A High-Dimensional Atlas of Human T Cell Diversity Reveals Tissue-Specific Trafficking and Cytokine Signatures

Immunity

Volumn 45, Issue 2, 2016, Pages 442-456

  Wong, Michael Thomas ^a   Ong, David Eng Hui ^b   Lim, Frances Sheau Huei ^b   Teng, Karen Wei Weng ^a   McGovern, Naomi ^a   Narayanan, Sriram ^a   Ho, Wen Qi ^a   Cerny, Daniela ^a,c   Tan, Henry Kun Kiaang ^d   Anicete, Rosslyn ^d   Tan, Bien Keem ^e   Lim, Tony Kiat Hon ^e   Chan, Chung Yip ^e   Cheow, Peng Chung ^e   Lee, Ser Yee ^e   Takano, Angela ^e   Tan, Eng Huat ^f   Tam, John Kit Chung ^g   Tan, Ern Yu ^h   Chan, Jerry Kok Yen ^d   Fink, Katja ^a   Bertoletti, Antonio ^a,i   Ginhoux, Florent ^a   Curotto de Lafaille, Maria Alicia ^a   Newell, Evan William ^a   more..

^a AGENCY FOR SCIENCE   (Singapore)

^b NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

^e SINGAPORE GENERAL HOSPITAL   (Singapore)

^f DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^g NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^h TAN TOCK SENG HOSPITAL   (Singapore)

ⁱ DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTEGRIN; ALPHA4 INTEGRIN; BETA1 INTEGRIN; BETA7 INTEGRIN; CD103 ANTIGEN; CD161 ANTIGEN; CD38 ANTIGEN; CD45RA ANTIGEN; CD45RO ANTIGEN; CD57 ANTIGEN; CHEMOKINE RECEPTOR CCR10; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CX3CR1; CHEMOKINE RECEPTOR CXCR5; CHEMOKINE RECEPTOR CXCR6; CUTANEOUS LYMPHOCYTE ASSOCIATED ANTIGEN; CYTOKINE; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 8; INTERLEUKIN 9; L SELECTIN; BIOLOGICAL MARKER; HOMING RECEPTOR; TRANSCRIPTOME;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BIODIVERSITY; BLOOD; CELL FUNCTION; CELL MIGRATION; CELL POPULATION; COLON; CONTROLLED STUDY; CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; HELPER CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE SYSTEM; LIVER; LUNG; LYMPHOID TISSUE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN; SPLEEN; T LYMPHOCYTE; TISSUE SPECIFICITY; TONSIL; UMBILICAL CORD BLOOD; ANIMAL; ANTIBODY SPECIFICITY; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MASS SPECTROMETRY; METABOLISM; PHYSIOLOGY; PROCEDURES; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; BIODIVERSITY; BIOMARKERS; BLOOD; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; HUMANS; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; MASS SPECTROMETRY; MICE; ORGAN SPECIFICITY; RECEPTORS, LYMPHOCYTE HOMING; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER; TRANSCRIPTOME;

EID: 84994242550     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.07.007     Document Type: Article

References (47)

