Rationally designed nanovehicles to overcome cancer chemoresistance

Advanced Drug Delivery Reviews

Volumn 65, Issue 13-14, 2013, Pages 1716-1730

  Livney, Yoav D ^a   Assaraf, Yehuda G ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Cancer; Diagnostic imaging; MDR; Multifunctional nanovehicles; Nanomedicine; Overcoming drug resistance; Polymeric nanoparticles; Quadrugnostic; Theranostic

Indexed keywords

CANCER; DIAGNOSTIC IMAGING; DRUG RESISTANCE; MDR; NANOVEHICLES; POLYMERIC NANOPARTICLES; QUADRUGNOSTIC; THERANOSTIC;

CHEMOTHERAPY; LIPOSOMES; MEDICAL NANOTECHNOLOGY; NANOPARTICLES; POLYMERS;

DISEASES;

ARABINOGALACTAN; CETRIMIDE; COPOLYMER; DIAGNOSTIC AGENT; DOXORUBICIN; LIGAND; LIPOSOME; LONIDAMINE; LOW MOLECULAR WEIGHT SURFACTANT; MACROGOL; MEMBRANE PROTEIN; METAL NANOPARTICLE; METHOTREXATE; MONOCLONAL ANTIBODY; N (2 HYDROXYPROPYL)METHACRYLAMIDE; NANOCARRIER; POLYCAPROLACTONE; POLYGLACTIN; POLYMER; PROTEIN ANTIBODY; PROTEIN MDM2; PROTEIN P53; PROTEIN TYROSINE KINASE INHIBITOR; SURFACTANT; THERANOSTIC NANOVEHICLE; TOPOTECAN; TRASTUZUMAB; UNCLASSIFIED DRUG; UNINDEXED DRUG; VERAPAMIL; VINCRISTINE;

ACTIVE TARGETING; BIODEGRADABILITY; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER RESISTANCE; CANCER STEM CELL; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CHEMOSENSITIZATION; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG FORMULATION; DRUG RELEASE; DRUG SOLUBILITY; GENE SILENCING; HUMAN; HYPERTHERMIA; MEDICAL DEVICE; MULTIDRUG RESISTANCE; NANOMEDICINE; NANOTECHNOLOGY; NONHUMAN; PASSIVE TARGETING; PH; PHOTODYNAMIC THERAPY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

CANCER; DIAGNOSTIC IMAGING; MDR; MULTIFUNCTIONAL NANOVEHICLES; NANOMEDICINE; OVERCOMING DRUG RESISTANCE; POLYMERIC NANOPARTICLES; QUADRUGNOSTIC; THERANOSTIC;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG CARRIERS; DRUG DESIGN; DRUG RESISTANCE, NEOPLASM; HUMANS; LIGANDS; NANOPARTICLES; NEOPLASMS;

EID: 84888205791     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2013.08.006     Document Type: Review

References (154)

1. Luqmani Y.A. Mechanisms of drug resistance in cancer chemotherapy. Med. Prin. Pract. 2005, 14:35-48.
2. Gao Z.B., Zhang L.N., Sun Y.J. Nanotechnology applied to overcome tumor drug resistance. J. Control. Release 2012, 162:45-55.
3. Gonen N., Assaraf Y.G. Antifolates in cancer therapy: structure, activity and mechanisms of drug resistance. Drug Resist. Updat. 2012, 15:183-210.
4. Adar Y., Stark M., Bram E.E., Nowak-Sliwinska P., van den Bergh H., Szewczyk G., Sarna T., Skladanowski A., Griffioen A.W., Assaraf Y.G. Imidazoacridinone-dependent lysosomal photodestruction: a pharmacological Trojan horse approach to eradicate multidrug-resistant cancers. Cell Death Dis. 2012, 3.
5. Ifergan I., Scheffer G.L., Assaraf Y.G. Novel extracellular vesicles mediate an ABCG2-dependent anticancer drug sequestration and resistance. Cancer Res. 2005, 65:10952-10958.
6. Goler-Baron V., Assaraf Y.G. Structure and function of ABCG2-rich extracellular vesicles mediating multidrug resistance. PLoS One 2011, 6.
7. Baguley B.C. Multiple drug resistance mechanisms in cancer. Mol. Biotechnol. 2010, 46:308-316.
8. Shapira A., Livney Y.D., Broxterman H.J., Assaraf Y.G. Nanomedicine for targeted cancer therapy: towards the overcoming of drug resistance. Drug Resist. Updat. 2011, 14:150-163.
9. Assaraf Y.G. Molecular basis of antifolate resistance. Cancer Metastasis Rev. 2007, 26:153-181.
10. Siddiqui A., Patwardhan G.A., Liu Y.Y., Nazzal S. Mixed backbone antisense glucosylceramide synthase oligonucleotide (MBO-asGCS) loaded solid lipid nanoparticles: In vitro characterization and reversal of multidrug resistance in NCI/ADR-RES cells. Int. J. Pharm. 2010, 400:251-259.
11. Cukierman E., Khan D.R. The benefits and challenges associated with the use of drug delivery systems in cancer therapy. Biochem. Pharmacol. 2010, 80:762-770.
