Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016 (2016), Article ID 2950503, 12 pages
http://dx.doi.org/10.1155/2016/2950503
Review Article

Mitochondria-Targeted Antioxidants: Future Perspectives in Kidney Ischemia Reperfusion Injury

1School of Medicine, University of Belgrade, Dr. Subotica 8, 11000 Belgrade, Serbia
2Clinic for Nephrology, Clinical Center of Serbia, Pasterova 2, 11000 Belgrade, Serbia
3Department of Life Sciences, Institute for Multidisciplinary Research, University of Belgrade, Kneza Vieslava 1, 11000 Belgrade, Serbia
4Department of Pharmacology, Clinical Pharmacology and Toxicology, School of Medicine, University of Belgrade, P.O. Box 38, 11000 Belgrade, Serbia
5Clinical Pharmacology Unit, University Children’s Hospital, 11000 Belgrade, Serbia

Received 19 February 2016; Accepted 28 April 2016

Academic Editor: Jacek Zielonka

Copyright © 2016 Aleksandra Kezic 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. R. W. Schrier, W. Wang, B. Poole, and A. Mitra, “Acute renal failure: definitions, diagnosis, pathogenesis, and therapy,” The Journal of Clinical Investigation, vol. 114, no. 1, pp. 5–14, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. G. M. Chertow, E. Burdick, M. Honour, J. V. Bonventre, and D. W. Bates, “Acute kidney injury, mortality, length of stay, and costs in hospitalized patients,” Journal of the American Society of Nephrology, vol. 16, no. 11, pp. 3365–3370, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Perico, D. Cattaneo, M. H. Sayegh, and G. Remuzzi, “Delayed graft function in kidney transplantation,” The Lancet, vol. 364, no. 9447, pp. 1814–1827, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Boletis, A. Balitsari, V. Filiopoulos et al., “Delayed renal graft function: the influence of immunosuppression,” Transplantation Proceedings, vol. 37, no. 5, pp. 2054–2059, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. D. P. Basile, “The endothelial cell in ischemic acute kidney injury: implications for acute and chronic function,” Kidney International, vol. 72, no. 2, pp. 151–156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. J. V. Bonventre and L. Yang, “Cellular pathophysiology of ischemic acute kidney injury,” The Journal of Clinical Investigation, vol. 121, no. 11, pp. 4210–4221, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. M. A. Venkatachalam, K. A. Griffin, R. Lan, H. Geng, P. Saikumar, and A. K. Bidani, “Acute kidney injury: a springboard for progression in chronic kidney disease,” American Journal of Physiology—Renal Physiology, vol. 298, no. 5, pp. F1078–F1094, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Devarajan, “Update on mechanisms of ischemic acute kidney injury,” Journal of the American Society of Nephrology, vol. 17, no. 6, pp. 1503–1520, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. A. J. Ristić, D. Savić, D. Sokić et al., “Hippocampal antioxidative system in mesial temporal lobe epilepsy,” Epilepsia, vol. 56, no. 5, pp. 789–799, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Bindoli and M. P. Rigobello, “Principles in redox signaling: from chemistry to functional significance,” Antioxidants & Redox Signaling, vol. 18, no. 13, pp. 1557–1593, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. M. É. Andrades, A. Morina, S. Spasić, and I. Spasojević, “Bench-to-bedside review: sepsis—from the redox point of view,” Critical Care, vol. 15, no. 5, article 230, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. S. J. Klebanoff, “Oxygen metabolism and the toxic properties of phagocytes,” Annals of Internal Medicine, vol. 93, no. 3, pp. 480–489, 1980. View at Publisher · View at Google Scholar · View at Scopus
  13. V. J. Thannickal and B. L. Fanburg, “Reactive oxygen species in cell signaling,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 279, no. 6, pp. L1005–L1028, 2000. View at Google Scholar · View at Scopus
  14. G. Ferrer-Sueta and R. Radi, “Chemical biology of peroxynitrite: kinetics, diffusion, and radicals,” ACS Chemical Biology, vol. 4, no. 3, pp. 161–177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Goldstein and G. Czapski, “Reactivity of ONOO-versus simultaneous generation of NO and O2- toward NADH,” Chemical Research in Toxicology, vol. 13, no. 8, pp. 736–741, 2000. View at Google Scholar
