Advances in understanding the pathogenesis of autoimmune disorders: Focus on chemokines and lymphocyte trafficking

British Journal of Haematology

Volumn 164, Issue 3, 2014, Pages 329-341

  Comerford, Iain ^a   Kara, Ervin E ^a   Mckenzie, Duncan R ^a   Mccoll, Shaun R ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Autoimmunity; Cell migration; Chemokines; Lymphocytes; T cells

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR10; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR3; CUTANEOUS T CELL ATTRACTING CHEMOKINE; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; FRACTALKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 22; INTERLEUKIN 23; MACROPHAGE DERIVED CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 2; RANTES; TUMOR NECROSIS FACTOR ALPHA;

AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; HUMAN; IMMUNOPATHOGENESIS; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; LYMPHOCYTIC INFILTRATION; MULTIPLE SCLEROSIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PSORIASIS; RECEPTOR BLOCKING; REVIEW; RHEUMATOID ARTHRITIS; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL;

AUTOIMMUNITY; CELL MIGRATION; CHEMOKINES; LYMPHOCYTES; T CELLS;

ANIMALS; AUTOIMMUNE DISEASES; CELL MOVEMENT; CHEMOKINES; HUMANS; INFLAMMATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTES;

EID: 84892480314     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12616     Document Type: Review

References (103)

1. Acosta-Rodriguez, E.V., Rivino, L., Geginat, J., Jarrossay, D., Gattorno, M., Lanzavecchia, A., Sallusto, F. & Napolitani, G. (2007) Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nature Immunology, 8, 639-646.
2. Ambrosini, E., Columba-Cabezas, S., Serafini, B., Muscella, A. & Aloisi, F. (2003) Astrocytes are the major intracerebral source of macrophage inflammatory protein-3alpha/CCL20 in relapsing experimental autoimmune encephalomyelitis and in vitro. Glia, 41, 290-300.
3. Ambrosini, E., Remoli, M.E., Giacomini, E., Rosicarelli, B., Serafini, B., Lande, R., Aloisi, F. & Coccia, E.M. (2005) Astrocytes produce dendritic cell-attracting chemokines in vitro and in multiple sclerosis lesions. Journal of Neuropathology and Experimental Neurology, 64, 706-715.
4. Arima, Y., Harada, M., Kamimura, D., Park, J.H., Kawano, F., Yull, F.E., Kawamoto, T., Iwakura, Y., Betz, U.A., Marquez, G., Blackwell, T.S., Ohira, Y., Hirano, T. & Murakami, M. (2012) Regional neural activation defines a gateway for autoreactive T cells to cross the blood-brain barrier. Cell, 148, 447-457.
5. Balashov, K.E., Rottman, J.B., Weiner, H.L. & Hancock, W.W. (1999) CCR5 (+) and CXCR3 (+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proceedings of the National Academy of Science of the USA, 96, 6873-6878.
6. Bonecchi, R., Bianchi, G., Bordignon, P.P., D'Ambrosio, D., Lang, R., Borsatti, A., Sozzani, S., Allavena, P., Gray, P.A., Mantovani, A. & Sinigaglia, F. (1998) Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. Journal of Experimental Medicine, 187, 129-134.
7. Boniface, K., Guignouard, E., Pedretti, N., Garcia, M., Delwail, A., Bernard, F.X., Nau, F., Guillet, G., Dagregorio, G., Yssel, H., Lecron, J.C. & Morel, F. (2007) A role for T cell-derived interleukin 22 in psoriatic skin inflammation. Clinical and Experimental Immunology, 150, 407-415.
8. Carvalho-Pinto, C., Garcia, M.I., Gomez, L., Ballesteros, A., Zaballos, A., Flores, J.M., Mellado, M., Rodriguez-Frade, J.M., Balomenos, D. & Martinez, A.C. (2004) Leukocyte attraction through the CCR5 receptor controls progress from insulitis to diabetes in non-obese diabetic mice. European Journal of Immunology, 34, 548-557.
9. Chan, J.R., Blumenschein, W., Murphy, E., Diveu, C., Wiekowski, M., Abbondanzo, S., Lucian, L., Geissler, R., Brodie, S., Kimball, A.B., Gorman, D.M., Smith, K., de Waal Malefyt, R., Kastelein, R.A., McClanahan, T.K. & Bowman, E.P. (2006) IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. Journal of Experimental Medicine, 203, 2577-2587.
