Possibilities to increase the effectiveness of doxorubicin in cancer cells killing

Drug Metabolism Reviews

Volumn 43, Issue 4, 2011, Pages 540-557

  Hanušová, Veronika ^a   Boušová, Iva ^a   Skálová, Lenka ^a  

^a Charles University in Prague Faculty of Pharmacy   (Czech Republic)

Author keywords

Doxorubicin conjugation; Doxorubicin deactivation; Efflux transporters; Oxidative stress; Resistance

Indexed keywords

2 PYRROLINODOXORUBICIN; ALPHA FETOPROTEIN; AMINOGLUTETHIMIDE; AN 162; CELL PENETRATING PEPTIDE; CHORIONIC GONADOTROPIN DERIVATIVE; COPOLYMER; CYCLOPHOSPHAMIDE; DAUNORUBICIN; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLLYSYLVALYLCYSTEINYLTHREONINAMIDE 2,7 DISULFIDE 2 PYRROLINODOXORUBICIN; DOXORUBICIN; EPIDERMAL GROWTH FACTOR DERIVATIVE; EPIRUBICIN; FOLIC ACID; GONADORELIN DERIVATIVE; GONADORELIN[6 DEXTRO LYSINE] 2 PYRROLINODOXORUBICIN; GONADORELIN[6 DEXTRO LYSINE] DOXORUBICIN; IDARUBICIN; IDARUBICINOL; LIPOSOME; METHOXYMORPHOLINYLDOXORUBICIN CONJUGATE; MITOXANTRONE; MONOCLONAL ANTIBODY; N (2 HYDROXYPROPYL)METHACRYLAMIDE; NSC 23925; PEPTIDE DERIVATIVE; PRODRUG; SOMATOSTATIN DERIVATIVE; TOCOFERSOLAN; TRANSFERRIN; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTINEOPLASTIC ACTIVITY; BREAST CARCINOMA; CANCER CELL; CARDIOTOXICITY; CELL KILLING; CYTOPATHOGENIC EFFECT; DISTRIBUTION VOLUME; DRUG ACTIVATION; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG METABOLISM; DRUG UPTAKE; ENCAPSULATION; HUMAN; MULTIDRUG RESISTANCE; NONHUMAN; OXIDATIVE STRESS; REVIEW;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BIOLOGICAL TRANSPORT; BIOTRANSFORMATION; CELL DEATH; CHEMISTRY, PHARMACEUTICAL; DOXORUBICIN; DRUG CARRIERS; DRUG COMPOUNDING; HUMANS; MEMBRANE TRANSPORT PROTEINS; NEOPLASMS;

EID: 80054920730     PISSN: 03602532     EISSN: 10979883     Source Type: Journal    
DOI: 10.3109/03602532.2011.609174     Document Type: Review

References (155)

1. Adamcova, M., Gersl, V., Hrdina, R., Melka, M., Mazurova, Y., Vavrova, J., et al. (1999). Cardiac troponin T as a marker of myocardial damage caused by antineoplastic drugs in rabbits. J Cancer Res Clin Oncol 125:268-274. (Pubitemid 29243098)
2. Ahmad, I., Mustafa, E., Mustafa, N., Tahtamouni, L., Abdalla, M. (2010). 2DG enhances the susceptibility of breast cancer cells to doxorubicin. Cent Eur J Biol 5:739-748.
3. Alakhova, D. Y., Rapoport, N. Y., Batrakova, E. V., Timoshin, A. A., Li, S., Nicholls, D., et al. (2010). Diferential metabolic responses to pluronic in MDR and non-MDR cells: a novel pathway for chemosensitization of drug resistant cancers. J Control Release 142:89-100.
4. Albright, C. F., Graciani, N., Han, W., Yue, E., Stein, R., Lai, Z., et al. (2005). Matrix metalloproteinase-activated doxorubicin prodrugs inhibit HT1080 xenograft growth better than doxorubicin with less toxicity. Mol Cancer Ter 4:751-760. (Pubitemid 40767119)
5. Anbharasi, V., Cao, N., Feng, S. S. (2010). Doxorubicin conjugated to D-alpha-tocopheryl polyethylene glycol succinate and folic acid as a prodrug for targeted chemotherapy. J Biomed Mater Res A 94A:730-743.
6. Appleyard, M. V., O'Neill, M. A., Murray, K. E., Paulin, F. E., Bray, S. E., Kernohan, N. M., et al. (2009). Seliciclib (CYC202, R-roscovitine) enhances the antitumor efect of doxorubicin in vivo in a breast cancer xenograft model. Int J Cancer 124:465-472.
7. Aroui, S., Brahim, S., De Waard, M., Breard, J., Kenani, A. (2009). Efcient induction of apoptosis by doxorubicin coupled to cell-penetrating peptides compared to unconjugated doxorubicin in the human breast cancer cell line MDA-MB 231. Cancer Lett 285:28-38.
8. Aroui, S., Brahim, S., De Waard, M., Kenani, A. (2010). Cytotoxicity, intracellular distribution, and uptake of doxorubicin and doxorubicin coupled to cell-penetrating peptides in diferent cell lines: a comparative study. Biochem Biophys Res Commun 391:419-425.
9. Arpino, G., Ciocca, D. R., Weiss, H., Allred, D. C., Daguerre, P., Vargas-Roig, L., et al. (2005). Predictive value of apoptosis, proliferation, HER-2, and topoisomerase IIalpha for anthracycline chemotherapy in locally advanced breast cancer. Breast Cancer Res Treat 92:69-75. (Pubitemid 40875080)
10. Ax, W., Soldan, M., Koch, L., Maser, E. (2000). Development of daunorubicin resistance in tumour cells by induction of carbonyl reduction. Biochem Pharmacol 59:293-300. (Pubitemid 30001756)
11. Bains, O. S., Karkling, M. J., Grigliatti, T. A., Reid, R. E., Riggs, K. W. (2009). Two nonsynonymous single nucleotide polymorphisms of human carbonyl reductase 1 demonstrate reduced in vitro metabolism of daunorubicin and doxorubicin. Drug Metab Dispos 37:1107-1114.