1. Acosta-Rodriguez, E.V., Rivino, L., Geginat, J., Jarrossay, D., Gattorno, M., Lanzavecchia, A., Sallusto, F., Napolitani, G., Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8 (2007), 639–646.
2. Amir, el-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., Pe'er, D., viSNE enables visualization of high dimensional single-cell data and reveals phenotypic heterogeneity of leukemia. Nat. Biotechnol. 31 (2013), 545–552.
3. Becher, B., Schlitzer, A., Chen, J., Mair, F., Sumatoh, H.R., Teng, K.W., Low, D., Ruedl, C., Riccardi-Castagnoli, P., Poidinger, M., et al. High-dimensional analysis of the murine myeloid cell system. Nat. Immunol. 15 (2014), 1181–1189.
4. Bendall, S.C., Simonds, E.F., Qiu, P., Amir, el-A.D., Krutzik, P.O., Finck, R., Bruggner, R.V., Melamed, R., Trejo, A., Ornatsky, O.I., et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332 (2011), 687–696.
5. Bendall, S.C., Nolan, G.P., Roederer, M., Chattopadhyay, P.K., A deep profiler's guide to cytometry. Trends Immunol. 33 (2012), 323–332.
6. Campbell, J.J., Qin, S., Unutmaz, D., Soler, D., Murphy, K.E., Hodge, M.R., Wu, L., Butcher, E.C., Unique subpopulations of CD56+ NK and NK-T peripheral blood lymphocytes identified by chemokine receptor expression repertoire. J. Immunol. 166 (2001), 6477–6482.
7. Cerny, D., Haniffa, M., Shin, A., Bigliardi, P., Tan, B.K., Lee, B., Poidinger, M., Tan, E.Y., Ginhoux, F., Fink, K., Selective susceptibility of human skin antigen presenting cells to productive dengue virus infection. PLoS Pathog., 10, 2014, e1004548.
8. Cheng, Y., Wong, M.T., van der Maaten, L., Newell, E.W., Categorical Analysis of Human T Cell Heterogeneity with One-Dimensional Soli-Expression by Nonlinear Stochastic Embedding. J. Immunol. 196 (2016), 924–932.
9. Cosmi, L., De Palma, R., Santarlasci, V., Maggi, L., Capone, M., Frosali, F., Rodolico, G., Querci, V., Abbate, G., Angeli, R., et al. Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor. J. Exp. Med. 205 (2008), 1903–1916.
10. Cox, D., Brennan, M., Moran, N., Integrins as therapeutic targets: lessons and opportunities. Nat. Rev. Drug Discov. 9 (2010), 804–820.
11. Duhen, T., Campbell, D.J., IL-1β promotes the differentiation of polyfunctional human CCR6+CXCR3+ Th1/17 cells that are specific for pathogenic and commensal microbes. J. Immunol. 193 (2014), 120–129.
12. Duhen, T., Geiger, R., Jarrossay, D., Lanzavecchia, A., Sallusto, F., Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat. Immunol. 10 (2009), 857–863.
13. Fu, H., Wang, A., Mauro, C., Marelli-Berg, F., T lymphocyte trafficking: molecules and mechanisms. Front. Biosci. (Landmark Ed.) 18 (2013), 422–440.
14. Ghoreschi, K., Laurence, A., Yang, X.P., Tato, C.M., McGeachy, M.J., Konkel, J.E., Ramos, H.L., Wei, L., Davidson, T.S., Bouladoux, N., et al. Generation of pathogenic T(H)17 cells in the absence of TGF-β signalling. Nature 467 (2010), 967–971.
15. Gibbons, D., Fleming, P., Virasami, A., Michel, M.L., Sebire, N.J., Costeloe, K., Carr, R., Klein, N., Hayday, A., Interleukin-8 (CXCL8) production is a signatory T cell effector function of human newborn infants. Nat. Med. 20 (2014), 1206–1210.
16. Griffith, J.W., Sokol, C.L., Luster, A.D., Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 32 (2014), 659–702.
17. Hamada, H., Garcia-Hernandez, Mde.L., Reome, J.B., Misra, S.K., Strutt, T.M., McKinstry, K.K., Cooper, A.M., Swain, S.L., Dutton, R.W., Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J. Immunol. 182 (2009), 3469–3481.
18. He, D., Wu, L., Kim, H.K., Li, H., Elmets, C.A., Xu, H., CD8+ IL-17-producing T cells are important in effector functions for the elicitation of contact hypersensitivity responses. J. Immunol. 177 (2006), 6852–6858.
19. Hong, M., Sandalova, E., Low, D., Gehring, A.J., Fieni, S., Amadei, B., Urbani, S., Chong, Y.S., Guccione, E., Bertoletti, A., Trained immunity in newborn infants of HBV-infected mothers. Nat. Commun., 6, 2015, 6588.
20. Islam, S.A., Luster, A.D., T cell homing to epithelial barriers in allergic disease. Nat. Med. 18 (2012), 705–715.
21. Kattah, M.G., Wong, M.T., Yocum, M.D., Utz, P.J., Cytokines secreted in response to Toll-like receptor ligand stimulation modulate differentiation of human Th17 cells. Arthritis Rheum. 58 (2008), 1619–1629.
22. Kim, C.H., Rott, L., Kunkel, E.J., Genovese, M.C., Andrew, D.P., Wu, L., Butcher, E.C., Rules of chemokine receptor association with T cell polarization in vivo. J. Clin. Invest. 108 (2001), 1331–1339.