  16. A. M. Michelson and J. Maral, “Carbonate anions; effects on the oxidation of luminol, oxidative hemolysis, γ-irradiation and the reaction of activated oxygen species with enzymes containing various active centres,” Biochimie, vol. 65, no. 2, pp. 95–104, 1983. View at Publisher · View at Google Scholar · View at Scopus
  17. Q. Chen, S. Moghaddas, C. L. Hoppel, and E. J. Lesnefsky, “Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria,” American Journal of Physiology—Cell Physiology, vol. 294, no. 2, pp. C460–C466, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Bajwa, G. R. Kinsey, and M. D. Okusa, “Immune mechanisms and novel pharmacological therapies of acute kidney injury,” Current Drug Targets, vol. 10, no. 12, pp. 1196–1204, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. S. A. Silver, H. Cardinal, K. Colwell, D. Burger, and J. G. Dickhout, “Acute kidney injury: preclinical innovations, challenges, and opportunities for translation,” Canadian Journal of Kidney Health and Disease, vol. 2, no. 1, article 30, pp. 1–11, 2015. View at Publisher · View at Google Scholar
  20. S. Faubel, L. S. Chawla, G. M. Chertow, S. L. Goldstein, B. L. Jaber, and K. D. Liu, “Ongoing clinical trials in AKI,” Clinical Journal of the American Society of Nephrology, vol. 7, no. 5, pp. 861–873, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Gassanov, A. M. Nia, E. Caglayan, and F. Er, “Remote ischemic preconditioning and renoprotection: from myth to a novel therapeutic option?” Journal of the American Society of Nephrology, vol. 25, no. 2, pp. 216–224, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Kalogeris, Y. Bao, and R. J. Korthuis, “Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs. preconditioning,” Redox Biology, vol. 2, no. 1, pp. 702–714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. Y.-R. Chen and J. L. Zweier, “Cardiac mitochondria and reactive oxygen species generation,” Circulation Research, vol. 114, no. 3, pp. 524–537, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. T. P. Dalton, H. G. Shertzer, and A. Puga, “Regulation of gene expression by reactive oxygen,” Annual Review of Pharmacology and Toxicology, vol. 39, pp. 67–101, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Irani, Y. Xia, J. L. Zweier et al., “Mitogenic signaling mediated by oxidants in ras-transformed fibroblasts,” Science, vol. 275, no. 5306, pp. 1649–1652, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Bolli, “The late phase of preconditioning,” Circulation Research, vol. 87, no. 11, pp. 972–983, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. W. Rouslin, “Mitochondrial complexes I, II, III, IV, and V in myocardial ischemia and autolysis,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 13, no. 6, pp. H743–H748, 1983. View at Google Scholar · View at Scopus
  28. J. E. Baker and B. Kalyanaraman, “Ischemia-induced changes in myocardial paramagnetic metabolites: implications for intracellular oxy-radical generation,” FEBS Letters, vol. 244, no. 2, pp. 311–314, 1989. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Mojia, J. B. Pristov, D. Maksimović-Ivanić et al., “Extracellular iron diminishes anticancer effects of vitamin C: an in vitro study,” Scientific Reports, vol. 4, article 5955, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Arduini, A. Mezzetti, E. Porreca et al., “Effect of ischemia and reperfusion on antioxidant enzymes and mitochondrial inner membrane proteins in perfused rat heart,” Biochimica et Biophysica Acta (BBA)—Molecular Cell Research, vol. 970, no. 2, pp. 113–121, 1988. View at Publisher · View at Google Scholar · View at Scopus
  31. W. Jassem, C. Ciarimboli, P. N. Cerioni, V. Saba, S. J. Norton, and G. Principato, “Glyoxalase II and glutathione levels in rat liver mitochondria during cold storage in Euro-Collins and University of Wisconsin solutions,” Transplantation, vol. 61, no. 9, pp. 1416–1420, 1996. View at Publisher · View at Google Scholar · View at Scopus
