Lymph node-derived lymphatic endothelial cells express functional costimulatory molecules and impair dendritic cell-induced allogenic T-cell proliferation

FASEB Journal

Volumn 26, Issue 7, 2012, Pages 2835-2846

  Nörder, Miriam ^a   Gutierrez, Maximiliano G ^a   Zicari, Sonia ^b   Cervi, Edoardo ^b   Caruso, Arnaldo ^b   Guzmán, Carlos A ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Antigen presentation; Immune modulation; Indoleamine 2,3 dioxygenase

Indexed keywords

GAMMA INTERFERON; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 6; INTERLEUKIN 8; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES;

ARTICLE; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL INTERACTION; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LYMPH NODE; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

ANTIGEN PRESENTATION; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL PROLIFERATION; CHEMOKINE CXCL10; DNA, COMPLEMENTARY; ENDOTHELIAL CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-GAMMA; LYMPH NODES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84863206217     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-205278     Document Type: Article

References (55)

1. Swartz, M. A., Hubbell, J. A., and Reddy, S. T. (2008) Lymphatic drainage function and its immunological implications: from dendritic cell homing to vaccine design. Semin. Immunol. 20, 147-156
2. Von Andrian, U. H., and Mempel, T. R. (2003) Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3, 867-878 (Pubitemid 37411716)
3. Podgrabinska, S., Kamalu, O., Mayer, L., Shimaoka, M., Snoeck, H., Randolph, G. J., and Skobe, M. (2009) Inflamed lymphatic endothelium suppresses dendritic cell maturation and function via Mac-1/ICAM-1-dependent mechanism. J. Immunol. 183, 1767-1779
4. Pegu, A., Qin, S., Fallert Junecko, B. A., Nisato, R. E., Pepper, M. S., and Reinhart, T. A. (2008) Human lymphatic endothelial cells express multiple functional TLRs. J. Immunol. 180, 3399-3405
5. Garrafa, E., Imberti, L., Tiberio, G., Prandini, A., Giulini, S. M., and Caimi, L. (2011) Heterogeneous expression of toll-like receptors in lymphatic endothelial cells derived from different tissues. Immunol. Cell Biol. 89, 475-481
6. Randolph, G. J., Angeli, V., and Swartz, M. A. (2005) Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5, 617-628 (Pubitemid 41113193)
7. Choi, J., Enis, D. R., Koh, K. P., Shiao, S. L., and Pober, J. S. (2004) T lymphocyte-endothelial cell interactions. Annu. Rev. Immunol. 22, 683-709 (Pubitemid 38680438)
8. Cunningham, A. C., Zhang, J. G., Moy, J. V., Ali, S., and Kirby, J. A. (1997) A comparison of the antigen-presenting capabilities of class II MHC-expressing human lung epithelial and endothelial cells. Immunology 91, 458-463 (Pubitemid 27304283)
9. Seino, K., Azuma, M., Bashuda, H., Fukao, K., Yagita, H., and Okumura, K. (1995) CD86 (B70/B7-2) on endothelial cells co-stimulates allogeneic CD4+ T cells. Int. Immunol. 7, 1331-1337
10. Saada, J. I., Pinchuk, I. V., Barrera, C. A., Adegboyega, P. A., Suarez, G., Mifflin, R. C., Di Mari, J. F., Reyes, V. E., and Powell, D. W. (2006) Subepithelial myofibroblasts are novel nonprofessional APCs in the human colonic mucosa. J. Immunol. 177, 5968-5979 (Pubitemid 44628810)
11. Hansen, A. B., Bouchelouche, K., and Olesen, J. D. (2001) Human lung microvascular endothelial cells activate allogeneic T cells through an LFA-3-dependent, but CD86-independent mechanism. APMIS 109, 849-856 (Pubitemid 34056340)
12. Linsley, P. S., and Ledbetter, J. A. (1993) The role of the CD28 receptor during T cell responses to antigen. Annu. Rev. Immunol. 11, 191-212 (Pubitemid 23115006)
13. Steinman, R. M. (1991) The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9, 271-296
14. Zhou, L. J., and Tedder, T. F. (1995) Human blood dendritic cells selectively express CD83, a member of the immunoglobulin superfamily. J. Immunol. 154, 3821-3835
15. Parish, C. R. (1999) Fluorescent dyes for lymphocyte migration and proliferation studies. Immunol. Cell Biol. 77, 499-508
16. Lyons, A. B., and Parish, C. R. (1994) Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171, 131-137 (Pubitemid 24140219)
