Nanomedicinal strategies to treat multidrug-resistant tumors: Current progress

Nanomedicine

Volumn 5, Issue 4, 2010, Pages 597-615

  Dong, Xiaowei ^a,b   Mumper, Russell J ^c  

^a University of Kentucky   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Brij; Drug delivery; Efflux transporters; Lipid formulation; Nanoparticle; P glycoprotein; Pluronic; Vitamin e tpgs

Indexed keywords

7 ETHYL 10 HYDROXYCAMPTOTHECIN; ANTHRACYCLINE DERIVATIVE; ANTINEOPLASTIC AGENT; BISANTRENE; COLCHICINE DERIVATIVE; DACTINOMYCIN; DOXORUBICIN; ETOPOSIDE; GLYCOPROTEIN P; IMATINIB; IRINOTECAN; LIPOSOME; MACROGOL; MESSENGER RNA; MITOXANTRONE; MONOCLONAL ANTIBODY; NANOCAPSULE; NANOPARTICLE; PACLITAXEL; PEPTIDE DERIVATIVE; POLOXAMER; POLYMER; SAQUINAVIR; SMALL INTERFERING RNA; SURFACTANT; TAXANE DERIVATIVE; TENIPOSIDE; UNINDEXED DRUG; VINCA ALKALOID; VINCRISTINE;

CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CELL LEVEL; DRUG ACCUMULATION; DRUG BLOOD LEVEL; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG FORMULATION; DRUG MEGADOSE; DRUG SAFETY; DRUG TARGETING; GENE; GENE INACTIVATION; GLIOMA; HUMAN; LIPOSOMAL GENE DELIVERY SYSTEM; MALIGNANT NEOPLASTIC DISEASE; MDR1 GENE; MICELLE; MULTIDRUG RESISTANCE; NANOENCAPSULATION; NANOMEDICINE; NANOTECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; RNA DEGRADATION; SOLID TUMOR; TISSUE PRESSURE; TUMOR VASCULARIZATION;

DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; NANOMEDICINE; NEOPLASMS;

EID: 77953368844     PISSN: 17435889     EISSN: None     Source Type: Journal    
DOI: 10.2217/nnm.10.35     Document Type: Review

References (164)

1. Cortes-Funes H, Coronado C: Role of anthracyclines in the era of targeted therapy. Cardiovasc. Toxicol. 7(2), 56-60 (2007).
2. Piccart M: The role of taxanes in the adjuvant treatment of early stage breast cancer. Breast Cancer Res. Treat. 79(Suppl. 1), S25-S34 (2003). (Pubitemid 36801908)
3. Leonard GD, Fojo T, Bates SE: The role of ABC transporters in clinical practice. Oncologist 8 (5), 411-424 (2003).
4. Leonard GD, Polgar O, Bates SE: ABC transporters and inhibitors: new targets, new agents. Curr. Opin. Invest. Drugs 3 (11), 1652-1659 (2002).
5. Gillet JP, Gottesman MM: Mechanisms of multidrug resistance in cancer. Methods Mol. Biol. 596, 47-75 (2010).
6. Campbell RB: Tumor physiology and delivery of nanopharmaceuticals. Anticancer Agents Med. Chem. 6(6), 503-512 (2006).
7. Fukumura D, Jain RK: Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc. Res. 74(2-3), 72-84 (2007).
8. Endrich B, Reinhold HS, Gross JF, Intaglietta M: Tissue perfusion inhomogeneity during early tumor growth in rats. J. Natl Cancer Inst. 62(2), 387-395 (1979).
9. Hamberg LM, Kristjansen PE, Hunter GJ, Wolf GL, Jain RK: Spatial heterogeneity in tumor perfusion measured with functional computed tomography at 0.05 microliter resolution. Cancer Res. 54(23), 6032-6036 (1994).
10. Jain RK: Determinants of tumor blood flow: a review. Cancer Res. 48(10), 2641-2658 (1988).
11. Hobbs SK, Monsky WL, Yuan F et al.: Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl Acad. Sci. USA 95(8), 4607-4612 (1998).
12. Rubin P, Casarett G: Microcirculation of tumors. I. Anatomy, function, and necrosis. Clin. Radiol. 17(3), 220-229 (1966).
13. Shubik P: Vascularization of tumors: a review. J. Cancer Res. Clin. Oncol. 103(3), 211-226 (1982).
14. Yuan F, Dellian M, Fukumura D et al.: Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size. Cancer Res. 55(17), 3752-3756 (1995).
15. Aukland K, Reed RK: Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol. Rev. 73(1), 1-78 (1993).
16. Boucher Y, Baxter LT, Jain RK: Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: implications for therapy. Cancer Res. 50(15), 4478-4484 (1990).
