Ambivalent effects of dendritic cells displaying prostaglandin E2-induced indoleamine 2,3-dioxygenase

European Journal of Immunology

Volumn 42, Issue 5, 2012, Pages 1117-1128

  Lanzinger, Margit ^a   Jürgens, Birgit ^a   Hainz, Ursula ^a   Dillinger, Barbara ^a   Raberger, Julia ^a   Fuchs, Dietmar ^b   Heitger, Andreas ^a  

^a CHILDREN'S CANCER RESEARCH INSTITUTE   (Austria)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Human dendritic cells; IL 23; Immunosuppression; Indoleamine 2,3 dioxygenase (IDO); Prostaglandin E2

Indexed keywords

GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 6; NEOPTERIN; PROSTAGLANDIN E2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL ACTIVITY; CELL MATURATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SPACE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TH1 CELL; TH17 CELL; TH2 CELL;

CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; DINOPROSTONE; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LYMPHOCYTE ACTIVATION; T-LYMPHOCYTES;

EID: 84860340144     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141765     Document Type: Article

References (58)

1. Moffett, J. R. and Namboodiri, M. A., Tryptophan and the immune response. Immunol. Cell Biol. 2003. 81: 247-265.
2. Munn, D. H., Shafizadeh, E., Attwood, J. T., Bondarev, I., Pashine, A. and Mellor, A. L., Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 1999. 189: 1363-1372.
3. Grohmann, U., Fallarino, F. and Puccetti, P., Tolerance, DCs and tryptophan: much ado about IDO. Trends Immunol. 2003. 24: 242-248.
4. Mellor, A. L. and Munn, D. H., IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 2004. 4: 762-774.
5. Orabona, C., Puccetti, P., Vacca, C., Bicciato, S., Luchini, A., Fallarino, F., Bianchi, R. et al., Toward the identification of a tolerogenic signature in IDO-competent dendritic cells. Blood 2006. 107: 2846-2854.
6. Jurgens, B., Hainz, U., Fuchs, D., Felzmann, T. and Heitger, A., Interferon-gamma-triggered indoleamine 2, 3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood 2009. 114: 3235-3243.
7. Munn, D. H., Zhou, M., Attwood, J. T., Bondarev, I., Conway, S. J., Marshall, B., Brown, C. and Mellor, A. L., Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998. 281: 1191-1193.
8. Hainz, U., Jurgens, B. and Heitger, A., The role of indoleamine 2, 3-dioxygenase in transplantation. Transpl. Int. 2007. 20: 118-127.
9. Jasperson, L. K., Bucher, C., Panoskaltsis-Mortari, A., Mellor, A. L., Munn, D. H. and Blazar, B. R., Inducing the tryptophan catabolic pathway, indoleamine 2, 3-dioxygenase (IDO), for suppression of graft-versus-host disease (GVHD) lethality. Blood 2009. 114: 5062-5070.
10. Prendergast, G. C., Immune escape as a fundamental trait of cancer: focus on IDO. Oncogene 2008. 27: 3889-3900.
11. Heitger, A., Regulation of expression and function of IDO in human dendritic cells. Curr. Med. Chem. 2011. 18: 2222-2233.
12. Takikawa, O., Habara-Ohkubo, A. and Yoshida, R., Induction of indoleamine 2, 3-dioxygenase in tumor cells transplanted into allogeneic mouse: interferon-gamma is the inducer. Adv. Exp. Med. Biol. 1991. 294: 437-444.
13. Huber, C., Batchelor, J. R., Fuchs, D., Hausen, A., Lang, A., Niederwieser, D., Reibnegger, G. et al., Immune response-associated production of neopterin. Release from macrophages primarily under control of interferon-gamma. J. Exp. Med. 1984. 160: 310-316.
14. Widner, B., Leblhuber, F., Walli, J., Tilz, G. P., Demel, U. and Fuchs, D., Tryptophan degradation and immune activation in Alzheimer's disease. J. Neural. Transm. 2000. 107: 343-353.
15. Hainz, U., Obexer, P., Winkler, C., Sedlmayr, P., Takikawa, O., Greinix, H., Lawitschka, A. et al., Monocyte-mediated T-cell suppression and augmented monocyte tryptophan catabolism after human hematopoietic stem-cell transplantation. Blood 2005. 105: 4127-4134.
16. Schrocksnadel, K., Wirleitner, B., Winkler, C. and Fuchs, D., Monitoring tryptophan metabolism in chronic immune activation. Clin. Chim. Acta. 2006. 364: 82-90.
