Tempol, a superoxide dismutase mimetic agent, ameliorates cisplatin-induced nephrotoxicity through alleviation of mitochondrial dysfunction in mice

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Ahmed, Lamiaa A ^a   Shehata, Nagwa I ^a   Abdelkader, Noha F ^a   Khattab, Mahmoud M ^a  

^a CAIRO UNIVERSITY   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE 3; CISPLATIN; CREATININE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE DISMUTASE; TEMPOL; UBIQUINOL CYTOCHROME C REDUCTASE; UREA; AMINE OXIDE; ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; SPIN LABELING;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOSE RESPONSE; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG PENETRATION; EHRLICH ASCITES TUMOR; ENZYME ACTIVITY; GLUCOSURIA; HISTOPATHOLOGY; KIDNEY TUBULE DAMAGE; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NEPHROTOXICITY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEINURIA; RENAL PROTECTION; SINGLE DRUG DOSE; UREA BLOOD LEVEL; ANIMAL; APOPTOSIS; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; KIDNEY DISEASES; LIPID PEROXIDATION; METABOLISM; MITOCHONDRION; SPIN LABELING; TREATMENT OUTCOME;

MUS;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CISPLATIN; CREATININE; CYCLIC N-OXIDES; DISEASE MODELS, ANIMAL; KIDNEY DISEASES; LIPID PEROXIDATION; MICE; MITOCHONDRIA; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPIN LABELS; TREATMENT OUTCOME; UREA;

EID: 84907486848     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108889     Document Type: Article

References (74)

1. Langerak AD, Dreisbach L.P. (2001) Chemotherapy regimens and cancer care. Texas: Landes Bioscience; Georgetown.
2. Sahni V, Choudhury D, Ahmed Z. (2009) Chemotherapy-associated renal dysfunction. Nat Rev Nephrol 8: 450-462.
3. Yao X, Panichpisal K, Kurtzman N., Nugent K. (2007) Cisplatin nephrotoxicity: a review. Am J Med Sci 334: 115-124.
4. Pabla N, Dong Z. (2008) Cisplatin nephrotoxicity: mechanisms and renoprotective strategies. Kidney Int 73: 994-1007.
5. Kilic U, Kilic E, Tuzcu Z., Tuzcu M, Ozercan IH, et al (2013) Melatonin suppresses cisplatin-induced nephrotoxicity via activation of Nrf-2/HO-1 pathway. Nutr Metab 10: 7.
6. Masuda H, Tanaka T, Takahama U. (1994) Cisplatin generates superoxide anion by interaction with DNA in a cell-free system. Biochem Biophys Res Commun 203: 1175-1180.
7. Kuhlmann MK, Burkhardt G, Kohler H. (1997) Insights into potential cellular mechanisms of cisplatin nephrotoxicity and their clinical application. Nephrol Dial Transplant 12: 2478-2480.
8. Liu L, Yang C, Herzog C., Seth R, Kaushal G.P. (2010) Proteasome inhibitors prevent cisplatin-induced mitochondrial release of apoptosis-inducing factor and markedly ameliorate cisplatin nephrotoxicity. Biochem Pharmacol 2: 137-146.
9. Zsengellér Z.K., Ellezian L, Brown D., Horváth B, Mukhopadhyay P., et al. (2012) Cisplatin nephrotoxicity involves mitochondrial injury with impaired tubular mitochondrial enzyme activity. J Histochem Cytochem 60: 521-529.
10. Qian W, Nishikawa M, Haque A.M., Hirose M., Mashimo M, et al. (2005) Mitochondrial density determines the cellular sensitivity to cisplatin-induced cell death. Am J Physiol Cell Physiol 289: C1466-C1475.
11. Galley HF (2011) Oxidative stress and mitochondrial dysfunction in sepsis. Br J Anaesth 107: 57-64.
12. Kaushal GP, Kaushal V, Hong X., Shah S.V. (2001) Role and regulation of activation of caspases in cisplatin-induced injury to renal tubular epithelial cells. Kidney Int 60: 1726-1736.
13. Yang C, Kaushal V, Haun R.S., Seth R., Shah SV, et al. (2008) Transcriptional activation of caspase -6 and -7 genes by cisplatin-induced p53 and its functional significance in cisplatin nephrotoxicity. Cell Death Differ 15: 530-544.
14. Lieberthal W, Triaca V, Levine J. (1996) Mechanisms of death induced by cisplatin in proximal tubular epithelial cells: apoptosis vs. necrosis. Am J Physiol Renal Physiol 39: F700-F708.
