Pro-inflammatory human Th17 cells selectively express P-glycoprotein and are refractory to glucocorticoids

Journal of Experimental Medicine

Volumn 211, Issue 1, 2014, Pages 89-104

  Ramesh, Radha ^a   Kozhaya, Lina ^b   McKevitt, Kelly ^c   Djuretic, Ivana M ^a   Carlson, Thaddeus J ^a   Quintero, Maria A ^d   McCauley, Jacob L ^d   Abreu, Maria T ^d   Unutmaz, Derya ^b   Sundrud, Mark S ^a,c  

^a Tempero Pharmaceuticals Inc   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD161 ANTIGEN; CHEMOKINE RECEPTOR CCR10; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON; GLUCOCORTICOID; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 22; INTERLEUKIN 23; MULTIDRUG RESISTANCE PROTEIN 1; STEM CELL FACTOR; T LYMPHOCYTE RECEPTOR;

ADULT; ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VIVO STUDY; INFLAMMATION; MALE; MEMORY T LYMPHOCYTE; MIDDLE AGED; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH1 CELL; TH17 CELL; YOUNG ADULT;

CROHN DISEASE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HUMANS; INTERFERON-GAMMA; MICROARRAY ANALYSIS; P-GLYCOPROTEIN; TH17 CELLS;

EID: 84892536761     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130301     Document Type: Article

References (58)

