Migratory conventional dendritic cells in the induction of peripheral T cell tolerance

Journal of Leukocyte Biology

Volumn 94, Issue 5, 2013, Pages 903-911

  Broggi, Achille ^a   Zanoni, Ivan ^a   Granucci, Francesca ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Lamina propria; Mesenteric lymph nodes; Retinoic acid; Skindraining lymph nodes

Indexed keywords

CD11B ANTIGEN; CD8 ANTIGEN; LANGERIN;

BARE LYMPHOCYTE SYNDROME; CELL POPULATION; DENDRITIC CELL; DISEASE COURSE; HOMEOSTASIS; HUMAN; IMMUNOLOGICAL TOLERANCE; INFECTION; INTESTINE; LANGERHANS CELL; LUNG; LYMPH NODE; LYMPHOCYTE MIGRATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKIN; STEADY STATE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

LAMINA PROPRIA; MESENTERIC LYMPH NODES; RETINOIC ACID; SKIN-DRAINING LYMPH NODES;

ANIMALS; ANTIGENS, CD; CELL MOVEMENT; DENDRITIC CELLS; HUMANS; IMMUNE TOLERANCE; INTEGRIN ALPHA CHAINS; LUNG; SKIN; T-LYMPHOCYTES;

EID: 84887008246     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0413222     Document Type: Review

References (60)

