Doxorubicin-induced in vivo nephrotoxicity involves oxidative stress-mediated multiple pro- and anti-apoptotic signaling pathways

Current Neurovascular Research

Volumn 9, Issue 4, 2012, Pages 282-295

  Lahoti, Tejas S ^a,b,c   Patel, Darshan ^a   Thekkemadom, Venkatesh ^a   Beckett, Robert ^a   Ray, Sidhartha D ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c MANCHESTER UNIVERSITY   (United States)

Author keywords

APAF 1; Apoptosis; Bad; Bax; Bcl 2; Bcl xL; Caspase 3; Doxorubicin; Lipid peroxidation; Mdm2; Necrosis; Nephrotoxicity; Oxidative stress; SOD

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; BETA ACTIN; CASPASE 3; CREATININE; DOXORUBICIN; GENOMIC DNA; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MDM2; PROTEIN P53; SUPEROXIDE DISMUTASE; UREA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DNA FRAGMENTATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE REPRESSION; HISTOPATHOLOGY; KIDNEY INJURY; KIDNEY PARENCHYMA; LIPID PEROXIDATION; MALE; MITOCHONDRION; NEPHROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; UREA NITROGEN BLOOD LEVEL; WEIGHT REDUCTION; WESTERN BLOTTING;

EID: 84870440754     PISSN: 15672026     EISSN: 18755739     Source Type: Journal    
DOI: 10.2174/156720212803530636     Document Type: Article

References (90)

1. Mitropoulos FA, Angelopoulou MK, Siakantaris MP, et al. Primary non-Hodgkin's lymphoma of the gall bladder. Leuk Lymphoma 2000;40(1-2):123-31.
2. Patel N, Joseph C, Corcoran GB, Ray SD. Silymarin modulates doxorubicininduced oxidative stress, Bcl-xL and p53 expression while preventing apoptotic and necrotic cell death in the liver. Toxicol Appl Pharmacol 2010;245(2):143-52.
3. Petrioli R, Fiaschi AI, Francini E, Pascucci A, Francini G. The role of doxorubicin and epirubicin in the treatment of patients with metastatic hormonerefractory prostate cancer. Cancer Treatment Rev 2008;34(8):710-8.
4. Poletti P, Bettini AC, Caremoli ER, Labianca R, Tondini C. Liposomalencapsulated doxorubicin (Myocet; D-99) and vinorelbine in previously treated metastatic breast cancer patients: a feasibility study. Tumori 2008;94(5):686-90.
5. Bozcali E, Dedeoglu DB, Karpuz V, Suzer O, Karpuz H. Cardioprotective effects of zofenopril, enalapril and valsartan against ischaemia/reperfusion injury as well as doxorubicincardiotoxicity. Acta Cardiol 2012;67(1):87-96.
6. Burke JF (Jr), Laucius JF, Brodovsky HS, Soriano RZ. Doxorubicin hydrochloride-associated renal failure. Arch Int Med 1977;137(3):385-8. (Pubitemid 9037753)
7. Salvatorelli E, Menna P, Surapaneni S, et al. Pharmacokinetic characterization of amrubicin cardiac safety in an ex vivo human myocardial strip model. I. Amrubicin accumulates to a lower level than doxorubicin or epirubicin. J Pharmacol Exp Ther 2012a; 341(2):464-73.
8. Salvatorelli E, Menna P, Surapaneni S, et al. Pharmacokinetic characterization of amrubicin cardiac safety in an ex vivo human myocardial strip model. II. Amrubicin shows metabolic advantages over doxorubicin and epirubicin. J Pharmacol Exp Ther 2012b; 341(2):474-83.