10. Christen, U., McGavern, D.B., Luster, A.D., von Herrath, M.G. & Oldstone, M.B. (2003) Among CXCR3 chemokines, IFN-gamma-inducible protein of 10 kDa (CXC chemokine ligand (CXCL) 10) but not monokine induced by IFN-gamma (CXCL9) imprints a pattern for the subsequent development of autoimmune disease. Journal of Immunology, 171, 6838-6845.
11. Christen, S., Holdener, M., Beerli, C., Thoma, G., Bayer, M., Pfeilschifter, J.M., Hintermann, E., Zerwes, H.G. & Christen, U. (2011) Small molecule CXCR3 antagonist NIBR2130 has only a limited impact on type 1 diabetes in a virus-induced mouse model. Clinical and Experimental Immunology, 165, 318-328.
12. Coppieters, K.T., Amirian, N., Pagni, P.P., Baca Jones, C., Wiberg, A., Lasch, S., Hintermann, E., Christen, U. & von Herrath, M.G. (2013) Functional redundancy of CXCR3/CXCL10 signaling in the recruitment of diabetogenic cytotoxic T lymphocytes to pancreatic islets in a virally induced autoimmune diabetes model. Diabetes, 62, 2492-2499.
13. Dardalhon, V., Awasthi, A., Kwon, H., Galileos, G., Gao, W., Sobel, R.A., Mitsdoerffer, M., Strom, T.B., Elyaman, W., Ho, I.C., Khoury, S., Oukka, M. & Kuchroo, V.K. (2008) IL-4 inhibits TGF-beta-induced Foxp3 + T cells and, together with TGF-beta, generates IL-9 + IL-10 + Foxp3 (-) effector T cells. Nature Immunology, 9, 1347-1355.
14. Duhen, T., Geiger, R., Jarrossay, D., Lanzavecchia, A. & Sallusto, F. (2009) Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nature Immunology, 10, 857-863.
15. Ehrlich, P. (1900) On immunity with special reference to cell life. Proceedings of the Royal Society of London, 66, 424-448.
16. El-Behi, M., Ciric, B., Dai, H., Yan, Y., Cullimore, M., Safavi, F., Zhang, G.X., Dittel, B.N. & Rostami, A. (2011) The encephalitogenicity of T (H) 17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nature Immunology, 12, 568-575.
17. Elhofy, A., Depaolo, R.W., Lira, S.A., Lukacs, N.W. & Karpus, W.J. (2009) Mice deficient for CCR6 fail to control chronic experimental autoimmune encephalomyelitis. Journal of Neuroimmunology, 213, 91-99.
18. Esplugues, E., Huber, S., Gagliani, N., Hauser, A.E., Town, T., Wan, Y.Y., O'Connor, W. Jr, Rongvaux, A., Van Rooijen, N., Haberman, A.M., Iwakura, Y., Kuchroo, V.K., Kolls, J.K., Bluestone, J.A., Herold, K.C. & Flavell, R.A. (2011) Control of TH17 cells occurs in the small intestine. Nature, 475, 514-518.
19. Eyerich, S., Eyerich, K., Pennino, D., Carbone, T., Nasorri, F., Pallotta, S., Cianfarani, F., Odorisio, T., Traidl-Hoffmann, C., Behrendt, H., Durham, S.R., Schmidt-Weber, C.B. & Cavani, A. (2009) Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. The Journal of Clinical Investigation, 119, 3573-3585.
20. Fife, B.T., Paniagua, M.C., Lukacs, N.W., Kunkel, S.L. & Karpus, W.J. (2001a) Selective CC chemokine receptor expression by central nervous system-infiltrating encephalitogenic T cells during experimental autoimmune encephalomyelitis. Journal of Neuroscience Research, 66, 705-714.
21. Fife, B.T., Kennedy, K.J., Paniagua, M.C., Lukacs, N.W., Kunkel, S.L., Luster, A.D. & Karpus, W.J. (2001b) CXCL10 (IFN-gamma-inducible protein-10) control of encephalitogenic CD4 + T cell accumulation in the central nervous system during experimental autoimmune encephalomyelitis. Journal of Immunology, 166, 7617-7624.
22. van der Fits, L., Mourits, S., Voerman, J.S., Kant, M., Boon, L., Laman, J.D., Cornelissen, F., Mus, A.M., Florencia, E., Prens, E.P. & Lubberts, E. (2009) Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. Journal of Immunology, 182, 5836-5845.
23. Forde, E.A., Dogan, R.N. & Karpus, W.J. (2011) CCR4 contributes to the pathogenesis of experimental autoimmune encephalomyelitis by regulating inflammatory macrophage function. Journal of Neuroimmunology, 236, 17-26.
