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International Journal of Endocrinology
Volume 2018, Article ID 3614303, 18 pages
https://doi.org/10.1155/2018/3614303
Review Article

The Renin-Angiotensin-Aldosterone System as a Therapeutic Target in Late Injury Caused by Ischemia-Reperfusion

University of Guadalajara, Institute of Experimental and Clinical Therapeutics, Department of Physiology, University Health Sciences Centre, Guadalajara, JAL, Mexico

Correspondence should be addressed to Alejandra Guillermina Miranda-Díaz; moc.kooltuo@1xeladnik

Received 18 July 2017; Revised 9 January 2018; Accepted 7 February 2018; Published 4 April 2018

Academic Editor: Brasilina Caroccia

Copyright © 2018 Simón Quetzalcóatl Rodríguez-Lara 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. C. E. Murry, R. B. Jennings, and K. A. Reimer, “Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium,” Circulation, vol. 74, no. 5, pp. 1124–1136, 1986. View at Publisher · View at Google Scholar · View at Scopus
  2. A. T. Turer and J. A. Hill, “Pathogenesis of myocardial ischemia–reperfusion injury and rationale for therapy,” The American Journal of Cardiology, vol. 106, no. 3, pp. 360–368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Kalogeris, C. P. Baines, M. Krenz, and R. J. Korthuis, “Cell biology of ischemia/reperfusion injury,” International Review of Cell and Molecular Biology, vol. 298, pp. 229–317, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Ruiz-Ortega, V. Esteban, and J. Egido, “The regulation of the inflammatory response through nuclear factor-κB pathway by angiotensin IV extends the role of the renin angiotensin system in cardiovascular diseases,” Trends in Cardiovascular Medicine, vol. 17, no. 1, pp. 19–25, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. R. A. Gomez, “Fate of renin cells during development and disease,” Hypertension, vol. 69, no. 3, pp. 387–395, 2017. View at Publisher · View at Google Scholar · View at Scopus
  6. N. J. Brown, “Contribution of aldosterone to cardiovascular and renal inflammation and fibrosis,” Nature Reviews Nephrology, vol. 9, no. 8, pp. 459–469, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Q. Rodríguez-Lara, E. G. Cardona-Muñoz, E. J. Ramírez-Lizardo et al., “Alternative interventions to prevent oxidative damage following ischemia/reperfusion,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 7190943, 16 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Blundell, B. L. Sibanda, and L. Pearl, “Three-dimensional structure, specificity and catalytic mechanism of renin,” Nature, vol. 304, no. 5923, pp. 273–275, 1983. View at Publisher · View at Google Scholar · View at Scopus
  9. P. M. Hobart, M. Fogliano, B. A. O’Connor, I. M. Schaefer, and J. M. Chirgwin, “Human renin gene: structure and sequence analysis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 81, no. 16, pp. 5026–5030, 1984. View at Publisher · View at Google Scholar · View at Scopus
  10. R. A. Gomez, B. Belyea, S. Medrano, E. S. Pentz, and M. L. S. Sequeira-Lopez, “Fate and plasticity of renin precursors in development and disease,” Pediatric Nephrology, vol. 29, no. 4, pp. 721–726, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Y. Yeh, K. H. Yeh, S. E. Chuang, Y. C. Song, and A. L. Cheng, “Suppression of MEK/ERK signaling pathway enhances cisplatin-induced NF-κB activation by protein phosphatase 4-mediated NF-κB p65 Thr dephosphorylation,” Journal of Biological Chemistry, vol. 279, no. 25, pp. 26143–26148, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Azhar, R. B. Runyan, C. Gard et al., “Ligand-specific function of transforming growth factor beta in epithelial-mesenchymal transition in heart development,” Developmental Dynamics, vol. 238, no. 2, pp. 431–442, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. Rahimi, “The role of renin angiotensin aldosterone system genes in diabetic nephropathy,” Canadian Journal of Diabetes, vol. 40, no. 2, pp. 178–183, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Kurihara, Y. Ozawa, K. Shinoda et al., “Neuroprotective effects of angiotensin II type 1 receptor (AT1R) blocker, telmisartan, via modulating AT1R and AT2R signaling in retinal inflammation,” Investigative Ophthalmology & Visual Science, vol. 47, no. 12, pp. 5545–5552, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. K. M. Cook and P. J. Hogg, “Post-translational control of protein function by disulfide bond cleavage,” Antioxidants & Redox Signaling, vol. 18, no. 15, pp. 1987–2015, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. E. R. Lumbers and K. G. Pringle, “Roles of the circulating renin-angiotensin-aldosterone system in human pregnancy,” American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, vol. 306, no. 2, pp. R91–R101, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Fukamizu, S. Takahashi, M. S. Seo et al., “Structure and expression of the human angiotensinogen gene. Identification of a unique and highly active promoter,” The Journal of Biological Chemistry, vol. 265, no. 13, pp. 7576–7582, 1990. View at Google Scholar
