Redox-sensitive glycogen synthase kinase 3β-directed control of mitochondrial permeability transition: Rheostatic regulation of acute kidney injury

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 849-858

  Wang, Zhen ^a,b   Ge, Yan ^b   Bao, Hui ^a,b   Dworkin, Lance ^b   Peng, Ai ^a   Gong, Rujun ^b  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b BROWN UNIVERSITY   (United States)

Author keywords

Acute kidney injury; Cyclophilin F; Free radicals; Glycogen synthase kinase 3 ; Mitochondrial permeability transition; Paraquat; Voltage dependent anion channel

Indexed keywords

CYCLOPHILIN; CYCLOPHILIN F; ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; PARAQUAT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL; CARRIER PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE;

ACUTE KIDNEY FAILURE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY DYSFUNCTION; KIDNEY TUBULE CELL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SENSITIZATION; ANIMAL; C57BL MOUSE; CELL LINE; ENZYMOLOGY; KIDNEY TUBULE; MALE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PHOSPHORYLATION; PROTEIN PROCESSING;

ACUTE KIDNEY INJURY; ANIMALS; CELL LINE; CYCLOPHILINS; GLYCOGEN SYNTHASE KINASE 3; KIDNEY TUBULES; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84883640597     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.08.169     Document Type: Article

References (69)

