Cisplatin Nephrotoxicity Involves Mitochondrial Injury with Impaired Tubular Mitochondrial Enzyme Activity

Journal of Histochemistry and Cytochemistry

Volumn 60, Issue 7, 2012, Pages 521-529

  Zsengellér, Zsuzsanna K ^a   Ellezian, Lena ^a   Brown, Dan ^a   Horváth, Béla ^b   Mukhopadhyay, Partha ^b   Kalyanaraman, Balaraman ^c   Parikh, Samir M ^a   Karumanchi, S Ananth ^a   Stillman, Isaac E ^a   Pacher, Pál ^b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c FREE RADICAL RESEARCH CENTER   (United States)

Author keywords

cisplatin; cytochrome c oxidase; functional electron microscopy; mitochondria; nephrotoxicity

Indexed keywords

CISPLATIN; CYTOCHROME C OXIDASE; CYTOCHROME C1; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; KIDNEY CORTEX; KIDNEY MEDULLA; KIDNEY PROXIMAL TUBULE; MALE; MICROSCOPY; MITOCHONDRION SWELLING; MOUSE; NEPHROTOXICITY; NONHUMAN; PRIORITY JOURNAL; ULTRASTRUCTURE ANALYSIS AND ELECTRON MICROSCOPY; ACUTE KIDNEY FAILURE; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MITOCHONDRION; PATHOLOGY;

ACUTE KIDNEY INJURY; ANIMALS; CISPLATIN; ELECTRON TRANSPORT COMPLEX IV; IMMUNOHISTOCHEMISTRY; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 84865847205     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155412446227     Document Type: Article

References (42)