12. Batist, G., Ramakrishnan, G., Rao, C. S., Chandrasekharan, A., Gutheil, J., Guthrie, T., et al. (2001). Reduced cardiotoxicity and preserved antitumor efcacy of liposome-encapsulated doxorubicin and cyclophosphamide compared with conventional doxorubicin and cyclophosphamide in a randomized, multicenter trial of metastatic breast cancer. J Clin Oncol 19:1444-1454. (Pubitemid 32202552)
13. Batrakova, E. V., Li, S., Brynskikh, A. M., Sharma, A. K., Li, Y., Boska, M., et al. (2010). Effects of pluronic and doxorubicin on drug uptake, cellular metabolism, apoptosis, and tumor inhibition in animal models of MDR cancers. J Control Release 143:290-301.
14. Bertheau, P., Plassa, F., Espie, M., Turpin, E., de Roquancourt, A., Marty, M., et al. (2002). Efect of mutated TP53 on response of advanced breast cancers to high-dose chemotherapy. Lancet 360:852-854. (Pubitemid 35257951)
15. Biesalski, H. K., Frank, J. (2003). Antioxidants in cancer therapy: is there a rationale to recommend antioxidants during cancer therapy? Biofactors 17:229-240. (Pubitemid 37267157)
16. Binaschi, M., Bigioni, M., Cipollone, A., Rossi, C., Goso, C., Maggi, C. A., et al. (2001). Anthracyclines: selected new developments. Curr Med Chem Anticancer Agents 1:113-130.
17. Bisi, A., Meli, M., Gobbi, S., Rampa, A., Tolomeo, M., Dusonchet, L. (2008). Multidrug resistance reverting activity and antitumor profle of new phenothiazine derivatives. Bioorg Med Chem 16:6474-6482. (Pubitemid 351794257)
18. Blanco, J. G., Leisenring, W. M., Gonzalez-Covarrubias, V. M., Kawashima, T. I., Davies, S. M., Relling, M. V., et al. (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. (Pubitemid 351969225)
19. Borst, P., Jonkers, J., Rottenberg, S. (2007). What makes tumors multidrug resistant? Cell Cycle 6: 2782-2787. (Pubitemid 350277170)
20. Brooks, T. A., O'Loughlin, K. L., Minderman, H., Bundy, B. N., Ford, L. A., Vredenburg, M. R., et al. (2007). Te 4'-O-benzylated doxorubicin analog WP744 overcomes resistance mediated by P-glycoprotein, multidrug resistance protein, and breast cancer resistance protein in cell lines and acute myeloid leukemia cells. Invest New Drugs 25:115-122. (Pubitemid 46020869)
21. Brozic, P., Golob, B., Gomboc, N., Rizner, T. L., Gobec, S. (2006). Cinnamic acids as new inhibitors of 17beta-hydroxysteroid dehydrogenase type 5 (AKR1C3). Mol Cell Endocrinol 248:233-235.
22. Cao, N., Feng, S. S. (2008). Doxorubicin conjugated to D-alpha-tocopheryl polyethylene glycol 1000 succinate (TPGS): conjugation chemistry, characterization, in vitro and in vivo evaluation. Biomaterials 29:3856-3865.
23. Carlquist, M., Frejd, T., Gorwa-Grauslund, M. F. (2008). Flavonoids as inhibitors of human carbonyl reductase 1. Chem Biol Interact 174:98-108.
24. Carta, A., Piras, S., Paglietti, G., Pricl, S., La, C. P., Busonera, B., et al. (2008). 2(3)-Aryl-thio(oxy)-methylquinoxaline derivatives: a new class of P-glycoprotein-mediated drug efux inhibitors. Med Chem 4:194-205. (Pubitemid 351827293)
25. Carvalho, C., Santos, R. X., Cardoso, S., Correia, S., Oliveira, P. J., Santos, M. S., et al. (2009). Doxorubicin: the good, the bad, and the ugly efect. Curr Med Chem 16:3267-3285.
26. Chearwae, W., Shukla, S., Limtrakul, P., Ambudkar, S. V. (2006). Modulation of the function of the multidrug resistance-linked ATP-binding cassette transporter ABCG2 by the cancer chemopreventive agent curcumin. Mol Cancer Ter 5:1995-2006. (Pubitemid 44336571)
27. Chen, Y., Jungsuwadee, P., Vore, M., Butterfeld, D. A., St.Clair, D. K. (2007). Collateral damage in cancer chemotherapy: oxidative stress in nontargeted tissues. Mol Interv 7:147-156. (Pubitemid 47026725)
28. Cheng, X., Gao, F., Xiang, J., Jiang, X., Chen, J., Zhang, J. (2011). Galactosylated alpha,beta-poly[(2-hydroxyethyl)-L-aspartamide]-bound doxorubicin: improved antitumor activity against hepatocellular carcinoma with reduced hepatotoxicity. Anticancer Drugs 22:136-147.
