CCL20 and β-defensin-2 induce arrest of human Th17 cells on inflamed endothelium in vitro under flow conditions

Journal of Immunology

Volumn 186, Issue 3, 2011, Pages 1411-1420

  Ghannam, Soufiane ^a   Dejou, Cécile ^a   Pedretti, Nathalie ^b,c   Giot, Jean Philipe ^a   Dorgham, Karim ^d   Boukhaddaoui, Hassan ^a   Deleuze, Virginie ^e   Bernard, François Xavier ^b,c   Jorgensen, Christian ^a   Yssel, Hans ^a   Pène, Jérôme ^a  

^a INSERM   (France)

^b BIOalternatives SAS   (France)

^c UNIVERSITÉ DE POITIERS   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA DEFENSIN 1; BETA DEFENSIN 2; BETA DEFENSIN 3; CD3 ANTIGEN; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CXCR4; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; INTERLEUKIN 22; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; INTERNALIZATION; KERATINOCYTE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; TH1 CELL; TH17 CELL; TH2 CELL; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

ANIMALS; APOPTOSIS; BETA-DEFENSINS; BLOOD FLOW VELOCITY; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL20; ENDOTHELIUM, VASCULAR; EPIDERMIS; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-17; INTERLEUKINS; KERATINOCYTES; L CELLS (CELL LINE); LIGANDS; LYMPHOCYTE ACTIVATION; MICE; RECEPTORS, CCR6; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 79251564771     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000597     Document Type: Article

References (58)