  18. 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 Publisher · View at Google Scholar
  19. L. Opie, “Renoprotection by angiotensin-receptor blockers and ACE inhibitors in hypertension,” The Lancet, vol. 358, no. 9296, pp. 1829–1831, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. P. Gohlke, S. Weiss, A. Jansen et al., “AT1 receptor antagonist telmisartan administered peripherally inhibits central responses to angiotensin II in conscious rats,” Journal of Pharmacology and Experimental Therapeutics, vol. 298, no. 1, pp. 62–70, 2001. View at Google Scholar
  21. J. P. van Kats, M. A. D. H. Schalekamp, P. D. Verdouw, D. J. Duncker, and A. H. J. Danser, “Intrarenal angiotensin II: interstitial and cellular levels and site of production,” Kidney International, vol. 60, no. 6, pp. 2311–2317, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. H. L. Jackman, M. G. Massad, M. Sekosan et al., “Angiotensin 1–9 and 1–7 release in human heart: role of cathepsin A,” Hypertension, vol. 39, no. 5, pp. 976–981, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. W. C. De Mello, “Angiotensin (1–7) re-establishes impulse conduction in cardiac muscle during ischaemia-reperfusion. The role of the sodium pump,” Journal of the Renin-Angiotensin-Aldosterone System, vol. 5, no. 4, pp. 203–208, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Araki, T. Masaki, I. Katsuragi, K. Tanaka, T. Kakuma, and H. Yoshimatsu, “Telmisartan prevents obesity and increases the expression of uncoupling protein 1 in diet-induced obese mice,” Hypertension, vol. 48, no. 1, pp. 51–57, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Pachauri, D. Garabadu, A. Goyal, and P. K. Upadhyay, “Angiotensin (1–7) facilitates cardioprotection of ischemic preconditioning on ischemia–reperfusion-challenged rat heart,” Molecular and Cellular Biochemistry, vol. 430, no. 1-2, pp. 99–113, 2017. View at Publisher · View at Google Scholar · View at Scopus
  26. C. J. Wruck, H. Funke-Kaiser, T. Pufe et al., “Regulation of transport of the angiotensin AT2 receptor by a novel membrane-associated Golgi protein,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 1, pp. 57–64, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. 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
  28. J. Wright, B. Yamamoto, and J. Harding, “Angiotensin receptor subtype mediated physiologies and behaviors: new discoveries and clinical targets,” Progress in Neurobiology, vol. 84, no. 2, pp. 157–181, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Wen, J. K. Gwathmey, and L.-H. Xie, “Oxidative stress-mediated effects of angiotensin II in the cardiovascular system,” World Journal of Hypertension, vol. 2, no. 4, pp. 34–44, 2012. View at Publisher · View at Google Scholar
  30. P. M. Abadir, D. B. Foster, M. Crow et al., “Identification and characterization of a functional mitochondrial angiotensin system,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 36, pp. 14849–14854, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Bosnyak, E. S. Jones, A. Christopoulos, M.-I. Aguilar, W. G. Thomas, and R. E. Widdop, “Relative affinity of angiotensin peptides and novel ligands at AT1 and AT2 receptors,” Clinical Science, vol. 121, no. 7, pp. 297–303, 2011. View at Publisher · View at Google Scholar
  32. N. J. Brown, “Aldosterone and end-organ damage,” Current Opinion in Nephrology and Hypertension, vol. 14, no. 3, pp. 235–241, 2005. View at Publisher · View at Google Scholar
  33. Y. Shimoni, K. Chen, T. Emmett, and G. Kargacin, “Aldosterone and the autocrine modulation of potassium currents and oxidative stress in the diabetic rat heart,” British Journal of Pharmacology, vol. 154, no. 3, pp. 675–687, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Messaoudi, F. Azibani, C. Delcayre, and F. Jaisser, “Aldosterone, mineralocorticoid receptor, and heart failure,” Molecular and Cellular Endocrinology, vol. 350, no. 2, pp. 266–272, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. A. M. Briones, A. Nguyen Dinh Cat, G. E. Callera et al., “Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus–associated obesity and vascular dysfunction,” Hypertension, vol. 59, no. 5, pp. 1069–1078, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. M. B. Nolly, C. I. Caldiz, A. M. Yeves et al., “The signaling pathway for aldosterone-induced mitochondrial production of superoxide anion in the myocardium,” Journal of Molecular and Cellular Cardiology, vol. 67, pp. 60–68, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. B. A. Maron, Y.