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Oxidative Medicine and Cellular Longevity
Volume 2014, Article ID 148798, 10 pages
http://dx.doi.org/10.1155/2014/148798
Research Article

Atorvastatin Represses the Angiotensin 2-Induced Oxidative Stress and Inflammatory Response in Dendritic Cells via the PI3K/Akt/Nrf 2 Pathway

1Shanghai Institute of Cardiovascular Diseases, Zhongshan Hospital, Fudan University, 180 Fenglin Road, Shanghai 200032, China
2Institute of Biomedical Science, Fudan University, 138 Yixueyuan Road, Shanghai 200032, China

Received 12 March 2014; Revised 11 June 2014; Accepted 11 June 2014; Published 3 July 2014

Academic Editor: Ryuichi Morishita

Copyright © 2014 Yuanji Ma 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. G. K. Hansson, “Inflammation, atherosclerosis, and coronary artery disease,” The New England Journal of Medicine, vol. 352, no. 16, pp. 1685–1695, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. W. Cao, Y. V. Bobryshev, R. S. Lord, R. E. Oakley, S. H. Lee, and J. Lu, “Dendritic cells in the arterial wall expresses C1q: potential significance in atherogenesis,” Cardiovascular Research, vol. 60, no. 1, pp. 175–186, 2003. View at Google Scholar
  3. Y. V. Bobryshev, “Dendritic cells in atherosclerosis: current status of the problem and clinical relevance,” European Heart Journal, vol. 26, no. 17, pp. 1700–1704, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. K. A. Nahmod, M. E. Vermeulen, S. Raiden et al., “Control of dendritic cell differentiation by angiotensin II,” The FASEB Journal, vol. 17, no. 3, pp. 491–493, 2003. View at Google Scholar · View at Scopus
  5. J. Sun, K. Hartvigsen, M. Y. Chou et al., “Deficiency of antigen-presenting cell invariant chain reduces atherosclerosis in mice,” Circulation, vol. 122, no. 8, pp. 808–820, 2010. View at Publisher · View at Google Scholar
  6. J. Ge, Q. Jia, C. Liang et al., “Advanced glycosylation end products might promote atherosclerosis through inducing the immune maturation of dendritic cells,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 10, pp. 2157–2163, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. RR. Packard, E. Maganto-García, I. Gotsman et al., “CD11c(+) dendritic cells maintain antigen processing, presentation capabilities, and CD4(+) T-cell priming efficacy under hypercholesterolemic conditions associated with atherosclerosis,” Circulation Research, vol. 103, no. 9, pp. 965–973, 2008. View at Publisher · View at Google Scholar
  8. E. L. Schiffrin and R. M. Touyz, “From bedside to bench to bedside: role of renin-angiotensin-aldosterone system in remodeling of resistance arteries in hypertension,” The American Journal of Physiology: Heart and Circulatory Physiology, vol. 287, no. 2, pp. H435–H446, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Sicard, S. Delemasure, C. Korandji et al., “Anti-hypertensive effects of rosuvastatin are associated with decreased inflammation and oxidative stress markers in hypertensive rats,” Free Radical Research, vol. 42, no. 3, pp. 226–236, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. O. Adam and U. Laufs, “Antioxidative effects of statins,” Archives of Toxicology, vol. 82, no. 12, pp. 885–892, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. M.-S. Zhou, E. A. Jaimes, and L. Raij, “Atorvastatin prevents end-organ injury in salt-sensitive hypertension: Role of eNOS and oxidant stress,” Hypertension, vol. 44, no. 2, pp. 186–190, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. A. R. Collins, C. J. Lyon, X. Xia et al., “Age-accelerated atherosclerosis correlates with failure to upregulate antioxidant genes,” Circulation Research, vol. 104, no. 6, pp. e42–e54, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Freigang, F. Ampenberger, G. Spohn et al., “Nrf2 is essential for cholesterol crystal-induced inflammasome activation and exacerbation of atherosclerosis,” European Journal of Immunology, vol. 41, no. 7, pp. 2040–2051, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Ishii, K. Itoh, S. Takahashi et al., “Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages,” The Journal of Biological Chemistry, vol. 275, no. 21, pp. 16023–16029, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. P. Hwang and H. G. Jeong, “Ginsenoside Rb1 protects against 6-hydroxydopamine-induced oxidative stress by increasing heme oxygenase-1 expression through an estrogen receptor-related PI3K/Akt/Nrf2-dependent pathway in human dopaminergic cells,” Toxicology and Applied Pharmacology, vol. 242, no. 1, pp. 18–28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. N. Nguyen, H. E. Kim, and S. G. Lee, “Caffeoylserotonin protects human keratinocyte HaCaT cells against H2O2 -induced oxidative stress and apoptosis through upregulation of HO-1 expression via activation of the PI3K/ Akt / Nrf 2 pathway,” Phytotherapy Research, vol. 27, no. 12, pp. 1810–1818, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. W. Su, A. Sun, D. Xu et al., “Tongxinluo inhibits oxidized low-density lipoprotein-induced maturation of human dendritic cells via activating peroxisome proliferator-activated receptor gamma pathway,” Journal of Cardiovascular Pharmacology, vol. 56, no. 2, pp. 177–183, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Sun, H. Liu, S. Wang et al., “Salvianolic acid B suppresses maturation of human monocyte-derived dendritic cells by activating PPARγ,” British Journal of Pharmacology, vol. 164, no. 8, pp. 2042–2053, 2011. View at Publisher · View at Google Scholar
