A correlation between cytotoxicity and reductase-mediated metabolism in cell lines treated with doxorubicin and daunorubicin

Journal of Pharmacology and Experimental Therapeutics

Volumn 347, Issue 2, 2013, Pages 375-387

  Bains, Onkar S ^a   Szeitz, András ^a   Lubieniecka, Joanna M ^a   Cragg, Gina E ^a   Grigliatti, Thomas A ^b   Riggs, K Wayne ^a   Reid, Ronald E ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Faculty of Science   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE KETONE REDUCTASE; ALDOKETOREDUCTASE 1A1; ALDOKETOREDUCTASE 1B1; ALDOKETOREDUCTASE 1B10; ALDOKETOREDUCTASE 1C1; ALDOKETOREDUCTASE 1C2; ALDOKETOREDUCTASE 1C3; ALDOKETOREDUCTASE 1C4; ALDOKETOREDUCTASE 7A2; CARBONYL REDUCTASE; CARBONYL REDUCTASE 1; CARBONYL REDUCTASE 3; DAUNORUBICIN; DOXORUBICIN; OXIDOREDUCTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CELL; CELL ACTIVITY; CELL ASSAY; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG EXPOSURE; DRUG METABOLISM; DRUG PENETRATION; DRUG STRUCTURE; ENZYME ACTIVITY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; INTESTINE CELL; KIDNEY CELL; LC 50; LIVER CELL; LUNG ALVEOLUS CELL; NONHUMAN; OVARY CELL; PANCREAS CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STRUCTURE ANALYSIS; WESTERN BLOTTING;

ALCOHOL OXIDOREDUCTASES; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL CULTURE TECHNIQUES; CELL LINE; CELL SURVIVAL; DAUNORUBICIN; DOXORUBICIN; HUMANS; LETHAL DOSE 50; ORGAN SPECIFICITY; RATS; SPECIES SPECIFICITY;

EID: 84886066848     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.206805     Document Type: Article

References (51)

