Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Upregulation of Lipopolysaccharide-Induced Interleukin-10 by Prostaglandin $A_1$ in Mouse Peritoneal Macrophages

  • Kim, Hyo-Young (Department of Microbiology, Aging-associated Vascular Disease Research Center, College of Medicine, Yeungnam University) ;
  • Kim, Jae-Ryong (Department of Biochemistry and Molecular Biology, Aging-associated Vascular Disease Research Center, College of Medicine, Yeungnam University) ;
  • Kim, Hee-Sun (Department of Microbiology, Aging-associated Vascular Disease Research Center, College of Medicine, Yeungnam University)
  • Published : 2008.06.30
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Abstract

The cyclopentenone prostaglandins (cyPGs) prostaglandin $A_1$ ($PGA_1$) and 15-deoxy-${\Delta}^{12,14}$-prostaglandin $J_2$ (15d-$PGJ_2$) have been reported to exhibit antiinflammatory activity in activated monocytes/macrophages. However, the effects of these two cyPGs on the expression of cytokine genes may differ. In this study, we investigated the mechanism of action of $PGA_1$ in lipopolysaccharide (LPS)-induced expression of inter leu kin (IL)-10 mRNA in mouse peritoneal macrophages. 15d-$PGJ_2$ inhibited expression of LPS-induced IL-10, whereas $PGA_1$ increased LPS-induced IL-10 expression. This synergistic effect of $PGA_1$ on LPS-induced IL-10 expression reached a maximum as early as 2 h after simultaneous $PGA_1$ and LPS treatment ($PGA_1$/LPS), and did not require new protein synthesis. The synergistic effect of $PGA_1$ was inhibited by GW9662, a specific peroxisome proliferator-activated receptor ${\gamma}(PPAR{\gamma})$ antagonist, and Bay-11-7082, a NF-${\kappa}B$ inhibitor. The extracellular signal-regulated kinases (ERK) inhibitor PD98059 increased the expression of $PGA_1$/LPS-induced IL-10 mRNA, rather than inhibiting the IL-10 expression. Moreover, $PGA_1$ inhibited LPS-induced ERK phosphorylation. The synergistic effect of $PGA_1$ on LPS-induced IL-10 mRNA and protein production was inhibited by p38 inhibitor PD169316, and $PGA_1$ increased LPS-induced p38 phosphorylation. In the case of stress-activated protein kinase/c-Jun $NH_2$-terminal kinase (SAPK/JNK), the SAPK/JNK inhibitor SP600125 did not inhibit IL-10 mRNA synthesis but inhibited the production of IL-10 protein remarkably. These results suggest that the synergistic effect of $PGA_1$ on LPS-induced IL-10 expression is NF-${\kappa}B$-dependent and mediated by mitogen-activated protein (MAP) kinases, p38, and SAPK/JNK signaling pathways, and also associated with the $PPAR{\gamma}$ pathway. Our data may provide more insight into the diverse mechanisms of $PGA_1$ effects on the expression of cytokine genes.

