CCR6 has a non-redundant role in the development of inflammatory bowel disease

European Journal of Immunology

Volumn 33, Issue 10, 2003, Pages 2937-2946

  Varona, Rosa ^a   Cadenas, Vanesa ^a   Flores, Juana ^b   Martínez A , Carlos ^a   Márquez, Gabriel ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Chemokines; Inflammation; Knockout mice; Mucosa

Indexed keywords

CHEMOKINE RECEPTOR CCR6; CYTOKINE; DEXTRAN SULFATE; TRINITROBENZENESULFONIC ACID; BETA CHEMOKINE; CCL20 PROTEIN, HUMAN; CCR6 PROTEIN, HUMAN; CHEMOKINE RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENTERITIS; ENTEROPATHY; HISTOPATHOLOGY; HOMEOSTASIS; IMMUNE RESPONSE; IN VIVO STUDY; INTESTINE MUCOSA; LEUKOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; COLITIS; GENETICS; PHYSIOLOGY;

ANIMALS; CHEMOKINES, CC; COLITIS; CYTOKINES; DEXTRAN SULFATE; DISEASE SUSCEPTIBILITY; INFLAMMATORY BOWEL DISEASES; MACROPHAGE INFLAMMATORY PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; RECEPTORS, CHEMOKINE; RNA, MESSENGER; TRINITROBENZENESULFONIC ACID;

EID: 0242303557     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200324347     Document Type: Article

References (47)

