Kinetics of anthracycline accumulation in multidrug-resistant tumor cells: Relationship to drug lipophilicity and serum albumin binding

Biochemical Pharmacology

Volumn 56, Issue 9, 1998, Pages 1209-1217

  Demant, Erland J F ^a   Friche, Ellen ^b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b FINSEN LABORATORY   (Denmark)

Author keywords

Anthracyclines; Lipophilicity; Multidrug resistance (MDR); P glycoprotein; Serum albumin; Transport kinetics

Indexed keywords

4' IODOESORUBICIN; ANTHRACYCLINE; DAUNORUBICIN; DOXORUBICIN; DOXORUBICINOL; IDARUBICIN; SERUM ALBUMIN;

AQUEOUS SOLUTION; ARTICLE; CANCER CELL CULTURE; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DATA ANALYSIS; DRUG ACCUMULATION; DRUG PROTEIN BINDING; DRUG UPTAKE; EHRLICH ASCITES TUMOR CELL; HUMAN; HUMAN CELL; LIPOPHILICITY; MATHEMATICAL MODEL; MEMBRANE PERMEABILITY; MEMBRANE TRANSPORT; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; SIMULATION;

EID: 0031772145     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(98)00255-X     Document Type: Article

References (58)

1. Gottesman MM and Pastan I, Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 62: 385-427, 1993.
2. Rosenberg MF, Callaghan R, Ford RC and Higgins CF, Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J Biol Chem 272: 10685-10694, 1997.
3. Danø K, Active outward transport of daunomycin in resistant Ehrlich ascites tumor cells. Biochim Biophys Acta 323: 466-483, 1973.
4. Skovsgaard T, Mechanisms of resistance to daunorubicin in Ehrlich ascites tumor cells. Cancer Res 38: 1785-1791, 1978.
5. Stein WD, Kinetics of the multidrug transporter (P-glycoprotein) and its reversal. Physiol Rev 77: 545-590, 1997.
6. Danø K, Development of resistance to adriamycin (NSC-123127) in Ehrlich ascites tumor in vivo. Cancer Chemother Rep 56: 321-326, 1972.
7. Coley HM, Twentyman PR and Workman P, Improved cellular accumulation is characteristic of anthracyclines which retain high activity in multidrug-resistant cell lines, alone or in combination with verapamil or cyclosporin A. Biochem Pharmacol 24: 4467-4475, 1989.
8. Facchetti I, Grandi M, Cucchi P, Geroni C, Penco S and Vigevani A, Influence of lipophilicity on cytotoxicity of anthracyclines in LoVo and LoVo/Dx human cell lines. Anti-Cancer Drug Design 6: 385-397, 1991.
9. Mülder HS, Dekker H, Pinedo HM and Lankelma J, The P-glycoprotein-mediated relative decrease in cytosolic free drug concentration is similar for several anthracyclines with varying lipophilicity. Biochem Pharmacol 50: 967-974, 1995.
10. Lampidis TJ, Kolonias D, Podona T, Israel M, Safa AR, Lothstein L, Savaraj N, Tapiero H and Priebe W, Circumvention of P-GP MDR as a function of anthracycline lipophilicity and charge. Biochemistry 36: 2679-2685, 1997.
11. Supino R, Necco A, Dasdia T, Casazza AM and Di Marco A, Relationship between effects on nucleic acid synthesis in cell cultures and cytotoxicity of 4-demethoxy derivatives of daunorubicin and adriamycin. Cancer Res 37: 4523-4528, 1977.
12. Barbieri B, Giuliani FC, Bordoni T, Casazza AM, Geroni C, Bellini O, Suarato A, Gioia B, Penco S and Arcamone F, Chemical and biological characterization of 4′-iodo-4′-deoxydoxorubicin. Cancer Res 47: 4001-4006, 1987.
13. Rivory LP, Pond SM and Winzor DJ, The influence of pH on the interaction of lipophilic anthracyclines with bovine serum albumin. Quantitative characterization by measurements of fluorescence quenching. Biochem Pharmacol 44: 2347-2355, 1992.
14. Chassany O, Urien S, Claudepierre P, Bastian G and Tillement JP, Comparative serum protein binding of anthracycline derivatives. Cancer Chemother Pharmacol 38: 571-573, 1996.
15. Rivory LP, Avent KM and Pond SM, Effects of lipophilicity and protein binding on the hepatocellular uptake and hepatic disposition of two anthracyclines, doxorubicin and iododoxorubicin. Cancer Chemother Pharmacol 38: 439-445, 1996.
16. Demant EJF and Friche E, Equilibrium binding of anthracycline cytostatics to serum albumin and small unilamellar phospholipid vesicles as measured by gel filtration. Biochem Pharmacol 55: 27-32, 1998.