12. Li R.T., Xie L., Zhu Z.S., Liu Q., Hu Y., Jiang X.Q., Yu L.X., Qian X.P., Guo W.H., Ding Y.T., Liu B.R. Reversion of pH-induced physiological drug resistance: a novel function of copolymeric nanoparticles. PLoS One 2011, 6.
13. Amiri-Kordestani L., Basseville A., Kurdziel K., Fojo A.T., Bates S.E. Targeting MDR in breast and lung cancer: discriminating its potential importance from the failure of drug resistance reversal studies. Drug Resist. Updat. 2012, 15:50-61.
14. Xia C.Q., Smith P.G. Drug efflux transporters and multidrug resistance in acute leukemia: therapeutic impact and novel approaches to mediation. Mol. Pharmacol. 2012, 82:1008-1021.
15. Assaraf Y.G. The role of multidrug resistance efflux transporters in antifolate resistance and folate homeostasis. Drug Resist. Updat. 2006, 9:227-246.
16. Szakacs G., Paterson J.K., Ludwig J.A., Booth-Genthe C., Gottesman M.M. Targeting multidrug resistance in cancer. Nat. Rev. Drug Discov. 2006, 5:219-234.
17. Gottesman M.M. Mechanisms of cancer drug resistance. Annu. Rev. Med. 2002, 53:615-627.
18. Dong X.W., Mumper R.J. Nanomedicinal strategies to treat multidrug-resistant tumors: current progress. Nanomedicine 2010, 5:597-615.
19. de Wilt L.H.A.M., Jansen G., Assaraf Y.G., van Meerloo J., Cloos J., Schimmer A.D., Chan E.T., Kirk C.J., Peters G.J., Kruyt F.A.E. Proteasome-based mechanisms of intrinsic and acquired bortezomib resistance in non-small cell lung cancer. Biochem. Pharmacol. 2012, 83:207-217.
20. Denison T.A., Bae Y.H. Tumor heterogeneity and its implication for drug delivery. J. Control. Release 2012, 164:187-191.
21. Bu H.H., Gao Y., Li Y.P. Overcoming multidrug resistance (MDR) in cancer by nanotechnology. Sci. China-Chem. 2010, 53:2226-2232.
22. Hu C.M.J., Zhang L.F. Nanoparticle-based combination therapy toward overcoming drug resistance in cancer. Biochem. Pharmacol. 2012, 83:1104-1111.
23. Montesinos R.N., Beduneau A., Pellequer Y., Lamprecht A. Delivery of P-glycoprotein substrates using chemosensitizers and nanotechnology for selective and efficient therapeutic outcomes. J. Control. Release 2012, 161:50-61.
24. Nobili S., Landini I., Mazzei T., Mini E. Overcoming tumor multidrug resistance using drugs able to evade P-glycoprotein or to exploit its expression. Med. Res. Rev. 2012, 32:1220-1262.
25. Zhang H., Jiang H., Wang X., Chen B.A. Reversion of multidrug resistance in tumor by biocompatible nanomaterials. Mini-Rev. Med. Chem. 2010, 10:737-745.
26. Parhi P., Mohanty C., Sahoo S.K. Nanotechnology-based combinational drug delivery: an emerging approach for cancer therapy. Drug Discov. Today 2012, 17:1044-1052.
27. Deng C., Jiang Y.J., Cheng R., Meng F.H., Zhong Z.Y. Biodegradable polymeric micelles for targeted and controlled anticancer drug delivery: promises, progress and prospects. Nano Today 2012, 7:467-480.
28. Wei Z., Yuan S., Chen Y.Z., Yu S.Y., Hao J.G., Luo J.Q., Sha X.Y., Fang X.L. Enhanced antitumor efficacy by Paclitaxel-loaded Pluronic P123/F127 mixed micelles against non-small cell lung cancer based on passive tumor targeting and modulation of drug resistance. Eur. J. Pharm. Biopharm. 2010, 75:341-353.
29. Bajelan E., Haeri A., Vali A.M., Ostad S.N., Dadashzadeh S. Co-delivery of doxorubicin and PSC 833 (Valspodar) by stealth nanoliposomes for efficient overcoming of multidrug resistance. J. Pharm. Pharm. Sci. 2012, 15:568-582.
30. Patel N.R., Rathi A., Mongayt D., Torchilin V.P. Reversal of multidrug resistance by co-delivery of tariquidar (XR9576) and paclitaxel using long-circulating liposomes. Int. J. Pharm. 2011, 416:296-299.
31. Liu Y., Huang L., Liu F. Paclitaxel nanocrystals for overcoming multidrug resistance in cancer. Mol. Pharm. 2010, 7:863-869.
32. Alvarez-Lorenzo C., Sosnik A., Concheiro A. PEO-PPO block copolymers for passive micellar targeting and overcoming multidrug resistance in cancer therapy. Curr. Drug Targets 2011, 12:1112-1130.
