Targeting mitochondria and reactive oxygen species-driven pathogenesis in diabetic nephropathy

Review of Diabetic Studies

Volumn 12, Issue 1, 2015, Pages 134-156

  Lindblom, Runa ^a,b   Higgins, Gavin ^a,b   Coughlan, Melinda ^a,b   de Haan, Judy B ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Apoptosis; Diabetes; Diabetic nephropathy; Kidney; Mitochondria; Mitochondrial dysfunction; Mitochondrial permeability transition; Necrosis; Reactive oxygen species; Therapy

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; BARDOXOLONE METHYL; CALCIUM; CELL NUCLEUS DNA; CINNAMALDEHYDE; CURCUMIN; CYCLOPHILIN D; DOXORUBICIN; EBSELEN; ELAMIPRETIDE; INOSITOL OXYGENASE; MANGIFERIN; METFORMIN; MITOCHONDRIAL DNA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MONOCYTE CHEMOTACTIC PROTEIN 1; NITROGEN DIOXIDE; PEROXYNITRITE; PROTEIN BAX; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; RESVERATROL; SULFORAPHANE; SUPEROXIDE; TRANSCRIPTION FACTOR NRF2; TRANSFORMING GROWTH FACTOR BETA; UBIQUINONE; UNINDEXED DRUG; VASCULAR CELL ADHESION MOLECULE 1; ALISPORIVIR; APOPTOSIS INDUCING FACTOR; CYCLOPHILIN INHIBITOR; CYCLOSPORIN A; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SANGLIFEHRIN A;

APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CELL DEATH; CLINICAL TRIAL (TOPIC); DIABETIC NEPHROPATHY; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DNA REPAIR; ENDOPLASMIC RETICULUM STRESS; GENE CONTROL; HUMAN; KIDNEY INJURY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; NONHUMAN; OXIDATIVE STRESS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); RESPIRATORY CHAIN; SENESCENCE; AUTOPHAGY; GENE OVEREXPRESSION; INFLAMMATION; MOLECULARLY TARGETED THERAPY; NECROSIS; RENAL PROTECTION; REVIEW; DIABETIC NEPHROPATHIES; DISEASE COURSE; DRUG EFFECTS; KIDNEY; METABOLISM; MITOCHONDRION; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; PHYSIOLOGY;

ANTIOXIDANTS; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; DISEASE PROGRESSION; HUMANS; KIDNEY; MITOCHONDRIA; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84947552407     PISSN: 16136071     EISSN: 16140575     Source Type: Journal    
DOI: 10.1900/RDS.2015.12.134     Document Type: Article

References (242)

1. Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature 2001. 414(6865):782-787.
2. Spiegel AM, Nabel EG. NIH research on obesity and type 2 diabetes: providing the scientific evidence base for actions to improve health. Nat Med 2006. 12(1):67-69.
3. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010. 87(1):4-14.
4. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, McCullough PA, Kasiske BL, Kelepouris E, Klag MJ, et al. Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Hypertension 2003. 42(5):1050-1065.
5. Schiele F. Renal dysfunction and coronary disease: a high-risk combination. J Nephrol 2009. 22(1):39-45.
6. Dinneen SF, Gerstein HC. The association of microalbuminuria and mortality in non-insulin-dependent diabetes mellitus. A systematic overview of the literature. Arch Intern Med 1997. 157(13):1413-1418.
7. Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, Halle JP, Young J, Rashkow A, Joyce C, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA 2001. 286(4):421-426.
8. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 2014. 20(7):1126-1167.
9. Jha JC, Gray SP, Barit D, Okabe J, El-Osta A, Namikoshi T, Thallas-Bonke V, Wingler K, Szyndralewiez C, Heitz F, et al. Genetic targeting or pharmacologic inhibition of NADPH oxidase nox4 provides renoprotection in long-term diabetic nephropathy. J Am Soc Nephrol 2014. 25(6):1237-1254.
10. Tonelli M, Sacks F, Pfeffer M, Jhangri GS, Curhan G, Cholesterol, Recurrent Events Trial I. Biomarkers of inflammation and progression of chronic kidney disease. Kidney Int 2005. 68(1):237-245.
11. Okamura DM, Himmelfarb J. Tipping the redox balance of oxidative stress in fibrogenic pathways in chronic kidney disease. Pediatr Nephrol 2009. 24(12):2309-2319.
12. McQueen MJ, Lonn E, Gerstein HC, Bosch J, Yusuf S. The HOPE (Heart Outcomes Prevention Evaluation) Study and its consequences. Scand J Clin Lab Invest Suppl 2005. 240:143-156.
13. Lonn E, Yusuf S, Hoogwerf B, Pogue J, Yi Q, Zinman B, Bosch J, Dagenais G, Mann JF, Gerstein HC. Effects of vitamin E on cardiovascular and microvascular outcomes in high-risk patients with diabetes: results of the HOPE study and MICRO-HOPE substudy. Diabetes Care 2002. 25(11):1919-1927.
14. Marchioli R, Levantesi G, Macchia A, Marfisi RM, Nicolosi GL, Tavazzi L, Tognoni G, Valagussa F. Vitamin E increases the risk of developing heart failure after myocardial infarction: Results from the GISSI-Prevenzione trial. J Cardiovasc Med (Hagerstown) 2006. 7(5):347-350.
15. Hakim FA, Pflueger A. Role of oxidative stress in diabetic kidney disease. Med Sci Monit 2010. 16(2):RA37-RA48.
16. Onozato ML, Tojo A, Goto A, Fujita T, Wilcox CS. Oxidative stress and nitric oxide synthase in rat diabetic nephropathy: effects of ACEI and ARB. Kidney Int 2002. 61(1):186-194.
17. Chander PN, Gealekman O, Brodsky SV, Elitok S, Tojo A, Crabtree M, Gross SS, Goligorsky MS. Nephropathy in Zucker diabetic fat rat is associated with oxidative and nitrosative stress: prevention by chronic therapy with a peroxynitrite scavenger ebselen. J Am Soc Nephrol 2004. 15(9):2391-2403.
18. Kakimoto M, Inoguchi T, Sonta T, Yu HY, Imamura M, Etoh T, Hashimoto T, Nawata H. Accumulation of 8-hydroxy-2'-deoxyguanosine and mitochondrial DNA deletion in kidney of diabetic rats. Diabetes 2002. 51(5):1588-1595.
19. Ha H, Lee HB. Reactive oxygen species amplify glucose signalling in renal cells cultured under high glucose and in diabetic kidney. Nephrology (Carlton) 2005. 10(Suppl):S7-S10.
20. Lee HB, Yu MR, Yang Y, Jiang Z, Ha H. Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J Am Soc Nephrol 2003. 14(8 Suppl 3):S241-S245.
21. Chew P, Yuen DY, Stefanovic N, Pete J, Coughlan MT, Jandeleit-Dahm KA, Thomas MC, Rosenfeldt F, Cooper ME, de Haan JB. Antiatherosclerotic and renoprotective effects of ebselen in the diabetic apolipoprotein E/GPx1-double knockout mouse. Diabetes 2010. 59(12):3198-3207.