1. R.L. Mehta, J.A. Kellum, S.V. Shah, B.A. Molitoris, C. Ronco, D.G. Warnock, and A. Levin Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury Crit. Care 11 2007
2. R. Toth, T. Breuer, Z. Cserep, D. Lex, L. Fazekas, E. Sapi, A. Szatmari, J. Gal, and A. Szekely Acute kidney injury is associated with higher morbidity and resource utilization in pediatric patients undergoing heart surgery Ann. Thorac. Surg. 93 2012 1984 1991
3. X. Valette, J.-J. Parienti, B. Plaud, P. Lehoux, D. Samba, and J.-L. Hanouz Incidence, morbidity, and mortality of contrast-induced acute kidney injury in a surgical intensive care unit: a prospective cohort study J. Crit. Care 27 2012 (322.e321-325)
4. 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 J. Am. Soc. Nephrol. 16 2005 3365 3370 (Pubitemid 46179340)
5. W.J. Mergner, B.F. Trump, J. Valigors, J. Garbus, and J.H. Dees Structural and functional changes in human kidney and liver mitochondria in acute cell injury after shock and trauma Am. J. Pathol. 66 1972 A36
6. A.M. Hall Pores for thought: new strategies to re-energize stressed mitochondria in acute kidney injury J. Am. Soc. Nephrol. 22 2011 986 989
7. S. Jankauskas, E. Plotnikov, I. Pevzner, A. Chupyrkina, V. Kirpatovsky, and D. Zorov Mitochondria-targeted antioxidant SkQR1 prevents acute kidney injury after ischemia/reperfusion, rhabdomyolysis and gentamicin toxicity FEBS J. 279 2012 (205-205)
8. L.E. Bakeeva, I.V. Barskov, M.V. Egorov, N.K. Isaev, V.I. Kapelko, A.V. Kazachenko, V.I. Kirpatovsky, S.V. Kozlovsky, V.L. Lakomkin, S.B. Levina, O.I. Pisarenko, E.Y. Plotnikov, V.B. Saprunova, L.I. Serebryakova, M.V. Skulachev, E.V. Stelmashook, I.M. Studneva, O.V. Tskitishvili, A.K. Vasilyeva, I.V. Victorov, D.B. Zorov, and V.P. Skulachev 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 (Moscow) 73 2008 1288 1299
9. P. Caro, J. Gomez, I. Sanchez, A. Naudi, V. Ayala, M. Lopez-Torres, R. Pamplona, and G. Barja Forty percent methionine restriction decreases mitochondrial oxygen radical production and leak at complex I during forward electron flow and lowers oxidative damage to proteins and mitochondrial DNA in rat kidney and brain mitochondria Rejuvenation Res 12 2009 421 434
10. G. Gobe, and D. Crane Mitochondria, reactive oxygen species and cadmium toxicity in the kidney Toxicol. Lett. 198 2010 49 55
11. M. Saotome, H. Katoh, Y. Yaguchi, T. Tanaka, T. Urushida, H. Satoh, and H. Hayashi Transient opening of mitochondrial permeability transition pore by reactive oxygen species protects myocardium from ischemia-reperfusion injury Am. J. Physiol. Heart Circ. Physiol 296 2009 H1125 H1132
12. C. Bonnard, A. Durand, S. Peyrol, E. Chanseaume, M.-A. Chauvin, B. Morio, H. Vidal, and J. Rieusset Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice J. Clin. Invest. 118 2008 789 800 (Pubitemid 351206566)
13. J.M. Bruey, C. Ducasse, P. Bonniaud, L. Ravagnan, S.A. Susin, C. Diaz-Latoud, S. Gurbuxani, A.P. Arrigo, G. Kroemer, E. Solary, and C. Garrido Hsp27 negatively regulates cell death by interacting with cytochrome c Nat. Cell Biol. 2 2000 645 652
14. J.G. Pastorino, J.B. Hoek, and N. Shulga Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity Cancer Res 65 2005 10545 10554 (Pubitemid 41743749)
15. M. Juhaszova, D.B. Zorov, Y. Yaniv, H.B. Nuss, S. Wang, and S.J. Sollott Role of glycogen synthase kinase-3beta in cardioprotection Circ. Res. 104 2009 1240 1252
16. E. Basso, V. Petronilli, M.A. Forte, and P. Bernardi Phosphate is essential for inhibition of the mitochondrial permeability transition pore by cyclosporin A and by cyclophilin D ablation J. Biol. Chem. 283 2008 26307 26311
17. V. Giorgio, M.E. Soriano, E. Basso, E. Bisetto, G. Lippe, M.A. Forte, and P. Bernardi Cyclophilin D in mitochondrial pathophysiology Biochim. Biophys. Acta Bioenerg 1797 2010 1113 1118
18. J.S. Park, R. Pasupulati, T. Feldkamp, N.F. Roeser, and J.M. Weinberg Cyclophilin D and the mitochondrial permeability transition in kidney proximal tubules after hypoxic and ischemic injury Am. J. Physiol. Renal Physiol 301 2011 F134 F150
19. C. Chinopoulos, and V. Adam-Vizi Modulation of the mitochondrial permeability transition by cyclophilin D: moving closer to F-0-F-1 ATP synthase? Mitochondrion 12 2012 41 45
20. T. Miura, and T. Miki GSK-3 beta, a therapeutic target for cardiomyocyte protection Circ. J. 73 2009 1184 1192
21. G.V. Rayasam, V.K. Tulasi, R. Sodhi, J.A. Davis, and A. Ray Glycogen synthase kinase 3: more than a namesake Br. J. Pharmacol. 156 2009 885 898
