Dendritic cell; IL-12; Prostaglandin D2; D prostanoid receptor; NF- kB
Abstract :
[en] Prostaglandin (PG) D(2), and its metabolites, are known to be important mediators during acute and chronic inflammation. However, their functions during the early phases of the immune response are poorly documented. In the present study, we show that PGD(2 )inhibits, in a dose-dependent manner, the CD40- and LPS-induced secretion of the Th1-driving factor IL-12 by murine splenic dendritic cells (DC), the most potent antigen-presenting cells. The inhibition of IL-12 production is mediated only in part by the cell surface G alpha s protein-coupled D prostanoid receptor (termed DP1) but not by the G alpha i protein-coupled DP receptor, DP2. We show that recruitment of DP1 in DC results in the activation of a cyclic AMP/protein kinase A pathway that is partially responsible for the inhibition of IL-12 production. We also suggest that the DP1-independent effects exerted by PGD(2) on IL-12 production may be due to the action of ist PGJ(2), but not PGF(2)alpha, metabolites. Electrophoretic mobility shift assays demonstrated that PGD(2) affects NF-kappa B activation through (the) DP1-independent pathway(s). Together these data suggest that PGD(2), by interacting with DP1 and by binding to other target cellular proteins, may regulate immune responses by affecting IL-12 production in DC
Disciplines :
Biochemistry, biophysics & molecular biology Laboratory medicine & medical technology
Author, co-author :
Faveeuw, Christelle; Institut Pasteur de Lille,Inserm U547, Lille, France
Gosset, Philippe; Inserm U416, Institut Pasteur de Lille, Lille, France
Bureau, Fabrice ; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire
Angeli, Veronique; Institut Pasteur de Lille, Inserm U547, Lille, France
Hirai, Hiroyuki; R&D Center, BML, Saitama, Japan
Maruyama, Takayuki; Minase Research Institute, Ono Pharmaceutical Co. Ltd., Osaka, Japan
Narumiya, Shuh; Faculty of Medicine, Kyoto University, Kyoto, Japan
Capron, Monique; Institut Pasteur de Lille, Inserm U547, Lille, France
Trottein, Francois; Institut Pasteur de Lille, Inserm U547, Lille, France
Language :
English
Title :
Prostaglandin D2 inhibits the production of interleukin-12 in murine dendritic cells through multiple signaling pathways.
Urade, Y. and Hayaishi, O., Prostaglandin D synthase: structure and function. Vitam. Horm. 2000. 58: 89-120.
Matsuoka, T., Hirata, M., Tanaka, H., Takahashi, Y., Murata, T., Kabashima, K., Sugimoto, Y., Kobayashi, T., Ushikubi, F., Aze, Y., Eguchi, N., Urade, Y., Yoshida, N., Kimura, K., Mizoguchi, A., Honda, Y., Nagai, H. and Narumiya, S., Prostaglandin D2 as a mediator of allergic asthma. Science 2000. 287: 2013-2017.
Hirai, H., Tanaka, K., Yoshie, O., Ogawa, K., Kenmotsu, K., Takamori, Y., Ichimasa, M., Sugamura, K., Nakamura, M., Takano. and Nagata, K., Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J. Exp. Med. 2001. 193: 255-261.
Monneret, G., Gravel, S., Diamond, M., Rokach, J. and Powell, W. S., Prostaglandin D2 is a potent chemoattractant for human eosinophils that acts via a novel DP receptor. Blood 2001. 98: 1942-1948.
Gilroy, D. W., Colville-Nash, P. R., Willis, D., Chivers, J., Paul-Clark, M. J. and Willoughby, D. A., Inducible cyclooxygenase may have anti-inflammatory properties. Nat. Med. 1999. 5: 698-701.
Ajuebor, M. N., Singh, A. and Wallace, J. L., Cyclooxygenase-2-derived prostaglandin D2 is an early anti-inflammatory signal in experimental colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2000. 279: 238-244.
Ianaro, A., Ialenti, A., Maffia, P., Pisano, B. and Di Rosa, M., Role of cyclopentenone prostaglandins in rat carrageenin pleurisy. FEBS Lett. 2001. 508: 61-66.
Narumiya, S., Y. Sugimoto, Y. and Ushikubi, F., Prostanoid receptors: structures, properties, and functions. Physiol. Rev. 1999. 79: 1193-1226.
Forman, B. M., Tontonoz, P., Chen, J., Brun, R. P., Spiegelman, B. M. and Evans, R. M., 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell 1995. 83: 803-812.
