Innate Lymphoid Cell Functionality. Cell 165, 1120–1133 (2016). doi: 10.1016/j.cell.2016.04.029; pmid: 27156451
17. G. R. Lee, P. E. Fields, T. J. Griffin IV, R. A. Flavell, Regulation of the Th2 cytokine locus by a locus control region. Immunity 19, 145–153 (2003). doi: 10.1016/S1074-7613(03)00179-1; pmid: 12871646
18. H. E. Liang et al., Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat. Immunol. 13, 58–66 (2011). doi: 10.1038/ni.2182; pmid: 22138715
19. K. Mohrs, A. E. Wakil, N. Killeen, R. M. Locksley, M. Mohrs, A two-step process for cytokine production revealed by IL-4 dual-reporter mice. Immunity 23, 419–429 (2005). doi: 10.1016/j.immuni.2005.09.006; pmid: 16226507
20. C. H. Chang et al., Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153, 1239–1251 (2013). doi: 10.1016/j.cell.2013.05.016; pmid: 23746840
21. + effector T cells. Nat. Immunol. 18, 1046–1057 (2017). pmid: 28714979
22. F. Salerno et al., Translational repression of pre-formed cytokine-encoding mRNA prevents chronic activation of memory T cells. Nat. Immunol. 19, 828–837 (2018). doi: 10.1038/s41590-018-0155-6; pmid: 29988089
23. + T cell responses. Science 335, 984–989 (2012). doi: 10.1126/science.1215418; pmid: 22323740
24. I. Okamoto, K. Kohno, T. Tanimoto, H. Ikegami, M. Kurimoto, Development of CD8+ effector T cells is differentially regulated by IL-18 and IL-12. J. Immunol. 162, 3202–3211 (1999). pmid: 10092771
25. P. P. Ahern et al., Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33, 279–288 (2010). doi: 10.1016/j.immuni.2010.08.010; pmid: 20732640
26. K. Hirota et al., Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12, 255–263 (2011). doi: 10.1038/ni.1993; pmid: 21278737
27. H 2 memory/effector cells that produce inflammatory IL-17 cytokine and promote the exacerbation of chronic allergic asthma. J. Exp. Med. 207, 2479–2491 (2010). doi: 10.1084/jem.20101376; pmid: 20921287
28. M. Panzer et al., Rapid in vivo conversion of effector T cells into Th2 cells during helminth infection. J. Immunol. 188, 615–623 (2012). doi: 10.4049/jimmunol.1101164; pmid: 22156341
29. C. Irvin et al., Increased frequency of dual-positive TH2/TH17 cells in bronchoalveolar lavage fluid characterizes a population of patients with severe asthma. J. Allergy Clin. Immunol. 134, 1175–1186.e7 (2014). doi: 10.1016/j.jaci.2014.05.038; pmid: 25042748
30. K. Hirota et al., Plasticity of Th17 cells in Peyer’s patches is responsible for the induction of T cell-dependent IgA responses. Nat. Immunol. 14, 372–379 (2013). doi: 10.1038/ ni.2552; pmid: 23475182
31. N. Gagliani et al., Th17 cells transdifferentiate into regulatory T cells during resolution of inflammation. Nature 523, 221–225 (2015). doi: 10.1038/nature14452; pmid: 25924064
32. K. Nakanishi, T. Yoshimoto, H. Tsutsui, H. Okamura, Interleukin-18 regulates both Th1 and Th2 responses. Annu. Rev. Immunol. 19, 423–474 (2001). doi: 10.1146/ annurev.immunol.19.1.423; pmid: 11244043
33. + Treg cell function in the intestine. Mucosal Immunol. 8, 1226–1236 (2015). doi: 10.1038/ mi.2015.13; pmid: 25736457
34. N. Arpaia et al., A Distinct Function of Regulatory T Cells in Tissue Protection. Cell 162, 1078–1089 (2015). doi: 10.1016/ j.cell.2015.08.021; pmid: 26317471
35. R. R. Ricardo-Gonzalez et al., Tissue signals imprint ILC2 identity with anticipatory function. Nat. Immunol. 19, 1093–1099 (2018). doi: 10.1038/s41590-018-0201-4; pmid: 30201992