Keywords

References

  1. Alleva, D. G., E. B. Johnson, F. M. Lio, S. A. Boehme, P. J. Conlon, and P. D. Crowe. 2002. Regulation of murine macrophage proinflammatory and anti-inflammatory cytokines by ligands for peroxisome proliferator-activated receptor-${\gamma}$: Counter-regulatory activity by IFN-${\gamma}$. J. Leukoc. Biol. 71: 677- 685
  2. Azuna, Y., M. Shinohara, P. L. Wang, and K. Ohura. 2001. 15- Deoxy-${\Delta}^{12.14}$-prostaglandin $J_2$ inhibits IL-10 and IL-12 production by macrophages. Biochem. Biophys. Res. Commun. 283: 344- 346 https://doi.org/10.1006/bbrc.2001.4783
  3. Bureau, F., C. Desmet, D. Melotte, F. Jaspar, C. Volanti, A. Vanderplasschen, P. P. Pastoret, J. Piette, and P. Lekeux. 2002. A proinflammatory role for the cyclopentenone prostaglandins at low micromolar concentrations: Oxidative stress-induced extracellular signal-regulated kinase activation without NFkappa B inhibition. J. Immunol. 168: 5318-5325 https://doi.org/10.4049/jimmunol.168.10.5318
  4. Chinetti, G., J. C. Fruchart, and B. Staels. 2000. Peroxisome proliferator-activated receptors (PPARs): Nuclear receptors at the crossroads between lipid metabolism and inflammation. Inflamm. Res. 49: 497-505 https://doi.org/10.1007/s000110050622
  5. Clark, R. B. 2002. The role of PPARs in inflammation and immunity. J. Leukoc. Biol. 71: 388-400
  6. Cunard, R., M. Ricote, D. DiCampli, D. C. Archer, D. A. Kahn, C. K. Glass, C. J. Kelly, and M. Ricote. 2002. Regulation of cytokine expression by ligands of peroxisome proliferator activated receptors. J. Immunol. 168: 2795-2802 https://doi.org/10.4049/jimmunol.168.6.2795
  7. Cuzzocrea, S., N. S. Wayman, E. Mazzon, L. Dugo, R. Di Paola, I. Serraino, et al. 2002. The cyclopentenone prostaglandin 15-deoxy-$\Delta^{12.14}$-prostaglandin $J_2$ attenuates the development of acute and chronic inflammation. Mol. Pharmacol. 61: 997- 1007 https://doi.org/10.1124/mol.61.5.997
  8. Erl, W., C. Weber, A. Zernecke, J. Neuzil, C. A. Vosseler, H. J. Kim, and P. C. Weber. 2004. Cyclopentenone prostaglandins induce endothelial cell apoptosis independent of the peroxisome proliferator-activated receptor-$\gamma$. Eur. J. Immunol. 34: 241-250 https://doi.org/10.1002/eji.200324053
  9. Fu, Y., N. Luo, and M. F. Lopes-Virella. 2002. Upregulation of interleukin-8 expression by prostaglandin $J_2$ $(15d-PGJ_2)$ in human THP-1 macrophages. Atherosclerosis 160: 11-20 https://doi.org/10.1016/S0021-9150(01)00541-X
  10. Harris, S. G., R. S. Smith, and R. P. Phipps. 2002. 15-Deoxy- $\Delta^{12.14}-PGJ_2$ induces IL-8 production in human T cells by a mitogen-activated protein kinase pathway. J. Immunol. 168: 1372-1379 https://doi.org/10.4049/jimmunol.168.3.1372
  11. Jiang, C., A. T. Ting, and B. Seed. 1998. PPAR-$\gamma$ agonists inhibit production of monocyte inflammatory cytokines. Nature 391: 82-86 https://doi.org/10.1038/34184
  12. Jostarndt, K., T. Rubic, H. Kuhn, M. W. Anthosen, L. Andera, N. Gellert, et al. 2004. Enzymatically modified low-density lipoprotein upregulates CD36 in low-differentiated monocytic cells in a peroxisome proliferator-activated receptor-$gamma$-dependent way. Biochem. Pharmacol. 67: 841-854 https://doi.org/10.1016/j.bcp.2003.09.041
  13. Kelly, G., B. Robert, R. Chris, G. Gary, H. Perry, and C. James. 2001. Differential effects of 15-deoxy-$\Delta^{12.14}$-prostaglandin $J_2$ and a peroxisome proliferator-activated receptor $\gamma$ agonist on macrophage activation. J. Leukoc. Biol. 69: 631-638
  14. Kim, H. Y., H. K. Kim, J. R. Kim, and H. S. Kim. 2005. Upregulation of LPS-induced chemokine KC expression by 15- deoxy-$\Delta^{12.14}$-prostaglandin $J_2$ in mouse peritoneal macrophages. Immunol. Cell Biol. 83: 286-293
  15. Kim, H. Y. and H. S. Kim. 2007. Upregulation of MIP-2 (CXCL2) expression by 15-deoxy-$\Delta^{12,\;14}$-prostaglandin $J_2$ in mouse peritoneal macrophages. Immunol. Cell Biol. 85: 60-67
  16. Kim, H. Y., J. R. Kim, and H. S. Kim. 2006. Synergistic effect of interleukin-10 on the expression of lipopolysaccharide-induced IP-10 (CXCL-10) mRNA in mouse peritoneal macrophges. J. Microbiol. Biotechnol. 16: 1605-1612
  17. Kim, J. E., H. J. Hur, K. W. Lee, and H. J. Lee. 2007. Antiinflammatory effects of recombinant arginine deiminase originating from Lactococcus lactis ssp. lactis ATCC 7962. J. Microbiol. Biotechnol. 17: 1491-1497
