CD49b defines functionally mature Treg cells that survey skin and vascular tissues

. 2018 Nov 05 ; 215 (11) : 2796-2814. [epub] 20181024

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30355617

Grantová podpora
F30 AI122721 NIAID NIH HHS - United States
P30 CA008748 NCI NIH HHS - United States
R37 AI034206 NIAID NIH HHS - United States
T32 GM007739 NIGMS NIH HHS - United States
Howard Hughes Medical Institute - United States

Regulatory T (Treg) cells prevent autoimmunity by limiting immune responses and inflammation in the secondary lymphoid organs and nonlymphoid tissues. While unique subsets of Treg cells have been described in some nonlymphoid tissues, their relationship to Treg cells in secondary lymphoid organs and circulation remains unclear. Furthermore, it is possible that Treg cells from similar tissue types share largely similar properties. We have identified a short-lived effector Treg cell subset that expresses the α2 integrin, CD49b, and exhibits a unique tissue distribution, being abundant in peripheral blood, vasculature, skin, and skin-draining lymph nodes, but uncommon in the intestines and in viscera-draining lymph nodes. CD49b+ Treg cells, which display superior functionality revealed by in vitro and in vivo assays, appear to develop after multiple rounds of cell division and TCR-dependent activation. Accordingly, single-cell RNA-seq analysis placed these cells at the apex of the Treg developmental trajectory. These results shed light on the identity and development of a functionally potent subset of mature effector Treg cells that recirculate through and survey peripheral tissues.

Zobrazit více v PubMed

Amir A.D., Davis K.L., Tadmor M.D., Simonds E.F., Levine J.H., Bendall S.C., Shenfeld D.K., Krishnaswamy S., Nolan G.P., and Pe’er D.. 2013. viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia. Nat. Biotechnol. 31:545–552. 10.1038/nbt.2594 PubMed DOI PMC

Anders S., McCarthy D.J., Chen Y., Okoniewski M., Smyth G.K., Huber W., and Robinson M.D.. 2013. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat. Protoc. 8:1765–1786. 10.1038/nprot.2013.099 PubMed DOI

Anders S., Pyl P.T., and Huber W.. 2015. HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 31:166–169. 10.1093/bioinformatics/btu638 PubMed DOI PMC

Anderson K.G., Mayer-Barber K., Sung H., Beura L., James B.R., Taylor J.J., Qunaj L., Griffith T.S., Vezys V., Barber D.L., and Masopust D.. 2014. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat. Protoc. 9:209–222. 10.1038/nprot.2014.005 PubMed DOI PMC

Arpaia N., Green J.A., Moltedo B., Arvey A., Hemmers S., Yuan S., Treuting P.M., and Rudensky A.Y.. 2015. A Distinct Function of Regulatory T Cells in Tissue Protection. Cell. 162:1078–1089. 10.1016/j.cell.2015.08.021 PubMed DOI PMC

Arvey A., van der Veeken J., Samstein R.M., Feng Y., Stamatoyannopoulos J.A., and Rudensky A.Y.. 2014. Inflammation-induced repression of chromatin bound by the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 15:580–587. 10.1038/ni.2868 PubMed DOI PMC

Azizi E., Carr A.J., Plitas G., Cornish A.E., Konopacki C., Prabhakaran S., Nainys J., Wu K., Kiseliovas V., Setty M., et al. . 2018. Single-cell Map of Diverse Immune Phenotypes in the Breast Tumor Microenvironment. Cell. 174:1293–1308.e36. 10.1016/j.cell.2018.05.060 PubMed DOI PMC

Bajénoff M., Breart B., Huang A.Y.C., Qi H., Cazareth J., Braud V.M., Germain R.N., and Glaichenhaus N.. 2006. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J. Exp. Med. 203:619–631. 10.1084/jem.20051474 PubMed DOI PMC

Bolger A.M., Lohse M., and Usadel B.. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30:2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC

Bolotin D.A., Poslavsky S., Mitrophanov I., Shugay M., Mamedov I.Z., Putintseva E.V., and Chudakov D.M.. 2015. MiXCR: software for comprehensive adaptive immunity profiling. Nat. Methods. 12:380–381. 10.1038/nmeth.3364 PubMed DOI

