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Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 6731093, 14 pages
http://dx.doi.org/10.1155/2016/6731093
Research Article

Age-Associated Changes in the Vascular Renin-Angiotensin System in Mice

1Division of Nephrology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul 137701, Republic of Korea
2Department of Internal Medicine, Incheon St. Mary’s Hospital, Incheon, Republic of Korea
3Department of Internal Medicine, Seoul St. Mary’s Hospital, Seoul, Republic of Korea
4Department of Internal Medicine, Yeouido St. Mary’s Hospital, Seoul, Republic of Korea

Received 16 December 2015; Revised 8 March 2016; Accepted 31 March 2016

Academic Editor: Andreas Daiber

Copyright © 2016 Hye Eun Yoon 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. E. G. Lakatta and D. Levy, “Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part I: aging arteries: a “set up” for vascular disease,” Circulation, vol. 107, no. 1, pp. 139–146, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. E. G. Lakatta, “Arterial and cardiac aging: Major shareholders in cardiovascular disease enterprises. Part III: cellular and molecular clues to heart and arterial aging,” Circulation, vol. 107, no. 3, pp. 490–497, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. J. C. Kovacic, P. Moreno, E. G. Nabel, V. Hachinski, and V. Fuster, “Cellular senescence, vascular disease, and aging: part 2 of a 2-part review: clinical vascular disease in the elderly,” Circulation, vol. 123, no. 17, pp. 1900–1910, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. H. E. Yoon and B. S. Choi, “The renin-angiotensin system and aging in the kidney,” Korean Journal of Internal Medicine, vol. 29, no. 3, pp. 291–295, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Conti, P. Cassis, and A. Benigni, “Aging and the renin-angiotensin system,” Hypertension, vol. 60, no. 4, pp. 878–883, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. R. M. Carey, “Cardiovascular and renal regulation by the angiotensin type 2 receptor: the AT2 receptor comes of age,” Hypertension, vol. 45, no. 5, pp. 840–844, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Hunyady and K. J. Catt, “Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II,” Molecular Endocrinology, vol. 20, no. 5, pp. 953–970, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. P. K. Mehta and K. K. Griendling, “Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system,” American Journal of Physiology—Cell Physiology, vol. 292, no. 1, pp. C82–C97, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Benigni, P. Cassis, and G. Remuzzi, “Angiotensin II revisited: new roles in inflammation, immunology and aging,” EMBO Molecular Medicine, vol. 2, no. 7, pp. 247–257, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Donoghue, F. Hsieh, E. Baronas et al., “A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1–9,” Circulation Research, vol. 87, no. 5, pp. E1–E9, 2000. View at Google Scholar · View at Scopus
  11. R. A. S. Santos, A. C. Simoes e Silva, C. Maric et al., “Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 14, pp. 8258–8263, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. R. A. S. Santos, A. J. Ferreira, and A. C. Simões e Silva, “Recent advances in the angiotensin-converting enzyme 2-angiotensin(1–7)-Mas axis,” Experimental Physiology, vol. 93, no. 5, pp. 519–527, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Nguyen, F. Delarue, C. Burcklé, L. Bouzhir, T. Giller, and J.-D. Sraer, “Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin,” The Journal of Clinical Investigation, vol. 109, no. 11, pp. 1417–1427, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. A. E. Cuadra, Z. Shan, C. Sumners, and M. K. Raizada, “A current view of brain renin-angiotensin system: is the (pro)renin receptor the missing link?” Pharmacology and Therapeutics, vol. 125, no. 1, pp. 27–38, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. A. D. de Kloet, E. G. Krause, and S. C. Woods, “The renin angiotensin system and the metabolic syndrome,” Physiology and Behavior, vol. 100, no. 5, pp. 525–534, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. J. H. Lim, E. N. Kim, M. Y. Kim et al., “Age-associated molecular changes in the kidney in aged mice,” Oxidative Medicine and Cellular Longevity, vol. 2012, Article ID 171383, 10 pages, 2012. View at Publisher · View at Google Scholar