1. Acosta-Rodriguez, E.V., L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, and G. Napolitani. 2007. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8:639-646. http://dx.doi.org/10 .1038/ni1467.
2. Afzali, B., P.J. Mitchell, F.C. Edozie, G.A. Povoleri, S.E. Dowson, L. Demandt, G. Walter, J.B. Canavan, C. Scotta, B. Menon, et al. 2013. CD161 expression characterizes a subpopulation of human regulatory T cells that produces IL-17 in a STAT3-dependent manner. Eur. J. Immunol. 43:2043-2054. http://dx.doi.org/10.1002/eji.201243296.
3. Ahern, P.P., C. Schiering, S. Buonocore, M.J. McGeachy, D.J. Cua, K.J. Maloy, and F. Powrie. 2010. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity. 33:279-288. http://dx .doi.org/10.1016/j.immuni.2010.08.010.
4. Alcorn, J.F., C.R. Crowe, and J.K. Kolls. 2010. TH17 cells in asthma and COPD. Annu. Rev. Physiol. 72:495-516. http://dx.doi.org/10.1146/annurev-physiol-021909-135926.
5. Aller, S.G., J. Yu, A. Ward, Y. Weng, S. Chittaboina, R. Zhuo, P.M. Harrell, Y.T. Trinh, Q. Zhang, I.L. Urbatsch, and G. Chang. 2009. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science. 323:1718-1722. http://dx.doi.org/10.1126/science.1168750.
6. Ano, S., Y. Morishima, Y. Ishii, K. Yoh, Y. Yageta, S. Ohtsuka, M. Matsuyama, M. Kawaguchi, S. Takahashi, and N. Hizawa. 2013. Transcription factors GATA-3 and RORγt are important for determining the phenotype of allergic airway inflammation in a murine model of asthma. J. Immunol. 190:1056-1065. http://dx.doi.org/10.4049/jimmunol.1202386.
7. Araki, K., A.H. Ellebedy, and R. Ahmed. 2011. TOR in the immune system. Curr. Opin. Cell Biol. 23:707-715. http://dx.doi.org/10.1016/j.ceb.2011.08.006.
8. Barnes, P.J., and I.M. Adcock. 2009. Glucocorticoid resistance in inflammatory diseases. Lancet. 373:1905-1917. http://dx.doi.org/10.1016/S0140-6736(09)60326-3.
9. + T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)-and Th2-inducing cytokines. J. Exp. Med. 195:603-616. http://dx.doi.org/10.1084/jem.20011629.
10. Chaudhary, P.M., and I.B. Roninson. 1991. Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells. Cell. 66:85-94. http://dx.doi.org/10.1016/0092-8674(91)90141-K.
11. Chen, Z., A. Laurence, Y. Kanno, M. Pacher-Zavisin, B.M. Zhu, C. Tato, A. Yoshimura, L. Hennighausen, and J.J. O'Shea. 2006. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc. Natl. Acad. Sci. USA. 103:8137-8142. http://dx.doi.org/10.1073/pnas.0600666103.
12. Codarri, L., G. Gyülvészi, V. Tosevski, L. Hesske, A. Fontana, L. Magnenat, T. Suter, and B. Becher. 2011. RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 12:560-567. http://dx.doi .org/10.1038/ni.2027.
13. Cohen, C.J., S.Q. Crome, K.G. MacDonald, E.L. Dai, D.L. Mager, and M.K. Levings. 2011. Human Th1 and Th17 cells exhibit epigenetic stability at signature cytokine and transcription factor loci. J. Immunol. 187:5615-5626. http://dx.doi.org/10.4049/jimmunol.1101058.
14. + T cell precursor. J. Exp. Med. 205:1903-1916. http://dx.doi.org/10.1084/jem.20080397.
15. Cosmi, L., L. Maggi, V. Santarlasci, M. Capone, E. Cardilicchia, F. Frosali, V. Querci, R. Angeli, A. Matucci, M. Fambrini, et al. 2010. Identification of a novel subset of human circulating memory CD4(+) T cells that produce both IL-17A and IL-4. J. Allergy Clin. Immunol. 125:222-230: e1-e4. http://dx.doi.org/10.1016/j.jaci.2009.10.012.
16. Cosmi, L., L. Maggi, V. Santarlasci, F. Liotta, and F. Annunziato. 2013. T helper cells plasticity in inflammation. Cytometry A.:n/a. http://dx.doi.org/10 .1002/cyto.a.22348.
17. Crowe, A., and A.M. Tan. 2012. Oral and inhaled corticosteroids: differences in P-glycoprotein (ABCB1) mediated efflux. Toxicol. Appl. Pharmacol. 260:294-302. http://dx.doi.org/10.1016/j.taap.2012.03.008.
18. Croxford, A.L., F. Mair, and B. Becher. 2012. IL-23: one cytokine in control of autoimmunity. Eur. J. Immunol. 42:2263-2273. http://dx.doi .org/10.1002/eji.201242598.
19. Duhen, T., R. Geiger, D. Jarrossay, A. Lanzavecchia, and F. Sallusto. 2009. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat. Immunol. 10:857-863. http://dx.doi .org/10.1038/ni.1767.
20. Esplugues, E., S. Huber, N. Gagliani, A.E. Hauser, T. Town, Y.Y. Wan, W. O'Connor Jr., A. Rongvaux, N. Van Rooijen, A.M. Haberman, et al. 2011. Control of TH17 cells occurs in the small intestine. Nature. 475:514-518. http://dx.doi.org/10.1038/nature10228.