  32. A. J. Whitmarsh and R. J. Davis, “Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways,” Journal of Molecular Medicine, vol. 74, no. 10, pp. 589–607, 1996. View at Publisher · View at Google Scholar · View at Scopus
  33. A. J. McGowan, M. C. Ruiz-Ruiz, A. M. Gorman, A. Lopez-Rivas, and T. G. Cotter, “Reactive oxygen intermediate(s) (ROI): common mediator(s) of poly(ADP-ribose)polymerase (PARP) cleavage and apoptosis,” FEBS Letters, vol. 392, no. 3, pp. 299–303, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. C. A. Latanich and L. H. Toledo-Pereyra, “Searching for NF-κB-based treatments of ischemia reperfusion injury,” Journal of Investigative Surgery, vol. 22, no. 4, pp. 301–315, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. T. C. Nichols, “NF-κB and reperfusion injury,” Drug News and Perspectives, vol. 17, no. 2, pp. 99–104, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. C. C. Cao, X. Q. Ding, Z. L. Ou et al., “In vivo transfection of NF-κB decoy oligodeoxynucleotides attenuate renal ischemia/reperfusion injury in rats,” Kidney International, vol. 65, no. 3, pp. 834–845, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Kezic, J. U. Becker, and F. Thaiss, “The effect of mTOR-inhibition on NF-κB activity in kidney ischemia-reperfusion injury in mice,” Transplantation Proceedings, vol. 45, no. 5, pp. 1708–1714, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. X. Wan, L. Fan, B. Hu et al., “Small interfering RNA targeting IKKβ prevents renal ischemia-reperfusion injury in rats,” American Journal of Physiology. Renal Physiology, vol. 300, no. 4, pp. F857–F863, 2011. View at Google Scholar
  39. J. Rius, M. Guma, C. Schachtrup et al., “NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α,” Nature, vol. 453, no. 7196, pp. 807–811, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. H.-L. Lee, C.-L. Chen, S. T. Yeh, J. L. Zweier, and Y.-R. Chen, “Biphasic modulation of the mitochondrial electron transport chain in myocardial ischemia and reperfusion,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 302, no. 7, pp. H1410–H1422, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Wang and J. L. Zweier, “Measurement of nitric oxide and peroxynitrite generation in the postischemic heart: evidence for peroxynitrite-mediated reperfusion injury,” Journal of Biological Chemistry, vol. 271, no. 46, pp. 29223–29230, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Saito and I. Miyagawa, “Real-time monitoring of nitric oxide in ischemia-reperfusion rat kidney,” Urological Research, vol. 28, no. 2, pp. 141–146, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. M. G. Salom, B. Arregui, L. F. Carbonell, F. Ruiz, J. L. González-Mora, and F. J. Fenoy, “Renal ischemia induces an increase in nitric oxide levels from tissue stores,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 289, no. 5, pp. R1459–R1466, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. L. M. Walker, J. L. York, S. Z. Imam, S. F. Ali, K. L. Muldrew, and P. R. Mayeux, “Oxidative stress and reactive nitrogen species generation during renal ischemia,” Toxicological Sciences, vol. 63, no. 1, pp. 143–148, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Noiri, T. Peresleni, F. Miller, and M. S. Goligorsky, “In vivo targeting of inducible NO synthase with oligodeoxynucleotides protects rat kidney against ischemia,” The Journal of Clinical Investigation, vol. 97, no. 10, pp. 2377–2383, 1996. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Chiao, Y. Kohda, P. McLeroy, L. Craig, S. Linas, and R. A. Star, “α-Melanocyte-stimulating hormone inhibits renal injury in the absence of neutrophils,” Kidney International, vol. 54, no. 3, pp. 765–774, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. P. K. Chatterjee, N. S. A. Patel, E. O. Kvale et al., “Inhibition of inducible nitric oxide synthase reduces renal ischemia/reperfusion injury,” Kidney International, vol. 61, no. 3, pp. 862–871, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Kezic, F. Thaiss, J. U. Becker, T. Y. Tsui, and M. Bajcetic, “Effects of everolimus on oxidative stress in kidney model of ischemia/reperfusion injury,” American Journal of Nephrology, vol. 37, no. 4, pp. 291–301, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Ling, P. E. Gengaro, C. L. Edelstein et al., “Effect of hypoxia on proximal tubules isolated from nitric oxide synthase knockout mice,” Kidney International, vol. 53, no. 6, pp. 1642–1646, 1998. View at Publisher · View at Google Scholar · View at Scopus