22. Xiao H, Li Y, Qi J, Wang H, Liu K. Peroxynitrite plays a key role in glomerular lesions in diabetic rats. J Nephrol 2009. 22(6):800-808.
23. Gorin Y, Block K, Hernandez J, Bhandari B, Wagner B, Barnes JL, Abboud HE. Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem 2005. 280(47):39616-39626.
24. Kanauchi M, Nishioka H, Hashimoto T. Oxidative DNA damage and tubulointerstitial injury in diabetic nephropathy. Nephron 2002. 91(2):327-329.
25. Hinokio Y, Suzuki S, Hirai M, Suzuki C, Suzuki M, Toyota T. Urinary excretion of 8-oxo-7, 8-dihydro-2'-deoxyguanosine as a predictor of the development of diabetic nephropathy. Diabetologia 2002. 45(6):877-882.
26. Evans JL, Goldfine ID, Maddux BA, Grodsky GM. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 2002. 23(5):599-622.
27. Studer RK, Craven PA, DeRubertis FR. Antioxidant inhibition of protein kinase C-signaled increases in transforming growth factor-beta in mesangial cells. Metabolism 1997. 46(8):918-925.
28. Ha H, Lee HB. Reactive oxygen species as glucose signaling molecules in mesangial cells cultured under high glucose. Kidney Int Suppl 2000. 77:S19-S25.
29. Border WA, Noble NA. TGF-beta in kidney fibrosis: a target for gene therapy. Kidney Int 1997. 51(5):1388-1396.
30. Yamamoto T, Noble NA, Miller DE, Border WA. Sustained expression of TGF-beta 1 underlies development of progressive kidney fibrosis. Kidney Int 1994. 45(3):916-927.
31. Ha H, Yu MR, Choi YJ, Kitamura M, Lee HB. Role of high glucose-induced nuclear factor-kappaB activation in monocyte chemoattractant protein-1 expression by mesangial cells. J Am Soc Nephrol 2002. 13(4):894-902.
32. Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh ST, Lee HB. Role of reactive oxygen species in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J Am Soc Nephrol 2005. 16(3):667-675.
33. Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 2008. 57(6):1446-1454.
34. Higgins GC, Coughlan MT. Mitochondrial dysfunction and mitophagy: the beginning and end to diabetic nephropathy? Br J Pharmacol 2014. 171(8):1917-1942.
35. Dorn GW. Molecular mechanisms that differentiate apoptosis from programmed necrosis. Toxicol Pathol 2013. 41(2):227-234.
36. Kyte J. Immunoferritin determination of the distribution of (Na+ + K+) ATPase over the plasma membranes of renal convoluted tubules. II. Proximal segment. J Cell Biol 1976. 68(2):304-318.
37. Kyte J. Immunoferritin determination of the distribution of (Na+ + K+) ATPase over the plasma membranes of renal convoluted tubules. I. Distal segment. J Cell Biol 1976. 68(2):287-303.
38. Agus ZS, Chiu PJ, Goldberg M. Regulation of urinary calcium excretion in the rat. Am J Physiol 1977. 232(6):F545-549.
39. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 2003. 278(38):36027-36031.
40. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 2002. 277(47):44784-44790.
41. Forbes JM, Ke BX, Nguyen TV, Henstridge DC, Penfold SA, Laskowski A, Sourris KC, Groschner LN, Cooper ME, Thorburn DR, Coughlan MT. Deficiency in mitochondrial complex I activity due to Ndufs6 gene trap insertion induces renal disease. Antioxid Redox Signal 2013. 19(4):331-343.
42. Maessen DE, Stehouwer CD, Schalkwijk CG. The role of methylglyoxal and the glyoxalase system in diabetes and other age-related diseases. Clin Sci (Lond) 2015. 128(12):839-861.
43. Gugliucci A, Menini T. The axis AGE-RAGE-soluble RAGE and oxidative stress in chronic kidney disease. Adv Exp Med Biol 2014. 824:191-208.
44. Coughlan MT, Thorburn DR, Penfold SA, Laskowski A, Harcourt BE, Sourris KC, Tan AL, Fukami K, Thallas-Bonke V, Nawroth PP, et al. RAGE-induced cytosolic ROS promote mitochondrial superoxide generation in diabetes. J Am Soc Nephrol 2009. 20(4):742-752.
45. Rosca MG, Mustata TG, Kinter MT, Ozdemir AM, Kern TS, Szweda LI, Brownlee M, Monnier VM, Weiss MF. Glycation of mitochondrial proteins from diabetic rat kidney is associated with excess superoxide formation. Am J Physiol Renal Physiol 2005. 289(2):F420-F430.
46. Kim KM, Kim YS, Jung DH, Lee J, Kim JS. Increased glyoxalase I levels inhibit accumulation of oxidative stress and an advanced glycation end product in mouse mesangial cells cultured in high glucose. Exp Cell Res 2012. 318(2):152-159.
47. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001. 414(6865):813-820.
48. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000. 404(6779):787-790.
49. Kiritoshi S, Nishikawa T, Sonoda K, Kukidome D, Senokuchi T, Matsuo T, Matsumura T, Tokunaga H, Brownlee M, Araki E. Reactive oxygen species from mitochondria induce cyclooxygenase-2 gene expression in human mesangial cells: potential role in diabetic nephropathy. Diabetes 2003. 52(10):2570-2577.
50. Zhan M, Usman IM, Sun L, Kanwar YS. Disruption of renal tubular mitochondrial quality control by Myo-inositol oxygenase in diabetic kidney disease. J Am Soc Nephrol 2015. 26(6):1304-1321.
51. Bock F, Shahzad K, Wang H, Stoyanov S, Wolter J, Dong W, Pelicci PG, Kashif M, Ranjan S, Schmidt S, et al. Activated protein C ameliorates diabetic nephropathy by epigenetically inhibiting the redox enzyme p66Shc. Proc Natl Acad Sci U S A 2013. 110(2):648-653.
52. Block K, Gorin Y, Abboud HE. Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci U S A 2009. 106(34):14385-14390.
53. Drummond GR, Selemidis S, Griendling KK, Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov 2011. 10(6):453-471.
54. Dikalov SI, Dikalova AE, Bikineyeva AT, Schmidt HH, Harrison DG, Griendling KK. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic Biol Med 2008. 45(9):1340-1351.
55. Jo SH, Son MK, Koh HJ, Lee SM, Song IH, Kim YO, Lee YS, Jeong KS, Kim WB, Park JW, et al. Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J Biol Chem 2001. 276(19):16168-16176.
56. You YH, Quach T, Saito R, Pham J, Sharma K. Metabolomics reveals a key role for fumarate in mediating the effects of NADPH oxidase 4 in diabetic kidney disease. J Am Soc Nephrol 2015. In press.
57. Coughlan MT, Thallas-Bonke V, Pete J, Long DM, Gasser A, Tong DC, Arnstein M, Thorpe SR, Cooper ME, Forbes JM. Combination therapy with the advanced glycation end product cross-link breaker, alagebrium, and angiotensin converting enzyme inhibitors in diabetes: synergy or redundancy? Endocrinology 2007. 148(2):886-895.