1. Butcher, E. C., and L. J. Picker. 1996. Lymphocyte homing and homeostasis. Science 272: 60-66.
2. Bargatze, R. F., and E. C. Butcher. 1993. Rapid G protein-regulated activation event involved in lymphocyte binding to high endothelial venules. J. Exp. Med. 178: 367-372.
3. Bargatze, R. F., M. A. Jutila, and E. C. Butcher. 1995. Distinct roles of L-selectin and integrins α 4 β 7 and LFA-1 in lymphocyte homing to Peyer's patch-HEV in situ: the multistep model confirmed and refined. Immunity 3: 99-108.
4. Warnock, R. A., S. Askari, E. C. Butcher, and U. H. von Andrian. 1998. Molecular mechanisms of lymphocyte homing to peripheral lymph nodes. J. Exp. Med. 187: 205-216.
5. Campbell, J. J., J. Hedrick, A. Zlotnik, M. A. Siani, D. A. Thompson, and E. C. Butcher. 1998. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 279: 381-384.
6. Campbell, J. J., G. Haraldsen, J. Pan, J. Rottman, S. Qin, P. Ponath, D. P. Andrew, R. Warnke, N. Ruffing, N. Kassam, et al. 1999. The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature 400: 776-780.
7. Baba, M., T. Imai, M. Nishimura, M. Kakizaki, S. Takagi, K. Hieshima, H. Nomiyama, and O. Yoshie. 1997. Identification of CCR6, the specific receptor for a novel lymphocyte-directed CC chemokine LARC. J. Biol. Chem. 272: 14893-14898.
8. Greaves, D. R., W. Wang, D. J. Dairaghi, M. C. Dieu, B. Saint-Vis, K. Franz-Bacon, D. Rossi, C. Caux, T. McClanahan, S. Gordon, et al. 1997. CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3α and is highly expressed in human dendritic cells. J. Exp. Med. 186: 837-844.
9. Cook, D. N., D. M. Prosser, R. Forster, J. Zhang, N. A. Kuklin, S. J. Abbondanzo, X. D. Niu, S. C. Chen, D. J. Manfra, M. T. Wiekowski, et al. 2000. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 12: 495-503.
10. Salazar-Gonzalez, R. M., J. H. Niess, D. J. Zammit, R. Ravindran, A. Srinivasan, J. R. Maxwell, T. Stoklasek, R. Yadav, I. R. Williams, X. Gu, et al. 2006. CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 24: 623-632.
11. + T cell crosspriming in vivo. Immunity 24: 191-201.
12. Varona, R., R. Villares, L. Carramolino, I. Goya, A. Zaballos, J. Gutiérrez, M. Torres, C. Martínez-A, and G. Márquez. 2001. CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J. Clin. Invest. 107: R37-R45.
13. Lechner, A., U. Ritter, R. Varona, G. Marquez, C. Bogdan, and H. Körner. 2007. Protective immunity and delayed type hypersensitivity reaction are uncoupled in experimental Leishmania major infection of CCR6-negative mice. Microbes Infect. 9: 291-299. (Pubitemid 46341931)
14. Varona, R., V. Cadenas, J. Flores, C. Martínez-A, and G. Márquez. 2003. CCR6 has a non-redundant role in the development of inflammatory bowel disease. Eur. J. Immunol. 33: 2937-2946.
15. Dieu, M. C., B. Vanbervliet, A. Vicari, J. M. Bridon, E. Oldham, S. Aït-Yahia, F. Brière, A. Zlotnik, S. Lebecque, and C. Caux. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188: 373-386.
16. Krzysiek, R., E. A. Lefevre, J. Bernard, A. Foussat, P. Galanaud, F. Louache, and Y. Richard. 2000. Regulation of CCR6 chemokine receptor expression and responsiveness to macrophage inflammatory protein-3α/CCL20 in human B cells. Blood 96: 2338-2345.
17. Liao, F., R. L. Rabin, C. S. Smith, G. Sharma, T. B. Nutman, and J. M. Farber. 1999. CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 α. J. Immunol. 162: 186-194.
18. 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.
19. Annunziato, F., L. Cosmi, V. Santarlasci, L. Maggi, F. Liotta, B. Mazzinghi, E. Parente, L. Filì, S. Ferri, F. Frosali, et al. 2007. Phenotypic and functional features of human Th17 cells. J. Exp. Med. 204: 1849-1861.
20. Singh, S. P., H. H. Zhang, J. F. Foley, M. N. Hedrick, and J. M. Farber. 2008. Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J. Immunol. 180: 214-221.
21. 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.
22. 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.