  50. D. B. Zorov, M. Juhaszova, and S. J. Sollott, “Mitochondrial ROS-induced ROS release: an update and review,” Biochimica et Biophysica Acta (BBA)—Bioenergetics, vol. 1757, no. 5-6, pp. 509–517, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. A. P. Halestrap, P. M. Kerr, S. Javadov, and K.-Y. Woodfield, “Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury of the heart,” Biochimica et Biophysica Acta—Bioenergetics, vol. 1366, no. 1-2, pp. 79–94, 1998. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Crompton, “The mitochondrial permeability transition pore and its role in cell death,” The Biochemical Journal, vol. 341, part 2, pp. 233–249, 1999. View at Google Scholar · View at Scopus
  53. G. F. Kelso, C. M. Porteous, C. V. Coulter et al., “Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties,” The Journal of Biological Chemistry, vol. 276, no. 7, pp. 4588–4596, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. V. P. Skulachev, V. N. Anisimov, Y. N. Antonenko et al., “An attempt to prevent senescence: a mitochondrial approach,” Biochimica et Biophysica Acta—Bioenergetics, vol. 1787, no. 5, pp. 437–461, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. H. M. Cochemé, G. F. Kelso, A. M. James et al., “Mitochondrial targeting of quinones: therapeutic implications,” Mitochondrion, vol. 7, pp. S94–S102, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. M. P. Murphy, “Selective targeting of bioactive compounds to mitochondria,” Trends in Biotechnology, vol. 15, no. 8, pp. 326–330, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. L. F. Yousif, K. M. Stewart, and S. O. Kelley, “Targeting mitochondria with organelle-specific compounds: strategies and applications,” ChemBioChem, vol. 10, no. 12, pp. 1939–1950, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. H. H. Szeto, “Mitochondria-targeted peptide antioxidants: novel neuroprotective agents,” The AAPS Journal, vol. 8, no. 3, pp. E521–E531, 2006. View at Publisher · View at Google Scholar · View at Scopus
  59. K. Zhao, G.-M. Zhao, D. Wu et al., “Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury,” Journal of Biological Chemistry, vol. 279, no. 33, pp. 34682–34690, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. C. C. Winterbourn, H. N. Parsons-Mair, S. Gebicki, J. M. Gebicki, and M. J. Davies, “Requirements for superoxide-dependent tyrosine hydroperoxide formation in peptides,” Biochemical Journal, vol. 381, no. 1, pp. 241–248, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. S. Asayama, E. Kawamura, S. Nagaoka, and H. Kawakami, “Design of manganese porphyrin modified with mitochondrial signal peptide for a new antioxidant,” Molecular Pharmaceutics, vol. 3, no. 4, pp. 468–470, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. L. N. Hanly, N. Chen, K. Aleksa et al., “N-acetylcysteine as a novel prophylactic treatment for ifosfamide-induced nephrotoxicity in children: translational pharmacokinetics,” Journal of Clinical Pharmacology, vol. 52, no. 1, pp. 55–64, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. S.-S. Sheu, D. Nauduri, and M. W. Anders, “Targeting antioxidants to mitochondria: a new therapeutic direction,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1762, no. 2, pp. 256–265, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. G. J. Gross and J. A. Auchampach, “Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs,” Circulation Research, vol. 70, no. 2, pp. 223–233, 1990. View at Google Scholar · View at Scopus
