Regulatory T Cells in Skin Facilitate Epithelial Stem Cell Differentiation

Cell - Tập 169 - Trang 1119-1129.e11 - 2017
Niwa Ali1,2, Bahar Zirak1, Robert Sanchez Rodriguez1, Mariela L. Pauli1, Hong-An Truong1, Kevin Lai1, Richard Ahn1, Kaitlin Corbin3, Margaret M. Lowe1, Tiffany C. Scharschmidt1, Keyon Taravati1, Madeleine R. Tan1, Roberto R. Ricardo-Gonzalez1, Audrey Nosbaum1, Marta Bertolini4, Wilson Liao1, Frank O. Nestle2, Ralf Paus5, George Cotsarelis6, Abul K. Abbas3
1Department of Dermatology, University of California, San Francisco, San Francisco, CA 94143, USA
2Cutaneous Medicine Unit, St. John’s Institute of Dermatology, King’s College London, London WC2R 2LS, UK
3Department of Pathology, University of California, San Francisco, San Francisco, CA 94143, USA
4Department of Dermatology, University of Muenster, 48149 Muenster, Germany
5Centre for Dermatological Research, University of Manchester & NIHR Manchester Biomedical Research Centre, Manchester M13 9PL, UK
6Department of Dermatology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA

Tài liệu tham khảo

Anders, 2010, Differential expression analysis for sequence count data, Genome Biol., 11, R106, 10.1186/gb-2010-11-10-r106 Anders, 2015, HTSeq--a Python framework to work with high-throughput sequencing data, Bioinformatics, 31, 166, 10.1093/bioinformatics/btu638 Arpaia, 2015, A distinct function of regulatory T cells in tissue protection, Cell, 162, 1078, 10.1016/j.cell.2015.08.021 Blanpain, 2009, Epidermal homeostasis: a balancing act of stem cells in the skin, Nat. Rev. Mol. Cell Biol., 10, 207, 10.1038/nrm2636 Blanpain, 2006, Canonical notch signaling functions as a commitment switch in the epidermal lineage, Genes Dev., 20, 3022, 10.1101/gad.1477606 Boldajipour, 2016, Tumor-infiltrating lymphocytes are dynamically desensitized to antigen but are maintained by homeostatic cytokine, JCI Insight, 1, e89289, 10.1172/jci.insight.89289 Brooker, 2006, Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear, Development, 133, 1277, 10.1242/dev.02284 Broz, 2014, Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity, Cancer Cell, 26, 638, 10.1016/j.ccell.2014.09.007 Burzyn, 2013, A special population of regulatory T cells potentiates muscle repair, Cell, 155, 1282, 10.1016/j.cell.2013.10.054 Castela, 2014, Effects of low-dose recombinant interleukin 2 to promote T-regulatory cells in alopecia areata, JAMA Dermatol., 150, 748, 10.1001/jamadermatol.2014.504 Chen, 2012, An RNA interference screen uncovers a new molecule in stem cell self-renewal and long-term regeneration, Nature, 485, 104, 10.1038/nature10940 Chow, 2013, Dermal regulatory T cells display distinct migratory behavior that is modulated during adaptive and innate inflammation, J. Immunol., 191, 3049, 10.4049/jimmunol.1203205 Cipolletta, 2012, PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells, Nature, 486, 549, 10.1038/nature11132 Clark, 2006, The vast majority of CLA+ T cells are resident in normal skin, J. Immunol., 176, 4431, 10.4049/jimmunol.176.7.4431 Cotsarelis, 1990, Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis, Cell, 61, 1329, 10.1016/0092-8674(90)90696-C de Hoon, 2004, Open source clustering software, Bioinformatics, 20, 1453, 10.1093/bioinformatics/bth078 Estrach, 2006, Jagged 1 is a beta-catenin target gene required for ectopic hair follicle formation in adult epidermis, Development, 133, 4427, 10.1242/dev.02644 Feuerer, 2009, Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters, Nat. Med., 15, 930, 10.1038/nm.2002 Friedman, 2010, Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics, J. Exp. Med., 207, 2733, 10.1084/jem.20091201 Fujisaki, 2011, In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche, Nature, 474, 216, 10.1038/nature10160 Gratz, 2013, Cutting Edge: memory regulatory t cells require IL-7 and not IL-2 for their maintenance in peripheral tissues, J. Immunol., 190, 4483, 10.4049/jimmunol.1300212 Headley, 2016, Visualization of immediate immune responses to pioneer metastatic cells in the lung, Nature, 531, 513, 10.1038/nature16985 Ito, 2005, Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis, Nat. Med., 11, 1351, 10.1038/nm1328 Jaks, 2008, Lgr5 marks cycling, yet long-lived, hair follicle stem cells, Nat. Genet., 40, 1291, 10.1038/ng.239 Kim, 