-Y. Zhang, D. E. Handy et al., “Aldosterone increases oxidant stress to impair guanylyl cyclase activity by cysteinyl thiol oxidation in vascular smooth muscle cells,” The Journal of Biological Chemistry, vol. 284, no. 12, pp. 7665–7672, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. B. G. Newfell, L. K. Iyer, N. N. Mohammad et al., “Aldosterone regulates vascular gene transcription via oxidative stress–dependent and–independent pathways,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 8, pp. 1871–1880, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Shibata, M. Nagase, S. Yoshida, H. Kawachi, and T. Fujita, “Podocyte as the target for aldosterone: roles of oxidative stress and Sgk1,” Hypertension, vol. 49, no. 2, pp. 355–364, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. N. G. Hattangady, L. O. Olala, W. B. Bollag, and W. E. Rainey, “Acute and chronic regulation of aldosterone production,” Molecular and Cellular Endocrinology, vol. 350, no. 2, pp. 151–162, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Patni, J. T. Mathew, L. Luan, N. Franki, P. N. Chander, and P. C. Singhal, “Aldosterone promotes proximal tubular cell apoptosis: role of oxidative stress,” American Journal of Physiology-Renal Physiology, vol. 293, no. 4, pp. F1065–F1071, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Queisser and N. Schupp, “Aldosterone, oxidative stress, and NF-κB activation in hypertension-related cardiovascular and renal diseases,” Free Radical Biology & Medicine, vol. 53, no. 2, pp. 314–327, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. P. R. Manna, J.-W. Soh, and D. M. Stocco, “The involvement of specific PKC isoenzymes in phorbol ester-mediated regulation of steroidogenic acute regulatory protein expression and steroid synthesis in mouse Leydig cells,” Endocrinology, vol. 152, no. 1, pp. 313–325, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. W. L. Miller, “Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter,” Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, vol. 1771, no. 6, pp. 663–676, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Sato, “Sterol metabolism and SREBP activation,” Archives of Biochemistry and Biophysics, vol. 501, no. 2, pp. 177–181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Muehlfelder, P.-A. Arias-Loza, K. H. Fritzemeier, and T. Pelzer, “Both estrogen receptor subtypes, ERα and ERβ, prevent aldosterone-induced oxidative stress in VSMC via increased NADPH bioavailability,” Biochemical and Biophysical Research Communications, vol. 423, no. 4, pp. 850–856, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. W. Ding, H. Guo, C. Xu, B. Wang, M. Zhang, and F. Ding, “Mitochondrial reactive oxygen species-mediated NLRP3 inflammasome activation contributes to aldosterone-induced renal tubular cells injury,” Oncotarget, vol. 7, no. 14, pp. 17479–17491, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. G. J. Gross and J. A. Auchampach, “Reperfusion injury: does it exist?” Journal of Molecular and Cellular Cardiology, vol. 42, no. 1, pp. 12–18, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Zhang, Z. Jia, X. Guo, and T. Yang, “Aldosterone induces epithelial-mesenchymal transition via ROS of mitochondrial origin,” American Journal of Physiology-Renal Physiology, vol. 293, no. 3, pp. F723–F731, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Zavadil, J. Haley, R. Kalluri, S. K. Muthuswamy, and E. Thompson, “Epithelial-mesenchymal transition,” Cancer Research, vol. 68, no. 23, pp. 9574–9577, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Kalluri and R. A. Weinberg, “The basics of epithelial-mesenchymal transition,” The Journal of Clinical Investigation, vol. 119, no. 6, pp. 1420–1428, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Zhang, H. Unal, C. Gati et al., “Structure of the angiotensin receptor revealed by serial femtosecond crystallography,” Cell, vol. 161, no. 4, pp. 833–844, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Lu, L. A. Cassis, C. W. Vander Kooi, and A. Daugherty, “Corrigendum: structure and functions of angiotensinogen,” Hypertension Research, vol. 39, no. 11, p. 827, 2016. View at Publisher · View at Google Scholar · View at Scopus
  54. B. A. Wilson, M. Nautiyal, T. M. Gwathmey, J. C. Rose, and M. C. Chappell, “Evidence for a mitochondrial angiotensin-(1–7) system in the kidney,” American Journal of Physiology-Renal Physiology, vol. 310, no. 7, pp. F637–F645, 2016. View at Publisher · View at Google Scholar · View at Scopus
  55. D. B. Zorov, C. R. Filburn, L.-O. Klotz, J. L. Zweier, and S. J. Sollott, “Reactive oxygen species (ROS-induced) ROS release,” Journal of Experimental Medicine, vol. 192, no. 7, pp. 1001–1014, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Zhang, G. W. Han, A. Batyuk et al., “Structural basis for selectivity and diversity in angiotensin II receptors,” Nature, vol. 544, no. 7650, pp. 327–332, 2017. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Ming, L. Songyan, C. Yawen et al., “trans-Polydatin protects the mouse heart against ischemia/reperfusion injury via inhibition of the renin–angiotensin system (RAS) and Rho kinase (ROCK) activity,” Food & Function, vol. 8, no. 6, pp. 2309–2321, 2017. View at Publisher · View at Google Scholar · View at Scopus
