IL-18 associates to microvesicles shed from human macrophages by a LPS/TLR-4 independent mechanism in response to P2X receptor stimulation

European Journal of Immunology

Volumn 42, Issue 12, 2012, Pages 3334-3345

  Gulinelli, Sara ^a   Salaro, Erica ^a   Vuerich, Marta ^a   Bozzato, Dania ^a   Pizzirani, Cinzia ^a   Bolognesi, Giorgio ^a   Idzko, Marco ^b   Virgilio, Francesco Di ^a   Ferrari, Davide ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Extracellular ATP; Human macrophages; IL 18; P2 receptors; P2X7

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; ADENOSINE TRIPHOSPHATE; CALCIMYCIN; CASPASE INHIBITOR; INTERLEUKIN 18; LIPOPOLYSACCHARIDE; PHOSPHATIDYLSERINE; POLYMYXIN B; PURINERGIC P2X RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; PURINERGIC RECEPTOR STIMULATING AGENT; TOLL LIKE RECEPTOR 4;

ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; CYTOSKELETON; EX VIVO STUDY; HUMAN; HUMAN CELL; INHIBITION KINETICS; MEMBRANE PERMEABILITY; MICROVESICLE; MOLECULAR MECHANICS; PRIORITY JOURNAL; STIMULATION; WESTERN BLOTTING;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ACETAMIDES; ADENOSINE TRIPHOSPHATE; ANTI-BACTERIAL AGENTS; CALCIMYCIN; CALCIUM IONOPHORES; CELL-DERIVED MICROPARTICLES; HUMANS; INTERLEUKIN-18; LIPOPOLYSACCHARIDES; MACROPHAGES; POLYMYXIN B; PROTEIN PRECURSORS; PURINERGIC P2X RECEPTOR AGONISTS; PURINERGIC P2X RECEPTOR ANTAGONISTS; PYRIDINES; QUINOLINES; RECEPTORS, PURINERGIC P2X4; RECEPTORS, PURINERGIC P2X7; SULFONAMIDES; TETRAZOLES; TOLL-LIKE RECEPTOR 4;

EID: 84871348057     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142268     Document Type: Article

References (49)