17. Leu AJ, Berk DA, Lymboussaki A, Alitalo K, Jain RK: Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res. 60(16), 4324-4327 (2000).
18. Padera TP, Stoll BR, Tooredman JB, Capen D, Di Tomaso E, Jain RK: Pathology: cancer cells compress intratumour vessels. Nature 427(6976), 695 (2004).
19. Padera TP, Kadambi A, Di Tomaso E et al.: Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296(5574), 1883-1886 (2002).
20. Saijo N: Chemotherapy: the more the better? Overview. Cancer Chemother. Pharmacol. 40(Suppl.), S100-S106 (1997).
21. Reed JC: Bcl-2: Prevention of apoptosis as a mechanism of drug resistance. Hematol. Oncol. Clin. North Am. 9(2), 451-473 (1995).
22. Morrow CS, Cowan KH: Glutathione s-transferases and drug resistance. Cancer Cells 2(1), 15-22 (1990).
23. Ling V, Thompson LH: Reduced permeability in CHO cells as a mechanism of resistance to colchicine. J. Cell. Physiol. 83(1), 103-116 (1974).
24. See YP, Carlsen SA, Till JE, Ling V: Increased drug permeability in Chinese hamster ovary cells in the presence of cyanide. Biochim. Biophys. Acta 373(2), 242-252 (1974).
25. Arao S, Suwa H, Mandai M et al.: Expression of multidrug resistance gene and localization of P-glycoprotein in human primary ovarian cancer. Cancer Res. 54(5), 1355-1359 (1994).
26. Arceci RJ: Clinical significance of P-glycoprotein in multidrug resistance malignancies. Blood 81(9), 2215-2222 (1993).
27. Bell DR, Gerlach JH, Kartner N, Buick RN, Ling V: Detection of P-glycoprotein in ovarian cancer: a molecular marker associated with multidrug resistance. J. Clin. Oncol. 3(3), 311-315 (1985).
28. Dalton WS, Grogan TM, Rybski JA et al.: Immunohistochemical detection and quantitation of P-glycoprotein in multiple drug-resistant human myeloma cells: Association with level of drug resistance and drug accumulation. Blood 73(3), 747-752 (1989).
29. Pirker R, Wallner J, Geissler K et al.: MDR1 gene expression and treatment outcome in acute myeloid leukemia. J. Natl Cancer Inst. 83(10), 708-712 (1991).
30. Sato H, Preisler H, Day R et al.: MDR1 transcript levels as an indication of resistant disease in acute myelogenous leukaemia. Br. J. Haematol. 75(3), 340-345 (1990).
31. List AF, Spier C, Greer J et al.: Phase I/II trial of cyclosporine as a chemotherapy-resistance modifier in acute leukemia. J. Clin. Oncol. 11(9), 1652-1660 (1993).
32. Marie JP, Bastie JN, Coloma F et al.: Cyclosporin A as a modifier agent in the salvage treatment of acute leukemia (AL). Leukemia 7(6), 821-824 (1993).
33. Higgins CF: ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113 (1992).
34. Kast C, Canfield V, Levenson R, Gros P: Transmembrane organization of mouse P-glycoprotein determined by epitope insertion and immunofluorescence. J. Biol. Chem. 271(16), 9240-9248 (1996).
35. Loo TW, Clarke DM: Membrane topology of a cysteine-less mutant of human P-glycoprotein. J. Biol. Chem. 270(2), 843-848 (1995).
36. Teodori E, Dei S, Martelli C, Scapecchi S, Gualtieri F: The functions and structure of ABC transporters: implications for the design of new inhibitors of Pgp and MRP1 to control multidrug resistance (MDR). Curr. Drug Targets 7(7), 893-909 (2006).
37. Fojo AT, Ueda K, Slamon DJ, Poplack DG, Gottesman MM, Pastan I: Expression of a multidrug-resistance gene in human tumors and tissues. Proc. Natl Acad. Sci. USA 84(1), 265-269 (1987).
38. Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, Willingham MC: Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc. Natl Acad. Sci. USA 84(21), 7735-7738 (1987).
39. Schinkel AH, Mol CA, Wagenaar E, Van Deemter L, Smit JJ, Borst P: Multidrug resistance and the role of P-glycoprotein knockout mice. Eur. J. Cancer 31A(7-8), 1295-1298 (1995).
40. Schinkel AH, Smit JJ, Van Tellingen O et al.: Disruption of the mouse MDR1A P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77(4), 491-502 (1994).
41. Schinkel AH, Wagenaar E, Van Deemter L, Mol CA, Borst P: Absence of the MDR1A P-glycoprotein in mice affects tissue distribution and pharmacokinetics of dexamethasone, digoxin, and cyclosporin A. J. Clin. Invest. 96(4), 1698-1705 (1995).