58. Winiarska K, Focht D, Sierakowski B, Lewandowski K, Orlowska M, Usarek M. NADPH oxidase inhibitor, apocynin, improves renal glutathione status in Zucker diabetic fatty rats: a comparison with melatonin. Chem Biol Interact 2014. 218:12-19.
59. Weisiger RA, Fridovich I. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 1973. 248(13):4793-4796.
60. Das R, Xu S, Quan X, Nguyen TT, Kong ID, Chung CH, Lee EY, Cha SK, Park KS. Upregulation of mitochondrial Nox4 mediates TGF-beta-induced apoptosis in cultured mouse podocytes. Am J Physiol Renal Physiol 2014. 306(2):F155-F167.
61. Habib SL. Diabetes and renal tubular cell apoptosis. World J Diabetes 2013. 4(2):27-30.
62. Towler DA. Mitochondrial ROS deficiency and diabetic complications: AMP(K)-lifying the adaptation to hyperglycemia. J Clin Invest 2013. 123(11):4573-4576.
63. Dugan LL, You YH, Ali SS, Diamond-Stanic M, Miyamoto S, DeCleves AE, Andreyev A, Quach T, Ly S, Shekhtman G, et al. AMPK dysregulation promotes diabetes-related reduction of superoxide and mitochondrial function. J Clin Invest 2013. 123(11):4888-4899.
64. Nishikawa T, Brownlee M, Araki E. Mitochondrial reactive oxygen species in the pathogenesis of early diabetic nephropathy. J Diabetes Invest 2015. 6(2):137-139.
65. Saul RL, Ames BN. Background levels of DNA damage in the population. Basic Life Sci 1986. 38:529-535.
66. Ames BN, Shigenaga MK. Oxidants are a major contributor to aging. Ann N Y Acad Sci 1992. 663:85-96.
67. Dizdaroglu M. Base-excision repair of oxidative DNA damage by DNA glycosylases. Mutat Res 2005. 591(1-2):45-59.
68. Feldenberg LR, Thevananther S, del Rio M, de Leon M, Devarajan P. Partial ATP depletion induces Fas- and caspase-mediated apoptosis in MDCK cells. Am J Physiol 1999. 276(6 Pt 2):F837-F846.
69. Eguchi Y, Srinivasan A, Tomaselli KJ, Shimizu S, Tsujimoto Y. ATP-dependent Steps in Apoptotic Signal Transduction. Cancer Res 1999. 59(9):2174-2181.
70. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 1997. 185(8):1481-1486.
71. Koh DW, Dawson TM, Dawson VL. Mediation of cell death by poly(ADP-ribose) polymerase-1. Pharmacol Res 2005. 52(1):5-6
72. Hassa PO. The molecular "Jekyll and Hyde" duality of PARP1 in cell death and cell survival. Front Biosci (Landmark Ed) 2009. 14:72-111.
73. Laval J. Role of DNA repair enzymes in the cellular resistance to oxidative stress. Pathol Biol (Paris) 1996. 44(1):14-24.
74. Hong SJ, Dawson TM, Dawson VL. Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol Sci 2004. 25(5):259-264.
75. Susztak K, Raff AC, Schiffer M, Bottinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 2006. 55(1):225-233.
76. Prakash A, Doublie S. Base Excision Repair in the Mitochondria. J Cell Biochem 2015.
77. Bohr VA, Stevnsner T, de Souza-Pinto NC. Mitochondrial DNA repair of oxidative damage in mammalian cells. Gene 2002. 286(1):127-134.
78. Campalans A, Moritz E, Kortulewski T, Biard D, Epe B, Radicella JP. Interaction with OGG1 is required for efficient recruitment of XRCC1 to base excision repair and maintenance of genetic stability after exposure to oxidative stress. Mol Cell Biol 2015. 35(9):1648-1658.
79. Nakabeppu Y, Tsuchimoto D, Ichinoe A, Ohno M, Ide Y, Hirano S, Yoshimura D, Tominaga Y, Furuichi M, Sakumi K. Biological significance of the defense mechanisms against oxidative damage in nucleic acids caused by reactive oxygen species: from mitochondria to nuclei. Ann N Y Acad Sci 2004. 1011:101-111.
80. Wu LL, Chiou CC, Chang PY, Wu JT. Urinary 8-OHdG: a marker of oxidative stress to DNA and a risk factor for cancer, atherosclerosis and diabetics. Clin Chim Acta 2004. 339(1-2):1-9.
81. Giovannini C, Piaggi S, Federico G, Scarpato R. High levels of gamma-H2AX foci and cell membrane oxidation in adolescents with type 1 diabetes. Mutat Res 2014. 770:128-135.
82. Prasad M, Bronson SC, Warrier T, Badarinath A, Rai S, Baid K, Sitaraman S, George A, Moses A, Saraswathy R, et al. Evaluation of DNA damage in Type 2 diabetes mellitus patients with and without peripheral neuropathy: A study in South Indian population. J Nat Sci Biol Med 2015. 6(1):80-84.
83. Cinkilic N, Kiyici S, Celikler S, Vatan O, Oz Gul O, Tuncel E, Bilaloglu R. Evaluation of chromosome aberrations, sister chromatid exchange and micronuclei in patients with type-1 diabetes mellitus. Mutat Res 2009. 676(1-2):1-4.
84. Gelaleti RB, Damasceno DC, Lima PH, Salvadori DM, Calderon Ide M, Peracoli JC, Rudge MV. Oxidative DNA damage in diabetic and mild gestational hyperglycemic pregnant women. Diabetol Metab Syndr 2015. 7:1.
85. Gelaleti RB, Damasceno DC, Salvadori DM, Marcondes JP, Lima PH, Morceli G, Calderon IM, Rudge MV. IRS-1 gene polymorphism and DNA damage in pregnant women with diabetes or mild gestational hyperglycemia. Diabetol Metab Syndr 2015. 7:30.
86. Simone S, Gorin Y, Velagapudi C, Abboud HE, Habib SL. Mechanism of Oxidative DNA Damage in Diabetes: Tuberin Inactivation and Downregulation of DNA Repair Enzyme 8-Oxo-7,8-Dihydro-2'-Deoxyguanosine-DNA Glycosylase. Diabetes 2008. 57(10):2626-2636.
87. Xu GW, Yao QH, Weng QF, Su BL, Zhang X, Xiong JH. Study of urinary 8-hydroxydeoxyguanosine as a biomarker of oxidative DNA damage in diabetic nephropathy patients. J Pharm Biomed Anal 2004. 36(1):101-104.
88. Dong QY, Cui Y, Chen L, Song J, Sun L. Urinary 8-hydroxydeoxyguanosine levels in diabetic retinopathy patients. Eur J Ophthalmol 2008. 18(1):94-98.
89. Valavanidis A, Vlachogianni T, Fiotakis C. 8-hydroxy-2' -deoxyguanosine (8-OHdG): A critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2009. 27(2):120-139.