15. Matsushima H, Yonemura K, Ohishi K., Hishida A. (1998) The role of oxygen free radicals in cisplatin-induced acute renal failure in rats. J Lab Clin Med 131: 518-526.
16. Okuda M, Masaki K, Fukatsu S., Hashimoto Y, Inui K. (2000) Role of apoptosis in cisplatin induced toxicity in the renal epithelial cell line LLC-PK1. Biochem Pharmacol 59: 195-201.
17. Shiraishi F, Curtis LM, Truong L, Poss K., Visner GA, et al. (2000) Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis. Am J Physiol Renal Physiol 278: F726-F736.
18. Wong GH, Elwell JH, Oberley L.W., Goeddel DV. (1989) Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 58: 923-931.
19. Eastgate J, Moreb J, Nick H.S., Suzuki K., Taniguchi N, et al. (1993) A role for manganese superoxide dismutase in radioprotection of hematopoietic stem cells by interleukin-1. Blood 81: 639-646.
20. Ho YS, Vincent R, Dey M.S., Slot JW, Crapo J.D. (1998) Transgenic models for the study of lung antioxidant defense: Enhanced manganese-containing superoxide dismutase activity gives partial protection to B6C3 hybrid mice exposed to hyperoxia. Am J Respir Cell Mol Biol 18: 538-547.
21. Shah SV, Baliga R, Rajapurkar M., Fonseca V.A. (2007) Oxidants in chronic kidney disease. J Am Soc Nephrol 18: 16-28.
22. Nassar T, Kadery B, Lotan C., Da'as N, Kleinman Y, et al. (2002) Effects of superoxide dismutase-mimetic compound tempol on endothelial dysfunction in streptozotocin induced diabetic rats. Eur J Pharmacol 436: 111-118.
23. McDonald MC, Zacharowski K, Bowes J., Cuzzocrea S, Thiemermann C. (1999) Tempol reduces infract size in rodent models of regional myocardial ischemia and reperfusion. Free Radic Biol Med 27: 493-503.
24. Metz JM, Smith D, Mick R., Lustig R, Mitchell J, et al (2004) A phase I study of topical tempol for the prevention of alopecia induced by whole brain radiotherapy. Clin Cancer Res 19: 6411-6417.
25. Kawai Y, Gemba M. (2007) Cisplatin-induced renal injury in LLC-PK1 cells. In: Proceedings of the 6th World Congress on Alternatives & Animal Use in the Life Sciences. p. 453-456.
26. Joy J, Nair C.K. (2008) Amelioration of cisplatin induced nephrotoxicity in Swiss albino mice by Rubia cordifolia extract. J Cancer Res Ther 4: 111-115.
27. Horváth B., Mukhopadhyay P, Kechrid M., Patel V, Tanchian G, et al (2012) β-Caryophyllene ameliorates cisplatin-induced nephrotoxicity in a cannabinoid 2 receptor-dependent manner. Free Radic Biol Med 52: 1325-1333.
28. Ramachandran L, Nair C.K. (2012) Radioprotection by tempol: Studies on tissue antioxidant levels, hematopoietic and gastrointestinal systems, in mice whole body exposed to sub-lethal doses of gamma radiation. Iran J Radiat Res 10: 1-10.
29. Cuzzocrea S, Pisano B, Dugo L., Ianaro A, Patel NS, et al (2004) Tempol reduces the activation of nuclear factor-kappaB in acute inflammation. Free Radic Res 38: 813-819.
30. Gao X, Zhang H, Schmidt A.M., Zhang C. (2008) AGE/RAGE produces endothelial dysfunction in coronary arterioles in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 295: H491-H498.
31. Sun MS, Hattori S, Kubo S., Awata H, Matsuda I, et al (2000) A mouse model of renal tubular injury of tyrosinemia type 1: development of de Toni Fanconi syndrome and apoptosis of renal tubular cells in Fah/Hpd double mutant mice. J Am Soc Nephrol 11: 291-300.
32. Ahmed LA, El-Maraghy SA (2013) Nicorandil ameliorates mitochondrial dysfunction in doxorubicin-induced heart failure in rats: possible mechanism of cardioprotection. Biochem Pharmacol 86: 1301-1310.