1. Nagler-Anderson, C., Man the barrier! Strategic defences in the intestinal mucosa. Nat. Rev. Immunol. 2001. 1: 59-67.
2. Blumberg, R. S., Saubermann, L. J. and Strober, W., Animal models of mucosal inflammation and their relation to human inflammatory bowel disease. Curr. Opin. Immunol. 1999. 11: 648-656.
3. Murphy, P. M., Baggiolini, M., Charo, I. F., Hebert, C. A., Horuk, R., Matsushima, K., Miller, L. H., Oppenheim, J. J. and Power, C. A., International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol. Rev. 2000. 52: 145-176.
4. Zlotnik, A. and Yoshie, O., Chemokines: a new classification system and their role in immunity. Immunity 2000. 12: 121-127.
5. Moser, B. and Loetscher, P., Lymphocyte traffic control by chemokines. Nat. Immunol. 2001. 2: 123-128.
6. Ansel, K. M. and Cyster, J. G., Chemokines in lymphopoiesis and lymphoid organ development. Curr. Opin. Immunol. 2001. 13: 172-179.
7. Sallusto, F., Mackay, C. R. and Lanzavecchia, A., The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 2000. 18: 593-620.
8. Gerard, C. and Rollins, B. J., Chemokines and disease. Nat. Immunol. 2001. 2: 108-115.
9. Mazzucchelli, L., Hauser, C., Zgraggen, K., Wagner, H., Hess, M., Laissue, J. A. and Mueller, C., Expression of interleukin-8 gene in inflammatory bowel disease is related to the histological grade of active inflammation. Am. J. Pathol. 1994. 144: 997-1007.
10. Grimm, M. C., Elsbury, S. K., Pavli, P. and Doe, W. F., Enhanced expression and production of monocyte chemoattractant protein-1 in inflammatory bowel disease mucosa. J. Leukoc. Biol. 1996. 59: 804-812.
11. Keates, S., Keates, A. C., Mizoguchi, E., Bhan, A. and Kelly, C. P., Enterocytes are the primary source of the chemokine ENA-78 in normal colon and ulcerative colitis. Am. J. Physiol. 1997. 273: G75-G82.
12. Wedemeyer, J., Lorentz, A., Goke, M., Meier, P. N., Flemming, P., Dahinden, C. A., Marms, M. P. and Bischoff, S. C., Enhanced production of monocyte chemotactic protein 3 in inflammatory bowel disease mucosa. Gut 1999. 44: 629-635.
13. Mazzucchelli, L., Hauser, C., Zgraggen, K., Wagner, H. E., Hess, M. W., Laissue, J. A. and Mueller, C., Differential in situ expression of the genes encoding the chemokines MCP-1 and RANTES in human inflammatory bowel disease. J. Pathol. 1996. 178: 201-206.
14. Baba, M., Imai, T., Nishimura, M., Kakizaki, M., Takagi, S., Hieshima, K., Nomiyama, H. and Yoshie, O., Identification of CCR6, the specific receptor for a novel lymphocyte-directed CC chemokine LARC. J. Biol. Chem. 1997. 272: 14893-14898.
15. Liao, F., Alderson, R., Su, J., Ullrich, S. J., Kreider, B. L. and Farber, J. M., STRL22 is a receptor for the CC chemokine MIP-3α. Biochem. Biophys. Res. Commun. 1997. 236: 212-217.
16. Power, C. A., Church, D. J., Meyer, A., Alouani, S., Proudfoot, A. E., Clark, L. I., Sozzani, S., Mantovani, A. and Wells, T. N., Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3α from lung dendritic cells. J. Exp. Med. 1997. 186: 825-835.
17. Greaves, D. R., Wang, W., Dairaghi, D. J., Dieu, M. C., de Saint-Vis, B., Franz-Bacon, K., Rossi, D., Caux, C., McClanahan, T., Gordon, S., Zlotnik, A. and Schall, T. J., CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3α and is highly expressed in human dendritic cells. J. Exp. Med. 1997. 186: 837-844.
18. Rossi, D. L., Vicari, A. P., Franz, B. K., McClanahan, T. K. and Zlotnik, A., Identification through bioinformatics of two new macrophage proinflammatory human chemokines: MIP-3α and MIP-3β. J. Immunol. 1997. 158: 1033-1036.
19. Hromas, R., Gray, P. W., Chantry, D., Godiska, R., Krathwohl, M., Fife, K., Bell, G. I., Takeda, J., Aronica, S., Gordon, M., Cooper, S., Broxmeyer, H. E. and Klemsz, M. J., Cloning and characterization of exodus, a novel β-chemokine. Blood 1997. 89: 3315-3322.
20. Dieu-Nosjean, M. C., Vanbervliet, B., Vicari, A., Bridon, J. M., Oldham, E., Aït-Yahia, S., Briere, F., Zlotnik, A., Lebecque, S. and Caux, C., Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 1998. 188: 373-386.
21. Carramolino, L., Kremer, L., Goya, I., Varona, R., Buesa, J. M., Gutierrez, J., Zaballos, A., Martinez, A. C. and Marquez, G., Down-regulation of the β-chemokine receptor CCR6 in dendritic cells mediated by TNF-α and IL-4. J. Leukoc. Biol. 1999. 66: 837-844.
22. Liao, F., Rabin, R. L., Smith, C. S., Sharma, G., Nutman, T. B. and Farber, J. M., CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3α. J. Immunol. 1999. 162: 186-194.
23. Varona, R., Zaballos, A., Gutierrez, J., Martin, P., Roncal, F., Albar, J. P., Ardavin, C. and Marquez, G., Molecular cloning, functional characterization and mRNA expression analysis of the murine chemokine receptor CCR6 and its specific ligand MIP-3α. FEBS Lett. 1998. 440: 188-194.