33. Chen C.H., Cuong N.V., Chen Y.T., So R.C., Liau I., Hsieh M.F. Overcoming multidrug resistance of breast cancer cells by the micellar doxorubicin nanoparticles of mPEG-PCL-graft-cellulose. J. Nanosci. Nanotechnol. 2011, 11:53-60.
34. Kunjachan S., Blauz A., Mockel D., Theek B., Kiessling F., Etrych T., Ulbrich K., van Bloois L., Storm G., Bartosz G., Rychlik B., Lammers T. Overcoming cellular multidrug resistance using classical nanomedicine formulations. Eur. J. Pharm. Sci. 2012, 45:421-428.
35. Zhang P., Ling G.X., Sun J., Zhang T.H., Yuan Y., Sun Y.B., Wang Z.Y., He Z.G. Multifunctional nanoassemblies for vincristine sulfate delivery to overcome multidrug resistance by escaping P-glycoprotein mediated efflux. Biomaterials 2011, 32:5524-5533.
36. Xia W., Low P.S. Folate-targeted therapies for cancer. J. Med. Chem. 2010, 53:6811-6824.
37. Dhawan D., Ramos-Vara J.A., Naughton J.F., Cheng L., Low P.S., Rothenbuhler R., Leamon C.P., Parker N., Klein P.J., Vlahov I.R., Reddy J.A., Koch M., Murphy L., Fourez L.M., Stewart J.C., Knapp D.W. Targeting folate receptors to treat invasive urinary bladder cancer. Cancer Res. 2013, 73:875-884.
38. Fang J., Nakamura H., Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 2011, 63:136-151.
39. Maeda H., Bharate G.Y., Daruwalla J. Polymeric drugs for efficient tumor-targeted drug delivery based on EPR-effect. Eur. J. Pharm. Biopharm. 2009, 71:409-419.
40. Lei T.J., Srinivasan S., Tang Y., Manchanda R., Nagesetti A., Fernandez-Fernandez A., McGoron A.J. Comparing cellular uptake and cytotoxicity of targeted drug carriers in cancer cell lines with different drug resistance mechanisms. Nanomedicine 2011, 7:324-332.
41. Fowers K.D., Kopecek J. Targeting of multidrug-resistant human ovarian carcinoma cells with anti-P-glycoprotein antibody conjugates. Macromol. Biosci. 2012, 12:502-514.
42. Punfa W., Yodkeeree S., Pitchakarn P., Ampasavate C., Limtrakul P. Enhancement of cellular uptake and cytotoxicity of curcumin-loaded PLGA nanoparticles by conjugation with anti-P-glycoprotein in drug resistance cancer cells. Acta Pharmacol. Sin. 2012, 33:823-831.
43. Mamot C., Ritschard R., Wicki A., Kung W., Schuller J., Herrmann R., Rochlitz C. Immunoliposomal delivery of doxorubicin can overcome multidrug resistance mechanisms in EGFR-overexpressing tumor cells. J. Drug Target. 2012, 20:422-432.
44. Nielsen D.L., Kumler I., Palshof J.A.E., Andersson M. Efficacy of HER2-targeted therapy in metastatic breast cancer. Monoclonal antibodies and tyrosine kinase inhibitors. Breast 2013, 22:1-12.
45. Colombo M., Corsi F., Foschi D., Mazzantini E., Mazzucchelli S., Morasso C., Occhipinti E., Polito L., Prosperi D., Ronchi S., Verderio P. HER2 targeting as a two-sided strategy for breast cancer diagnosis and treatment: outlook and recent implications in nanomedical approaches. Pharmacol. Res. 2010, 62:150-165.
46. Pinhassi R., Assaraf Y., Farber S., Stark M., Ickowicz D., Drori S., Domb A., Livney Y. Arabinogalactan-Folic acid-drug conjugate for targeted delivery and target-activated release of anticancer drugs to folate receptor-overexpressing cells. Biomacromolecules 2010, 11:294-303.
47. Das M., Sahoo S.K. Folate decorated dual drug loaded nanoparticle: role of curcumin in enhancing therapeutic potential of nutlin-3a by reversing multidrug resistance. PLoS One 2012, 7.
48. Thiyagarajan S., Thirumalai K., Nirmala S., Biswas J., Krishnakumar S. Effect of curcumin on lung resistance-related protein (LRP) in retinoblastoma cells. Curr. Eye Res. 2009, 34:845-851.
49. Wang X., Li J., Wang Y.X., Koenig L., Gjyrezi A., Giannakakou P., Shin E.H., Tighiouart M., Chen Z., Nie S.M., Shin D.M. A folate receptor-targeting nanoparticle minimizes drug resistance in a human cancer model. ACS Nano 2011, 5:6184-6194.
50. Ai S.B., Jia T., Ai W.L., Duan J.L., Liu Y.M., Chen J., Liu X., Yang F., Tian Y., Huang Z.B. Targeted delivery of doxorubicin through conjugation with EGF receptor-binding peptide overcomes drug resistance in human colon cancer cells. Br. J. Pharmacol. 2013, 168:1719-1735.
51. Milane L., Duan Z.F., Amiji M. Development of EGFR-targeted polymer blend nanocarriers for combination paclitaxel/lonidamine delivery to treat multi-drug resistance in human breast and ovarian tumor cells. Mol. Pharm. 2011, 8:185-203.