33. Lowry OH, Rosebrough NJ, Farr A.L., Randall R.J. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
34. Buege JA, Aust S.D. (1978) Microsomal lipid peroxidation. Methods Enzymol 52: 302-310.
35. Beutler E, Duron O, Kelly B.M. (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61: 882-888.
36. Marklund SL (1985) Pyrogallol autooxidation. In: Greenwald RA, editor. Handbook of Methods for Oxygen Radical Research. Florida, Boca Raton: CRC Press. p. 243-247.
37. Abei H (1984) Catalase in vitro. Methods Enzymol 105: 121-126.
38. Hinkle PC (1995) Oxygen proton and phosphate fluxes and stoichiometries. In: Brown GC, Cooper CE, editors. Bioenergetics: a practical approach. Oxford: IRL Press. p. 1-16.
39. Banerjee K, Sinha M, Pham CLL, Jana S, Chanda D., et al. (2010) Synuclein induced membrane depolarization and loss of phosphorylation capacity of isolated rat brain mitochondria: Implications in Parkinson's disease. FEBS Lett 584: 1571-1576.
40. Bagh MB, Maiti AK, Roy A, Chakrabarti S. (2008) Dietary supplementation with N-acetylcysteine, α-tocopherol and α-lipoic acid prevents age related decline in Na+, K+ ATPase activity and associated peroxidative damage in rat brain synaptosomes. Biogerontol 9: 421-428.
41. Lowry OH, Passonneau JV, Hasselberger F.X., Schulz D.W. (1964) Effect of ischemia on known substances and cofactors of the glycolytic pathways in brain. Biol Chem 239: 18-30.
42. Sharman EH, Bondy S.C. (2001) Effects of age and dietary antioxidants on cerebral electron transport chain activity. Neurobiol Aging 22: 629-634.
43. Storrie B, Madden E.A. (1990) Isolation of subcellular organelles. Methods Enzymol 182: 203-225.
44. Mukhopadhyay P, Rajesh M, Pan H., Patel V, Mukhopadhyay B, et al (2010) Cannabinoid-2 receptor limits inflammation, oxidative/nitrosative stress, and cell death in nephropathy. Free Radic Biol Med 48: 457-467.
45. Kloner RA, Fishbein MC, Braunwald E, Maroko P.R. (1978) Effect of propranolol on mitochondrial morphology during acute myocardial ischemia. Am J Cardiol 41: 880-886.
46. Osman AM, Sayed-Ahmed MM, Khayyal M.T., El-Merzabani MM (1993) Hyperthermic potentiation of cisplatin on solid Ehrlich carcinoma. Tumori 79: 268-272.
47. Dos Santos N.A., Carvalho Rodrigues MA, Martins NM, dos Santos AC (2012) Cisplatin-induced nephrotoxicity and targets of nephroprotection: an update. Arch Toxicol 86: 1233-1250.
48. Kidera Y, Kawakami H, Sakiyama T., Okamoto K, Tanaka K, et al (2014) Risk factors for cisplatin-induced nephrotoxicity and potential of magnesium supplementation for renal protection. PLoS One 9: e101902.
49. Mora Lde O., Antunes LM, Francescato H.D., Bianchi Mde L (2003) The effects of oral glutamine on cisplatin-induced nephrotoxicity in rats. Pharmacol Res 47: 517-522.
50. Ries F, Klastersky J. (1986) Nephrotoxicity induced by cancer chemotherapy with special emphasis on cisplatin toxicity. Am J Kidney Dis 8: 368-379.
51. Safirstein R, Winston J, Goldstein M., Model M, Dikman S, et al (1986) Cisplatin nephrotoxicity. Am J Kidney Dis 8: 356-367.
52. Somani SM, Husain K, Whitworth C., Trammel GL, Malafa M, et al. (2000) Dose-dependent protection by lipoic acid against cisplatin induced nephrotox-icity in rats: antioxidant defense system. Pharmacol Toxicol 86: 234-241.
53. Silva CR, Greggi Antunes LM, Bianchi M.L. (2001) Antioxidant action of bixin against cisplatin-induced chromosome aberrations and lipid peroxidation in rats. Pharmacol Res 43: 561-566.
54. Zhang L, Cooper AJ, Krasnikov B.F., Xu H., Bubber P, et al. (2006) Cisplatin-induced toxicity is associated with platinum deposition in mouse kidney mitochondria in vivo and with selective inactivation of the alpha-ketoglutarate dehydrogenase complex in LLC-PK1 cells. Biochemistry 45: 8959-8971.
55. Godwin AK, Meister A, O'Dwyer PJ, Huang CS, Hamilton T.C., et al. (1992) High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci 89: 3070-3074.