24. Frigerio, S., Junt, T., Lu, B., Gerard, C., Zumsteg, U., Hollander, G.A. & Piali, L. (2002) Beta cells are responsible for CXCR3-mediated T-cell infiltration in insulitis. Nature Medicine, 8, 1414-1420.
25. Gao, P., Zhou, X.Y., Yashiro-Ohtani, Y., Yang, Y.F., Sugimoto, N., Ono, S., Nakanishi, T., Obika, S., Imanishi, T., Egawa, T., Nagasawa, T., Fujiwara, H. & Hamaoka, T. (2003) The unique target specificity of a nonpeptide chemokine receptor antagonist: selective blockade of two Th1 chemokine receptors CCR5 and CXCR3. Journal of Leukocyte Biology, 73, 273-280.
26. Garcia-Lopez, M.A., Sanchez-Madrid, F., Rodriguez-Frade, J.M., Mellado, M., Acevedo, A., Garcia, M.I., Albar, J.P., Martinez, C. & Marazuela, M. (2001) CXCR3 chemokine receptor distribution in normal and inflamed tissues: expression on activated lymphocytes, endothelial cells, and dendritic cells. Laboratory Investigation, 81, 409-418.
27. Gerlag, D.M., Hollis, S., Layton, M., Vencovsky, J., Szekanecz, Z., Braddock, M. & Tak, P.P. (2010) Preclinical and clinical investigation of a CCR5 antagonist, AZD5672, in patients with rheumatoid arthritis receiving methotrexate. Arthritis and Rheumatism, 62, 3154-3160.
28. 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., Grainger, J.R., Chen, Q., Kanno, Y., Watford, W.T., Sun, H.W., Eberl, G., Shevach, E.M., Belkaid, Y., Cua, D.J., Chen, W. & O'Shea, J.J. (2010) Generation of pathogenic T (H) 17 cells in the absence of TGF-beta signalling. Nature, 467, 967-971.
29. Gray, E.E., Suzuki, K. & Cyster, J.G. (2011) Cutting edge: identification of a motile IL-17-producing gammadelta T cell population in the dermis. Journal of Immunology, 186, 6091-6095.
30. Gunther, C., Carballido-Perrig, N., Kaesler, S., Carballido, J.M. & Biedermann, T. (2012) CXCL16 and CXCR6 are upregulated in psoriasis and mediate cutaneous recruitment of human CD8 + T cells. The Journal of Investigative Dermatology, 132, 626-634.
31. Gyulveszi, G., Haak, S. & Becher, B. (2009) IL-23-driven encephalo-tropism and Th17 polarization during CNS-inflammation in vivo. European Journal of Immunology, 39, 1864-1869.
32. Harper, E.G., Guo, C., Rizzo, H., Lillis, J.V., Kurtz, S.E., Skorcheva, I., Purdy, D., Fitch, E., Iordanov, M. & Blauvelt, A. (2009) Th17 cytokines stimulate CCL20 expression in keratinocytes in vitro and in vivo: implications for psoriasis pathogenesis. The Journal of Investigative Dermatology, 129, 2175-2183.
33. Hedrick, M.N., Lonsdorf, A.S., Shirakawa, A.K., Richard Lee, C.C., Liao, F., Singh, S.P., Zhang, H.H., Grinberg, A., Love, P.E., Hwang, S.T. & Farber, J.M. (2009) CCR6 is required for IL-23-induced psoriasis-like inflammation in mice. The Journal of Clinical Investigation, 119, 2317-2329.
34. Hedrick, M.N., Lonsdorf, A.S., Hwang, S.T. & Farber, J.M. (2010) CCR6 as a possible therapeutic target in psoriasis. Expert Opinion on Therapeutic Targets, 14, 911-922.
35. Hinks, A., Martin, P., Flynn, E., Eyre, S., Packham, J., Barton, A., Worthington, J. & Thomson, W. (2010) Association of the CCR5 gene with juvenile idiopathic arthritis. Genes and Immunity, 11, 584-589.
36. Hirota, K., Yoshitomi, H., Hashimoto, M., Maeda, S., Teradaira, S., Sugimoto, N., Yamaguchi, T., Nomura, T., Ito, H., Nakamura, T., Sakaguchi, N. & Sakaguchi, S. (2007) Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. Journal of Experimental Medicine, 204, 2803-2812.