29. Choi, J. Y., Nowell, S. A., Blanco, J. G., Ambrosone, C. B. (2006). Te role of genetic variability in drug metabolism pathways in breast cancer prognosis. Pharmacogenomics 7:613-624. (Pubitemid 43891417)
30. Church, S. L., Grant, J. W., Ridnour, L. A., Oberley, L. W., Swanson, P. E., Meltzer, P. S., et al. (1993). Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Natl Acad Sci USA 90:3113-3117. (Pubitemid 23113568)
31. Clementi, M. E., Giardina, B., Di, S. E., Mordente, A., Misiti, F. (2003). Doxorubicin-derived metabolites induce release of cytochrome C and inhibition of respiration on cardiac isolated mitochondria. Anticancer Res 23:2445-2450. (Pubitemid 36897113)
32. Conklin, K. A. (2004). Cancer chemotherapy and antioxidants. J Nutr 134:3201S-3204S. (Pubitemid 39470116)
33. Crivellari, D., Lombardi, D., Spazzapan, S., Veronesi, A., Tofoli, G. (2004). New oral drugs in older patients: a review of idarubicin in elderly patients. Crit Rev Oncol Hematol 49:153-163. (Pubitemid 38175441)
34. Dai, C. L., Liang, Y. J., Chen, L. M., Zhang, X., Deng, W. J., Su, X. D., et al. (2009a). Sensitization of ABCB1 overexpressing cells to chemotherapeutic agents by FG020326 via binding to ABCB1 and inhibiting its function. Biochem Pharmacol 78:355-364.
35. Dai, C. L., Liang, Y. J., Wang, Y. S., Tiwari, A. K., Yan, Y. Y., Wang, F., et al. (2009b). Sensitization of ABCG2-overexpressing cells to conventional chemotherapeutic agent by sunitinib was associated with inhibiting the function of ABCG2. Cancer Lett 279:74-83.
36. Das, A., Durrant, D., Mitchell, C., Mayton, E., Hoke, N. N., Salloum, F. N., et al. (2010). Sildenafl increases chemotherapeutic efcacy of doxorubicin in prostate cancer and ameliorates cardiac dysfunction. Proc Natl Acad Sci USA 107:18202-18207.
37. Derdak, Z., Mark, N. M., Beldi, G., Robson, S. C., Wands, J. R., Bafy, G. (2008). Te mitochondrial uncoupling protein-2 promotes chemoresistance in cancer cells. Cancer Res 68:2813-2819. (Pubitemid 351556280)
38. Di, L. A., Isola, J. (2003). Topoisomerase II alpha as a marker predicting the efcacy of anthracyclines in breast cancer: are we at the end of the beginning? Clin Breast Cancer 4:179-186. (Pubitemid 37185053)
39. Doroshow, J. H. (1986). Prevention of doxorubicin-induced killing of MCF-7 human breast cancer cells by oxygen radical scavengers and iron chelating agents. Biochem Biophys Res Commun 135:330-335. (Pubitemid 16064007)
40. Duan, Z., Choy, E., Hornicek, F. J. (2009). NSC23925, identifed in a high-throughput cell-based screen, reverses multidrug resistance. PLoS One 4:e7415.
41. Dunkern, T. R., Wedemeyer, I., Baumgartner, M., Fritz, G., Kaina, B. (2003). Resistance of p53 knockout cells to doxorubicin is related to reduced formation of DNA strand breaks rather than impaired apoptotic signaling. DNA Repair (Amst) 2:49-60. (Pubitemid 35435438)
42. Elan Pharmaceuticals Myocet. (2000). Elan gains European approval for Myocet. Te Pharma Letter August 2.
43. Emons, G., Kaufmann, M., Gorchev, G., Tsekova, V., Grundker, C., Gunthert, A. R., et al. (2010). Dose escalation and pharmacokinetic study of AEZS-108 (AN-152), an LHRH agonist linked to doxorubicin, in women with LHRH receptor-positive tumors. Gynecol Oncol 119:457-461.
44. Erlund, I., Silaste, M. L., Alfthan, G., Rantala, M., Kesaniemi, Y. A., Aro, A. (2002). Plasma concentrations of the favonoids hesperetin, naringenin, and quercetin in human subjects following their habitual diets, and diets high or low in fruit and vegetables. Eur J Clin Nutr 56:891-898.
45. Estrela, J. M., Ortega, A., Obrador, E. (2006). Glutathione in cancer biology and therapy. Crit Rev Clin Lab Sci 43:143-181. (Pubitemid 43860449)
46. Ferreira, A. L., Matsubara, L. S., Matsubara, B. B. (2008). Anthracycline-induced cardiotoxicity. Cardiovasc Hematol Agents Med Chem 6:278-281.
47. Fisher, P. W., Salloum, F., Das, A., Hyder, H., Kukreja, R. C. (2005). Phosphodiesterase-5 inhibition with sildenafl attenuates cardiomyocyte apoptosis and left ventricular dysfunction in a chronic model of doxorubicin cardiotoxicity. Circulation 111:1601-1610. (Pubitemid 40525159)
48. Florent, J. C., Monneret, C. (2008). Doxorubicin conjugates for selective delivery to tumors. In: Krohn, K. (Ed.), Anthracycline chemistry and biology II (pp. 99-140). Heidelberg, Germany: Springer Berlin.
49. Fruttero, R., Crosetti, M., Chegaev, K., Guglielmo, S., Gasco, A., Berardi, F., et al. (2010). Phenylsulfonylfuroxans as modulators of multidrug-resistance-associated protein-1 and P-glycoprotein. J Med Chem 53:5467-5475.
50. Gandhi, L., Harding, M. W., Neubauer, M., Langer, C. J., Moore, M., Ross, H. J., et al. (2007). A phase II study of the safety and efcacy of the multidrug resistance inhibitor VX-710 combined with doxorubicin and vincristine in patients with recurrent small cell lung cancer. Cancer 109:924-932. (Pubitemid 46333534)
51. Gavelova, M., Hladikova, J., Vildova, L., Novotna, R., Vondracek, J., Krcmar, P., et al. (2008). Reduction of doxorubicin and oracin and induction of carbonyl reductase in human breast carcinoma MCF-7 cells. Chem Biol Interact 176:9-18.