23. Rossi, D. L., A. P. Vicari, K. Franz-Bacon, T. K. McClanahan, and A. Zlotnik. 1997. Identification through bioinformatics of two new macrophage proinflammatory human chemokines: MIP-3α and MIP-3β. J. Immunol. 158: 1033-1036.
24. Hieshima, K., T. Imai, G. Opdenakker, J. Van Damme, J. Kusuda, H. Tei, Y. Sakaki, K. Takatsuki, R. Miura, O. Yoshie, and H. Nomiyama. 1997. Molecular cloning of a novel human CC chemokine liver and activation-regulated chemokine (LARC) expressed in liver. Chemotactic activity for lymphocytes and gene localization on chromosome 2. J. Biol. Chem. 272: 5846-5853.
25. Schutyser, E., S. Struyf, and J. Van Damme. 2003. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 14: 409-426. (Pubitemid 37099454)
26. Yang, D., O. Chertov, S. N. Bykovskaia, Q. Chen, M. J. Buffo, J. Shogan, M. Anderson, J. M. Schröder, J. M. Wang, O. M. Howard, and J. J. Oppenheim. 1999. β-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286: 525-528.
27. García, J. R., F. Jaumann, S. Schulz, A. Krause, J. Rodríguez-Jiménez, U. Forssmann, K. Adermann, E. Klüver, C. Vogelmeier, D. Becker, et al. 2001. Identification of a novel, multifunctional β-defensin (human β-defensin 3) with specific antimicrobial activity. Its interaction with plasma membranes of Xenopus oocytes and the induction of macrophage chemoattraction. Cell Tissue Res. 306: 257-264.
28. Hinrichsen, K., R. Podschun, S. Schubert, J. M. Schröder, J. Harder, and E. Proksch. 2008. Mouse β-defensin-14, an antimicrobial ortholog of human β-defensin-3. Antimicrob. Agents Chemother. 52: 1876-1879.
29. Hoover, D. M., C. Boulègue, D. Yang, J. J. Oppenheim, K. Tucker, W. Lu, and J. Lubkowski. 2002. The structure of human macrophage inflammatory protein-3α /CCL20. Linking antimicrobial and CC chemokine receptor-6-binding activities with human β-defensins. J. Biol. Chem. 277: 37647-37654.
30. Hirota, K., H. Yoshitomi, M. Hashimoto, S. Maeda, S. Teradaira, N. Sugimoto, T. Yamaguchi, T. Nomura, H. Ito, T. Nakamura, 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: 2803-2812.
31. Reboldi, A., C. Coisne, D. Baumjohann, F. Benvenuto, D. Bottinelli, S. Lira, A. Uccelli, A. Lanzavecchia, B. Engelhardt, and F. Sallusto. 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: 514-523.
32. Scheffold, A., A. Radbruch, and M. Assenmacher. 2010. Phenotyping and separation of leukocyte populations based on affinity labelling. In Methods in Microbiology, 2nd edition. Volume 32: Immunology of infection. S. E. Kaufmann, and D. Kabelitz, eds. Academic Press, San Diego, CA. p. 23-58.
33. Yssel, H., and H. Spits. 2002. In vitro culture of subpopulations of human T lymphocytes. In Protocols in Immunology. J. Coligan, A. M. Kruisbeek, J. Margulies, E. M. Shevach, and W. Strober, eds. John Wyley and Sons, New York. p. 7-19.
34. Pène, J., S. Chevalier, L. Preisser, E. Vénéreau, M. H. Guilleux, S. Ghannam, J. P. Molès, Y. Danger, E. Ravon, S. Lesaux, et al. 2008. Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes. J. Immunol. 180: 7423-7430.
35. Yssel, H., J. E. De Vries, M. Koken, W. Van Blitterswijk, and H. Spits. 1984. Serum-free medium for generation and propagation of functional human cytotoxic and helper T cell clones. J. Immunol. Methods 72: 219-227. (Pubitemid 14092011)
36. Boniface, K., F. X. Bernard, M. Garcia, A. L. Gurney, J. C. Lecron, and F. Morel. 2005. IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J. Immunol. 174: 3695-3702. (Pubitemid 40354080)
37. Alon, R., G. Cinamon, and F. W. Luscinskas. 2005. Real time in vitro assays for studying leukocyte transendothelial migration under physiological flow conditions. In Leukocyte Trafficking. A. Hamann, and B. Engelhardt, eds. Wiley-VCH Verlag, Weinheim, Germany. p. 437-454.
38. Quiñones-Mateu, M. E., M. M. Lederman, Z. Feng, B. Chakraborty, J. Weber, H. R. Rangel, M. L. Marotta, M. Mirza, B. Jiang, P. Kiser, et al. 2003. Human epithelial b-defensins 2 and 3 inhibit HIV-1 replication. AIDS 17: F39-F48.
39. Sallusto, F., C. R. Mackay, and A. Lanzavecchia. 2000. The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18: 593-620.