2007, Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice, Nat. Immunol., 8, 191, 10.1038/ni1428 Lecuit, 2007, Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis, Nat. Rev. Mol. Cell Biol., 8, 633, 10.1038/nrm2222 Levy, 2005, Distinct stem cell populations regenerate the follicle and interfollicular epidermis, Dev. Cell, 9, 855, 10.1016/j.devcel.2005.11.003 Li, 2009, The Sequence Alignment/Map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Lin, 2007, Regulatory T cell development in the absence of functional Foxp3, Nat. Immunol., 8, 359, 10.1038/ni1445 Lindsay, 2015, Antigen recognition in the islets changes with progression of autoimmune islet infiltration, J. Immunol., 194, 522, 10.4049/jimmunol.1400626 Looney, 2011, Stabilized imaging of immune surveillance in the mouse lung, Nat. Methods, 8, 91, 10.1038/nmeth.1543 Lowry, 2005, Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells, Genes Dev., 19, 1596, 10.1101/gad.1324905 Matheu, 2013, Three phases of CD8 T cell response in the lung following H1N1 influenza infection and sphingosine 1 phosphate agonist therapy, PLoS ONE, 8, e58033, 10.1371/journal.pone.0058033 Meier-Stiegen, 2010, Activated Notch1 target genes during embryonic cell differentiation depend on the cellular context and include lineage determinants and inhibitors, PLoS ONE, 5, e11481, 10.1371/journal.pone.0011481 Morris, 2004, Capturing and profiling adult hair follicle stem cells, Nat. Biotechnol., 22, 411, 10.1038/nbt950 Müller-Röver, 2001, A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages, J. Invest. Dermatol., 117, 3, 10.1046/j.0022-202x.2001.01377.x Nagao, 2012, Stress-induced production of chemokines by hair follicles regulates the trafficking of dendritic cells in skin, Nat. Immunol., 13, 744, 10.1038/ni.2353 Nosbaum, 2016, Cutting edge: regulatory T cells facilitate cutaneous wound healing, J. Immunol., 196, 2010, 10.4049/jimmunol.1502139 Panduro, 2016, Tissue Tregs, Annu. Rev. Immunol., 34, 609, 10.1146/annurev-immunol-032712-095948 Petukhova, 2010, Genome-wide association study in alopecia areata implicates both innate and adaptive immunity, Nature, 466, 113, 10.1038/nature09114 Reich, 2006, GenePattern 2.0, Nat. Genet., 38, 500, 10.1038/ng0506-500 Rubtsov, 2008, Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces, Immunity, 28, 546, 10.1016/j.immuni.2008.02.017 Sanchez Rodriguez, 2014, Memory regulatory T cells reside in human skin, J. Clin. Invest., 124, 1027, 10.1172/JCI72932 Sano, 2016, Intravital imaging of mouse urothelium reveals activation of extracellular signal-regulated kinase by stretch-induced intravesical release of ATP, Physiol. Rep., 4, e13033, 10.14814/phy2.13033 Scharschmidt, 2015, A wave of regulatory T cells into neonatal skin mediates tolerance to commensal microbes, Immunity, 43, 1011, 10.1016/j.immuni.2015.10.016 Sojka, 2011, Regulatory T cells inhibit acute IFN-γ synthesis without blocking T-helper cell type 1 (Th1) differentiation via a compartmentalized requirement for IL-10, Proc. Natl. Acad. Sci. USA, 108, 18336, 10.1073/pnas.1110566108 Thornton, 2012, Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung, J. Exp. Med., 209, 1183, 10.1084/jem.20112667 Trapnell, 2009, TopHat: discovering splice junctions with RNA-seq, Bioinformatics, 25, 1105, 10.1093/bioinformatics/btp120 Trempus, 2003, Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34, J. Invest. Dermatol., 120, 501, 10.1046/j.1523-1747.2003.12088.x Tumbar, 2004, Defining the epithelial stem cell niche in skin, Science, 303, 359, 10.1126/science.1092436 Vas, 2004, Soluble Jagged-1 is able to inhibit the function of its multivalent form to induce hematopoietic stem cell self-renewal in a surrogate in vitro assay, J. Leukoc. Biol., 75, 714, 10.1189/jlb.1003462 Vauclair, 2005, Notch1 is essential for postnatal hair follicle development and homeostasis, Dev. Biol., 284, 184, 10.1016/j.ydbio.2005.05.018 Villalta, 2014, Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy, Sci. Transl. Med., 6, 258ra142, 10.1126/scitranslmed.3009925 Vinegoni, 2012, Motion compensation using a suctioning stabilizer for intravital microscopy, Intravital, 1, 115, 10.4161/intv.23017 Zaid, 2014, Persistence of skin-resident memory T cells within an epidermal niche, Proc. Natl. Acad. Sci. USA, 111, 5307, 10.1073/pnas.1322292111