Doxorubicin-gallium-transferrin conjugate overcomes multidrug resistance: Evidence for drug accumulation in the nucleus of drug resistant MCF-7/ADR cells

Anticancer Research

Volumn 20, Issue 2 A, 2000, Pages 799-808

  Wang, Fen ^a   Jiang, Xianpeng ^a   Yang, Ding Cheng ^a   Elliott, Robert L ^a   Head, Jonathan F ^a  

^a The Mastology Research Institute   (United States)

Author keywords

Doxorubicin; Drug resistance; Gallium; Multidrug resistance; Transferrin

Indexed keywords

DOXORUBICIN; FERRIC CHLORIDE; GALLIUM NITRATE; MULTIDRUG RESISTANCE PROTEIN; TRANSFERRIN; TRANSFERRIN RECEPTOR;

ARTICLE; BREAST CANCER; CANCER CELL; CELL MEMBRANE TRANSPORT; CELL NUCLEUS; CELL STRAIN MCF 7; CELL STRUCTURE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA SYNTHESIS; DRUG ACCUMULATION; DRUG CONJUGATION; DRUG CYTOTOXICITY; DRUG DISTRIBUTION; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HUMAN; HUMAN CELL; IC 50; ISOTOPE LABELING; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL DIVISION; CYTOPLASM; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; FEMALE; GENES, MDR; HUMANS; MITOCHONDRIA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; ORGANOMETALLIC COMPOUNDS; P-GLYCOPROTEIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFERRIN; TUMOR CELLS, CULTURED;

