The Mitochondria-Targeted Antioxidants and Remote Kidney Preconditioning Ameliorate Brain Damage through Kidney-to-Brain Cross-Talk

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Silachev, Denis N ^a   Isaev, Nikolay K ^a,b   Pevzner, Irina B ^a   Zorova, Ljubava D ^a   Stelmashook, Elena V ^a,b   Novikova, Svetlana V ^a,b   Plotnikov, Egor Y ^a   Skulachev, Vladimir P ^a   Zorov, Dmitry B ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b RESEARCH CENTER OF NEUROLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

[10 (6' PLASTOQUINONYL)DECYLRHODAMINE]; GLYCOGEN SYNTHASE KINASE 3BETA; PLASTOQUINONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DEFENSE MECHANISM; EMBRYO; IMMUNOCYTOCHEMISTRY; KIDNEY FUNCTION; KIDNEY TUBULE EPITHELIUM; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MITOCHONDRION; NEPHRECTOMY; NEPHROTOXICITY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; REMOTE KIDNEY PRECONDITIONING; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

ANIMALS; ANTIOXIDANTS; BRAIN; EPITHELIAL CELLS; ERYTHROPOIETIN; GENTAMICINS; IMMUNOASSAY; INFARCTION, MIDDLE CEREBRAL ARTERY; ISCHEMIA; ISCHEMIC PRECONDITIONING; KIDNEY; KIDNEY TUBULES; MALE; MITOCHONDRIA; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLASTOQUINONE; RATS; RHODAMINES;

RATTUS;

EID: 84871334541     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051553     Document Type: Article

References (55)

