Skin-resident innate lymphoid cells converge on a pathogenic effector state.
Animals
Cell Differentiation
Cell Lineage
Chromatin
/ genetics
Disease Models, Animal
Female
Immunity, Innate
/ immunology
Inflammation
/ genetics
Interleukin-23
/ immunology
Latent Class Analysis
Lymphocytes
/ classification
Male
Mice
Psoriasis
/ genetics
RNA, Small Cytoplasmic
/ genetics
Reproducibility of Results
Skin
/ immunology
Time Factors
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
received:
23
10
2018
accepted:
24
12
2020
pubmed:
5
2
2021
medline:
23
7
2021
entrez:
4
2
2021
Statut:
ppublish
Résumé
Tissue-resident innate lymphoid cells (ILCs) help sustain barrier function and respond to local signals. ILCs are traditionally classified as ILC1, ILC2 or ILC3 on the basis of their expression of specific transcription factors and cytokines
Identifiants
pubmed: 33536623
doi: 10.1038/s41586-021-03188-w
pii: 10.1038/s41586-021-03188-w
pmc: PMC8336632
mid: NIHMS1658011
doi:
Substances chimiques
Chromatin
0
Interleukin-23
0
RNA, Small Cytoplasmic
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
128-132Subventions
Organisme : NCATS NIH HHS
ID : UL1 TR001863
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL107202
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI026918
Pays : United States
Organisme : NCI NIH HHS
ID : K99 CA256526
Pays : United States
Organisme : NIAID NIH HHS
ID : R37 AI026918
Pays : United States
Organisme : NIAMS NIH HHS
ID : K08 AR075880
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Références
Vivier, E. et al. Innate lymphoid cells: 10 years on. Cell 174, 1054–1066 (2018).
pubmed: 30142344
doi: 10.1016/j.cell.2018.07.017
Spencer, S. P. et al. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 343, 432–437 (2014).
pubmed: 24458645
pmcid: 4313730
doi: 10.1126/science.1247606
Roediger, B. et al. Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nat. Immunol. 14, 564–573 (2013).
pubmed: 23603794
pmcid: 4282745
doi: 10.1038/ni.2584
Teunissen, M. B. M. et al. Composition of innate lymphoid cell subsets in the human skin: enrichment of NCR
pubmed: 24658504
doi: 10.1038/jid.2014.146
Villanova, F. et al. Characterization of innate lymphoid cells in human skin and blood demonstrates increase of NKp44
pubmed: 24352038
doi: 10.1038/jid.2013.477
Pantelyushin, S. et al. Rorγt+ innate lymphocytes and γδ T cells initiate psoriasiform plaque formation in mice. J. Clin. Invest. 122, 2252–2256 (2012).
pubmed: 22546855
pmcid: 3366412
doi: 10.1172/JCI61862
Huang, Y. et al. IL-25-responsive, lineage-negative KLRG1
pubmed: 25531830
doi: 10.1038/ni.3078
Bernink, J. H. et al. Interleukin-12 and -23 control plasticity of CD127
pubmed: 26187413
doi: 10.1016/j.immuni.2015.06.019
Cella, M., Otero, K. & Colonna, M. Expansion of human NK-22 cells with IL-7, IL-2, and IL-1β reveals intrinsic functional plasticity. Proc. Natl Acad. Sci. USA 107, 10961–10966 (2010).
pubmed: 20534450
pmcid: 2890739
doi: 10.1073/pnas.1005641107
Ohne, Y. et al. IL-1 is a critical regulator of group 2 innate lymphoid cell function and plasticity. Nat. Immunol. 17, 646–655 (2016).
pubmed: 27111142
doi: 10.1038/ni.3447
Silver, J. S. et al. Inflammatory triggers associated with exacerbations of COPD orchestrate plasticity of group 2 innate lymphoid cells in the lungs. Nat. Immunol. 17, 626–635 (2016).
pubmed: 27111143
pmcid: 5345745
doi: 10.1038/ni.3443
Bal, S. M. et al. IL-1β, IL-4 and IL-12 control the fate of group 2 innate lymphoid cells in human airway inflammation in the lungs. Nat. Immunol. 17, 636–645 (2016).