56. Anderson ME, Naganuma A, Meister A. (1990) Protection against cisplatin toxicity by administration of glutathione ester. FASEB J 4: 3251-3255.
57. Husain K, Morris C, Whitworth C., Trammel GL, Rybak LP, et al. (1996) 4-methylthiobenzoic acid protection against cisplatin nephrotoxicity: antioxidant system. Fundam Appl Toxicol 32: 278-284.
58. Marullo R, Werner E, Degtyareva N., Moore B, Altavilla G, et al (2013) Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PLoS ONE 8: e81162.
59. Zhang JG, Lindup W.E. (1994) Cisplatin nephrotoxicity: decreases in mitochon-drial protein sulphydryl concentration and calcium uptake by mitochondria from rat renal cortical slices. Biochem Pharmacol 47: 1127-1135.
60. Kruidering M, Vandewater B, Deheer E., Mulder GJ, Nagelkerke J.F. (1996) The use of porcine proximal tubular cells for studying nephrotoxicity in vitro: The role of oxidative stress in cisplatin-induced cell death. ATLA-Altern Lab Anim 24: 161-172.
61. Tanabe K, Tamura Y, Lanaspa M.A., Miyazaki M., Suzuki N, et al. (2012) Epicatechin limits renal injury by mitochondrial protection in cisplatin nephropathy. Am J Physiol Renal Physiol 303: F1264-F1274.
62. Gordon JA, Gattone V.H. (1986) Mitochondrial alterations in cisplatin induced acute renal failure. Am J Physiol Renal Physiol 250: F991-F998.
63. Tengan CH, Rodrigues GS, Godinho R.O. (2012) Nitric oxide in skeletal muscle: role on mitochondrial biogenesis and function. Int J Mol Sci 13: 17160-17184.
64. Santos NA, Bezerra CS, Martins N.M., Curti C., Bianchi ML, et al. (2008) Hydroxyl radical scavenger ameliorates cisplatin-induced nephrotoxicity by preventing oxidative stress, redox state unbalance, impairment of energetic metabolism and apoptosis in rat kidney mitochondria. Cancer Chemother Pharmacol 61: 145-155.
65. Lahoti TS, Patel D, Thekkemadom V., Beckett R, Ray S.D. (2012) Doxorubicin-induced in vivo nephrotoxicity involves oxidative stress-mediated multiple pro-and anti-apoptotic signaling pathways. Curr Neurovasc Res 9: 282-295.
66. Hassan I, Chibber S, Khan A.A., Naseem I. (2012) Riboflavin ameliorates cisplatin induced toxicities under photoillumination. PLoS ONE 7: e36273.
67. Terada Y, Inoue K, Matsumoto T., Ishihara M, Hamada K, et al (2013) 5-Aminolevulinic acid protects against cisplatin-induced nephrotoxicity without compromising the anticancer efficiency of cisplatin in rats in vitro and in vivo. PLoS ONE 8: e80850.
68. Wilcox CS, Pearlman A. (2008) Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 60: 418-469.
69. Karatas Y, Secilmis MA, Karayaylali I, Doran F., Buyukafsar K, et al. (2004) Effect of tempol (4-hydroxy tempo) on gentamicin-induced nephrotoxicity in rats. Fundam Clin Pharmacol 18: 79-83.
70. Naghibi B, Ghafghazi T, Haihashemi V., Talebi A, Taheri D. (2007) The effect of 2,3-dihydroxybenzoic acid and tempol in prevention of vancomycin-induced nephrotoxicity in rats. Toxicol 232: 192-199.
71. Samai M, Sharpe MA, Gard P.R., Chatterjee P.K. (2007) Comparison of the effects of the superoxide dismutase mimetics EUK-134 and tempol on paraquat-induced nephrotoxicity. Free Radic Biol Med 43: 528-534.
72. Alpert E, Altman H, Totary H., Gruzman A, Barnea D, et al (2004) 4-Hydroxy tempol-induced impairment of mitochondrial function and augmentation of glucose transport in vascular endothelial and smooth muscle cells. Biochem Pharmacol 67: 1985-1995.
73. Schubert R, Erker L, Barlow C., Yakushiji H, Larson D, et al (2004) Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice. Hum Mol Genet 13: 1793-1802.
74. Chatterjee PK, Cuzzocrea S, Brown P.A., Zacharowski K., Stewart KN, et al. (2000) Tempol, a membrane-permeable radical scavenger, reduces oxidant stress-mediated renal dysfunction and injury in the rat. Kidney Int 58: 658-673.