42. Gottesman MM: Mechanisms of cancer drug resistance. Annu. Rev. Med. 53, 615-627 (2002).
43. Loo TW, Clarke DM: Recent progress in understanding the mechanism of P-glycoprotein-mediated drug efflux. J. Membr. Biol. 206(3), 173-185 (2005).
44. Nadali F, Pourfathollah AA, Alimoghaddam CK et al.: Multidrug resistance inhibition by antisense oligonucleotide against MDR1/ mRNA in P-glycoprotein expressing leukemic cells. Hematology 12 (5), 393-401 (2007).
45. Ren Y, Wang Y, Zhang Y, Wei D: Overcoming multidrug resistance in human carcinoma cells by an antisense-oligodeoxynucleotide-doxorubicin conjugate in vitro and in vivo. Mol. Pharm. 5(4), 579-587 (2008).
46. Stewart AJ, Canitrot Y, Baracchini E et al.: Reduction of expression of the multidrug resistance protein (MRP) in human tumor cells by antisense phosphorothioate oligonucleotides. Biochem. Pharmacol. 51(4), 461-469 (1996).
47. Kawabata S, Oka M, Shiozawa K et al.: Breast cancer resistance protein directly confers SN-38 resistance of lung cancer cells. Biochem. Biophys. Res. Commun. 280(5), 1216-1223 (2001).
48. Krühn A, Wang A, Fruehauf JH, Lage H: Delivery of short hairpin RNA by transkingdom RNA interference modulates the classical ABCB1-mediated multidrug-resistant phenotype of cancer cells. Cell Cycle 8(20), 3349-3354 (2009).
49. Xia Z, Zhu Z, Zhang L et al.: Specific reversal of MDR1/P-gp-dependent multidrug resistance by RNA interference in colon cancer cells. Oncol. Rep. 20(6), 1433-1439 (2008).
50. Stege A, Krühn A, Lage H: Overcoming multidrug resistance by RNA interference. Methods Mol. Biol. 596, 447-465 (2010).
51. Duan Z, Brakora KA, Seiden MY: Inhibition of ABCB1 (MDR1) and ABCB4 (MDR3) expression by small interfering RNA and reversal of paclitaxel resistance in human ovarian cancer cells. Mol. Cancer Ther. 3(7), 833-838 (2004).
52. Lv H, He Z, Liu X, Yuan J, Yu Y, Chen Z: Reversal of BCRP-mediated multidrug resistance by stable expression of small interfering RNAs. J. Cell Biochem. 102(1), 75-81 (2007).
53. Saad M, Garbuzenko OB, Minko T: Co-delivery of siRNA and an anticancer drug for treatment of multidrug-resistant cancer. Nanomedicine 3(6), 761-776 (2008).
54. Patil YB, Swaminathan SK, Sadhukha,T, Ma L, Panyam J: The use of nanoparticle-mediated targeted gene silencing and drug delivery to overcome tumor drug resistance. Biomaterials 31, 358-365 (2010).
55. Watanabe T, Naito M, Kokubu N, Tsuruo T: Regression of established tumors expressing P-glycoprotein by combination of adriamycin, cyclosporine derivatives, and MRK16 antibodies. J. Natl Cancer Inst. 89(7), 512-518 (1997).
56. Goda K, Fenyvesi F, Bacsó Z et al.: Complete inhibition of P-glycoprotein by simultaneous treatment with a distinct class of modulators and the UIC2 monoclonal antibody. J. Pharmacol. Exp. Ther. 320(1), 81-88 (2006).
57. Ono C, Takao A, Atsumi R: Absorption, distribution, and excretion of DJ-927, a novel orally effective taxane, in mice, dogs, and monkeys. Biol. Pharm. Bull. 27(3), 345-351 (2004).
58. Shionoya M, Jimbo T, Kitagawa M, Soga T, Tohgo A: DJ-927, a novel oral taxane, overcomes P-glycoprotein-mediated multidrug resistance in vitro and in vivo. Cancer Sci. 94(5), 459-466 (2003).
59. Cassinelli G, Lanzi C, Supino R et al.: Cellular bases of the antitumor activity of the novel taxane IDN 5109 (BAY59-8862) on hormone-refractory prostate cancer. Clin. Cancer Res. 8(8), 2647-2654 (2002).
60. Polizzi D, Pratesi G, Monestiroli S et al.: Oral efficacy and bioavailability of a novel taxane. Clin. Cancer Res. 6(5), 2070-2074 (2000).