EID: 0034009726     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Young RC: Mechanisms to improve chemotherapy effectiveness. Cancer (Phila.) 65: 815-822, 1992.
2. Fojo A, Akiyama SI, Gottesman MM and Pastan I: Reduced drug accumulation in multiply drug-resistant human KB carcinoma cell lines. Cancer Res 45: 3002-3007, 1985.
3. Goldenberg GJ, Wand H and Blair GW: Resistance to adriamycin: relationship of cytotoxicity to drug uptake and DNA single-and double-strand breakage in cloned cell lines of adriamycin-sensitive and resistant P388 leukemia. Cancer Res 46: 2978-2983, 1986.
4. Dean SW, Gibson NW and Tew KD: Selection of nitrogen mustard resistance in a rat tumor cell line results in loss of guanine-06-alkyl transferase activity. Mol Pharmacol 30: 77-80, 1986.
5. Anderson RE, Standefer JC, Truop, GM and Pogue LE: Partial characterization of a mitomycin-C resistant T cell. J Leukocyte Biol 41: 39-44, 1987.
6. Goldie JH and Coldman AJ: The genetic origin of drug resistance in neoplasms: implications for systemic therapy. Cancer Res 44: 3643-3653, 1984.
7. Batist G, Tulpule A, Sinha BK, Katki AG, Myers CE and Cowan KH: Overexpression of a novel anionic glutathione transferase in multidrug-resistant human breast cancer cells. J Biol Chem 261: 15544-15549, 1986.
8. Kleinberger T, Etkin S and Lavi S: Carcinogen-mediated methotrexate resistance and dihydrofolate reductase amplification in chinese hamster cells. Mol Cell Biol 6: 1958-1964, 1986.
9. Armstrong DK, Gordon GB, Hilton J, Streeper RT and Colvin OM: Hepsulfam sensitivity in human breast cancer cell lines: The role of glutathione and glutathione s-transferase in resistance. Cancer Res 52: 1416-1421, 1992.
10. Timothy R, Bailey HH and Gipp JJ: Transfection of complementary DNAs for the heavy and light subunits of human gamma-glutamylcysteine synthetase results in an elevation of intracellular glutathione and resistance to melphalan. Cancer Res 55: 4771-4775, 1995.
11. Cole SPC, Chanda ER, Dick FP, Gerlach JH and Mirski SEL: Non-Pglycoprotein mediated multidrug resistance in a small cell lung cancer cell line: evidence for decreased susceptibility to drug-induced DNA damage and reduced levels of topoisomcrase II. Cancer Res 51: 3345-3352, 1991.
12. Inaba M, Fujikura R and Sakurai Y: Active efflux common to vincristine and daunorubicin in vincristine-resistant P388 leukemia. Biochem Pharmacol 30: 1863-1865, 1981.
13. Slovak ML, Hoeltge GA, Dalton WS and Trent JM: Pharmacological and biological evidence for differing mechanisms of doxorubicin resistance in two human tumor cell lines. Cancer Res 48: 2793-2797, 1988.
14. Colvin M and Chabner BA: Alkylating agents. In: Cancer chermotherapy: Principles and Practice (Chabner BA and Collins JM, eds.). Philadephia, J. B. Lippincott Co., 1990, pp. 276-313.
15. Gottesman MM: How cancer cells evade chemotherapy. Cancer Res 53: 747-754, 1993.
16. Endicott JA and Ling V: The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu Rev Biochem 58: 137-171, 1989.
17. McGrath T and Center MS: Adriamycin resistance in HL-60 cells in the absence of detectable P-glycoprotein. Biochem Biophys Res Commun 145: 1171-1176, 1987.
18. Versantvoort CHM, Broxterman HJ, Pinedo HM, de Vries EGE, Feller N, Kuiper CM and Lankelma J: Energy-dependent processes involved in reduced drug accumulation in multidrug-resistant human lung cancer cell lines without P-glycoprotein expression. Cancer Res 52: 17-23, 1992.
19. Hindenburg AA, Gervasoni JE, Krishna S, Stewart BJ, Rosado M, Lutzky J, Bhalla K, Baker MA and Taub RN: Intercellular distribution and pharmacokinetics of daunorubicin in anthracycline-sensitive and -resistant HL-60 cells. Cancer Res 49: 4607-4614, 1989.
20. Cole SPC, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AMV and Deeley RG: Overexpresion of a transporter gene in a multidrug-resistant human lung cancer cell line. Science (Washington DC) 258: 1650-1654, 1992.
21. Zaman GJR, Versantvoort CHM, Smit JJM, Eijdems EWHM, de Haas M, Smith AJ, Broxterman HJ, Mulder NH, de Vries EGE, Baas F and Borst P: Analysis of the expression of MRP, the gene for a new putative transmembrane drug transporter, in human multidrug resistant lung cancer cell line. Cancer Res 53: 1747-1750, 1993.
22. Barrand MA, Heppell-Parton AC, Wright KA, Rabbitts PH and Twentyman PR: A 190-kilodalton protein overexpressed in non-P-glycoprotein-containing multidrug-resistance cells and its relationship to the mrp gene. J Natl Cancer Inst 86: 110-117, 1994.