90. Orhan H, van Holland B, Krab B, Moeken J, Vermeulen NP, Hollander P, Meerman JH. Evaluation of a multi-parameter biomarker set for oxidative damage in man: increased.urinary excretion of lipid, protein and DNA oxidation products after one hour of exercise. Free Radic Res 2004. 38(12):1269-1279.
91. Lai CH, Liou SH, Lin HC, Shih TS, Tsai PJ, Chen JS, Yang T, Jaakkola JJ, Strickland PT. Exposure to traffic exhausts and oxidative DNA damage. Occup Environ Med 2005. 62(4):216-222.
92. Bohr VA, Dianov GL. Oxidative DNA damage processing in nuclear and mitochondrial DNA. Biochimie 1999. 81(1-2):155-160.
93. Yakes FM, Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 1997. 94(2):514-519.
94. Gao Y, Katyal S, Lee Y, Zhao J, Rehg JE, Russell HR, McKinnon PJ. DNA ligase III is critical for mtDNA integrity but not Xrcc1-mediated nuclear DNA repair. Nature 2011. 471(7337):240-244.
95. de Souza-Pinto NC, Wilson Iii DM, Stevnsner TV, Bohr VA. Mitochondrial DNA, base excision repair and neurodegeneration. DNA Repair 2008. 7(7):1098-1109.
96. Suematsu N, Tsutsui H, Wen J, Kang D, Ikeuchi M, Ide T, Hayashidani S, Shiomi T, Kubota T, Hamasaki N, Takeshita A. Oxidative stress mediates tumor necrosis factor-alpha-induced mitochondrial DNA damage and dysfunction in cardiac myocytes. Circulation 2003. 107(10):1418-1423.
97. Madsen-Bouterse SA, Mohammad G, Kanwar M, Kowluru RA. Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with its progression. Antioxid Redox Signal 2010. 13(6):797-805.
98. Czajkaa AS, Gnudib L, Parsadea CK, Jonesa P, Reidc F, Malika AN. Altered mitochondrial function, mitochondrial DNA and reduced metabolic flexibility in patients with diabetic nephropathy. EBioMedicine 2015. 2(6):499-512.
99. Merecz A, Markiewicz L, Sliwinska A, Kosmalski M, Kasznicki J, Drzewoski J, Majsterek I. Analysis of oxidative DNA damage and its repair in Polish patients with diabetes mellitus type 2: Role in pathogenesis of diabetic neuropathy. Adv Med Sci 2015. 60(2):220-230.
100. Kasznicki J, Kosmalski M, Sliwinska A, Mrowicka M, Stanczyk M, Majsterek I, Drzewoski J. Evaluation of oxidative stress markers in pathogenesis of diabetic neuropathy. Mol Biol Rep 2012. 39(9):8669-8678.
101. Lu J, Li X, Zhang M, Chen Z, Wang Y, Zeng C, Liu Z, Chen H. Regulation of MUTYH, a DNA repair enzyme, in renal proximal tubular epithelial cells. Oxid Med Cell Longev 2014. In press.
102. Cai Z, Chen H, Tao J, Guo W, Liu X, Zheng B, Sun W, Wang Y. Association of Base Excision Repair Gene Polymorphisms with ESRD Risk in a Chinese Population. Oxid Med Cell Longev 2012. 2012:10.
103. Cai Z, Guo W, Chen H, Tao J, Cao L, Sun W, Wang Y. Base excision repair gene polymorphisms are associated with inflammation in patients undergoing chronic hemodialysis. Biochem Biophys Res Commun 2012. 424(3):611-615.
104. Bernstein C, Bernstein H, Payne CM, Garewal H. DNA repair/pro-apoptotic dual-role proteins in five major DNA repair pathways: fail-safe protection against carcinogenesis. Mutat Res 2002. 511(2):145-178.
105. Ashkenazi A, Dixit VM. Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 1999. 11(2):255-260.
106. Eguchi Y, Shimizu S, Tsujimoto Y. Intracellular ATP Levels Determine Cell Death Fate by Apoptosis or Necrosis. Cancer Res 1997. 57(10):1835-1840.
107. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 2007. 9(12):2277-2293.
108. Herman-Edelstein M, Thomas MC, Thallas-Bonke V, Saleem M, Cooper ME, Kantharidis P. Dedifferentiation of immortalized human podocytes in response to transforming growth Factor-beta: a model for diabetic podocytopathy. Diabetes 2011. 60(6):1779-1788.
109. Sanchez-Nino MD, Sanz AB, Lorz C, Gnirke A, Rastaldi MP, Nair V, Egido J, Ruiz-Ortega M, Kretzler M, Ortiz A. BASP1 promotes apoptosis in diabetic nephropathy. J Am Soc Nephrol 2010. 21(4):610-621.
110. Kumar D, Robertson S, Burns KD. Evidence of apoptosis in human diabetic kidney. Mol Cell Biochem 2004. 259(1-2):67-70.
111. Kumar D, Zimpelmann J, Robertson S, Burns KD. Tubular and interstitial cell apoptosis in the streptozotocin-diabetic rat kidney. Nephron Exp Nephrol 2004. 96(3):E77-E88.
112. Susztak K, Ciccone E, McCue P, Sharma K, Böttinger EP. Multiple metabolic hits converge on CD36 as novel mediator of tubular epithelial apoptosis in diabetic nephropathy. Plos Med 2005. 2(2):e45.
113. Lorz C, Benito-Martín A, Boucherot A, Ucero AC, Rastaldi MP, Henger A, Armelloni S, Santamaría B, Berthier CC, Kretzler M, et al. The death ligand TRAIL in diabetic nephropathy. J Am Soc Nephrol 2008. 19(5):904-914.
114. Sanchez-Nino MD, Benito-Martin A, Ortiz A. New paradigms in cell death in human diabetic nephropathy. Kidney Int 2010. 78(8):737-744.
115. Chang YH, Lin KD, He SR, Hsieh MC, Hsiao JY, Shin SJ. Serum osteoprotegerin and tumor necrosis factor related apoptosis inducing-ligand (TRAIL) are elevated in type 2 diabetic patients with albuminuria and serum osteoprotegerin is independently associated with the severity of diabetic nephropathy. Metabolism 2011. 60(8):1064-1069.
116. Verzola D, Gandolfo MT, Ferrario F, Rastaldi MP, Villaggio B, Gianiorio F, Giannoni M, Rimoldi L, Lauria F, Miji M, et al. Apoptosis in the kidneys of patients with type II diabetic nephropathy. Kidney Int 2007. 72(10):1262-1272.
117. Baba K, Minatoguchi S, Sano H, Kagawa T, Murata I, Takemura G, Hirano T, Ohashi H, Takemura M, Fujiwara T, Fujiwara H. Involvement of apoptosis in patients with diabetic nephropathy: A study on plasma soluble Fas levels and pathological findings. Nephrology (Carlton) 2004. 9(2):94-99.
118. Kelly DJ, Stein-Oakley A, Zhang Y, Wassef L, Maguire J, Koji T, Thomson N, Wilkinson-Berka JL, Gilbert RE. Fas-induced apoptosis is a feature of progressive diabetic nephropathy in transgenic (mRen-2)27 rats: attenuation with renin-angiotensin blockade. Nephrology (Carlton) 2004. 9(1):7-13.