1. Villadangos, J., Schnorrer, P. (2007) Intrinsic and cooperative antigen presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7, 543-555.
2. Villadangos, J., Heath, W. (2005) Life cycle, migration and antigen presenting functions of spleen and lymph node dendritic cells: limitations of the Langerhans cells paradigm. Semin. Immunol. 17, 262-272.
3. Shortman, K., Naik, S. (2007) Steady-state and inflammatory dendritic cell development. Nat. Rev. Immunol. 7, 19-30.
4. Coombes, J., Powrie, F. (2008) Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8, 435-446.
5. Pugh, C., MacPherson, G., Steer, H. (1983) Characterization of nonlymphoid cells derived from rat peripheral lymph. J. Exp. Med. 157, 1758-1779.
6. Huang, F., Platt, N., Wykes, M., Major, J., Powell, T., Jenkins, C., MacPherson, G. (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.
7. Jaensson, E., Uronen-Hansson, H., Pabst, O., Eksteen, B., Tian, J., Coombes, J., Berg, P.-L., Davidsson, T., Powrie, F., Johansson-Lindbom, B., Agace, W. (2008) Small intestinal CD103 dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205, 2139-2149.
8. Schulz, O., Jaensson, E., Persson, E., Liu, X., Worbs, T., Agace, W., 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.
9. Bogunovic, M., Ginhoux, F., Helft, J., Shang, L., Hashimoto, D., Greter, M., Liu, K., Jakubzick, C., Ingersoll, M., Leboeuf, M., Stanley, E., Nussenzweig, M., Lira, S., Randolph, G., Merad, M. (2009) Origin of the lamina propria dendritic cell network. Immunity. 31, 513-525.
10. Persson, E., Jaensson, E., Agace, W. (2010) The diverse ontogeny and function of murine small intestinal dendritic cell/macrophage subsets. Immunobiology. 215, 692-697.
11. Worbs, T., Bode, U., Yan, S., Hoffmann, M., Hintzen, G., Bernhardt, G., Förster, R., 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.
12. Jang, M., Sougawa, N., Tanaka, T., Hirata, T., Hiroi, T., Tohya, K., Guo, Z., Umemoto, E., Ebisuno, Y., Yang, B.-G., Seoh, J.-Y., Lipp, M., Kiyono, H., Miyasaka, M. (2006) CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J. Immunol. 176, 803-810.
13. Johansson-Lindbom, B., Svensson, M., Pabst, O., Palmqvist, C., Marquez, G., Förster, R., Agace, W. (2005) Functional specialization of gut CD103 dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202, 1063-1073.
14. Schulz, O., Pabst, O. (2013) Antigen sampling in the small intestine. Trends. Immunol. 34, 155-161.
15. Farache, J., Koren, I., Milo, I., Gurevich, I., Kim, K.-W., Zigmond, E., Furtado, G., Lira, S., Shakhar, G. (2013) Luminal bacteria recruit CD103() dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 38, 581-595.
16. Wilson, N., Young, L., Kupresanin, F., Naik, S., Vremec, D., Heath, W., Akira, S., Shortman, K., Boyle, J., Maraskovsky, E., Belz, G., Villadangos, J. (2008) Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol. Cell biol. 86, 200-205.
17. McDole, J. R., Wheeler, L. W., McDonald, K. G., Wang, B., Konjufca, V., Knoop, K. A., Newberry, R. D., Miller, M. J. (2012) Goblet cells deliver luminal antigen to CD103 dendritic cells in the small intestine. Nature 483, 345-349.
18. Sun, C.-M., Hall, J., Blank, R., Bouladoux, N., Oukka, M., Mora, J., Belkaid, Y. (2007) Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785.
19. Coombes, J., Siddiqui, K. R., Arancibia-Cárcamo, C., Hall, J., Sun, C.-M., Belkaid, Y., Powrie, F. (2007) A functionally specialized population of mucosal CD103 DCs induces Foxp3 regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764.
20. Semmrich, M., Plantinga, M., Svensson-Frej, M., Uronen-Hansson, H., Gustafsson, T., Mowat, A., Yrlid, U., Lambrecht, B., Agace, W. (2012) Directed antigen targeting in vivo identifies a role for CD103 dendritic cells in both tolerogenic and immunogenic T cell responses. Mucosal. Immunol. 5, 150-160.
21. Vitali, C., Mingozzi, F., Broggi, A., Barresi, S., Zolezzi, F., Bayry, J., Raimondi, G., Zanoni, I., Granucci, F. (2012) Migratory, and not lymphoidresident, dendritic cells maintain peripheral self-tolerance and prevent autoimmunity via induction of iTreg cells. Blood 120, 1237-1245.
22. Abbas, A., Benoist, C., Bluestone, J., Campbell, D., Ghosh, S., Hori, S., Jiang, S., Kuchroo, V., Mathis, D., Roncarolo, M., Rudensky, A., Sakaguchi, S., Shevach, E., Vignali, D. A., Ziegler, S. (2013) Regulatory T cells: recommendations to simplify the nomenclature. Nat. Immunol. 14, 307-308.
23. Bain, C. C., Mowat, A. M. (2011) Intestinal macrophages: specialized adaptation to a unique environment. Eur. J. Immunol. 41, 2494-2498.