52. Gebauer, G., Fehm, T., Beck, E. P., Berkholz, A., Licht, P., Jager, W. (2003). Cytotoxic efect of conjugates of doxorubicin and human chorionic gonadotropin (hCG) in breast cancer cells. Breast Cancer Res Treat 77:125-131. (Pubitemid 36197613)
53. Gersl, V., Mazurova, Y., Bajgar, J., Melka, M., Hrdina, R., Palicka, V. (1996). Lack of cardiotoxicity of a new antineoplastic agent, a synthetic derivative of indenoisochinoline: comparison with daunorubicin in rabbits. Arch Toxicol 70:645-651. (Pubitemid 26258632)
54. Gewirtz, D. A. (1999). A critical evaluation of the mechanisms of action proposed for the antitumor efects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 57:727-741. (Pubitemid 29094544)
55. Gonzalez-Covarrubias, V., Kalabus, J. L., Blanco, J. G. (2008). Inhibition of polymorphic human carbonyl reductase 1 (CBR1) by the cardioprotectant favonoid 7-monohydroxyethyl rutoside (monoHER). Pharm Res 25:1730-1734.
56. Greco, F., Vicent, M. J., Gee, S., Jones, A. T., Gee, J., Nicholson, R. I., et al. (2007). Investigating the mechanism of enhanced cytotoxicity of HPMA copolymer-Dox-AGM in breast cancer cells. J Control Release 117:28-39. (Pubitemid 46164864)
57. Greco, F., Vicent, M. J., Penning, N. A., Nicholson, R. I., Duncan, R. (2005). HPMA copolymer-aminoglutethimide conjugates inhibit aromatase in MCF-7 cell lines. J Drug Target 13:459-470. (Pubitemid 43347843)
58. Green, P. S., Leeuwenburgh, C. (2002). Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim Biophys Acta 1588:94-101.
59. Gruber, R., van Haarlem, L. J., Warnaar, S. O., Holz, E., Riethmuller, G. (2000). The human antimouse immunoglobulin response and the anti-idiotypic network have no influence on clinical outcome in patients with minimal residual colorectal cancer treated with monoclonal antibody CO17-1A. Cancer Res 60:1921-1926. (Pubitemid 30207653)
60. Grundker, C., Gunthert, A. R., Westphalen, S., Emons, G. (2002). Biology of the gonadotropin-releasing hormone system in gynecological cancers. Eur J Endocrinol 146:1-14. (Pubitemid 34126412)
61. Guano, F, Pourquier, P, Tinelli, S, Binaschi, M, Bigioni, M, Animati, F, et al. (1999). Topoisomerase poisoning activity of novel disaccharide anthracyclines. Mol Pharmacol 56:77-84. (Pubitemid 29309814)
62. Gunthert, A. R., Grundker, C., Bongertz, T., Nagy, A., Schally, A. V., Emons, G. (2004). Induction of apoptosis by AN-152, a cytotoxic analog of luteinizing hormone-releasing hormone (LHRH), in LHRH-R positive human breast cancer cells is independent of multidrug resistance-1 (MDR-1) system. Breast Cancer Res Treat 87:255-264. (Pubitemid 39505942)
63. Hanusova, V., Kralova, V., Schroterova, L., Trilecova, L., Pakostova, A., Skalova, L. (2010). Te efectiveness of oracin in enhancing the cytotoxicity of doxorubicin through the inhibition of doxorubicin deactivation in breast cancer MCF7 cells. Xenobiotica 40:681-690.
64. Harris, L., Batist, G., Belt, R., Rovira, D., Navari, R., Azarnia, N., et al. (2002). Liposome-encapsulated doxorubicin compared with conventional doxorubicin in a randomized multicenter trial as frst-line therapy of metastatic breast carcinoma. Cancer 94:25-36. (Pubitemid 34049039)
65. Indermaur, M. D., Xiong, Y., Kamath, S. G., Boren, T., Hakam, A, Wenham, R. M., et al. (2010). Genomic-directed targeted therapy increases endometrial cancer cell sensitivity to doxorubicin. Am J Obstet Gynecol 203:158.e1-158.e40.
66. Inoue, A., Narumi, K., Matsubara, N., Sugawara, S., Saijo, Y., Satoh, K., et al. (2000). Administration of wild-type p53 adenoviral vector synergistically enhances the cytotoxicity of anti-cancer drugs in human lung cancer cells irrespective of the status of p53 gene. Cancer Lett 157:105-112. (Pubitemid 30421238)
67. Janssens, J. P., Russo, J., Russo, I., Michiels, L., Donders, G., Verjans, M., et al. (2007). Human chorionic gonadotropin (hCG) and prevention of breast cancer. Mol Cell Endocrinol 269:93-98. (Pubitemid 46483827)
68. Kaiserova, H., Simunek, T., van der Vijgh, W. J., Bast, A., Kvasnickova, E. (2007). Flavonoids as protectors against doxorubicin cardiotoxicity: role of iron chelation, antioxidant activity, and inhibition of carbonyl reductase. Biochim Biophys Acta 1772:1065-1074. (Pubitemid 47314227)
69. Kassner, N., Huse, K., Martin, H. J., Godtel-Armbrust, U., Metzger, A., Meineke, I., et al. (2008). Carbonyl reductase 1 is a predominant doxorubicin reductase in the human liver. Drug Metab Dispos 36:2113-2120.
70. Kattan, Z., Minig, V., Leroy, P., Dauca, M., Becuwe, P. (2008). Role of manganese superoxide dismutase on growth and invasive properties of human estrogen-independent breast cancer cells. Breast Cancer Res Treat 108:203-215. (Pubitemid 351311363)
71. Kim, B., Choi, Y., Lee, Y., Joe, Y., Hong, S. (2010). N,N-Dimethyl phytosphingosine sensitizes HL-60/MX2, a multidrug-resistant variant of HL-60 cells, to doxorubicin-induced cytotoxicity through ROS-mediated release of cytochrome c and AIF. Apoptosis 15:982-993.
