Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2017, Article ID 3924912, 10 pages
https://doi.org/10.1155/2017/3924912
Research Article

15-Deoxy-Δ12,14-prostaglandin J2 Exerts Antioxidant Effects While Exacerbating Inflammation in Mice Subjected to Ureteral Obstruction

1Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
2Division of Integrative Physiology, Department of Medical Cell Biology, Uppsala University, Uppsala, Sweden
3Division of Drug Research, Department of Medical Health Sciences, Linköping University, Linköping, Sweden

Correspondence should be addressed to Rikke Nørregaard; kd.ua.nilc@nr

Received 28 November 2016; Revised 17 February 2017; Accepted 12 March 2017; Published 19 April 2017

Academic Editor: Babette B. Weksler

Copyright © 2017 Line Nilsson et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Dendooven, D. A. Ishola Jr, T. Q. Nguyen et al., “Oxidative stress in obstructive nephropathy,” International Journal of Experimental Pathology, vol. 92, no. 3, pp. 202–210, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. E. Ricciotti and G. A. FitzGerald, “Prostaglandins and inflammation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 5, pp. 986–1000, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. D. W. Gilroy, P. R. Colville-Nash, D. Willis, J. Chivers, M. J. Paul-Clark, and D. A. Willoughby, “Inducible cyclooxygenase may have anti-inflammatory properties,” Nature Medicine, vol. 5, no. 6, pp. 698–701, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Shibata, M. Kondo, T. Osawa, N. Shibata, M. Kobayashi, and K. Uchida, “15-deoxy-delta 12,14-prostaglandin J2. A prostaglandin D2 metabolite generated during inflammatory processes,” The Journal of Biological Chemistry, vol. 277, no. 12, pp. 10459–10466, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Zingarelli and J. A. Cook, “Peroxisome proliferator-activated receptor-gamma is a new therapeutic target in sepsis and inflammation,” Shock, vol. 23, no. 5, pp. 393–399, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. J. M. Kaplan, J. A. Cook, P. W. Hake, M. O'Connor, T. J. Burroughs, and B. Zingarelli, “15-deoxy-delta(12,14)-prostaglandin J(2) (15D-PGJ(2)), a peroxisome proliferator activated receptor gamma ligand, reduces tissue leukosequestration and mortality in endotoxic shock,” Shock, vol. 24, no. 1, pp. 59–65, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Abdelrahman, M. Collin, and C. Thiemermann, “The peroxisome proliferator-activated receptor-gamma ligand 15-deoxydelta12,14 prostaglandin J2 reduces the organ injury in hemorrhagic shock,” Shock, vol. 22, no. 6, pp. 555–561, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. M. A. Monroy, K. K. Opperman, M. Pucciarelli, S. Yerrum, D. A. Berg, and J. M. Daly, “The PPARgamma ligand 15d-PGJ2 modulates macrophage activation after injury in a murine trauma model,” Shock, vol. 28, no. 2, pp. 186–191, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Kobayashi, S. Ueki, G. Mahemuti et al., “Physiological levels of 15-deoxy-delta12,14-prostaglandin J2 prime eotaxin-induced chemotaxis on human eosinophils through peroxisome proliferator-activated receptor-gamma ligation,” Journal of Immunology, vol. 175, no. 9, pp. 5744–5750, 2005. View at Publisher · View at Google Scholar
  10. R. Schuligoi, E. Sturm, P. Luschnig et al., “CRTH2 and D-type prostanoid receptor antagonists as novel therapeutic agents for inflammatory diseases,” Pharmacology, vol. 85, no. 6, pp. 372–382, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Kansanen, A. M. Kivela, and A. L. Levonen, “Regulation of Nrf2-dependent gene expression by 15-deoxy-delta12,14-prostaglandin J2,” Free Radical Biology & Medicine, vol. 47, no. 9, pp. 1310–1317, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Itoh, M. Mochizuki, Y. Ishii et al., “Transcription factor Nrf2 regulates inflammation by mediating the effect of 