24. Paidassi, H., Acharya, M., Zhang, A., Mukhopadhyay, S., Kwon, M., Chow, C., Stuart, L. M., Savill, J., Lacy-Hulbert, A. (2011) Preferential expression of integrin alphavbeta8 promotes generation of regulatory T cells by mouse CD103 dendritic cells. Gastroenterology 141, 1813-1820.
25. Travis, M. A., Reizis, B., Melton, A. C., Masteller, E., Tang, Q., Proctor, J. M., Wang, Y., Bernstein, X., Huang, X., Reichardt, L. F., Bluestone, J. A., Sheppard, D. (2007) Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature 449, 361-365.
26. Mucida, D., Park, Y., Kim, G., Turovskaya, O., Scott, I., Kronenberg, M., Cheroutre, H. (2007) Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317, 256-260.
27. Iwata, M., Hirakiyama, A., Eshima, Y., Kagechika, H., Kato, C., Song, S.-Y. (2004) Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538.
28. Cerovic, V., Houston, S., Scott, C., Aumeunier, A., Yrlid, U., Mowat, A., Milling, S. (2013) Intestinal CD103() dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 6, 104-113.
29. Denning, T., Norris, B., Medina-Contreras, O., Manicassamy, S., Geem, D., Madan, R., Karp, C., Pulendran, B. (2011) Functional specializations of intestinal dendritic cell and macrophage subsets that control Th17 and regulatory T cell responses are dependent on the T cell/APC ratio, source of mouse strain, and regional localization. J Immunol. 187, 733-747.
30. Guilliams, M., Crozat, K., Henri, S., Tamoutounour, S., Grenot, P., Devilard, E., de Bovis, B., Alexopoulou, L., Dalod, M., Malissen, B. (2010) Skin-draining lymph nodes contain dermis-derived CD103(-) dendritic cells that constitutively produce retinoic acid and induce Foxp3() regulatory T cells. Blood 115, 1958-1968.
31. Persson, E., Uronen-Hansson, H., Semmrich, M., Rivollier, A., Hägerbrand, K., Marsal, J., Gudjonsson, S., Håkansson, U., Reizis, B., Kotarsky, K., Agace, W. (2013) IRF4 transcription-factor-dependent CD103()CD11b() dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38, 958-969.
32. Jaensson-Gyllenbäck, E., Kotarsky, K., Zapata, F., Persson, E., Gundersen, T., Blomhoff, R., Agace, W. (2011) Bile retinoids imprint intestinal CD103 dendritic cells with the ability to generate gut-tropic T cells. Mucosal Immunol. 4, 438-447.
33. Villablanca, E. J., Wang, S., de Calisto, J., Gomes, D. C., Kane, M. A., Napoli, J. L., Blaner, W. S., Kagechika, H., Blomhoff, R., Rosemblatt, M., Bono, M. R., von Andrian, U. H., Mora, J. R. (2011) MyD88 and retinoic acid signaling pathways interact to modulate gastrointestinal activities of dendritic cells. Gastroenterology 141, 176-185.
34. Molenaar, R., Knippenberg, M., Goverse, G., Olivier, B. J., de Vos, A. F., O'Toole, T., Mebius, R. E. (2011) Expression of retinaldehyde dehydrogenase enzymes in mucosal dendritic cells and gut-draining lymph node stromal cells is controlled by dietary vitamin A. J. Immunol. 186, 1934-1942.
35. Hadis, U., Wahl, B., Schulz, O., Hardtke-Wolenski, M., Schippers, A., Wagner, N., Müller, W., Sparwasser, T., Förster, R., Pabst, O. (2011) Intestinal tolerance requires gut homing and expansion of FoxP3 regulatory T cells in the lamina propria. Immunity 34, 237-246.
36. Cassani, B., Villablanca, E. J., Quintana, F. J., Love, P. E., Lacy-Hulbert, A., Blaner, W. S., Sparwasser, T., Snapper, S. B., Weiner, H. L., Mora, J. R. (2011) Gut-tropic T cells that express integrin alpha4beta7 and CCR9 are required for induction of oral immune tolerance in mice. Gastroenterology 141, 2109-2118.
37. Guilliams, M., Henri, S., Tamoutounour, S., Ardouin, L., Schwartz-Cornil, I., Dalod, M., Malissen, B. (2010) From skin dendritic cells to a simplified classification of human and mouse dendritic cell subsets. Eur. J. Immunol. 40, 2089-2094.
38. Henri, S., Poulin, L., Tamoutounour, S., Ardouin, L., Guilliams, M., de Bovis, B., Devilard, E., Viret, C., Azukizawa, H., Kissenpfennig, A., Malissen, B. (2010) CD207 CD103 dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207, 189-206.
39. Idoyaga, J., Fiorese, C., Zbytnuik, L., Lubkin, A., Miller, J., Malisen, B., Mucida, D., Merad, M., Steinman, R. (2013) Specialized role of migratory dendritic cells in peripheral tolerance induction. J. Clin. Invest. 123, 844-854.
40. Ohl, L., Mohaupt, M., Czeloth, N., Hintzen, G., Kiafard, Z., Zwirner, J., Blankenstein, T., Henning, G., Förster, R. (2004) CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 21, 279-288.