17. Braun, D., Longman, R. S. and Albert, M. L., A two-step induction of indoleamine 2, 3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood 2005. 106: 2375-2381.
18. von Bergwelt-Baildon, M. S., Popov, A., Saric, T., Chemnitz, J., Classen, S., Stoffel, M. S., Fiore, F. et al., CD25 and indoleamine 2, 3-dioxygenase are up-regulated by prostaglandin E2 and expressed by tumor-associated dendritic cells in vivo: additional mechanisms of T-cell inhibition. Blood 2006. 108: 228-237.
19. Jonuleit, H., Kuhn, U., Muller, G., Steinbrink, K., Paragnik, L., Schmitt, E., Knop, J. and Enk, A. H., Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur. J. Immunol. 1997. 27: 3135-3142.
20. Rieser, C., Bock, G., Klocker, H., Bartsch, G. and Thurnher, M., Prostaglandin E2 and tumor necrosis factor alpha cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J. Exp. Med. 1997. 186: 1603-1608.
21. Krause, P., Singer, E., Darley, P. I., Klebensberger, J., Groettrup, M. and Legler, D. F., Prostaglandin E2 is a key factor for monocyte-derived dendritic cell maturation: enhanced T cell stimulatory capacity despite IDO. J. Leukoc. Biol. 2007. 82: 1106-1114.
22. Legler, D. F., Bruckner, M., Uetz-von Allmen, E. and Krause, P., Prostaglandin E2 at new glance: novel insights in functional diversity offer therapeutic chances. Int. J. Biochem. Cell. Biol. 2010. 42: 198-201.
23. Thurnher, M., Lipids in dendritic cell biology: messengers, effectors, and antigens. J. Leukoc. Biol. 2007. 81: 154-160.
24. Sakata, D., Yao, C. and Narumiya, S., Prostaglandin E2, an immunoactivator. J. Pharmacol. Sci. 2010. 112: 1-5.
25. Kalinski, P., Hilkens, C. M., Snijders, A., Snijdewint, F. G. and Kapsenberg, M. L., IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J. Immunol. 1997. 159: 28-35.
26. Kalinski, P., Vieira, P. L., Schuitemaker, J. H., de Jong, E. C. and Kapsenberg, M. L., Prostaglandin E(2) is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001. 97: 3466-3469.
27. Reis e Sousa, C., Dendritic cells in a mature age. Nat. Rev. Immunol. 2006. 6: 476-483.
28. Scandella, E., Men, Y., Gillessen, S., Forster, R. and Groettrup, M., Prostaglandin E2 is a key factor for CCR7 surface expression and migration of monocyte-derived dendritic cells. Blood 2002. 100: 1354-1361.
29. Krause, P., Bruckner, M., Uermosi, C., Singer, E., Groettrup, M. and Legler, D. F., Prostaglandin E(2) enhances T-cell proliferation by inducing the costimulatory molecules OX40L, CD70, and 4-1BBL on dendritic cells. Blood 2009. 113: 2451-2460.
30. Kalinski, P., Hilkens, C. M., Wierenga, E. A. and Kapsenberg, M. L., T-cell priming by type-1 and type-2 polarized dendritic cells: the concept of a third signal. Immunol. Today 1999. 20: 561-567.
31. Felzmann, T., Huttner, K. G., Breuer, S. K., Wimmer, D., Ressmann, G., Wagner, D., Paul, P. et al., Semi-mature IL-12 secreting dendritic cells present exogenous antigen to trigger cytolytic immune responses. Cancer Immunol. Immunother 2005. 54: 769-780.
32. Moller, I., Michel, K., Frech, N., Burger, M., Pfeifer, D., Frommolt, P., Veelken, H. et al., Dendritic cell maturation with poly(I:C)-based versus PGE2-based cytokine combinations results in differential functional characteristics relevant to clinical application. J. Immunother. 2008. 31: 506-519.
33. Napolitani, G., Acosta-Rodriguez, E. V., Lanzavecchia, A. and Sallusto, F., Prostaglandin E2 enhances Th17 responses via modulation of IL-17 and IFN-gamma production by memory CD4+ T cells. Eur. J. Immunol. 2009. 39: 1301-1312.
34. McGeachy, M. J. and Cua, D. J., Th17 cell differentiation: the long and winding road. Immunity 2008. 28: 445-453.
35. Weaver, C. T. and Hatton, R. D., Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective. Nat. Rev. Immunol. 2009. 9: 883-889.
36. Muller, A. J., DuHadaway, J. B., Donover, P. S., Sutanto-Ward, E. and Prendergast, G. C., Inhibition of indoleamine 2, 3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat. Med. 2005. 11: 312-319.
37. Munn, D. H., Mellor, A. L., Rossi, M. and Young, J. W., Dendritic cells have the option to express IDO-mediated suppression or not. Blood 2005. 105: 2618.