Braun A., Dewert N., Brunnert F., Schnabel V., Hardenberg J.-H., Richter B., Zachmann K., Cording S., Claßen A., Brans R., et al. . 2015. Integrin αE(CD103) Is Involved in Regulatory T-Cell Function in Allergic Contact Hypersensitivity. J. Invest. Dermatol. 135:2982–2991. 10.1038/jid.2015.287 PubMed DOI

Burzyn D., Kuswanto W., Kolodin D., Shadrach J.L., Cerletti M., Jang Y., Sefik E., Tan T.G., Wagers A.J., Benoist C., and Mathis D.. 2013. A special population of regulatory T cells potentiates muscle repair. Cell. 155:1282–1295. 10.1016/j.cell.2013.10.054 PubMed DOI PMC

Camberis M., Le Gros G., and Urban J. Jr. 2003. Animal model of Nippostrongylus brasiliensis and Heligmosomoides polygyrus. Curr. Protoc. Immunol. Chapter 19:19.12. PubMed

Carlson C.M., Endrizzi B.T., Wu J., Ding X., Weinreich M.A., Walsh E.R., Wani M.A., Lingrel J.B., Hogquist K.A., and Jameson S.C.. 2006. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature. 442:299–302. 10.1038/nature04882 PubMed DOI

Casey K.A., Fraser K.A., Schenkel J.M., Moran A., Abt M.C., Beura L.K., Lucas P.J., Artis D., Wherry E.J., Hogquist K., et al. . 2012. Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J. Immunol. 188:4866–4875. 10.4049/jimmunol.1200402 PubMed DOI PMC

Chen J., Diacovo T.G., Grenache D.G., Santoro S.A., and Zutter M.M.. 2002. The α(2) integrin subunit-deficient mouse: a multifaceted phenotype including defects of branching morphogenesis and hemostasis. Am. J. Pathol. 161:337–344. 10.1016/S0002-9440(10)64185-5 PubMed DOI PMC

Chinen T., Kannan A.K., Levine A.G., Fan X., Klein U., Zheng Y., Gasteiger G., Feng Y., Fontenot J.D., and Rudensky A.Y.. 2016. An essential role for the IL-2 receptor in Treg cell function. Nat. Immunol. 17:1322–1333. 10.1038/ni.3540 PubMed DOI PMC

Cipolletta D., Feuerer M., Li A., Kamei N., Lee J., Shoelson S.E., Benoist C., and Mathis D.. 2012. PPAR-γ is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature. 486:549–553. 10.1038/nature11132 PubMed DOI PMC

Delacher M., Imbusch C.D., Weichenhan D., Breiling A., Hotz-Wagenblatt A., Träger U., Hofer A.C., Kägebein D., Wang Q., Frauhammer F., et al. . 2017. Genome-wide DNA-methylation landscape defines specialization of regulatory T cells in tissues. Nat. Immunol. 18:1160–1172. 10.1038/ni.3799 PubMed DOI PMC

Denzler R., Agarwal V., Stefano J., Bartel D.P., and Stoffel M.. 2014. Assessing the ceRNA hypothesis with quantitative measurements of miRNA and target abundance. Mol. Cell. 54:766–776. 10.1016/j.molcel.2014.03.045 PubMed DOI PMC

Fan X., and Rudensky A.Y.. 2016. Hallmarks of Tissue-Resident Lymphocytes. Cell. 164:1198–1211. 10.1016/j.cell.2016.02.048 PubMed DOI PMC

Feng Y., van der Veeken J., Shugay M., Putintseva E.V., Osmanbeyoglu H.U., Dikiy S., Hoyos B.E., Moltedo B., Hemmers S., Treuting P., et al. . 2015. A mechanism for expansion of regulatory T-cell repertoire and its role in self-tolerance. Nature. 528:132–136. PubMed PMC

Feuerer M., Herrero L., Cipolletta D., Naaz A., Wong J., Nayer A., Lee J., Goldfine A.B., Benoist C., Shoelson S., and Mathis D.. 2009. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 15:930–939. 10.1038/nm.2002 PubMed DOI PMC

Filzmoser P., and Gschwandtner M.. 2018. mvoutlier: Multivariate Outlier Detection Based on Robust Methods. Available at: https://cran.r-project.org/web/packages/mvoutlier/index.html (accessed June 15, 2018).