  17. F. Paneni, S. Costantino, and F. Cosentino, “Molecular pathways of arterial aging,” Clinical Science, vol. 128, no. 2, pp. 69–79, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Czypiorski, L. L. Rabanter, J. Altschmied, and J. Haendeler, “Redox balance in the aged endothelium,” Zeitschrift fur Gerontologie und Geriatrie, vol. 46, no. 7, pp. 635–638, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Wang, J. Zhang, S. J. Walker, R. Dworakowski, E. G. Lakatta, and A. M. Shah, “Involvement of NADPH oxidase in age-associated cardiac remodeling,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 4, pp. 765–772, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. S.-S. Gu, Y. Zhang, X.-L. Li et al., “Involvement of the skeletal renin-angiotensin system in age-related osteoporosis of ageing mice,” Bioscience, Biotechnology and Biochemistry, vol. 76, no. 7, pp. 1367–1371, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Villapol and J. M. Saavedra, “Neuroprotective effects of angiotensin receptor blockers,” The American Journal of Hypertension, vol. 28, no. 3, pp. 289–299, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. Huang, S. Wongamorntham, J. Kasting et al., “Renin increases mesangial cell transforming growth factor-β1 and matrix proteins through receptor-mediated, angiotensin II-independent mechanisms,” Kidney International, vol. 69, no. 1, pp. 105–113, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Kurauchi-Mito, A. Ichihara, K. Bokuda et al., “Significant roles of the (pro)renin receptor in integrity of vascular smooth muscle cells,” Hypertension Research, vol. 37, no. 9, pp. 830–835, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. Z. Li, J. Froehlich, Z. S. Galis, and E. G. Lakatta, “Increased expression of matrix metalloproteinase-2 in the thickened intima of aged rats,” Hypertension, vol. 33, no. 1, pp. 116–123, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Takasaki, A. V. Chobanian, R. Sarzani, and P. Brecher, “Effect of hypertension on fibronectin expression in the rat aorta,” Journal of Biological Chemistry, vol. 265, no. 35, pp. 21935–21939, 1990. View at Google Scholar · View at Scopus
  26. D. C. Crawford, A. V. Chobanian, and P. Brecher, “Angiotensin II induces fibronectin expression associated with cardiac fibrosis in the rat,” Circulation Research, vol. 74, no. 4, pp. 727–739, 1994. View at Publisher · View at Google Scholar · View at Scopus
  27. R. M. Carey, “Update on the role of the AT2 receptor,” Current Opinion in Nephrology and Hypertension, vol. 14, no. 1, pp. 67–71, 2005. View at Google Scholar
  28. J. Gao, J. Chao, K.-J. K. Parbhu et al., “Ontogeny of angiotensin type 2 and type 1 receptor expression in mice,” Journal of the Renin-Angiotensin-Aldosterone System, vol. 13, no. 3, pp. 341–352, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. E. F. Grady, L. A. Sechi, C. A. Griffin, M. Schambelan, and J. E. Kalinyak, “Expression of AT2 receptors in the developing rat fetus,” Journal of Clinical Investigation, vol. 88, no. 3, pp. 921–933, 1991. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Millan, D. M. Jacobowitz, G. Aguilera, and K. J. Catt, “Differential distribution of at1 and at2 angiotensin II receptor subtypes in the rat brain during development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 24, pp. 11440–11444, 1991. View at Publisher · View at Google Scholar · View at Scopus
  31. G. M. Ciuffo, M. Viswanathan, A. M. Seltzer, K. Tsutsumi, and J. M. Saavedra, “Glomerular angiotensin II receptor subtypes during development of rat kidney,” American Journal of Physiology—Renal Fluid and Electrolyte Physiology, vol. 265, no. 2, part 2, pp. F264–F271, 1993. View at Google Scholar · View at Scopus
  32. K. Tsutsumi and J. M. Saavedra, “Characterization and development of angiotensin II receptor subtypes (AT1 and AT2) in rat brain,” American Journal of Physiology-Regulatory Integrative and Comparative Physiology, vol. 261, no. 1, part 2, pp. R209–R216, 1991. View at Google Scholar · View at Scopus
  33. K. Tsutsumi and J. M. Saavedra, “Characterization of AT2 angiotensin II receptors in rat anterior cerebral arteries,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 261, no. 3, part 2, pp. H667–H670, 1991. View at Google Scholar · View at Scopus