  58. X. Qiu, K. Brown, M. D. Hirschey, E. Verdin, and D. Chen, “Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation,” Cell Metabolism, vol. 12, no. 6, pp. 662–667, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. Q. N. Dinh, M. J. Young, M. A. Evans, G. R. Drummond, C. G. Sobey, and S. Chrissobolis, “Aldosterone-induced oxidative stress and inflammation in the brain are mediated by the endothelial cell mineralocorticoid receptor,” Brain Research, vol. 1637, pp. 146–153, 2016. View at Publisher · View at Google Scholar · View at Scopus
  60. M. D. Brand and D. G. Nicholls, “Assessing mitochondrial dysfunction in cells,” Biochemical Journal, vol. 435, no. 2, pp. 297–312, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. Z. Zhao and J. Vinten-Johansen, “Postconditioning: reduction of reperfusion-induced injury,” Cardiovascular Research, vol. 70, no. 2, pp. 200–211, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. D. Obal, S. Dettwiler, C. Favoccia, H. Scharbatke, B. Preckel, and W. Schlack, “The influence of mitochondrial KATP-channels in the cardioprotection of preconditioning and postconditioning by sevoflurane in the rat in vivo,” Anesthesia & Analgesia, vol. 101, no. 5, pp. 1252–1260, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. P. S. Brookes, E. P. Salinas, K. Darley-Usmar et al., “Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome crelease,” The Journal of Biological Chemistry, vol. 275, no. 27, pp. 20474–20479, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. I. Batinic-Haberle, A. Tovmasyan, E. R. H. Roberts, Z. Vujaskovic, K. W. Leong, and I. Spasojevic, “SOD therapeutics: latest insights into their structure–activity relationships and impact on the cellular redox-based signaling pathways,” Antioxidants & Redox Signaling, vol. 20, no. 15, pp. 2372–2415, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. B. Kalyanaraman, “Teaching the basics of redox biology to medical and graduate students: oxidants, antioxidants and disease mechanisms,” Redox Biology, vol. 1, no. 1, pp. 244–257, 2013. View at Publisher · View at Google Scholar · View at Scopus
  66. M. J. Morgan and Z. G. Liu, “Crosstalk of reactive oxygen species and NF-κB signaling,” Cell Research, vol. 21, no. 1, pp. 103–115, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Nagase and T. Fujita, “Role of Rac1–mineralocorticoid-receptor signalling in renal and cardiac disease,” Nature Reviews Nephrology, vol. 9, no. 2, pp. 86–98, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. Li, K. Suino, J. Daugherty, and H. E. Xu, “Structural and biochemical mechanisms for the specificity of hormone binding and coactivator assembly by mineralocorticoid receptor,” Molecular Cell, vol. 19, no. 3, pp. 367–380, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. V. G. Grivennikova and A. D. Vinogradov, “Generation of superoxide by the mitochondrial complex I,” Biochimica et Biophysica Acta (BBA)-Bioenergetics, vol. 1757, no. 5-6, pp. 553–561, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. K. R. Messner and J. A. Imlay, “Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase,” The Journal of Biological Chemistry, vol. 277, no. 45, pp. 42563–42571, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. J. J. Saris, P. A. C. 't Hoen, I. M. Garrelds et al., “Prorenin induces intracellular signaling in cardiomyocytes independently of angiotensin II,” Hypertension, vol. 48, no. 4, pp. 564–571, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Maack and M. Böhm, “Targeting mitochondrial oxidative stress in heart failure,” Journal of the American College of Cardiology, vol. 58, no. 1, pp. 83–86, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. K. M. Baker, G. W. Booz, and D. E. Dostal, “Cardiac actions of angiotensin II: role of an intracardiac renin-angiotensin system,” Annual Review of Physiology, vol. 54, no. 1, pp. 227–241, 1992. View at Publisher · View at Google Scholar