1. Ax W, Soldan M, Koch L., and Maser E (2000) Development of daunorubicin resistance in tumour cells by induction of carbonyl reduction. Biochem Pharmacol 59: 293-300.
2. Bains OS, Grigliatti TA, Reid R.E., and Riggs KW (2010b) Naturally occurring variants of human aldo-keto reductases with reduced in vitro metabolism of daunorubicin and doxorubicin. J Pharmacol Exp Ther 335:533-545.
3. Bains OS, Karkling MJ, Grigliatti T.A., Reid RE, and Riggs KW (2009) Two non-synonymous single nucleotide polymorphisms of human carbonyl reductase 1 demonstrate reduced in vitro metabolism of daunorubicin and doxorubicin. Drug Metab Dispos 37:1107-1114.
4. Bains OS, Karkling MJ, Lubieniecka J.M., Grigliatti TA, Reid RE, and Riggs KW (2010a) Naturally occurring variants of human CBR3 alter anthracycline in vitro metabolism. J Pharmacol Exp Ther 332:755-763.
5. Bains OS, Takahashi RH, Pfeifer T.A., Grigliatti TA, Reid RE, and Riggs KW (2008) Two allelic variants of aldo-keto reductase 1A1 exhibit reduced in vitro metabolism of daunorubicin. Drug Metab Dispos 36:904-910.
6. Barry E, Alvarez JA, Scully R.E., Miller TL, and Lipshultz SE (2007) Anthracycline-induced cardiotoxicity: course, pathophysiology, prevention and management. Expert Opin Pharmacother 8:1039-1058.
7. Behnia K and Boroujerdi M (1999) Inhibition of aldo-keto reductases by phenobarbital alters metabolism, pharmacokinetics and toxicity of doxorubicin in rats. J Pharm Pharmacol 51:1275-1282.
8. Bernardini N, Giannessi F, Bianchi F., Dolfi A, Lupetti M, Zaccaro L., Malvaldi G, and Del Tacca M (1991) Comparative activity of doxorubicin and its major metabolite, doxorubicinol, on V79/AP4 fibroblasts: a morphofunctional study. Exp Mol Pathol 55:238-250.
9. Blanco JG, Leisenring WM, Gonzalez-Covarrubias VM, Kawashima T.I., Davies SM, Relling MV, Robison LL, Sklar C.A., Stovall M., and Bhatia S (2008) Genetic polymorphisms in the carbonyl reductase 3 gene CBR3 and the NAD(P)H: quinone oxidoreductase 1 gene NQO1 in patients who developed anthracycline-related congestive heart failure after childhood cancer. Cancer 112:2789-2795.
10. Brouwer CA, Gietema JA, van den Berg MP, Bink-Boelkens MT, Elzenga NJ, Haaksma J, Kamps WA, Vonk JM, de Vries EG, and Postma A (2006) Long-term cardiac follow-up in survivors of a malignant bone tumour. Ann Oncol 17: 1586-1591.
11. Choi HS, Park ES, Kang H.J., Shin HY, Noh CI, Yun YS, Ahn H.S., and Choi JY (2010) Dexrazoxane for preventing anthracycline cardiotoxicity in children with solid tumors. J Korean Med Sci 25:1336-1342.
12. Cummings J, Anderson L, Willmott N., and Smyth JF (1991) The molecular pharmacology of doxorubicin in vivo. Eur J Cancer 27:532-535.
13. Danesi R, Fogli S, Gennari A., Conte P, and Del Tacca M (2002) Pharmacokinetic-pharmacodynamic relationships of the anthracycline anticancer drugs. Clin Pharmacokinet 41:431-444.
14. Deng S and Wojnowski L (2007) Genotyping the risk of anthracycline- induced cardiotoxicity. Cardiovasc Toxicol 7:129-134.
15. Forrest GL, Gonzalez B, Tseng W., Li X, and Mann J (2000) Human carbonyl reductase overexpression in the heart advances the development of doxorubicin-induced cardiotoxicity in transgenic mice. Cancer Res 60:5158-5164.
16. Gavelová M, Hladíková J, Vildová L, Novotná R, Vondrácek J, Krcmár P, Machala M, and Skálová L (2008) Reduction of doxorubicin and oracin and induction of carbonyl reductase in human breast carcinoma MCF-7 cells. Chem Biol Interact 176: 9-18.
17. Gewirtz DA (1999) A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 57:727-741.
18. Gonzalez B, Akman S, Doroshow J., Rivera H, Kaplan WD, and Forrest GL (1995) Protection against daunorubicin cytotoxicity by expression of a cloned human carbonyl reductase cDNA in K562 leukemia cells. Cancer Res 55:4646-4650.
19. Hanna AD, Janczura M, Cho E., Dulhunty AF, and Beard NA (2011) Multiple actions of the anthracycline daunorubicin on cardiac ryanodine receptors. Mol Pharmacol 80:538-549.
20. Hempel G, Flege S, Würthwein G, and Boos J (2002) Peak plasma concentrations of doxorubicin in children with acute lymphoblastic leukemia or non-Hodgkin lymphoma. Cancer Chemother Pharmacol 49:133-141.
21. Hrdina R, Gersl V, Klimtová I, Simûnek T, Machácková J, and Adamcová M (2000) Anthracycline-induced cardiotoxicity. Acta Med (Hradec Kralove) 43:75-82.
22. Jin Y and Penning TM (2007) Aldo-keto reductases and bioactivation/ detoxication. Annu Rev Pharmacol Toxicol 47:263-292.
23. Jones RL (2008) Utility of dexrazoxane for the reduction of anthracycline-induced cardiotoxicity. Expert Rev Cardiovasc Ther 6:1311-1317.
24. Kassner N, Huse K, Martin H-J, Gödtel-Armbrust U, Metzger A, Meineke I, Brockmöller J, Klein K, Zanger UM, and Maser E, et al. (2008) Carbonyl reductase 1 is a predominant doxorubicin reductase in the human liver. Drug Metab Dispos 36: 2113-2120.
25. Klugmann FB, Decorti G, Candussio L., Grill V, Mallardi F, and Baldini L (1986) Inhibitors of adriamycin-induced histamine release in vitro limit adriamycin cardiotoxicity in vivo. Br J Cancer 54:743-748.
26. Lachâtre F., Marquet P, Ragot S., Gaulier JM, Cardot P, and Dupuy JL (2000) Simultaneous determination of four anthracyclines and three metabolites in human serum by liquid chromatography-electrospray mass spectrometry. J Chromatogr B Biomed Sci Appl 738:281-291.