119. Justo P, Sanz AB, Lorz C, Egido J, Ortiz A. Lethal activity of FADD death domain in renal tubular epithelial cells. Kidney Int 2006. 69(12):2205-2211.
120. Erkan E, De Leon M, Devarajan P. Albumin overload induces apoptosis in LLC-PK(1) cells. Am J Physiol Renal Physiol 2001. 280(6):F1107-F1114.
121. Cipollone F, Chiarelli F, Iezzi A, Fazia ML, Cuccurullo C, Pini B, De Cesare D, Torello M, Tumini S, Cuccurullo F, Mezzetti A. Relationship between reduced BCL-2 expression in circulating mononuclear cells and early nephropathy in type 1 diabetes. Int J Immunopathol Pharmacol 2005. 18(4):625-635.
122. Ortiz A, Ziyadeh FN, Neilson EG. Expression of apoptosis-regulatory genes in renal proximal tubular epithelial cells exposed to high ambient glucose and in diabetic kidneys. J Investig Medi 1997. 45(2):50-56.
123. Liu F, Brezniceanu ML, Wei CC, Chenier I, Sachetelli S, Zhang SL, Filep JG, Ingelfinger JR, Chan JS. Overexpression of angiotensinogen increases tubular apoptosis in diabetes. J Am Soc Nephrol 2008. 19(2):269-280.
124. Qiu LQ, Sinniah R, I-Hong Hsu S. Downregulation of Bcl-2 by podocytes is associated with progressive glomerular injury and clinical indices of poor renal prognosis in human IgA nephropathy. J Am Soc Nephrol 2004. 15(1):79-90.
125. Goumenos DS, Tsamandas AC, Kalliakmani P, Tsakas S, Sotsiou F, Bonikos DS, Vlachojannis JG. Expression of apoptosis-related proteins bcl-2 and bax along with transforming growthfactor (TGF-beta1) in the kidney of patients with glomerulonephritides. Ren Fail 2004. 26(4):361-367.
126. Lau GJ, Godin N, Maachi H, Lo CS, Wu SJ, Zhu JX, Brezniceanu ML, Chenier I, Fragasso-Marquis J, Lattouf JB, et al. Bcl-2-modifying factor induces renal proximal tubular cell apoptosis in diabetic mice. Diabetes 2012. 61(2):474-484.
127. Gerecova G, Kopanicova J, Jaka P, Behalova L, Juhasova B, Bhatia-Kissova I, Forte M, Polcic P, Mentel M. BH3-only proteins Noxa, Bik, Bmf, and Bid activate Bax and Bak indirectly when studied in yeast model. FEMS Yeast Res 2013. 13(8):747-754.
128. Rane MJ, Song Y, Jin S, Barati MT, Wu R, Kausar H, Tan Y, Wang Y, Zhou G, Klein JB, et al. Interplay between Akt and p38 MAPK pathways in the regulation of renal tubular cell apoptosis associated with diabetic nephropathy. Am J Physiol Renal Physiol 2010. 298(1):F49-F61.
129. Wagener FA, Dekker D, Berden JH, Scharstuhl A, van der Vlag J. The role of reactive oxygen species in apoptosis of the diabetic kidney. Apoptosis 2009. 14(12):1451-1458.
130. Song P, Yang S, Xiao L, Xu X, Tang C, Yang Y, Ma M, Zhu J, Liu F, Sun L. PKCdelta promotes high glucose induced renal tubular oxidative damage via regulating activation and translocation of p66Shc. Oxid Med Cell Longev 2014. 2014:746531.
131. Sun L, Xiao L, Nie J, Liu FY, Ling GH, Zhu XJ, Tang WB, Chen WC, Xia YC, Zhan M, et al. p66Shc mediates high-glucose and angiotensin II-induced oxidative stress renal tubular injury via mitochondrial-dependent apoptotic pathway. Am J Physiol Renal Physiol 2010. 299(5):F1014-1025.
132. Verzola D, Ratto E, Villaggio B, Parodi EL, Pontremoli R, Garibotto G, Viazzi F. Uric acid promotes apoptosis in human proximal tubule cells by oxidative stress and the activation of NADPH oxidase NOX 4. Plos One 2014. 9(12):e115210.
133. Susnow N, Zeng L, Margineantu D, Hockenbery DM. Bcl-2 family proteins as regulators of oxidative stress. Semin Cancer Biol 2009. 19(1):42-49.
134. D'Alessio M, De Nicola M, Coppola S, Gualandi G, Pugliese L, Cerella C, Cristofanon S, Civitareale P, Ciriolo MR, Bergamaschi A, et al. Oxidative Bax dimerization promotes its translocation to mitochondria independently of apoptosis. Faseb j 2005. 19(11):1504-1506.
135. Karch J, Molkentin JD. Regulated necrotic cell death: the passive aggressive side of Bax and Bak. Circ Res 2015. 116(11):1800-1809.
136. Whelan RS, Konstantinidis K, Wei AC, Chen Y, Reyna DE, Jha S, Yang Y, Calvert JW, Lindsten T, Thompson CB, et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci U S A 2012. 109(17):6566-6571.
137. Dewson G, Kluck RM. Mechanisms by which Bak and Bax permeabilise mitochondria during apoptosis. J Cell Sci 2009. 122(16):2801-2808.
138. Lin SH, Perera MN, Nguyen T, Datskovskiy D, Miles M, Colombini M. Bax forms two types of channels, one of which is voltage-gated. Biophys J 2011. 101(9):2163-2169.
139. Chen Y, Gui D, Chen J, He D, Luo Y, Wang N. Down-regulation of PERK-ATF4-CHOP pathway by Astragaloside IV is associated with the inhibition of endoplasmic reticulum stress-induced podocyte apoptosis in diabetic rats. Cell Physiol Biochem 2014. 33(6):1975-1987.
140. Baban B, Liu JY, Mozaffari MS. Endoplasmic reticulum stress response and inflammatory cytokines in type 2 diabetic nephropathy: Role of indoleamine 2,3-dioxygenase and programmed death-1. Exp Mol Pathol 2013. 94(2):343-351.
141. Brosius FC, Kaufman RJ. Is the ER stressed out in diabetic kidney disease? J Am Soc Nephrol 2008. 19(11):2040-2042.
142. Forbes JM, Coughlan MT, Cooper ME. Oxidative stress as a major culprit in kidney disease in diabetes. Diabetes 2008. 57(6):1446-1454.
143. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 Regulates a Subset of Endoplasmic Reticulum Resident Chaperone Genes in the Unfolded Protein Response. Mol Cell Biol 2003. 23(21):7448-7459.
144. Chen Y, Brandizzi F. IRE1: ER stress sensor and cell fate executor. Trends Cell Biol 2013. 23(11):547-555.
145. Fonseca SG, Gromada J, Urano F. Endoplasmic reticulum stress and pancreatic beta-cell death. Trends Endocrinol Metab 2011. 22(7):266-274.
146. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, Biden TJ. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 2007. 50(4):752-763.
147. Lindenmeyer MT, Rastaldi MP, Ikehata M, Neusser MA, Kretzler M, Cohen CD, Schlöndorff D. Proteinuria and hyperglycemia induce endoplasmic reticulum stress. J Am Soc Nephrol 2008. 19(11):2225-2236.
148. Zhuang A, Forbes JM. Stress in the kidney is the road to pERdition: is endoplasmic reticulum stress a pathogenic mediator of diabetic nephropathy? J Endocrinol 2014. 222(3):R97-111.
149. Inagi R. Endoplasmic reticulum stress as a progression factor for kidney injury. Curr Opin Pharmacol 2010. 10(2):156-165.
150. Brezniceanu ML, Lau CJ, Godin N, Chenier I, Duclos A, Ethier J, Filep JG, Ingelfinger JR, Zhang SL, Chan JS. Reactive oxygen species promote caspase-12 expression and tubular apoptosis in diabetic nephropathy. J Am Soc Nephrol 2010. 21(6):943-954.
151. Cheema MU, Damkier HH, Nielsen J, Poulsen ET, Enghild JJ, Fenton RA, Praetorius J. Distal renal tubules are deficient in aggresome formation and autophagy upon aldosterone administration. Plos One 2014. 9(7):e101258.
152. Feissner RF, Skalska J, Gaum WE, Sheu SS. Crosstalk signaling between mitochondrial Ca(2+) and ROS. Front Biosci (Landmark Ed) 2009. 14:1197-1218.
153. Grimm S. The ER–mitochondria interface: The social network of cell death. Biochim Biophys Acta 2012. 1823(2):327-334.
154. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004. 287(4):C817-C833.
155. Pospisilik JA, Knauf C, Joza N, Benit P, Orthofer M, Cani PD, Ebersberger I, Nakashima T, Sarao R, Neely G, et al. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 2007. 131(3):476-491.
156. Sano R, Reed JC. ER stress-induced cell death mechanisms. Biochim Biophys Acta 2013. 1833(12):3460-3470.
157. Wang X, Olberding KE, White C, Li C. Bcl-2 proteins regulate ER membrane permeability to luminal proteins during ER stress-induced apoptosis. Cell Death Differ 2011. 18(1):38-47.
158. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J, Thompson CB. Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol 2003. 162(1):59-69.
159. Kennedy D, Mnich K, Samali A. Heat shock preconditioning protects against ER stress-induced apoptosis through the regulation of the BH3-only protein BIM. FEBS Open Bio 2014. 4:813-821.
160. Morishima N, Nakanishi K, Tsuchiya K, Shibata T, Seiwa E. Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J Biol Chem 2004. 279(48):50375-50381.
161. Lin ML, Chen SS, Huang RY, Lu YC, Liao YR, Reddy MV, Lee CC, Wu TS. Suppression of PI3K/Akt signaling by synthetic bichalcone analog TSWU-CD4 induces ER stress- and Bax/Bak-mediated apoptosis of cancer cells. Apoptosis 2014. 19(11):1637-1653.
162. Matsuzaki S, Hiratsuka T, Kuwahara R, Katayama T, Tohyama M. Caspase-4 is partially cleaved by calpain via the impairment of Ca2+ homeostasis under the ER stress. Neurochem Int 2010. 56(2):352-356.
163. Sansanwal P, Kambham N, Sarwal MM. Caspase-4 may play a role in loss of proximal tubules and renal injury in nephropathic cystinosis. Pediatr Nephrol 2010. 25(1):105-109.
164. Sanchez-Nino MD, Sanz AB, Ortiz A. Caspase-12 and Diabetic Nephropathy: From Mice to Men? J Am Soc Nephrol 2010. 21(6):886-888.
165. Deegan S, Saveljeva S, Logue SE, Pakos-Zebrucka K, Gupta S, Vandenabeele P, Bertrand MJ, Samali A. Deficiency in the mitochondrial apoptotic pathway reveals the toxic potential of autophagy under ER stress conditions. Autophagy 2014. 10(11):1921-1936.
166. Ueda M, Li S, Itoh M, Hayakawa-Yano Y, Wang MX, Hayakawa M, Hasebe-Matsubara R, Ohta K, Ohta E, Mizuno A, et al. Polyglutamine expansion disturbs the endoplasmic reticulum formation, leading to caspase-7 activation through Bax. Biochem Biophys Res Commun 2014. 443(4):1232-1238.
167. Gill MB, Bockhorst K, Narayana P, Perez-Polo JR. Bax shuttling after neonatal hypoxia-ischemia: hyperoxia effects. J Neurosci Res 2008. 86(16):3584-3604.
168. Bonneau B, Prudent J, Popgeorgiev N, Gillet G. Non-apoptotic roles of Bcl-2 family: the calcium connection. Biochim Biophys Acta 2013. 1833(7):1755-1765.
169. Small DM, Bennett NC, Roy S, Gabrielli BG, Johnson DW, Gobe GC. Oxidative stress and cell senescence combine to cause maximal renal tubular epithelial cell dysfunction and loss in an in vitro model of kidney disease. Nephron Exp Nephrol 2012. 122(3-4):123-130.
170. Frippiat C, Chen QM, Zdanov S, Magalhaes J-P, Remacle J, Toussaint O. Subcytotoxic H2O2 stress triggers a release of transforming growth factor-beta1, which induces biomarkers of cellular senescence of human diploid fibroblasts. J Biol Chem 2001. 276(4):2531-2537.
171. de Haan JB, Bladier C, Lotfi-Miri M, Taylor J, Hutchinson P, Crack PJ, Hertzog P, Kola I. Fibroblasts derived from Gpx1 knockout mice display senescent-like features and are susceptible to H2O2-mediated cell death. Free Radic Biol Med 2004. 36(1):53-64.
172. Zhu K, Kakehi T, Matsumoto M, Iwata K, Ibi M, Ohshima Y, Zhang J, Liu J, Wen X, Taye A, et al. NADPH oxidase NOX1 is involved in activation of protein kinase C and premature senescence in early stage diabetic kidney. Free Radic Biol Med 2015. 83:21-30.
173. Verzola D, Gandolfo MT, Gaetani G, Ferraris A, Mangerini R, Ferrario F, Villaggio B, Gianiorio F, Tosetti F, Weiss U, et al. Accelerated senescence in the kidneys of patients with type 2 diabetic nephropathy. Am J Physiol Renal Physiol 2008. 295(5):F1563-1573.
174. Lee HC, Yin PH, Lu CY, Chi CW, Wei YH. Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells. Biochem J 2000. 348(Pt 2):425-432.
175. Malik AN, Shahni R, Iqbal MM. Increased peripheral blood mitochondrial DNA in type 2 diabetic patients with nephropathy. Diabetes Res Clin Pract 2009. 86(2):E22-E24.
176. Nakamura T, Ushiyama C, Suzuki S, Hara M, Shimada N, Ebihara I, Koide H. Urinary excretion of podocytes in patients with diabetic nephropathy. Nephrol Dial Transplant 2000. 15(9):1379-1383.