9. Ray SD, Patel D, Wong V, Bagchi D. In vivo protection of DNA damage associated apoptotic and necrotic cell deaths during acetaminophen-induced nephrotoxicity, amiodarone-induced lung toxicity and doxorubicin-induced cardiotoxicity by a novel IH636 grape seed proanthocyanidin extract. Res Commu Mol Pathol Pharmacol 2000;107(1-2):137-66. (Pubitemid 32240572)
10. Ferreira AL, Matsubara LS, Matsubara BB. Cardiovas. Hematol. Agents Med Chem 2008;6(4):278-8.
11. Castells MC. Hypersensitivity to antineoplastic agents. Curr Pharm Des 2008;14(27):2892-901.
12. Zhang J, Clark JR Jr, Herman EH, Ferrans VJ. Doxorubicininduced apoptosis in spontaneously hypertensive rats: differential effects in heart, kidney and intestine, and inhibition by ICRF-187. J Mol Cellu Cardiol 1996;28(9):1931-43. (Pubitemid 26340553)
13. Hickey EJ, Raje RR, Reid VE, Gross SM, Ray SD. Diclofenac induced in vivo nephrotoxicity may involve oxidative stress mediated massive genomic DNA fragmentation and apoptotic death. Free Rad Biol Med 2001;31(2):139-152. (Pubitemid 32607581)
14. Schnellmann RG, et al., Toxic response to kidney. In: Curtis Klaassen. Casarret and Doull's 7th Ed., Toxicology McGraw-Hill Publications. 2008:582-608.
15. Bhatt S, Patel C, Ray SD. Differential expression of pro-apoptotic and antiapoptotic genes during diclofenac-induced oxidative stressmediated nephrotoxicity in vivo. The FASEB J 2008; Vol. 22, Abst#917.9.
16. Dos Santos NA, Carvalho Rodrigues MA, Martins NM, Dos Santos AC. Cisplatin-induced nephrotoxicity and targets of nephroprotection: an update. Arch Toxicol 2012; (Epub ahead of print)
17. Horváth B, Mukhopadhyay P, Kechrid M, Patel V, et al. γ-Caryophyllene ameliorates cisplatin-induced nephrotoxicity in a cannabinoid 2 receptordependent manner. Free Rad Biol Med 2012;52(8):1325-33.
18. Lee IC, Kim SH, Lee SM, Baek HS, et al. Melatonin attenuates gentamicininduced nephrotoxicity and oxidative stress in rats. Arch Toxicol 2012; [Epub ahead of print]
19. Mordente A, Minotti G, Martorana GE, et al. Anthracycline secondary alcohol metabolite formation in human or rabbit heart: biochemical aspects and pharmacologic implications. Biochem Pharmacol 2003;66(6):989-98. (Pubitemid 37086708)
20. Bárdi E, Bobok I, V Oláh A, Kappelmayer J, Kiss C. Anthracycline antibiotics induce acute renal tubular toxicity in children with cancer. Pathol Oncol Res 2007;13(3):249-53. (Pubitemid 350221228)
21. Mordente A, Meucci E, Silvestrini A, Martorana G E, Giardina B. New developments in anthracycline-induced cardiotoxicity. Curr Me Chem 2009;16(13):1656-72.
22. Kassner N, Huse K, Martin HJ, Gödtel-Armbrust U, Carbonyl reductase 1 is a predominant doxorubicin reductase in the human liver. Drug Metab Dispos 2008;36(10):2113-20.
23. Bains OS, Karkling MJ, Lubieniecka JM, Grigliatti TA, Reid RE, Riggs KW. Naturally occurring variants of human CBR3 alter anthracycline in vitro metabolism. J Pharmacol Exp Ther 2010;332(3):755-63.
24. Novotna R, Wsol V, Xiong G, Maser E. Inactivation of the anticancer drugs doxorubicin and oracin by aldo-keto reductase (AKR) 1C3. Toxicol Lett 2008;181(1):1-6.