72. Kim, J. H., Chae, M., Kim, W. K., Kim, Y. J., Kang, H. S., Kim, H. S., et al. (2011). Salinomycin sensitizes cancer cells to the efects of doxorubicin and etoposide treatment by increasing DNA damage and reducing p21 protein. Br J Pharmacol 162:773-784.
73. Koka, S., Das, A., Zhu, S. G., Durrant, D., Xi, L., Kukreja, R. C. (2010). Long-acting phosphodiesterase-5 inhibitor tadalafl attenuates doxorubicin-induced cardiomyopathy without interfering with chemotherapeutic efect. J Pharmacol Exp Ter 334:1023-1030.
74. Kratz, F. (2008). Acid-sensitive prodrugs of doxorubicin. In: Krohn, K. (Ed.), Anthracycline chemistry and biology II (pp. 73-97). Heidelberg, Germany: Springer Berlin.
75. Krebs, L. J., Wang, X., Nagy, A., Schally, A. V., Prasad, P. N., Liebow, C. (2002). A conjugate of doxorubicin and an analog of luteinizing hormone-releasing hormone shows increased efcacy against oral and laryngeal cancers. Oral Oncol 38:657-663.
76. Krebs, L. J., Wang, X., Pudavar, H. E., Bergey, E. J., Schally, A. V., Nagy, A., et al. (2000). Regulation of targeted chemotherapy with cytotoxic lutenizing hormone-releasing hormone analogue by epidermal growth factor. Cancer Res 60:4194-4199. (Pubitemid 30636604)
77. Krishna, R., Mayer, L. D. (1999). Te use of liposomal anticancer agents to determine the roles of drug pharmacodistribution and P-glycoprotein (PGP) blockade in overcoming multidrug resistance (MDR). Anticancer Res 19:2885-2891. (Pubitemid 30042567)
78. Kuijper, T. M., Ruigrok-Ritstier, K., Verhoef-Post, M., Piersma, D., Bruysters, M. W., Berns, E. M., et al. (2009). LH receptor gene expression is essentially absent in breast tumor tissue: implications for treatment. Mol Cell Endocrinol 302:58-64.
79. Kuninaka, S., Ichinose, Y., Koja, K., Toh, Y. (2000). Suppression of manganese superoxide dismutase augments sensitivity to radiation, hyperthermia and doxorubicin in colon cancer cell lines by inducing apoptosis. Br J Cancer 83:928-934.
80. Kweon, S. H., Song, J. H., Kim, T. S. (2010). Resveratrol-mediated reversal of doxorubicin resistance in acute myeloid leukemia cells via downregulation of MRP1 expression. Biochem Biophys Res Commun 395:104-110.
81. Lage, H., Dietel, M. (2002). Multiple mechanisms confer diferent drug-resistant phenotypes in pancreatic carcinoma cells. J Cancer Res Clin Oncol 128:349-357. (Pubitemid 34824176)
82. Lage, H., Helmbach, H., Dietel, M., Schadendorf, D. (2000). Modulation of DNA topoisomerase II activity and expression in melanoma cells with acquired drug resistance. Br J Cancer 82:488-491. (Pubitemid 30045402)
83. Lal, S., Sandanaraj, E., Wong, Z. W., Ang, P. C., Wong, N. S., Lee, E. J., et al. (2008a). CBR1 and CBR3 pharmacogenetics and their infuence on doxorubicin disposition in Asian breast cancer patients. Cancer Sci 99:2045-2054.
84. Lal, S., Wong, Z. W., Sandanaraj, E., Xiang, X., Ang, P. C., Lee, E. J., et al. (2008b). Infuence of ABCB1 and ABCG2 polymorphisms on doxorubicin disposition in Asian breast cancer patients. Cancer Sci 99:816-823. (Pubitemid 351448088)
85. Leonard, R. C., Williams, S., Tulpule, A., Levine, A. M., Oliveros, S. (2009). Improving the therapeutic index of anthracycline chemotherapy: focus on liposomal doxorubicin (Myocet). Breast 18:218-224.
86. Liang, G., Tang, A., Lin, X., Li, L., Zhang, S., Huang, Z., et al. (2010). Green tea catechins augment the antitumor activity of doxorubicin in an in vivo mouse model for chemoresistant liver cancer. Int J Oncol 37:111-123.
87. Liang, J. F., Yang, V. C. (2005). Synthesis of doxorubicin-peptide conjugate with multidrug resistant tumor cell killing activity. Bioorg Med Chem Lett 15:5071-5075. (Pubitemid 41400186)
88. Lin, X., Zhang, F., Bradbury, C. M., Kaushal, A., Li, L., Spitz, D. R., et al. (2003). 2-Deoxy-D-glucose-induced cytotoxicity and radiosensitization in tumor cells is mediated via disruptions in thiol metabolism. Cancer Res 63:3413-3417. (Pubitemid 36735902)
89. Liscovitch, M., Lavie, Y. (2002). Cancer multidrug resistance: a review of recent drug discovery research. IDrugs 5:349-355. (Pubitemid 38133051)
90. Liu, J. H., Cao, L., Luo, P. G., Yang, S. T., Lu, F., Wang, H., et al. (2010). Fullerene-conjugated doxorubicin in cells. ACS Appl Mater Interfaces 2:1384-1389.