1. Inal, J. M., Ansa-Addo, E. A., Stratton, D., Kholia, S., Antwi-Baffour, S. S., Jorfi, S. and Lange, S., Microvesicles in health and disease. Arch. Immunol. Ther. Exp. (Warsz) 2012. 60: 107-121.
2. Turola, E., Furlan, R., Bianco, F., Matteoli, M. and Verderio, C., Microglial microvesicle secretion and intercellular signaling. Front. Physiol. 2012. 3: 149.
3. Sarkar, A., Mitra, S., Mehta, S., Raices, R. and Wewers, M. D., Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS One 2009. 4: e7140.
4. Wang, J. G., Williams, J. C., Davis, B. K., Jacobson, K., Doerschuk, C. M., Ting, J. P. and Mackman, N., Monocytic microparticles activate endothelial cells in an IL-1β-dependent manner. Blood 2011. 118: 2366-2374.
5. Mokarizadeh, A., Delirezh, N., Morshedi, A., Mosayebi, G., Farshid, A. A. and Mardani, K., Microvesicles derived from mesenchymal stem cells: potent organelles for induction of tolerogenic signaling. Immunol. Lett. 2012. 147: 47-54.
6. MacKenzie, A., Wilson, H. L., Kiss-Toth, E., Dower, S. K., North, R. A. and Surprenant, A., Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 2001. 15: 825-835.
7. Okamura, H., Tsutsi, H., Komatsu, T., Yutsudo, M., Hakura, A., Tanimoto, T., Torigoe, K. et al., Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995. 378: 88-91.
8. Akira, S., The role of IL-18 in innate immunity. Curr. Opin. Immunol. 2000. 12: 59-63.
9. Boraschi, D. and Dinarello, C. A., IL-18 in autoimmunity. Eur. Cytokine. Netw. 2006. 17: 224-252.
10. Puren, A. J., Fantuzzi, G., Gu, Y., Su, M. S. and Dinarello, C. A., Interleukin-18 (IFNgamma-inducing factor) induces IL-8 and IL-1beta via TNFalpha production from non-CD14+ human blood mononuclear cells. J. Clin. Invest. 1998. 101: 711-721.
11. McInnes, I. B., Gracie, J. A., Leung, B. P., Wie, X. Q. and Liew, F. Y., Interleukin 18: a pleiotropic participant in chronic inflammation. Immunol. Today 2000. 21: 312-315.
12. Ghayur, T., Banerjee, S., Hugunin, M., Butler, D., Herzog, L., Carter, A., Quintal, L. et al., Caspase-1 processes IFN-gamma-inducing factor and regulates LPS-induced IFN-gamma production. Nature 1997. 386: 619-623.
13. Gu, Y., Kuidam, K., Tsutsuim, H., Kum, G., Hsiaom, K., Flemingm, M. A., Hayashi, N. et al., Activation of interferon-gamma inducing factor mediated by interleukin-1beta converting enzyme. Science 1997. 275: 206-209.
14. Ushio, S., Namba, M., Okura, T., Hattori, K., Nukada, Y., Akita, K., Tanabe, F. et al., Cloning of the cDNA for human IFN-gamma-inducing factor, expression in Escherichia coli, and studies on the biologic activities of the protein. J. Immunol. 1996. 156: 4274-4279.
15. Abbracchio, M. P. and Burnstock, G., Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol. Ther. 1994. 64: 445-475.
16. von Kügelgen, I. and Wetter, A., Molecular pharmacology of P2Y-receptors. Naunyn Schmiedebergs Arch. Pharmacol. 362: 310-323.
17. Seman, M., Adriouch, S., Scheuplein, F., Krebs, C., Freese, D., Glowacki, G., Deterre, P. et al., NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 2003. 19: 571-582.
18. Di Virgilio, F., Chiozzi, P., Ferrari, D., Falzoni, S., Sanz, J. M., Morelli, A., Torboli, M. et al., Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 2001. 97: 587-600.
19. el-Moatassim, C. and Dubyak, G. R., A novel pathway for the activation of phospholipase D by P2z purinergic receptors in BAC1.2F5 macrophages. J. Biol. Chem. 1992. 267: 23664-23673.
20. Hu, Y., Fisette, P. L., Denlinger, L. C., Guadarrama, A. G., Sommer, J. A., Proctor, R. A. and Bertics, P. J., Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages. J. Biol. Chem. 1998. 273: 27170-27175.
21. Aga, M., Watters, J. J., Pfeiffer, Z. A., Wiepz, G. J., Sommer, J. A. and Bertics, P. J., Evidence for nucleotide receptor modulation of cross talk between MAP kinase and NF-kappa B signaling pathways in murine RAW 264.7 macrophages. Am. J. Physiol. Cell. Physiol. 2004. 286: C923-C930.
22. Falzoni, S., Chiozzi, P., Ferrari, D., Buell, G. and Di Virgilio, F., P2X(7) receptor and polykarion formation. Mol. Biol. Cell 2000. 11: 3169-3176.
23. Lister, M. F., Sharkey, J., Sawatzky, D. A., Hodgkiss, J. P., Davidson, D. J., Rossi, A. G. and Finlayson, K., The role of the purinergic P2X7 receptor in inflammation. J. Inflamm. (Lond.) 2007. 4: 5.
24. Pizzirani, C., Ferrari, D., Chiozzi, P., Adinolfi, E., Sandonà, D., Savaglio, E. and Di Virgilio, F., Stimulation of P2 receptors causes release of IL-1beta-loaded microvesicles from human dendritic cells. Blood 2007. 109: 3856-3864.
25. Gallucci, S. and Matzinger, P., Danger signals: SOS to the immune system. Curr. Opin. Immunol. 2001. 13: 114-119.
26. Mehta, V. B., Hart, J. and Wewers, M. D., ATP-stimulated release of interleukin (IL)-1beta and IL-18 requires priming by lipopolysaccharide and is independent of caspase-1 cleavage. J. Biol. Chem. 2001. 276: 3820-3826.