25. Minotti G, Recalcati S, Mordente A, Liberi G, et al. The secondary alcohol metabolite of doxorubicin irreversibly inactivates aconitase/iron regulatory protein-1 in cytosolic fractions from human myocardium. FASEB J 1998;12(7):541-52. (Pubitemid 28183513)
26. Erratum in: FASEB J 1998;12(9):732.
27. Pawówska J, Tarasiuk J, Wolf CR, Paine MJ, Borowski E. Differential ability of cytostatics from anthraquinone group to generate free radicals in three enzymatic systems: NADH dehydrogenase, NADPH cytochrome P450 reductase, and xanthine oxidase. Oncol Res 2003;13(5):245-52. (Pubitemid 38166378)
28. Thornalley PJ, Bannister WH, Bannister JV. Reduction of oxygen by NADH/NADH dehydrogenase in the presence of adriamycin. Free Radic Res Commun 1986;2(3):163-71.
29. Nohl H, Gille L, Staniek K. The exogenous NADH dehydrogenase of heart mitochondria is the key enzyme responsible for selective cardiotoxicity of anthracyclines. Z Naturforsch C 1998;53(3-4):279-85. (Pubitemid 28214237)
30. Gustafson DL, Swanson JD, Pritsos CA. Role of xanthine oxidase in the potentiation of doxorubicin-induced cardiotoxicity by mitomycin C. Cancer Commun 1991;3(9):299-304.
31. Vásquez-Vivar J, Martasek P, Hogg N, Masters BS, et al. Endothelial nitric oxide synthase-dependent superoxide generation from adriamycin. Biochemistry 1997;36(38):11293-7. (Pubitemid 27408610)
32. Fogli S, Nieri P, Breschi MC. The role of nitric oxide in anthracycline toxicity and prospects for pharmacologic prevention of cardiac damage. FASEB J 2004;18(6):664-75. (Pubitemid 38451788)
33. Miyamoto Y, Koh YH, Park YS, Fujiwara N, et. al. Oxidative stress caused by inactivation of glutathione peroxidase and adaptive responses. Biol Chem 2003;384(4):567-74. (Pubitemid 36609172)
34. Licata S, Saponiero A, Mordente A, Minotti G. Doxorubicin Metabolism and Toxicity in Human Myocardium: Role of Cytoplasmic Deglycosidation and Carbonyl Reduction. Chem Res Toxicol 2000;13(5), 414-420. (Pubitemid 30327162)
35. PharmGKB: http://www.pharmgkb.org/pathway/PA165292177).
36. Francescato HDC, Marin EC, Cunha Fde Q, et al. Role of endogenous hydrogen sulfide on renal damage induced by adriamycin injection. Arch Toxicol 2011;85(12):1597-606.
37. Ray SD, Patel N, Shah N, Nagori A, Naqvi A, Stohs SJ. Preexposure to a novel nutritional mixture containing a series of phytochemicals prevents acetaminophen-induced programmed and unprogrammed cell deaths by enhancing BCL-XL expression and minimizing oxidative stress in the liver. Mol Cell Biochem 2006;293(1-2):119-36. (Pubitemid 44843007)
38. Wallace KB. Adriamycin-induced interference with cardiac mitochondrial calcium homeostasis. Cardiovas Toxicol 2007;7(2):101-107. (Pubitemid 47339855)
39. Hohorst HJ, Arese P, Bartels H, Stratmann D, Talke H. Enzymatische harnstoff bestimmungim blut und serum im optischen test nach wrburg. Klin Wochenschr 1965;43:174-179.
40. Jaffe M. Ueber den Niederschlag welchen Pikrinsäure in normalen Harn erzeugt und über eine neue reaction des Kreatinins. Z Physiol Chem 1886;10:391-400.
41. Ray SD, Balasubramanian G, Bagchi D, Reddy CS. Ca (2+) - calmodulin antagonist chlorpromazine and poly (ADP-ribose) polymerase modulators 4-aminobenzamide and nicotinamide influence hepatic expression of BCL-XL and P53 and protect against acetaminophen-induced programmed and unprogrammed cell death in mice. Free Radic Biol Med 2001;31(3):277-91. (Pubitemid 32675333)
42. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autooxidation of pyrogallol and convenient assay for superoxide dismutase. Euro J Biochem 1974;47:469-474.