36. S. A. Eming, T. A. Wynn, P. Martin, Inflammation and metabolism in tissue repair and regeneration. Science 356, 1026–1030 (2017). doi: 10.1126/science.aam7928; pmid: 28596335
37. J. Zhu et al., Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat. Immunol. 5, 1157–1165 (2004). doi: 10.1038/ni1128; pmid: 15475959
38. Y. P. Rubtsov et al., Stability of the regulatory T cell lineage in vivo. Science 329, 1667–1671 (2010). doi: 10.1126/ science.1191996; pmid: 20929851
39. E. Bettelli et al., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235–238 (2006). doi: 10.1038/nature04753; pmid: 16648838
40. P. Mombaerts et al., Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature 360, 225–231 (1992). doi: 10.1038/360225a0; pmid: 1359428
41. G. J. McKenzie et al., Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9, 423–432 (1998). doi: 10.1016/ S1074-7613(00)80625-1; pmid: 9768762
42. R. Yagi et al., The transcription factor GATA3 is critical for the development of all IL-7Ra-expressing innate lymphoid cells. Immunity 40, 378–388 (2014). doi: 10.1016/ j.immuni.2014.01.012; pmid: 24631153
43. S. Srinivas et al., Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4 (2001). doi: 10.1186/1471-213X-1-4; pmid: 11299042
44. S. Conlan et al., Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. Genome Biol. 13, R64 (2012). doi: 10.1186/gb-2012-13-7-r64; pmid: 22830599
45. S. Naik et al., Compartmentalized control of skin immunity by resident commensals. Science 337, 1115–1119 (2012). doi: 10.1126/science.1225152; pmid: 22837383
46. P. Dash et al., Paired analysis of TCRa and TCRb chains at the single-cell level in mice. J. Clin. Invest. 121, 288–295 (2011). doi: 10.1172/JCI44752; pmid: 21135507
47. G. Sun et al., The zinc finger protein cKrox directs CD4 lineage differentiation during intrathymic T cell positive selection. Nat. Immunol. 6, 373–381 (2005). doi: 10.1038/ni1183; pmid: 15750595
48. N. Kimblin et al., Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc. Natl. Acad. Sci. U.S.A. 105, 10125–10130 (2008). doi: 10.1073/pnas.0802331105; pmid: 18626016
49. + T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27, 203–213 (2007). doi: 10.1016/j.immuni.2007.07.007; pmid: 17707129
50. B. Li, C. N. Dewey, RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011). doi: 10.1186/1471-2105-12-323; pmid: 21816040
51. M. I. Love, W. Huber, S. Anders, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014). doi: 10.1186/s13059-014-0550-8; pmid: 25516281
52. A. Dobin et al., STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013). doi: 10.1093/bioinformatics/ bts635; pmid: 23104886
53. H. Xu et al., FastUniq: A fast de novo duplicates removal tool for paired short reads. PLOS ONE 7, e52249 (2012). doi: 10.1371/journal.pone.0052249; pmid: 23284954
54. S. Heinz et al., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010). doi: 10.1016/j.molcel.2010.05.004; pmid: 20513432
55. A. Butler, P. Hoffman, P. Smibert, E. Papalexi, R. Satija, Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018). doi: 10.1038/nbt.4096; pmid: 29608179
56. B. E. Keyes et al., Impaired Epidermal to Dendritic T Cell Signaling Slows Wound Repair in Aged Skin. Cell 167, 1323–1338.e14 (2016). doi: 10.1016/j.cell.2016.10.052; pmid: 27863246
57. M. Lochner, H. Wagner, M. Classen, I. Förster, Generation of neutralizing mouse anti-mouse IL-18 antibodies for inhibition of inflammatory responses in vivo. J. Immunol. Methods 259, 149–157 (2002). doi: 10.1016/S0022-1759(01)00505-1; pmid: 11730850