21. Eyerich, S., K. Eyerich, D. Pennino, T. Carbone, F. Nasorri, S. Pallotta, F. Cianfarani, T. Odorisio, C. Traidl-Hoffmann, H. Behrendt, et al. 2009. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J. Clin. Invest. 119:3573-3585.
22. Flammer, J.R., and I. Rogatsky. 2011. Minireview: Glucocorticoids in autoimmunity: unexpected targets and mechanisms. Mol. Endocrinol. 25:1075-1086. http://dx.doi.org/10.1210/me.2011-0068.
23. Ghoreschi, K., A. Laurence, X.P. Yang, C.M. Tato, M.J. McGeachy, J.E. Konkel, H.L. Ramos, L. Wei, T.S. Davidson, N. Bouladoux, et al. 2010. Generation of pathogenic T(H)17 cells in the absence of TGF-β signalling. Nature. 467:967-971. http://dx.doi.org/10.1038/nature09447.
24. Gottesman, M.M., T. Fojo, and S.E. Bates. 2002. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer. 2:48-58. http://dx.doi.org/10.1038/nrc706.
25. Hirota, K., J.H. Duarte, M. Veldhoen, E. Hornsby, Y. Li, D.J. Cua, H. Ahlfors, C. Wilhelm, M. Tolaini, U. Menzel, et al. 2011. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12:255-263. http://dx.doi.org/10.1038/ni.1993.
26. Hueber, W., B.E. Sands, S. Lewitzky, M. Vandemeulebroecke, W. Reinisch, P.D. Higgins, J. Wehkamp, B.G. Feagan, M.D. Yao, M. Karczewski, et al., for the Secukinumab in Crohn's Disease Study Group. 2012. Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn's disease: unexpected results of a randomised, double-blind placebo-controlled trial. Gut. 61:1693-1700. http://dx.doi.org/10.1136/gutjnl-2011-301668.
27. Hyafil, F., C. Vergely, P. Du Vignaud, and T. Grand-Perret. 1993. In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res. 53:4595-4602.
28. Josefowicz, S.Z., L.F. Lu, and A.Y. Rudensky. 2012. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30:531-564. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141623.
29. Kebir, H., I. Ifergan, J.I. Alvarez, M. Bernard, J. Poirier, N. Arbour, P. Duquette, and A. Prat. 2009. Preferential recruitment of interferongamma-expressing TH17 cells in multiple sclerosis. Ann. Neurol. 66:390-402. http://dx.doi.org/10.1002/ana.21748.
30. Kleinschek, M.A., K. Boniface, S. Sadekova, J. Grein, E.E. Murphy, S.P. Turner, L. Raskin, B. Desai, W.A. Faubion, R. de Waal Malefyt, et al. 2009. Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J. Exp. Med. 206:525-534. http://dx.doi.org/10.1084/jem.20081712.
31. Kryczek, I., E. Zhao, Y. Liu, Y. Wang, L. Vatan, W. Szeliga, J. Moyer, A. Klimczak, A. Lange, and W. Zou. 2011. Human TH17 cells are longlived effector memory cells. Sci. Transl. Med. 3:104ra100.
32. Lee, Y., A. Awasthi, N. Yosef, F.J. Quintana, S. Xiao, A. Peters, C. Wu, M. Kleinewietfeld, S. Kunder, D.A. Hafler, et al. 2012. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 13:991-999. http://dx.doi.org/10.1038/ni.2416.
33. Ludescher, C., J. Thaler, D. Drach, J. Drach, M. Spitaler, C. Gattringer, H. Huber, and J. Hofmann. 1992. Detection of activity of P-glycoprotein in human tumour samples using rhodamine 123. Br. J. Haematol. 82:161-168. http://dx.doi.org/10.1111/j.1365-2141.1992.tb04608.x.
34. Maggi, L., V. Santarlasci, M. Capone, M.C. Rossi, V. Querci, A. Mazzoni, R. Cimaz, R. De Palma, F. Liotta, E. Maggi, et al. 2012. Distinctive features of classic and nonclassic (Th17 derived) human Th1 cells. Eur. J. Immunol. 42:3180-3188. http://dx.doi.org/10.1002/eji.201242648.
35. Manel, N., D. Unutmaz, and D.R. Littman. 2008. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat. Immunol. 9:641-649. http://dx.doi.org/10.1038/ni.1610.
36. McGeachy, M.J., K.S. Bak-Jensen, Y. Chen, C.M. Tato, W. Blumenschein, T. McClanahan, and D.J. Cua. 2007. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat. Immunol. 8:1390-1397. http://dx.doi.org/10.1038/ni1539.
37. McGeachy, M.J., Y. Chen, C.M. Tato, A. Laurence, B. Joyce-Shaikh, W.M. Blumenschein, T.K. McClanahan, J.J. O'Shea, and D.J. Cua. 2009. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 10:314-324. http://dx.doi.org/10.1038/ni.1698.
38. McKinley, L., J.F. Alcorn, A. Peterson, R.B. Dupont, S. Kapadia, A. Logar, A. Henry, C.G. Irvin, J.D. Piganelli, A. Ray, and J.K. Kolls. 2008. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 181:4089-4097.