1. Cocheme HM, Kelso GF, James AM, Ross MF, Trnka J, et al. (2007) Mitochondrial targeting of quinones: therapeutic implications. Mitochondrion 7Suppl: S94-102.
2. Skulachev VP, (2007) A biochemical approach to the problem of aging: "megaproject" on membrane-penetrating ions. The first results and prospects. Biochemistry (Mosc) 72: 1385-1396.
3. Anisimov VN, Bakeeva LE, Egormin PA, Filenko OF, Isakova EF, et al. (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 5. SkQ1 prolongs lifespan and prevents development of traits of senescence. Biochemistry (Mosc) 73: 1329-1342.
4. Antonenko YN, Avetisyan AV, Bakeeva LE, Chernyak BV, Chertkov VA, et al. (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 1. Cationic plastoquinone derivatives: synthesis and in vitro studies. Biochemistry (Mosc) 73: 1273-1287.
5. Bakeeva LE, Barskov IV, Egorov MV, Isaev NK, Kapelko VI, et al. (2008) 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 (Mosc) 73: 1288-1299.
6. Neroev VV, Archipova MM, Bakeeva LE, Fursova AZh, Grigorian EN, et al. (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 4. Age-related eye disease. SkQ1 returns vision to blind animals. Biochemistry (Mosc) 73: 1317-1328.
7. Kelso GF, Porteous CM, Coulter CV, Hughes G, Porteous WK, et al. (2001) Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J Biol Chem 276: 4588-4596.
8. Skulachev VP, (2009) New data on biochemical mechanism of programmed senescence of organisms and antioxidant defense of mitochondria. Biochemistry (Mosc) 74: 1400-1403.
9. Plotnikov EY, Silachev DN, Chupyrkina AA, Danshina MI, Jankauskas SS, et al. (2010) New-generation Skulachev ions exhibiting nephroprotective and neuroprotective properties. Biochemistry (Mosc) 75: 145-150.
10. Plotnikov EY, Chupyrkina AA, Jankauskas SS, Pevzner IB, Silachev DN, et al. (2011) Mechanisms of nephroprotective effect of mitochondria-targeted antioxidants under rhabdomyolysis and ischemia/reperfusion. Biochim Biophys Acta 1812: 77-86.
11. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, et al. (2002) Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22: 10291-10301.
12. Paliege A, Rosenberger C, Bondke A, Sciesielski L, Shina A, et al. (2010) Hypoxia-inducible factor-2alpha-expressing interstitial fibroblasts are the only renal cells that express erythropoietin under hypoxia-inducible factor stabilization. Kidney Int 77: 312-318.
13. Hagen T (2012) Oxygen versus reactive oxygen in the regulation of HIF-1alpha: The Balance Tips. Biochem Res Int: doi:10.1155/2012/436981.
14. Huang LE, Arany Z, Livingston DM, Bunn HF, (1996) Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 271: 32253-32259.
15. Ivan M, Kondo K, Yang H, Kim W, Valiando J, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468.
16. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
17. Diwan V, Jaggi AS, Singh M, Singh N, Singh D, (2008) Possible involvement of erythropoietin in remote renal preconditioning-induced cardioprotection in rats. J Cardiovasc Pharmacol 51: 126-130.
18. Ishida T, Yarimizu K, Gute DC, Korthuis RJ, (1997) Mechanisms of ischemic preconditioning. Shock 8: 86-94.
19. Tapuria N, Kumar Y, Habib MM, Abu Amara M, Seifalian AM, et al. (2008) Remote ischemic preconditioning: a novel protective method from ischemia reperfusion injury-a review. J Surg Res 150: 304-330.
20. McClanahan TB, Nao BS, Wolke LJ, Martin BJ, Mertz TE, et al. (1993) Brief renal occlusion and reperfusion reduces myocardial infarct size in rabbits. FASEB J 7: A118.
21. Juhaszova M, Zorov DB, Kim SH, Pepe S, Fu Q, et al. (2004) Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest 113: 1535-1549.
22. Plotnikov EY, Kazachenko AV, Vyssokikh MY, Vasileva AK, Tcvirkun DV, et al. (2007) The role of mitochondria in oxidative and nitrosative stress during ischemia/reperfusion in the rat kidney. Kidney Int 72: 1493-1502.
23. Longa EZ, Weinstein PR, Carlson S, Cummins R, (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20: 84-91.
24. Silachev DN, Uchevatkin AA, Pirogov YA, Zorov DB, Isaev NK, (2009) Comparative evaluation of two methods for studies of experimental focal ischemia: magnetic resonance tomography and triphenyltetrazoleum detection of brain injuries. Bull Exp Biol Med 147: 269-272.
25. Barone FC, Clark RK, Feuerstein G, Lenkinski RE, Sarkar SK, (1991) Quantitative comparison of magnetic resonance imaging (MRI) and histologic analyses of focal ischemic damage in the rat. Brain Res Bull 26: 285-291.
26. Jolkkonen J, Puurunen K, Rantakomi S, Harkonen A, Haapalinna A, et al. (2000) Behavioral effects of the alpha(2)-adrenoceptor antagonist, atipamezole, after focal cerebral ischemia in rats. Eur J Pharmacol 400: 211-219.
27. Brewer GJ, (1995) Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J Neurosci Res 42: 674-683.
28. McCarthy KD, de Vellis J, (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85: 890-902.
29. Hunter AJ, Green AR, Cross AJ, (1995) Animal models of acute ischaemic stroke: can they predict clinically successful neuroprotective drugs? Trends Pharmacol Sci 16: 123-128.