91. Lopez de Cerain, A., Marin, A., Idoate, M. A., Tunon, M. T., Bello, J. (1999). Carbonyl reductase and NADPH cytochrome P450 reductase activities in human tumoral versus normal tissues. Eur J Cancer 35:320-324. (Pubitemid 29136786)
92. Louis, M., Rosato, R. R., Battaglia, E., Neguesque, A., Lapotre, A., Grant, S., et al. (2005). Modulation of sensitivity to doxorubicin by the histone deacetylase inhibitor sodium butyrate in breast cancer cells. Int J Oncol 26:1569-1574.
93. Lu, F., Haque, S. A., Yang, S. T., Luo, P. G., Gu, L., Kitaygorodskiy, A., et al. (2009). Aqueous compatible fullerene-doxorubicin conjugates. J Phys Chem C Nanomater Interfaces 113:17768-17773.
94. Lutsenko, S. V., Feldman, N. B., Gumanov, S. G., Rodina, A. V., Severin, S. E. (2000). Cytotoxic activity, accumulation, and intracellular distribution of anthracycline antibiotics and their conjugates with the epidermal growth factor in sensitive and resistant MCF-7 cells. Biochemistry (Mosc.) 65:1299-1304.
95. Lutsenko, S. V., Feldman, N. B., Severin, S. E. (2002). Cytotoxic and antitumor activities of doxorubicin conjugates with the epidermal growth factor and its receptor-binding fragment. J Drug Target 10:567-571. (Pubitemid 36124355)
96. MacGrogan, G., Rudolph, P., Mascarel Id, I., Mauriac, L., Durand, M., Avril, A., et al. (2003). DNA topoisomerase IIalpha expression and the response toprimary chemotherapy in breast cancer. Br J Cancer 89:666-671. (Pubitemid 37076170)
97. Maeda, D. Y., Mahajan, S. S., Atkins, W. M., Zebala, J. A. (2006). Bivalent inhibitors of glutathione S-transferase: the efect of spacer length on isozyme selectivity. Bioorg Med Chem Lett 16:3780-3783. (Pubitemid 44137245)
98. Mahajan, S., Atkins, W. M. (2005). Te chemistry and biology of inhibitors and pro-drugs targeted to glutathione S-transferases. Cell Mol Life Sci 62:1221-1233.
99. Maheo, K., Vibet, S., Steghens, J. P., Dartigeas, C., Lehman, M., Bougnoux, P.,. et al(2005). Diferential sensitization of cancer cells to doxorubicin by DHA: a role for lipoperoxidation. Free Radic Biol Med 39:742-751. (Pubitemid 41139889)
100. Mailloux, R. J., Adjeitey, C. N., Harper, M. E. (2010). Genipin-induced inhibition of uncoupling protein-2 sensitizes drug-resistant cancer cells to cytotoxic agents. PLoS One 5:e13289.
101. Mi, Y. J., Liang, Y. J., Huang, H. B., Zhao, H. Y., Wu, C. P., Wang, F., et al. (2010). Apatinib (YN968D1) reverses multidrug resistance by inhibiting the efux function of multiple ATP-binding cassette transporters. Cancer Res 70:7981-7991.
102. Minotti, G., Menna, P., Salvatorelli, E., Cairo, G., Gianni, L. (2004). Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56:185-229. (Pubitemid 38720829)
103. Mitra, S., Gaur, U., Ghosh, P. C., Maitra, A. N. (2001). Tumour targeted delivery of encapsulated dextran-doxorubicin conjugate using chitosan nanoparticles as carrier. J Control Release 74:317-323. (Pubitemid 32727639)
104. Mordente, A., Minotti, G., Martorana, G. E., Silvestrini, A., Giardina, B., Meucci, E. (2003). Anthracycline secondary alcohol metabolite formation in human or rabbit heart: biochemical aspects and pharmacologic implications. Biochem Pharmacol 66:989-998. (Pubitemid 37086708)
105. Moriya, T., Suzuki, T., Pilichowska, M., Ariga, N., Kimura, N., Ouchi, N., et al. (2001). Immunohistochemical expression of gonadotropin releasing hormone receptor in human breast carcinoma. Pathol Int 51:333-337. (Pubitemid 32589020)
106. Nagy, A., Schally, A. V. (2005). Targeting of cytotoxic luteinizing hormone-releasing hormone analogs to breast, ovarian, endometrial, and prostate cancers. Biol Reprod 73:851-859. (Pubitemid 41507486)
107. Nagy, A., Schally, A. V., Armatis, P., Szepeshazi, K., Halmos, G., Kovacs, M., et al. (1996). Cytotoxic analogs of luteinizing hormone-releasing hormone containing doxorubicin or 2-pyrrolinodoxorubicin, a derivative 500-1000 times more potent. Proc Natl Acad Sci USA 93:7269-7273. (Pubitemid 26243538)
108. Ng, R., Better, N., Green, M. D. (2006). Anticancer agents and cardiotoxicity. Semin Oncol 33:2-14. (Pubitemid 43214484)
109. Ozben, T. (2006). Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Lett 580:2903-2909. (Pubitemid 43729172)
110. Patanasethanont, D., Nagai, J., Matsuura, C., Fukui, K., Sutthanut, K., Sripanidkulchai, B. O., et al. (2007). Modulation of function of multidrug resistance associated-proteins by Kaempferia parvifora extracts and their components. Eur J Pharmacol 566:67-74. (Pubitemid 46782813)
111. Penault-Llorca, F., Cayre, A., Bouchet Mishellany, F., Amat, S., Feillel, V., Le Bouedec, G., et al. (2003). Induction chemotherapy for breast carcinoma: predictive markers and relation with outcome. Int J Oncol 22:1319-1325.
112. Perego, P., Corna, E., De Cesare, M., Gatti, L., Polizzi, D., Pratesi, G., et al. (2001). Role of apoptosis and apoptosis-related genes in cellular response and antitumor efcacy of anthracyclines. Curr Med Chem 8:31-37.