52. Kiziltepe T., Ashley J.D., Stefanick J.F., Qi Y.M., Alves N.J., Handlogten M.W., Suckow M.A., Navari R.M., Bilgicer B. Rationally engineered nanoparticles target multiple myeloma cells, overcome cell-adhesion-mediated drug resistance, and show enhanced efficacy in vivo. Blood Cancer J. 2012, 2.
53. Jiang J., Yang S.-j., Wang J.-c., Yang L.-j., Xu Z.-z., Yang T., Liu X.-y., Zhang Q. Sequential treatment of drug-resistant tumors with RGD-modified liposomes containing siRNA or doxorubicin. Eur. J. Pharm. Biopharm. 2010, 76:170-178.
54. Xiong X.-B., Ma Z., Lai R., Lavasanifar A. The therapeutic response to multifunctional polymeric nano-conjugates in the targeted cellular and subcellular delivery of doxorubicin. Biomaterials 2010, 31:757-768.
55. Zhang Y.F., Wang J.C., Bian D.Y., Zhang X., Zhang Q. Targeted delivery of RGD-modified liposomes encapsulating both combretastatin A-4 and doxorubicin for tumor therapy: in vitro and in vivo studies. Eur. J. Pharm. Biopharm. 2010, 74:467-473.
56. Cao Y., Chen D.D., Zhao P.G., Liu L.N., Huang X.Y., Qi C., Liu Y.L., He H.X., Wang Q., Liu Y., Chen S. Intracellular delivery of mitomycin c with targeted polysaccharide conjugates against multidrug resistance. Ann. Biomed. Eng. 2011, 39:2456-2465.
57. Cao Y., Gu Y., Liu L.N., Yang Y., Zhao P.G., Su P., Liu L.Y., Qi C., Lei X., Yang C.J. Reversion of multidrug resistance using self-organized nanoparticles holding both doxorubicin and targeting moiety. Lett. Drug Des. Discov. 2010, 7:500-506.
58. Patil Y.B., Swaminathan S.K., Sadhukha T., Ma L., Panyam J. The use of nanoparticle-mediated targeted gene silencing and drug delivery to overcome tumor drug resistance. Biomaterials 2010, 31:358-365.
59. Sebens S., Schafer H. The tumor stroma as mediator of drug resistance - a potential target to improve cancer therapy?. Curr. Pharm. Biotechnol. 2012, 13:2259-2272.
60. Yu Y., Wang Z.H., Zhang L., Yao H.J., Zhang Y., Li R.J., Ju R.J., Wang X.X., Zhou J., Li N., Lu W.L. Mitochondrial targeting topotecan-loaded liposomes for treating drug-resistant breast cancer and inhibiting invasive metastases of melanoma. Biomaterials 2012, 33:1808-1820.
61. Li P.Y., Lai P.S., Hung W.C., Syu W.J. Poly(l-lactide)-vitamin E TPGS nanoparticles enhanced the cytotoxicity of doxorubicin in drug-resistant MCF-7 breast cancer cells. Biomacromolecules 2010, 11:2576-2582.
62. Stuart M.A.C., Huck W.T.S., Genzer J., Muller M., Ober C., Stamm M., Sukhorukov G.B., Szleifer I., Tsukruk V.V., Urban M., Winnik F., Zauscher S., Luzinov I., Minko S. Emerging applications of stimuli-responsive polymer materials. Nat. Mater. 2010, 9:101-113.
63. Tomasina J., Lheureux S., Gauduchon P., Rault S., Malzert-Freon A. Nanocarriers for the targeted treatment of ovarian cancers. Biomaterials 2013, 34:1073-1101.
64. He Q.J., Gao Y., Zhang L.X., Zhang Z.W., Gao F., Ji X.F., Li Y.P., Shi J.L. A pH-responsive mesoporous silica nanoparticles-based multi-drug delivery system for overcoming multi-drug resistance. Biomaterials 2011, 32:7711-7720.
65. Lee C.H., Cheng S.H., Huang I.P., Souris J.S., Yang C.S., Mou C.Y., Lo L.W. Intracellular pH-responsive mesoporous silica nanoparticles for the controlled release of anticancer chemotherapeutics. Angew. Chem. Int. Ed. 2010, 49:8214-8219.
66. Waugh A., Grant A. Anatomy and Physiology in Health and Illness 2007, Churchill Livingstone Elsevier. 10th ed.
67. Shalviri A., Raval G., Prasad P., Chan C., Liu Q., Heerklotz H., Rauth A.M., Wu X.Y. pH-dependent doxorubicin release from terpolymer of starch, polymethacrylic acid and polysorbate 80 nanoparticles for overcoming multi-drug resistance in human breast cancer cells. Eur. J. Pharm. Biopharm. 2012, 82:587-597.
68. Kim D., Lee E.S., Oh K.T., Gao Z.G., Bae Y.H. Doxorubicin-loaded polymeric micelle overcomes multidrug resistance of cancer by double-targeting folate receptor and early endosomal pH. Small 2008, 4:2043-2050.