  19. I. G. Habeos, P. G. Ziros, D. Chartoumpekis, A. Psyrogiannis, V. Kyriazopoulou, and A. G. Papavassiliou, “Simvastatin activates Keap 1/Nrf2 signaling in rat liver,” Journal of Molecular Medicine, vol. 86, pp. 1279–1285, 2008. View at Google Scholar
  20. D. Chartoumpekis, P. G. Ziros, A. Psyrogiannis, V. Kyriazopoulou, A. G. Papavassiliou, and I. G. Habeos, “Simvastatin lowers reactive oxygen species level by Nrf2 activation via PI3K/Akt pathway,” Biochemical and Biophysical Research Communications, vol. 396, no. 2, pp. 463–466, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Yilmaz, C. Reiss, A. Weng et al., “Differential effects of statins on relevant functions of human monocyte-derived dendritic cells,” Journal of Leukocyte Biology, vol. 79, pp. 529–538, 2006. View at Google Scholar
  22. M. Lechmann, N. Shuman, A. Wakeham, and T. W. Mak, “The CD83 reporter mouse elucidates the activity of the CD83 promoter in B, T, and dendritic cell populations in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 33, pp. 11887–11892, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Elgueta, M. J. Benson, V. C. de Vries, A. Wasiuk, Y. Guo, and R. J. Noelle, “Molecular mechanism and function of CD40/CD40L engagement in the immune system,” Immunological Reviews, vol. 229, no. 1, pp. 152–172, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Verhasselt, C. Buelens, F. Willems, D. de Groote, N. Haeffner-Cavaillon, and M. Goldman, “Bacterial lipopolysaccharide stimulates the production of cytokines and the expression of costimulatory molecules by human peripheral blood dendritic cells: evidence for a soluble CD14-dependent pathway,” Journal of Immunology, vol. 158, no. 6, pp. 2919–2925, 1997. View at Google Scholar · View at Scopus
  25. J. Zhang and S. D. Crowley, “The role of type 1 angiotensin receptors on T lymphocytes in cardiovascular and renal diseases,” Current Hypertension Reports, vol. 15, no. 1, pp. 39–46, 2013. View at Publisher · View at Google Scholar
  26. A. L. Eggler, K. A. Gay, and A. D. Mesecar, “Molecular mechanisms of natural products in chemoprevention: induction of cytoprotective enzymes by Nrf2,” Molecular Nutrition and Food Research, vol. 52, no. 1, pp. S84–S94, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Wang, P. Liu, and J. K. Liao, “Pleiotropic effects of statin therapy: molecular mechanisms and clinical results,” Trends in Molecular Medicine, vol. 14, no. 1, pp. 37–44, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Wassmann, U. Laufs, K. Müller et al., “Cellular antioxidant effects of atorvastatin in vitro and in vivo,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 22, no. 2, pp. 300–305, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Virdis, M. F. Neves, F. Amiri, R. M. Touyz, and E. L. Schiffrin, “Role of NAD(P)H oxidase on vascular alterations in angiotensin II-infused mice,” Journal of Hypertension, vol. 22, no. 3, pp. 535–542, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Zhou, E. A. Jaimes, and L. Raij, “Vascular but not cardiac remodeling is associated with superoxide production in angiotensin II hypertension,” Journal of Hypertension, vol. 23, no. 9, pp. 1737–1743, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. C. de Ciuceis, F. Amiri, P. Brassard, D. H. Endemann, R. M. Touyz, and E. L. Schiffrin, “Reduced vascular remodeling, endothelial dysfunction, and oxidative stress in resistance arteries of angiotensin II-infused macrophage colony-stimulating factor-deficient mice: evidence for a role in inflammation in angiotensin-induced vascular injury,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 10, pp. 2106–2113, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. A. M. Briones, N. Rodríguez-Criado, R. Hernanz et al., “Atorvastatin prevents angiotensin II-induced vascular remodeling and oxidative stress,” Hypertension, vol. 54, pp. 142–149, 2009. View at Publisher · View at Google Scholar
  33. J. S. Lee and Y. J. Surh, “Nrf2 as a novel molecular target for chemoprevention,” Cancer Letters, vol. 224, no. 2, pp. 171–184, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. S. X. Liu, Y. Zhang, Y. F. Wang et al., “Upregulation of heme oxygenase-1 expression by hydroxysafflor yellow A conferring protection from anoxia/reoxygenation-induced apoptosis in H9c2 cardiomyocytes,” International Journal of Cardiology, vol. 160, no. 2, pp. 95–101, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. X. L. Chen, G. Dodd, S. Thomas et al., “Activation of Nrf 2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 290, no. 5, pp. H1862–H1870, 2006. View at Google Scholar
  36. X. L. Chen and C. Kunsch, “Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases,” Current Pharmaceutical Design, vol. 10, no. 8, pp. 879–891, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Ishikawa and Y. Maruyama, “Heme oxygenase as an intrinsic defense system in vascular wall: implication against atherogenesis.,” Journal of atherosclerosis and thrombosis, vol. 8, no. 3, pp. 63–70, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. K. Ishikawa, M. Navab, N. Leitinger, A. M. Fogelman, and A. J. Lusis, “Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL,” Journal of Clinical Investigation, vol. 100, no. 5, pp. 1209–1216, 1997. View at Publisher · View at Google Scholar · View at Scopus