113. Quan, Z. W., Yang, Y., Li, J. Y., Gong, W., Qin, Y. Y., Li, S. G. (2010). Te mechanisms of somatostatin induced enhanced chemosensitivity of gallbladder cancer cell line to doxorubicin: cell cycle modulation plus target enzyme up-regulation. Biomed Pharmacother 64:451-457.
114. Ramachandran, C., Samy, T. S., Huang, X. L., Yuan, Z. K., Krishan, A. (1993). Doxorubicin-induced DNA breaks, topoisomerase II activity, and gene expression in human melanoma cells. Biochem Pharmacol 45:1367-1371. (Pubitemid 23098338)
115. Ravid, A., Rocker, D., Machlenkin, A., Rotem, C., Hochman, A., Kessler-Icekson, G., et al. (1999). 1,25-Dihydroxyvitamin D3 enhances the susceptibility of breast cancer cells to doxorubicin-induced oxidative damage. Cancer Res 59:862-867. (Pubitemid 29086740)
116. Ravizza, R., Gariboldi, M. B., Molteni, R., Monti, E. (2008). Linalool, a plant-derived monoterpene alcohol, reverses doxorubicin resistance in human breast adenocarcinoma cells. Oncol Rep 20:625-630.
117. Robert, N. J., Vogel, C. L., Henderson, I. C., Sparano, J. A., Moore, M. R., Silverman, P., et al. (2004). Te role of the liposomal anthracyclines and other systemic therapies in the management of advanced breast cancer. Semin Oncol 31:106-146. (Pubitemid 40023244)
118. Rooseboom, M., Commandeur, J. N., Vermeulen, N. P. (2004). Enzyme-catalyzed activation of anticancer prodrugs. Pharmacol Rev 56:53-102. (Pubitemid 38314580)
119. Ruiz-Ruiz, C., Robledo, G., Cano, E., Redondo, J. M., Lopez-Rivas, A. (2003). Characterization of p53-mediated up-regulation of CD95 gene expression upon genotoxic treatment in human breast tumor cells. J Biol Chem 278:31667-31675. (Pubitemid 37048345)
120. Ruzza, P., Rosato, A., Rossi, C. R., Floreani, M., Quintieri, L. (2009). Glutathione transferases as targets for cancer therapy. Anticancer Agents Med Chem 9:763-777.
121. Sadzuka, Y., Hatakeyama, H., Sonobe, T. (2010). Enhancement of doxorubicin concentration in the M5076 ovarian sarcoma cells by cucurbitacin E co-treatment. Int J Pharm 383:186-191.
122. Schally, A. V., Nagy, A. (2002). New approaches to treatment of various cancers based on cytotoxic analogs of LHRH, somatostatin, and bombesin. Life Sci 72:2305-2320. (Pubitemid 36287676)
123. Schimmel, K. J., Richel, D. J., van den Brink, R. B., Guchelaar, H. J. (2004). Cardiotoxicity of cytotoxic drugs. Cancer Treat Rev 30:181-191. (Pubitemid 38418056)
124. Sereno, M., Brunello, A., Chiappori, A., Barriuso, J., Casado, E., Belda, C., et al. (2008). Cardiac toxicity: old and new issues in anti-cancer drugs. Clin Transl Oncol 10:35-46.
125. Shi, L. X., Ma, R., Lu, R., Xu, Q., Zhu, Z. F., Wang, L., et al. (2008). Reversal efect of tyroservatide (YSV) tripeptide on multi-drug resistance in resistant human hepatocellular carcinoma cell line BEL-7402/5-FU. Cancer Lett 269:101-110.
126. Simunek, T., Sterba, M., Popelova, O., Adamcova, M., Hrdina, R., Gersl, V. (2009). Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep 61:154-171.
127. Sinha, B. K., Katki, A. G., Batist, G., Cowan, K. H., Myers, C. E. (1987a). Adriamycin-stimulated hydroxyl radical formation in human breast tumor cells. Biochem Pharmacol 36:793-796. (Pubitemid 17038019)
128. Sinha, B. K., Katki, A. G., Batist, G., Cowan, K. H., Myers, C. E. (1987b). Diferential formation of hydroxyl radicals by adriamycin in sensitive and resistant MCF-7 human breast tumor cells: implications for the mechanism of action. Biochemistry 26:3776-3781. (Pubitemid 17127450)
129. Sinha, B. K., Mimnaugh, E. G., Rajagopalan, S., Myers, C. E. (1989). Adriamycin activation and oxygen free radical formation in human breast tumor cells: protective role of glutathione peroxidase in adriamycin resistance. Cancer Res 49:3844-3848. (Pubitemid 19197408)
130. Slaninova, I., Brezinova, L., Koubikova, L., Slanina, J. (2009). Dibenzocyclooctadiene lignans overcome drug resistance in lung cancer cells-study of structure-activity relationship. Toxicol In Vitro 23:1047-1054.
131. Sparano, J. A., Winer, E. P. (2001). Liposomal anthracyclines for breast cancer. Semin Oncol 28:32-40. (Pubitemid 32879937)
132. Stearns, V., Singh, B., Tsangaris, T., Crawford, J. G., Novielli, A., Ellis, M. J., et al. (2003). A prospective randomized pilot study to evaluate predictors of response in serial core biopsies to single agent neoadjuvant doxorubicin or paclitaxel for patients with locally advanced breast cancer. Clin Cancer Res 9:124-133. (Pubitemid 36109724)
133. Swenson, K. K., Sladek, M. L., Lally, R. M., Tuttle, T. M. (2001). Educating patients on sentinel lymph node dissection for breast cancer. Cancer Pract 9:92-96. (Pubitemid 32220617)
134. Tan, M. L., Choong, P. F., Dass, C. R. (2009). Review: doxorubicin delivery systems based on chitosan for cancer therapy. J Pharm Pharmacol 61:131-142.