40. Campbell, J. J., and E. C. Butcher. 2000. Chemokines in tissue-specific and microenvironment-specific lymphocyte homing. Curr. Opin. Immunol. 12: 336-341.
41. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314.
42. Fitzhugh, D. J., S. Naik, S. W. Caughman, and S. T. Hwang. 2000. Cutting edge: C-C chemokine receptor 6 is essential for arrest of a subset of memory T cells on activated dermal microvascular endothelial cells under physiologic flow conditions in vitro. J. Immunol. 165: 6677-6681.
43. Dieu-Nosjean, M. C., C. Massacrier, B. Homey, B. Vanbervliet, J. J. Pin, A. Vicari, S. Lebecque, C. Dezutter-Dambuyant, D. Schmitt, A. Zlotnik, and C. Caux. 2000. Macrophage inflammatory protein 3a is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J. Exp. Med. 192: 705-718.
44. Charbonnier, A. S., N. Kohrgruber, E. Kriehuber, G. Stingl, A. Rot, and D. Maurer. 1999. Macrophage inflammatory protein 3a is involved in the constitutive trafficking of epidermal langerhans cells. J. Exp. Med. 190: 1755-1768.
45. Iwasaki, A., and B. L. Kelsall. 2000. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage in- flammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J. Exp. Med. 191: 1381-1394.
46. Tanaka, Y., T. Imai, M. Baba, I. Ishikawa, M. Uehira, H. Nomiyama, and O. Yoshie. 1999. Selective expression of liver and activation-regulated chemokine (LARC) in intestinal epithelium in mice and humans. Eur. J. Immunol. 29: 633-642.
47. Meissner, A., O. Zilles, R. Varona, K. Jozefowski, U. Ritter, G. Marquez, R. Hallmann, and H. Korner. 2003. CC chemokine ligand 20 partially controls adhesion of naive B cells to activated endothelial cells under shear stress. Blood 102: 2724-2727.
48. Liang, S. C., X. Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203: 2271-2279.
49. Röhrl, J., D. Yang, J. J. Oppenheim, and T. Hehlgans. 2010. Specific binding and chemotactic activity of mBD4 and its functional orthologue hBD2 to CCR6-expressing cells. J. Biol. Chem. 285: 7028-7034.
50. Vongsa, R. A., N. P. Zimmerman, and M. B. Dwinell. 2009. CCR6 regulation of the actin cytoskeleton orchestrates human β defensin-2- and CCL20-mediated restitution of colonic epithelial cells. J. Biol. Chem. 284: 10034-10045.
51. Soruri, A., J. Grigat, U. Forssmann, J. Riggert, and J. Zwirner. 2007. β-Defensins chemoattract macrophages and mast cells but not lymphocytes and dendritic cells: CCR6 is not involved. Eur. J. Immunol. 37: 2474-2486.
52. Niyonsaba, F., H. Ogawa, and I. Nagaoka. 2004. Human β-defensin-2 functions as a chemotactic agent for tumour necrosis factor-α-treated human neutrophils. Immunology 111: 273-281. (Pubitemid 38365749)
53. +) memory T lymphocytes results in down-regulation of cell-surface CXCR4 expression and a strongly reduced capacity to migrate in response to stromal cell-derived factor-1. Int. Immunol. 11: 1451-1462.
54. Caux, C., B. Vanbervliet, C. Massacrier, S. Ait-Yahia, C. Vaure, K. Chemin, M. C. Dieu-Nosjean And, and A. Vicari. 2002. Regulation of dendritic cell recruitment by chemokines. Transplantation 73(1 Suppl): S7-S11.
55. Förster, R., E. Kremmer, A. Schubel, D. Breitfeld, A. Kleinschmidt, C. Nerl, G. Bernhardt, and M. Lipp. 1998. Intracellular and surface expression of the HIV-1 coreceptor CXCR4/fusin on various leukocyte subsets: rapid internalization and recycling upon activation. J. Immunol. 160: 1522-1531.
56. Thomas, S. Y., A. Banerji, B. D. Medoff, C. M. Lilly, and A. D. Luster. 2007. Multiple chemokine receptors, including CCR6 and CXCR3, regulate antigen-induced T cell homing to the human asthmatic airway. J. Immunol. 179: 1901-1912.
57. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387: 569-572.
58. Lin, S. L., C. W. Chien, C. L. Han, E. S. Chen, S. H. Kao, Y. J. Chen, and F. Liao. 2010. Temporal proteomics profiling of lipid rafts in CCR6-activated T cells reveals the integration of actin cytoskeleton dynamics. J. Proteome Res. 9: 283-297.