15-deoxy-delta(12,14)-prostaglandin j(2),” Molecular and Cellular Biology, vol. 24, no. 1, pp. 36–45, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Nilsson, K. Madsen, S. Krag, J. Frøkiær, B. L. Jensen, and R. Norregaard, “Disruption of cyclooxygenase type 2 exacerbates apoptosis and renal damage during obstructive nephropathy,” American Journal of Physiology. Renal Physiology, vol. 309, no. 12, pp. 1035–1048, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Gurtler, N. Kunz, M. Gomolka et al., “Stain-free technology as a normalization tool in western blot analysis,” Analytical Biochemistry, vol. 433, no. 2, pp. 105–111, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Dalle-Donne, R. Rossi, D. Giustarini, A. Milzani, and R. Colombo, “Protein carbonyl groups as biomarkers of oxidative stress,” Clinica Chimica Acta, vol. 329, no. 1-2, pp. 23–38, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Ghosh and M. Karin, “Missing pieces in the NF-kappaB puzzle,” Cell, vol. 109, Supplement 1, no. 2, pp. S81–S96, 2002. View at Google Scholar
  17. D. S. Kang, C. H. Kwon, J. Y. Park et al., “15-deoxy-delta12,14-prostaglandin J2 induces renal epithelial cell death through NF-kappaB-dependent and MAPK-independent mechanism,” Toxicology and Applied Pharmacology, vol. 216, no. 3, pp. 426–435, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. D. R. Lee, C. H. Kwon, J. Y. Park, Y. K. Kim, and J. S. Woo, “15-deoxy-delta(12,14)-prostaglandin J(2) induces mitochondrial-dependent apoptosis through inhibition of PKA/NF-kappaB in renal proximal epithelial cells,” Toxicology, vol. 258, no. 1, pp. 17–24, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. Lin, Y. Chen, J. Lv et al., “Kidney injury molecule-1 expression in IgA nephropathy and its correlation with hypoxia and tubulointerstitial inflammation,” American Journal of Physiology. Renal Physiology, vol. 306, no. 8, pp. F885–F895, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Kinter, J. T. Wolstenholme, B. A. Thornhill, E. A. Newton, M. L. McCormick, and R. L. Chevalier, “Unilateral ureteral obstruction impairs renal antioxidant enzyme activation during sodium depletion,” Kidney International, vol. 55, no. 4, pp. 1327–1334, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. B. H. Choi, K. S. Kang, and M. K. Kwak, “Effect of redox modulating NRF2 activators on chronic kidney disease,” Molecules, vol. 19, no. 8, pp. 12727–12759, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. S. D. Chung, T. Y. Lai, C. T. Chien, and H. J. Yu, “Activating nrf-2 signaling depresses unilateral ureteral obstruction-evoked mitochondrial stress-related autophagy, apoptosis and pyroptosis in kidney,” PloS One, vol. 7, no. 10, Article ID e47299, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Chung, H. E. Yoon, S. J. Kim et al., “Oleanolic acid attenuates renal fibrosis in mice with unilateral ureteral obstruction via facilitating nuclear translocation of Nrf2,” Nutrition & Metabolism (London), vol. 11, no. 1, p. 2, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. H. J. Kim and N. D. Vaziri, “Contribution of impaired Nrf2-Keap1 pathway to oxidative stress and inflammation in chronic renal failure,” American Journal of Physiology. Renal Physiology, vol. 298, no. 3, pp. F662–F671, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. X. Zhang, L. Lu, C. Dixon et al., “Stress protein activation by the cyclopentenone prostaglandin 15-deoxy-delta12,14-prostaglandin J2 in human mesangial cells,” Kidney International, vol. 65, no. 3, pp. 798–810, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. J. Zhang, X. Yang, Q. Y. Kong et al., “Effect of 15d-PGJ2 on the expression of CD40 and RANTES induced by IFN-gamma and TNF-alpha on renal tubular epithelial cells (HK-2),” American Journal of Nephrology, vol. 26, no. 4, pp. 356–362, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. X. Li, H. Kimura, K. Hirota