30. Slemmer JE, Shacka JJ, Sweeney MI, Weber JT, (2008) Antioxidants and free radical scavengers for the treatment of stroke, traumatic brain injury and aging. Curr Med Chem 15: 404-414.
31. Becker LB, (2004) New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res 61: 461-470.
32. Adlam VJ, Harrison JC, Porteous CM, James AM, Smith RA, et al. (2005) Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J 19: 1088-1095.
33. Hobbs CE, Murphy MP, Smith RA, Oorschot DE, (2008) Neonatal rat hypoxia-ischemia: Effect of the anti-oxidant mitoquinol, and S-PBN. Pediatr Int 50: 481-488.
34. Antonenko YN, Roginsky VA, Pashkovskaya AA, Rokitskaya TI, Kotova EA, et al. (2008) Protective effects of mitochondria-targeted antioxidant SkQ in aqueous and lipid membrane environments. J Membr Biol 222: 141-149.
35. Isaev NK, Novikova SV, Stelmashuk EV, Barskov IV, Silachev DN, et al. (2012) Mitochondria targeted plastoquinone antioxidant SkQR1 decreases trauma-induced neurological deficit in rat. Biochemistry (Mosc) 77: 1201-1206.
36. Skulachev MV, Antonenko YN, Anisimov VN, Chernyak BV, Cherepanov DA, et al. (2011) Mitochondrial-targeted plastoquinone derivatives. Effect on senescence and acute age-related pathologies. Curr Drug Targets 12: 800-826.
37. Jelkmann W, Pagel H, Hellwig T, Fandrey J, (1997) Effects of antioxidant vitamins on renal and hepatic erythropoietin production. Kidney Int 51: 497-501.
38. Neumcke I, Schneider B, Fandrey J, Pagel H, (1999) Effects of pro- and antioxidative compounds on renal production of erythropoietin. Endocrinology 140: 641-645.
39. Canbolat O, Fandrey J, Jelkmann W, (1998) Effects of modulators of the production and degradation of hydrogen peroxide on erythropoietin synthesis. Respir Physiol 114: 175-183.
40. Zembron-Lacny A, Slowinska-Lisowska M, Szygula Z, Witkowski K, Szyszka K, (2009) The comparison of antioxidant and hematological properties of N-acetylcysteine and alpha-lipoic acid in physically active males. Physiol Res 58: 855-861.
41. Momeni M, De Kock M, Devuyst O, Liistro G, (2011) Effect of N-acetyl-cysteine and hyperoxia on erythropoietin production. Eur J Appl Physiol 111: 2681-2686.
42. Hildebrandt W, Alexander S, Bartsch P, Droge W, (2002) Effect of N-acetyl-cysteine on the hypoxic ventilatory response and erythropoietin production: linkage between plasma thiol redox state and O(2) chemosensitivity. Blood 99: 1552-1555.
43. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA, (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature. 378: 785-789.
44. Juhaszova M, Zorov DB, Yaniv Y, Nuss HB, Wang S, et al. (2009) Role of glycogen synthase kinase-3beta in cardioprotection. Circ Res 104: 1240-1252.
45. Bhat RV, Budd Haeberlein SL, Avila J, (2004) Glycogen synthase kinase 3: a drug target for CNS therapies. J Neurochem 89: 1313-1317.
46. Miura T, Tanno M, Sato T, (2010) Mitochondrial kinase signalling pathways in myocardial protection from ischaemia/reperfusion-induced necrosis. Cardiovasc Res 88: 7-15.
47. Quiroz JA, Machado-Vieira R, Zarate CAJ, Manji HK, (2010) Novel insights into lithium's mechanism of action: neurotrophic and neuroprotective effects. Neuropsychobiology 62: 50-60.
48. Noguchi CT, Asavaritikrai P, Teng R, Jia Y, (2007) Role of erythropoietin in the brain. Crit Rev Oncol Hematol 64: 159-171.
49. Diwan V, Kant R, Jaggi AS, Singh N, Singh D, (2008) Signal mechanism activated by erythropoietin preconditioning and remote renal preconditioning-induced cardioprotection. Mol Cell Biochem 315: 195-201.
50. Ludman AJ, Yellon DM, Hasleton J, Ariti C, Babu GG, et al. (2011) Effect of erythropoietin as an adjunct to primary percutaneous coronary intervention: a randomised controlled clinical trial. Heart 97: 1560-1565.
51. Najjar SS, Rao SV, Melloni C, Raman SV, Povsic TJ, et al. (2011) Intravenous erythropoietin in patients with ST-segment elevation myocardial infarction: REVEAL: a randomized controlled trial. JAMA 305: 1863-1872.
52. Prunier F, Biere L, Gilard M, Boschat J, Mouquet F, et al. (2012) Single high-dose erythropoietin administration immediately after reperfusion in patients with ST-segment elevation myocardial infarction: results of the erythropoietin in myocardial infarction trial. Am Heart J 163: 200-207.
53. Ehrenreich H, Weissenborn K, Prange H, Schneider D, Weimar C, et al. (2009) Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 40: e647-656.
54. Ehrenreich H, Kastner A, Weissenborn K, Streeter J, Sperling S, et al. (2011) Circulating damage marker profiles support a neuroprotective effect of erythropoietin in ischemic stroke patients. Mol Med 17: 1306-1310.
55. Bergmann M, Haufe S, von Knobelsdorff-Brenkenhoff F, Mehling H, Wassmuth R, et al. (2011) A pilot study of chronic, low-dose epoetin-{beta} following percutaneous coronary intervention suggests safety, feasibility, and efficacy in patients with symptomatic ischaemic heart failure. Eur J Heart Fail 13: 560-568.