Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing

Journal of Experimental Medicine

Volumn 202, Issue 8, 2005, Pages 1063-1073

  Johansson Lindbom, Bengt ^a   Svensson, Marcus ^a   Pabst, Oliver ^b   Palmqvist, Caroline ^a   Marquez, Gabriel ^c   Förster, Reinhold ^b   Agace, William W ^a  

^a LUND UNIVERSITY   (Sweden)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; ALPHA4 BETA7 INTEGRIN; CD103 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR9; GAMMA INTERFERON; LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; EFFECTOR CELL; IMMUNOREGULATION; INTERFERON PRODUCTION; INTESTINE EPITHELIUM; INTESTINE LYMPHATIC TISSUE; LAMINA PROPRIA; LYMPHOCYTE HOMING; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MESENTERY LYMPH NODE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE ACTIVATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL MOVEMENT; DENDRITIC CELLS; FLOW CYTOMETRY; INTEGRIN ALPHA CHAINS; INTERFERON TYPE II; INTESTINAL MUCOSA; LYMPHOCYTE SUBSETS; LYMPHOID TISSUE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CHEMOKINE;

EID: 26844538936     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20051100     Document Type: Article

References (40)

1. Kunkel, E.J., and E.C. Butcher. 2002. Chemokines and the tissue-specific migration of lymphocytes. Immunity. 16:1-4.
2. + T cells activated in cutaneous or mucosal lymphoid tissues. J. Exp. Med. 195:135-141.
3. Svensson, M., J. Marsal, A. Ericsson, L. Carramolino, T. Broden, G. Marquez, and W.W. Agace. 2002. CCL25 mediates the localization of recently activated CD8alphabeta(+) lymphocytes to the small-intestinal mucosa. J. Clin. Invest. 110:1113-1121.
4. Calzascia, T., F. Masson, W. Di Berardino-Besson, E. Contassot, R. Wilmotte, M. Aurrand-Lions, C. Ruegg, P.Y. Dietrich, and P.R. Walker. 2005. Homing phenotypes of tumor-specific CD8 T cells are predetermined at the tumor site by crosspresenting APCs. Immunity. 22:175-184.
5. Johansson-Lindbom, B., M. Svensson, M.-A. Wurbel, B. Malissen, G. Márquez, and W. Agace. 2003. Selective generation of gut-tropic T cells in gut-associated lymphoid tissue (GALT); requirement for GALT dendritic cells and adjuvant. J. Exp. Med. 198:963-969.
6. Lefrancois, L., C.M. Parker, S. Olson, W. Muller, N. Wagner, M.P. Schon, and L. Puddington. 1999. The role of β7 integrins in CD8 T cell trafficking during an antiviral immune response. J. Exp. Med. 189:1631-1638.
7. Dudda, J.C., J.C. Simon, and S. Martin. 2004. Dendritic cell immunization route determines CD8+ T cell trafficking to inflamed skin: role for tissue microenvironment and dendritic cells in establishment of T cell-homing subsets. J. Immunol. 172:857-863.
8. Reiss, Y., A.E. Proudfoot, C.A. Power, J.J. Campbell, and E.C. Butcher. 2001. CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J. Exp. Med. 194:1541-1547.
9. Tietz, W., Y. Allemand, E. Borges, D. von Laer, R. Hallmann, D. Vestweber, and A. Hamann. 1998. CD4+ T cells migrate into inflamed skin only if they express ligands for E- and P-selectin. J. Immunol. 161:963-970.
10. 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.
11. Mora, J.R., M.R. Bono, N. Manjunath, W. Weninger, L.L. Cavanagh, M. Rosemblatt, and U.H. von Andrian. 2003. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature. 424:88-93.
12. Stagg, A.J., M.A. Kamm, and S.C. Knight. 2002. Intestinal dendritic cells increase T cell expression of alpha4beta7 integrin. Eur. J. Immunol. 32:1445-1454.
13. Iwata, M., A. Hirakiyama, Y. Eshima, H. Kagechika, C. Kato, and S.Y. Song. 2004. Retinoic acid imprints gut-homing specificity on T cells. Immunity. 21:527-538.
14. Mora, J.R., G. Cheng, D. Picarella, M. Briskin, N. Buchanan, and U.H. von Andrian. 2005. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J. Exp. Med. 201:303-316.
15. Mowat, A.M. 2005. Dendritic cells and immune responses to orally administered antigens. Vaccine. 23:1797-1799.
16. Anjuere, F., C. Luci, M. Lebens, D. Rousseau, C. Hervouet, G. Milon, J. Holmgren, C. Ardavin, and C. Czerkinsky. 2004. In vivo adjuvant-induced mobilization and maturation of gut dendritic cells after oral administration of cholera toxin. J. Immunol. 173:5103-5111.
17. MacPherson, G.G., S. Fossum, and B. Harrison. 1989. Properties of lymph-borne (veiled) dendritic cells in culture. II. Expression of the IL-2 receptor: role of GM-CSF. Immunology. 68:108-113.
18. Turnbull, E.L., U. Yrlid, C.D. Jenkins, and G.G. Macpherson. 2005. Intestinal dendritic cell subsets: differential effects of systemic TLR4 stimulation on migratory fate and activation in vivo. J. Immunol. 174:1374-1384.