135. Tanaka, M., Bateman, R., Rauh, D., Vaisberg, E., Ramachandani, S., Zhang, C., et al. (2005). An unbiased cell morphology-based screen for new, biologically active small molecules. PLoS Biol 3:e128.
136. Tao, L. Y., Liang, Y. J., Wang, F., Chen, L. M., Yan, Y. Y., Dai, C. L., et al. (2009). Cediranib (recentin, AZD2171) reverses A. Cancer Chemother Pharmacol 64:961-969.
137. Teodoulou, M., Hudis, C. (2004). Cardiac profles of liposomal anthracyclines: greater cardiac safety versus conventional doxorubicin? Cancer 100:2052-2063. (Pubitemid 38580322)
138. Tieva, A., Stattin, P., Wikstrom, P., Bergh, A., Damber, J. E. (2001). Gonadotropin-releasing hormone receptor expression in the human prostate. Prostate 47:276-284. (Pubitemid 32521747)
139. Vaclavikova, R., Kondrova, E., Ehrlichova, M., Boumendjel, A., Kovar, J., Stopka, P., et al. (2008). Te efect of favonoid derivatives on doxorubicin transport and metabolism. Bioorg Med Chem 16:2034-2042. (Pubitemid 351226568)
140. Veitch, Z. W., Guo, B., Hembruf, S. L., Bewick, A. J., Heibein, A. D., Eng, J., et al. (2009). Induction of 1C aldoketoreductases and other drug dose-dependent genes upon acquisition of anthracycline resistance. Pharmacogenet Genomics 19:477-488.
141. Viale, P. H., Yamamoto, D. S. (2008). Cardiovascular toxicity associated with cancer treatment. Clin J Oncol Nurs 12:627-638.
142. Vibet, S., Goupille, C., Bougnoux, P., Steghens, J. P., Gore, J., Maheo, K. (2008). Sensitization by docosahexaenoic acid (DHA) of breast cancer cells to anthracyclines through loss of glutathione peroxidase (GPx1) response. Free Radic Biol Med 44:1483-1491.
143. Vicent, M. J., Greco, F., Nicholson, R. I., Paul, A., Grifths, P. C., Duncan, R. (2005). Polymer therapeutics designed for a combination therapy of hormone-dependent cancer. Angew Chem Int Ed Engl 44:4061-4066. (Pubitemid 40886448)
144. Weiss, R. B. (1992). Te anthracyclines: will we ever fnd a better doxorubicin? Semin Oncol 19:670-686. (Pubitemid 23004844)
145. Wesolowska, O., Wisniewski, J., Sroda, K., Krawczenko, A., Bielawska-Pohl, A., Paprocka, M., et al. (2010). 8-Prenylnaringenin is an inhibitor of multidrug resistance-associated transporters, P-glycoprotein and MRP1. Eur J Pharmacol 644:32-40.
146. Yang, X, Liu, G, Li, H, Zhang, Y, Song, D, Li, C, et al. (2010). Novel oxadiazole analogues derived from ethacrynic acid: design, synthesis, and structure-activity relationships in inhibiting the activity of glutathione S-transferase P1-1 and cancer cell proliferation. J Med Chem 53:1015-1022.
147. Yeung, B. H., Wong, K. Y., Lin, M. C., Wong, C. K., Mashima, T., Tsuruo, T., et al. (2008). Chemosensitisation by manganese superoxide dismutase inhibition is caspase-9 dependent and involves extracellular signal-regulated kinase 1/2. Br J Cancer 99:283-293.
148. Zajdel, A., Wilczok, A., Latocha, M., Dzierzewicz, Z. (2011). Efect of polyunsaturated fatty acids on doxorubicin cytotoxicity in glioma cells in vitro. Adv Clin Exp Med 19:481-487.
149. Zhang, C, Peng, Y, Wang, F, Tan, X, Liu, N, Fan, S, et al. (2010a). A synthetic cantharidin analog for the enhancement of doxorubicin suppression of stem cell-derived aggressive sarcoma. Biomaterials 31:9535-9543.
150. Zhang, F., Aft, R. L. (2009). Chemosensitizing and cytotoxic efects of 2-deoxy-D-glucose on breast cancer cells. J Cancer Res Ter 5(Suppl):S41-S43.
151. Zhang, F. Y., Du, G. J., Zhang, L., Zhang, C. L., Lu, W. L., Liang, W. (2009a). Naringenin enhances the anti-tumor efect of doxorubicin through selectively inhibiting the activity of multidrug resistance-associated proteins but not P-glycoprotein. Pharm Res 26:914-925.
152. Zhang, S., Sagawa, K., Arnold, R. D., Tseng, E., Wang, X., Morris, M. E. (2010b). Interactions between the favonoid biochanin A and P-glycoprotein substrates in rats: in vitro and in vivo. J Pharm Sci 99:430-441.
153. Zhang, Y. W., Shi, J., Li, Y. J., Wei, L. (2009b). Cardiomyocyte death in doxorubicin-induced cardiotoxicity. Arch Immunol Ter Exp (Warsz.) 57:435-445.
154. Zheng, T., Wang, J., Song, X., Meng, X., Pan, S., Jiang, H., et al. (2010). Nutlin-3 cooperates with doxorubicin to induce apoptosis of human hepatocellular carcinoma cells through p53 or p73 signaling pathways. J Cancer Res Clin Oncol 136:1597-1604.
155. Zimmermann, T. J., Niesen, F. H., Pilka, E. S., Knapp, S., Oppermann, U., Maier, M. E. (2009). Discovery of a potent and selective inhibitor for human carbonyl reductase 1 from propionate scanning applied to the macrolide zearalenone. Bioorg Med Chem 17:530-536.