Fontenot J.D., Rasmussen J.P., Williams L.M., Dooley J.L., Farr A.G., and Rudensky A.Y.. 2005. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 22:329–341. 10.1016/j.immuni.2005.01.016 PubMed DOI

Garrod K.R., Wei S.H., Parker I., and Cahalan M.D.. 2007. Natural killer cells actively patrol peripheral lymph nodes forming stable conjugates to eliminate MHC-mismatched targets. Proc. Natl. Acad. Sci. USA. 104:12081–12086. 10.1073/pnas.0702867104 PubMed DOI PMC

Gerlach C., Moseman E.A., Loughhead S.M., Alvarez D., Zwijnenburg A.J., Waanders L., Garg R., de la Torre J.C., and von Andrian U.H.. 2016. The Chemokine Receptor CX3CR1 Defines Three Antigen-Experienced CD8 T Cell Subsets with Distinct Roles in Immune Surveillance and Homeostasis. Immunity. 45:1270–1284. 10.1016/j.immuni.2016.10.018 PubMed DOI PMC

Gonzalez A., Andre-Schmutz I., Carnaud C., Mathis D., and Benoist C.. 2001. Damage control, rather than unresponsiveness, effected by protective DX5+ T cells in autoimmune diabetes. Nat. Immunol. 2:1117–1125. 10.1038/ni738 PubMed DOI

Habart D., Cheli Y., Nugent D.J., Ruggeri Z.M., and Kunicki T.J.. 2013. Conditional knockout of integrin α2β1 in murine megakaryocytes leads to reduced mean platelet volume. PLoS One. 8:e55094 10.1371/journal.pone.0055094 PubMed DOI PMC

Haghverdi L., Buettner F., and Theis F.J.. 2015. Diffusion maps for high-dimensional single-cell analysis of differentiation data. Bioinformatics. 31:2989–2998. 10.1093/bioinformatics/btv325 PubMed DOI

Hemler M.E., Jacobson J.G., and Strominger J.L.. 1985. Biochemical characterization of VLA-1 and VLA-2. Cell surface heterodimers on activated T cells. J. Biol. Chem. 260:15246–15252. PubMed

Hirahara K., Liu L., Clark R.A., Yamanaka K., Fuhlbrigge R.C., and Kupper T.S.. 2006. The majority of human peripheral blood CD4+CD25highFoxp3+ regulatory T cells bear functional skin-homing receptors. J. Immunol. 177:4488–4494. 10.4049/jimmunol.177.7.4488 PubMed DOI

Holtkötter O., Nieswandt B., Smyth N., Müller W., Hafner M., Schulte V., Krieg T., and Eckes B.. 2002. Integrin α 2-deficient mice develop normally, are fertile, but display partially defective platelet interaction with collagen. J. Biol. Chem. 277:10789–10794. 10.1074/jbc.M112307200 PubMed DOI

Huehn J., Siegmund K., Lehmann J.C.U., Siewert C., Haubold U., Feuerer M., Debes G.F., Lauber J., Frey O., Przybylski G.K., et al. . 2004. Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J. Exp. Med. 199:303–313. 10.1084/jem.20031562 PubMed DOI PMC

Ikebuchi R., Teraguchi S., Vandenbon A., Honda T., Shand F.H.W., Nakanishi Y., Watanabe T., and Tomura M.. 2016. A rare subset of skin-tropic regulatory T cells expressing Il10/Gzmb inhibits the cutaneous immune response. Sci. Rep. 6:35002 10.1038/srep35002 PubMed DOI PMC

Itohara S., Mombaerts P., Lafaille J., Iacomini J., Nelson A., Clarke A.R., Hooper M.L., Farr A., and Tonegawa S.. 1993. T cell receptor delta gene mutant mice: independent generation of alpha beta T cells and programmed rearrangements of gamma delta TCR genes. Cell. 72:337–348. 10.1016/0092-8674(93)90112-4 PubMed DOI

Izraelson M., Nakonechnaya T.O., Moltedo B., Egorov E.S., Kasatskaya S.A., Putintseva E.V., Mamedov I.Z., Staroverov D.B., Shemiakina I.I., Zakharova M.Y., et al. . 2018. Comparative analysis of murine T-cell receptor repertoires. Immunology. 153:133–144. 10.1111/imm.12857 PubMed DOI PMC