23. Mackay, L.K., Wynne-Jones, E., Freestone, D., Pellicci, D.G., Mielke, L.A., Newman, D.M., Braun, A., Masson, F., Kallies, A., Belz, G.T., Carbone, F.R., T-box Transcription Factors Combine with the Cytokines TGF-β and IL-15 to Control Tissue-Resident Memory T Cell Fate. Immunity 43 (2015), 1101–1111.
24. Newell, E.W., Davis, M.M., Beyond model antigens: high-dimensional methods for the analysis of antigen-specific T cells. Nat. Biotechnol. 32 (2014), 149–157.
25. Newell, E.W., Sigal, N., Bendall, S.C., Nolan, G.P., Davis, M.M., Cytometry by time-of-flight shows combinatorial cytokine expression and virus-specific cell niches within a continuum of CD8+ T cell phenotypes. Immunity 36 (2012), 142–152.
26. Park, C.O., Kupper, T.S., The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat. Med. 21 (2015), 688–697.
27. Sallusto, F., Lenig, D., Mackay, C.R., Lanzavecchia, A., Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J. Exp. Med. 187 (1998), 875–883.
28. Sallusto, F., Lenig, D., Förster, R., Lipp, M., Lanzavecchia, A., Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401 (1999), 708–712.
29. Sathaliyawala, T., Kubota, M., Yudanin, N., Turner, D., Camp, P., Thome, J.J., Bickham, K.L., Lerner, H., Goldstein, M., Sykes, M., et al. Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 38 (2013), 187–197.
30. Shekhar, K., Brodin, P., Davis, M.M., Chakraborty, A.K., Automatic Classification of Cellular Expression by Nonlinear Stochastic Embedding (ACCENSE). Proc. Natl. Acad. Sci. USA 111 (2014), 202–207.
31. Singh, S.P., Zhang, H.H., Foley, J.F., Hedrick, M.N., Farber, J.M., Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J. Immunol. 180 (2008), 214–221.
32. Skon, C.N., Lee, J.Y., Anderson, K.G., Masopust, D., Hogquist, K.A., Jameson, S.C., Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells. Nat. Immunol. 14 (2013), 1285–1293.
33. Tang, X.Z., Jo, J., Tan, A.T., Sandalova, E., Chia, A., Tan, K.C., Lee, K.H., Gehring, A.J., De Libero, G., Bertoletti, A., IL-7 licenses activation of human liver intrasinusoidal mucosal-associated invariant T cells. J. Immunol. 190 (2013), 3142–3152.
34. Thome, J.J., Farber, D.L., Emerging concepts in tissue-resident T cells: lessons from humans. Trends Immunol. 36 (2015), 428–435.
35. Thome, J.J., Yudanin, N., Ohmura, Y., Kubota, M., Grinshpun, B., Sathaliyawala, T., Kato, T., Lerner, H., Shen, Y., Farber, D.L., Spatial map of human T cell compartmentalization and maintenance over decades of life. Cell 159 (2014), 814–828.
36. Thome, J.J., Bickham, K.L., Ohmura, Y., Kubota, M., Matsuoka, N., Gordon, C., Granot, T., Griesemer, A., Lerner, H., Kato, T., Farber, D.L., Early-life compartmentalization of human T cell differentiation and regulatory function in mucosal and lymphoid tissues. Nat. Med. 22 (2016), 72–77.
37. Trifari, S., Kaplan, C.D., Tran, E.H., Crellin, N.K., Spits, H., Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(H)-17, T(H)1 and T(H)2 cells. Nat. Immunol. 10 (2009), 864–871.
38. van der Maaten, L., Hinton, G., Visualizing high-dimensional data using t-SNE. J. Mach. Learn. Res. 9 (2008), 2579–2605.
39. Viola, A., Luster, A.D., Chemokines and their receptors: drug targets in immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 48 (2008), 171–197.
40. Wang, J., Li, F., Wei, H., Lian, Z.X., Sun, R., Tian, Z., Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation. J. Exp. Med. 211 (2014), 2397–2410.
41. Westermann, J., Pabst, R., Distribution of lymphocyte subsets and natural killer cells in the human body. Clin. Investig. 70 (1992), 539–544.
42. Wong, M.T., Ye, J.J., Alonso, M.N., Landrigan, A., Cheung, R.K., Engleman, E., Utz, P.J., Regulation of human Th9 differentiation by type I interferons and IL-21. Immunol. Cell Biol. 88 (2010), 624–631.
43. Wong, M.T., Chen, J., Narayanan, S., Lin, W., Anicete, R., Kiaang, H.T., De Lafaille, M.A., Poidinger, M., Newell, E.W., Mapping the Diversity of Follicular Helper T Cells in Human Blood and Tonsils Using High-Dimensional Mass Cytometry Analysis. Cell Rep. 11 (2015), 1822–1833.
44. Yamane, H., Paul, W.E., Early signaling events that underlie fate decisions of naive CD4(+) T cells toward distinct T-helper cell subsets. Immunol. Rev. 252 (2013), 12–23.
45. Yen, H.R., Harris, T.J., Wada, S., Grosso, J.F., Getnet, D., Goldberg, M.V., Liang, K.L., Bruno, T.C., Pyle, K.J., Chan, S.L., et al. Tc17 CD8 T cells: functional plasticity and subset diversity. J. Immunol. 183 (2009), 7161–7168.
46. Zhu, J., Paul, W.E., Heterogeneity and plasticity of T helper cells. Cell Res. 20 (2010), 4–12.
47. Zúñiga, L.A., Jain, R., Haines, C., Cua, D.J., Th17 cell development: from the cradle to the grave. Immunol. Rev. 252 (2013), 78–88.