22. U.G. Kang, M.S. Seo, M.-S. Roh, Y. Kim, S.C. Yoon, and Y.S. Kim The effects of clozapine on the GSK-3-mediated signaling pathway FEBS Lett. 560 2004 115 119 (Pubitemid 38264303)
23. A. Martinez, A. Castro, I. Dorronsoro, and M. Alonso Glycogen synthase kinase 3 (GSK-3) inhibitors as new promising drugs for diabetes, neurodegeneration, cancer, and inflammation Med. Res. Rev. 22 2002 373 384 (Pubitemid 34620473)
24. B.W. Doble, and J.R. Woodgett GSK-3: tricks of the trade for a multi-tasking kinase J. Cell Sci. 116 2003 1175 1186 (Pubitemid 36410657)
25. P.J. Nelson, and L. Cantley GSK3β plays dirty in acute kidney injury J. Am. Soc. Nephrol. 21 2010 199 200
26. H. Bao, Y. Ge, S. Zhuang, L.D. Dworkin, Z. Liu, and R. Gong Inhibition of glycogen synthase kinase-3beta prevents NSAID-induced acute kidney injury Kidney Int. 81 2012 662 673
27. C. Howard, S. Tao, H.-C. Yang, A.B. Fogo, J.R. Woodgett, R.C. Harris, and R. Rao Specific deletion of glycogen synthase kinase-3beta in the renal proximal tubule protects against acute nephrotoxic injury in mice Kidney Int. 82 2012 1000 1009
28. Z. Wang, A. Havasi, J. Gall, R. Bonegio, Z. Li, H. Mao, J.H. Schwartz, and S.C. Borkan GSK3β promotes apoptosis after renal ischemic injury J. Am. Soc. Nephrol. 21 2010 284 294
29. R. Gong, A. Rifai, Y. Ge, S. Chen, and L.D. Dworkin Hepatocyte growth factor suppresses proinflammatory NF kappa B activation through GSK3 beta inactivation in renal tubular epithelial cells J. Biol. Chem. 283 2008 7401 7410
30. P.R. Castello, D.A. Drechsel, and M. Patel Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain J. Biol. Chem. 282 2007 14186 14193 (Pubitemid 47100444)
31. C. Zhu, S. Huang, Y. Yuan, G. Ding, R. Chen, B. Liu, T. Yang, and A. Zhang Mitochondrial dysfunction mediates aldosterone-induced podocyte damage: a therapeutic target of PPAR gamma Am. J. Pathol. 178 2011 2020 2031
32. C. Enrique Guerrero-Beltran, M. Calderon-Oliver, E. Martinez-Abundis, E. Tapia, G. Zarco-Marquez, C. Zazueta, and J. Pedraza-Chaverri Protective effect of sulforaphane against cisplatin-induced mitochondrial alterations and impairment in the activity of NAD(P)H:quinone oxidoreductase 1 and gamma glutamyl cysteine ligase: studies in mitochondria isolated from rat kidney and in LLC-PK1 cells Toxicol. Lett 199 2010 80 92
33. H.H. Szeto, S. Liu, Y. Soong, D. Wu, S.F. Darrah, F.Y. Cheng, Z. Zhao, M. Ganger, C.Y. Tow, and S.V. Seshan Mitochondria-targeted peptide accelerates ATP recovery and reduces ischemic kidney injury J. Am. Soc. Nephrol. 22 2011 1041 1052
34. A.M. Silva, and P.J. Oliveira Evaluation of respiration with Clark type electrode in isolated mitochondria and permeabilized animal cells Methods Mol. Biol. (Clifton, NJ) 810 2012 7 24
35. R. Gong, A. Rifai, and L.D. Dworkin Hepatocyte growth factor suppresses acute renal inflammation by inhibition of endothelial E-selectin Kidney Int. 69 2006 1166 1174
36. A.C. Johnson, K. Becker, and R.A. Zager Parenteral iron formulations differentially affect MCP-1, HO-1, and NGAL gene expression and renal responses to injury Am. J. Physiol. Renal Physiol 299 2010 F426 F435
37. F. Chiara, A. Gambalunga, M. Sciacovelli, A. Nicolli, L. Ronconi, D. Fregona, P. Bernardi, A. Rasola, and A. Trevisan Chemotherapeutic induction of mitochondrial oxidative stress activates GSK-3alpha/beta and Bax, leading to permeability transition pore opening and tumor cell death Cell Death Dis. 3 2012 (e444-e444)
38. T.Y. Aw Tissue oxidative stress revisited: significance of ROS and redox signaling Semin. Cell Dev. Biol. 23 2012 (721-721)
39. N. Suzuki, S. Koussevitzky, R. Mittler, and G. Miller ROS and redox signalling in the response of plants to abiotic stress Plant Cell Environ. 35 2012 259 270
40. P.D. Ray, B.-W. Huang, and Y. Tsuji Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling Cell. Signalling 24 2012 981 990
41. M. D'Amelio, M. Sheng, and F. Cecconi Caspase-3 in the central nervous system: beyond apoptosis Trends Neurosci. 35 2012 700 709
42. J. Niquet, S.G. Allen, R.A. Baldwin, and C.G. Wasterlain Evidence of caspase-3 activation in hyposmotic stress-induced necrosis Neurosci. Lett. 356 2004 225 227 (Pubitemid 38186692)
43. A.G. Porter, and R.U. Janicke Emerging roles of caspase-3 in apoptosis Cell Death Differ. 6 1999 99 104 (Pubitemid 29082297)
44. Y. Ge, J. Si, L. Tian, S. Zhuang, L.D. Dworkin, and R. Gong Conditional ablation of glycogen synthase kinase 3 beta in postnatal mouse kidney Lab. Invest. 91 2011 85 96
45. M. Crompton The mitochondrial permeability transition pore and its role in cell death Biochem. J 341 1999 233 249 (Pubitemid 29373645)