61. Altstadt TJ, Fairchild CR, Golik J et al.: Synthesis and antitumor activity of novel c-7 paclitaxel ethers: discovery of BMS-184476. J. Med. Chem. 44(26), 4577-4583 (2001).
62. Rose WC, Fairchild C, Lee FY: Preclinical antitumor activity of two novel taxanes. Cancer Chemother. Pharmacol. 47(2), 97-105 (2001).
63. Gelmon KA, Latreille J, Tolcher A et al.: Phase I dose-finding study of a new taxane, RPR 109881a, administered as a one-hour intravenous infusion days 1 and 8 to patients with advanced solid tumors. J. Clin. Oncol. 18(24), 4098-4108 (2000).
64. Kurata T, Shimada Y, Tamura Tet al.: Phase I and pharmacokinetic study of a new taxoid, RPR 109881a, given as a 1-hour intravenous infusion in patients with advanced solid tumors. J. Clin. Oncol. 18(17), 3164-3171 (2000).
65. Lissianskaya A, Gershanovich M, Ognerubov N, Golubeva O, Pratt J: Paclitaxel injectable emulsion: Phase 2a study of weekly administration in patients with platinum-resistant ovarian cancer. Proc. Am. Soc. Clin. Oncol. 22, 5047 (2004).
66. Sadava D, Coleman A, Kane SE: Liposomal daunorubicin overcomes drug resistance in human breast, ovarian and lung carcinoma cells. J. Liposome Res. 12(4), 301-309 (2002). (Pubitemid 36008393)
67. Gatouillat G, Odot J, Balasse E et al.: Immunization with liposome-anchored pegylated peptides modulates doxorubicin sensitivity in P-glycoprotein-expressing p388 cells. Cancer Lett. 257(2), 165-171 (2007).
68. Hamada H, Tsuruo T: Functional role for the 170- to 180-kDa glycoprotein specific to drug-resistant tumor cells as revealed by monoclonal antibodies. Proc. Natl Acad. Sci. USA 83(20), 7785-7789 (1986).
69. Mechetner EB, Roninson IB: Efficient inhibition of P-glycoprotein- mediated multidrug resistance with a monoclonal antibody. Proc. Natl Acad. Sci. USA 89(13), 5824-5828 (1992).
70. Tsuruo T, Iida H, Tsukagoshi S, Sakurai Y: Overcoming of vincristine resistance in p388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Res. 41(5), 1967-1972 (1981).
71. Tsuruo T, Iida H, Yamashiro M, Tsukagoshi S, Sakurai Y: Enhancement of vincristine- and adriamycin-induced cytotoxicity by verapamil in p388 leukemia and its sublines resistant to vincristine and adriamycin. Biochem. Pharmacol. 31(19), 3138-3140 (1982).
72. Kerr DJ, Graham J, Cummings J et al.: The effect of verapamil on the pharmacokinetics of adriamycin. Cancer Chemother. Pharmacol. 18(3), 239-242 (1986).
73. Bates S, Kang M, Meadows B et al.: A Phase I study of infusional vinblastine in combination with the P-glycoprotein antagonist PSC 833 (valspodar). Cancer 92(6), 1577-1590 (2001). (Pubitemid 32947844)
74. Nobili S, landini I, Giglioni B, Mini E: Pharmacological strategies for overcoming multidrug resistance. Curr. Drug Targets 7(7), 861-879 (2006).
75. Bangham AD, Standish MM, Watkins JC: Diffusion of univalent ions across the lamellae of swollen phospholipids. J. Mol. Biol. 13(1), 238-252 (1965).
76. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R: Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2(12), 751-760 (2007).
77. Alexis F, Rhee JW, Richie JP, Radovic-Moreno AF, Langer R, Farokhzad OC: New frontiers in nanotechnology for cancer treatment. Urol. Oncol. 26(1), 74-85 (2008).
78. Jang SH, Wientjes MG, Lu D, Au JL: Drug delivery and transport to solid tumors. Pharm. Res. 20(9), 1337-1350 (2003).
79. Haley B, Frenkel E: Nanoparticles for drug delivery in cancer treatment. Urol. Oncol. 26(1), 57-64 (2008).
80. Thierry B: Drug nanocarriers and functional nanoparticles: applications in cancer therapy. Curr. Drug Deliv. 6(4), 391-403 (2009).
81. Gindy ME, Prud'homme RK: Multifunctional nanoparticles for imaging, delivery and targeting in cancer therapy. Expert Opin. Drug Deliv. 6(8), 865-878 (2009).
82. Pridgen EM, Langer R, Farokhzad OC: Biodegradable, polymeric nanoparticle delivery systems for cancer therapy. Nanomedicine 2(5), 669-680 (2007).