69. Wang J.L., Sun J., Chen Q., Gao Y., Li L., Li H., Leng D.L., Wang Y.J., Sun Y.H., Jing Y.K., Wang S.L., He Z.G. Star-shape copolymer of lysine-linked di-tocopherol polyethylene glycol 2000 succinate for doxorubicin delivery with reversal of multidrug resistance. Biomaterials 2012, 33:6877-6888.
70. Meng H.A., Xue M., Xia T.A., Zhao Y.L., Tamanoi F., Stoddart J.F., Zink J.I., Nel A.E. Autonomous in vitro anticancer drug release from mesoporous silica nanoparticles by pH-sensitive nanovalves. J. Am. Chem. Soc. 2010, 132:12690-12697.
71. Huang I.P., Sun S.P., Cheng S.H., Lee C.H., Wu C.Y., Yang C.S., Lo L.W., Lai Y.K. Enhanced chemotherapy of cancer using pH-sensitive mesoporous silica nanoparticles to antagonize P-glycoprotein-mediated drug resistance. Mol. Cancer Ther. 2011, 10:761-769.
72. Gao Y., Chen L.L., Zhang Z.W., Chen Y., Li Y.P. Reversal of multidrug resistance by reduction-sensitive linear cationic click polymer/iMDR1-pDNA complex nanoparticles. Biomaterials 2011, 32:1738-1747.
73. Satchi-Fainaro R., Duncan R., Barnes C.M. Polymer therapeutics for cancer: current status and future challenges 2006, 193:1-65.
74. Lukianova-Hleb E.Y., Ren X.Y., Townley D., Wu X.W., Kupferman M.E., Lapotko D.O. Plasmonic nanobubbles rapidly detect and destroy drug-resistant tumors. Theranostics 2012, 2:976-987.
75. Lukianova-Hleb E.Y., Belyanin A., Kashinath S., Wu X., Lapotko D.O. Plasmonic nanobubble-enhanced endosomal escape processes for selective and guided intracellular delivery of chemotherapy to drug-resistant cancer cells. Biomaterials 2012, 33:1821-1826.
76. Lukianova-Hleb E.Y., Ren X., Zasadzinski J.A., Wu X., Lapotko D.O. Plasmonic nanobubbles enhance efficacy and selectivity of chemotherapy against drug-resistant cancer cells. Adv. Mater. 2012, 24:3831-3837.
77. Kievit F.M., Wang F.Y., Fang C., Mok H., Wang K., Silber J.R., Ellenbogen R.G., Zhang M.Q. Doxorubicin loaded iron oxide nanoparticles overcome multidrug resistance in cancer in vitro. J. Control. Release 2011, 152:76-83.
78. Li B., Xu H., Li Z., Yao M.F., Xie M., Shen H.J., Shen S., Wang X.S., Jin Y. Bypassing multidrug resistance in human breast cancer cells with lipid/polymer particle assemblies. Int. J. Nanomed. 2012, 7:187-197.
79. Li Z., Li B., Wang M., Xie M., Shen H.J., Shen S., Wang X.S., Guo X.M., Yao M.F., Jin Y. The role of endosome evasion bypass in the reversal of multidrug resistance by lipid/nanoparticle assemblies. J. Mater. Chem. B 2013, 1:1466-1474.
80. Li L.L., Huang X.L., Liu T.L., Liu H.Y., Hao N.J., Chen D., Zhang Y.Q., Li L.F., Tang F.Q. Overcoming multidrug resistance with mesoporous silica nanorods as nanocarrier of doxorubicin. J. Nanosci. Nanotechnol. 2012, 12:4458-4466.
81. Shen J.N., He Q.J., Gao Y., Shi J.L., Li Y.P. Mesoporous silica nanoparticles loading doxorubicin reverse multidrug resistance: performance and mechanism. Nanoscale 2011, 3:4314-4322.
82. Sarisozen C., Vural I., Levchenko T., Hincal A.A., Torchilin V.P. PEG-PE-based micelles co-loaded with paclitaxel and cyclosporine A or loaded with paclitaxel and targeted by anticancer antibody overcome drug resistance in cancer cells. Drug Deliv. 2012, 19:169-176.
83. Song X.R., Zheng Y., He G., Yang L., Luo Y.F., He Z.Y., Li S.Z., Li J.M., Yu S., Luo X., Hou S.X., Wei Y.Q. Development of PLGA nanoparticles simultaneously loaded with vincristine and verapamil for treatment of hepatocellular carcinoma. J. Pharm. Sci. 2010, 99:4874-4879.
84. Misra R., Sahoo S.K. Coformulation of doxorubicin and curcumin in Poly(d,l-lactide-co-glycolide) nanoparticles suppresses the development of multidrug resistance in K562 cells. Mol. Pharm. 2011, 8:852-866.
85. Wang Y., Guo M., Lu Y., Ding L.Y., Ron W.T., Liu Y.Q., Song F.F., Yu S.Q. Alpha-tocopheryl polyethylene glycol succinate-emulsified poly(lactic-co-glycolic acid) nanoparticles for reversal of multidrug resistance in vitro. Nanotechnology 2012, 23.