39. Miossec, P., T. Korn, and V.K. Kuchroo. 2009. Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 361:888-898. http://dx.doi.org/10 .1056/NEJMra0707449.
40. Muranski, P., Z.A. Borman, S.P. Kerkar, C.A. Klebanoff, Y. Ji, L. Sanchez-Perez, M. Sukumar, R.N. Reger, Z. Yu, S.J. Kern, et al. 2011. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity. 35:972-985. http://dx.doi.org/10.1016/j.immuni.2011.09.019.
41. Mutalithas, K., C. Guillen, C. Day, C.E. Brightling, I.D. Pavord, and A.J. Wardlaw. 2010. CRTH2 expression on T cells in asthma. Clin. Exp. Immunol. 161:34-40.
42. Nistala, K., S. Adams, H. Cambrook, S. Ursu, B. Olivito, W. de Jager, J.G. Evans, R. Cimaz, M. Bajaj-Elliott, and L.R. Wedderburn. 2010. Th17 plasticity in human autoimmune arthritis is driven by the inflammatory environment. Proc. Natl. Acad. Sci. USA. 107:14751-14756. http://dx.doi .org/10.1073/pnas.1003852107.
43. + central memory T cells. J. Exp. Med. 200:725-735. http://dx.doi .org/10.1084/jem.20040774.
44. Roberts, M.M., B.W. Swart, P.J. Simmons, R.L. Basser, C.G. Begley, and L.B. To. 1999. Prolonged release and c-kit expression of haemopoietic precursor cells mobilized by stem cell factor and granulocyte colony stimulating factor. Br. J. Haematol. 104:778-784. http://dx.doi.org/10.1046/j.1365-2141.1999.01231.x.
45. Sallusto, F., D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 401:708-712. http://dx.doi.org/10.1038/44385.
46. Sallusto, F., C.E. Zielinski, and A. Lanzavecchia. 2012. Human Th17 subsets. Eur. J. Immunol. 42:2215-2220. http://dx.doi.org/10.1002/eji.201242741
47. Schinkel, A.H. 1997. The physiological function of drug-transporting P-glycoproteins. Semin. Cancer Biol. 8:161-170. http://dx.doi.org/10.1006/scbi.1997.0068.
48. Simmons, P.J., D.I. Leavesley, J.P. Levesque, B.W. Swart, D.N. Haylock, L.B. To, L.K. Ashman, and C.A. Juttner. 1994. The mobilization of primitive hemopoietic progenitors into the peripheral blood. Stem Cells. 12:187-201, discussion :201-202.
49. Sincock, P.M., and L.K. Ashman. 1997. Expression of c-Kit and functional drug efflux are correlated in de novo acute myeloid leukaemia. Leukemia. 11:1850-1857. http://dx.doi.org/10.1038/sj.leu.2400823.
50. So, T., S.W. Lee, and M. Croft. 2008. Immune regulation and control of regulatory T cells by OX40 and 4-1BB. Cytokine Growth Factor Rev. 19:253-262. http://dx.doi.org/10.1016/j.cytogfr.2008.04.003.
51. Strouse, J.J., I. Ivnitski-Steele, A. Waller, S.M. Young, D. Perez, A.M. Evangelisti, O. Ursu, C.G. Bologa, M.B. Carter, V.M. Salas, et al. 2013. Fluorescent substrates for flow cytometric evaluation of efflux inhibition in ABCB1, ABCC1, and ABCG2 transporters. Anal. Biochem. 437:77-87. http://dx.doi.org/10.1016/j.ab.2013.02.018.
52. Sundrud, M.S., S.M. Grill, D. Ni, K. Nagata, S.S. Alkan, A. Subramaniam, and D. Unutmaz. 2003. Genetic reprogramming of primary human T cells reveals functional plasticity in Th cell differentiation. J. Immunol. 171:3542-3549.
53. Sundrud, M.S., S.B. Koralov, M. Feuerer, D.P. Calado, A.E. Kozhaya, A. Rhule-Smith, R.E. Lefebvre, D. Unutmaz, R. Mazitschek, H. Waldner, et al. 2009. Halofuginone inhibits TH17 cell differentiation by activating the amino acid starvation response. Science. 324:1334-1338. http://dx.doi .org/10.1126/science.1172638.
54. Trifari, S., C.D. Kaplan, E.H. Tran, N.K. Crellin, and H. Spits. 2009. 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. 10:864-871. http://dx.doi.org/10.1038/ni.1770.
55. Turtle, C.J., H.M. Swanson, N. Fujii, E.H. Estey, and S.R. Riddell. 2009. A distinct subset of self-renewing human memory CD8+ T cells survives cytotoxic chemotherapy. Immunity. 31:834-844. http://dx.doi.org/10 .1016/j.immuni.2009.09.015.
56. + human memory T cells. J. Exp. Med. 208:1875-1887. http://dx.doi.org/10 .1084/jem.20102516.
57. Weiss, J., and W.E. Haefeli. 2010. Impact of ATP-binding cassette transporters on human immunodeficiency virus therapy. Int Rev Cell Mol Biol. 280:219-279. http://dx.doi.org/10.1016/S1937-6448(10)80005-X.
58. Zorzi, F., I. Monteleone, M. Sarra, E. Calabrese, I. Marafini, M. Cretella, S. Sedda, L. Biancone, F. Pallone, and G. Monteleone. 2013. Distinct profiles of effector cytokines mark the different phases of Crohn's disease. PLoS ONE. 8:e54562. http://dx.doi.org/10.1371/journal.pone .0054562.