83. Karakotchian M, Fraser IS: An ultrastructural study of microvascular inter-endothelial tight junctions in normal endometrium. Micron 38(6), 632-636 (2007).
84. Torchilin V: Tumor delivery of macromolecular drugs based on the EPR effect. Adv. Drug Deliv. Rev. DOI:10.1016/j.addr.2010.03.011 (2010) (Epubahead of print).
85. Gopinathan A, Tuveson DA: The use of GEM models for experimental cancer therapeutics. Dis. Model Mech. 1(2-3), 83-86 (2008).
86. Carrstensen H, Muller RH, Muller BW: Particle size, surface hydrophobicity and interaction with serum of parenteral fat emulsions and model drug carriers as parameters related to RES uptake. Clin. Nutr. 11(5), 289-297 (1992).
87. Norman ME, Williams P, Illum L: Human serum albumin as a probe for surface conditioning (opsonization) of block copolymer-coated microspheres. Biomaterials 13(12), 841-849 (1992).
88. Owens DE, Peppas NA: Opsonization, biodistribution and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 307(1), 93-102 (2006).
89. Chen LT, Weiss L: The role of the sinus wall in the passage of erythrocytes through the spleen. Blood 41(4), 529-537 (1973).
90. Moghimi SM, Hunter AC, Murray JC: Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 53(2), 283-318 (2001).
91. Moghimi SM, Porter CJ, Muir IS, Illum L, Davis SS: Non-phagocytic uptake of intravenously injected microspheres in rat spleen: influence of particle size and hydrophilic coating. Biochem. Biophys. Res. Commun. 177(2), 861-866 (1991).
92. Stegemann S, Leveiller F, Franchi D, De Jong H, Linden H: When poor solubility becomes an issue: from early stage to proof of concept. Eur. J. Pharm. Sci. 31(5), 249-261 (2007).
93. Liu P, Wang B, Weili Qiao JL: Multi-anticancer drugs encapsulated in the micelle: a novel chemotherapy to cancer. Med. Hypotheses 71(3), 379-381 (2008).
94. Benny O, Fainaru O, Adini A et al.: An orally delivered small-molecule formulation with antiangiogenic and anticancer activity. Nat. Biotechnol. 26(7), 799-807 (2008).
95. Sarmento B, Martins S, Ferreira D, Souto EB: Oral insulin delivery by means of solid lipid nanoparticles. Int. J. Nanomed. 2(4), 743-749 (2007).
96. Cosco D, Celia C, Cilurzo F, Trapasso E, Paolino D: Colloidal carriers for the enhanced delivery through the skin. Expert Opin. Drug Deliv. 5(7), 737-755 (2008).
97. Mainardes RM, Urban MC, Cinto PO et al.: Colloidal carriers for ophthalmic drug delivery. Curr. Drug Targets 6(3), 363-371 (2005).
98. Constantinides PP, Chaubal MV, Shorr R: Advances in lipid nanodispersions for parenteral drug delivery and targeting. Adv. Drug Deliv. Rev. 60(6), 757-767 (2008).
99. Tamilvanan S: Oil-in-water lipid emulsions: implications for parenteral and ocular delivering systems. Prog. Lipid Res. 43(6), 489-533 (2004).
100. Constantinides PP, Wasan KM: Lipid formulation strategies for enhancing intestinal transport and absorption of P-glycoprotein (P-gp) substrate drugs: in vitro/in vivo case studies. J. Pharm. Sci. 96(2), 235-248 (2007).
101. Riehm H, Biedler JL: Potentiation of drug effect by Tween 80 in Chinese hamster cells resistant to actinomycin D and daunomycin. Cancer Res. 32(6), 1195-1200 (1972).
102. Seelig A, Gerebtzoff G: Enhancement of drug absorption by noncharged detergents through membrane and P-glycoprotein binding. Expert Opin. Drug Metab. Toxicol. 2(5), 733-752 (2006).
103. Bogman K, Zysset Y, Degen L et al.: P-glycoprotein and surfactants: effect on intestinal talinolol absorption. Clin. Pharmacol. Ther. 77(1), 24-32 (2005).
104. Foger F, Hoyer H, Kafedjiiski K, Thaurer M, Bernkop-Schnurch A: In vivo comparison of various polymeric and low molecular mass inhibitors of intestinal P-glycoprotein. Biomaterials 27(34), 5855-5860 (2006).
105. Dintaman JM, Silverman JA: Inhibition of P-glycoprotein by d-a-tocopheryl polyethylene glycol 1000 succinate (TPGS). Pharm. Res. 16(10), 1550-1556 (1999).
106. Collnot EM, Baldes C, Wempe MF et al.: Influence of vitamin E TPGS poly(ethylene glycol) chain length on apical efflux transporters in Caco-2 cell monolayers. J. Control. Release 111(1-2), 35-40 (2006).