86. Zhang Y.Q., Tang L., Sun L.L., Bao J.B., Song C.X., Huang L.Q., Liu K.X., Tian Y., Tian G., Li Z., Sun H.F., Mei L. A novel paclitaxel-loaded poly(epsilon-caprolactone)/Poloxamer 188 blend nanoparticle overcoming multidrug resistance for cancer treatment. Acta Biomater. 2010, 6:2045-2052.
87. Li X.R., Li P.Z., Zhang Y.H., Zhou Y.X., Chen X.W., Huang Y.Q., Liu Y. Novel mixed polymeric micelles for enhancing delivery of anticancer drug and overcoming multidrug resistance in tumor cell lines simultaneously. Pharm. Res. 2010, 27:1498-1511.
88. Saxena V., Hussain M.D. Poloxamer 407/TPGS mixed micelles for delivery of gambogic acid to breast and multidrug-resistant cancer. Int. J. Nanomed. 2012, 7:713-721.
89. Dong X., Mattingly C.A., Tseng M.T., Cho M.J., Liu Y., Adams V.R., Mumper R.J. Doxorubicin and paclitaxel-loaded lipid-based nanoparticles overcome multidrug resistance by inhibiting P-glycoprotein and depleting ATP. Cancer Res. 2009, 69:3918-3926.
90. Ma P., Dong X., Swadley C.L., Gupte A., Leggas M., Ledebur H.C., Mumper R.J. Development of idarubicin and doxorubicin solid lipid nanoparticles to overcome Pgp-mediated multiple drug resistance in leukemia. J. Biomed. Nanotechnol. 2009, 5:151-161.
91. Li R.B., Wu R., Zhao L., Wu M.H., Yang L., Zou H.F. P-glycoprotein antibody functionalized carbon nanotube overcomes the multidrug resistance of human leukemia cells. ACS Nano 2010, 4:1399-1408.
92. Langcharoen P., Punfa W., Yodkeeree S., Kasinrerk W., Ampasavate C., Anuchapreeda S., Limtrakul P. Anti-P-glycoprotein conjugated nanoparticles for targeting drug delivery in cancer treatment. Arch. Pharm. Res. 2011, 34:1679-1689.
93. Ji X.F., Gao Y., Chen L.L., Zhang Z.W., Deng Y.H., Li Y.P. Nanohybrid systems of non-ionic surfactant inserting liposomes loading paclitaxel for reversal of multidrug resistance. Int. J. Pharm. 2012, 422:390-397.
94. MacDiarmid J.A., Amaro-Mugridge N.B., Madrid-Weiss J., Sedliarou I., Wetzel S., Kochar K., Brahmbhatt V.N., Phillips L., Pattison S.T., Petti C., Stillman B., Graham R.M., Brahmbhatt H. Sequential treatment of drug-resistant tumors with targeted minicells containing siRNA or a cytotoxic drug. Nat. Biotechnol. 2009, 27:643-651.
95. Xu Z.H., Zhang Z.W., Chen Y., Chen L.L., Lin L.P., Li Y.P. The characteristics and performance of a multifunctional nanoassembly system for the co-delivery of docetaxel and iSur-pDNA in a mouse hepatocellular carcinoma model. Biomaterials 2010, 31:916-922.
96. MacDiarmid J.A., Brahmbhatt H. Minicells: Versatile vectors for targeted drug or si/shRNA cancer therapy. Current Opinion in Biotechnology 2011, 22:909-916.
97. Wang J.Q., Tao X.Y., Zhang Y.F., Wei D.Z., Ren Y.H. Reversion of multidrug resistance by tumor targeted delivery of antisense oligodeoxynucleotides in hydroxypropyl-chitosan nanoparticles. Biomaterials 2010, 31:4426-4433.
98. Shao S.L., Zhang W.W., Li X.Y., Zhang Z.Z., Yun D.Z., Fu B., Zuo M.X. Reversal of MDR1 gene-dependent multidrug resistance in HL60/HT9 cells using short hairpin RNA expression vectors. Cancer Biother. Radiopharm. 2010, 25:171-177.
99. Macadangdang B., Zhang N., Lund P.E., Marple A.H., Okabe M., Gottesman M.M., Appella D.H., Kimchi-Sarfaty C. Inhibition of multidrug resistance by SV40 pseudovirion delivery of an antigene peptide nucleic acid (PNA) in cultured cells. PLoS One 2011, 6.
100. He Y., Bi Y., Hua Y., Liu D.Y., Wen S., Wang Q., Li M.Y., Zhu J., Lin T., He D.W., Li X.L., Wang Z.G., Wei G.H. Ultrasound microbubble-mediated delivery of the siRNAs targeting MDR1 reduces drug resistance of yolk sac carcinoma L2 cells. J. Exp. Clin. Cancer Res. 2011, 30.
101. Milane L., Ganesh S., Shah S., Duan Z.F., Amiji M. Multi-modal strategies for overcoming tumor drug resistance: hypoxia, the Warburg effect, stem cells, and multifunctional nanotechnology. J. Control. Release 2011, 155:237-247.