  34. L. A. Sechi, C. A. Griffin, E. F. Grady, J. E. Kalinyak, and M. Schambelan, “Characterization of angiotensin II receptor subtypes in rat heart,” Circulation Research, vol. 71, no. 6, pp. 1482–1489, 1992. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Aguilera, S. Kapur, P. Feuillan, B. Sunar-Akbasak, and A. J. Bathia, “Developmental changes in angiotensin II receptor subtypes and AT1 receptor mRNA in rat kidney,” Kidney International, vol. 46, no. 4, pp. 973–979, 1994. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Shanmugam, C. Llorens-Cortes, E. Clauser, P. Corvol, and J. M. Gasc, “Expression of angiotensin II AT2 receptor mRNA during development of rat kidney and adrenal gland,” American Journal of Physiology, vol. 268, no. 5, part 2, pp. F922–F930, 1995. View at Google Scholar
  37. S. Shanmugam, P. Corvol, and J.-M. Gasc, “Angiotensin II type 2 receptor mRNA expression in the developing cardiopulmonary system of the rat,” Hypertension, vol. 28, no. 1, pp. 91–97, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. M. M. Bachschmid, S. Schildknecht, R. Matsui et al., “Vascular aging: chronic oxidative stress and impairment of redox signaling—consequences for vascular homeostasis and disease,” Annals of Medicine, vol. 45, no. 1, pp. 17–36, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Gilliam-Davis, V. S. Payne, S. O. Kasper, E. N. Tommasi, M. E. Robbins, and D. I. Diz, “Long-term AT1 receptor blockade improves metabolic function and provides renoprotection in Fischer-344 rats,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 293, no. 3, pp. H1327–H1333, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. K. E. Herbert, Y. Mistry, R. Hastings, T. Poolman, L. Niklason, and B. Williams, “Angiotensin II-mediated oxidative DNA damage accelerates cellular senescence in cultured human vascular smooth muscle cells via telomere-dependent and independent pathways,” Circulation Research, vol. 102, no. 2, pp. 201–208, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. U. Förstermann and W. C. Sessa, “Nitric oxide synthases: regulation and function,” European Heart Journal, vol. 33, no. 7, pp. 829–837, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. H. G. Zecchin, R. M. N. Bezerra, J. B. C. Carvalheira et al., “Insulin signalling pathways in aorta and muscle from two animal models of insulin resistance—the obese middle-aged and the spontaneously hypertensive rats,” Diabetologia, vol. 46, no. 4, pp. 479–491, 2003. View at Google Scholar · View at Scopus
  43. B. van der Loo, R. Labugger, J. N. Skepper et al., “Enhanced peroxynitrite formation is associated with vascular aging,” The Journal of Experimental Medicine, vol. 192, no. 12, pp. 1731–1743, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Basso, N. Paglia, I. Stella et al., “Protective effect of the inhibition of the renin-angiotensin system on aging,” Regulatory Peptides, vol. 128, no. 3, pp. 247–252, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Konior, A. Schramm, M. Czesnikiewicz-Guzik, and T. J. Guzik, “NADPH oxidases in vascular pathology,” Antioxidants and Redox Signaling, vol. 20, no. 17, pp. 2794–2814, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. S. I. Dikalov, A. E. Dikalova, A. T. Bikineyeva, H. H. H. W. Schmidt, D. G. Harrison, and K. K. Griendling, “Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production,” Free Radical Biology and Medicine, vol. 45, no. 9, pp. 1340–1351, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. F. E. Rey, M. E. Cifuentes, A. Kiarash, M. T. Quinn, and P. J. Pagano, “Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O2- and systolic blood pressure in mice,” Circulation Research, vol. 89, no. 5, pp. 408–414, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Ray, C. E. Murdoch, M. Wang et al., “Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 6, pp. 1368–1376, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Schröder, M. Zhang, S. Benkhoff et al., “Nox4 Is a protective reactive oxygen species generating vascular NADPH oxidase,” Circulation Research, vol. 110, no. 9, pp. 1217–1225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. B. Guzik, A. Sagan, D. Ludew et al., “Mechanisms of oxidative stress in human aortic aneurysms—association with clinical risk factors for atherosclerosis and disease severity,” International Journal of Cardiology, vol. 168, no. 3, pp. 2389–2396, 2013. View at Publisher · View at Google Scholar · View at Scopus