37. Homey, B., Dieu-Nosjean, M.C., Wiesenborn, A., Massacrier, C., Pin, J.J., Oldham, E., Catron, D., Buchanan, M.E., Muller, A., de Waal Malefyt, R., Deng, G., Orozco, R., Ruzicka, T., Lehmann, P., Lebecque, S., Caux, C. & Zlotnik, A. (2000) Up-regulation of macrophage inflammatory protein-3 alpha/CCL20 and CC chemokine receptor 6 in psoriasis. Journal of Immunology, 164, 6621-6632.
38. Homey, B., Alenius, H., Muller, A., Soto, H., Bowman, E.P., Yuan, W., McEvoy, L., Lauerma, A.I., Assmann, T., Bunemann, E., Lehto, M., Wolff, H., Yen, D., Marxhausen, H., To, W., Sedgwick, J., Ruzicka, T., Lehmann, P. & Zlotnik, A. (2002) CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nature Medicine, 8, 157-165.
39. Horuk, R. (2009) Chemokine receptor antagonists: overcoming developmental hurdles. Nature Reviews. Drug Discovery, 8, 23-33.
40. Jager, A., Dardalhon, V., Sobel, R.A., Bettelli, E. & Kuchroo, V.K. (2009) Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. Journal of Immunology, 183, 7169-7177.
41. Kara, E.E., Comerford, I., Bastow, C.R., Fenix, K.A., Litchfield, W., Handel, T.M. & McColl, S.R. (2013) Distinct chemokine receptor axes regulate Th9 cell trafficking to allergic and autoimmune inflammatory sites. Journal of Immunology, 191, 1110-1117.
42. Karpus, W.J., Lukacs, N.W., McRae, B.L., Strieter, R.M., Kunkel, S.L. & Miller, S.D. (1995) An important role for the chemokine macrophage inflammatory protein-1 alpha in the pathogenesis of the T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis. Journal of Immunology, 155, 5003-5010.
43. Kennedy, K.J., Strieter, R.M., Kunkel, S.L., Lukacs, N.W. & Karpus, W.J. (1998) Acute and relapsing experimental autoimmune encephalomyelitis are regulated by differential expression of the CC chemokines macrophage inflammatory protein-1alpha and monocyte chemotactic protein-1. Journal of Neuroimmunology, 92, 98-108.
44. Klein, R.S., Izikson, L., Means, T., Gibson, H.D., Lin, E., Sobel, R.A., Weiner, H.L. & Luster, A.D. (2004) IFN-inducible protein 10/CXC chemokine ligand 10-independent induction of experimental autoimmune encephalomyelitis. Journal of Immunology, 172, 550-559.
45. Kochi, Y., Okada, Y., Suzuki, A., Ikari, K., Terao, C., Takahashi, A., Yamazaki, K., Hosono, N., Myouzen, K., Tsunoda, T., Kamatani, N., Furuichi, T., Ikegawa, S., Ohmura, K., Mimori, T., Matsuda, F., Iwamoto, T., Momohara, S., Yamanaka, H., Yamada, R., Kubo, M., Nakamura, Y. & Yamamoto, K. (2010) A regulatory variant in CCR6 is associated with rheumatoid arthritis susceptibility. Nature Genetics, 42, 515-519.
46. Kohler, R.E., Comerford, I., Townley, S., Haylock-Jacobs, S., Clark-Lewis, I. & McColl, S.R. (2008) Antagonism of the chemokine receptors CXCR3 and CXCR4 reduces the pathology of experimental autoimmune encephalomyelitis. Brain Pathology, 18, 504-516.
47. van Kuijk, A.W., Vergunst, C.E., Gerlag, D.M., Bresnihan, B., Gomez-Reino, J.J., Rouzier, R., Verschueren, P.C., van der Leij, C., Maas, M., Kraan, M.C. & Tak, P.P. (2010) CCR5 blockade in rheumatoid arthritis: a randomised, double-blind, placebo-controlled clinical trial. Annals of the Rheumatic Diseases, 69, 2013-2016.
48. Laggner, U., Di Meglio, P., Perera, G.K., Hundhausen, C., Lacy, K.E., Ali, N., Smith, C.H., Hayday, A.C., Nickoloff, B.J. & Nestle, F.O. (2011) Identification of a novel proinflammatory human skin-homing Vgamma9Vdelta2 T cell subset with a potential role in psoriasis. Journal of Immunology, 187, 2783-2793.
49. Lee, S.M., Yang, H., Tartar, D.M., Gao, B., Luo, X., Ye, S.Q., Zaghouani, H. & Fang, D. (2011) Prevention and treatment of diabetes with resveratrol in a non-obese mouse model of type 1 diabetes. Diabetologia, 54, 1136-1146.