pubmed: 27111145
doi: 10.1038/ni.3444
Vonarbourg, C. et al. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt
pubmed: 21093318
pmcid: 3042726
doi: 10.1016/j.immuni.2010.10.017
Bernink, J. H. et al. c-Kit-positive ILC2s exhibit an ILC3-like signature that may contribute to IL-17-mediated pathologies. Nat. Immunol. 20, 992–1003 (2019).
pubmed: 31263279
doi: 10.1038/s41590-019-0423-0
Gasteiger, G., Fan, X., Dikiy, S., Lee, S. Y. & Rudensky, A. Y. Tissue residency of innate lymphoid cells in lymphoid and nonlymphoid organs. Science 350, 981–985 (2015).
pubmed: 26472762
pmcid: 4720139
doi: 10.1126/science.aac9593
Kobayashi, T. et al. Homeostatic control of sebaceous glands by innate lymphoid cells regulates commensal bacteria equilibrium. Cell 176, 982–997 (2019).
pubmed: 30712873
pmcid: 6532063
doi: 10.1016/j.cell.2018.12.031
Zeis, P. et al. In situ maturation and tissue adaptation of type 2 innate lymphoid cell progenitors. Immunity 53, 775–792 (2020).
pubmed: 33002412
pmcid: 7611573
doi: 10.1016/j.immuni.2020.09.002
Ghaedi, M. et al. Single-cell analysis of RORα tracer mouse lung reveals ILC progenitors and effector ILC2 subsets. J. Exp. Med. 217, e20182293 (2020).
pubmed: 31816636
doi: 10.1084/jem.20182293
Lim, A. I. et al. Systemic human ILC precursors provide a substrate for tissue ILC differentiation. Cell 168, 1086–1100 (2017).
pubmed: 28283063
doi: 10.1016/j.cell.2017.02.021
Huang, Y. et al. S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense. Science 359, 114–119 (2018).
pubmed: 29302015
pmcid: 6956613
doi: 10.1126/science.aam5809
Li, Z. et al. Epidermal Notch1 recruits RORγ
pubmed: 27099134
pmcid: 4844683
doi: 10.1038/ncomms11394
Chan, J. R. et al. IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J. Exp. Med. 203, 2577–2587 (2006).
pubmed: 17074928
pmcid: 2118145
doi: 10.1084/jem.20060244
Cai, Y. et al. Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity 35, 596–610 (2011).
pubmed: 21982596
pmcid: 3205267
doi: 10.1016/j.immuni.2011.08.001
Califano, D. et al. Transcription factor Bcl11b controls identity and function of mature type 2 innate lymphoid cells. Immunity 43, 354–368 (2015).
pubmed: 26231117
pmcid: 4657441
doi: 10.1016/j.immuni.2015.07.005
Blei, D. M., Ng, A. Y. & Jordan, M. I. Latent Dirichlet allocation. J. Mach. Learn. Res. 3, 29 (2003).
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).
pubmed: 10835412
pmcid: 1461096
doi: 10.1093/genetics/155.2.945
Dey, K. K., Hsiao, C. J. & Stephens, M. Visualizing the structure of RNA-seq expression data using grade of membership models. PLoS Genet. 13, e1006599 (2017).
pubmed: 28333934
pmcid: 5363805
doi: 10.1371/journal.pgen.1006599
Blei, D. M. Probabilistic topic models. Commun. ACM 55, 77–84 (2012).
doi: 10.1145/2133806.2133826
Szabo, P. A. et al. Single-cell transcriptomics of human T cells reveals tissue and activation signatures in health and disease. Nat. Commun. 10, 4706 (2019).
pubmed: 31624246
pmcid: 6797728
doi: 10.1038/s41467-019-12464-3
Cao, Z., Sun, X., Icli, B., Wara, A. K. & Feinberg, M. W. Role of Kruppel-like factors in leukocyte development, function, and disease. Blood 116, 4404–4414 (2010).
pubmed: 20616217
pmcid: 2996110
doi: 10.1182/blood-2010-05-285353
Galloway, A. et al. RNA-binding proteins ZFP36L1 and ZFP36L2 promote cell quiescence. Science 352, 453–459 (2016).