Shibata, T., Kondo, M., Osawa, T., Shibata, N., Kobayashi, M. and Uchida, K., 15-Deoxy-delta12,14-prostaglandin J2: A prostaglandin D2 metabolite generated during inflammatory processes. J. Biol. Chem. 2002. 277: 10459-10466.
Rossi, A., Kapahi, P., Natoli, G., Takahashi, T., Chen, Y., Karin, M. and Santoro, M. G., Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature 2000. 403: 103-108.
Straus, D. S., Pascual, G., Li, M., Welch, J. S., Ricote, M., Hsiang, C. H., Sengchanthalangsy, L. L., Ghosh, G. and Glass, C, K., 15-Deoxy-delta 12,14-prostaglandin J2 inhibits multiple steps in the NF-κB signaling pathway. Proc. Natl. Acad. Sci. USA 2000. 97: 4844-4849.
Banchereau, J. and Steinman, R. M., Dendritic cells and the control of immunity. Nature 1998. 392: 245-252.
Lanzavecchia, A. and Sallusto, F., The instructive role of dendritic cells on T cell responses: lineages, plasticity and kinetics. Curr. Opin. Immunol. 2001. 3:291-298.
Angeli, V., Faveeuw, C., Roye, O., Fontaine, J., Teissier, E., Capron, A., Wolowczuk, I., Capron, M. and Trottein, F., Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection. J. Exp. Med. 2001. 193: 1138-1148.
Trinchieri, G. and Scott, P., Interleukin-12: a proinflammatory cytokine with immunoregulatory functions. Res. Immunol. 1995. 146: 423-431.
Celia, M., Scheidegger, D., Palmer-Lehmann, K., Lane, P., Lanzavecchia, A. and Alber, G., Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 1996. 184: 747-752.
Rieser, C., Bock, G., Klocker, H., Bartsch, G. and Thurnher, M., PGE2 and TNFα cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J. Exp. Med. 1997. 186: 1603-1608.
Kalinski, P., Vieira, P. L., Schuitemaker, J. H., de Jong, E. C. and Kapsenberg, M. L. PGE2 is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001. 97: 3466-3469.
Aloisi, F., Penna, G., Cerase, J., Menendez Iglesias, B. and Adorini, L., IL-12 production by central nervous system microglia is inhibited by astrocytes. J. Immunol. 1997. 159: 1604-1612.
Staples, K. J., Bergmann, M., Tamita, K., Houslay, M. D., McPhee, I., Barnes, P. J., Glembycz, M. A. and Newton, R., Adenosine 3′,5′-cyclic monophosphate (cAMP)-dependent inhibition of IL-5 from human T lymphocytes is not mediated by the cAMP-dependent protein kinase A. J. Immunol. 2001. 167: 2074-2080.
Martin, M. C., Dransfield, I., Haslett, C. and Rossi, A. G., Cyclic AMP regulation of neutrophil apoptosis occurs via a novel protein kinase A-independent signaling pathway. J. Biol. Chem. 2001. 276: 45041-4550.
Francis, S. H. and Corbin, J. D., Cyclic nucleotide-dependent protein kinases: intracellular receptors for cAMP and cGMP action. Crit. Rev. Clin. Lab. Sci. 1999. 36: 275-328.
Nedachi, T., Akahori, M., Ariga, M., Sakamoto, H., Suzuki, N., Umesaki, K., Hakuno, F. and Takahashi, S. I., Tyrosine kinase and phosphatidylinositol 3-kinase activation are required for cyclic adenosine 3′,5′-monophosphate-dependent potentiation of deoxyribonucleic acid synthesis induced by insulin-like growth factor-I in FRTL-5 cells. Endocrinology 2000. 141: 2429-2438.
Erhardt, P., Troppmair, J., Rapp, U. R. and Cooper, G. M., Differential regulation of Raf-1 and B-Raf and Ras-dependent activation of mitogen-activated protein kinase by cyclic AMP in PC12 cells. Mol. Cell. Biol. 1995. 15: 5524-5530.
Plevin, R., Malarkey, K., Aidulis, D., McLees, A. and Gould, G. W., Cyclic AMP inhibitors inhibits PDGF-stimulated mitogen-activated protein kinase activity in rat aortic smooth muscle cells via inactivation of c-Raf-1 kinase and induction of MAP kinase phosphatase-1. Cell. Signal. 1997. 9: 323-328.