  74. F. Safari, S. Hajizadeh, S. Shekarforoush, G. Bayat, M. Foadoddini, and A. Khoshbaten, “Influence of ramiprilat and losartan on ischemia reperfusion injury in rat hearts,” Journal of the Renin-Angiotensin-Aldosterone System, vol. 13, no. 1, pp. 29–35, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. E. Messadi-Laribi, V. Griol-Charhbili, A. Pizard et al., “Tissue kallikrein is involved in the cardioprotective effect of AT1-receptor blockade in acute myocardial ischemia,” The Journal of Pharmacology and Experimental Therapeutics, vol. 323, no. 1, pp. 210–216, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Lavu, O. Boss, P. J. Elliott, and P. D. Lambert, “Sirtuins—novel therapeutic targets to treat age-associated diseases,” Nature Reviews Drug Discovery, vol. 7, no. 10, pp. 841–853, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. V. B. Pillai, N. R. Sundaresan, V. Jeevanandam, and M. P. Gupta, “Mitochondrial SIRT3 and heart disease,” Cardiovascular Research, vol. 88, no. 2, pp. 250–256, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. S. A. Samant, H. J. Zhang, Z. Hong et al., “SIRT3 deacetylates and activates OPA1 to regulate mitochondrial dynamics during stress,” Molecular and Cellular Biology, vol. 34, no. 5, pp. 807–819, 2014. View at Publisher · View at Google Scholar · View at Scopus
  79. A. J. Tompkins, L. S. Burwell, S. B. Digerness, C. Zaragoza, W. L. Holman, and P. S. Brookes, “Mitochondrial dysfunction in cardiac ischemia–reperfusion injury: ROS from complex I, without inhibition,” Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, vol. 1762, no. 2, pp. 223–231, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. J. C. Newman, W. He, and E. Verdin, “Mitochondrial protein acylation and intermediary metabolism: regulation by sirtuins and implications for metabolic disease,” The Journal of Biological Chemistry, vol. 287, no. 51, pp. 42436–42443, 2012. View at Publisher · View at Google Scholar · View at Scopus
  81. N. R. Sundaresan, M. Gupta, G. Kim, S. B. Rajamohan, A. Isbatan, and M. P. Gupta, “Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3a-dependent antioxidant defense mechanisms in mice,” The Journal of Clinical Investigation, vol. 119, no. 9, pp. 2758–2771, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. J. H. Lee, J. H. O’Keefe, D. Bell, D. D. Hensrud, and M. F. Holick, “Vitamin D deficiency: an important, common, and easily treatable cardiovascular risk factor?” Journal of the American College of Cardiology, vol. 52, no. 24, pp. 1949–1956, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Zittermann, “Vitamin D and disease prevention with special reference to cardiovascular disease,” Progress in Biophysics and Molecular Biology, vol. 92, no. 1, pp. 39–48, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. J. H. Lee, T. Jarreau, A. Prasad, C. Lavie, J. O’Keefe, and H. Ventura, “Nutritional assessment in heart failure patients,” Congestive Heart Failure, vol. 17, no. 4, pp. 199–203, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. J. Duszyński, R. Kozieł, W. Brutkowski, J. Szczepanowska, and K. Zabłocki, “The regulatory role of mitochondria in capacitative calcium entry,” Biochimica et Biophysica Acta (BBA) - Bioenergetics, vol. 1757, no. 5-6, pp. 380–387, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. P. Brookes and V. M. Darley-Usmar, “Hypothesis: the mitochondrial NO• signaling pathway, and the transduction of nitrosative to oxidative cell signals: an alternative function for cytochrome C oxidase,” Free Radical Biology & Medicine, vol. 32, no. 4, pp. 370–374, 2002. View at Publisher · View at Google Scholar · View at Scopus
  87. D. D. Thomas, X. Liu, S. P. Kantrow, and J. R. Lancaster, “The biological lifetime of nitric oxide: implications for the perivascular dynamics of NO and O2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 1, pp. 355–360, 2001. View at Publisher · View at Google Scholar
  88. M. J. Goldenthal and J. Marín-García, “Mitochondrial signaling pathways: a receiver/integrator organelle,” Molecular and Cellular Biochemistry, vol. 262, no. 1/2, pp. 1–16, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. B. Chance, H. Sies, and A. Boveris, “Hydroperoxide metabolism in mammalian organs,” Physiological Reviews, vol. 59, no. 3, pp. 527–605, 1979. View at Publisher · View at Google Scholar
  90. J. F. Turrens, “Mitochondrial formation of reactive oxygen species,” The Journal of Physiology, vol. 552, no. 2, pp. 335–344, 2003. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Cadenas and K. J. A. Davies, “Mitochondrial free radical generation, oxidative stress, and aging,” Free Radical Biology & Medicine, vol. 29, no. 3-4, pp. 222–230, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. S. V. Brodsky, S. Gao, H. Li, and M. S. Goligorsky, “Hyperglycemic switch from mitochondrial nitric oxide to superoxide production in endothelial cells,” American Journal of Physiology-Heart and Circulatory Physiology, vol. 283, no. 5, pp. H2130–H2139, 2002. View at Publisher · View at Google Scholar