107. Lo YL: Relationships between the hydrophilic-lipophilic balance values of pharmaceutical excipients and their multidrug resistance modulating effect in Caco-2 cells and rat intestines. J. Control. Release 90(1), 37-48 (2003).
108. Batrakova EV, Li S, Alakhov VY, Miller DW, Kabanov AV: Optimal structure requirements for Pluronic block copolymers in modifying P-glycoprotein drug efflux transporter activity in bovine brain microvessel endothelial cells. J. Pharmacol. Exp. Ther. 304(2), 845-854 (2003).
109. Loe DW, Sharom FJ: Interaction of multidrug-resistant chinese hamster ovary cells with amphiphiles. Br. J. Cancer 68(2), 342-351 (1993).
110. Rege BD, Kao JP, Polli JE: Effects of nonionic surfactants on membrane transporters in Caco-2 cell monolayers. Eur. J. Pharm. Sci. 16(4-5), 237-246 (2002).
111. Yamazaki T, Sato Y, Hanai M et al.: Non-ionic detergent Tween 80 modulates VP-16 resistance in classical multidrug resistant K562 cells via enhancement of VP-16 influx. Cancer Lett. 149(1-2), 153-161 (2000).
112. Dass CR: Drug delivery in cancer using liposomes. Methods Mol. Biol. 437, 177-182 (2008).
113. Mayer LD, Shabbits JA: The role for liposomal drug delivery in molecular and pharmacological strategies to overcome multidrug resistance. Cancer Metastasis Rev. 20(1-2), 87-93 (2001).
114. Rahman A, Husain SR, Siddiqui J et al.: Liposome-mediated modulation of multidrug resistance in human HL-60 leukemia cells. J. Natl Cancer Inst. 84(24), 1909-1915 (1992).
115. Thierry AR, Dritschilo A, Rahman A: Effect of liposomes on P-glycoprotein function in multidrug resistant cells. Biochem. Biophys. Res. Commun. 187(2), 1098-1105 (1992).
116. Warren L, Jardillier JC, Malarska A, Akeli MG: Increased accumulation of drugs in multidrug-resistant cells induced by liposomes. Cancer Res. 52(11), 3241-3245 (1992).
117. Ford JM, Hait WN: Pharmacology of drugs that alter multidrug resistance in cancer. Pharmacol. Rev. 42(3), 155-199 (1990).
118. Booser DJ, Esteva FJ, Rivera E et al.: Phase II study of liposomal annamycin in the treatment of doxorubicin-resistant breast cancer. Cancer Chemother. Pharmacol. 50(1), 6-8 (2002).
119. Hu YP, Henry-Toulme N, Robert J: Failure of liposomal encapsulation of doxorubicin to circumvent multidrug resistance in an in vitro model of rat glioblastoma cells. Eur. J. Cancer 31A(3), 389-394 (1995).
120. Rivera E, Valero V, Esteva FJ et al.: Lack of activity of stealth liposomal doxorubicin in the treatment of patients with anthracycline-resistant breast cancer. Cancer Chemother. Pharmacol. 49(4), 299-302 (2002).
121. Wang Y, Eksborg S, Lewensohn R, Lindberg A, Liliemark E: In vitro cellular accumulation and cytotoxicity of liposomal and conventional formulations of daunorubicin and doxorubicin in resistant K562 cells. Anticancer Drugs 10(10), 921-928 (1999).
122. Li X, Lu WL, Liang GW et al.: Effect of stealthy liposomal topotecan plus amlodipine on the multidrug-resistant leukaemia cells in vitro and xenograft in mice. Eur. J. Clin. Invest. 36(6), 409-418 (2006).
123. Wu J, Lu Y, Lee A et al.: Reversal of multidrug resistance by transferrin-conjugated liposomes co-encapsulating doxorubicin and verapamil. J. Pharm. Pharm. Sci. 10(3), 350-357 (2007).
124. Wang J, Goh B, Lu W et al.: In vitro cytotoxicity of stealth liposomes co-encapsulating doxorubicin and verapamil on doxorubicin-resistant tumor cells. Biol. Pharm. Bull. 28(5), 822-828 (2005).
125. Muller RH, Mader K, Gohla S: Solid lipid nanoparticles (SLN) for controlled drug delivery - a review of the state of the art. Eur. J. Pharm. Biopharm. 50(1), 161-177 (2000).
126. Manjunath K, Reddy JS, Venkateswarlu V: Solid lipid nanoparticles as drug delivery systems. Methods Find. Exp. Clin. Pharm. 27(2), 127-144 (2005).