  18. Lee, D. E., H. Y. Kim, I. H. Song, S. K. Kim, J. H. Seul, and H. S. Kim. 2004. Effect of leptin on the expression of lipopolysaccharide-induced chemokine KC mRNA in the mouse peritoneal macrophages. J. Microbiol. Biotechnol. 14: 722-729
  19. Marx, N., F. Mach, A. Sauty, J. H. Leung, M. N. Sarafi, R. M. Randohoff, P. Libby, J. Plutzky, and A. D. Luster. 2000. Peroxisome proliferator-activated receptor-${\gamma}$ activators inhibit IFN-$\gamma$-induced expression of the T cell-active CXC chemokines IP-10, Mig, and I-TAC in human endothelial cells. J. Immunol. 164: 6503-6508 https://doi.org/10.4049/jimmunol.164.12.6503
  20. Masamune, A., K. Kikuta, M. Satoh, Y. Sakai, A. Satoh, and T. Shimosegawa. 2002. Ligands of peroxisome proliferator activated receptor-$\gamma$ block activation of pancreatic stellate cells. J. Biol. Chem. 277: 141-147 https://doi.org/10.1074/jbc.M107582200
  21. Meade, E. A., T. M. Mcintyre, G. A. Zimmerman, and S. M. Prescott. 1999. Peroxisome proliferators enhance cyclooxygenase- 2 expression in epithelial cells. J. Biol. Chem. 274: 8328-8334 https://doi.org/10.1074/jbc.274.12.8328
  22. Reilly, C. M., J. C. Oates, J. Suidan, M. B. Crosby, P. V. Halushka, and G. S. Gilkeson. 2001. Prostaglandin $J_2$ inhibition of mesangial cell iNOS expression. Clin. Immunol. 3: 337-345
  23. Ricote, M., A. C. Li, T. M. Willson, C. J. Kelly, and C. K. Glass. 1998. The peroxisome proliferator-activated receptor-$\gamma$ is a negative regulator of macrophage activation. Nature 391: 79- 82 https://doi.org/10.1038/34178
  24. Ricote, M., J. T. Huang, J. S. Welch, and C. K. Glass. 1999. The peroxisome proliferator-activated receptor $\gamma$ (PPAR$\gamma$) as a regulator of monocyte/macrophage function. J. Leukoc. Biol. 66: 733-739 https://doi.org/10.1002/jlb.66.5.733
  25. Rosen, E. D., C. J. Walkey, P. Puigserver, and B. M. Spiegelman. 2000. Transcriptional regulation of adipogenesis. Genes Dev. 14: 1293-1307
  26. Rossi, A., G. Elia, and M. G. Santoro. 1997. Inhibition of nuclear factor $\kappa$B by prostaglandin A1: An effect associated with heat shock transcription factor activation. Proc. Natl. Acad. Sci. USA 94: 746-750
  27. Sawano, H., M. Haneda, T. Sugimoto, K. Inoki, D. Koya, and R. Kikkawa. 2002. 15-Deoxy-$\Delta^{12,\;14}$-prostaglandin $J_2$ inhibits IL- 1$\beta$-induced cyclooxygenase-2 expression in mesangial cells. Kidney Int. 61: 1957-1967 https://doi.org/10.1046/j.1523-1755.2002.00351.x
  28. Simonin, M. A., K. Bordji, S. Boyault, A. Bianchi, E. Gouze, P. Becume, M. Dauca, P. Netter, and B. Terlain. 2002. PPAR-$\gamma$ ligands modulate effects of LPS in stimulated rat synovial fibroblasts. Am. J. Physiol. Cell Physiol. 282: 125-133 https://doi.org/10.1152/ajpcell.2002.282.1.C125
  29. Straus, D. S. and C. K. Glass. 2001. Cyclopentenone prostaglandins: New insight on biological activities and cellular targets. Med. Res. Rev. 3: 185-210
  30. Straus, D. S., G. Pascual, M. Li, J. S. Welch, M. Ricote, C. H. Hsiang, L. L. Sengchanthalangsy, G. Ghosh, and C. K. Glass. 2000. 15-Deoxy-$\Delta^{12,\;14}$-prostaglandin $J_2$ inhibits multiple steps in the NF- $\kappa$B signaling pathway. Proc. Natl. Acad. Sci. USA 97: 4844-4849
  31. Wayman, N. S., Y. Hattori, M. C. McDonald, H. Mota-Filipe, S. Cuzzocrea, B. Pisano, P. K. Chatterjee, and C. Thiemermann. 2002. Ligands of the peroxisome proliferator-activated receptors (PPAR-gamma and PPAR-alpha) reduce myocardial infarct size. FASEB J. 16: 1027-1040 https://doi.org/10.1096/fj.01-0793com
  32. Wilmer, W. A., C. Dixon, L. Lu, T. Hilbelink, and B. H. Rovin. 2001. A cyclopentenone prostaglandin activates mesangial MAP kinase independently of PPAR$\gamma$ . Biochem. Biophys. Res.Commun. 281: 57-62 https://doi.org/10.1006/bbrc.2001.4301
  33. Zhang, X., J. M. Wang, W. H. Gong, N. Mukaida, and H. A. Young. 2001. Differential regulation of chemokine gene expression by 15-deoxy-$\Delta^{12,\;14}$-prostaglandin $J_2$ . J. Immunol. 166: 7104-7111 https://doi.org/10.4049/jimmunol.166.12.7104
  34. Zhao, M. L., C. F. Brosnan, and S. C. Lee. 2004. 15-Deoxydelta (12,14)-$PGJ_2$ inhibits astrocyte IL-1 signaling: Inhibition of NF-kappaB and MAP kinase pathways and suppression of cytokine and chemokine expression. J. Neuroimmunol. 153: 132-142 https://doi.org/10.1016/j.jneuroim.2004.05.003