Josefowicz S.Z., Lu L.-F., and Rudensky A.Y.. 2012. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30:531–564. 10.1146/annurev.immunol.25.022106.141623 PubMed DOI PMC

Kamanaka M., Kim S.T., Wan Y.Y., Sutterwala F.S., Lara-Tejero M., Galán J.E., Harhaj E., and Flavell R.A.. 2006. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity. 25:941–952. 10.1016/j.immuni.2006.09.013 PubMed DOI

Kamran P., Sereti K.-I., Zhao P., Ali S.R., Weissman I.L., and Ardehali R.. 2013. Parabiosis in mice: a detailed protocol. J. Vis. Exp. 80:1–5. PubMed PMC

Kassiotis G., Gray D., Kiafard Z., Zwirner J., and Stockinger B.. 2006. Functional specialization of memory Th cells revealed by expression of integrin CD49b. J. Immunol. 177:968–975. 10.4049/jimmunol.177.2.968 PubMed DOI

Kerdiles Y.M., Beisner D.R., Tinoco R., Dejean A.S., Castrillon D.H., DePinho R.A., and Hedrick S.M.. 2009. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 10:176–184. 10.1038/ni.1689 PubMed DOI PMC

Kim D., Pertea G., Trapnell C., Pimentel H., Kelley R., and Salzberg S.L.. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14:R36 10.1186/gb-2013-14-4-r36 PubMed DOI PMC

Kim J.M., Rasmussen J.P., and Rudensky A.Y.. 2007. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8:191–197. 10.1038/ni1428 PubMed DOI

Kolodin D., van Panhuys N., Li C., Magnuson A.M., Cipolletta D., Miller C.M., Wagers A., Germain R.N., Benoist C., and Mathis D.. 2015. Antigen- and cytokine-driven accumulation of regulatory T cells in visceral adipose tissue of lean mice. Cell Metab. 21:543–557. 10.1016/j.cmet.2015.03.005 PubMed DOI PMC

Korn L.L., Hubbeling H.G., Porrett P.M., Yang Q., Barnett L.G., and Laufer T.M.. 2014. Regulatory T cells occupy an isolated niche in the intestine that is antigen independent. Cell Reports. 9:1567–1573. 10.1016/j.celrep.2014.11.006 PubMed DOI

Langmead B., and Salzberg S.L.. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 9:357–359. 10.1038/nmeth.1923 PubMed DOI PMC

Lee J.Y., Skon C.N., Lee Y.J., Oh S., Taylor J.J., Malhotra D., Jenkins M.K., Rosenfeld M.G., Hogquist K.A., and Jameson S.C.. 2015. The transcription factor KLF2 restrains CD4+ T follicular helper cell differentiation. Immunity. 42:252–264. 10.1016/j.immuni.2015.01.013 PubMed DOI PMC

Levine A.G., Arvey A., Jin W., and Rudensky A.Y.. 2014. Continuous requirement for the TCR in regulatory T cell function. Nat. Immunol. 15:1070–1078. 10.1038/ni.3004 PubMed DOI PMC

Levine A.G., Hemmers S., Baptista A.P., Schizas M., Faire M.B., Moltedo B., Konopacki C., Schmidt-Supprian M., Germain R.N., Treuting P.M., and Rudensky A.Y.. 2017. Suppression of lethal autoimmunity by regulatory T cells with a single TCR specificity. J. Exp. Med. 214:609–622. PubMed PMC

Levine J.H., Simonds E.F., Bendall S.C., Davis K.L., Amir A.D., Tadmor M.D., Litvin O., Fienberg H.G., Jager A., Zunder E.R., et al. . 2015. Data-Driven Phenotypic Dissection of AML Reveals Progenitor-like Cells that Correlate with Prognosis. Cell. 162:184–197. 10.1016/j.cell.2015.05.047 PubMed DOI PMC

Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., and Durbin R.. 1000 Genome Project Data Processing Subgroup . 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 25:2078–2079. 10.1093/bioinformatics/btp352 PubMed DOI PMC