177. Soltoff SP. ATP and the regulation of renal cell function. Annu Rev Physiol 1986. 48:9-31.
178. Halestrap AP. What is the mitochondrial permeability transition pore? J Mol Cell Cardiol 2009. 46(6):821-831.
179. Halestrap AP, Pasdois P. The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta 2009. 1787(11):1402-1415.
180. Bernardi P. The mitochondrial permeability transition pore: a mystery solved? Front Physiol 2013. 4:95.
181. Karch J, Molkentin JD. Identifying the components of the elusive mitochondrial permeability transition pore. Proc Natl Acad Sci U S A 2014. 111(29):10396-10397.
182. Takebayashi S, Kaneda K. Mitochondrial derangement: possible initiator of microalbuminuria in NIDDM. J Diabet Complications 1991. 5(2-3):104-106.
183. Kaneda K, Iwao J, Sakata N, Takebayashi S. Correlation between mitochondrial enlargement in renal proximal tubules and microalbuminuria in rats with early streptozotocin-induced diabetes. Acta Pathol Jpn 1992. 42(12):855-860.
184. Yu T, Robotham JL, Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc Natl Acad Sci U S A 2006. 103(8):2653-2658.
185. Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta 1995. 1241(2):139-176.
186. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 1999. 341(Pt 2):233-249.
187. Halestrap AP. Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans 2006. 34(Pt 2):232-237.
188. Armstrong JS. The role of the mitochondrial permeability transition in cell death. Mitochondrion 2006. 6(5):225-234.
189. Zorov DB, Juhaszova M, Yaniv Y, Nuss HB, Wang S, Sollott SJ. Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc Res 2009. 83(2):213-225.
190. Baines CP. The molecular composition of the mitochondrial permeability transition pore. J Mol Cell Cardiol 2009. 46(6):850-857.
191. Baines CP, Kaiser RA, Sheiko T, Craigen WJ, Molkentin JD. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol 2007. 9(5):550-555.
192. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP, MacGregor GR, Wallace DC. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004. 427(6973):461-465.
193. Krauskopf A, Eriksson O, Craigen WJ, Forte MA, Bernardi P. Properties of the permeability transition in VDAC1(-/-) mitochondria. Biochim Biophys Acta 2006. 1757(5-6):590-595.
194. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci U S A 2005. 102(34):12005-12010.
195. Woodfield K, Ruck A, Brdiczka D, Halestrap AP. Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem J 1998. 336(Pt 2):287-290.
196. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005. 434(7033):658-662.
197. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T, Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005. 434(7033):652-658.
198. Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M, Glick GD, Petronilli V, Zoratti M, Szabo I, et al. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc Natl Acad Sci U S A 2013. 110(15):5887-5892.
199. Alavian KN, Beutner G, Lazrove E, Sacchetti S, Park HA, Licznerski P, Li H, Nabili P, Hockensmith K, Graham M, et al. An uncoupling channel within the c-subunit ring of the F1FO ATP synthase is the mitochondrial permeability transition pore. Proc Natl Acad Sci U S A 2014. 111(29):10580-10585.
200. Takeyama N, Miki S, Hirakawa A, Tanaka T. Role of the mitochondrial permeability transition and cytochrome C release in hydrogen peroxide-induced apoptosis. Exp Cell Res 2002. 274(1):16-24.
201. Batandier C, Leverve X, Fontaine E. Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J Biol Chem 2004. 279(17):17197-17204.
202. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, Korsmeyer SJ. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2002. 2(1):55-67.
203. Boveris A, Oshino N, Chance B. The cellular production of hydrogen peroxide. Biochem J 1972. 128(3):617-630.
204. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003. 552(Pt 2):335-344.
205. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta 2006. 1757(5-6):509-517.
206. Whelan RS, Konstantinidis K, Wei AC, Chen Y, Reyna DE, Jha S, Yang Y, Calvert JW, Lindsten T, Thompson CB, et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci U S A 2012. 109(17):6566-6571.
207. Devalaraja-Narashimha K, Diener AM, Padanilam BJ. Cyclophilin D gene ablation protects mice from ischemic renal injury. Am J Physiol Renal Physiol 2009. 297(3):F749-F759.
208. Gooch JL, Barnes JL, Garcia S, Abboud HE. Calcineurin is activated in diabetes and is required for glomerular hypertrophy and ECM accumulation. Am J Physiol Renal Physiol 2003. 284(1):F144-F154.
209. Oliveira PJ, Esteves TC, Seica R, Moreno AJ, Santos MS. Calcium-dependent mitochondrial permeability transition is augmented in the kidney of Goto-Kakizaki diabetic rat. Diabetes Metab Res Rev 2004. 20(2):131-136.
210. Smith RA, Porteous CM, Gane AM, Murphy MP. Delivery of bioactive molecules to mitochondria in vivo. Proc Natl Acad Sci U S A 2003. 100(9):5407-5412.
211. Mukhopadhyay P, Horvath B, Zsengeller Z, Zielonka J, Tanchian G, Holovac E, Kechrid M, Patel V, Stillman IE, Parikh SM, et al. Mitochondrial-targeted antioxidants represent a promising approach for prevention of cisplatin-induced nephropathy. Free Radic Biol Med 2012. 52(2):497-506.
212. Tabara LC, Poveda J, Martin-Cleary C, Selgas R, Ortiz A, Sanchez-Nino MD. Mitochondria-targeted therapies for acute kidney injury. Expert Rev Mol Med 2014. 16:e13.
213. Subramanian S, Kalyanaraman B, Migrino RQ. Mitochondrially targeted antioxidants for the treatment of cardiovascular diseases. Recent Pat Cardiovasc Drug Discov 2010. 5(1):54-65.
214. Chacko BK, Reily C, Srivastava A, Johnson MS, Ye Y, Ulasova E, Agarwal A, Zinn KR, Murphy MP, Kalyanaraman B, Darley-Usmar V. Prevention of diabetic nephropathy in Ins2(+/)(-)(AkitaJ) mice by the mitochondria-targeted therapy MitoQ. Biochem J 2010. 432(1):9-19.
215. Bolisetty S, Traylor A, Zarjou A, Johnson MS, Benavides GA, Ricart K, Boddu R, Moore RD, Landar A, Barnes S, et al. Mitochondria-targeted heme oxygenase-1 decreases oxidative stress in renal epithelial cells. Am J Physiol Renal Physiol 2013. 305(3):F255-F264.
216. Nakamura Y, Feng Q, Kumagai T, Torikai K, Ohigashi H, Osawa T, Noguchi N, Niki E, Uchida K. Ebselen, a glutathione peroxidase mimetic seleno-organic compound, as a multifunctional antioxidant. Implication for inflammation-associated carcinogenesis. J Biol Chem 2002. 277(4):2687-2694.
217. Tan SM, Sharma A, Yuen DY, Stefanovic N, Krippner G, Mugesh G, Chai Z, de Haan JB. The modified selenenyl amide, M-hydroxy ebselen, attenuates diabetic nephropathy and diabetes-associated atherosclerosis in ApoE/GPx1 double knockout mice. Plos One 2013. 8(7):e69193.