127. Sahoo SK, Labhasetwar V: Enhanced antiproliferative activity of transferrin-conjugated paclitaxel-loaded nanoparticles is mediated via sustained intracellular drug retention. Mol. Pharm. 2(5), 373-383 (2005).
128. Barraud L, Merle P, Soma E et al.: Increase of doxorubicin sensitivity by doxorubicin-loading into nanoparticles for hepatocellular carcinoma cells in vitro and in vivo. J. Hepatol. 42(5), 736-743 (2005).
129. Chavanpatil MD, Khdair A, Gerard B et al.: Surfactant-polymer nanoparticles overcome P-glycoprotein-mediated drug efflux. Mol. Pharm. 4(5), 730-738 (2007).
130. Bennis S, Chapey C, Couvreur P, Robert J: Enhanced cytotoxicity of doxorubicin encapsulated in polyisohexylcyanoacrylate nanospheres against multidrug-resistant tumour cells in culture. Eur. J. Cancer 30A(1), 89-93 (1994).
131. Colin De Verdiere A, Dubernet C, Nemati F, Poupon MF, Puisieux F, Couvreur P: Uptake of doxorubicin from loaded nanoparticles in multidrug-resistant leukemic murine cells. Cancer Chemother. Pharmacol. 33(6), 504-508 (1994).
132. Wong HL, Rauth AM, Bendayan R et al.: A new polymer-lipid hybrid nanoparticle system increases cytotoxicity of doxorubicin against multidrug-resistant human breast cancer cells. Pharm. Res. 23(7), 1574-1585 (2006). (Pubitemid 43993820)
133. Astier A, Doat B, Ferrer MJ et al.: Enhancement of adriamycin antitumor activity by its binding with an intracellular sustained-release form, polymethacrylate nanospheres, in U-937 cells. Cancer Res. 48(7), 1835-1841 (1988).
134. Colin De Verdiere A, Dubernet C, Nemati F et al.: Reversion of multidrug resistance with polyalkylcyanoacrylate nanoparticles: towards a mechanism of action. Br. J. Cancer 76(2), 198-205 (1997).
135. Pepin X, Attali L, Domrault C et al.: On the use of ion-pair chromatography to elucidate doxorubicin release mechanism from polyalkylcyanoacrylate nanoparticles at the cellular level. J. Chromatogr. B Biomed. Sci. Appl. 702(1-2), 181-191 (1997).
136. Brigger I, Dubernet C, Couvreur P: Nanoparticles in cancer therapy and diagnosis. Adv. Drug Deliv. Rev. 54(5), 631-651 (2002).
137. Wong HL, Bendayan R, Rauth AM, Xue HY, Babakhanian K, Wu XY: A mechanistic study of enhanced doxorubicin uptake and retention in multidrug resistant breast cancer cells using a polymer-lipid hybrid nanoparticle system. J. Pharmacol. Exp. Ther. 317(3), 1372-1381 (2006).
138. Garcion E, Lamprecht A, Heurtault B et al.: A new generation of anticancer, drug-loaded, colloidal vectors reverses multidrug resistance in glioma and reduces tumor progression in rats. Mol. Cancer Ther. 5(7), 1710-1722 (2006).
139. Lamprecht A, Benoit JP: Etoposide nanocarriers suppress glioma cell growth by intracellular drug delivery and simultaneous P-glycoprotein inhibition. J. Control. Release 112(2), 208-213 (2006).
140. Dong X, Mattingly CA, Tseng MTet al.: Doxorubicin and paclitaxel-loaded lipid-based nanoparticles overcome multidrug resistance by inhibiting P-glycoprotein and depleting ATP. Cancer Res. 69(9), 3918-3926 (2009).
141. Koziara JM, Whisman TR, Tseng MT, Mumper RJ: In vivo efficacy of novel paclitaxel nanoparticles in paclitaxel-resistant human colorectal tumors. J. Control. Release 112(3), 312-319 (2006).
142. Chavanpatil MD, Patil Y, Panyam J: Susceptibility of nanoparticle- encapsulated paclitaxel to P-glycoprotein-mediated drug efflux. Int. J. Pharm. 320(1-2), 150-156 (2006).
143. Omelyanenko V, Kopeckova P, Gentry C, Kopecek J: Targetable HPMA copolymer-adriamycin conjugates. Recognition, internalization and subcellular fate. J. Control. Release 53(1-3), 25-37 (1998).
144. Nori A, Kopecek J: Intracellular targeting of polymer-bound drugs for cancer chemotherapy. Adv. Drug Deliv. Rev. 57(4), 609-636 (2005).
145. Kopecek J, Kopeckova P, Minko T, Lu Z: HPMA copolymer-anticancer drug conjugates: design, activity and mechanism of action. Eur. J. Pharm. Biopharm. 50(1), 61-81 (2000).