102. Cao P.X., Bae Y. Polymer nanoparticulate drug delivery and combination cancer therapy. Future Oncol. 2012, 8:1471-1480.
103. Zahedi P., De Souza R., Huynh L., Piquette-Miller M., Allen C. Combination drug delivery strategy for the treatment of multidrug resistant ovarian cancer. Mol. Pharm. 2011, 8:260-269.
104. Liu Y.Y., Han T.Y., Yu J.Y., Bitterman A., Le A., Giuliano A.E., Cabot M.C. Oligonucleotides blocking glucosylceramide synthase expression selectively reverse drug resistance in cancer cells. J. Lipid Res. 2004, 45:933-940.
105. Chen Y.C., Bathula S.R., Li J., Huang L. Multifunctional nanoparticles delivering small interfering RNA and doxorubicin overcome drug resistance in cancer. J. Biol. Chem. 2010, 285:22639-22650.
106. Li F., Niu S.M., Sun J., Zhu H.S., Ba Q.J., Guo Y., Shi D.L. Efficient in vitro TRAIL-gene delivery in drug-resistant A2780/DDP ovarian cancer cell line via magnetofection. J. Nanomater. 2011, 2011:1-7.
107. Mena S., Ortega A., Estrela J.M. Oxidative stress in environmental-induced carcinogenesis. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2009, 674:36-44.
108. Batrakova E., Li S., Alakhov V., Elmquist W., Miller D., Kabanov A. Sensitization of cells overexpressing multidrug-resistant proteins by pluronic P85. Pharm. Res. 2003, 20:1581-1590.
109. Tamm I., Wang Y., Sausville E., Scudiero D.A., Vigna N., Oltersdorf T., Reed J.C. IAP-family protein Survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res. 1998, 58:5315-5320.
110. Shen J.A., Yin Q., Chen L.L., Zhang Z.W., Li Y.P. Co-delivery of paclitaxel and survivin shRNA by pluronic P85-PEI/TPGS complex nanoparticles to overcome drug resistance in lung cancer. Biomaterials 2012, 33:8613-8624.
111. Alama A., Orengo A.M., Ferrini S., Gangemi R. Targeting cancer-initiating cell drug-resistance: a roadmap to a new-generation of cancer therapies?. Drug Discov. Today 2012, 17:435-442.
112. Gottschling S., Schnabel P.A., Herth F.J.F., Herpel E. Are we missing the target? - Cancer stem cells and drug resistance in non-small cell lung cancer. Cancer Genomics Proteomics 2012, 9:275-286.
113. Lacerda L., Pusztai L., Woodward W.A. The role of tumor initiating cells in drug resistance of breast cancer: implications for future therapeutic approaches. Drug Resist. Updat. 2010, 13:99-108.
114. LaBarge M.A. The difficulty of targeting cancer stem cell niches. Clin. Cancer Res. 2010, 16:3121-3129.
115. Wang Z.W., Li Y.W., Ahmad A., Azmi A.S., Kong D.J., Banerjee S., Sarkar F.H. Targeting miRNAs involved in cancer stem cell and EMT regulation: an emerging concept in overcoming drug resistance. Drug Resist. Updat. 2010, 13:109-118.
116. Wang C.-H., Chiou S.-H., Chou C.-P., Chen Y.-C., Huang Y.-J., Peng C.-A. Photothermolysis of glioblastoma stem-like cells targeted by carbon nanotubes conjugated with CD133 monoclonal antibody. Nanomedicine 2011, 7:69-79.
117. Gilstrap K., Hu X., Lu X., He X. Nanotechnology for energy-based cancer therapies. Am. J. Cancer Res. 2011, 1:508-520.
118. Lu H.L., Syu W.J., Nishiyama N., Kataoka K., Lai P.S. Dendrimer phthalocyanine-encapsulated polymeric micelle-mediated photochemical internalization extends the efficacy of photodynamic therapy and overcomes drug-resistance in vivo. J. Control. Release 2011, 155:458-464.
119. 4 nanoparticles combined with chemotherapy and hyperthermia to overcome multidrug resistance. Int. J. Nanomed. 2012, 7:2261-2269.
120. Xing R.J., Bhirde A.A., Wang S.J., Sun X.L., Liu G., Hou Y.L., Chen X.Y. Hollow iron oxide nanoparticles as multidrug resistant drug delivery and imaging vehicles. Nano Res. 2013, 6:1-9.
121. Ai S.B., Duan J.L., Liu X., Bock S., Tian Y.A., Huang Z.B. Biological evaluation of a novel doxorubicin-peptide conjugate for targeted delivery to EGF receptor-overexpressing tumor cells. Mol. Pharm. 2011, 8:375-386.
122. Alberts D.S., Blessing J.A., Landrum L.M., Warshal D.P., Martin L.P., Rose S.L., Bonebrake A.J., Ramondetta L.M. Phase II trial of nab-paclitaxel in the treatment of recurrent or persistent advanced cervix cancer: a gynecologic oncology group study. Gynecol. Oncol. 2012, 127:451-455.