46. J.-R. Koo, J.-C. Kim, J.-W. Yoon, G.-H. Kim, R.-W. Jeon, H.-J. Kim, D.-W. Chae, and J.-W. Noh Failure of continuous venovenous hemofiltration to prevent death in paraquat poisoning Am. J. Kidney Dis. 39 2002 55 59 (Pubitemid 34062496)
47. C. Bullivant Accidental poisoning by paraquat: report of two cases in man Br. Med. J 1 1966 1272
48. I.B. Gawarammana, and N.A. Buckley Medical management of paraquat ingestion Br. J. Clin. Pharmacol. 72 2011 745 757
49. G.M. Copland, A. Kolin, and H.S. Shulman Fatal pulmonary intra-alveolar fibrosis after paraquat ingestion N. Engl. J. Med. 291 1974 290 292
50. A.C. Rodrigues Lacerda, M. d.G. Rodrigues-Machado, P.L. Mendes, R.D. Novaes, G.M. Cavalcante Carvalho, W.A. Zin, F. Gripp, and C.C. Coimbra Paraquat (PQ)-induced pulmonary fibrosis increases exercise metabolic cost, reducing aerobic performance in rats J. Toxicol. Sci. 34 2009 671 679
51. M.S. Rose, E.A. Lock, L.L. Smith, and I. Wyatt Paraquat accumulation: tissue and species specificity Biochem. Pharmacol. 25 1976 419 423
52. S.J. Kim, H.W. Gil, J.O. Yang, E.Y. Lee, and S.Y. Hong The clinical features of acute kidney injury in patients with acute paraquat intoxication Nephrol. Dial. Transplant. 24 2009 1226 1232
53. E.Y. Lee, K.Y. Kwang, J.O. Yang, and S.Y. Hong Predictors of survival after acute paraquat poisoning Toxicol. Ind. Health 18 2002 201 206
54. W. Yang, and E. Tiffany-Castiglioni Paraquat-induced apoptosis in human neuroblastoma SH-SY5Y cells: involvement of p53 and mitochondria J. Toxicol. Environ. Health Part A 71 2008 289 299 (Pubitemid 351218582)
55. C. Velez-Pardo, M. Jimenez-Del-Rio, S. Lores-Arnaiz, and J. Bustamante Protective effects of the synthetic cannabinoids CP55,940 and JWH-015 on rat brain mitochondria upon paraquat exposure Neurochem. Res 35 2010 1323 1332
56. P. Costantini, V. Petronilli, R. Colonna, and P. Bernardi On the effects of paraquat on isolated mitochondria: evidence that paraquat causes opening of the cyclosporin A-sensitive permeability transition pore synergistically with nitric oxide Toxicology 99 1995 77 88
57. C.L. Huang, Y.C. Lee, Y.C. Yang, T.Y. Kuo, and N.K. Huang Minocycline prevents paraquat-induced cell death through attenuating endoplasmic reticulum stress and mitochondrial dysfunction Toxicol. Lett. 209 2012 203 210
58. A.M. Hall, R.J. Unwin, M.G. Hanna, and M.R. Duchen Renal function and mitochondrial cytopathy (MC): more questions than answers QJM 101 2008 755 766
59. F. Kielar, M.E. Helsel, Q. Wang, and K.J. Franz Prochelator BHAPI protects cells against paraquat-induced damage by ROS-triggered iron chelation Metallomics 4 2012 899 909
60. U. Aksu, C. Demirci, and C. Ince The pathogenesis of acute kidney injury and the toxic triangle of oxygen, reactive oxygen species and nitric oxide J.A. Kellum, C. Ronco, J.L. Vincent, Controversies in Acute Kidney Injury 2011 Karger Basel 119 128
61. Z. Sedaghat, M. Kadkhodaee, B. Seifi, E. Salehi, A. Najafi, and L. Dargahi Remote peraconditioning reduces oxidative stress, downaregulates cyclooxygenasea2 expression and attenuates ischaemia/reperfusionainduced acute kidney injury Clin. Exp. Pharmacol. Physiol. 40 2013 97 103
62. G. Kroemer, L. Galluzzi, and C. Brenner Mitochondrial membrane permeabilization in cell death Physiol. Rev. 87 2007 99 163 (Pubitemid 46209992)
63. V. Borutaite Mitochondria as decision-makers in cell death Environ. Mol. Mutagen. 51 2010 406 416
64. J.J. Lemasters, A.L. Nieminen, T. Qian, L.C. Trost, S.P. Elmore, Y. Nishimura, R.A. Crowe, W.E. Cascio, C.A. Bradham, D.A. Brenner, and B. Herman The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy Biochim. Biophys. Acta 1366 1998 177 196 (Pubitemid 28467031)
65. O. Cuvillier, and T. Levade Sphingosine 1-phosphate antagonizes apoptosis of human leukemia cells by inhibiting release of cytochrome c and Smac/DIABLO from mitochondria Blood 98 2001 2828 2836
66. G. Kroemer, B. Dallaporta, and M. Resche-Rigon The mitochondrial death/life regulator in apoptosis and necrosis Annu. Rev. Physiol. 60 1998 619 642 (Pubitemid 28157889)
67. D.B. Zorov, C.R. Filburn, L.O. Klotz, J.L. Zweier, and S.J. Sollott Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes J. Exp. Med. 192 2000 1001 1014
68. D.B. Zorov, M. Juhaszova, and S.J. Sollott Mitochondrial ROS-induced ROS release: an update and review Biochim. Biophys. Acta 1757 2006 509 517
69. N.R. Brady, A. Hamacher-Brady, H.V. Westerhoff, and R.A. Gottlieb A wave of reactive oxygen species (ROS)-induced ROS release in a sea of excitable mitochondria Antioxid. Redox Signaling 8 2006 1651 1665 (Pubitemid 44726339)