Liston A., Nutsch K.M., Farr A.G., Lund J.M., Rasmussen J.P., Koni P.A., and Rudensky A.Y.. 2008. Differentiation of regulatory Foxp3+ T cells in the thymic cortex. Proc. Natl. Acad. Sci. USA. 105:11903–11908. 10.1073/pnas.0801506105 PubMed DOI PMC

Liu Z., Gerner M.Y., Van Panhuys N., Levine A.G., Rudensky A.Y., and Germain R.N.. 2015. Immune homeostasis enforced by co-localized effector and regulatory T cells. Nature. 528:225–230. 10.1038/nature16169 PubMed DOI PMC

Love M.I., Huber W., and Anders S.. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15:550 10.1186/s13059-014-0550-8 PubMed DOI PMC

Luo C.T., Liao W., Dadi S., Toure A., and Li M.O.. 2016. Graded Foxo1 activity in Treg cells differentiates tumour immunity from spontaneous autoimmunity. Nature. 529:532–536. 10.1038/nature16486 PubMed DOI PMC

Mackay L.K., Rahimpour A., Ma J.Z., Collins N., Stock A.T., Hafon M.-L., Vega-Ramos J., Lauzurica P., Mueller S.N., Stefanovic T., et al. . 2013. The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat. Immunol. 14:1294–1301. 10.1038/ni.2744 PubMed DOI

Madamanchi A., Santoro S.A., and Zutter M.M.. 2014. Alpha2beta1 integrin. I Domain Integrins. Springer Netherlands, Dordrecht, Netherlands: pp. 41–60. PubMed

Maere S., Heymans K., and Kuiper M.. 2005. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics. 21:3448–3449. 10.1093/bioinformatics/bti551 PubMed DOI

Merico D., Isserlin R., Stueker O., Emili A., and Bader G.D.. 2010. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One. 5:e13984 10.1371/journal.pone.0013984 PubMed DOI PMC

Mombaerts P., Clarke A.R., Rudnicki M.A., Iacomini J., Itohara S., Lafaille J.J., Wang L., Ichikawa Y., Jaenisch R., Hooper M.L., et al. . 1992. Mutations in T-cell antigen receptor genes alpha and beta block thymocyte development at different stages. Nature. 360:225–231. 10.1038/360225a0 PubMed DOI

Morton A.M., Sefik E., Upadhyay R., Weissleder R., Benoist C., and Mathis D.. 2014. Endoscopic photoconversion reveals unexpectedly broad leukocyte trafficking to and from the gut. Proc. Natl. Acad. Sci. USA. 111:6696–6701. 10.1073/pnas.1405634111 PubMed DOI PMC

O’Sullivan T.E., Rapp M., Fan X., Weizman O.-E., Bhardwaj P., Adams N.M., Walzer T., Dannenberg A.J., and Sun J.C.. 2016. Adipose-Resident Group 1 Innate Lymphoid Cells Promote Obesity-Associated Insulin Resistance. Immunity. 45:428–441. 10.1016/j.immuni.2016.06.016 PubMed DOI PMC

Ohnmacht C., Park J., Cording S., Wing J.B., Atarashi K., Obata Y., Gaboriau-Routhiau V., Marques R., Dulauroy S., Fedoseeva M., et al. . 2015. The microbiota regulates type 2 immunity through RORγt+ T cells. Science. 349:989–993. 10.1126/science.aac4263 PubMed DOI

Onishi Y., Fehervari Z., Yamaguchi T., and Sakaguchi S.. 2008. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA. 105:10113–10118. 10.1073/pnas.0711106105 PubMed DOI PMC

Peng H., Jiang X., Chen Y., Sojka D.K., Wei H., Gao X., Sun R., Yokoyama W.M., and Tian Z.. 2013. Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123:1444–1456. 10.1172/JCI66381 PubMed DOI PMC

Polic B., Kunkel D., Scheffold A., and Rajewsky K.. 2001. How alpha beta T cells deal with induced TCR alpha ablation. Proc. Natl. Acad. Sci. USA. 98:8744–8749. 10.1073/pnas.141218898 PubMed DOI PMC

Ray S.J., Franki S.N., Pierce R.H., Dimitrova S., Koteliansky V., Sprague A.G., Doherty P.C., de Fougerolles A.R., and Topham D.J.. 2004. The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity. 20:167–179. 10.1016/S1074-7613(04)00021-4 PubMed DOI