38. Terness, P., Chuang, J. J., Bauer, T., Jiga, L. and Opelz, G., Regulation of human auto- and alloreactive T cells by indoleamine 2, 3-dioxygenase (IDO)-producing dendritic cells: too much ado about IDO? Blood 2005. 105: 2480-2486.
39. Terness, P., Chuang, J. J. and Opelz, G., The immunoregulatory role of IDO-producing human dendritic cells revisited. Trends Immunol. 2006. 27: 68-73.
40. Khayrullina, T., Yen, J. H., Jing, H. and Ganea, D., In vitro differentiation of dendritic cells in the presence of prostaglandin E2 alters the IL-12/IL-23 balance and promotes differentiation of Th17 cells. J. Immunol. 2008. 181: 721-735.
41. Lee, Y. K., Turner, H., Maynard, C. L., Oliver, J. R., Chen, D., Elson, C. O. and Weaver, C. T., Late developmental plasticity in the T helper 17 lineage. Immunity 2009. 30: 92-107.
42. Ghoreschi, K., Laurence, A., Yang, X. P., Hirahara, K. and O'Shea, J. J., T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol. 2011. 32: 395-401.
43. Wan, Y. Y., Multi-tasking of helper T cells. Immunology 2010. 130: 166-171.
44. Dhodapkar, M. V., Steinman, R. M., Sapp, M., Desai, H., Fossella, C., Krasovsky, J., Donahoe, S. M. et al., Rapid generation of broad T-cell immunity in humans after a single injection of mature dendritic cells. J. Clin. Invest. 1999. 104: 173-180.
45. Khader, S. A., Partida-Sanchez, S., Bell, G., Jelley-Gibbs, D. M., Swain, S., Pearl, J. E., Ghilardi, N. et al., Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection. J. Exp. Med. 2006. 203: 1805-1815.
46. Muthuswamy, R., Mueller-Berghaus, J., Haberkorn, U., Reinhart, T. A., Schadendorf, D. and Kalinski, P., PGE(2) transiently enhances DC expression of CCR7 but inhibits the ability of DCs to produce CCL19 and attract naive T cells. Blood 2010. 116: 1454-1459.
47. Muthuswamy, R., Urban, J., Lee, J. J., Reinhart, T. A., Bartlett, D. and Kalinski, P., Ability of mature dendritic cells to interact with regulatory T cells is imprinted during maturation. Cancer Res. 2008. 68: 5972-5978.
48. Munn, D. H., Sharma, M. D., Hou, D., Baban, B., Lee, J. R., Antonia, S. J., Messina, J. L. et al., Expression of indoleamine 2, 3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest. 2004. 114: 280-290.
49. Fallarino, F., Vacca, C., Orabona, C., Belladonna, M. L., Bianchi, R., Marshall, B., Keskin, D. B. et al., Functional expression of indoleamine 2, 3-dioxygenase by murine CD8 alpha(+) dendritic cells. Int. Immunol. 2002. 14: 65-68.
50. Chen, W., Liang, X., Peterson, A. J., Munn, D. H. and Blazar, B. R., The indoleamine 2, 3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J. Immunol. 2008. 181: 5396-5404.
51. Boor, P. P., Metselaar, H. J., Jonge, S., Mancham, S., van der Laan, L. J. and Kwekkeboom, J., Human plasmacytoid dendritic cells induce CD8 LAG-3 Foxp3 CTLA-4 regulatory T cells that suppress allo-reactive memory T cells. Eur. J. Immunol. 2011. 41: 1663-1674.
52. Fallarino, F., Grohmann, U., You, S., McGrath, B. C., Cavener, D. R., Vacca, C., Orabona, C. et al., Tryptophan catabolism generates autoimmune-preventive regulatory T cells. Transpl. Immunol. 2006. 17: 58-60.
53. Banchereau, J. and Palucka, A. K., Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 2005. 5: 296-306.
54. Gilboa, E., DC-based cancer vaccines. J. Clin. Invest. 2007. 117: 1195-1203.
55. Palucka, K., Ueno, H., Zurawski, G., Fay, J. and Banchereau, J., Building on dendritic cell subsets to improve cancer vaccines. Curr. Opin. Immunol. 2010. 22: 258-263.
56. Heitger, A., Winklehner, P., Obexer, P., Eder, J., Zelle-Rieser, C., Kropshofer, G., Thurnher, M. et al., Defective T-helper cell function after T-cell-depleting therapy affecting naive and memory populations. Blood 2002. 99: 4053-4062.
57. Lyons, A. B. and Parish, C. R., Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 1994. 171: 131-137.
58. Takikawa, O., Kuroiwa, T., Yamazaki, F. and Kido, R., Mechanism of interferon-gamma action. Characterization of indoleamine 2, 3-dioxygenase in cultured human cells induced by interferon-gamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J. Biol. Chem. 1988. 263: 2041-2048.