43. Bulku E, Stohs SJ, Cicero L, Brooks T, Halley H, Ray SD. Curcumin exposure modulates multiple pro-apoptotic and antiapoptotic signaling pathways to antagonize acetaminophen-induced toxicity. Curr Neurovasc Res 2012;9(1):58-71.
44. Ray SD, Mumaw VR, Raje RR, Fariss MW. Protection of acetaminopheninduced hepatocellular apoptosis and necrosis by cholesteryl hemisuccinate pretreatment. J Pharmacol Exp Therapeu 1996;279:1470-1483. (Pubitemid 27166797)
45. Burton K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 1956;62:315-322.
46. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227(5259):680-85.
47. Syed I, Rathod J, Parmar M, Corcoran GB, Ray SD. Matrix metalloproteinase-9, -10, and -12, MDM2 and p53 expression in mouse liver during dimethylnitrosamine-induced oxidative stress and genomic injury. Mol Cell Biochem 2012;365(1-2):351-61.
48. Ajith TA, Aswathy MS, Hema U. Protective effect of Zingiber officinale roscoe against anticancer drug doxorubicin-induced acute nephrotoxicity. Food & Chem Toxicol 2008;46(9):3178-81.
49. Ibrahim SS, Hafez EE. Hashishe MM. Presymptomatic breast cancer in Egypt: role of BRCA 1 and BRCA2 tumor suppressor genes mutations detection. J Exp Clin Cancer Res 2010;29(1):82.
50. Zordoky BN, Anwar-Mohamed A, Aboutabl ME, El-Kadi AO. Acute doxorubicin toxicity differentially alters cytochrome P450 expression and arachidonic acid metabolism in rat kidney and liver. Drug Metab Dispos 2011;39(8):1440-50.
51. Bertani T, Rocchi G, Sacchi G, Mecca G, Remuzzi G. Adriamycininduced glomerulosclerosis in the rat. Am J Kidney Dis 1986a; 7(1):12-9.
52. Bertani T, Cutillo F, Zoja C, Broggini M, Remuzzi G. Tubulointerstitial lesions mediate renal damage in adriamycin glomerulopathy. Kidney Int 1986b; 30(4):488-96. (Pubitemid 16000793)
53. Ibrahim MA, Ashour OM, Ibrahim YF, et al. Angiotensinconverting enzyme inhibition and angiotensin AT (1)-receptor antagonism equally improve doxorubicin-induced cardiotoxicity and nephrotoxicity. Pharmacol Res 2009;60(5):373-81.
54. Pereira CV, Nadanaciva S, Oliveira PJ, Will Y. The contribution of oxidative stress to drug-induced organ toxicity and its detection in vitro and in vivo. Expert Opi Drug Metab Toxicol 2012;8(2):219-237.
55. Ashour AE, Sayed-Ahmed MM, Abd-Allah AR et al. Metformin rescues the myocardium from Doxorubicin-induced energy starvation and mitochondrial damage in rats. Oxid Med Cell Longev 2012;2012:434195. [Epub]
56. Fariss MW, Lippman HR, Mumaw VR, Ray SD. Cholesteryl hemisuccinate treatment protects rodents from the toxic effects of acetaminophen, adriamycin, carbon tetrachloride, chloroform and galactosamine. Toxicol Lett. 1997;90(2-3):133-44. (Pubitemid 27096528)
57. Huelsenbeck J, Henninger C, Schad A, et al. Inhibition of Rac1 signaling by lovastatin protects against anthracycline-induced cardiac toxicity. Cell Death Dis 2011;2:e190. doi:10.1038/cddis.2011.65.
58. Xiao J, Sun GB, Sun B, Wu Y, et al. Kaempferol protects against doxorubicininduced cardiotoxicity in vivo and in vitro. Toxicology 2012;292(1):53-62.