  93. F. L. Muller, Y. Liu, and H. Van Remmen, “Complex III releases superoxide to both sides of the inner mitochondrial membrane,” The Journal of Biological Chemistry, vol. 279, no. 47, pp. 49064–49073, 2004. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Y. Andreyev, Y. E. Kushnareva, and A. A. Starkov, “Mitochondrial metabolism of reactive oxygen species,” Biochemistry, vol. 70, no. 2, pp. 200–214, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. M. K. Shigenaga, T. M. Hagen, and B. N. Ames, “Oxidative damage and mitochondrial decay in aging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 23, pp. 10771–10778, 1994. View at Publisher · View at Google Scholar · View at Scopus
  96. E. M. V. de Cavanagh, B. Piotrkowski, N. Basso et al., “Enalapril and losartan attenuate mitochondrial dysfunction in aged rats,” The FASEB Journal, vol. 17, no. 9, pp. 1096–1098, 2003. View at Publisher · View at Google Scholar
  97. S. H. Kaufmann and M. O. Hengartner, “Programmed cell death: alive and well in the new millennium,” Trends in Cell Biology, vol. 11, no. 12, pp. 526–534, 2001. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Molitch, R. DeFronzo, M. Franz et al., “Nephropathy in diabetes,” Diabetes Care, vol. 27, pp. S79–S83, 2004. View at Publisher · View at Google Scholar
  99. N. E. Sirett, A. S. McLean, J. J. Bray, and J. I. Hubbard, “Distribution of angiotensin II receptors in rat brain,” Brain Research, vol. 122, no. 2, pp. 299–312, 1977. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Peters, B. Kranzlin, S. Schaeffer et al., “Presence of renin within intramitochondrial dense bodies of the rat adrenal cortex,” American Journal of Physiology-Endocrinology and Metabolism, vol. 271, no. 3, pp. E439–E450, 1996. View at Publisher · View at Google Scholar
  101. B. Erdmann, K. Fuxe, and D. Ganten, “Subcellular localization of angiotensin II immunoreactivity in the rat cerebellar cortex,” Hypertension, vol. 28, no. 5, pp. 818–824, 1996. View at Publisher · View at Google Scholar · View at Scopus
  102. J. Bosch, E. Lonn, J. Pogue et al., “Long-term effects of ramipril on cardiovascular events and on diabetes: results of the HOPE study extension,” Circulation, vol. 112, no. 9, pp. 1339–1346, 2005. View at Publisher · View at Google Scholar · View at Scopus
  103. T. Münzel and J. F. Keaney, “Are ACE inhibitors a “magic bullet” against oxidative stress?” Circulation, vol. 104, no. 13, pp. 1571–1574, 2001. View at Publisher · View at Google Scholar · View at Scopus
  104. S. S. Katyare and J. G. Satav, “Effect of streptozotocin-induced diabetes on oxidative energy metabolism in rat kidney mitochondria. A comparative study of early and late effects,” Diabetes, Obesity and Metabolism, vol. 7, no. 5, pp. 555–562, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. J. F. Diaz-Villanueva, R. Diaz-Molina, and V. Garcia-Gonzalez, “Protein folding and mechanisms of proteostasis,” International Journal of Molecular Sciences, vol. 16, no. 12, pp. 17193–17230, 2015. View at Publisher · View at Google Scholar · View at Scopus
  106. C. M. Oslowski and F. Urano, “Measuring ER stress and the unfolded protein response using mammalian tissue culture system,” Methods in Enzymology, vol. 490, pp. 71–92, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. C. Xu, B. Bailly-Maitre, and J. C. Reed, “Endoplasmic reticulum stress: cell life and death decisions,” The Journal of Clinical Investigation, vol. 115, no. 10, pp. 2656–2664, 2005. View at Publisher · View at Google Scholar · View at Scopus
  108. W. G. Van Riel, R. F. van Golen, M. J. Reiniers, M. Heger, and T. M. van Gulik, “How much ischemia can the liver tolerate during resection?” HepatoBiliary Surgery and Nutrition, vol. 5, no. 1, pp. 58–71, 2016. View at Publisher · View at Google Scholar
  109. H. Zhou, J. Zhu, S. Yue et al., “The dichotomy of endoplasmic reticulum stress response in liver ischemia-reperfusion injury,” Transplantation, vol. 100, no. 2, pp. 365–372, 2016. View at Publisher · View at Google Scholar · View at Scopus
  110. E. E. Montalvo-Jave, T. Escalante-Tattersfield, J. A. Ortega-Salgado, E. Pina, and D. A. Geller, “Factors in the pathophysiology of the liver ischemia–reperfusion injury,” Journal of Surgical Research, vol. 147, no. 1, pp. 153–159, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. S. Iravanian and S. C. Dudley Jr, “The renin-angiotensin-aldosterone system (RAAS) and cardiac arrhythmias,” Heart Rhythm, vol. 5, no. 6, pp. S12–S17, 2008. View at Publisher · View at Google Scholar · View at Scopus
  112. M. P. Blaustein, “Calcium transport and buffering in neurons,” Trends in Neurosciences, vol. 11, no. 10, pp. 438–443, 1988. View at Publisher · View at Google Scholar · View at Scopus
  113. J. A. Gorter, J. J. Petrozzino, E. M. Aronica et al., “Global ischemia induces downregulation of glur2 mRNA and increases AMPA receptor-mediated Ca2+ influx in hippocampal CA1 neurons of gerbil,” The Journal of Neuroscience, vol. 17, no. 16, pp. 6179–6188, 1997. View at Google Scholar
