An immune paradox: How can the same chemokine axis regulate both immune tolerance and activation?: CCR6/CCL20: A chemokine axis balancing immunological tolerance and inflammation in autoimmune disease

BioEssays

Volumn 32, Issue 12, 2010, Pages 1067-1076

  Comerford, Iain ^a   Bunting, Mark ^a   Fenix, Kevin ^a   Haylock Jacobs, Sarah ^a   Litchfield, Wendel ^a   Harata Lee, Yuka ^a   Turvey, Michelle ^a   Brazzatti, Julie ^a   Gregor, Carly ^a   Nguyen, Phillip ^a   Kara, Ervin ^a   McColl, Shaun R ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Autoimmunity; CCL20; CCR6; Chemokine; Th17

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CCR6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA;

ARTHRITIS; AUTOIMMUNITY; ENCEPHALITIS; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOLOGY; INFLAMMATORY CELL; LEUKOCYTE MOTILITY; MULTIPLE SCLEROSIS; REGULATORY T LYMPHOCYTE; REVIEW; TH17 CELL;

ADAPTIVE IMMUNITY; AUTOIMMUNE DISEASES; CHEMOKINE CCL20; HUMANS; IMMUNE TOLERANCE; INFLAMMATION; RECEPTORS, CCR6; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 78649512344     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201000063     Document Type: Review

References (95)