  65. A. Szewczyk, W. Jarmuszkiewicz, and W. S. Kunz, “Mitochondrial potassium channels,” IUBMB Life, vol. 61, no. 2, pp. 134–143, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. B. J. Snow, F. L. Rolfe, M. M. Lockhart et al., “A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant MitoQ as a disease-modifying therapy in Parkinson's disease,” Movement Disorders, vol. 25, no. 11, pp. 1670–1674, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. E. J. Gane, F. Weilert, D. W. Orr et al., “The mitochondria-targeted anti-oxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients,” Liver International, vol. 30, no. 7, pp. 1019–1026, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. A. M. James, H. M. Cochemé, R. A. J. Smith, and M. P. Murphy, “Interactions of mitochondria-targeted and untargeted ubiquinones with the mitochondrial respiratory chain and reactive oxygen species: implications for the use of exogenous ubiquinones as therapies and experimental tools,” The Journal of Biological Chemistry, vol. 280, no. 22, pp. 21295–21312, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Mukhopadhyay, B. Horváth, Z. Zsengellėr et al., “Mitochondrial reactive oxygen species generation triggers inflammatory response and tissue injury associated with hepatic ischemia–reperfusion: therapeutic potential of mitochondrially targeted antioxidants,” Free Radical Biology and Medicine, vol. 53, no. 5, pp. 1123–1138, 2012. View at Publisher · View at Google Scholar · View at Scopus
  70. V. J. Adlam, J. C. Harrison, C. M. Porteous et al., “Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury,” The FASEB Journal, vol. 19, no. 9, pp. 1088–1095, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. T. Mitchell, D. Rotaru, H. Saba, R. A. J. Smith, M. P. Murphy, and L. A. MacMillan-Crow, “The mitochondria-targeted antioxidant mitoquinone protects against cold storage injury of renal tubular cells and rat kidneys,” Journal of Pharmacology and Experimental Therapeutics, vol. 336, no. 3, pp. 682–692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. A. J. Dare, E. A. Bolton, G. J. Pettigrew, J. A. Bradley, K. Saeb-Parsy, and M. P. Murphy, “Protection against renal ischemia-reperfusion injury in vivo by the mitochondria targeted antioxidant MitoQ,” Redox Biology, vol. 5, pp. 163–168, 2015. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. N. Antonenko, A. V. Avetisyan, L. E. Bakeeva et al., “Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies,” Biochemistry, vol. 73, no. 12, pp. 1273–1287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. L. E. Bakeeva, I. V. Barskov, M. V. Egorov et al., “Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 2. Treatment of some ROS- and age-related diseases (heart arrhythmia, heart infarctions, kidney ischemia, and stroke),” Biochemistry, vol. 73, no. 12, pp. 1288–1299, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. E. Y. Plotnikov, A. K. Vasileva, A. A. Arkhangelskaya, I. B. Pevzner, V. P. Skulachev, and D. B. Zorov, “Interrelations of mitochondrial fragmentation and cell death under ischemia/reoxygenation and UV-irradiation: protective effects of SkQ1, lithium ions and insulin,” FEBS Letters, vol. 582, no. 20, pp. 3117–3124, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. E. Y. Plotnikov, A. A. Chupyrkina, S. S. Jankauskas et al., “Mechanisms of nephroprotective effect of mitochondria-targeted antioxidants under rhabdomyolysis and ischemia/reperfusion,” Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease, vol. 1812, no. 1, pp. 77–86, 2011. View at Publisher · View at Google Scholar · View at Scopus
  77. E. J. Sharples and M. M. Yaqoob, “Erythropoietin in experimental acute renal failure,” Nephron Experimental Nephrology, vol. 104, no. 3, pp. e83–e88, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. E. J. Sharples, N. Patel, P. Brown et al., “Erythropoietin protects the kidney against the injury and dysfunction caused by ischemia-reperfusion,” Journal of the American Society of Nephrology, vol. 15, no. 8, pp. 2115–2124, 2004. View at Publisher · View at Google Scholar · View at Scopus