  114. W. Paschen, “Disturbances of calcium homeostasis within the endoplasmic reticulum may contribute to the development of ischemic-cell damage,” Medical Hypotheses, vol. 47, no. 4, pp. 283–288, 1996. View at Publisher · View at Google Scholar · View at Scopus
  115. C. K. Petito, W. A. Pulsinelli, G. Jacobson, and F. Plum, “Edema and vascular permeability in ischemia: comparison between ischemic neuronal damage and infarction,” Journal of Neuropathology & Experimental Neurology, vol. 41, no. 4, pp. 423–436, 1982. View at Publisher · View at Google Scholar · View at Scopus
  116. J. M. Hallenbeck, “Inflammatory reactions at the blood-endothelial interface in acute stroke,” Advances in Neurology, vol. 71, pp. 281–301, 1996. View at Google Scholar
  117. R. J. Harris, L. Symon, N. M. Branston, and M. Bayhan, “Changes in extracellular calcium activity in cerebral ischaemia,” Journal of Cerebral Blood Flow & Metabolism, vol. 1, no. 2, pp. 203–209, 1981. View at Publisher · View at Google Scholar · View at Scopus
  118. E. Siemkowicz and A. J. Hansen, “Brain extracellular ion composition and EEG activity following 10 minutes ischemia in normo- and hyperglycemic rats,” Stroke, vol. 12, no. 2, pp. 236–240, 1981. View at Publisher · View at Google Scholar · View at Scopus
  119. G. A. Dienel, “Regional accumulation of calcium in postischemic rat brain,” Journal of Neurochemistry, vol. 43, no. 4, pp. 913–925, 1984. View at Publisher · View at Google Scholar · View at Scopus
  120. J. K. Deshpande, B. K. Siesjö, and T. Wieloch, “Calcium accumulation and neuronal damage in the rat hippocampus following cerebral ischemia,” Journal of Cerebral Blood Flow & Metabolism, vol. 7, no. 1, pp. 89–95, 1987. View at Publisher · View at Google Scholar · View at Scopus
  121. P. E. Czabotar, G. Lessene, A. Strasser, and J. M. Adams, “Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy,” Nature Reviews Molecular Cell Biology, vol. 15, no. 1, pp. 49–63, 2014. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Elmore, “Apoptosis: a review of programmed cell death,” Toxicologic Pathology, vol. 35, no. 4, pp. 495–516, 2007. View at Publisher · View at Google Scholar · View at Scopus
  123. G. Ichim and S. W. G. Tait, “A fate worse than death: apoptosis as an oncogenic process,” Nature Reviews Cancer, vol. 16, no. 8, pp. 539–548, 2016. View at Publisher · View at Google Scholar · View at Scopus
  124. S. W. G. Tait and D. R. Green, “Mitochondria and cell death: outer membrane permeabilization and beyond,” Nature Reviews Molecular Cell Biology, vol. 11, no. 9, pp. 621–632, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. J. M. Brown and L. D. Attardi, “The role of apoptosis in cancer development and treatment response,” Nature Reviews Cancer, vol. 5, no. 3, pp. 231–237, 2005. View at Publisher · View at Google Scholar
  126. S. Fulda and K.-M. Debatin, “Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy,” Oncogene, vol. 25, no. 34, pp. 4798–4811, 2006. View at Publisher · View at Google Scholar · View at Scopus
  127. H. C. Chen, M. Kanai, A. Inoue-Yamauchi et al., “An interconnected hierarchical model of cell death regulation by the BCL-2 family,” Nature Cell Biology, vol. 17, no. 10, pp. 1270–1281, 2015. View at Publisher · View at Google Scholar · View at Scopus
  128. R. S. Y. Wong, “Apoptosis in cancer: from pathogenesis to treatment,” Journal of Experimental & Clinical Cancer Research, vol. 30, no. 1, p. 87, 2011. View at Publisher · View at Google Scholar · View at Scopus
  129. L. Gong, Y. Tang, R. An, M. Lin, L. Chen, and J. Du, “RTN1-C mediates cerebral ischemia/reperfusion injury via ER stress and mitochondria-associated apoptosis pathways,” Cell Death & Disease, vol. 8, no. 10, article e3080, 2017. View at Publisher · View at Google Scholar
  130. H. Li, Y. Wang, C. Wei et al., “Mediation of exogenous hydrogen sulfide in recovery of ischemic post-conditioning-induced cardioprotection via down-regulating oxidative stress and up-regulating PI3K/Akt/GSK-3β pathway in isolated aging rat hearts,” Cell & Bioscience, vol. 5, no. 1, p. 11, 2015. View at Publisher · View at Google Scholar · View at Scopus
  131. Y. Lee, H.-Y. Lee, and Å. B. Gustafsson, “Regulation of autophagy by metabolic and stress signaling pathways in the heart,” Journal of Cardiovascular Pharmacology, vol. 60, no. 2, pp. 118–124, 2012. View at Publisher · View at Google Scholar · View at Scopus
  132. Z. Yang and D. J. Klionsky, “Mammalian autophagy: core molecular machinery and signaling regulation,” Current Opinion in Cell Biology, vol. 22, no. 2, pp. 124–131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  133. A. Kuma, M. Hatano, M. Matsui et al., “The role of autophagy during the early neonatal starvation period,” Nature, vol. 432, no. 7020, pp. 1032–1036, 2004. View at Publisher · View at Google Scholar · View at Scopus