17. Epperson, D. E., and Pober, J. S. (1994) Antigen-presenting function of human endothelial cells. Direct activation of resting CD8 T cells. J. Immunol. 153, 5402-5412 (Pubitemid 24377676)
18. Savage, C. O., Hughes, C. C., McIntyre, B. W., Picard, J. K., and Pober, J. S. (1993) Human CD4+ T cells proliferate to HLADR+ allogeneic vascular endothelium. Identification of accessory interactions. Transplantation 56, 128-134 (Pubitemid 23220586)
19. Luster, A. D. (1998) Chemokines-chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338, 436-445
20. Neville, L. F., Mathiak, G., and Bagasra, O. (1997) The immunobiology of interferon-gamma inducible protein 10 kDa (IP-10): a novel, pleiotropic member of the C-X-C chemokine superfamily. Cytokine Growth Factor Rev. 8, 207-219 (Pubitemid 28077928)
21. Hanaoka, R., Kasama, T., Muramatsu, M., Yajima, N., Shiozawa, F., Miwa, Y., Negishi, M., Ide, H., Miyaoka, H., Uchida, H., and Adachi, M. (2003) A novel mechanism for the regulation of IFN-γ inducible protein-10 expression in rheumatoid arthritis. Arthritis Res. Ther. 5, R74-R81
22. Taub, D. D., Lloyd, A. R., Conlon, K., Wang, J. M., Ortaldo, J. R., Harada, A., Matsushima, K., Kelvin, D. J., and Oppenheim, J. J. (1993) Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J. Exp. Med. 177, 1809-1814 (Pubitemid 23146150)
23. Mestas, J., and Hughes, C. C. (2001) Endothelial cell costimulation of T cell activation through CD58-CD2 interactions involves lipid raft aggregation. J. Immunol. 167, 4378-4385 (Pubitemid 32954314)
24. Mellor, A. L., and Munn, D. H. (2004) IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4, 762-774 (Pubitemid 39336293)
25. Mellor, A. L., and Munn, D. H. (1999) Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation? Immunol. Today 20, 469-473 (Pubitemid 29476077)
26. Beutelspacher, S. C., Tan, P. H., McClure, M. O., Larkin, D. F., Lechler, R. I., and George, A. J. (2006) Expression of indoleamine 2,3-dioxygenase (IDO) by endothelial cells: implications for the control of alloresponses. Am. J. Transplant. 6, 1320-1330 (Pubitemid 44030315)
27. Hassanain, H. H., Chon, S. Y., and Gupta, S. L. (1993) Differential regulation of human indoleamine 2,3-dioxygenase gene expression by interferons-gamma and -alpha. Analysis of the regulatory region of the gene and identification of an interferon-gamma-inducible DNA-binding factor. J. Biol. Chem. 268, 5077-5084 (Pubitemid 23081633)
28. Taylor, M. W., and Feng, G. S. (1991) Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5, 2516-2522 (Pubitemid 21905800)
29. McDouall, R. M., Page, C. S., Hafizi, S., Yacoub, M. H., and Rose, M. L. (1996) Alloproliferation of purified CD4+ T cells to adult human heart endothelial cells, and study of second-signal requirements. Immunology 89, 220-226 (Pubitemid 26340126)
30. Opitz, B., Hippenstiel, S., Eitel, J., and Suttorp, N. (2007) Extra-and intracellular innate immune recognition in endothelial cells. Thromb. Haemost. 98, 319-326 (Pubitemid 47250234)
31. Mazanet, M. M., and Hughes, C. C. (2002) B7-H1 is expressed by human endothelial cells and suppresses T-cell cytokine synthesis. J. Immunol. 169, 3581-3588
32. Walker, J. D., Maier, C. L., and Pober, J. S. (2009) Cytomegalo-virus- infected human endothelial cells can stimulate allogeneic CD4+ memory T cells by releasing antigenic exosomes. J. Immunol. 182, 1548-1559
33. Civin, C. I., Strauss, L. C., Brovall, C., Fackler, M. J., Schwartz, J. F., and Shaper, J. H. (1984) Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J. Immunol. 133, 157-165 (Pubitemid 14076703)
34. Baumhueter, S., Dybdal, N., Kyle, C., and Lasky, L. A. (1994) Global vascular expression of murine CD34, a sialomucin-like endothelial ligand for L-selectin. Blood 84, 2554-2565 (Pubitemid 24317387)
35. Fiedler, U., Christian, S., Koidl, S., Kerjaschki, D., Emmett, M. S., Bates, D. O., Christofori, G., and Augustin, H. G. (2006) The sialomucin CD34 is a marker of lymphatic endothelial cells in human tumors. Am. J. Pathol. 168, 1045-1053 (Pubitemid 43327754)
36. Tang, H. L., and Cyster, J. G. (1999) Chemokine up-regulation and activated T cell attraction by maturing dendritic cells. Science 284, 819-822 (Pubitemid 29291350)
