Paclitaxel and docetaxel stimulation of doxorubicinol formation in the human heart: Implications for cardiotoxicity of doxorubicin-taxane chemotherapies

Journal of Pharmacology and Experimental Therapeutics

Volumn 318, Issue 1, 2006, Pages 424-433

  Salvatorelli, Emanuela ^a   Menna, Pierantonio ^a   Cascegna, Sabrina ^a   Liberi, Giovanni ^a   Calafiore, Antonio M ^b   Gianni, Luca ^c   Minotti, Giorgio ^a  

^a UNIVERSITY OF CHIETI   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

^c NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE REDUCTASE; ANTHRACYCLINE DERIVATIVE; CREMOPHOR; DOCETAXEL; DOXORUBICIN; DOXORUBICINOL; DRUG VEHICLE; IMIRESTAT; OXIDOREDUCTASE INHIBITOR; PACLITAXEL; POLYSORBATE 80; QUERCETIN; TAXANE DERIVATIVE; TOLRESTAT;

ADULT; AGED; ALLOSTERISM; ARTICLE; CARDIOTOXICITY; CHEMOTHERAPY; CONTROLLED STUDY; CYTOSOL; DOSE RESPONSE; DRUG EFFECT; DRUG UPTAKE; FEMALE; HEART MUSCLE; HUMAN; HUMAN TISSUE; MALE; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

AGED; ALLOSTERIC REGULATION; ANTINEOPLASTIC AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; FEMALE; HUMANS; MALE; MIDDLE AGED; MYOCARDIUM; PACLITAXEL; TAXOIDS;

EID: 33745263272     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.106.103846     Document Type: Article

References (40)