1. Aggarwal SK.A histochemical approach to the mechanism of action of cisplatin and its analogues.J Histochem Cytochem. 1993;7:1053-1073.
2. Anderson WA,Bara G,Seligman AM.The ultrastructural localization of cytochrome oxidase via cytochrome.J Histochem Cytochem. 1975;1:13-20.
3. Bertoni-Freddari C,Fattoretti P,Casoli T,Di Stefano G,Solazzi M,Gracciotti N,Pompei P.Mapping of mitochondrial metabolic competence by cytochrome oxidase and succinic dehydrogenase cytochemistry.J Histochem Cytochem. 2001;9:1191-1192.
4. Brady HR,Kone BC,Stromski ME,Zeidel ML,Giebisch G,Gullans SR.Mitochondrial injury: an early event in cisplatin toxicity to renal proximal tubules.Am J Physiol. 1990;258 (5): F1181-F1187.
5. Brooks C,Wei Q,Cho SG,Dong Z.Regulation of mitochondrial dynamics in acute kidney injury in cell culture and rodent models.J Clin Invest. 2009;119:1275-1285.
6. Bulger RE.Renal damage caused by heavy metals.Toxicol Pathol. 1986;1:58-65.
7. Chirino YI,Hernández-Pando R,Pedraza-Chaverrí J.Peroxynitrite decomposition catalyst ameliorates renal damage and protein nitration in cisplatin-induced nephrotoxicity in rats.BMC Pharmacol. 2004;4:20.
8. Chirino YI,Pedraza-Chaverri J.Role of oxidative and nitrosative stress in cisplatin-induced nephrotoxicity.Exp Toxicol Pathol. 2009;61 (3): 223-242.
9. Chirino YI,Trujillo J,Sánchez-González DJ,Martínez-Martínez CM,Cruz C,Bobadilla NA,Pedraza-Chaverri J.Selective iNOS inhibition reduces renal damage induced by cisplatin.Toxicol Lett. 2008;176 (1): 48-57.
10. Davis CA,Nick HS,Agarwal A.Manganese superoxide dismutase attenuates Cisplatin-induced renal injury: importance of superoxide.J Am Soc Nephrol. 2001;12:2683-2690.
11. Dentino M,Luft FC,Yum MN,Williams SD,Einhorn LH.Long term effect of cis-diamminedichloride platinum (CDDP) on renal function and structure in man.Cancer. 1978;4:1274-1281.
12. Dobyan DC,Levi J,Jacobs C,Kosek J,Weiner MW.Mechanism of cis-platinum nephrotoxicity: II. Morphologic observations.J Pharmacol Exp Ther. 1980;3:551-556.
13. Dubowitz V1985. Muscle biopsy: a practical approach. 2nd ed.Lavenham, UK: Lavenham Press. p. 21.Lavenham, UK: Lavenham Press; 1985:21.
14. Gonzales-Vitale JC,Hayes DM,Cvitkovic E,Sternberg SS.The renal pathology in clinical trials of cis-platinum (II) diamminedichloride.Cancer. 1977;4:1362-1371.
15. Gordon JA,Gattone VH.Mitochondrial alterations in cisplatin-induced acute renal failure.Am J Physiol. 1986;250 (6): F991-F998.
16. Hershey SJ,Simon TW,Baste C.Histochemical localization of cytochrome oxidase in gastric mucosa.J Histochem Cytochem. 1975;4:271-282.
17. Holthöfer H,Kretzler M,Haltia A,Solin ML,Taanman JW,Schägger H,Kriz W,Kerjaschki D,Schlöndorff D.Altered gene expression and functions of mitochondria in human nephrotic syndrome.FASEB J. 1999;3:523-532.
18. Jones TW,Chorpa S,Kaufman JS,Flamenbaum W,Trump BFToxicol Pathol. 1985:296-305.
19. Kruidering M,Van de Water B,de Heer E,Mulder GJ,Nagelkerke JF.Cisplatin-induced nephrotoxicity in porcine proximal tubular cells: mitochondrial dysfunction by inhibition of complexes I to IV of the respiratory chain.J Pharmacol Exp Ther. 1997;2:638-649.
20. Langerak, Dreisbach LPGeorgetown, TX: Landes Bioscience; 2001:.
21. Lebrecht D,Setzer B,Rohrbach R,Walker UA.Mitochondrial DNA and its respiratory chain products are defective in doxorubicin nephrosis.Nephrol Dial Transplant. 2004;19:329-336.
22. Liu L,Yang C,Herzog C,Seth R,Kaushal GP.Proteasome inhibitors prevent cisplatin-induced mitochondrial release of apoptosis-inducing factor and markedly ameliorate cisplatin nephrotoxicity.Biochem Pharmacol. 2010;2:137-146.
23. Mahad DJ,Ziabreva I,Campbell G,Lax N,White K,Hanson PS,Lassmann H,Turnbull DM.Mitochondrial changes within axons in multiple sclerosis.Brain. 2009;5:1161-1174.
24. Matsushima H,Yonemura K,Ohishi K,Hishida A.The role of oxygen free radicals in cisplatin-induced acute renal failure in rats.J Lab Clin Med. 1998;131 (6): 518-526.
25. Mukhopadhyay P,Horváth B,Kechrid M,Tanchian G,Rajesh M,Naura AS,Boulares AH,Pacher P.Poly(ADP-ribose) polymerase-1 is a key mediator of cisplatin-induced kidney inflammation and injury.Free Radic Biol Med. 2011;9:1774-1788.
26. Mukhopadhyay P,Horváth B,Zsengellér 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.
27. Mukhopadhyay P,Pan H,Rajesh M,Bátkai S,Patel V,Harvey-White J,Mukhopadhyay B,Haskó G,Gao B,Mackie K, et al.CB1 cannabinoid receptors promote oxidative/nitrosative stress, inflammation and cell death in a murine nephropathy model.Br J Pharmacol. 2010;3:657-668.
28. Mukhopadhyay P,Rajesh M,Pan H,Patel V,Mukhopadhyay B,Bátkai S,Gao B,Haskó G,Pacher P.Cannabinoid-2 receptor limits inflammation, oxidative/nitrosative stress, and cell death in nephropathy.Free Radic Biol Med. 2010;3:457-467.
29. Nowak G.Protein kinase C-alpha and ERK1/2 mediate mitochondrial dysfunction, decreases in active Na+ transport, and cisplatin-induced apoptosis in renal cells.J Biol Chem. 2002;45:43377-43388.
30. Pan H,Mukhopadhyay P,Rajesh M,Patel V,Mukhopadhyay B,Gao B,Haskó G,Pacher P.Cannabidiol attenuates cisplatin-induced nephrotoxicity by decreasing oxidative/nitrosative stress, inflammation, and cell death.J Pharmacol Exp Ther. 2009;328 (3): 708-714.
31. Racusen LC,Solez K.Nephrotoxic tubular and interstitial lesions: morphology and classification.Toxicol Pathol. 1986;1:45-57.
32. Ramesh G,Reeves WB.TNF-alpha mediates chemokine and cytokine expression and renal injury in cisplatin nephrotoxicity.J Clin Invest. 2002;6:835-842.
33. Ries F,Klastersky J.Nephrotoxicity induced by cancer chemotherapy with special emphasis on cisplatin toxicity.Am J Kidney Dis. 1986;5:368-379.
34. Safirstein R,Winston J,Goldstein M,Moel D,Dikman S,Guttenplan J.Cisplatin nephrotoxicity.Am J Kidney Dis. 1986;5:356-367.
35. Sahni V,Choudhury D,Ahmed Z.Chemotherapy-associated renal dysfunction.Nat Rev Nephrol. 2009;8:450-462.
36. Santos NA,Catão CS,Martins NM,Curti C,Bianchi ML,Santos AC.Cisplatin-induced nephrotoxicity is associated with oxidative stress, redox state unbalance, impairment of energetic metabolism and apoptosis in rat kidney mitochondria.Arch Toxicol. 2007;7:495-504.
37. Schrier RW.Cancer therapy and renal injury.J Clin Invest. 2002;110 (6): 743-745.
38. Seligman AM,Karnovsky MJ,Wasserkrug HL,Hanker JS.Nondroplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic reagent, diaminobenzidine (DAB).J Cell Biol. 1968;1:1-14.
39. Tanji N,Tanji K,Kambham N,Markowitz GS,Bell A,D'agati VD.Adefovir nephrotoxicity: possible role of mitochondrial DNA depletion. Hum Pathol. 2001;7:734-740.
40. Ward JM,Fauvie KA.The nephrotoxic effects of cis- diammine-dichloroplatinum (II) (NSC-119875) in male F344 rats.Toxicol Appl Pharmacol. 1976;3:535-547.
41. Zhang B,Ramesh G,Norbury CC,Reeves WB.Cisplatin induced nephrotoxicity is mediated by tumor necrosis factor-alpha produced by renal parenchymal cells.Kidney Int. 2007;72:37-44.
42. Zhang JG,Lindup WE.Cisplatin nephrotoxicity: decreases in mitochondrial protein sulphydryl concentration and calcium uptake by mitochondria from rat renal cortical slices.Biochem Pharmacol. 1994;7:1127-1135.