50. Lee, Y.H., Bae, S.C. & Song, G.G. (2013) Association between the chemokine receptor 5 delta32 polymorphism and rheumatoid arthritis: a meta-analysis. Modern Rheumatology, 23, 304-310.
51. Lehtimaki, S., Tillander, S., Puustinen, A., Matikainen, S., Nyman, T., Fyhrquist, N., Savinko, T., Majuri, M.L., Wolff, H., Alenius, H. & Lauerma, A. (2010) Absence of CCR4 exacerbates skin inflammation in an oxazolone-induced contact hypersensitivity model. The Journal of Investigative Dermatology, 130, 2743-2751.
52. Leipe, J., Grunke, M., Dechant, C., Reindl, C., Kerzendorf, U., Schulze-Koops, H. & Skapenko, A. (2010) Role of Th17 cells in human autoimmune arthritis. Arthritis and Rheumatism, 62, 2876-2885.
53. Li, X., Yuan, F.L., Lu, W.G., Zhao, Y.Q., Li, C.W., Li, J.P. & Xu, R.S. (2010) The role of interleukin-17 in mediating joint destruction in rheumatoid arthritis. Biochemical and Biophysical Research Communications, 397, 131-135.
54. Lim, H.W., Lee, J., Hillsamer, P. & Kim, C.H. (2008) Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3 + regulatory T cells. Journal of Immunology, 180, 122-129.
55. Linterman, M.A., Liston, A. & Vinuesa, C.G. (2012) T-follicular helper cell differentiation and the co-option of this pathway by non-helper cells. Immunological Reviews, 247, 143-159.
56. Liston, A., Kohler, R.E., Townley, S., Haylock-Jacobs, S., Comerford, I., Caon, A.C., Webster, J., Harrison, J.M., Swann, J., Clark-Lewis, I., Korner, H. & McColl, S.R. (2009) Inhibition of CCR6 function reduces the severity of experimental autoimmune encephalomyelitis via effects on the priming phase of the immune response. Journal of Immunology, 182, 3121-3130.
57. Liu, L., Huang, D., Matsui, M., He, T.T., Hu, T., Demartino, J., Lu, B., Gerard, C. & Ransohoff, R.M. (2006) Severe disease, unaltered leukocyte migration, and reduced IFN-gamma production in CXCR3-/- mice with experimental autoimmune encephalomyelitis. Journal of Immunology, 176, 4399-4409.
58. Loetscher, P., Uguccioni, M., Bordoli, L., Baggiolini, M., Moser, B., Chizzolini, C. & Dayer, J.M. (1998) CCR5 is characteristic of Th1 lymphocytes. Nature, 391, 344-345.
59. Lowes, M.A., Kikuchi, T., Fuentes-Duculan, J., Cardinale, I., Zaba, L.C., Haider, A.S., Bowman, E.P. & Krueger, J.G. (2008) Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. The Journal of Investigative Dermatology, 128, 1207-1211.
60. Mabuchi, T., Takekoshi, T. & Hwang, S.T. (2011) Epidermal CCR6 + gammadelta T cells are major producers of IL-22 and IL-17 in a murine model of psoriasiform dermatitis. Journal of Immunology, 187, 5026-5031.
61. Mabuchi, T., Singh, T.P., Takekoshi, T., Jia, G.F., Wu, X., Kao, M.C., Weiss, I., Farber, J.M. & Hwang, S.T. (2013) CCR6 is required for epidermal trafficking of gammadelta-T cells in an IL-23-induced model of psoriasiform dermatitis. The Journal of Investigative Dermatology, 133, 164-171.
62. Matsui, M., Weaver, J., Proudfoot, A.E., Wujek, J.R., Wei, T., Richer, E., Trapp, B.D., Rao, A. & Ransohoff, R.M. (2002) Treatment of experimental autoimmune encephalomyelitis with the chemokine receptor antagonist Met-RANTES. Journal of Neuroimmunology, 128, 16-22.
63. Mirshahpanah, P., Li, Y.Y., Burkhardt, N., Asadullah, K. & Zollner, T.M. (2008) CCR4 and CCR10 ligands play additive roles in mouse contact hypersensitivity. Experimental Dermatology, 17, 30-34.
64. Mohan, K. & Issekutz, T.B. (2007) Blockade of chemokine receptor CXCR3 inhibits T cell recruitment to inflamed joints and decreases the severity of adjuvant arthritis. Journal of Immunology, 179, 8463-8469.
65. Moriguchi, K., Miyamoto, K., Tanaka, N., Yoshie, O. & Kusunoki, S. (2013) The importance of CCR4 and CCR6 in experimental autoimmune encephalomyelitis. Journal of Neuroimmunology, 257, 53-58.
