Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans

Journal of Experimental Medicine

Volumn 205, Issue 9, 2008, Pages 2139-2149

  Jaensson, Elin ^a   Uronen Hansson, Heli ^a   Pabst, Oliver ^b   Eksteen, Bertus ^c   Tian, Jiong ^b   Coombes, Janine L ^d   Berg, Pia Lena ^e   Davidsson, Thomas ^e   Powrie, Fiona ^d   Johansson Lindbom, Bengt ^a   Agace, William W ^a  

^a LUND UNIVERSITY   (Sweden)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CHEMOKINE RECEPTOR CCR9; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; LAMINA PROPRIA; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD; CELLS, CULTURED; CONSERVED SEQUENCE; DENDRITIC CELLS; FLOW CYTOMETRY; HUMANS; INTEGRIN ALPHA CHAINS; INTEGRINS; INTESTINE, SMALL; INTESTINES; LYMPH NODES; MICE; MICE, INBRED BALB C; RECEPTORS, CCR; T-LYMPHOCYTES;

EID: 51049092467     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20080414     Document Type: Article

References (56)

1. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y.J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811.
2. Steinman, R.M., and H. Hemmi. 2006. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 311:17-58.
3. Henri, S., D. Vremec, A. Kamath, J. Waithman, S. Williams, C. Benoist, K. Burnham, S. Saeland, E. Handman, and K. Shortman. 2001. The dendritic cell populations of mouse lymph nodes. J. Immunol. 167:741-748.
4. Shortman, K., and Y.J. Liu. 2002. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2:151-161.
5. Pulendran, B., J.L. Smith, G. Caspary, K. Brasel, D. Pettit, E. Maraskovsky, and C.R. Maliszewski. 1999. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo. Proc. Natl. Acad. Sci. USA. 96:1036-1041.
6. Villadangos, J.A., and P. Schnorrer. 2007. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7:543-555.
7. Cox, K., M. North, M. Burke, H. Singhal, S. Renton, N. Aqel, S. Islam, and S.C. Knight. 2005. Plasmacytoid dendritic cells (PDC) are the major DC subset innately producing cytokines in human lymph nodes. J. Leukoc. Biol. 78:1142-1152.
8. Mora, J.R., M. Iwata, B. Eksteen, S.Y. Song, T. Junt, B. Senman, K.L. Otipoby, A. Yokota, H. Takeuchi, P. Ricciardi-Castagnoli, et al. 2006. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science. 314:1157-1160.
9. O'Mahony, L., L. O'Callaghan, J. McCarthy, D. Shilling, P. Scully, S. Sibartie, E. Kavanagh, W.O. Kirwan, H.P. Redmond, J.K. Collins, and F. Shanahan. 2006. Differential cytokine response from dendritic cells to commensal and pathogenic bacteria in different lymphoid compartments in humans. Am. J. Physiol. Gastrointest. Liver Physiol. 290:G839-G845.
10. Takahashi, K., K. Asagoe, J. Zaishun, H. Yanai, T. Yoshino, K. Hayashi, and T. Akagi. 1998. Heterogeneity of dendritic cells in human superficial lymph node: in vitro maturation of immature dendritic cells into mature or activated interdigitating reticulum cells. Am. J. Pathol. 153:745-755.
11. Johansson, C., and B.L. Kelsall. 2005. Phenotype and function of intestinal dendritic cells. Semin. Immunol. 17:284-294.
12. Johansson-Lindbom, B., M. Svensson, M.A. Wurbel, B. Malissen, G. Marquez, 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.
13. 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.
14. 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.
15. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204:1757-1764.
16. Sun, C.M., J.A. Hall, R.B. Blank, N. Bouladoux, M. Oukka, J.R. Mora, and Y. Belkaid. 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.
17. + dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202:1063-1073.
18. 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.
19. Kang, S.G., H.W. Lim, O.M. Andrisani, H.E. Broxmeyer, and C.H. Kim. 2007. Vitamin A metabolites induce gut-homing FoxP3+ regulatory T cells. J. Immunol. 179:3724-3733.
20. 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.
21. Svensson, M., B. Johansson-Lindbom, F. Zapata, E. Jaensson, L. Austenaa, R. Blomhoff, and W.W. Agace. 2008. Retinoic acid receptor signaling levels and antigen dose regulate gut homing receptor expression on CD8+ T cells. Mucosal Immunology. 1:38-48.
22. Annacker, O., J.L. Coombes, V. Malmstrom, H.H. Uhlig, T. Bourne, B. Johansson-Lindbom, W.W. Agace, C.M. Parker, and F. Powrie. 2005. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202:1051-1061.
23. Sung, S.S., S.M. Fu, C.E. Rose Jr., F. Gaskin, S.T. Ju, and S.R. Beaty. 2006. A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J. Immunol. 176:2161-2172.