27. Lakhman SS, Ghosh D, and Blanco JG (2005) Functional significance of a natural allelic variant of human carbonyl reductase 3 (CBR3). Drug Metab Dispos 33: 254-257.
28. Licata S, Saponiero A, Mordente A., and Minotti G (2000) Doxorubicin metabolism and toxicity in human myocardium: role of cytoplasmic deglycosidation and carbonyl reduction. Chem Res Toxicol 13:414-420.
29. Lipp HP and Bokemeyer C (1999) Anthracyclines and other intercalating agents, in Anticancer Drug Toxicity: Prevention, Management and Clinical Pharmacokinetics (Lipp HP ed) pp 81-113, Marcel Dekker, New York.
30. Liu J, Mao W, Ding B., and Liang CS (2008) ERKs/p53 signal transduction pathway is involved in doxorubicin-induced apoptosis in H9c2 cells and cardiomyocytes. Am J Physiol Heart Circ Physiol 295:H1956-H1965.
31. Lubieniecka JM, Liu J, Heffner D., Graham J, Reid RE, Hogge D, Grigliatti T.A., and Riggs WK (2012) Single-nucleotide polymorphisms in aldo-keto and carbonyl reductase genes are not associated with acute cardiotoxicity after daunorubicin chemotherapy. Cancer Epidemiol Biomarkers Prev 21:2118-2120.
32. Martin HJ, Breyer-Pfaff U, Wsol V., Venz S, Block S, and Maser E (2006) Purification and characterization of akr1b10 from human liver: role in carbonyl reduction of xenobiotics. Drug Metab Dispos 34:464-470.
33. Menna P, Recalcati S, Cairo G., and Minotti G (2007) An introduction to the metabolic determinants of anthracycline cardiotoxicity. Cardiovasc Toxicol 7:80-85.
34. Minotti G, Menna P, Salvatorelli E., Cairo G, and Gianni L (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56:185-229.
35. Mordente A, Meucci E, Martorana G.E., Giardina B., and Minotti G (2001) Human heart cytosolic reductases and anthracycline cardiotoxicity. IUBMB Life 52:83-88.
36. Mordente A, Meucci E, Silvestrini A., Martorana GE, and Giardina B (2009) New developments in anthracycline-induced cardiotoxicity. Curr Med Chem 16: 1656-1672.
37. O'Connor T., Ireland LS, Harrison D.J., and Hayes JD (1999) Major differences exist in the function and tissue-specific expression of human aflatoxin B1 aldehyde reductase and the principal human aldo-keto reductase AKR1 family members. Biochem J 343:487-504.
38. Ohara H, Miyabe Y, Deyashiki Y., Matsuura K, and Hara A (1995) Reduction of drug ketones by dihydrodiol dehydrogenases, carbonyl reductase and aldehyde reductase of human liver. Biochem Pharmacol 50:221-227.
39. Olson LE, Bedja D, Alvey S.J., Cardounel AJ, Gabrielson KL, and Reeves RH (2003) Protection from doxorubicin-induced cardiac toxicity in mice with a null allele of carbonyl reductase 1. Cancer Res 63:6602-6606.
40. Olson RD, Mushlin PS, Brenner D.E., Fleischer S., Cusack BJ, Chang BK, and Boucek RJ, Jr (1988) Doxorubicin cardiotoxicity may be caused by its metabolite, doxorubicinol. Proc Natl Acad Sci USA 85:3585-3589.
41. Plandé J, Platel D, Tariosse L, and Robert J (2006) Experimental study of dexrazoxane-anthracycline combinations using the model of isolated perfused rat heart. Toxicol Lett 161:37-42.
42. Plebuch M, Soldan M, Hungerer C., Koch L, and Maser E (2007) Increased resistance of tumor cells to daunorubicin after transfection of cDNAs coding for anthracycline inactivating enzymes. Cancer Lett 255:49-56.
43. Sawyer DB, Peng X, Chen B., Pentassuglia L, and Lim CC (2010) Mechanisms of anthracycline cardiac injury: can we identify strategies for cardioprotection? Prog Cardiovasc Dis 53:105-113.
44. Simûnek T., Stérba M, Popelová O, Adamcová M, Hrdina R, and Gersl V (2009) Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep 61:154-171.
45. Skovsgaard T and Nissen NI (1982) Membrane transport of anthracyclines. Pharmacol Ther 18:293-311.
46. Sparreboom A, Nooter K, and Verweij J (2002) Mechanisms of action of cancer chemotherapy agents: antitumor antibiotics, in The Cancer Handbook (Alison MR ed) pp 1-13, John Wiley & Sons, New York.
47. Tak E, Lee S, Lee J., Rashid MA, Kim YW, Park JH, Park W.S., Shokat KM, Ha J, and Kim SS (2011) Human carbonyl reductase 1 upregulated by hypoxia renders resistance to apoptosis in hepatocellular carcinoma cells. J Hepatol 54:328-339.
48. Veitch ZW, Guo B, Hembruff S.L., Bewick AJ, Heibein AD, Eng J, Cull S., Maclean DA, and Parissenti AM (2009) Induction of 1C aldoketoreductases and other drug dose-dependent genes upon acquisition of anthracycline resistance. Pharmacogenet Genomics 19:477-488.
49. Volkan-Salanci B., Aksoy H, Kiratli PÖ, Tülümen E, Güler N, Öksüzoglu B, Tokgözoglu L, Erbas B, and Alikasifoglu M (2012) The relationship between changes in functional cardiac parameters following anthracycline therapy and carbonyl reductase 3 and glutathione S transferase Pi polymorphisms. J Chemother 24:285-291.
50. Wojtacki J, Lewicka-Nowak E, and Lesniewski-Kmak K (2000) Anthracycline-induced cardiotoxicity: clinical course, risk factors, pathogenesis, detection and prevention - review of the literature. Med Sci Monit 6:411-420.
51. Wouters KA, Kremer LC, Miller T.L., Herman EH, and Lipshultz SE (2005) Protecting against anthracycline-induced myocardial damage: a review of the most promising strategies. Br J Haematol 131:561-578.