1. Trepel F. 1974. Number and distribution of lymphocytes in man. A critical analysis. Klin Wochenschr 52: 511-5.
2. Baggiolini M. 1998. Chemokines and leukocyte traffic. Nature 392: 565-8.
3. Sallusto F, Baggiolini M. 2008. Chemokines and leukocyte traffic. Nat Immunol 9: 949-52.
4. Sallusto F, Mackay CR, Lanzavecchia A. 2000. The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol 18: 593-620.
5. Gale LM, McColl SR. 1999. Chemokines: extracellular messengers for all occasions? BioEssays 21: 17-28.
6. + regulatory T cells. Nat Immunol 4: 330-6.
7. Thompson C, Powrie F. 2004. Regulatory T cells. Curr Opin Pharmacol 4: 408-14.
8. Weaver CT, Hatton RD. 2009. Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective. Nat Rev Immunol 9: 883-9.
9. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6: 1123-32.
10. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, et al. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-4.
11. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, et al. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-89.
12. Stephens LA, Malpass KH, Anderton SM. 2009. Curing CNS autoimmune disease with myelin-reactive Foxp3+ Treg. Eur J Immunol 39: 1108-17.
13. + regulatory cells within the central nervous system. J Immunol 175: 3025-32.
14. Langrish CL, Chen Y, Blumenschein WM, Mattson J, et al. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201: 233-40.
15. Ebert LM, Schaerli P, Moser B. 2005. Chemokine-mediated control of T cell traffic in lymphoid and peripheral tissues. Mol Immunol 42: 799-809.
16. Yamazaki T, Yang XO, Chung Y, Fukunaga A, et al. 2008. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 181: 8391-401.
17. Singh SP, Zhang HH, Foley JF, Hedrick MN, et al. 2008. Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J Immunol 180: 214-21.
18. Annunziato F, Cosmi L, Santarlasci V, Maggi L, et al. 2007. Phenotypic and functional features of human Th17 cells. J Exp Med 204: 1849-61.
19. + T-cell subset. Blood 105: 2877-86.
20. Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, et al. 2007. Surface phenotype and antigenic specificity of human interleukin 17- producing T helper memory cells. Nat Immunol 8: 639-46.
21. + regulatory T cells. J Immunol 180: 122-9.
22. + regulatory T cells bear functional skin-homing receptors. J Immunol 177: 4488-94.
23. Schutyser E, Struyf S, Van Damme J. 2003. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 14: 409-26.
24. Power CA, Church DJ, Meyer A, Alouani S, et al. 1997. Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3alpha from lung dendritic cells. J Exp Med 186: 825-35.
25. Perez-Canadillas JM, Zaballos A, Gutierrez J, Varona R, et al. 2001. NMR solution structure of murine CCL20/MIP-3alpha, a chemokine that specifically chemoattracts immature dendritic cells and lymphocytes through its highly specific interaction with the beta-chemokine receptor CCR6. J Biol Chem 276: 28372-9.
26. Greaves DR, Wang W, Dairaghi DJ, Dieu MC, et al. 1997. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells. J Exp Med 186: 837-44.
27. Dieu MC, Vanbervliet B, Vicari A, Bridon JM, et al. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J Exp Med 188: 373-86.
28. Rivino L, Gruarin P, Haringer B, Steinfelder S, et al. 2010. CCR6 is expressed on an IL-10-producing, autoreactive memory T cell population with context-dependent regulatory function. J Exp Med 207: 565-77.
29. Liao F, Rabin RL, Smith CS, Sharma G, et al. 1999. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 alpha. J Immunol 162: 186-94.
30. + T lymphocytes. J Immunol 168: 65-72.
31. Haas JD, Gonzalez FH, Schmitz S, Chennupati V, et al. 2009. CCR6 and NK1.1 distinguish between IL-17A and IFN-gamma-producing gammadelta effector T cells. Eur J Immunol 39: 3488-97.
32. Martin B, Hirota K, Cua DJ, Stockinger B, et al. 2009. Interleukin-17 producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31: 321-30.
33. Krzysiek R, Lefevre EA, Bernard J, Foussat A, et al. 2000. Regulation of CCR6 chemokine receptor expression and responsiveness to macrophage inflammatory protein-3alpha/CCL20 in human B cells. Blood 96: 2338-45.
34. Yamashiro S, Wang JM, Yang D, Gong WH, et al. 2000. Expression of CCR6 and CD83 by cytokine-activated human neutrophils. Blood 96: 3958-63.
35. Vanbervliet B, Homey B, Durand I, Massacrier C, et al. 2002. Sequential involvement of CCR2 and CCR6 ligands for immature dendritic cell recruitment: possible role at inflamed epithelial surfaces. Eur J Immunol 32: 231-42.
36. Dieu-Nosjean MC, Massacrier C, Vanbervliet B, Fridman WH, et al. 2001. IL-10 induces CCR6 expression during Langerhans cell development while IL-4 and IFN-gamma suppress it. J Immunol 167: 5594-602.
37. Casamayor-Palleja M, Mondiere P, Verschelde C, Bella C, et al. 2002. BCR ligation reprograms B cells for migration to the T zone and B-cell follicle sequentially. Blood 99: 1913-21.
38. Cook DN, Prosser DM, Forster R, Zhang J, et al. 2000. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 12: 495-503.