24. Iwasaki, A. and Kelsall, B. L., Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J. Exp. Med. 2000. 191; 1381-1394.
25. Tanaka, Y., Imai, T., Baba, M., Ishikawa, I., Uehira, M., Nomiyama, H. and Yoshie, O., Selective expression of liver and activation-regulated chemokine (LARC) in intestinal epithelium in mice and humans. Eur. J. Immunol. 1999. 29: 633-642.
26. Izadpanah, A., Dwinell, M. B., Eckmann, L., Varki, N. M. and Kagnoff, M. F., Regulated MIP-3α/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. Gastrointest. Liver Physiol. 2001. 280: G710-G719.
27. Charbonnier, A. S., Kohrgruber, N., Kriehuber, E., Stingl, G., Rot, A. and Maurer, D., Macrophage inflammatory protein 3α is involved in the constitutive trafficking of epidermal Langerhans cells. J. Exp. Med. 1999. 190: 1755-1768.
28. Homey, B., Dieu-Nosjean, M. C., Wiesenborn, A., Massacrier, C., Pin, J. J., Oldham, E., Catron, D., Buchanan, M. E., Muller, A., deWaal Malefyt, R., Deng, G., Orozco, R., Ruzicka, T., Lehmann, P., Lebecque, S., Caux, C. and Zlotnik, A., Upregulation of macrophage inflammatory protein-3α/CCL20 and CC chemokine receptor 6 in psoriasis. J. Immunol. 2000. 164: 6621-6632.
29. Dieu-Nosjean, M. C., Massacrier, C., Homey, B., Vanbervliet, B., Pin, J. J., Vicari, A., Lebecque, S., Dezutter-Dambuyant, C., Schmitt, D., Zlotnik, A. and Caux, C., Macrophage inflammatory protein 3α is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J. Exp. Med. 2000. 192: 705-718.
30. Cook, D. N., Prosser, D. M., Forster, R., Zhang, J., Kuklin, N. A., Abbondanzo, S. J., Niu, X. D., Chen, S. C., Manfra, D. J., Wiekowski, M. T., Sullivan, L. M., Smith, S. R., Greenberg, H. B., Narula, S. K., Lipp, M. and Lira, S. A., CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 2000. 12: 495-503.
31. Varona, R., Villares, R., Carramolino, L., Goya, I. I., Zaballos, A. A., Gutierrez, J., Torres, M., Martinez, A. C. and Marquez, G., CCR6-deficient mice have impaired leukocyte homeostasis and altered contact hypersensitivity and delayed-type hypersensitivity responses. J. Clin. Invest. 2001. 107: R37-R45.
32. Strober, W., Fuss, I. J. and Blumberg, R. S., The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 2002. 20: 495-549.
33. Okayasu, I., Hatakeyama, S., Yamada, M., Ohkusa, T., Inagaki, Y. and Nakaya, R., A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990. 98: 694-702.
34. Elson, C. O., Beagley, K. W., Sharmanov, A. T., Fujihashi, K., Kiyono, H., Tennyson, G. S., Cong, Y., Black, C. A., Ridwan, B. W. and McGhee, J. R., Hapten-induced model of murine inflammatory bowel disease: mucosa immune responses and protection by tolerance. J. Immunol. 1996. 157: 2174-2185.
35. Bhan, A. K., Mizoguchi, E., Smith, R. N. and Mizoguchi, A., Colitis in transgenic and knockout animals as models of human inflammatory bowel disease. Immunol. Rev. 1999. 169: 195-207.
36. + lymphocyte-associated Th2-type immune response in the intestine. J. Immunol. 2000. 164: 6303-6312.
37. Dieleman, L. A., Palmen, M. J., Akol, H., Bloemena, E., Pena, A. S., Meuwissen, S. G. and Van Rees, E. P., Chronic-experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin. Exp. Immunol. 1998. 114: 385-391.
38. Strober, W., Ludviksson, B. R. and Fuss, I. J., The pathogenesis of mucosal inflammation in murine models of inflammatory bowel disease and Crohn disease. Ann. Intern. Med. 1998. 128: 848-856.
39. Lentsch, A. B., Shanley, T. P., Sarma, V. and Ward, P. A., In vivo suppression of NF-κB and preservation of IκB alpha by interleukin-10 and interleukin-13. J. Clin. Invest. 1997. 100: 2443-2448.
40. + Th1- like responses. J. Clin. Invest. 1996. 98: 1010-1020.
41. Bouma, G., Kaushiva, A. and Strober, W., Experimental murine colitis is regulated by two genetic loci, including one on chromosome 11 that regulates IL-12 responses. Gastroenterology 2002. 123: 554-565.
42. Dohi, T., Fujihashi, K., Kiyono, H., Elson, C. O. and McGhee, J. R., Mice deficient in Th1- and Th2-type cytokines develop distinct forms of hapten-induced colitis. Gastroenterology 2000. 119: 724-733.
43. high T cells. Eur. J. Immunol. 2001. 31: 1465-1474.
44. Pitman, R. S. and Blumberg, R. S., First line of defense: the role of the intestinal epithelium as an active component of the mucosal immune system. J. Gastroenterol. 2000. 35: 805-814.
45. Mashimo, H., Wu, D. C., Podolsky, D. K. and Fishman, M. C., Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 1996. 274: 262-265.
46. Neurath, M. F., Fuss, I., Kelsall, B. L., Stuber, E. and Strober, W., Antibodies to interleukin 12 abrogate established experimental colitis in mice. J. Exp. Med. 1995. 182: 1281-1290.
47. Higuchi, R., Fockler, C., Dollinger, G. and Watson, R., Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology (NY) 1993. 11: 1026-1030.