  79. Y. R. Song, T. Lee, S. J. You et al., “Prevention of acute kidney injury by erythropoietin in patients undergoing coronary artery bypass grafting: a pilot study,” American Journal of Nephrology, vol. 30, no. 3, pp. 253–260, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Juhaszova, D. B. Zorov, S. H. Kim et al., “Glycogen synthase kinase- 3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore,” Journal of Clinical Investigation, vol. 113, no. 11, pp. 1535–1549, 2004. View at Publisher · View at Google Scholar
  81. Z. Wang, Y. Ge, H. Bao, L. Dworkin, A. Peng, and R. Gong, “Redox-sensitive glycogen synthase kinase 3β-directed control of mitochondrial permeability transition: rheostatic regulation of acute kidney injury,” Free Radical Biology and Medicine, vol. 65, pp. 849–858, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. E. Y. Plotnikov, A. V. Kazachenko, M. Y. Vyssokikh et al., “The role of mitochondria in oxidative and nitrosative stress during ischemia/reperfusion in the rat kidney,” Kidney International, vol. 72, no. 12, pp. 1493–1502, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. P. Mukhopadhyay, B. Horváth, Z. Zsengellér et al., “Mitochondrial-targeted antioxidants represent a promising approach for prevention of cisplatin-induced nephropathy,” Free Radical Biology and Medicine, vol. 52, no. 2, pp. 497–506, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. S. S. Jankauskas, E. Y. Plotnikov, M. A. Morosanova et al., “Mitochondria-targeted antioxidant SkQR1 ameliorates gentamycin-induced renal failure and hearing loss,” Biochemistry, vol. 77, no. 6, pp. 666–670, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. H. T. F. Facundo, J. G. de Paula, and A. J. Kowaltowski, “Mitochondrial ATP-sensitive K+ channels prevent oxidative stress, permeability transition and cell death,” Journal of Bioenergetics and Biomembranes, vol. 37, no. 2, pp. 75–82, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. H. T. F. Facundo, J. G. de Paula, and A. J. Kowaltowski, “Mitochondrial ATP-sensitive K+ channels are redox-sensitive pathways that control reactive oxygen species production,” Free Radical Biology and Medicine, vol. 42, no. 7, pp. 1039–1048, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. F. Domoki, F. Bari, K. Nagy, D. W. Busija, and L. Siklós, “Diazoxide prevents mitochondrial swelling and Ca2+ accumulation in CA1 pyramidal cells after cerebral ischemia in newborn pigs,” Brain Research, vol. 1019, no. 1-2, pp. 97–104, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Ichinose, H. Yonemochi, T. Sato, and T. Saikawa, “Diazoxide triggers cardioprotection against apoptosis induced by oxidative stress,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 284, no. 6, pp. H2235–H2241, 2003. View at Publisher · View at Google Scholar · View at Scopus
  89. W. B. Reeves and S. V. Shah, “Activation of potassium channels contributes to hypoxic injury in proximal tubules,” The Journal of Clinical Investigation, vol. 94, no. 6, pp. 2289–2294, 1994. View at Publisher · View at Google Scholar · View at Scopus
  90. Z. Sun, X. Zhang, K. Ito et al., “Amelioration of oxidative mitochondrial DNA damage and deletion after renal ischemic injury by the KATP channel opener diazoxide,” American Journal of Physiology—Renal Physiology, vol. 294, no. 3, pp. F491–F498, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. S. Javadov, M. Karmazyn, and N. Escobales, “Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases,” Journal of Pharmacology and Experimental Therapeutics, vol. 330, no. 3, pp. 670–678, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Morin, R. Assaly, S. Paradis, and A. Berdeaux, “Inhibition of mitochondrial membrane permeability as a putative pharmacological target for cardioprotection,” Current Medicinal Chemistry, vol. 16, no. 33, pp. 4382–4398, 2009. View at Publisher · View at Google Scholar · View at Scopus
  93. K. Devalaraja-Narashimha, A. M. Diener, and B. J. Padanilam, “Cyclophilin D gene ablation protects mice from ischemic renal injury,” American Journal of Physiology—Renal Physiology, vol. 297, no. 3, pp. F749–F759, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. C. W. Yang, H. J. Ahn, H. J. Han et al., “Pharmacological preconditioning with low-dose cyclosporine or FK506 reduces subsequent ischemia/reperfusion injury in rat kidney,” Transplantation, vol. 72, no. 11, pp. 1753–1759, 2001. View at Publisher · View at Google Scholar · View at Scopus