39. Varona R, Villares R, Carramolino L, Goya I, et al. 2001. CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J Clin Invest 107: R37-R45.
40. + dendritic cells. J Immunol 171: 2797-803.
41. Westphal S, Lugering A, von Wedel J, von Eiff C, et al. 2008. Resistance of chemokine receptor 6-deficient mice to Yersinia enterocolitica infection: evidence of defective M-cell formation in vivo. Am J Pathol 172: 671-80.
42. + regulatory T-cell development and M-cell formation inside Peyer's patches. Am J Pathol 166: 1647-54.
43. Takatori H, Kanno Y, Watford WT, Tato CM, et al. 2009. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 206: 35-41.
44. Brand S, Olszak T, Beigel F, Tato CM, et al. 2006. Cell differentiation dependent expressed CCR6 mediates ERK-1/2, SAPK/JNK, and Akt signaling resulting in proliferation and migration of colorectal cancer cells. J Cell Biochem 97: 709-23.
45. + T-cell-mediated acute graft-versus-host disease responses. Blood 106: 18-26.
46. Lechner A, Ritter U, Varona R, Marquez G, et al. 2007. Protective immunity and delayed type hypersensitivity reaction are uncoupled in experimental Leishmania major infection of CCR6-negative mice. Microbes Infect 9: 291-9.
47. Wang C, Kang SG, Lee J, Sun Z, et al. 2009. The roles of CCR6 in migration of Th17 cells and regulation of effector T-cell balance in the gut. Mucosal Immunol 2: 173-83.
48. Paradis TJ, Cole SH, Nelson RT, Gladue RP. 2008. Essential role of CCR6 in directing activated T cells to the skin during contact hypersensitivity. J Invest Dermatol 128: 628-33.
49. + T cell cross priming in vivo Immunity 24: 191-201.
50. + regulatory T cells in the control of experimental CNS autoimmune disease. J Neuroimmunol 193: 1-11.
51. Furlan R, Rovaris M, Martinelli Boneschi F, Khademi M, et al. 2005. Immunological patterns identifying disease course and evolution in multiple sclerosis patients. J Neuroimmunol 165: 192-200.
52. Ambrosini E, Remoli ME, Giacomini E, Rosicarelli B, et al. 2005. Astrocytes produce dendritic cell-attracting chemokines in vitro and in multiple sclerosis lesions. J Neuropathol Exp Neurol 64: 706-15.
53. Kivisakk P, Trebst C, Liu Z, Tucky BH, et al. 2002. T-cells in the cerebrospinal fluid express a similar repertoire of inflammatory chemokine receptors in the absence or presence of CNS inflammation: implications for CNS trafficking. Clin Exp Immunol 129: 510-8.
54. Kohler RE, Caon AC, Willenborg DO, Clark-Lewis I, et al. 2003. A role for macrophage inflammatory protein-3 alpha/CC chemokine ligand 20 in immune priming during T cell-mediated inflammation of the central nervous system. J Immunol 170: 6298-306.
55. Liston A, Kohler RE, Townley S, Haylock-Jacobs S, et al. 2009. Inhibition of CCR6 function reduces the severity of experimental autoimmune encephalomyelitis via effects on the priming phase of the immune response. J Immunol 182: 3121-30.
56. Serafini B, Columba-Cabezas S, Di Rosa F, Aloisi F. 2000. Intracerebral recruitment and maturation of dendritic cells in the onset and progression of experimental autoimmune encephalomyelitis. Am J Pathol 157: 1991-2002.
57. Ambrosini E, Columba-Cabezas S, Serafini B, Muscella A, et al. 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.
58. Reboldi A, Coisne C, Baumjohann D, Benvenuto F, et al. 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. Nat Immunol 10: 514-23.
59. Villares R, Cadenas V, Lozano M, Almonacid L, et al. 2009. CCR6 regulates EAE pathogenesis by controlling regulatory CD4+ T-cell recruitment to target tissues. Eur J Immunol 39: 1671-81.
60. Elhofy A, Depaolo RW, Lira SA, Lukacs NW, et al. 2009. Mice deficient for CCR6 fail to control chronic experimental autoimmune encephalomyelitis. J Neuroimmunol 213: 91-9.
61. Salama AD, Chitnis T, Imitola J, Ansari MJ, et al. 2003. Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J Exp Med 198: 71-8.
62. Durelli L, Conti L, Clerico M, Boselli D, et al. 2009. T-helper 17 cells expand in multiple sclerosis and are inhibited by interferon-beta. Ann Neurol 65: 499-509.
63. Stahl EA, Raychaudhuri S, Remmers EF, Xie G, et al. 2010. Genomewide association study meta-analysis identifies seven new rheumatoid arthritis risk loci. Nat Genet 42: 508-14.
64. Kochi Y, Okada Y, Suzuki A, Ikari K, et al. 2010. A regulatory variant in CCR6 is associated with rheumatoid arthritis susceptibility. Nat Genet 42: 515-9.
65. Matsui T, Akahoshi T, Namai R, Hashimoto A, et al. 2001. Selective recruitment of CCR6-expressing cells by increased production of MIP-3 alpha in rheumatoid arthritis. Clin Exp Immunol 125: 155-61.
66. Chevrel G, Garnero P, Miossec P. 2002. Addition of interleukin 1 (IL1) and IL17 soluble receptors to a tumour necrosis factor alpha soluble receptor more effectively reduces the production of IL6 and macrophage inhibitory protein-3alpha and increases that of collagen in an in vitro model of rheumatoid synoviocyte activation. Ann Rheum Dis 61: 730-3.