  134. Z. Xie and D. J. Klionsky, “Autophagosome formation: core machinery and adaptations,” Nature Cell Biology, vol. 9, no. 10, pp. 1102–1109, 2007. View at Publisher · View at Google Scholar · View at Scopus
  135. A. M. Orogo and Å. B. Gustafsson, “Therapeutic targeting of autophagy: potential and concerns in treating cardiovascular disease,” Circulation Research, vol. 116, no. 3, pp. 489–503, 2015. View at Publisher · View at Google Scholar · View at Scopus
  136. E. Iwai-Kanai, H. Yuan, C. Huang et al., “A method to measure cardiac autophagic flux in vivo,” Autophagy, vol. 4, no. 3, pp. 322–329, 2008. View at Publisher · View at Google Scholar · View at Scopus
  137. L. Galluzzi, E. Morselli, J. M. Vicencio et al., “Life, death and burial: multifaceted impact of autophagy,” Biochemical Society Transactions, vol. 36, no. 5, pp. 786–790, 2008. View at Publisher · View at Google Scholar · View at Scopus
  138. G. Kroemer and B. Levine, “Autophagic cell death: the story of a misnomer,” Nature Reviews Molecular Cell Biology, vol. 9, no. 12, pp. 1004–1010, 2008. View at Publisher · View at Google Scholar · View at Scopus
  139. H. Zhu, P. Tannous, J. L. Johnstone et al., “Cardiac autophagy is a maladaptive response to hemodynamic stress,” Journal of Clinical Investigation, vol. 117, no. 7, pp. 1782–1793, 2007. View at Publisher · View at Google Scholar · View at Scopus
  140. A. Nakai, O. Yamaguchi, T. Takeda et al., “The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress,” Nature Medicine, vol. 13, no. 5, pp. 619–624, 2007. View at Publisher · View at Google Scholar · View at Scopus
  141. Y. Matsui, H. Takagi, X. Qu et al., “Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and beclin 1 in mediating autophagy,” Circulation Research, vol. 100, no. 6, pp. 914–922, 2007. View at Publisher · View at Google Scholar · View at Scopus
  142. G. Kroemer, L. Galluzzi, P. Vandenabeele et al., “Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009,” Cell Death & Differentiation, vol. 16, no. 1, pp. 3–11, 2009. View at Publisher · View at Google Scholar · View at Scopus
  143. D. J. Klionsky, “Cell biology: regulated self-cannibalism,” Nature, vol. 431, no. 7004, pp. 31-32, 2004. View at Publisher · View at Google Scholar · View at Scopus
  144. D. C. Rubinsztein, J. E. Gestwicki, L. O. Murphy, and D. J. Klionsky, “Potential therapeutic applications of autophagy,” Nature Reviews Drug Discovery, vol. 6, no. 4, pp. 304–312, 2007. View at Publisher · View at Google Scholar · View at Scopus
  145. B. A. Rothermel and J. A. Hill, “Myocyte autophagy in heart disease: friend or foe?” Autophagy, vol. 3, no. 6, pp. 632–634, 2007. View at Publisher · View at Google Scholar
  146. L. Yan, D. E. Vatner, S.-J. Kim et al., “Autophagy in chronically ischemic myocardium,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 39, pp. 13807–13812, 2005. View at Publisher · View at Google Scholar · View at Scopus
  147. E. R. Porrello, A. D’Amore, C. L. Curl et al., “Angiotensin II type 2 receptor antagonizes angiotensin II type 1 receptor–mediated cardiomyocyte autophagy,” Hypertension, vol. 53, no. 6, pp. 1032–1040, 2009. View at Publisher · View at Google Scholar · View at Scopus
  148. T. Matsusaka, J. Hymes, and I. Ichikawa, “Angiotensin in progressive renal diseases: theory and practice,” Journal of the American Society of Nephrology, vol. 7, no. 10, pp. 2025–2043, 1996. View at Google Scholar
  149. M. W. Taal and B. M. Brenner, “Renoprotective benefits of RAS inhibition: from ACEI to angiotensin II antagonists,” Kidney International, vol. 57, no. 5, pp. 1803–1817, 2000. View at Publisher · View at Google Scholar · View at Scopus
  150. M. Bhaskaran, K. Reddy, N. Radhakrishanan, N. Franki, G. Ding, and P. C. Singhal, “Angiotensin II induces apoptosis in renal proximal tubular cells,” American Journal of Physiology-Renal Physiology, vol. 284, no. 5, pp. F955–F965, 2003. View at Publisher · View at Google Scholar
  151. R. Singh, A. K. Singh, N. Alavi, and D. J. Leehey, “Mechanism of increased angiotensin II levels in glomerular mesangial cells cultured in high glucose,” Journal of the American Society of Nephrology, vol. 14, no. 4, pp. 873–880, 2003. View at Publisher · View at Google Scholar · View at Scopus
  152. S. Lodha, D. Dani, R. Mehta et al., “Angiotensin II-induced mesangial cell apoptosis: role of oxidative stress,” Molecular Medicine, vol. 8, no. 12, pp. 830–840, 2002. View at Google Scholar
  153. N. Mizushima, “Autophagy: process and function,” Genes & Development, vol. 21, no. 22, pp. 2861–2873, 2007. View at Publisher · View at Google Scholar · View at Scopus
  154. S. Xiong, G. Salazar, N. Patrushev et al., “Peroxisome proliferator-activated receptor γ coactivator-1α is a central negative regulator of vascular senescence,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 5, pp. 988–998, 2013. View at Publisher · View at Google Scholar · View at Scopus