Rubtsov Y.P., Rasmussen J.P., Chi E.Y., Fontenot J., Castelli L., Ye X., Treuting P., Siewe L., Roers A., Henderson W.R. Jr., et al. . 2008. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity. 28:546–558. 10.1016/j.immuni.2008.02.017 PubMed DOI

Rubtsov Y.P., Niec R.E., Josefowicz S., Li L., Darce J., Mathis D., Benoist C., and Rudensky A.Y.. 2010. Stability of the regulatory T cell lineage in vivo. Science. 329:1667–1671. 10.1126/science.1191996 PubMed DOI PMC

Sather B.D., Treuting P., Perdue N., Miazgowicz M., Fontenot J.D., Rudensky A.Y., and Campbell D.J.. 2007. Altering the distribution of Foxp3(+) regulatory T cells results in tissue-specific inflammatory disease. J. Exp. Med. 204:1335–1347. 10.1084/jem.20070081 PubMed DOI PMC

Schiering C., Krausgruber T., Chomka A., Fröhlich A., Adelmann K., Wohlfert E.A., Pott J., Griseri T., Bollrath J., Hegazy A.N., et al. . 2014. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature. 513:564–568. 10.1038/nature13577 PubMed DOI PMC

Sebzda E., Zou Z., Lee J.S., Wang T., and Kahn M.L.. 2008. Transcription factor KLF2 regulates the migration of naive T cells by restricting chemokine receptor expression patterns. Nat. Immunol. 9:292–300. 10.1038/ni1565 PubMed DOI

Sefik E., Geva-Zatorsky N., Oh S., Konnikova L., Zemmour D., McGuire A.M., Burzyn D., Ortiz-Lopez A., Lobera M., Yang J., et al. . 2015. MUCOSAL IMMUNOLOGY. Individual intestinal symbionts induce a distinct population of RORγ+ regulatory T cells. Science. 349:993–997. 10.1126/science.aaa9420 PubMed DOI PMC

Setty M., Tadmor M.D., Reich-Zeliger S., Angel O., Salame T.M., Kathail P., Choi K., Bendall S., Friedman N., and Pe’er D.. 2016. Wishbone identifies bifurcating developmental trajectories from single-cell data. Nat. Biotechnol. 34:637–645. 10.1038/nbt.3569 PubMed DOI PMC

Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., and Ideker T.. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13:2498–2504. 10.1101/gr.1239303 PubMed DOI PMC

Shugay M., Britanova O.V., Merzlyak E.M., Turchaninova M.A., Mamedov I.Z., Tuganbaev T.R., Bolotin D.A., Staroverov D.B., Putintseva E.V., Plevova K., et al. . 2014. Towards error-free profiling of immune repertoires. Nat. Methods. 11:653–655. 10.1038/nmeth.2960 PubMed DOI

Shugay M., Bagaev D.V., Turchaninova M.A., Bolotin D.A., Britanova O.V., Putintseva E.V., Pogorelyy M.V., Nazarov V.I., Zvyagin I.V., Kirgizova V.I., et al. . 2015. VDJtools: Unifying Post-analysis of T Cell Receptor Repertoires. PLOS Comput. Biol. 11:e1004503 10.1371/journal.pcbi.1004503 PubMed DOI PMC

Skon C.N., Lee J.-Y., Anderson K.G., Masopust D., Hogquist K.A., and Jameson S.C.. 2013. Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat. Immunol. 14:1285–1293. 10.1038/ni.2745 PubMed DOI PMC

Śledzińska A., Hemmers S., Mair F., Gorka O., Ruland J., Fairbairn L., Nissler A., Müller W., Waisman A., Becher B., and Buch T.. 2013. TGF-β signalling is required for CD4+ T cell homeostasis but dispensable for regulatory T cell function. PLoS Biol. 11:e1001674 10.1371/journal.pbio.1001674 PubMed DOI PMC

Sojka D.K., Plougastel-Douglas B., Yang L., Pak-Wittel M.A., Artyomov M.N., Ivanova Y., Zhong C., Chase J.M., Rothman P.B., Yu J., et al. . 2014. Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells. eLife. 3:e01659 10.7554/eLife.01659 PubMed DOI PMC