24. Hintzen, G., L. Ohl, M.L. del Rio, J.I. Rodriguez-Barbosa, O. Pabst, J.R. Kocks, J. Krege, S. Hardtke, and R. Forster. 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.
25. del Rio, M.L., J.I. Rodriguez-Barbosa, E. Kremmer, and R. Forster. 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.
26. 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.
27. Schon, M.P., A. Arya, E.A. Murphy, C.M. Adams, U.G. Strauch, W.W. Agace, J. Marsal, J.P. Donohue, H. Her, D.R. Beier, et al. 1999. Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J. Immunol. 162:6641-6649.
28. Strauch, U.G., R.C. Mueller, X.Y. Li, M. Cernadas, J.M. Higgins, D.G. Binion, and C.M. Parker. 2001. Integrin alpha E(CD103)beta 7 mediates adhesion to intestinal microvascular endothelial cell lines via an E-cadherin-independent interaction. J. Immunol. 166:3506-3514.
29. 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.
30. 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.
31. + T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease. J. Exp. Med. 201:1647-1657.
32. 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.
33. Agace, W.W. 2006. Tissue-tropic effector T cells: generation and targeting opportunities. Nat. Rev. Immunol. 6:682-692.
34. Yeum, K.J., and R.M. Russell. 2002. Carotenoid bioavailability and bioconversion. Annu. Rev. Nutr. 22:483-504.
35. Saurer, L., K.C. McCullough, and A. Summerfield. 2007. In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J. Immunol. 179:3504-3514.
36. Elgueta, R., F.E. Sepulveda, F. Vilches, L. Vargas, J.R. Mora, M.R. Bono, and M. Rosemblatt. 2008. Imprinting of CCR9 on CD4 T cells requires IL-4 signaling on mesenteric lymph node dendritic cells. J. Immunol. 180:6501-6507.
37. Yrlid, U., C.D. Jenkins, and G.G. MacPherson. 2006. Relationships between distinct blood monocyte subsets and migrating intestinal lymph dendritic cells in vivo under steady-state conditions. J. Immunol. 176:4155-4162.
38. Varol, C., L. Landsman, D.K. Fogg, L. Greenshtein, B. Gildor, R. Margalit, V. Kalchenko, F. Geissmann, and S. Jung. 2007. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med. 204:171-180.
39. Jakubzick, C., F. Tacke, F. Ginhoux, A.J. Wagers, N. van Rooijen, M. Mack, M. Merad, and G.J. Randolph. 2008. Blood monocyte subsets differentially give rise to CD103+ and CD103- pulmonary dendritic cell populations. J. Immunol. 180:3019-3027.
40. Jang, M.H., N. Sougawa, T. Tanaka, T. Hirata, T. Hiroi, K. Tohya, Z. Guo, E. Umemoto, Y. Ebisuno, B.G. Yang, et al. 2006. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J. Immunol. 176:803-810.
41. 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.
42. + dendritic cells. J. Exp. Med. 204:3147-3156.
43. + dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204:3119-3131.
44. + dendritic cells survey the skin in the steady state. J. Exp. Med. 204:3133-3146.
45. Wilson, N.S., D. El-Sukkari, G.T. Belz, C.M. Smith, R.J. Steptoe, W.R. Heath, K. Shortman, and J.A. Villadangos. 2003. Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood. 102:2187-2194.
46. Shortman, K., and S.H. Naik. 2007. Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 7:19-30.
47. Zhang, M., H. Tang, Z. Guo, H. An, X. Zhu, W. Song, J. Guo, X. Huang, T. Chen, J. Wang, and X. Cao. 2004. Splenic stroma drives mature dendritic cells to differentiate into regulatory dendritic cells. Nat. Immunol. 5:1124-1133.
48. Kabashima, K., T.A. Banks, K.M. Ansel, T.T. Lu, C.F. Ware, and J.G. Cyster. 2005. Intrinsic lymphotoxin-beta receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity. 22:439-450.
49. Liu, K., C. Waskow, X. Liu, K. Yao, J. Hoh, and M. Nussenzweig. 2007. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat. Immunol. 8:578-583.
50. Geissmann, F. 2007. The origin of dendritic cells. Nat. Immunol. 8:558-560.
51. Worbs, T., U. Bode, S. Yan, M.W. Hoffmann, G. Hintzen, G. Bernhardt, R. Forster, and O. Pabst. 2006. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203:519-527.
52. 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.
53. 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.
54. Sheasley-O'Neill, S.L., C.C. Brinkman, A.R. Ferguson, M.C. Dispenza, and V.H. Engelhard. 2007. Dendritic cell immunization route determines integrin expression and lymphoid and nonlymphoid tissue distribution of CD8 T cells. J. Immunol. 178:1512-1522.
55. 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.
56. Pabst, O., L. Ohl, M. Wendland, M.A. Wurbel, E. Kremmer, B. Malissen, and R. Forster. 2004. Chemokine receptor CCR9 contributes to the localization of plasma cells to the small intestine. J. Exp. Med. 199:411-416.