41. Bedoui, S., Whitney, P., Waithman, J., Eidsmo, L., Wakim, L., Caminschi, I., Allan, R., Wojtasiak, M., Shortman, K., Carbone, F., Brooks, A., Heath, W. (2009) Cross-presentation of viral and self antigens by skinderived CD103 dendritic cells. Nat. Immunol. 10, 488-495.
42. Azukizawa, H., Döhler, A., Kanazawa, N., Nayak, A., Lipp, M., Malissen, B., Autenrieth, I., Katayama, I., Riemann, M., Weih, F., BerberichSiebelt, F., Lutz, M. (2011) Steady state migratory RelB langerin dermal dendritic cells mediate peripheral induction of antigen-specific CD4 CD25 Foxp3 regulatory T cells. Eur. J. Immunol. 41, 1420-1434.
43. Hemmi, H., Idoyaga, J., Suda, K., Suda, N., Kennedy, K., Noda, M., Aderem, A., Steinman, R. (2009) A new triggering receptor expressed on myeloid cells (Trem) family member, Trem-like 4, binds to dead cells and is a DNAX activation protein 12-linked marker for subsets of mouse macrophages and dendritic cells. J. Immunol. 182, 1278-1286.
44. Rosenblum, M., Gratz, I., Paw, J., Lee, K., Marshak-Rothstein, A., Abbas, A. (2011) Response to self antigen imprints regulatory memory in tissues. Nature 480, 538-542.
45. Gomez de Agüero, M., Vocanson, M., Hacini-Rachinel, F., Taillardet, M., Sparwasser, T., Kissenpfennig, A., Malissen, B., Kaiserlian, D., Dubois, B. (2012) Langerhans cells protect from allergic contact dermatitis in mice by tolerizing CD8()TcellsandactivatingFoxp3() regulatory T cells. J. Clin. Invest. 122, 1700-1711.
46. Del Rio, M.-L., Bernhardt, G., Rodriguez-Barbosa, J.-I., Förster, R. (2010) Development and functional specialization of CD103 dendritic cells. Immunol. Rev. 234, 268-281.
47. Del Rio, M.-L., Rodriguez-Barbosa, J.-I., Kremmer, E., Förster, R. (2007) CD103 and CD103 bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4 and CD8 T cells. J. Immunol. 178, 6861-6866.
48. Nakano, H., Burgents, J., Nakano, K., Whitehead, G., Cheong, C., Bortner, C., Cook, D. (2013) Migratory properties of pulmonary dendritic cells are determined by their developmental lineage. Mucosal Immunol. 6, 678-691.
49. Hintzen, G., Ohl, L., del Rio, M.-L., Rodriguez-Barbosa, J.-I., Pabst, O., Kocks, J., Krege, J., Hardtke, S., Förster, R. (2006) Induction of tolerance to innocuous inhaled antigen relies on a CCR7-dependent dendritic cell-mediated antigen transport to the bronchial lymph node. J Immunol. 177, 7346-7354.
50. Yamazaki, S., Dudziak, D., Heidkamp, G., Fiorese, C., Bonito, A., Inaba, K., Nussenzweig, M., Steinman, R. (2008) CD8 CD205 splenic dendritic cells are specialized to induce Foxp3 regulatory T cells. J. Immunol. 181, 6923-6933.
51. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M., von Boehmer, H. (2005) Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6, 1219-1227.
52. Poulin, L., Henri, S., de Bovis, B., Devilard, E., Kissenpfennig, A., Malissen, B. (2007) The dermis contains langerin dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204, 3119-3131.
53. Pulendran, B., Tang, H., Manicassamy, S. (2010) Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat. Immunol. 11, 647-655.
54. Matzinger, P., and Kamala, T. (2011) Tissue-based class control: the other side of tolerance. Nat. Rev. Immunol. 11, 221-230.
55. Yamazaki, S., Iyoda, T., Tarbell, K., Olson, K., Velinzon, K., Inaba, K., Steinman, R. M. (2003) Direct expansion of functional CD25+CD4+ regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198, 235-247.
56. Yokota, A., Takeuchi, H., Maeda, N., Ohoka, Y., Kato, C., Song, S. Y., Iwata, M. (2009) GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int. Immunol. 21, 361-377.
57. Bogdan, C., Erb, K., Schuler, G., Lutz, M. B. (2002) Repetitive injections of dendritic cells matured with tumor necrosis factor alpha induce antigen-specific protection of mice from autoimmunity. J. Exp. Med. 195, 15-21.
58. Jiang, A., Bloom, O., Ono, S., Cui, W., Unternaehrer, J., Jiang, S., Whitney, J. A., Connolly, J., Banchereau, J., Mellman, I. (2007) Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity. 27, 610-624.
59. Haribhai, D., Williams, J., Jia, S., Nickerson, D., Schmitt, E., Edwards, B., Ziegelbauer, J., Yassai, M., Li, S.-H., Relland, L., Wise, P., Chen, A., Zheng, Y.-Q., Simpson, P., Gorski, J., Salzman, N., Hessner, M., Chatila, T., Williams, C. (2011) A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity. Immunity. 35, 109-122.
60. Klein, L., Hinterberger, M., Wirnsberger, G., Kyewski, B. (2009) Antigen presentation in the thymus for positive selection and central tolerance induction. Nat. Rev. Immunol. 9, 833-844.