66. Morimoto, J., Yoneyama, H., Shimada, A., Shigihara, T., Yamada, S., Oikawa, Y., Matsushima, K., Saruta, T. & Narumi, S. (2004) CXC chemokine ligand 10 neutralization suppresses the occurrence of diabetes in nonobese diabetic mice through enhanced beta cell proliferation without affecting insulitis. Journal of Immunology, 173, 7017-7024.
67. Muller, M., Carter, S.L., Hofer, M.J., Manders, P., Getts, D.R., Getts, M.T., Dreykluft, A., Lu, B., Gerard, C., King, N.J. & Campbell, I.L. (2007) CXCR3 signaling reduces the severity of experimental autoimmune encephalomyelitis by controlling the parenchymal distribution of effector and regulatory T cells in the central nervous system. Journal of Immunology, 179, 2774-2786.
68. Narumi, S., Kaburaki, T., Yoneyama, H., Iwamura, H., Kobayashi, Y. & Matsushima, K. (2002) Neutralization of IFN-inducible protein 10/CXCL10 exacerbates experimental autoimmune encephalomyelitis. European Journal of Immunology, 32, 1784-1791.
69. Ni, J., Zhu, Y.N., Zhong, X.G., Ding, Y., Hou, L.F., Tong, X.K., Tang, W., Ono, S., Yang, Y.F. & Zuo, J.P. (2009) The chemokine receptor antagonist, TAK-779, decreased experimental autoimmune encephalomyelitis by reducing inflammatory cell migration into the central nervous system, without affecting T cell function. British Journal of Pharmacology, 158, 2046-2056.
70. Nistala, K., Adams, S., Cambrook, H., Ursu, S., Olivito, B., de Jager, W., Evans, J.G., Cimaz, R., Bajaj-Elliott, M. & Wedderburn, L.R. (2010) Th17 plasticity in human autoimmune arthritis is driven by the inflammatory environment. Proceedings of the National Academy of Science of the USA, 107, 14751-14756.
71. O'Boyle, G., Fox, C.R., Walden, H.R., Willet, J.D., Mavin, E.R., Hine, D.W., Palmer, J.M., Barker, C.E., Lamb, C.A., Ali, S. & Kirby, J.A. (2012) Chemokine receptor CXCR3 agonist prevents human T-cell migration in a humanized model of arthritic inflammation. Proceedings of the National Academy of Science of the USA, 109, 4598-4603.
72. Odoardi, F., Sie, C., Streyl, K., Ulaganathan, V.K., Schlager, C., Lodygin, D., Heckelsmiller, K., Nietfeld, W., Ellwart, J., Klinkert, W.E., Lottaz, C., Nosov, M., Brinkmann, V., Spang, R., Lehrach, H., Vingron, M., Wekerle, H., Flugel-Koch, C. & Flugel, A. (2012) T cells become licensed in the lung to enter the central nervous system. Nature, 488, 675-679.
73. Pantelyushin, S., Haak, S., Ingold, B., Kulig, P., Heppner, F.L., Navarini, A.A. & Becher, B. (2012) Rorgammat + innate lymphocytes and gammadelta T cells initiate psoriasiform plaque formation in mice. The Journal of Clinical Investigation, 122, 2252-2256.
74. Patel, D.D., Zachariah, J.P. & Whichard, L.P. (2001) CXCR3 and CCR5 ligands in rheumatoid arthritis synovium. Clinical Immunology, 98, 39-45.
75. Perera, G.K., Di Meglio, P. & Nestle, F.O. (2012) Psoriasis. Annual Review of Pathology: Mechanisms of Disease, 7, 385-422.
76. Qin, S., Rottman, J.B., Myers, P., Kassam, N., Weinblatt, M., Loetscher, M., Koch, A.E., Moser, B. & Mackay, C.R. (1998) The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. The Journal of Clinical Investigation, 101, 746-754.
77. Rampersad, R.R., Tarrant, T.K., Vallanat, C.T., Quintero-Matthews, T., Weeks, M.F., Esserman, D.A., Clark, J., Di Padova, F., Patel, D.D., Fong, A.M. & Liu, P. (2011) Enhanced Th17-cell responses render CCR2-deficient mice more susceptible for autoimmune arthritis. PLoS ONE, 6, e25833.
78. Reboldi, A., Coisne, C., Baumjohann, D., Benvenuto, F., Bottinelli, D., Lira, S., Uccelli, A., Lanzavecchia, A., Engelhardt, B. & Sallusto, F. (2009) C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nature Immunology, 10, 514-523.