  95. D. Singh, V. Chander, and K. Chopra, “Cyclosporine protects against ischemia/reperfusion injury in rat kidneys,” Toxicology, vol. 207, no. 3, pp. 339–347, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. D. K. Ysebaert, K. E. De Greef, E. J. Nouwen, G. A. Verpooten, E. J. Eyskens, and M. E. De Broe, “Influence of cyclosporin A on the damage and regeneration of the kidney after severe ischemia/reperfusion injury,” Transplantation Proceedings, vol. 29, no. 5, pp. 2348–2351, 1997. View at Publisher · View at Google Scholar · View at Scopus
  97. G. M. Gonçalves, M. A. Cenedeze, C. Q. Feitoza et al., “The role of immunosuppressive drugs in aggravating renal ischemia and reperfusion injury,” Transplantation Proceedings, vol. 39, no. 2, pp. 417–420, 2007. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Zhao, G.-M. Zhao, D. Wu et al., “Cell-permeable peptide antioxidants targeted to inner mitochondrial membrane inhibit mitochondrial swelling, oxidative cell death, and reperfusion injury,” The Journal of Biological Chemistry, vol. 279, no. 33, pp. 34682–34690, 2004. View at Publisher · View at Google Scholar · View at Scopus
  99. D. A. Brown, H. N. Sabbah, and S. R. Shaikh, “Mitochondrial inner membrane lipids and proteins as targets for decreasing cardiac ischemia/reperfusion injury,” Pharmacology and Therapeutics, vol. 140, no. 3, pp. 258–266, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. D.-F. Dai, T. Chen, H. Szeto et al., “Mitochondrial targeted antioxidant peptide ameliorates hypertensive cardiomyopathy,” Journal of the American College of Cardiology, vol. 58, no. 1, pp. 73–82, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. L. Yang, K. Zhao, N. Y. Calingasan, G. Luo, H. H. Szeto, and M. F. Beal, “Mitochondria targeted peptides protect against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity,” Antioxidants & Redox Signaling, vol. 11, no. 9, pp. 2095–2104, 2009. View at Google Scholar
  102. S. Cho, H. H. Szeto, E. Kim, H. Kim, A. T. Tolhurst, and J. T. Pinto, “A novel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36,” Journal of Biological Chemistry, vol. 282, no. 7, pp. 4634–4642, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. R. A. Kloner, S. L. Hale, W. Dai et al., “Reduction of ischemia/reperfusion injury with bendavia, a mitochondria-targeting cytoprotective peptide,” Journal of the American Heart Association, vol. 1, no. 3, pp. e001644–e001644, 2012. View at Publisher · View at Google Scholar
  104. D. A. Brown, S. L. Hale, C. P. Baines et al., “Reduction of early reperfusion injury with the mitochondria-targeting peptide bendavia,” Journal of Cardiovascular Pharmacology and Therapeutics, vol. 19, no. 1, pp. 121–132, 2014. View at Publisher · View at Google Scholar · View at Scopus
  105. A. K. Chakrabarti, K. Feeney, C. Abueg et al., “Rationale and design of the EMBRACE STEMI Study: a phase 2a, randomized, double-blind, placebo-controlled trial to evaluate the safety, tolerability and efficacy of intravenous Bendavia on reperfusion injury in patients treated with standard therapy including primary percutaneous coronary intervention and stenting for ST-segment elevation myocardial infarction,” American Heart Journal, vol. 165, no. 4, pp. 509–514.e7, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. H. H. Szeto, S. Liu, Y. Soong et al., “Mitochondria-targeted peptide accelerates ATP recovery and reduces ischemic kidney injury,” Journal of the American Society of Nephrology, vol. 22, no. 6, pp. 1041–1052, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. A. Eirin, Z. Li, X. Zhang et al., “A mitochondrial permeability transition pore inhibitor improves renal outcomes after revascularization in experimental atherosclerotic renal artery stenosis,” Hypertension, vol. 60, no. 5, pp. 1242–1249, 2012. View at Publisher · View at Google Scholar · View at Scopus
