The role of CD103+ dendritic cells in the intestinal mucosal immune system

Frontiers in Immunology

Volumn 2, Issue JUL, 2011, Pages

  Ruane, Darren Thomas ^a   Lavelle, Ed C ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

CD103+ dendritic cells; Dendritic cells; Intestine

Indexed keywords

EID: 84874042768     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2011.00025     Document Type: Article

References (48)

1. Annacker, O., Coombes, J. L., Malm-strom, V., Uhlig, H. H., Bourne, T., Johansson-Lindbom, B., Agace, W. W., Parker, C. M., and Powrie, F. (2005). Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202, 1051-1061.
2. Atarashi, K., Nishimura, J., Shima, T., Umesaki, Y., Yamamoto, M., Onoue, M., Yagita, H., Ishii, N., Evans, R., Honda, K., and Takeda, K. (2008). ATP drives lamina propria T(H)17 cell differentiation. Nature 455,808-812.
3. Azizi, A., Kumar, A., Diaz-Mitoma, F., and Mestecky, J. (2010). Enhancing oral vaccine potency by targeting intestinal M cells. PLoS Pathog. 6, e1001147. doi: 10.1371/jour-nal.ppat.1001147
4. Beitnes, A. C., Raki, M., Lundin, K. E., Jahnsen, J., Sollid, L. M., and Jahnsen, F. L. (2011). Density of CD163(+) CD11c(+) dendritic cells increases and CD103(+) dendritic cells decreases in the coeliac lesion. Scand. J. Immunol. doi: 10.1111/j.1365-3083.2011.02549.x
5. Bluestone, J.A., and Abbas,A.K. (2003). Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3, 253-257.
6. Bogunovic, M., Ginhoux, F., Helft, J., Shang, L., Hashimoto, D., Greter, M., Liu, K., Jakubzick, C., Ingersoll, M. A., Leboeuf, M., Stanley, E. R., Nussenzweig, M., Lira, S. A., Randolph, G. J, and Merad, M. (2009). Origin of the lamina propria dendritic cell network. Immunity 31, 513-525.
7. Cepek, K. L., Shaw, S. K., Parker, C. M., Russell, G. J., Morrow, J. S., Rimm, D. L., and Brenner, M. B. (1994). Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372, 190-193.
8. Cerf-Bensussan, N., Jarry, A., Brousse, N., Lisowska-Grospierre, B., Guy-Grand, D., and Griscelli, C. (1987). A monoclonal antibody (HML-1) defining a novel membrane molecule present on human intestinal lymphocytes. Eur. J. Immunol. 17, 1279-1285.
9. Coombes, J. L., Siddiqui, K. R., Arancibia-Cárcamo, C. V., Hall, J., Sun, C. M., Belkaid, Y., and Powrie, F. (2007). A functionally specialized population of mucosal CD 103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764.
10. Cozzo, C., Larkin, J. III, and Caton, A. J. (2003). Cutting edge: self-peptides drive the peripheral expansion of CD4+CD25+ regulatory T cells. J. Immunol. 171, 5678-5682.
11. del Rio, M. L., Bernhardt, G., Rodriguez-Barbosa, J. I., and Förster, R. (2010). Development and functional specialization of CD 103+ dendritic cells. Immunol. Rev. 234, 268-281.
12. del Rio, M. L., Rodriguez-Barbosa, J. I., Bölter, J., Ballmaier, M., Dittrich-Breiholz, O., Kracht, M., Jung, S., and Förster, R. (2008). CX3CR1+ c-kit+ bone marrow cells give rise to CD 103+ and CD 103-dendritic cells with distinct functional properties. J. Immunol. 181, 6178-6188.
13. Dustin, M. L., Garcia-Aguilar, J., Hibbs, M. L., Larson, R. S., Stacker, S. A., Staunton, D. E., Wardlaw, A. J., and Springer, T. A. (1989). Structure and regulation of the leukocyte adhesion receptor LFA-1 and its coun-terreceptors, ICAM-1 and ICAM-2. Cold Spring Harb. Symp. Quant. Biol. 54(Pt 2), 753-765.
14. Fontenot, J. D., Gavin, M. A., and Rudensky, A. Y. (2003). Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330-336.
15. Galan, J. E., and Curtiss, R. III. (1989). Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. U.S.A. 86, 6383-6387.
16. Garba, M. L., Pilcher, C. D., Bing-ham, A. L., Eron, J., and Frelinger, J. A. (2002). HIV antigens can induce TGF-beta(1)-producing immunoregulatory CD8+ T cells. J. Immunol. 168,2247-2254.
17. Gebert, A., Goke, M., Rothkötter, H. J., and Dietrich, C. E (2000). The mechanisms of antigen uptake in the small and large intestines: the roll of the M cells for the initiation of immune responses. Z. Gastroenterol. 38,855-872.
18. Ginhoux, F., Tacke, F., Angeli, V., Bogunovic, M., Loubeau, M., Dai, X. M., Stanley, E. R., Randolph, G. J., and Merad, M. (2006). Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7, 265-273.
19. Haynes, L. M., Vanderlugt, C. L., Dal Canto, M. C., Melvold, R. W., and Miller, S. D. (2000). CD8(+) T cells from Theiler's virus-resistant BALB/cByJ mice downregulate pathogenic virus-specific CD4(+) T cells. J. Neuroimmunol. 106,43-52.
20. Helft, J., Ginhoux, F., Bogunovic, M., and Merad, M. (2010). Origin and functional heterogeneity of non-lymphoid tissue dendritic cells in mice. Immunol Rev. 234, 55-75.
21. Iliev, I. D., Mileti, E., Matteoli, G., Chieppa, M., and Rescigno, M. (2009). Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2, 340-350.