79. Rothhammer, V., Heink, S., Petermann, F., Srivastava, R., Claussen, M.C., Hemmer, B. & Korn, T. (2011) Th17 lymphocytes traffic to the central nervous system independently of alpha4 integrin expression during EAE. Journal of Experimental Medicine, 208, 2465-2476.
80. Rottman, J.B., Smith, T.L., Ganley, K.G., Kikuchi, T. & Krueger, J.G. (2001) Potential role of the chemokine receptors CXCR3, CCR4, and the integrin alphaEbeta7 in the pathogenesis of psoriasis vulgaris. Laboratory Investigation, 81, 335-347.
81. Sarkar, S.A., Lee, C.E., Victorino, F., Nguyen, T.T., Walters, J.A., Burrack, A., Eberlein, J., Hildemann, S.K. & Homann, D. (2012) Expression and regulation of chemokines in murine and human type 1 diabetes. Diabetes, 61, 436-446.
82. Sato, W., Aranami, T. & Yamamura, T. (2007) Cutting edge: human Th17 cells are identified as bearing CCR2 + CCR5- phenotype. Journal of Immunology, 178, 7525-7529.
83. Scheibel, I., Veit, T., Neves, A.G., Souza, L., Prezzi, S., Machado, S., Kohem, C., Icarelli, M., Xavier, R., Brenol, J.C. & Chies, J.A. (2008) Differential CCR5Delta32 allelic frequencies in juvenile idiopathic arthritis subtypes: evidence for different regulatory roles of CCR5 in rheumatological diseases. Scandinavian Journal of Rheumatology, 37, 13-17.
84. Singh, S.P., Zhang, H.H., Foley, J.F., Hedrick, M.N. & Farber, J.M. (2008) Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. Journal of Immunology, 180, 214-221.
85. Sorensen, T.L., Tani, M., Jensen, J., Pierce, V., Lucchinetti, C., Folcik, V.A., Qin, S., Rottman, J., Sellebjerg, F., Strieter, R.M., Frederiksen, J.L. & Ransohoff, R.M. (1999) Expression of specific chemokines and chemokine receptors in the central nervous system of multiple sclerosis patients. The Journal of Clinical Investigation, 103, 807-815.
86. Sporici, R. & Issekutz, T.B. (2010) CXCR3 blockade inhibits T-cell migration into the CNS during EAE and prevents development of adoptively transferred, but not actively induced, disease. European Journal of Immunology, 40, 2751-2761.
87. Stahl, E.A., Raychaudhuri, S., Remmers, E.F., Xie, G., Eyre, S., Thomson, B.P., Li, Y., Kurreeman, F.A., Zhernakova, A., Hinks, A., Guiducci, C., Chen, R., Alfredsson, L., Amos, C.I., Ardlie, K.G., Barton, A., Bowes, J., Brouwer, E., Burtt, N.P., Catanese, J.J., Coblyn, J., Coenen, M.J., Costenbader, K.H., Criswell, L.A., Crusius, J.B., Cui, J., de Bakker, P.I., De Jager, P.L., Ding, B., Emery, P., Flynn, E., Harrison, P., Hocking, L.J., Huizinga, T.W., Kastner, D.L., Ke, X., Lee, A.T., Liu, X., Martin, P., Morgan, A.W., Padyukov, L., Posthumus, M.D., Radstake, T.R., Reid, D.M., Seielstad, M., Seldin, M.F., Shadick, N.A., Steer, S., Tak, P.P., Thomson, W., van der Helm-van Mil, A.H., van der Horst-Bruinsma, I.E., van der Schoot, C.E., van Riel, P.L., Weinblatt, M.E., Wilson, A.G., Wolbink, G.J., Wordsworth, B.P., Wijmenga, C., Karlson, E.W., Toes, R.E., de Vries, N., Begovich, A.B., Worthington, J., Siminovitch, K.A., Gregersen, P.K., Klareskog, L. & Plenge, R.M. (2010) Genome-wide association study meta-analysis identifies seven new rheumatoid arthritis risk loci. Nature Genetics, 42, 508-514.
88. Stritesky, G.L., Yeh, N. & Kaplan, M.H. (2008) IL-23 promotes maintenance but not commitment to the Th17 lineage. Journal of Immunology, 181, 5948-5955.
89. Stromnes, I.M., Cerretti, L.M., Liggitt, D., Harris, R.A. & Goverman, J.M. (2008) Differential regulation of central nervous system autoimmunity by T (H) 1 and T (H) 17 cells. Nature Medicine, 14, 337-342.