23. Krishnamachary N and Center MS: The mrp gene associated with a non-P-glycoprotein multidrug resistance encodes a 190-kDa membrane bound glycoprotein. Cancer Res 53: 3658-3661, 1993.
24. Nooter K and Stoter G: Molecular mechanisms of multidrug resistance in cancer chemotherapy. Pathol Res Pract 197: 768-780, 1996.
25. Flens MJ, Izquierdo MA, Scheffer GL, Fritz JM, Meijer CJLM, Scheper RJ and Zaman GJR: Immunochemical detection of the mutidrug resistance associated protein MRP in human multidrug-resistant tumor cells by monoclonal antibodies. Cancer Res 54: 4557-4563, 1994.
26. Gervasoni JE Jr, Fields SZ, Krishna S, Baker MA, Rosado M, Thuraisamy K, Hindenburg AA and Taub RN: Subcellular distribution of daunorubicin in P-glycoprotein-positive and - negative drug-resistant cell lines using laser-assisted confocal microscopy. Cancer Res 51: 4955-4963, 1991.
27. Breuninger LM, Paul S, Gaughan K, Miki T, Chan A, Aaronson SA and Kruh GD: Expression of multidrug resistance-associated protein in NIH/3T3 cells confers multidrug resistance associated with increased drug efflux and altered intracellular drug distribution. Cancer Res 55: 5342-5347, 1995.
28. Dietel M, Arps H, Lage H and Niendorf A: Membrane vesicle formation due to acquired mitoxantrone resistance in human gastric carcinoma cell line EPG85-257. Cancer Res 50: 6100-6106, 1990.
29. Venne A, Li S, Mandeville R, Kabanov A and Alakhov V: Hypersensitizing effect of pluronic L61 on cytotoxic activity, transport, and subcellular distribution of doxoruhicin in multiple drug-resistant cells. Cancer Res 56: 3626-3629, 1996.
30. Sivam GP, Martin PJ, Reifeld RA and Mueller BM: Therapeutic efficacy of a Doxorubicin immunoconjugate in a preclinical model of spontaneous metastatic human melanoma. Cancer Res 55: 2352-2356, 1995.
31. Dillman RO, Shawler DL, Johnson DE, Meyer DL, Koziol J and Frincke JM: Preclinical trials with combinations and conjugates of T101 monoclonal antibody and doxorubicin. Cancer Res 46: 4886-4891, 1986.
32. Hatano T, Ohkawa K and Mastsuda M: Cytotoxic effect of the protein-doxorubicin conjugates on the multidrug-resistant human myclogenous leukemia cell line, K562, in vitro. Tumour Biol 14: 288-294, 1993.
33. Ohkawa K, Hatano T, Yamada K, Joh K. Takada K, Tsukada Y and Matsuda M: Bovine serum albumin-doxorubicin conjugates overcome multidrug resistance in a rat hepatoma. Cancer Res 53: 4238-4242, 1993.
34. Berczi A, Barabas K, Sizensky JA and Faulk WP: Adriamycin conjugates of human transferrin bind transferrin receptors and kill K562 and HL60 cells. Arch Biochem Biophys 300: 356-363, 1993.
35. Courtney-Luck, NS, Epenetos AA, Moore R, Larche M, Pectasides D, Dhokia B and Ritter MA: Development of primary and secondary immune responses to mouse monoclonal antibodies used in the diagnosis and therapy of malignant neoplasms. Cancer Res 46: 6489-6493, 1986.
36. Welch S: Transferrin: The iron carrier. CRC Press, pp 169-170.
37. Barabas K and Faulk WP: Transferrin receptors associate with drug resistance in cancer cells. Biochem Biophys Res Commun 197: 702-708, 1993.
38. Fritzer M, Szekeres T, Szuts V, Jarayam HN and Goldenberg H: Cytotoxic effects of a doxorubicin-transferrin conjugate in multidrug-resistant KB cells. Biochem Pharmacol 51: 489-493, 1996.
39. Barabas K, Sizensky JA and Faulk WP: Transferrin conjugates of adriamycin are cytotoxic without intercalating nuclear DNA. J Biol Chem 267: 9437-9442, 1992.
40. Lemieux P and Pagé M: Sensitivity of multidrug-resistant MCF-7 cells to a transferrin-doxorubicin conjugate. Anticancer Res 14: 397-403, 1994.
41. Elliott RL, Elliott MC, Wang F and Head JF: Breast carcinoma and the role of iron metabolism. A cytochemical, tissue culture, and ultrastructural study. Ann NY Acad Sci 698: 159-166, 1993.
42. Sun IL, Sun EE, Crane FL, Morre DJ and Faulk WP: Inhibition of transplasma membrane electron transport by transferrin-adriamycin conjugates. Biochem Biophys. Acta 1105: 84-88, 1992.
43. Wang F, Jiang XP, Yang DC, Elliott RL and Head JF: Effects of gallium and galiium-transferrin on DNA synthesis, ferritin gene expression and cellular ferritin synthesis in MCF-7 cells. Proc American Association for Cancer Research 38: 601, 1997.
44. Chen CJ, Chin JE, Ueda K, Clark DP, Pastan I, Gottesman MM and Roninson I: Internal duplication and homology with bacterial transport proteins in the mdr1 (P-glycoprotein) gene from multidrug-resistant human cells. Cell 47: 381-389, 1986.
45. Wang F, Ledford L, Head JF and Elliott RL: A novel cell culture technique for electron microscopy. Microscopy Research and Technique 26: 517-522, 1993.
