IL-17+ CD8+ T cells: Differentiation, phenotype and role in inflammatory disease

Immunology Letters

Volumn 178, Issue , 2016, Pages 20-26

  Srenathan, Ushani ^a   Steel, Kathryn ^a   Taams, Leonie S ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

CD8+; Disease; IL 17; Inflammation; Tc17

Indexed keywords

CD8 ANTIGEN; CYTOKINE; INTERLEUKIN 17; AUTACOID; BIOLOGICAL MARKER;

ARTICLE; CELL PLASTICITY; CYTOKINE PRODUCTION; CYTOTOXICITY; HUMAN; INFLAMMATORY DISEASE; INTERLEUKIN 17+ CD8+ T LYMPHOCYTE; LYMPHOCYTE CULTURE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; NONHUMAN; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; BIOMARKERS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MICE; PHENOTYPE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 84971596825     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2016.05.001     Document Type: Article

References (54)

1. [1] Rouvier, E., Luciani, M.F., Mattei, M.G., Denizot, F., Golstein, P., CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. J. Immunol. 150 (1993), 5445–5456.
2. [2] Teunissen, M.B.M., Bos, J.D., Koomen, C.W., de Waal Malefyt, R., Wierenga, E.A., Interleukin-17 and interferon-gamma synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J. Invest. Dermatol. 111 (1998), 645–649.
3. [3] Kryczek, I., Bruce, A.T., Gudjonsson, J.E., Johnston, A., Aphale, A., Vatan, L., et al. Induction of IL-17+ T cell trafficking and development by IFN-gamma: mechanism and pathological relevance in psoriasis. J. Immunol. 181 (2008), 4733–4741.
4. [4] Hijnen, D., Knol, E.F., Gent, Y.Y., Giovannone, B., Beijn, S.J., Kupper, T.S., Bruijnzeel-Koomen, C.A., Clark, R.A., CD8+ T cells in the lesional skin of atopic dermatitis and psoriasis patients are an important source of IFN-gamma, IL-13, IL-17, and IL-22. J. Invest. Dermatol. 133 (2013), 973–979.
5. [5] Ortega, C., Fernandez, A.S., Carrillo, J.M., Romero, P., Molina, I.J., Moreno, J.C., et al. IL-17-producing CD8+ T lymphocytes from psoriasis skin plaques are cytotoxic effector cells that secrete Th17-related cytokines. J. Leukoc. Biol. 86 (2009), 435–443.
6. [6] Res, P.C.M., Piskin, G., de Boer, O.J., van der Loos, C.M., Teeling, P., Bos, J.D., et al. Overrepresentation of IL-17A and IL-22 producing CD8 T cells in lesional skin suggests their involvement in the pathogenesis of psoriasis. PLoS One, 5, 2010, e14108.
7. [7] Menon, B., Gullick, N.J., Walter, G.J., Rajasekhar, M., Garrood, T., Evans, H.G., et al. IL-17+ CD8+ T-cells are enriched in the joints of patients with psoriatic arthritis and correlate with disease activity and joint damage progression. Arthritis Rheum. 66 (2014), 1272–1281.
8. [8] Tzartos, J.S., Friese, M.A., Craner, M.J., Palace, J., Newcombe, J., Esiri, M.M., et al. Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis. Am. J. Pathol. 172 (2008), 146–155.
9. [9] Marwaha, A.K., Crome, S.Q., Panagiotopoulos, C., Berg, K.B., Qin, H., Ouyang, Q., et al. Cutting edge: increased IL-17-secreting T cells in children with new-onset type 1 diabetes. J. Immunol. 185 (2010), 3814–3818.
10. [10] Billerbeck, E., Kang, Y.-H., Walker, L., Lockstone, H., Grafmueller, S., Fleming, V., et al. Analysis of CD161 expression on human CD8+ T cells defines a distinct functional subset with tissue-homing properties. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 3006–3011.
11. [11] Li, X., Zhou, Q., Yang, W.B., Xiong, X.Z., Du, R.H., Zhang, J.C., Pleural mesothelial cells promote expansion of IL-17-producing CD8+ T cells in tuberculous pleural effusion. J. Clin. Immunol. 33 (2013), 775–787.
12. [12] Chang, Y., Nadigel, J., Boulais, N., Bourbeau, J., Maltais, F., Eidelman, D.H., et al. CD8 positive T cells express IL-17 in patients with chronic obstructive pulmonary disease. Respir. Res. 12 (2011), 1–10.
13. [13] Acosta-Rodriguez, E.V., Napolitani, G., Lanzavecchia, A., Sallusto, F., Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8 (2007), 942–949.