17. Friche E, Jensen PB, Roed H, Skovsgaard T and Nissen NI, In vitro circumvention of anthracycline-resistance in Ehrlich ascites tumour by anthracycline analogues. Biochem Pharmacol 39: 1721-1726, 1990.
18. Friche E, Jensen PB, Skovsgaard T and Nissen NI, Evaluation of 4′-deoxy-4′-iododoxorubicin in sensitive and multidrug-resistant Ehrlich ascites tumour. J Cell Pharmacol 1: 57-65, 1990.
19. Demant EJF, Sehested M and Jensen PB, A model for computer simulation of P-glycoprotein and transmembrane ApH-mediated anthracycline transport in multidrug-resistant tumor cells. Biochim Biophys Acta 1055: 117-125, 1990.
20. Bachur NR, Moore AL, Bernstein IG and Liu A, Tissue distribution and disposition of daunomycin (NSC-82151) in mice: fluorometric and isotopic methods. Cancer Chemother Rep 54: 89-94, 1970.
21. Skovsgaard T, Transport and binding of daunorubicin, adriamycin, and rubidazone in Ehrlich ascites tumor cells. Biochem Pharmacol 26: 215-222, 1977.
22. Tarasiuk J, Frezard F, Garnier-Suillerot A and Gattegno L, Anthracycline incorporation in human lymphocytes. Kinetics of uptake and nuclear concentrations. Biochim Biophys Acta 1013: 109-117, 1989.
23. Demant EJF and Sehested M, Recognition of anthracycline binding domains in bovine serum albumin and design of a free fatty acid sensor protein. Biochim Biophys Acta 1156: 151-160, 1993.
24. Frezard F and Garnier-Suillerot A, Determination of the osmotic active drug concentration in the cytoplasm of anthracycline-resistant and -sensitive K562 cells. Biochim Biophys Acta 1091: 29-35, 1991.
25. Ohkuma S, Use of fluorescein isothiocyanate-dextran to measure proton pumping in lysosomes and related organelles. Methods Enzymol 174: 131-154, 1989.
26. Folch J, Ascoli I, Lees M, Meath JA and LeBaron FN, Preparation of lipid extracts from brain tissue. J Biol Chem 191: 833-841, 1951.
27. 13C NMR spectroscopic study of wild-type and multidrug-resistant Ehrlich ascites tumor cells. Oncol Res 5: 119-126, 1993.
28. Skovsgaard T, Carrier-mediated transport of daunorubicin, adriamycin, and rubidazone in Ehrlich ascites tumour cells. Biochem Pharmacol 27: 1221-1227, 1978.
29. Frezard F and Garnier-Suillerot A, Comparison of the binding of anthracycline derivatives to purified DNA and to cell nuclei. Biochim Biophys Acta 1036: 121-127, 1990.
30. Dalmark M and Storm HH, A fickian diffusion transport process with features of transport catalysis. Doxorubicin transport in human red blood cells. J Gen Physiol 78: 349-364, 1981.
31. Frezard F and Garnier-Suillerot A, DNA-containing liposomes as a model for the study of cell membrane permeation by anthracycline derivatives. Biochemistry 30: 5038-5043, 1991.
32. Frezard F and Garnier-Suillerot A, Comparison of the membrane transport of anthracycline derivatives in drug-resistant and drug-sensitive K562 cells. Eur J Biochem 196: 483-491, 1991.
33. Siegfried JM, Burke TG and Tritton TR, Cellular transport of anthracyclines by passive diffusion. Implications for drug resistance. Biochem Pharmacol 34: 593-598, 1985.
34. Roepe PD, The role of the MDR protein in altered drug translocation across tumor cell membranes. Biochim Biophys Acta 1241: 385-406, 1995.
35. Cullis PR, Hope MJ, Bally MB, Madden TD, Mayer LD and Fenske DB, Influence of pH gradients on the transbilayer transport of drugs, lipids, peptides and metal ions into large unilamellar vesicles. Biochim Biophys Acta 1331: 187-211, 1997.
36. Sehested M, Skovsgaard T, Van Deurs B and Winther-Nielsen H, Increase in nonspecific adsorptive endocytosis in anthracycline- and vinca alkaloid-resistant Ehrlich ascites tumor cell lines. J Natl Cancer Inst 78: 171-179, 1987.
37. Frézard F and Garnier-Suillerot A, Permeability of lipid bilayer to anthracycline derivatives. Role of the bilayer composition and of the temperature. Biochim Biophys Acta 1389: 13-22, 1998.