et al., “Hypoxia reduces the expression and anti-inflammatory effects of peroxisome proliferator-activated receptor-gamma in human proximal renal tubular cells,” Nephrology, Dialysis, Transplantation, vol. 22, no. 4, pp. 1041–1051, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Bancos, C. J. Baglole, I. Rahman, and R. P. Phipps, “Induction of heme oxygenase-1 in normal and malignant B lymphocytes by 15-deoxy-delta(12,14)-prostaglandin J(2) requires Nrf2,” Cellular Immunology, vol. 262, no. 1, pp. 18–27, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. E. M. Sikorski, T. Hock, N. Hill-Kapturczak, and A. Agarwal, “The story so far: molecular regulation of the heme oxygenase-1 gene in renal injury,” American Journal of Physiology. Renal Physiology, vol. 286, no. 3, pp. F425–F441, 2004. View at Publisher · View at Google Scholar
  30. V. Esteban, O. Lorenzo, M. Ruperez et al., “Angiotensin II, via AT1 and AT2 receptors and NF-kappaB pathway, regulates the inflammatory response in unilateral ureteral obstruction,” Journal of the American Society of Nephrology, vol. 15, no. 6, pp. 1514–1529, 2004. View at Google Scholar
  31. J. U. Scher and M. H. Pillinger, “The anti-inflammatory effects of prostaglandins,” Journal of Investigative Medicine, vol. 57, no. 6, pp. 703–708, 2009. View at Publisher · View at Google Scholar
  32. P. K. Chatterjee, N. S. Patel, S. Cuzzocrea et al., “The cyclopentenone prostaglandin 15-deoxy-delta(12,14)-prostaglandin J2 ameliorates ischemic acute renal failure,” Cardiovascular Research, vol. 61, no. 3, pp. 630–643, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. D. A. Jans and S. Hubner, “Regulation of protein transport to the nucleus: central role of phosphorylation,” Physiological Reviews, vol. 76, no. 3, pp. 651–685, 1996. View at Google Scholar
  34. D. S. Straus, G. Pascual, M. Li et al., “15-deoxy-delta 12,14-prostaglandin J2 inhibits multiple steps in the NF-kappa B signaling pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 9, pp. 4844–4849, 2000. View at Google Scholar
  35. A. E. Martinez, F. J. Sanchez-Gomez, B. Diez-Dacal, C. L. Oeste, and D. Perez-Sala, “15-deoxy-delta(12,14)-prostaglandin J2 exerts pro- and anti-inflammatory effects in mesangial cells in a concentration-dependent manner,” Inflammation & Allergy Drug Targets, vol. 11, no. 1, pp. 58–65, 2012. View at Publisher · View at Google Scholar
  36. A. Castrillo, P. G. Traves, P. Martin-Sanz, S. Parkinson, P. J. Parker, and L. Bosca, “Potentiation of protein kinase C zeta activity by 15-deoxy-delta(12,14)-prostaglandin J(2) induces an imbalance between mitogen-activated protein kinases and NF-kappa B that promotes apoptosis in macrophages,” Molecular and Cellular Biology, vol. 23, no. 4, pp. 1196–1208, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Reyes-Martin, M. Alique, T. Parra, J. P. Hornedo, and J. Lucio-Cazana, “Cyclooxygenase-independent inhibition of H2O2-induced cell death by S-ketoprofen in renal cells,” Pharmacological Research, vol. 55, no. 4, pp. 295–302, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Chen, J. Li, J. Wang et al., “15-deoxy- gamma 12,14-prostaglandin J2 reduces liver impairment in a model of ConA-induced acute hepatic inflammation by activation of PPAR gamma and reduction in NF- kappa B activity,” PPAR Research, vol. 2014, p. 215631, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. R. G. Townley and S. Agrawal, “CRTH2 antagonists in the treatment of allergic responses involving TH2 cells, basophils, and eosinophils,” Annals of Allergy, Asthma & Immunology, vol. 109, no. 6, pp. 365–374, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Ito, X. Yan, N. Nagata et al., “PGD2-CRTH2 pathway promotes tubulointerstitial fibrosis,” Journal of the American Society of Nephrology, vol. 23, no. 11, pp. 1797–1809, 2012. View at Publisher · View at Google Scholar · View at Scopus