19. Brenan, M., and M. Puklavec. 1992. The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J. Exp. Med. 175:1457-1465.
20. Kilshaw, P.J. 1993. Expression of the mucosal T cell integrin alpha M290 beta 7 by a major subpopulation of dendritic cells in mice. Eur. J. Immunol. 23:3365-3368.
21. Ericsson, A., M. Svensson, A. Arya, and W.W. Agace. 2004. CCL25/CCR9 promotes the induction and function of CD103 on intestinal intraepithelial lymphocytes. Eur. J. Immunol. 34:2720-2729.
22. Martin, P., S.R. Ruiz, G.M. del Hoyo, F. Anjuere, H.H. Vargas, M. Lopez-Bravo, and C. Ardavin. 2002. Dramatic increase in lymph node dendritic cell number during infection by the mouse mammary tumor virus occurs by a CD62L-dependent blood-borne DC recruitment. Blood. 99:1282-1288.
23. Lutz, M.B., and G. Schuler. 2002. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 23:445-449.
24. Stoitzner, P., S. Holzmann, A.D. McLellan, L. Ivarsson, H. Stossel, M. Kapp, U. Kammerer, P. Douillard, E. Kampgen, F. Koch, et al. 2003. Visualization and characterization of migratory Langerhans cells in murine skin and lymph nodes by antibodies against Langerin/CD207. J. Invest. Dermatol. 120:266-274.
25. Ohl, L., M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, and R. Forster. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 21:279-288.
26. Forster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Muller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 99:23-33.
27. Schluns, K.S., W.C. Kieper, S.C. Jameson, and L. Lefrancois. 2000. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat. Immunol. 1:426-432.
28. Zhang, X., S. Sun, I. Hwang, D.F. Tough, and J. Sprent. 1998. Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity. 8:591-599.
29. Bimczok, D., E.N. Sowa, H. Faber-Zuschratter, R. Pabst, and H.J. Rothkotter. 2005. Site-specific expression of CD11b and SIRPalpha (CD172a) on dendritic cells: implications for their migration patterns in the gut immune system. Eur. J. Immunol. 35:1418-1427.
30. Pabst, O., H. Herbrand, T. Worbs, M. Friedrichsen, S. Yan, M.W. Hoffmann, H. Korner, G. Bernhardt, R. Pabst, and R. Forster. 2005. Cryptopatches and isolated lymphoid follicles: dynamic lymphoid tissues dispensable for the generation of intraepithelial lymphocytes. Eur. J. Immunol. 35:98-107.
31. Cerf-Bensussan, N., A. Jarry, N. Brousse, B. Lisowska-Grospierre, D. Guy-Grand, and C. Griscelli. 1987. A monoclonal antibody (HML-1) defining a novel membrane molecule present on human intestinal lymphocytes. Eur. J. Immunol. 17:1279-1285.
32. Kilshaw, P.J., and S.J. Murant. 1990. A new surface antigen on intraepithelial lymphocytes in the intestine. Eur. J. Immunol. 20:2201-2207.
33. Cepek, K.L., S.K. Shaw, C.M. Parker, G.J. Russell, J.S. Morrow, D.L. Rimm, and M.B. Brenner. 1994. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha(E)beta(7) integrin. Nature. 372:190-193.
34. + T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease. J. Exp. Med. 201:1647-1657.
35. Barnard, J.A., G.J. Warwick, L.I. Gold, Y.H. Chin, J.P. Cai, and X.M. Xu. 1993. Localization of transforming growth factor beta isoforms in the normal murine small intestine and colon. Gastroenterology. 105:67-73.
36. Dudda, J.C., A. Lembo, E. Bachtanian, J. Huehn, C. Siewert, A. Hamann, E. Kremmer, R. Forster, and S.F. Martin. 2005. Dendritic cells govern induction and reprogramming of polarized tissue-selective homing receptor patterns of T cells: important roles for soluble factors and tissue microenvironments. Eur. J. Immunol. 35:1056-1065.
37. Malmstrom, V., D. Shipton, B. Singh, A. Al-Shamkhani, M.J. Puklavec, A.N. Barclay, and F. Powrie. 2001. CD134L expression on dendritic cells in the mesenteric lymph nodes drives colitis in T cell-restored SCID mice. J. Immunol. 166:6972-6981.
38. Fillatreau, S., and D. Gray. 2003. T cell accumulation in B cell follicles is regulated by dendritic cells and is independent of B cell activation. J. Exp. Med. 197:195-206.
39. Huang, F.P., N. Platt, M. Wykes, J.R. Major, T.J. Powell, C.D. Jenkins, and G.G. MacPherson. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191:435-444.
40. Carramolino, L., A. Zaballos, L. Kremer, R. Villares, P. Martin, C. Ardavin, A.C. Martinez, and G. Marquez. 2001. Expression of CCR9 beta-chemokine receptor is modulated in thymocyte differentiation and is selectively maintained in CD8(+) T cells from secondary lymphoid organs. Blood. 97:850-857.