Stephens G.L., Andersson J., and Shevach E.M.. 2007. Distinct subsets of FoxP3+ regulatory T cells participate in the control of immune responses. J. Immunol. 178:6901–6911. 10.4049/jimmunol.178.11.6901 PubMed DOI

Suffia I., Reckling S.K., Salay G., and Belkaid Y.. 2005. A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J. Immunol. 174:5444–5455. 10.4049/jimmunol.174.9.5444 PubMed DOI

Thomson A.W., and Knolle P.A.. 2010. Antigen-presenting cell function in the tolerogenic liver environment. Nat. Rev. Immunol. 10:753–766. 10.1038/nri2858 PubMed DOI

Tokoyoda K., Zehentmeier S., Hegazy A.N., Albrecht I., Grün J.R., Löhning M., and Radbruch A.. 2009. Professional memory CD4+ T lymphocytes preferentially reside and rest in the bone marrow. Immunity. 30:721–730. 10.1016/j.immuni.2009.03.015 PubMed DOI

Tomura M., Honda T., Tanizaki H., Otsuka A., Egawa G., Tokura Y., Waldmann H., Hori S., Cyster J.G., Watanabe T., et al. . 2010. Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice. J. Clin. Invest. 120:883–893. 10.1172/JCI40926 PubMed DOI PMC

van der Maaten L., and Hinton G.. 2008. Visualizing high-dimensional data using t-SNE. J. Mach. Learn. Res. 9:2579–2605.

van Dijk D., Nainys J., Sharma R., Kathail P., Carr A.J., Moon K.R., Mazutis L., Wolf G., Krishnaswamy S., and Pe’er D.. 2017. MAGIC: A diffusion-based imputation method reveals gene-gene interactions in single-cell RNA-sequencing data. https://www.biorxiv.org/content/early/2017/02/25/111591 (Preprint posted February 25, 2017).

von Andrian U.H., and Mackay C.R.. 2000. T-cell function and migration. Two sides of the same coin. N. Engl. J. Med. 343:1020–1034. 10.1056/NEJM200010053431407 PubMed DOI

Weber J.P., Fuhrmann F., Feist R.K., Lahmann A., Al Baz M.S., Gentz L.-J., Vu Van D., Mages H.W., Haftmann C., Riedel R., et al. . 2015. ICOS maintains the T follicular helper cell phenotype by down-regulating Krüppel-like factor 2. J. Exp. Med. 212:217–233. 10.1084/jem.20141432 PubMed DOI PMC

Werr J., Johansson J., Eriksson E.E., Hedqvist P., Ruoslahti E., and Lindbom L.. 2000. Integrin alpha(2)beta(1) (VLA-2) is a principal receptor used by neutrophils for locomotion in extravascular tissue. Blood. 95:1804–1809. PubMed

Wolfenson H., Lavelin I., and Geiger B.. 2013. Dynamic regulation of the structure and functions of integrin adhesions. Dev. Cell. 24:447–458. 10.1016/j.devcel.2013.02.012 PubMed DOI PMC

Yang S., Fujikado N., Kolodin D., Benoist C., and Mathis D.. 2015. Immune tolerance. Regulatory T cells generated early in life play a distinct role in maintaining self-tolerance. Science. 348:589–594. 10.1126/science.aaa7017 PubMed DOI PMC

Yuan X., Dee M.J., Altman N.H., and Malek T.R.. 2015. IL-2Rβ-dependent signaling and CD103 functionally cooperate to maintain tolerance in the gut mucosa. J. Immunol. 194:1334–1346. 10.4049/jimmunol.1400955 PubMed DOI PMC

Zhang N., and Bevan M.J.. 2013. Transforming growth factor-β signaling controls the formation and maintenance of gut-resident memory T cells by regulating migration and retention. Immunity. 39:687–696. 10.1016/j.immuni.2013.08.019 PubMed DOI PMC

Zheng G.X.Y., Terry J.M., Belgrader P., Ryvkin P., Bent Z.W., Wilson R., Ziraldo S.B., Wheeler T.D., McDermott G.P., Zhu J., et al. . 2017. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8:14049 10.1038/ncomms14049 PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Convergence, plasticity, and tissue residence of regulatory T cell response via TCR repertoire prism

. 2024 Apr 09 ; 12 () : . [epub] 20240409

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...