37. Kawai, T., Seki, M., Hiromatsu, K., Eastcott, J. W., Watts, G. F., Sugai, M., Smith, D. J., Porcelli, S. A., and Taubman, M. A. (1999) Selective diapedesis of Th1 cells induced by endothelial cell RANTES. J. Immunol. 163, 3269-3278 (Pubitemid 29431828)
38. Yoneyama, H., Narumi, S., Zhang, Y., Murai, M., Baggiolini, M., Lanzavecchia, A., Ichida, T., Asakura, H., and Matsushima, K. (2002) Pivotal role of dendritic cell-derived CXCL10 in the retention of T helper cell 1 lymphocytes in secondary lymph nodes. J. Exp. Med. 195, 1257-1266 (Pubitemid 34564328)
39. Tan, P. H., Chan, C., Xue, S. A., Dong, R., Ananthesayanan, B., Manunta, M., Kerouedan, C., Cheshire, N. J., Wolfe, J. H., Haskard, D. O., Taylor, K. M., and George, A. J. (2004) Phenotypic and functional differences between human saphenous vein (HSVEC) and umbilical vein (HUVEC) endothelial cells. Atherosclerosis 173, 171-183 (Pubitemid 38469784)
40. London, C. A., Lodge, M. P., and Abbas, A. K. (2000) Functional responses and costimulator dependence of memory CD4+ T cells. J. Immunol. 164, 265-272 (Pubitemid 30012999)
41. Fontenot, A. P., Gharavi, L., Bennett, S. R., Canavera, S. J., Newman, L. S., and Kotzin, B. L. (2003) CD28 costimulation independence of target organ versus circulating memory antigen-specific CD4+ T cells. J. Clin. Invest. 112, 776-784 (Pubitemid 38057718)
42. Davis, S. J., and van der Merwe, P. A. (1996) The structure and ligand interactions of CD2: implications for T-cell function. Immunol. Today 17, 177-187 (Pubitemid 26113086)
43. Savage, C. O., Hughes, C. C., Pepinsky, R. B., Wallner, B. P., Freedman, A. S., and Pober, J. S. (1991) Endothelial cell lymphocyte function-associated antigen-3 and an unidentified ligand act in concert to provide costimulation to human peripheral blood CD4+ T cells. Cell. Immunol. 137, 150-163
44. Hughes, C. C., Savage, C. O., and Pober, J. S. (1990) Endothelial cells augment T cell interleukin 2 production by a contact-dependent mechanism involving CD2/LFA-3 interaction. J. Exp. Med. 171, 1453-1467 (Pubitemid 20167543)
45. Grakoui, A., Bromley, S. K., Sumen, C., Davis, M. M., Shaw, A. S., Allen, P. M., and Dustin, M. L. (1999) The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221-227 (Pubitemid 29329988)
46. Hamann, D., Baars, P. A., Hooibrink, B., and van Lier, R. W. (1996) Heterogeneity of the human CD4+ T-cell population: two distinct CD4+ T-cell subsets characterized by coexpression of CD45RA and CD45RO isoforms. Blood 88, 3513-3521 (Pubitemid 26365587)
47. Baecher-Allan, C., Brown, J. A., Freeman, G. J., and Hafler, D. A. (2001) CD4+ CD25 high regulatory cells in human peripheral blood. J. Immunol. 167, 1245-1253 (Pubitemid 32703119)
48. Kotani, A., Hori, T., Matsumura, Y., and Uchiyama, T. (2002) Signaling of gp34 (OX40 ligand) induces vascular endothelial cells to produce a CC chemokine RANTES/CCL5. Immunol. Lett. 84, 1-7 (Pubitemid 34879913)
49. Watts, T. H. (2005) TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23, 23-68
50. Murphy, K., Travers, P., and Walport, M. (2008) Janeway's Immunobiology. Garland Science, Taylor & Francis Group, New York
51. Wulfing, C., and Davis, M. M. (1998) A receptor/cytoskeletal movement triggered by costimulation during T cell activation. Science 282, 2266-2269 (Pubitemid 29004077)
52. Pfefferkorn, E. R. (1984) Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl. Acad. Sci. U. S. A. 81, 908-912
53. Hayashi, T., Rao, S. P., Takabayashi, K., Van Uden, J. H., Kornbluth, R. S., Baird, S. M., Taylor, M. W., Carson, D. A., Catanzaro, A., and Raz, E. (2001) Enhancement of innate immunity against Mycobacterium avium infection by immunostimulatory DNA is mediated by indoleamine 2,3-dioxygenase. Infect. Immun. 69, 6156-6164 (Pubitemid 32885177)
54. Carlin, J. M., Borden, E. C., Sondel, P. M., and Byrne, G. I. (1989) Interferon-induced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. J. Leukoc. Biol. 45, 29-34 (Pubitemid 19043368)
55. Cohen, J. N., Guidi, C. J., Tewalt, E. F., Qiao, H., Rouhani, S. J., Ruddell, A., Farr, A. G., Tung, K. S., and Engelhard, V. H. (2010) Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J. Exp. Med. 207, 681-688