1. Baker SD, Zhao M, Lee CKK, Verweij J, Zabelina Y, Brahmer JR, Wolff AC, Sparreboom A, and Carducci MA (2004) Comparative pharmacokinetics of weekly and every-three-weeks docetaxel. Clin Cancer Res 10:1976-1983.
2. Barski OA, Gabbay KH, and Bohren KM (1996) The C-terminal loop of aldehyde reductase determines the substrate and inhibitor specificity. Biochemistry 35:14276-14280.
3. Barski OA, Gabbay KH, Grimshaw CE, and Bohren KM (1995) Mechanism of human aldehyde reductase: characterization of the active site pocket. Biochemistry 34:11264-11275.
4. 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.
5. 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.
6. D'Incalci M, Schuller J, Colombo T, Zucchetti M, and Riva A (1998) Taxoids in combination with anthracyclines and other agents: pharmacokinetic considerations. Semin Oncol 25 (Suppl 13):16-20.
7. Engel FB, Hauck L, Cardoso MC, Leonhardt H, Dietz R, and von Harsdorf R (1999) A mammalian myocardial cell-free system to study cell cycle reentry in terminally differentiated cardiomyocytes. Circ Res 85:294-301.
8. Felsted RL, Gee M, and Bachur NR (1974) Rat liver daunorubicin reductase. An aldo-keto reductase. J Biol Chem 249:3672-3679.
9. Finlay GJ and Baguley BC (2000) Effects of protein binding on the in vitro activity of antitumour acridine derivatives and related anticancer drugs. Cancer Chemother Pharmacol 45:417-422.
10. Forrest GL and Gonzalez B (2000) Carbonyl reductase. Chem Biol Interact 129:21-40.
11. 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.
12. Gambliel HA, Burke BE, Cusack BJ, Walsh GM, Zhang YL, Mushlin PS, and Olson RD (2002) Doxorubicin and C-13 deoxydoxorubicin effects on ryanodine receptor gene expression. Biochem Biophys Res Commun 291:433-438.
13. 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.
14. Gianni L, Baselga J, Eiermann W, Guillem Porta V, Semiglazov V, Lluch A, Zambetti M, Sabadell D, Raab G, Llombart Cussac A, et al. (European Cooperative Trial in Operable Breast Cancer Study Group) (2005) Feasibility and tolerability of sequential doxorubicin/paclitaxel followed by cyclophosphamide, methotrexate and fluorouracil and its effects on tumor response as preoperative therapy. Clin Cancer Res 11:8715-8721.
15. Gianni L, Munzone E, Capri G, Fulfaro F, Tarenzi E, Villani F, Spreafico C, Laffranchi A, Caraceni A, Martini C, et al. (1995) Paclitaxel by 3-hour infusion in combination with bolus doxorubicin in women with untreated metastatic breast cancer: high antitumor efficacy and cardiac effects in a dose-finding and sequence-finding study. J Clin Oncol 13:2688-2699.
16. Gianni L, Vigano L, Locatelli A, Capri G, Giani A, Tarenzi E, and Bonadonna G (1997) Human pharmacokinetic characterization and in vitro study of the interaction between doxorubicin and paclitaxel in patients with breast cancer. J Clin Oncol 15:1906-1915.
17. Grasselli G, Vigano L, Capri, Locatelli A, Tarenzi E, Spreafico C, Bertuzzi A, Giani A, Materazzo C, Cresta S, et al. (2001) Clinical and pharmacologic study of the epirubicin and paclitaxel combination in women with metastatic breast cancer. J Clin Oncol 19:2222-2231.
18. Kessel D (1992) Properties of Cremophor EL micelles probed by fluorescence. Photochem Photobiol 56:447-451.
19. Loos WJ, Baker SD, Verweij J, Boonstra JG, and Sparreboom A (2003) Clinical pharmacokinetics of unbound docetaxel: role of polysorbate 80 and serum proteins. Clin Pharmacol Ther 74:364-371.
20. Maessen PA, Mross KB, Pinedo HM, and van der Vijgh WJ (1987) Metabolism of epidoxorubicin in animals: absence of glucuronidation. Cancer Chemother Pharmacol 20:85-87.
21. Martin M, Pienkowski T, Mackey J, Pawlicki M, Guastalla JP, Weaver C, Tomiak E, Al-Tweigeri T, Chap L, Juhos E, et al., and Breast Cancer International Research Group 001 Investigators (2005) Adjuvant docetaxel for node-positive breast cancer. N Engl J Med 352:2302-2313.
22. McNamara PJ, Blouin RA, and Brazzell RK (1988) Serum protein binding of AL01576. Pharm Res (NY) 5:319-321.
23. 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.
24. Minotti G, Parlani M, Salvatorelli E, Menna P, Cipollone A, Animati F, Maggi CA, and Manzini S (2001a) Impairment of myocardial contractility by anticancer anthracyclines: role of secondary alcohol metabolites and evidence of reduced toxicity by a novel disaccharide analogue. Br J Pharmacol 134:1271-1280.
25. Minotti G, Saponiero A, Licata S, Menna A, Calafiore AM, Teodori G, and Gianni L (2001b) Paclitaxel and docetaxel enhance the metabolism of doxorubicin to toxic species in human myocardium. Clin Cancer Res 7:1511-1515.
26. Mushlin PS, Cusack BJ, Boucek RJ Jr, Andrejuk T, Li X, and Olson RD (1993) Time-related increases in cardiac concentrations of doxorubicinol could interact with doxorubicin to depress myocardial contractile function. Br J Pharmacol 110:975-982.
27. Mylari BL, Beyer TA, and Siegel TW (1991) A highly specific aldose reductase inhibitor ethyl 1-benzyl-3-hydroxy-25H-oxopyrrole-4-carboxylate and its congeners. J Med Chem 34:1011-1018.
28. Nabholtz JM, Falkson C, Campos D, Szanto J, Martin M, Chan S, Pienkowski T, Zaluski J, Pinter T, Krzakowski M, et al. (2003) Docetaxel and doxorubicin compared with doxorubicin and cyclophosphamide as first-line chemotherapy for metastatic breast cancer: results of a randomized, multicenter, phase III trial. J Clin Oncol 21:968-975.
29. Nabholtz JM, Pienkowski T, Mackey J, Pawlicki M, Guastalla JP, Vogel C, Weaver C, Walley B, Martin M, Chap L, et al. (2002) Phase III trial comparing TAC (docetaxel, doxorubicin, cyclophosphamide) with FAC (5-fluorouracil, doxorubicin, cyclophosphamide) in the adjuvant treatment of node positive breast cancer (BC) patients: interim analysis of the BCIRG 001 study. Proc Am Soc Clin Oncol 21:141A.
30. Ng SSW, Figg WD, and Sparreboom A (2004) Taxane-mediated antiangiogenesis in vitro: influence of formulation vehicles and binding proteins. Cancer Res 64:821-824.
31. Olson LE, Bedja D, Alvey SJ, 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.
32. Olson RD and Mushlin PS (1990) Doxorubicin cardiotoxicity: analysis of prevailing hypotheses. FASEB J 4:3076-3086.
33. Olson RD, Mushlin PS, Brenner DE, Fleischer S, Chang BK, Cusack BJ, and Boucek RJ Jr (1988) Doxorubicin cardiotoxicity may be due to its metabolite, doxorubicinol. Proc Natl Acad Sci USA 85:3585-3589.
34. Perotti S, Cresta G, Grasselli G, Capri G, Minotti G, and Gianni L (2003) Cardiotoxic effects of anthracycline-taxane combinations. Expert Opin Drug Saf 2:59-71.
35. Salvatorelli E, Guarnieri S, Menna P, Liberi G, Calafiore AM, Mariggiò MA, Mordente A, Gianni L, and Minotti G (2006) Defective one or two electron reduction of the anticancer anthracycline epirubicin in human heart: relative importance of vesicular sequestration and impaired efficiency of electron addition. J Biol Chem 281:10990-11001.
36. Slupe A, Williams B, Larson C, Lee LM, Primbs T, Bruesch AJ, Bjorklund C, Warner DL, Peloquin J, Shadle SE, et al. (2005) Reduction of 13-deoxydoxorubicin and daunorubicinol anthraquinones by human carbonyl reductase. Cardiovasc Toxicol 5:365-376.
37. Sparreboom A, Verweij J, van der Burg ME, Loos WJ, Brouwer E, Vigano L, Locatelli A, de Vos AI, Nooter K, Stoter G, et al. (1998) Disposition of Cremophor EL in humans limits the potential for modulation of the multidrug resistance phenotype in vivo. Clin Cancer Res 4:1937-1942.
38. Stewart DJ, Grewaal D, Green RM, Mikhael N, Goel R, Montpetit VA, and Redmond MD (1993) Concentrations of doxorubicin and its metabolites in human autopsy heart and other tissues. Anticancer Res 13:1945-1952.
39. ten Tije AK, Verweij J, Loos WJ, and Sparreboom A (2003) Pharmacological effects of formulation vehicles: implications for cancer chemotherapy. Clin Pharmacokinet 42:665-685.
40. Valero V and Hortobagyi GN (2003) Are anthracycline-taxane regimens the new standard of care in the treatment of metastatic breast cancer? J Clin Oncol 21:959-962.