Reduction of doxorubicin resistance in P-glycoprotein overexpressing cells by hybrid cell-penetrating and drug-binding peptide

Journal of Drug Targeting

Volumn 18, Issue 6, 2010, Pages 477-487

  Zheng, Zhaohua ^a   Aojula, Harmesh ^a   Clarke, David ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Cell penetrating peptide; Doxorubicin; Endosomal release; Multidrug resistance; Noncovalent; P glycoprotein

Indexed keywords

ARGINYLLYSYLLYSYLARGINYLARGINYLGLUTAMINYLARGINYLARGINYLARGINYLLEUCYLTRYPTOPHYLSERYLPROPYLTRYPTOPHYLTYROSYLGLYCYLGLYCYLSERYLTRYPTOPHAN; CHLOROQUINE; DOXORUBICIN; GLYCOPROTEIN P; PEPTIDE; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; DRUG CARRIER; MULTIDRUG RESISTANCE PROTEIN; PEPTIDE FRAGMENT; TAT PEPTIDE (49-57), HUMAN IMMUNODEFICIENCY VIRUS 1; TRANSACTIVATOR PROTEIN;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; DRUG BINDING; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; ENDOCYTOSIS; HUMAN; HUMAN CELL; LEUKEMIA CELL; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; BIOSYNTHESIS; CELL PROLIFERATION; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; FLOW CYTOMETRY; K562 CELL LINE; PERMEABILITY; SOLUBILITY; SPECTROFLUOROMETRY;

ANTIBIOTICS, ANTINEOPLASTIC; CELL PROLIFERATION; CELL SURVIVAL; DOXORUBICIN; DRUG CARRIERS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; HUMANS; K562 CELLS; MICROSCOPY, CONFOCAL; P-GLYCOPROTEIN; PEPTIDE FRAGMENTS; PERMEABILITY; SOLUBILITY; SPECTROMETRY, FLUORESCENCE; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 77953238614     PISSN: 1061186X     EISSN: 10292330     Source Type: Journal    
DOI: 10.3109/10611860903548347     Document Type: Article

References (51)