59. Injac R, Boskovic M, Perse M, et al., "Acute doxorubicin nephrotoxicity in rats with malignant neoplasm can be successfully treated with fullerenol C60 (OH) 24 via suppression of oxidative stress". Pharmacol Rep 2008;60(5):742-9.
60. Pal S, Sil PC. A 43 kD protein from the leaves of the herb Cajanus indicus L. modulatesdoxorubicin induced nephrotoxicity via MAPKs and both mitochondria dependent and independent pathways. Biochimie 2012;94(6):1356-67.
61. Ayla S, Seckin I, Tanriverdi G, et al. Doxorubicin induced nephrotoxicity: protective effect of nicotinamide. Int J Cell Biol 2011;2011:390238. [Epub]
62. Bárdi E, Bobok I, V Oláh A, et al. Anthracycline antibiotics induce acute renal tubular toxicity in children with cancer. Pathol Oncol Res 2007;13(3):249-53.
63. Guo J, Ananthakrishnan R, Qu W, et al. RAGE mediates podocyte injury in adriamycin-induced glomerulosclerosis. J Am Soc Nephrol 2008;19(5):961-72.
64. Si H, Banga RS, Kapitsinou P, et al. Human and murine kidneys show gender-and species-specific gene expression differences in response to injury. PLoS One 2009;4(3):e4802.
65. Roubaud G, Gross-Goupil M, Wallerand H, et al. Combination of gemcitabine and doxorubicin in rapidly progressive metastatic renal cell carcinoma and/or sarcomatoid renal cell carcinoma. Oncology 2011;80(3-4):214-8.
66. Boonsanit D, Kanchanapangka S, Buranakarl C. L-carnitine ameliorates doxorubicin-induced nephrotic syndrome in rats. Nephrol 2006;11(4):313-20. (Pubitemid 44086876)
67. Menini S, Ricci C, Scipioni A, et al. Advanced lipoxidation endproducts mediate lipid-induced glomerular injury: role of receptormediated mechanisms. J Pathol 2009;218(3):360-9.
68. Mross K, Maessen P, van der Vijgh WJ, et al. Pharmacokinetics and metabolism of epidoxorubicin and doxorubicin in humans. J Clin Oncol 1988;6(3):517-26. (Pubitemid 18090701)
69. Abo-Salem OM. The protective effect of aminoguanidine on doxorubicin-induced nephropathy in rats.
70. Sheridan AM, Fitzpatrick S, Wang C, et al. Lipid peroxidation contributes to hydrogen peroxideinduced cytotoxicity in renal epithelial cells. Kidney Intl 1996;49:88-93. (Pubitemid 26022831)
71. Ray SD, Lam TS, Rotollo JA, et al. Oxidative stress is the master operator of drug and chemically-induced programmed and unprogrammed cell death: Implications of natural antioxidants in vivo. Biofactors 2004;21(1-4):223-32. (Pubitemid 40921858)
72. Deepa PR, Varalakshmi P. Influence of a low-molecular-weight heparin derivative on the nitric oxide levels and apoptotic DNA damage in Adriamycin induced cardiac and renal toxicity. Toxicology 2006;217(2-3):176-83. (Pubitemid 41773833)
73. Papeta N, Zheng Z, Schon EA, et al. Prkdc participates in mitochondrial genome maintenance and prevents Adriamycininduced nephropathy in mice. J Clin Invest 2010;120(11):4055-64. doi:10.1172/JCI43721. [Epub 2010]
74. Marechal X, Montaigne D, Marciniak C, et al. Doxorubicininduced cardiac dysfunction is attenuated by ciclosporin treatment in mice through improvements in mitochondrial bioenergetics. Clin Sci (Lond) 2011;121(9):405-13.
75. Ascensão A, Lumini-Oliveira J, Machado NG, et al. Acute exercise protects against calcium-induced cardiac mitochondrial permeability transition pore opening in doxorubicin-treated rats. Clin Sci (Lond) 2011;120(1):37-49.