14. [14] Chen, Z., Tato, C.M., Muul, L., Laurence, A., O'Shea, J.J., Distinct regulation of interleukin-17 in human T helper lymphocytes. Arthritis Rheum. 56 (2007), 2936–2946.
15. [15] Wilson, N.J., Boniface, K., Chan, J.R., McKenzie, B.S., Blumenschein, W.M., Mattson, J.D., et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8 (2007), 950–957.
16. [16] Manel, N., Unutmaz, D., Littman, D.R., The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat. Immunol. 9 (2008), 641–649.
17. [17] Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T.B., Oukka, M., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006), 235–238.
18. [18] Mangan, P.R., Harrington, L.E., O'Quinn, D.B., Helms, W.S., Bullard, D.C., Elson, C.O., et al. Transforming growth factor-[beta] induces development of the TH17 lineage. Nature 441 (2006), 231–234.
19. [19] Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M., Stockinger, B., TGF-beta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-Producing T cells. Immunity 24 (2006), 179–189.
20. [20] Korn, T., Bettelli, E., Gao, W., Awasthi, A., Jager, A., Strom, T.B., et al. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 448 (2007), 484–487.
21. [21] Kondo, T., Takata, H., Matsuki, F., Takiguchi, M., Cutting edge: phenotypic characterization and differentiation of human CD8+ T cells producing IL-17. J. Immunol. 182 (2009), 1794–1798.
22. [22] Gras, R., Garcia, M.I., Gomez, R., de la Mata, F.J., Munoz-Fernandez, M.A., Lopez-Fernandez, L.A., Carbosilane dendrimer 2G-NN16 represses Tc17 differentiation in primary T CD8+ lymphocytes. Mol. Pharm. 9 (2012), 102–110.
23. [23] Hamada, H., Garcia-Hernandez Mde, L., Reome, J.B., Misra, S.K., Strutt, T.M., McKinstry, K.K., et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J. Immunol. 182 (2009), 3469–3481.
24. [24] Huber, M., Heink, S., Grothe, H., Guralnik, A., Reinhard, K., Elflein, K., et al. A Th17-like developmental process leads to CD8(+) Tc17 cells with reduced cytotoxic activity. Eur. J. Immunol. 39 (2009), 1716–1725.
25. [25] Liu, S.J., Tsai, J.P., Shen, C.R., Sher, Y.P., Hsieh, C.L., Yeh, Y.C., et al. Induction of a distinct CD8 Tnc17 subset by transforming growth factor-beta and interleukin-6. J. Leukoc. Biol. 82 (2007), 354–360.
26. [26] Yen, H.R., Harris, T.J., Wada, S., Grosso, J.F., Getnet, D., Goldberg, M.V., et al. Tc17CD8 T cells: functional plasticity and subset diversity. J. Immunol. 183 (2009), 7161–7168.
27. [27] Curtis, M.M., Way, S.S., Wilson, C.B., IL-23 promotes the production of IL-17 by antigen-specific CD8 T cells in the absence of IL-12 and type-I interferons. J. Immunol. 183 (2009), 381–387.
28. [28] Yeh, N., Glosson, N.L., Wang, N., Guindon, L., McKinley, C., Hamada, H., et al. Tc17 cells are capable of mediating immunity to vaccinia virus by acquisition of a cytotoxic phenotype. J. Immunol. 185 (2010), 2089–2098.
29. [29] Huber, M., Heink, S., Pagenstecher, A., Reinhard, K., Ritter, J., Visekruna, A., et al. IL-17A secretion by CD8+ T cells supports Th17-mediated autoimmune encephalomyelitis. J. Clin. Invest. 123 (2013), 247–260.
30. [30] Gartlan, K.H., Markey, K.A., Varelias, A., Bunting, M.D., Koyama, M., Kuns, R.D., et al. Tc17 cells are a proinflammatory, plastic lineage of pathogenic CD8+ T cells that induce GVHD without antileukemic effects. Blood 126 (2015), 1609–1620.
31. [31] Dwivedi, V.P., Tousif, S., Bhattacharya, D., Prasad, D.V.R., Van Kaer, L., Das, J., et al. Transforming growth factor-β protein inversely regulates in vivo differentiation of interleukin-17 (IL-17)-producing CD4(+) and CD8(+) T Cells. J. Biol. Chem. 287 (2012), 2943–2947.
32. [32] Ciric, B., El-behi, M., Cabrera, R., Zhang, G.X., Rostami, A., IL-23 drives pathogenic IL-17-producing CD8+ t cells. J. Immunol. 182 (2009), 5296–5305.
33. [33] Nurieva, R., Yang, X.O., Martinez, G., Zhang, Y., Panopoulos, A.D., Ma, L., et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448 (2007), 480–483.
34. [34] 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.