1. Astriab-Fisher A, Sergueev D, Fisher M, Shaw BR, Juliano RL. (2002). Conjugates of antisense oligonucleotides with the Tat and antennapedia cell-penetrating peptides: effects on cellular uptake, binding to target sequences, and biologic actions. Pharm Res, 19: 744-754.
2. Barraud L, Merle P, Soma E, Lefrançois L, Guerret S, Chevallier M, Dubernet C, Couvreur P, Trépo C, Vitvitski L. (2005). Increase of doxorubicin sensitivity by doxorubicin-loading into nanoparticles for hepatocellular carcinoma cells in vitro and in vivo. J Hepatol, 42: 736-743.
3. Chen YN, Sharma SK, Ramsey TM, Jiang L, Martin MS, Baker K, Adams PD, Bair KW, Kaelin WG Jr. (1999). Selective killing of transformed cells by cyclin/cyclin-dependent kinase 2 antagonists. Proc Natl Acad Sci USA, 96: 4325-4329.
4. de la Fuente JM, Berry CC. (2005). Tat Peptide as an Efficient Molecule to Translocate Gold Nanoparticles into the Cell Nucleus. Bioconjug Chem, 16: 1176-1180.
5. Duncan R. (2006). Polymer conjugates as anticancer nanomedicines. Nat Rev Cancer, 6: 688-701.
6. Fawell S, Seery J, Daikh Y, Moore C, Chen LL, Pepinsky B, Barsoum J. (1994). Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA, 91: 664-668.
7. Filipits M. (2004). Mechanisms of cancer: mutidrug resistance. Drug Discov Today: Dis Mech, 1: 229-234.
8. Ford JM, Hait WN. (1993). Pharmacologic circumvention of multidrug resistance. Cytotechnology, 12: 171-212.
9. Frankel AD, Pabo CO. (1988). Cellular uptake of the tat protein from human immunodeficiency virus. Cell, 55: 1189-1193.
10. Fretz MM, Penning NA, Al-Taei S, Futaki S, Takeuchi T, Nakase I, Storm G, Jones AT. (2007). Temperature-, concentration- and cholesterol-dependent translocation of L- and D-octa-arginine across the plasma and nuclear membrane of CD34+ leukaemia cells. Biochem J, 403: 335-342.
11. Gaber MH. (2002). Modulation of doxorubicin resistance in multidrug-resistance cells by targeted liposomes combined with hyperthermia. J Biochem Mol Biol Biophys, 6: 309-314.
12. Gottesman MM, Cardarelli C, Goldenberg S, Licht T, Pastan I. (1998). Selection and maintenance of multidrug-resistant cells. Meth Enzymol, 292: 248-258.
13. Gottesman MM, Pastan I. (1990). Mechanisms of drug resistance in cancer therapy. Europ J Pharmacol, 183: 17-18.
14. Gupta B, Levchenko TS, Torchilin VP. (2005). Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv Drug Deliv Rev, 57: 637-651.
15. Hovorka O, St'astný M, Etrych T, Subr V, Strohalm J, Ulbrich K, Ríhová B. (2002). Differences in the intracellular fate of free and polymer-bound doxorubicin. J Control Release, 80: 101-117.
16. Ichikawa M, Yoshimura A, Sumizawa T, Shudo N, Kuwazuru Y, Furukawa T, Akiyama S. (1991). Interaction of organic chemicals with P-glycoprotein in the adrenal gland, kidney, and a multidrug-resistant KB cell. J Biol Chem, 266: 903-908.
17. Kanzawa F, Nishio K, Ishida T, Fukuda M, Kurokawa H, Fukumoto H, Nomoto Y, Fukuoka K, Bojanowski K, Saijo N. (1997). Antitumour activities of a new benzo[c]phenanthridine agent, 2,3- (methylenedioxy)-5-methyl-7-hydroxy-8- methoxybenzo[c] phena nthridini um hydrogensulphate dihydrate (NK109), against several drug-resistant human tumour cell lines. Br J Cancer, 76: 571-581.
18. Karukstis KK, Thompson EH, Whiles JA, Rosenfeld RJ. (1998). Deciphering the fluorescence signature of daunomycin and doxorubicin. Biophys Chem, 73: 249-263.
19. Kobayashi T, Ishida T, Okada Y, Ise S, Harashima H, Kiwada H. (2007). Effect of transferrin receptor-targeted liposomal doxorubicin in P-glycoprotein-mediated drug resistant tumor cells. Int J Pharm, 329: 94-102.
20. Krishna R, Mayer LD. (1997). Liposomal doxorubicin circumvents PSC 833-free drug interactions, resulting in effective therapy of multidrug-resistant solid tumors. Cancer Res, 57: 5246-5253.
21. Larsen AK, Escargueil AE, Skladanowski A. (2000). Resistance mechanisms associated with altered intracellular distribution of anticancer agents. Pharmacol Ther, 85: 217-229.
22. Leslie EM, Deeley RG, Cole SP. (2005). Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol, 204: 216-237.
23. Liang JF, Yang VC. (2005). Synthesis of doxorubicin-peptide conjugate with multidrug resistant tumor cell killing activity. Bioorg Med Chem Lett, 15: 5071-5075.
24. Mamot C, Drummond DC, Hong K, Kirpotin DB, Park JW. (2003). Liposome-based approaches to overcome anticancer drug resistance. Drug Resist Updat, 6: 271-279.
25. Mazel M, Clair P, Rousselle C, Vidal P, Scherrmann JM, Mathieu D, Temsamani J. (2001). Doxorubicin-peptide conjugates overcome multidrug resistance. Anticancer Drugs, 12: 107-116.
26. Merrifield B. (1986). Solid phase synthesis. Science, 232: 341-347.
27. Minko T, Kopecková P, Pozharov V, Kopecek J. (1998). HPMA copolymer bound adriamycin overcomes MDR1 gene encoded resistance in a human ovarian carcinoma cell line. J Control Release, 54: 223-233.