90. Sugiyama, H., Gyulai, R., Toichi, E., Garaczi, E., Shimada, S., Stevens, S.R., McCormick, T.S. & Cooper, K.D. (2005) Dysfunctional blood and target tissue CD4 + CD25high regulatory T cells in psoriasis: mechanism underlying unrestrained pathogenic effector T cell proliferation. Journal of Immunology, 174, 164-173.
91. Sumaria, N., Roediger, B., Ng, L.G., Qin, J., Pinto, R., Cavanagh, L.L., Shklovskaya, E., de St, Fazekas, Groth, B., Triccas, J.A. & Weninger, W. (2011) Cutaneous immunosurveillance by self-renewing dermal gammadelta T cells. Journal of Experimental Medicine, 208, 505-518.
92. Tran, E.H., Kuziel, W.A. & Owens, T. (2000) Induction of experimental autoimmune encephalomyelitis in C57BL/6 mice deficient in either the chemokine macrophage inflammatory protein-1alpha or its CCR5 receptor. European Journal of Immunology, 30, 1410-1415.
93. Trifari, S., Kaplan, C.D., Tran, E.H., Crellin, N.K. & Spits, H. (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. Nature Immunology, 10, 864-871.
94. Vila, J., Isaacs, J.D. & Anderson, A.E. (2009) Regulatory T cells and autoimmunity. Current Opinion in Hematology, 16, 274-279.
95. Villares, R., Cadenas, V., Lozano, M., Almonacid, L., Zaballos, A., Martinez, A.C. & Varona, R. (2009) CCR6 regulates EAE pathogenesis by controlling regulatory CD4 + T-cell recruitment to target tissues. European Journal of Immunology, 39, 1671-1681.
96. Wedderburn, L.R., Robinson, N., Patel, A., Varsani, H. & Woo, P. (2000) Selective recruitment of polarized T cells expressing CCR5 and CXCR3 to the inflamed joints of children with juvenile idiopathic arthritis. Arthritis and Rheumatism, 43, 765-774.
97. Xu, W., Li, R., Dai, Y., Wu, A., Wang, H., Cheng, C., Qiu, W., Lu, Z., Zhong, X., Shu, Y., Kermode, A.G. & Hu, X. (2013) IL-22 secreting CD4 + T cells in the patients with neuromyelitis optica and multiple sclerosis. Journal of Neuroimmunology, 261, 87-91.
98. Yamada, Y., Okubo, Y., Shimada, A., Oikawa, Y., Yamada, S., Narumi, S., Matsushima, K. & Itoh, H. (2012) Acceleration of diabetes development in CXC chemokine receptor 3 (CXCR3)-deficient NOD mice. Diabetologia, 55, 2238-2245.
99. Yamazaki, T., Yang, X.O., Chung, Y., Fukunaga, A., Nurieva, R., Pappu, B., Martin-Orozco, N., Kang, H.S., Ma, L., Panopoulos, A.D., Craig, S., Watowich, S.S., Jetten, A.M., Tian, Q. & Dong, C. (2008) CCR6 regulates the migration of inflammatory and regulatory T cells. Journal of Immunology, 181, 8391-8401.
100. Yang, Y.F., Mukai, T., Gao, P., Yamaguchi, N., Ono, S., Iwaki, H., Obika, S., Imanishi, T., Tsujimura, T., Hamaoka, T. & Fujiwara, H. (2002) A non-peptide CCR5 antagonist inhibits collagen-induced arthritis by modulating T cell migration without affecting anti-collagen T cell responses. European Journal of Immunology, 32, 2124-2132.
101. Zaba, L.C., Cardinale, I., Gilleaudeau, P., Sullivan-Whalen, M., Suarez-Farinas, M., Fuentes-Duculan, J., Novitskaya, I., Khatcherian, A., Bluth, M.J., Lowes, M.A. & Krueger, J.G. (2007) Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. Journal of Experimental Medicine, 204, 3183-3194.
102. Zaba, L.C., Fuentes-Duculan, J., Eungdamrong, N.J., Abello, M.V., Novitskaya, I., Pierson, K.C., Gonzalez, J., Krueger, J.G. & Lowes, M.A. (2009) Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. The Journal of Investigative Dermatology, 129, 79-88.
103. Zhang, N., Pan, H.F. & Ye, D.Q. (2011) Th22 in inflammatory and autoimmune disease: prospects for therapeutic intervention. Molecular and Cellular Biochemistry, 353, 41-46.