pubmed: 27102483
doi: 10.1126/science.aad5978
Yosef, N. et al. Dynamic regulatory network controlling T
pubmed: 23467089
pmcid: 3637864
doi: 10.1038/nature11981
Wang, S. et al. Regulatory innate lymphoid cells control innate intestinal inflammation. Cell 171, 201–216 (2017).
pubmed: 28844693
doi: 10.1016/j.cell.2017.07.027
Robinette, M. L. et al. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16, 306–317 (2015).
pubmed: 25621825
pmcid: 4372143
doi: 10.1038/ni.3094
Wallrapp, A. et al. The neuropeptide NMU amplifies ILC2-driven allergic lung inflammation. Nature 549, 351–356 (2017).
pubmed: 28902842
pmcid: 5746044
doi: 10.1038/nature24029
Nelson, B. H. IL-2, regulatory T cells, and tolerance. J. Immunol. 172, 3983–3988 (2004).
pubmed: 15034008
doi: 10.4049/jimmunol.172.7.3983
Watts, T. H. TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23, 23–68 (2005).
pubmed: 15771565
doi: 10.1146/annurev.immunol.23.021704.115839
Wallrapp, A. et al. Calcitonin gene-related peptide negatively regulates alarmin-driven type 2 innate lymphoid cell responses. Immunity 51, 709–723 (2019).
pubmed: 31604686
pmcid: 7076585
doi: 10.1016/j.immuni.2019.09.005
Schiebinger, G. et al. Optimal-transport analysis of single-cell gene expression identifies developmental trajectories in reprogramming. Cell 176, 1517 (2019).
pubmed: 30849376
pmcid: 6615720
doi: 10.1016/j.cell.2019.02.026
Farrell, J. A. et al. Single-cell reconstruction of developmental trajectories during zebrafish embryogenesis. Science 360, eaar3131 (2018).
pubmed: 29700225
pmcid: 6247916
doi: 10.1126/science.aar3131
Haghverdi, L., Büttner, M., Wolf, F. A., Buettner, F. & Theis, F. J. Diffusion pseudotime robustly reconstructs lineage branching. Nat. Methods 13, 845–848 (2016).
pubmed: 27571553
doi: 10.1038/nmeth.3971
Constantinides, M. G., McDonald, B. D., Verhoef, P. A. & Bendelac, A. A committed precursor to innate lymphoid cells. Nature 508, 397–401 (2014).
pubmed: 24509713
pmcid: 4003507
doi: 10.1038/nature13047
Klose, C. S. N. et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 157, 340–356 (2014).
pubmed: 24725403
doi: 10.1016/j.cell.2014.03.030
Yu, Y. et al. Single-cell RNA-seq identifies a PD-1
pubmed: 27749818
doi: 10.1038/nature20105
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902 (2019).
pubmed: 31178118
pmcid: 6687398
doi: 10.1016/j.cell.2019.05.031
Ciofani, M. et al. A validated regulatory network for Th17 cell specification. Cell 151, 289–303 (2012).
pubmed: 23021777
pmcid: 3503487
doi: 10.1016/j.cell.2012.09.016
Li, P. et al. BATF-JUN is critical for IRF4-mediated transcription in T cells. Nature 490, 543–546 (2012).
pubmed: 22992523
pmcid: 3537508
doi: 10.1038/nature11530
van der Fits, L. et al. Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J. Immunol. 182, 5836–5845 (2009).
pubmed: 19380832
doi: 10.4049/jimmunol.0802999
Tusi, B. K. et al. Population snapshots predict early haematopoietic and erythroid hierarchies. Nature 555, 54–60 (2018).
pubmed: 29466336
pmcid: 5899604
doi: 10.1038/nature25741
Laurenti, E. & Göttgens, B. From haematopoietic stem cells to complex differentiation landscapes. Nature 553, 418–426 (2018).
pubmed: 29364285
pmcid: 6555401
doi: 10.1038/nature25022
Weinreich, M. A. et al. KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 31, 122–130 (2009).