35. [35] Stritesky, G.L., Yeh, N., Kaplan, M.H., IL-23 promotes maintenance but not commitment to the Th17 lineage. J. Immunol. 181 (2008), 5948–5955.
36. [36] Sarin, R., Wu, X., Abraham, C., Inflammatory disease protective R381Q IL23 receptor polymorphism results in decreased primary CD4+ and CD8+ human T-cell functional responses. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 9560–9565.
37. [37] Chu, C.Q., Swart, D., Alcorn, D., Tocker, J., Elkon, K.B., Interferon-gamma regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17. Arthritis Rheum. 56 (2007), 1145–1151.
38. [38] Intlekofer, A.M., Banerjee, A., Takemoto, N., Gordon, S.M., Dejong, C.S., Shin, H., et al. Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 321 (2008), 408–411.
39. [39] Ysebrant de Lendonck, L., Tonon, S., Nguyen, M., Vandevenne, P., Welsby, I., Martinet, V., et al. Interferon regulatory factor 3 controls interleukin-17 expression in CD8 T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), E3189–E3197.
40. [40] Maggi, L., Santarlasci, V., Capone, M., Peired, A., Frosali, F., Crome, S.Q., et al. CD161 is a marker of all human IL-17-producing T-cell subsets and is induced by RORC. Eur. J. Immunol. 40 (2010), 2174–2181.
41. [41] Singh, S.P., Zhang, H.H., Foley, J.F., Hedrick, M.N., Human, Farber J.M., T cells that are able to produce IL-17 express the chemokine receptor CCR6. J. Immunol. 180 (2008), 214–221.
42. [42] Miossec, P., Korn, T., Kuchroo, V.K., Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 361 (2009), 888–898.
43. [43] Chiricozzi, A., Guttman-Yassky, E., Suarez-Farinas, M., Nograles, K.E., Tian, S., Cardinale, I., et al. Integrative responses to IL-17 and TNF-alpha in human keratinocytes account for key inflammatory pathogenic circuits in psoriasis. J. Invest. Dermatol. 131 (2011), 677–687.
44. [44] Goldberg, M., Nadiv, O., Luknar-Gabor, N., Agar, G., Beer, Y., Katz, Y., Synergism between tumor necrosis factor alpha and interleukin-17 to induce IL-23 p19 expression in fibroblast-like synoviocytes. Mol. Immunol. 46 (2009), 1854–1859.
45. [45] Boniface, K., Blumenschein, W.M., Brovont-Porth, K., McGeachy, M.J., Basham, B., Desai, B., et al. Human Th17 cells comprise heterogeneous subsets including IFN-gamma-producing cells with distinct properties from the Th1 lineage. J. Immunol. 185 (2010), 679–687.
46. [46] Nograles, K.E., Zaba, L.C., Guttman-Yassky, E., Fuentes-Duculan, J., Suarez-Farinas, M., Cardinale, I., et al. Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br. J. Dermatol. 159 (2008), 1092–1102.
47. [47] Codarri, L., Gyulveszi, G., Tosevski, V., Hesske, L., Fontana, A., Magnenat, L., et al. RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12 (2011), 560–567.
48. [48] Hirota, K., Duarte, J.H., Veldhoen, M., Hornsby, E., Li, Y., Cua, D.J., et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12 (2011), 255–263.
49. [49] Hinrichs, C.S., Kaiser, A., Paulos, C.M., Cassard, L., Sanchez-Perez, L., Heemskerk, B., et al. Type 17CD8+ T cells display enhanced antitumor immunity. Blood 114 (2009), 596–599.
50. [50] Tajima, M., Wakita, D., Satoh, T., Kitamura, H., Nishimura, T., IL-17/IFN-gamma double producing CD8+ T (Tc17/IFN-gamma) cells: a novel cytotoxic T-cell subset converted from Tc17 cells by IL-12. Int. Immunol. 23 (2011), 751–759.
51. [51] Satoh, T., Tajima, M., Wakita, D., Kitamura, H., Nishimura, T., The development of IL-17/IFN-gamma-double producing CTLs from Tc17 cells is driven by epigenetic suppression of Socs3 gene promoter. Eur. J. Immunol. 42 (2012), 2329–2342.
52. [52] Cortes, A., Hadler, J., Pointon, J.P., Robinson, P.C., Karaderi, T., Leo, P., et al. Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci. Nat. Genet. 45 (2013), 730–738.
53. [53] Jostins, L., Ripke, S., Weersma, R.K., Duerr, R.H., McGovern, D.P., Hui, K.Y., et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491 (2012), 119–124.
54. [54] Tsoi, L.C., Spain, S.L., Knight, J., Ellinghaus, E., Stuart, P.E., Capon, F., et al. Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat. Genet. 44 (2012), 1341–1348.