218. Filipovska A, Kelso GF, Brown SE, Beer SM, Smith RA, Murphy MP. Synthesis and characterization of a triphenylphosphonium-conjugated peroxidase mimetic. Insights into the interaction of ebselen with mitochondria. J Biol Chem 2005. 280(25):24113-24126.
219. Szeto HH, Liu S, Soong Y, Wu D, Darrah SF, Cheng FY, Zhao Z, Ganger M, Tow CY, Seshan SV. Mitochondria-targeted peptide accelerates ATP recovery and reduces ischemic kidney injury. J Am Soc Nephrol 2011. 22(6):1041-1052.
220. Chakrabarti AK, Feeney K, Abueg C, Brown DA, Czyz E, Tendera M, Janosi A, Giugliano RP, Kloner RA, Weaver WD, 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. Am Heart J 2013. 165(4):509-514.
221. Javadov S, Karmazyn M, Escobales N. Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases. J Pharmacol Exp Ther 2009. 330(3):670-678.
222. Halestrap AP, Davidson AM. Inhibition of Ca2(+)-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem J 1990. 268(1):153-160.
223. Tanveer A, Virji S, Andreeva L, Totty NF, Hsuan JJ, Ward JM, Crompton M. Involvement of cyclophilin D in the activation of a mitochondrial pore by Ca2+ and oxidant stress. Eur J Biochem 1996. 238(1):166-172.
224. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, Elbelghiti R, Cung TT, Bonnefoy E, Angoulvant D, et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008. 359(5):473-481.
225. Li C, Lim SW, Sun BK, Yang CW. Chronic cyclosporine nephrotoxicity: new insights and preventive strategies. Yonsei Med J 2004. 45(6):1004-1016.
226. Ptak RG, Gallay PA, Jochmans D, Halestrap AP, Ruegg UT, Pallansch LA, Bobardt MD, de Bethune MP, Neyts J, De Clercq E, et al. Inhibition of human immunodeficiency virus type 1 replication in human cells by Debio-025, a novel cyclophilin binding agent. Antimicrob Agents Chemother 2008. 52(4):1302-1317.
227. Tiepolo T, Angelin A, Palma E, Sabatelli P, Merlini L, Nicolosi L, Finetti F, Braghetta P, Vuagniaux G, Dumont JM, et al. The cyclophilin inhibitor Debio 025 normalizes mitochondrial function, muscle apoptosis and ultrastructural defects in Col6a1(-/-) myopathic mice. Br J Pharmacol 2009. 157(6):1045-1052.
228. Angelin A, Tiepolo T, Sabatelli P, Grumati P, Bergamin N, Golfieri C, Mattioli E, Gualandi F, Ferlini A, Merlini L, et al. Mitochondrial dysfunction in the pathogenesis of Ullrich congenital muscular dystrophy and prospective therapy with cyclosporins. Proc Natl Acad Sci U S A 2007. 104(3):991-996.
229. Tiepolo T, Angelin A, Palma E, Sabatelli P, Merlini L, Nicolosi L, Finetti F, Braghetta P, Vuagniaux G, Dumont JM, et al. The cyclophilin inhibitor Debio 025 normalizes mitochondrial function, muscle apoptosis and ultrastructural defects in Col6a1-/- myopathic mice. Br J Pharmacol 2009. 157(6):1045-1052.
230. Quarato G, D'Aprile A, Gavillet B, Vuagniaux G, Moradpour D, Capitanio N, Piccoli C. The cyclophilin inhibitor alisporivir prevents hepatitis C virus-mediated mitochondrial dysfunction. Hepatology 2012. 55(5):1333-1343.
231. Liang HL, Sedlic F, Bosnjak Z, Nilakantan V. SOD1 and MitoTEMPO partially prevent mitochondrial permeability transition pore opening, necrosis, and mitochondrial apoptosis after ATP depletion recovery. Free Radic Biol Med 2010. 49(10):1550-1560.
232. Wang Z, Bao H, Ge Y, Zhuang S, Peng A, Gong R. Pharmacological targeting of GSK3beta confers protection against podocytopathy and proteinuria by desensitizing mitochondrial permeability transition. Br J Pharmacol 2015. 172(3):895-909.
233. de Zeeuw D, Audhya P, Bakris GL, Chin M, Christ-Schmidt H, Goldsberry A, Houser M, Krauth M, Lambers Heerspink HJ, McMurray JJ, et al. Bardoxolone methyl in type 2 diabetes and stage 4 chronic kidney disease. N Engl J Med 2013. 369(26):2492-2503.
234. Tan SM, Sharma A, Stefanovic N, Yuen DY, Karagiannis TC, Meyer C, Ward KW, Cooper ME, de Haan JB. Derivative of bardoxolone methyl, dh404, in an inverse dose-dependent manner lessens diabetes-associated atherosclerosis and improves diabetic kidney disease. Diabetes 2014. 63(9):3091-3103.
235. Trujillo J, Chirino YI, Molina-Jijon E, Anderica-Romero AC, Tapia E, Pedraza-Chaverri J. Renoprotective effect of the antioxidant curcumin: Recent findings. Redox Biol 2013. 1:448-456.
236. Jiang T, Huang Z, Lin Y, Zhang Z, Fang D, Zhang DD. The protective role of Nrf2 in streptozotocin-induced diabetic nephropathy. Diabetes 2010. 59(4):850-860.
237. Xu Y, Nie L, Yin YG, Tang JL, Zhou JY, Li DD, Zhou SW. Resveratrol protects against hyperglycemia-induced oxidative damage to mitochondria by activating SIRT1 in rat mesangial cells. Toxicol Appl Pharmacol 2012. 259(3):395-401.
238. Alhaider AA, Korashy HM, Sayed-Ahmed MM, Mobark M, Kfoury H, Mansour MA. Metformin attenuates streptozotocin-induced diabetic nephropathy in rats through modulation of oxidative stress genes expression. Chem Biol Interact 2011. 192(3):233-242.
239. Pal PB, Sinha K, Sil PC. Mangiferin attenuates diabetic nephropathy by inhibiting oxidative stress mediated signaling cascade, TNFalpha related and mitochondrial dependent apoptotic pathways in streptozotocin-induced diabetic rats. Plos One 2014. 9(9):e107220.
240. Sedeek M, Gutsol A, Montezano AC, Burger D, Nguyen Dinh Cat A, Kennedy CR, Burns KD, Cooper ME, Jandeleit-Dahm K, Page P, et al. Renoprotective effects of a novel Nox1/4 inhibitor in a mouse model of Type 2 diabetes. Clin Sci (Lond) 2013. 124(3):191-202.
241. ten Freyhaus H, Huntgeburth M, Wingler K, Schnitker J, Baumer AT, Vantler M, Bekhite MM, Wartenberg M, Sauer H, Rosenkranz S. Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc Res 2006. 71(2):331-341.
242. Lv M, Chen Z, Hu G, Li Q. Therapeutic strategies of diabetic nephropathy: recent progress and future perspectives. Drug Discov Today 2015. 20(3):332-346.