27. Piccini, A., Carta, S., Tassi, S., Lasiglié, D., Fossati, G. and Rubartelli, A., ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc. Natl. Acad. Sci. USA 2008. 105: 8067-8072.
28. Perregaux, D. G., McNiff, P., Laliberte, R., Conklyn, M. and Gabel, C. A., Identification and characterization of a novel class of interleukin-1 post-translational processing inhibitors. J. Immunol. 2000. 165: 4615-4623.
29. Obregon, C., Rothen-Rutishauser, B., Gitahi, S. K., Gehr, P. and Nicod, L. P., Exovesicles from human activated dendritic cells fuse with resting dendritic cells, allowing them to present alloantigens. Am. J. Pathol. 2006. 169: 2127-2136.
30. Aoki, N., Jin-No, S., Nakagawa, Y., Asai, N., Arakawa, E., Tamura, N., Tamura, T. et al., Identification and characterization of microvesicles secreted by 3T3-L1 adipocytes: redox- and hormone-dependent induction of milk fat globule-epidermal growth factor 8-associated microvesicles. Endocrinology 2007. 148: 3850-3862.
31. Bianco, F., Pravettoni, E., Colombo, A., Schenk, U., Moller, T., Matteoli, M. and Verderio, C., Astrocyte-derived ATP induces vesicle shedding and IL-1 beta release from microglia. J. Immunol. 2005. 174: 7268-7277.
32. Pelegrin, P. and Surprenant, A., Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J. 2006. 25: 5071-5082.
33. Andrei, C., Margiocco, P., Poggi, A., Lotti, L. V., Torrisi, M. R. and Rubartelli, A., Phospholipases C and A2 control lysosome-mediated IL-1 beta secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. USA 2004. 101: 10241-10242.
34. Gardella, S., Andrei, C., Poggi, A., Zocchi, M. R. and Rubartelli, A., Control of interleukin-18 secretion by dendritic cells: role of calcium influxes. FEBS Lett. 2000. 481: 245-248.
35. Perregaux, D., Barberia, J., Lanzetti, A. J., Geoghegan, K. F., Carty, T. J. and Gabel, C. A., IL-1 beta maturation: evidence that mature cytokine formation can be induced specifically by nigericin. J. Immunol. 1992. 149: 1294-303.
36. Walev, I., Reske, K., Palmer, M., Valeva, A. and Bhakdi, S., Potassium-inhibited processing of IL-1 beta in human monocytes. EMBO J. 1995. 14: 1607-1614.
37. Hentze, H., Lin, X. Y., Choi, M. S. and Porter, A. G., Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1-independent necrosis triggered by the microbial toxin nigericin. Cell Death Differ. 2003. 10: 956-968.
38. Tsubery, H., Ofek, I., Cohen, S. and Fridkin, M., The functional association of polymyxin B with bacterial lipopolysaccharide is stereospecific: studies on polymyxin B nonapeptide. Biochemistry 2000. 39: 11837-11844.
39. Cuéllar, A., Fonseca, A. and Gómez, A., Effect of lipopolysaccharides on human dendritic cell cultures and its inhibition by polymyxin B. Biomedica 2004. 24: 413-422.
40. Guo, Y. B., Chen, L. P., Cao, H. W., Wang, N., Zheng, J. and Xiao, G. X., Polymyxin B antagonizing biological activity of lipopolysaccharide. Chin. J. Traumatol. 2007. 10: 180-183.
41. Ferrari, D., Pizzirani, C., Adinolfi, E., Forchap, S., Sitta, B., Turchet, L., Falzoni, S. et al., The antibiotic polymyxin B modulates P2X7 receptor function. J. Immunol. 2004. 173: 4652-4660.
42. Ferrari, D., Pizzirani, C., Gulinelli, S., Callegari, G., Chiozzi, P., Idzko, M., Panther, E. and Di Virgilio, F., Modulation of P2X7 receptor functions by polymyxin B: crucial role of the hydrophobic tail of the antibiotic molecule. Br. J. Pharmacol. 2007. 150: 445-454.
43. Noreen, M., Shah, M. A., Mall, S. M., Choudhary, S., Hussain, T., Ahmed, I., Jalil, S. F. and Raza, M. I., TLR4 polymorphisms and disease susceptibility. Inflamm. Res. 2012. 61: 177-188.
44. Arican, O., Aral, M., Sasmaz, S. and Ciragil, P., Serum levels of TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm. 2005. 5: 273-279.
45. Bellora, F., Castriconi, R., Doni, A., Cantoni, C., Moretta, L., Mantovani, A., Moretta, A. et al., M-CSF induces the expression of a membrane-bound form of IL-18 in a subset of human monocytes differentiating in vitro toward macrophages. Eur. J. Immunol. 42: 1618-1626.
46. Qu, Y., Misaghi, S., Newton, K., Gilmour, L. L., Louie, S., Cupp, J. E., Dubyak, G. R. et al., Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J. Immunol. 2011. 186: 6553-6561.
47. Pirhonen, J., Sareneva, T., Julkunen, I. and Matikainen, S., Virus infection induces proteolytic processing of IL-18 in human macrophages via caspase-1 and caspase-3 activation. Eur. J. Immunol. 2001. 31: 726-733.
48. Fantuzzi, G., Reed, D. A. and Dinarello, C. A., IL-12-induced IFN-gamma is dependent on caspase-1 processing of the IL-18 precursor. J. Clin. Invest. 1999. 104: 761-767.
49. Tsutsui, H., Kayagaki, N., Kuida, K., Nakano, H., Hayashi, N., Takeda, K., Matsui, K. et al., Caspase-1-independent, Fas/Fas ligand-mediated IL-18 secretion from macrophages causes acute liver injury in mice. Immunity 1999. 11: 359-367.