  108. N. Parajuli and L. A. MacMillan-Crow, “Role of reduced manganese superoxide dismutase in ischemia-reperfusion injury: a possible trigger for autophagy and mitochondrial biogenesis?” American Journal of Physiology—Renal Physiology, vol. 304, no. 3, pp. F257–F267, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. H. L. Liang, G. Hilton, J. Mortensen, K. Regner, C. P. Johnson, and V. Nilakantan, “MnTMPyP, a cell-permeant SOD mimetic, reduces oxidative stress and apoptosis following renal ischemia-reperfusion,” American Journal of Physiology—Renal Physiology, vol. 296, no. 2, pp. F266–F276, 2009. View at Publisher · View at Google Scholar · View at Scopus
  110. K. Dobashi, B. Ghosh, J. K. Orak, I. Singh, and A. K. Singh, “Kidney ischemia-reperfusion: modulation of antioxidant defenses,” Molecular and Cellular Biochemistry, vol. 205, no. 1-2, pp. 1–11, 2000. View at Publisher · View at Google Scholar · View at Scopus
  111. H. Saba, I. Batinic-Haberle, S. Munusamy et al., “Manganese porphyrin reduces renal injury and mitochondrial damage during ischemia/reperfusion,” Free Radical Biology and Medicine, vol. 42, no. 10, pp. 1571–1578, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. J. Cohen, T. Dorai, C. Ding, I. Batinic-Haberle, and M. Grasso, “The administration of renoprotective agents extends warm ischemia in a rat model,” Journal of Endourology, vol. 27, no. 3, pp. 343–348, 2013. View at Publisher · View at Google Scholar · View at Scopus
  113. T. Dorai, A. I. Fishman, C. Ding, I. Batinic-Haberle, D. S. Goldfarb, and M. Grasso, “Amelioration of renal ischemia-reperfusion injury with a novel protective cocktail,” Journal of Urology, vol. 186, no. 6, pp. 2448–2454, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. 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
  115. S. Miriyala, I. Spasojevic, A. Tovmasyan et al., “Manganese superoxide dismutase, MnSOD and its mimics,” Biochimica et Biophysica Acta, vol. 1822, no. 5, pp. 794–814, 2012. View at Publisher · View at Google Scholar · View at Scopus
  116. I. Batinic-Haberle, I. Spasojevic, H. M. Tse et al., “Design of Mn porphyrins for treating oxidative stress injuries and their redox-based regulation of cellular transcriptional activities,” Amino Acids, vol. 42, no. 1, pp. 95–113, 2012. View at Publisher · View at Google Scholar · View at Scopus
  117. I. Batinic-Haberle, A. Tovmasyan, and I. Spasojevic, “An educational overview of the chemistry, biochemistry and therapeutic aspects of Mn porphyrins—from superoxide dismutation to H2O2-driven pathways,” Redox Biology, vol. 5, pp. 43–65, 2015. View at Publisher · View at Google Scholar · View at Scopus
  118. R. A. J. Smith, C. M. Porteous, C. V. Coulter, and M. P. Murphy, “Selective targeting of an antioxidant to mitochondria,” European Journal of Biochemistry, vol. 263, no. 3, pp. 709–716, 1999. View at Publisher · View at Google Scholar
  119. S. E. Brown, M. F. Ross, A. Sanjuan-Pla, A.-R. B. Manas, R. A. J. Smith, and M. P. Murphy, “Targeting lipoic acid to mitochondria: synthesis and characterization of a triphenylphosphonium-conjugated α-lipoyl derivative,” Free Radical Biology and Medicine, vol. 42, no. 12, pp. 1766–1780, 2007. View at Publisher · View at Google Scholar · View at Scopus
  120. A. Filipovska, G. F. Kelso, S. E. Brown, S. M. Beer, R. A. J. Smith, and M. P. Murphy, “Synthesis and characterization of a triphenylphosphonium-conjugated peroxidase mimetic: insights into the interaction of ebselen with mitochondria,” The Journal of Biological Chemistry, vol. 280, no. 25, pp. 24113–24126, 2005. View at Publisher · View at Google Scholar · View at Scopus
  121. P. K. Chatterjee, S. Cuzzocrea, P. A. J. Brown et al., “Tempol, a membrane-permeable radical scavenger, reduces oxidant stress-mediated renal dysfunction and injury in the rat,” Kidney International, vol. 58, no. 2, pp. 658–673, 2000. View at Publisher · View at Google Scholar · View at Scopus
  122. U. Aksu, B. Ergin, R. Bezemer et al., “Scavenging reactive oxygen species using tempol in the acute phase of renal ischemia/reperfusion and its effects on kidney oxygenation and nitric oxide levels,” Intensive Care Medicine Experimental, vol. 3, article 21, 2015. View at Publisher · View at Google Scholar