Urade, Y., Ujihara, M., Horiguchi, Y., lkai, K. and Hayaishi, O. The major source of endogenous prostaglandin D2 production is likely antigen-presenting cells. Localization of glutathione-requiring prostaglandin D synthetase in histiocytes, dendritic, and Kupffer cells in various rat tissues. J. Immunol. 1989. 143: 2982-2989.
Tanaka, K., Ogawa, K., Sugamura, K., Nakamura, M., Takano, S. and Nagata, K., Differential production of prostaglandin D2 by human helper T cell subsets. J. Immunol. 2000. 164: 2277-2280.
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.
Steinbrink, K., Paragnik, L., Jonuleit, H., Tuting, T., Knop, J. and Enk, A. H., Induction of dendritic cell maturation and modulation of dendritic cell-induced immune responses by prostaglandins. Arch. Dermatol. Res. 2000. 292: 437-445.
Kalinski, P., Hilkens, C. M., Snijders, A., Snijdewint, F. G. and Kapsenberg, M.L., IL-12-deficient dendritic cells, generated in the presence of PGE2, promote type 2 cytokine production in maturing human naive T helper cells. J. Immunol. 1997. 159: 28-35.
Kalinski, P., Schuitemaker, J. H., Hilkens, C. M. and Kapsenberg, M. L., Prostaglandin E2 induces the final maturation of IL-12-deficient CD1a+CD83+ dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J. Immunol. 1998. 161: 2804-2809.
Faries, M. B., Bedrosian, I., Xu, S., Koski, G., Roros, J. G., Moise, M. A., Nguyen, H. Q., Engels, F. H., Cohen, P. A. and Czerniecki, B. J., Calcium signaling inhibits interleukin-12 production and activates CD83+ dendritic cells that induce Th2 cell development. Blood 2001. 98: 2489-2497.
Wright, D. H., Metters, K. M., Abramovitz, M. and Ford-Hutchinson, A. W., Characterization of the recombinant human prostanoid DP receptor and identification of L-644,698, a novel selective DP agonist. Br. J. Pharmacol. 1998. 123: 1317-1324.
Monneret, G., Li, H., Vasilescu, J., Rokach, J. and Powell, W. S., 15-Deoxy-delta 12,14-prostaglandins D2 and J2 are potent activators of human eosinophils. J. Immunol. 2002. 168: 3563-3569.
Pai, R., Soreghan, B., Szabo, I., Pavelka, M., Baatar, D. and Tarnawski, A. S., PGE2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy. Nat. Med. 2002. 8: 289-293.
Tilley, S. L., Coffman, T. M. and Koller, B. H., Mixed messages: modulation of inflammation and immune responses by prostaglandins and thromboxanes. J. Clin. Invest. 2001. 108: 15-23.
Azuma, Y., Shinohara, M., Wang, P. L. and Ohura, K., 15-Deoxy-delta(12,14)-prostaglandin J2 inhibits IL-10 and IL-12 production by macrophages. Biochem. Biophys. Res. Commun. 2001. 283: 344-346.
Faveeuw, C., Fougeray, S., Angeli, V., Fontaine, J., Chinetti, G., Gosset, P., Delerive, P., Maliszewski, C., Capron, M., Staels, B., Moser, M. and Trottein, F., Peroxisome proliferator-activated receptor gamma activators inhibit interleukin-12 production in murine dendritic cells. FEBS Lett. 2000. 486: 261-266.
Gosset, P., Charbonnier, A. S., Delerive, P., Fontaine, J., Staels, B., Pestel, J., Tonnel, A. B. and Trottein, F., Peroxisome proliferator-activated receptor gamma activators affect the maturation of human monocyte-derived dendritic cells. Eur. J. Immunol. 2001. 31: 2857-2865.
Murphy, T. L., Cleveland, M. G., Kulesza, P., Magram, J. and Murphy, K. M., Regulation of interleukin 12 p40 expression through an NF-κB half-site. Mol. Cell. Biol. 1995. 15: 5258-5267.
Bureau, F., Delhalle, S., Bonizzi, G., Fievez, L., Dogne, S., Kirschvink, N., Vanderplasschen, A., Merville, M. P., Bours, V. and Lekeux, P., Mechanisms of persistent NF-κB activity in the bronchi of an animal model of asthma. J. Immunol. 2000. 165: 5822-5830.
Parry, G. C. and Mackman, N., Role of cyclic AMP response element-binding protein in cyclic AMP inhibition of NF-κB-mediated trancription. J. Immunol. 1997. 159: 5450-5456.