22. Iwata, M., Hirakiyama, A., Eshima, Y., Kagechika, H., Kato, C., and Song, S. Y. (2004). Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538.
23. Jaensson, E., Uronen-Hansson, H., Pabst, O., Eksteen, B., Tian, J., Coombes, J. L., Berg, P. L., Davids-son, T., Powrie, F., Johansson-Lindbom, B., and Agace, W. W. (2008). Small intestinal CD 103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205,2139-2149.
24. Jaensson-Gyllenback, E., Kotarsky, K., Zapata, F., Persson, E. K., Gunder-sen, T. E., Blomhoff, R., and Agace, W. W. (2011). Bile retinoids imprint intestinal CD103(+) dendritic cells with the ability to generate gut-tropic T cells. Mucosal Immunol 4, 438-447.
25. Johansson-Lindbom, B., Svensson, M., Pabst, O., Palmqvist, C., Marquez, G., Förster, R., and Agace, W. W. (2005). Functional specialization of gut CD 103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202, 1063-1073.
26. Kelsall, B. (2008). Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunol. 1,460-469.
27. Kilshaw, P. J., and Murant, S. J. (1990). A new surface antigen on intraepithe-lial lymphocytes in the intestine. Eur. J. Immunol. 20,2201-2207.
28. Laffont, S., Siddiqui, K. R., and Powrie, F. (2010). Intestinal inflammation abrogates the tolerogenic properties of MLN CD103+ dendritic cells. Eur. J. Immunol. 40,1877-1883.
29. Lehmann, J., Huehn, J., de la Rosa, M., Maszyna, F., Kretschmer, U, Krenn, V., Brunner, M., Scheffold, A., and Hamann, A. (2002). Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25- regulatory T cells. Proc. Natl. Acad. Sci. U.S.A. 99, 13031-13036.
30. Matteoli, G., Mazzini, E., Iliev, I. D., Mileti, E., Fallarino, F., Puc-cetti, P., Chieppa, M., and Rescigno, M. (2010). Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T reg-ulatory/T effector cell balance and oral tolerance induction. Gut 59, 595-604.
31. Merad, M., and Manz, M. G. (2009). Dendritic cell homeostasis. Blood 113,3418-3427.
32. Mills, K. H. (2004). Regulatory T cells: friend or foe in immunity to infection? Nat. Rev. Immunol. 4, 841-855.
33. Niess, J. H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B. A., Vyas, J. M., Boes, M., Ploegh, H. L., Fox, J. G., Littman, D. R., and Reinecker, H. C. (2005). CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307,254-258.
34. Powrie, F., Carlino, J., Leach, M. W., Mauze, S., and Coffman, R. L. (1996). A critical role for transforming growth factor-beta but not inter-leukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 183,2669-2674.
35. Rescigno, M., and Di Sabatino, A. (2009). Dendritic cells in intestinal homeostasis and disease. J. Clin. Invest. 119,2441-2450.
36. Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J. P., and Ricciardi-Castagnoli, P. (2001). Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367.
37. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., and Toda, M. (1995). Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155,1151-1164.
38. Schlickum, S., Sennefelder, H., Friedrich, M., Harms, G., Lohse, M. J., Kilshaw, P., and Schön, M. P. (2008). Integrin alpha E(CD103)beta 7 influences cellular shape and motility in a ligand-dependent fashion. Blood 112, 619-625.
39. Schulz, O., Jaensson, E., Persson, E. K., Liu, X., Worbs, T., Agace, W. W., and Pabst, O. (2009). Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 206, 3101-3114.
40. Shimizu, J., Yamazaki, S., Takahashi, T., Ishida, Y., and Sakaguchi, S. (2002). Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3, 135-142.
41. Springer, T. A. (1994). Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76,301-314.
42. Springer, T. A. (1995). Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu. Rev. Physiol. 57, 827-872.
43. Steinman, R. M., and Cohn, Z. A. (1973). Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantita-tion, tissue distribution. J. Exp. Med. 137, 1142-1162.
44. Strauch, U. G., Grunwald, N., Ober-meier, F., Gürster, S., and Rath, H. C. (2010). Loss of CD103+ intestinal dendritic cells during colonic inflammation. World J. Gastroenterol. 16,21-29.
45. Uss, E., Rowshani, A. T., Hooibrink, B., Lardy, N. M., van Lier, R. A., and Ten Berge, I. J. (2006). CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J. Immunol. 177,2775-2783.
46. Varol, C., Vallon-Eberhard, A., Eli-nav, E., Aychek, T., Shapira, Y., Luche, H., Fehling, H. J., Hardt, W. D., Shakhar, G., and Jung, S. (2009). Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502-512.
47. Worbs, T., and Bode, U., Yan, S., Hoffmann, M. W., Hintzen, G., Bern-hardt, G., Förster, R., and Pabst, O. (2006). Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203, 519-527.
48. Wright, J. R. (2005). Immunoregula-tory functions of surfactant proteins. Nat. Rev. Immunol. 5, 58-68.