46. Calendi E, Di Marco A, Reggiani B, Scarpinato B and Valentini L: On physico-chemical interactions between Daunomycin and Nucleic Acids. Biochim Biophys 103: 25-49, 1965.
47. Love R, Studzinski GP and Ellem KA: Use of Antimetabolites in the study of normal and abnormal cell function. Federation Proc 24: 1206-1216, 1965.
48. Simard R: Specific nuclear and nucleolar ultrastructural lesions induced by proflavine and similarly acting antimetabolites in tissue culture. Cancer Res 26: 2316-2328, 1966.
49. Merski JA, Daskal Y, Crooke ST and Busch H: Acute ultrastructural effects of the antitumor antibiotic carminomycin on nucleoli of rat tissues. Cancer Res 39: 1239-1244, 1979.
50. Sognier MA, Zhang Y, Eberle RL, Sweei KM, Altenberg GA and Belli JA: Sequestration of doxorubicin in vesicles in a multidrug-resistant cell line (LZ-100). Bichem Pharmacol 48: 291-401, 1994.
51. Schuurhuis GJ, Broxterman HJ, deLange JHM, Pinedo HM, van Heijiningen THM, Kuiper CM, Scheffer GL, Scheper RJ, van Kalken CK. Baak JPA and Lankelma J: Early multidrug resistance, defined by changes in intracellular doxorubicin distribution, independent of P-glycoprotein. Br J Cancer 64: 857-861, 1991.
52. Schuurhuis GJ, Broxterman H and Cervantes A: Quantitative determination of factors contributing to doxorubicin resistance in multidrug resistant cells. J Natl Cancer Inst 81: 1887-1894, 1989.
53. Pagano RE and Slight R: Defining lipid transport pathways in animal cells. Science (Wash. DC) 229: 1051-1057, 1985.
54. Pastan I and Willingham MD: Receptor-mediated endocytosis: coated pits, receptosomes and the Golgi. In: Oncogenes and Growth Factors (Bradshaw RA and Prentis S eds). New York, Elisevier Science Publishers, 1987, pp 238-247.
55. Dano K: Active outward transport of daunorubicin in resistant Ehrlich ascites tumor cells. Biochem Biophys Acta 323: 466-483, 1973.
56. Cornwell MM, Pastan I and Gottesman MM: Ceitain calcium channel blockers bind specifically to multidrug-resistant human KB carcinoma membrane vesicles and inhibit drug binding to P-glucoprotein. J Biol Chem 262: 2166-2170, 1987.
57. Schested 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.
58. Hindendurg A, Baker M, Gleyzer E, Stewart V, Case N and Taub RN: Effect of verapamil and other agents on the distribution of anthracyclines and on reversal of drug resistance. Cancer Res 47: 1421-1425, 1987.
59. Scheffer GL, Wijingaard PLJ, Flens MJ, Izquierdo MA, Slovak ML, Pinedo HM, Meijer CJL, Clevers HC and Scheper RJ: The drug resistance-related protein LRP is the human major vault protein. Nat Med 1: 578-582, 1995.
60. Izquierdo MA, van der Zee AGJ, Vermorken JB, van der Valk P, Belien JAM, Giaccone G, Scheffer GL, Flens MJ, Pinedo HM, Kenenmans P, meijer CJLM, de Vries EGE and Scheper RJ: Drug resistance-associated marker LRP for prediction of response to chemotherapy and prognoses in advanced ovarian carcinoma. J Natl Cancer Inst 87: 1231-1237, 1995.
61. Barrand MA, Rhodes T, Center MS and Twentyman PR: Chemosensitization and drug accumulation effects of cyclosporin A, PSC-833 and verapamil in human MDR large cell lung cancer cells expressing a 190k membrane protein distinct for P-glycoprotein. Eur J Cancer 29: 408-415, 1993.
62. Cole SPC, Sparks KE, Fraser K, Loe DW, Grant CE and Wilson GM: Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 54: 5902-5910, 1995.
63. Schindler M, Sharon G, Hoff E and Simon SM: Defective pH regulation of acidic compartments in human breast cancer cells (MCF-7) is normalized in adriamycin-resistant cells (MCF-7/ADR). Biochemistry 35: 2811-2817, 1996.
64. Yeh CJG and Faulk WP: Killing of human tumor cells in culture with adriamycin conjugates of human transferrin. Clin Immunol Immunopathol 32: 1-11, 1984.
65. Demant EJF and Norskov-Lauritsen N: Binding of transferrin-iron by adriamycin at acidic pH. FEBS Lett 196: 321-324, 1986.
66. Berczi A, Ruthner M, Szuts V, Fritzer M, Schweinzer E and Goldenberg OH: Influence of conjugation of doxorubicin to transferrin on the iron uptake by K562 cells via receptor-mediated endocytosis. J Biochem 215: 427-436, 1993.
67. Ruthner M, Berczi A and Goldenberg H: Interaction of a doxorubicin-transferrin conjugate with isolated transferrin receptors. Life Sciences 54: 35-40, 1994.
68. Alakhov VY, Moskaleva EY, Batrakova EV and Kabanov AV: Hypersensitization of multidrug resistant human ovarian carcinoma cell by pluronic P85 block copolymer. Bioconjugate Chem 7: 209-216, 1996.
69. Faulk WP, Hsi BL and Stevens PL: Transferrin and transferrin receptors in carcinoma of the breast. Lancet 2: 390-392, 1980.