38. Nielsen D, Maare C and Skovsgaard T, Influx of daunorubicin in multidrug-resistant Ehrlich ascites tumour cells: Correlation to expression of P-glycoprotein and efflux. Influence of verapamil. Biochem Pharmacol 50: 443-450, 1995.
39. Spoelstra EC, Westerhoff HV, Dekker H and Lankelma J, Kinetics of daunorubicin transport by P-glycoprotein of intact cancer cells. Eur J Biochem 207: 567-579, 1992.
40. Pereira E, Borrel MN, Fiallo M and Garnier-Suillerot A, Non-competitive inhibition of P-glycoprotein-associated efflux of THP-adriamycin by verapamil in living K562 leukemia cells. Biochim Biophys Acta 1225: 209-216, 1994.
41. Borrel MN, Fiallo M, Priebe W and Garnier-Suillerot A, P-glycoprotein-mediated efflux of hydroxyrubicin, a neutral anthracycline derivative, in resistant K562 cells. FEBS Lett 356: 287-290, 1994.
42. Ghauharali RI, Westerhoff HV, Dekker H and Lankelma J, Saturable P-glycoprotein kinetics assayed by fluorescence studies of drug efflux from suspended human KB8-5 cells. Biochim Biophys Acta 1278: 213-222, 1996.
43. Sehested M, Simpson D, Skovsgaard T and Jensen PB, Freeze-fracture study of plasma membranes of wild-type and daunorubicin-resistant Ehrlich ascites tumor and P388 leukemia cells. Virchows Arch B Cell Pathol 56: 327-335, 1989.
44. Sharom FJ, Yu X and Doige CA, Functional reconstitution of drug transport and ATPase activity in proteoliposomes containing partially purified P-glycoprotein. J Biol Chem 268: 24197-24202, 1993.
45. Urbatsch IL, Al-Shawi MK and Senior AE, Characterization of the ATPase activity of purified Chinese hamster P-glycoprotein. Biochemistry 33: 7069-7076, 1994.
46. Eksborg S, Ehrsson H and Ekqvist B, Protein binding of anthraquinone glycosides, with special reference to adriamycin. Cancer Chemother Pharmacol 10: 7-10, 1982.
47. Dalmark M and Johansen P, Molecular association between doxorubicin (adriamycin) and DNA-derived bases, nucleosides, nucleotides, other aromatic compounds, and proteins in aqueous solution. Mol Pharmacol 22: 158-165, 1982.
48. Broxterman HJ, Kuiper CM, Schuurhuis GJ, Van der Hoeven JJM, Pinedo HM and Lankelma J, Daunomycin accumulation in resistant tumor cells as a screening model for resistance-modifying drugs: Role of protein binding. Cancer Lett 35: 87-95, 1987.
49. Demant EJF, Jensen PB and Sehested M, Characterization of the cooperative cross-linking of doxorubicin N-hydroxysuccinimide ester derivatives to water-soluble proteins. Biochim Biophys Acta 1118: 83-90, 1991.
50. Lieb WR and Stein WD, Non-stokesian nature of transverse diffusion within human red cell membranes. J Membrane Biol 92: 111-119, 1986.
51. Burke TG and Tritton TR, Structural basis of anthracycline selectivity for unilamellar phosphatidylcholine vesicles: An equilibrium binding study. Biochemistry 24: 1768-1776, 1985.
52. Gallois L, Fiallo M, Laigle A, Priebe W and Garnier-Suillerot A, The overall partitioning of anthracyclines into phosphatidyl-containing model membranes depends neither on the drug charge nor the presence of anionic phospholipids. Eur J Biochem 241: 879-887, 1996.
53. Zucker SD, Goessling W and Gollan JL, Kinetics of bilirubin transfer between serum albumin and membrane vesicles. Insight into the mechanism of organic anion delivery to the hepatocyte plasma membrane. J BiolChem 270: 1074-1081, 1995.
54. Kamp F, Zakim D, Zhang F, Noy N and Hamilton JA, Fatty acid flip-flop in phospholipid bilayers is extremely fast. Biochemistry 34: 11928-11937, 1995.
55. Tewey KM, Rowe TC, Yang L, Halligan BD and Liu LF, Adriamycin-induced DNA damage mediated by mammalian DNA-topoisomerase II. Science 226: 466-468, 1984.
56. Friche E, Danks MK, Schmidt CA and Beck WT, Decreased DNA topoisomerase II in daunorubicin-resistant Ehrlich ascites tumor cells. Cancer Res 51: 4213-4218, 1991.
57. Friche E, Danks MK and Beck WT, Characterization of tumor cell resistance to 4′-deoxy-4′-iododoxorubicin developed in Ehrlich ascites cells in vivo. Cancer Res 52: 5701-5706, 1992.
58. Menozzi M, Valentini L, Vannini E and Arcamone F, Self-association of doxorubicin and related compounds in aqueous solution. J Pharm Sci 73: 766-770, 1984.