67. Ruth JH, Shahrara S, Park CC, Morel JC, et al. 2003. Role of macrophage inflammatory protein-3alpha and its ligand CCR6 in rheumatoid arthritis. Lab Invest 83: 579-88.
68. Chabaud M, Page G, Miossec P. 2001. Enhancing effect of IL-1, IL-17, and TNF-alpha on macrophage inflammatory protein-3alpha production in rheumatoid arthritis: regulation by soluble receptors and Th2 cytokines. J Immunol 167: 6015-20.
69. Kawashiri SY, Kawakami A, Iwamoto N, Fujikawa K, et al. 2009. Proinflammatory cytokines synergistically enhance the production of chemokine ligand 20 (CCL20) from rheumatoid fibroblast-like synovial cells in vitro and serum CCL20 is reduced in vivo by biologic diseasemodifying antirheumatic drugs. J Rheumatol 36: 2397-402.
70. (+) memory T cells in rheumatoid arthritis synovium. Arthritis Res 2: 415-23.
71. Shen H, Goodall JC, Hill Gaston JS. 2009. Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis. Arthritis Rheum 60: 1647-56.
72. Murphy CA, Langrish CL, Chen Y, Blumenschein W, et al. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198: 1951-7.
73. Hirota K, Yoshitomi H, Hashimoto M, Maeda S, et al. 2007. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med 204: 2803-12.
74. Pene J, Chevalier S, Preisser L, Venereau E, et al. 2008. Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes. J Immunol 180: 7423-30.
75. Kirkham BW, Lassere MN, Edmonds JP, Juhasz KM, et al. 2006. Synovial membrane cytokine expression is predictive of joint damage progression in rheumatoid arthritis: a two-year prospective study (the DAMAGE study cohort). Arthritis Rheum 54: 1122-31.
76. Yamada H, Nakashima Y, Okazaki K, Mawatari T, et al. 2008. Th1 but not Th17 cells predominate in the joints of patients with rheumatoid arthritis. Ann Rheum Dis 67: 1299-304.
77. Ehrenstein MR, Evans JG, Singh A, Moore S, et al. 2004. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med 200: 277-85.
78. Valencia X, Stephens G, Goldbach-Mansky R, Wilson M, et al. 2006. TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 108: 253-61.
79. Nistala K, Moncrieffe H, Newton KR, Varsani H, et al. 2008. Interleukin- 17-producing T cells are enriched in the joints of children with arthritis, but have a reciprocal relationship to regulatory T cell numbers. Arthritis Rheum 58: 875-87.
80. Olivito B, Simonini G, Ciullini S, Moriondo M, et al. 2009. Th17 transcription factor RORC2 is inversely correlated with FOXP3 expression in the joints of children with juvenile idiopathic arthritis. J Rheumatol 36: 2017-24.
81. Parronchi P, Romagnani P, Annunziato F, Sampognaro S, et al. 1997. Type 1 T-helper cell predominance and interleukin-12 expression in the gut of patients with Crohn's disease. Am J Pathol 150: 823-32.
82. Heller F, Florian P, Bojarski C, Richter J, et al. 2005. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129: 550-64.
83. Barrett JC, Hansoul S, Nicolae DL, Cho JH, et al. 2008. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 40: 955-62.
84. Van Limbergen J, Wilson DC, Satsangi J. 2009. The genetics of Crohn's disease. Annu Rev Genomics Hum Genet 10: 89-116.
85. Noble C, Nimmo E, Gaya D, Russell RK, et al. 2006. Novel susceptibility genes in inflammatory bowel disease. World J Gastroenterol 12: 1991-9.
86. Rodriguez-Bores L, Fonseca GC, Villeda MA, Yamamoto-Furusho JK. 2007. Novel genetic markers in inflammatory bowel disease. World J Gastroenterol 13: 5560-70.
87. Kaser A, Ludwiczek O, Holzmann S, Moschen AR, et al. 2004. Increased expression of CCL20 in human inflammatory bowel disease. J Clin Immunol 24: 74-85.
88. Kwon JH, Keates S, Bassani L, Mayer LF, et al. 2002. Colonic epithelial cells are a major site of macrophage inflammatory protein 3alpha (MIP-3alpha) production in normal colon and inflammatory bowel disease. Gut 51: 818-26.
89. Katchar K, Kelly CP, Keates S, O'Brien MJ, et al. 2007. MIP-3alpha neutralizing monoclonal antibody protects against TNBS-induced colonic injury and inflammation in mice. Am J Physiol Gastrointest Liver Physiol 292: G1263-G71.
90. Teramoto K, Miura S, Tsuzuki Y, Hokari R, et al. 2005. Increased lymphocyte trafficking to colonic microvessels is dependent on MAdCAM-1 and C-C chemokine mLARC/CCL20 in DSS-induced mice colitis. Clin Exp Immunol 139: 421-8.
91. Kristensen NN, Brudzewsky D, Gad M, Claesson MH. 2006. Chemokines involved in protection from colitis by CD4+CD25+ regulatory T cells. Inflamm Bowel Dis 12: 612-8.
92. Varona R, Cadenas V, Flores J, Martinez AC, et al. 2003. CCR6 has a nonredundant role in the development of inflammatory bowel disease. Eur J Immunol 33: 2937-46.
93. DeVries ME, Kelvin AA, Xu L, Ran L, et al. 2006. Defining the origins and evolution of the chemokine/chemokine receptor system. J Immunol 176: 401-15.
94. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, et al. 2006. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24: 677-88.
95. Dieu-Nosjean MC, Massacrier C, Homey B, Vanbervliet B, et al. 2000. Macrophage inflammatory protein 3alpha is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J Exp Med 192: 705-18.