pubmed: 19592277
pmcid: 2724594
doi: 10.1016/j.immuni.2009.05.011
Esplugues, E. et al. Control of T
pubmed: 21765430
pmcid: 3148838
doi: 10.1038/nature10228
Liang, H. E. et al. Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat. Immunol. 13, 58–66 (2011).
pubmed: 22138715
pmcid: 3242938
doi: 10.1038/ni.2182
Price, A. E., Reinhardt, R. L., Liang, H. E. & Locksley, R. M. Marking and quantifying IL-17A-producing cells in vivo. PLoS ONE 7, e39750 (2012).
pubmed: 22768117
pmcid: 3387253
doi: 10.1371/journal.pone.0039750
Price, A. E. et al. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl Acad. Sci. USA 107, 11489–11494 (2010).
pubmed: 20534524
pmcid: 2895098
doi: 10.1073/pnas.1003988107
Smith, T., Heger, A. & Sudbery, I. UMI-tools: modeling sequencing errors in Unique Molecular Identifiers to improve quantification accuracy. Genome Res. 27, 491–499 (2017).
pubmed: 28100584
pmcid: 5340976
doi: 10.1101/gr.209601.116
Li, B. et al. Cumulus provides cloud-based data analysis for large-scale single-cell and single-nucleus RNA-seq. Nat. Methods 17, 793–798 (2020).
pubmed: 32719530
pmcid: 7437817
doi: 10.1038/s41592-020-0905-x
Hafemeister, C. & Satija, R. Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. Genome Biol. 20, 296 (2019).
pubmed: 31870423
pmcid: 6927181
doi: 10.1186/s13059-019-1874-1
Wolf, F. A., Angerer, P. & Theis, F. J. SCANPY: large-scale single-cell gene expression data analysis. Genome Biol. 19, 15 (2018).
pubmed: 29409532
pmcid: 5802054
doi: 10.1186/s13059-017-1382-0
Jacomy, M., Venturini, T., Heymann, S. & Bastian, M. ForceAtlas2, a continuous graph layout algorithm for handy network visualization designed for the Gephi software. PLoS ONE 9, e98679 (2014).
pubmed: 24914678
pmcid: 4051631
doi: 10.1371/journal.pone.0098679
Erosheva, E. A. Latent Class Representation of the Grade of Membership Model (University of Washington, 2006).
Taddy, M. On estimation and selection for topic models. Proc. Mach. Learn. Res. 22, 1184–1193 (2012).
Blei, D. M., Jordan, M. I., Griffiths, T. L. & Tenenbaum, J. B. Hierarchical topic models and the nested chinese restaurant process. In Proc. 16th International Conference on Neural Information Processing Systems (eds Thrun, S., Saul, L. K. & Schölfopf, B.) 17–24 (MIT Press, 2003).
Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17, 261–272 (2020).
pubmed: 32015543
pmcid: 7056644
doi: 10.1038/s41592-019-0686-2
Finak, G. et al. MAST: a flexible statistical framework for assessing transcriptional changes and characterizing heterogeneity in single-cell RNA sequencing data. Genome Biol. 16, 278 (2015).
pubmed: 26653891
pmcid: 4676162
doi: 10.1186/s13059-015-0844-5
Yates, A. D. et al. Ensembl 2020. Nucleic Acids Res. 48 (D1), D682–D688 (2020).
pubmed: 31691826
Stuart, T., Srivastava, A., Lareau, C. & Satija, R. Multimodal single-cell chromatin analysis with Signac. Preprint at https://doi.org/10.1101/2020.11.09.373613 (2020).
Cusanovich, D. A. et al. Multiplex single cell profiling of chromatin accessibility by combinatorial cellular indexing. Science 348, 910–914 (2015).
pubmed: 25953818
pmcid: 4836442
doi: 10.1126/science.aab1601
Schep, A. N., Wu, B., Buenrostro, J. D. & Greenleaf, W. J. chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data. Nat. Methods 14, 975–978 (2017).
pubmed: 28825706
pmcid: 5623146
doi: 10.1038/nmeth.4401
Khan, A. et al. JASPAR 2018: update of the open-access database of transcription factor binding profiles and its web framework. Nucleic Acids Res. 46 (D1), D260–D266 (2018).
pubmed: 29140473
doi: 10.1093/nar/gkx1126