146. Minko T, Kopeckova P, Kopecek J: Chronic exposure to HPMA copolymer-bound adriamycin does not induce multidrug resistance in a human ovarian carcinoma cell line. J. Control. Release 59(2), 133-148 (1999).
147. Minko T, Kopeckova P, Kopecek J: Comparison of the anticancer effect of free and HPMA copolymer-bound adriamycin in human ovarian carcinoma cells. Pharm. Res. 16(7), 986-996 (1999). (Pubitemid 29368143)
148. Minko T, Kopeckova P, Kopecek J: Preliminary evaluation of caspases-dependent apoptosis signaling pathways of free and HPMA copolymer-bound doxorubicin in human ovarian carcinoma cells. J. Control. Release 71(3), 227-237 (2001).
149. Minko T, Kopeckova P, Kopecek J: Efficacy of the chemotherapeutic action of HPMA copolymer-bound doxorubicin in a solid tumor model of ovarian carcinoma. Int. J. Cancer 86(1), 108-117 (2000).
150. Piskin, Kaitian X, Denkbas EB, Kucukyavuz Z: Novel PDLLA/PEG copolymer micelles as drug carriers. J. Biomater. Sci. 7(4), 359-373 (1995).
151. La SB, Okano T, Kataoka K: Preparation and characterization of the micelle-forming polymeric drug indomethacin-incorporated poly(ethylene oxide)-poly(b-benzyl l-aspartate) block copolymer micelles. J. Pharm. Sci. 85(1), 85-90 (1996).
152. Alakhov VY, Moskaleva E, Batrakova EV, Kabanov AV: Hypersensitization of multidrug resistant human ovarian carcinoma cells by Pluronic P85 block copolymer. Bioconjug. Chem. 7(2), 209-216 (1996).
153. Batrakova EV, Kabanov AV: Pluronic block copolymers: evolution of drug delivery concept from inert nanocarriers to biological response modifiers. J. Control. Release 130(2), 98-106 (2008).
154. Kabanov AV, Batrakova EV, Alakhov VY: Pluronic block copolymers for overcoming drug resistance in cancer. Adv. Drug Deliv. Rev. 54(5), 759-779 (2002).
155. Alakhov VY, Klinski E, Li S et al.: Block copolymer-based formulation of doxorubicin. From cell screen to clinical trials. Colloids Surf. B Biointerfaces 16, 113-134 (1999).
156. Batrakova EV, Li S, Li Y, Alakhov VY, Elmquist WF, Kabanov AV: Distribution kinetics of a micelle-forming block copolymer Pluronic P85. J. Control. Release 100(3), 389-397 (2004).
157. Pruitt JD, Husseini G, Rapoport N, Pitt WG: Stabilization of Pluronic P-105 micelles with an interpenetrating network of N,N-diethylacrylamide. Macromolecules 33, 9306-9309 (2000).
158. Yang TF, Chen CN, Chen MC, Lai CH, Liang HF, Sung HW: Shell-crosslinked Pluronic l121 micelles as a drug delivery vehicle. Biomaterials 28(4), 725-734 (2007).
159. Batrakova EV, Li S, Vinogradov SV, Alakhov VY, Miller DW, Kabanov AV: Mechanism of Pluronic effect on P-glycoprotein efflux system in blood-brain barrier: contributions of energy depletion and membrane fluidization. J. Pharmacol. Exp. Ther. 299(2), 483-493 (2001).
160. Batrakova EV, Li S, Li Y, Alakhov VY, Kabanov AV: Effect of Pluronic P85 on ATPase activity of drug efflux transporters. Pharm. Res. 21(12), 2226-2233 (2004).
161. Batrakova EV, Li S, Elmquist WF, Miller DW, Alakhov VY, Kabanov AV: Mechanism of sensitization of MDR cancer cells by Pluronic block copolymers: selective energy depletion. Br. J. Cancer 85(12), 1987-1997 (2001).
162. Minko T, Batrakova EV, Li S et al.: Pluronic block copolymers alter apoptotic signal transduction of doxorubicin in drug-resistant cancer cells. J. Control. Release 105(3), 269-278 (2005).
163. Batrakova EV, Li S, Alakhov VY, Elmquist WF, Miller DW, Kabanov AV: Sensitization of cells overexpressing multidrug-resistant proteins by Pluronic P85. Pharm. Res. 20(10), 1581-1590 (2003).
164. Alakhova DY, Rapoport NY, Batrakova EV et al.: Differential metabolic responses to Pluronic in MDR and non-MDR cells: a novel pathway for chemosensitization of drug resistant cancers. J. Control. Release 142(1), 89-100 (2009).