28. Moon C, Kwon YM, Lee WK, Park YJ, Yang VC. (2007). In vitro assessment of a novel polyrotaxane-based drug delivery system integrated with a cell-penetrating peptide. J Control Release, 124: 43-50.
29. Munteanu E, Verdier M, Grandjean-Forestier F, Stenger C, Jayat-Vignoles C, Huet S, Robert J, Ratinaud MH. (2006). Mitochondrial localization and activity of P-glycoprotein in doxorubicin-resistant K562 cells. Biochem Pharmacol, 71: 1162-1174.
30. Nagata J, Kijima H, Hatanaka H, Asai S, Miyachi H, Abe Y, Yamazaki H, Nakamura M, Watanabe N, Mine T, Kondo T, Scanlon KJ, Ueyama Y. (2002). Reversal of drug resistance using hammerhead ribozymes against multidrug resistance-associated protein and multidrug resistance 1 gene. Int J Oncol, 21: 1021-1026.
31. Naito S, Yokomizo A, Koga H. (1999). Mechanisms of drug resistance in chemotherapy for urogenital carcinoma. Int J Urol, 6: 427-439.
32. Nieth C, Priebsch A, Stege A, Lage H. (2003). Modulation of the classical multidrug resistance (MDR) phenotype by RNA interference (RNAi). FEBS Lett, 545: 144-150.
33. Nori A, Jensen KD, Tijerina M, Kopecková P, Kopecek J. (2003). Tatconjugated synthetic macromolecules facilitate cytoplasmic drug delivery to human ovarian carcinoma cells. Bioconjug Chem, 14: 44-50.
34. Popkov M, Lussier I, Medvedkine V, Estève PO, Alakhov V, Mandeville R. (1998). Multidrug-resistance drug-binding peptides generated by using a phage display library. Eur J Biochem, 251: 155-163.
35. Pratesi G, Beretta GL, Zunino F. (2004). Gimatecan, a novel camptothecin with a promising preclinical profile. Anticancer Drugs, 15: 545-552.
36. Priebe W, Perez-Soler R. (1993). Design and tumor targeting of anthracyclines able to overcome multidrug resistance: a double-advantage approach. Pharmacol Ther, 60: 215-234.
37. Sandgren S, Cheng F, Belting M. (2002). Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide. Role for cell-surface proteoglycans. J Biol Chem, 277: 38877-38883.
38. Shiraishi T, Nielsen PE. (2006). Enhanced delivery of cell-penetrating peptide-peptide nucleic acid conjugates by endosomal disruption. Nat Protoc, 1: 633-636.
39. St'astný M, Strohalm J, Plocová D, Ulbrich K, Ríhová B. (1999). A possibility to overcome P-glycoprotein (PGP)-mediated multidrug resistance by antibody-targeted drugs conjugated to N-(2-hydroxypropyl)methacrylamide (HPMA) copolymer carrier. Eur J Cancer, 35: 459-466.
40. Tarasiuk J, Frézard F, Garnier-Suillerot A, Gattegno L. (1989). Anthracycline incorporation in human lymphocytes. Kinetics of uptake and nuclear concentration. Biochim Biophys Acta, 1013: 109-117.
41. Temsamani J, Vidal P. (2004). The use of cell-penetrating peptides for drug delivery. Drug Discov Today, 9: 1012-1019.
42. Teodori E, Dei S, Scapecchi S, Gualtieri F. (2002). The medicinal chemistry of multidrug resistance (MDR) reversing drugs. Farmaco, 57: 385-415.
43. Thierry AR, Rahman A, Dritschilo A. (1993). Overcoming multidrug resistance in human tumor cells using free and liposomally encapsulated antisense oligodeoxynucleotides. Biochem Biophys Res Commun, 190: 952-960.
44. Tkaczyk-Gobis K, Tarasiuk J, Seksek O, Stefanska B, Borowski E, Garnier-Suillerot A. (2001). Transport of new non-cross-resistant antitumor compounds of the benzoperimidine family in multidrug resistant cells. Eur J Pharmacol, 413: 131-141.
45. Tseng YL, Liu JJ, Hong RL. (2002). Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study. Mol Pharmacol, 62: 864-872.
46. van Vlerken LE, Duan Z, Seiden MV, Amiji MM. (2007). Modulation of intracellular ceramide using polymeric nanoparticles to overcome multidrug resistance in cancer. Cancer Res, 67: 4843-4850.
47. Vauthier C, Dubernet C, Chauvierre C, Brigger I, Couvreur P. (2003). Drug delivery to resistant tumors: the potential of poly(alkyl cyanoacrylate) nanoparticles. J Control Release, 93: 151-160.
48. Xiong XB, Huang Y, Lu WL, Zhang X, Zhang H, Nagai T, Zhang Q. (2005). Enhanced intracellular delivery and improved antitumor efficacy of doxorubicin by sterically stabilized liposomes modified with a synthetic RGD mimetic. J Control Release, 107: 262-275. (Pubitemid 41316289)
49. Yague E, Armesilla AL, Harrison G, Elliott J, Sardini A, Higgins CF, Raguz S. (2003). P-glycoprotein (MDR1) expression in leukemic cells is regulated at two distinct steps, mRNA stabilization and translational initiation. J Biol Chem, 278: 10344-10352.
50. Zhao M, Weissleder R. (2004). Intracellular cargo delivery using tat peptide and derivatives. Med Res Rev, 24: 1-12.
51. Zhou Y, Gottesman MM, Pastan I. (1999). The extracellular loop between TM5 and TM6 of P-glycoprotein is required for reactivity with monoclonal antibody UIC2. Arch Biochem Biophys, 367: 74-80.