76. Qin XJ, He W, Hai CX, Liang X, Liu R. Protection of multiple antioxidants Chinese herbal medicine on the oxidative stress induced by Adriamycin chemotherapy. J Appl Toxicol 2008;28(3):271-82. (Pubitemid 351518114)
77. Shang YC, Chong ZZ, Wang S, Maiese K. Erythropoietin and Wnt1 govern pathways of mTOR, Apaf-1, and XIAP in inflammatory microglia. Curr Neurovasc Res 2011;8(4):270-85.
78. Wang S, Chong ZZ, Shang YC, Maiese K. Wnt1 inducible signaling pathway protein 1 (WISP1) blocks neurodegeneration through phosphoinositide 3 kinase/Akt1 and apoptotic mitochondrial signaling involving Bad, Bax, Bim, and Bcl-xL. Curr Neurovasc Res 2012;9(1):20-31.
79. Cory S, Adams JM. The Bcl2 family: regulators of the cellular lifeor death switch. Nat Rev Cancer 2002;2:647-656. (Pubitemid 37328916)
80. Erster S, Moll UM. Stress-induced p53 runs a transcriptionindependent death program. Biochem Biophys Res Commun 2005;331:843-850. (Pubitemid 40615515)
81. Nithipongvanitch R, Ittarat W, Cole MA, et al. Mitochondrial and nuclear p 53 localization in cardiomyocytes: redox modulation by doxorubicin (adriamycin) ? Antioxid Redox Signal 2007;9:1001-1008. (Pubitemid 46919601)
82. L'Ecuyer T, Sanjeev S, Thomas R, Novak R, Das L, Campbell W, Heide RV. DNA damage is an early event in doxorubicin-induced cardiac myocyte death. Am J Physiol Heart Circ Physiol 2006;291:H1273-H1280. (Pubitemid 44343672)
83. Eno CO, Zhao G, Olberding KE, Li C. The Bcl-2 proteins Noxa and Bcl-xL coordinately regulate oxidative stress-induced apoptosis. Biochem J 2012;444(1):69-78.
84. Eno CO, Eckenrode EF, Olberding KE, Zhao G, White C, Li C. Distinct Roles of Mitochondria-and ER-localized Bcl-xL in Apoptosis Resistance and Ca2+ Homeostasis. Mol Biol Cell 2012; [Epub ahead of print]
85. Mathai JP, Germain M, Shore GC. BH3-only BIK regulates BAX, BAKdependent release of Ca2+ from endoplasmic reticulum stores and mitochondrial apoptosis during stress-induced cell death. J Biol Chem 2005;280(25):23829-36. (Pubitemid 40884869)
86. Robles AI, Bemmels NA, Foraker AB, Harris CC. APAF-1 Is a Transcriptional Target of p53 in DNA Damage-induced Apoptosis. Can Res 2001;6:6660-64. (Pubitemid 32896481)
87. Ecder T, Melnikov VY, Stanley M, et al. Caspases, Bcl-2 proteins and apoptosis in autosomal-dominant polycystic kidney disease. Kidney Intl 2002;61, 1220-30. (Pubitemid 34304482)
88. Conus S, Rossé T, Borner C. Failure of Bcl-2 family members to interact with APAF-1 in normal and apoptotic cells. Cell Death Differ 2000;7(10):947-54.
89. Venkatesan B, Prabhu SD, Venkatachalam K, et al. WNT1-inducible signaling pathway protein-1 activates diverse cell survival pathways and blocks doxorubicin-induced cardiomyocyte death. Cell Signal 2010;22(5):809-20.
90. Ray SD and Corcoran GB. Cell death and apoptosis: In: Ballantyne B, Marrs T, Turner P, Eds. General and Applied Toxicology, Vol. I, 3rd Edition, London: Stockton/McMillan Publications; ISBN# 978-0-470-72327-2, Pp. 248-312, 2009.