123. Shapira A., Assaraf Y., Epstein D., Livney Y. Beta-casein nanoparticles as an oral delivery system for chemotherapeutic drugs: impact of drug structure and properties on co-assembly. Pharm. Res. 2010, 27:2175-2186.
124. Shapira A., Assaraf Y., Livney Y. Beta-casein nanovehicles for oral delivery of chemotherapeutic drugs. Nanomedicine 2010, 6:119-126.
125. Shapira A., Markman G., Assaraf Y., Livney Y. Beta-casein-based nanovehicles for oral delivery of chemotherapeutic drugs: drug-protein interactions and mitoxantrone loading capacity. Nanomedicine 2010, 6:547-555.
126. Shapira A., Davidson I., Avni N., Assaraf Y.G., Livney Y.D. β-Casein nanoparticle-based oral drug delivery system for potential treatment of gastric carcinoma: stability, target-activated release and cytotoxicity. Eur. J. Pharm. Biopharm. 2012, 80:298-305.
127. Livney Y. Milk proteins as vehicles for bioactives. Curr. Opin. Colloid Interface Sci. 2010, 15:73-83.
128. Duan J.H., Mansour H.M., Zhang Y.D., Deng X.M., Chen Y.X., Wang J.W., Pan Y.F., Zhao J.F. Reversion of multidrug resistance by co-encapsulation of doxorubicin and curcumin in chitosan/poly(butyl cyanoacrylate) nanoparticles. Int. J. Pharm. 2012, 426:193-201.
129. Ren F., Chen R.D., Wang Y., Sun Y.B., Jiang Y.D., Li G.F. Paclitaxel-loaded poly(n-butylcyanoacrylate) nanoparticle delivery system to overcome multidrug resistance in ovarian cancer. Pharm. Res. 2011, 28:897-906.
130. Singh M., Bhatnagar P., Srivastava A.K., Kumar P., Shukla Y., Gupta K.C. Enhancement of cancer chemosensitization potential of cisplatin by tea polyphenols poly(lactide-co-glycolide) nanoparticles. J. Biomed. Nanotechnol. 2011, 7:202-202.
131. van Vlerken L.E., Duan Z.F., Little S.R., Seiden M.V., Amiji M.M. Augmentation of therapeutic efficacy in drug-resistant tumor models using ceramide coadministration in temporal-controlled polymer-blend nanoparticle delivery systems. AAPS J. 2010, 12:171-180.
132. Ling G.X., Zhang P., Zhang W.P., Sun J., Meng X.X., Qin Y.M., Deng Y.H., He Z.G. Development of novel self-assembled DS-PLGA hybrid nanoparticles for improving oral bioavailability of vincristine sulfate by P-gp inhibition. J. Control. Release 2010, 148:241-248.
133. Bisht S., Mizuma M., Feldmann G., Ottenhof N.A., Hong S.-M., Pramanik D., Chenna V., Karikari C., Sharma R., Goggins M.G., Rudek M.A., Ravi R., Maitra A., Maitra A. Systemic administration of polymeric nanoparticle-encapsulated curcumin (NanoCurc) blocks tumor growth and metastases in preclinical models of pancreatic cancer. Mol. Cancer Ther. 2010, 9:2255-2264.
134. Pramanik D., Campbell N.R., Das S., Gupta S., Chenna V., Bisht S., Sysa-Shah P., Bedja D., Karikari C., Steenbergen C., Gabrielson K.L., Maitra A. A composite polymer nanoparticle overcomes multidrug resistance and ameliorates doxorubicin-associated cardiomyopathy. Oncotarget 2012, 3:640-650.
135. Du Y.Z., Wang L., Yuan H., Hu F.Q. Linoleic acid-grafted chitosan oligosaccharide micelles for intracellular drug delivery and reverse drug resistance of tumor cells. Int. J. Biol. Macromol. 2011, 48:215-222.
136. Xu Y.Y., Du Y.Z., Yuan H., Liu L.N., Niu Y.P., Hu F.Q. Improved cytotoxicity and multidrug resistance reversal of chitosan based polymeric micelles encapsulating oxaliplatin. J. Drug Target. 2011, 19:344-353.
137. Vergara D., Bellomo C., Zhang X.C., Vergaro V., Tinelli A., Lorusso V., Rinaldi R., Lvov Y.M., Leporatti S., Maffia M. Lapatinib/Paclitaxel polyelectrolyte nanocapsules for overcoming multidrug resistance in ovarian cancer. Nanomedicine 2012, 8:891-899.
138. Zhang P., Ling G.X., Pan X.L., Sun J., Zhang T.H., Pu X.H., Yin S.L., He Z.G. Novel nanostructured lipid-dextran sulfate hybrid carriers overcome tumor multidrug resistance of mitoxantrone hydrochloride. Nanomedicine 2012, 8:185-193.
139. Urbinati G., Marsaud V., Renoir J.M. Anticancer drugs in liposomal nanodevices: a target delivery for a targeted therapy. Curr. Top. Med. Chem. 2012, 12:1693-1712.
140. Ho J.A.A., Fan N.C., Jou A.F.J., Wu L.C., Sun T.P. Monitoring the subcellular localization of doxorubicin in CHO-K1 using MEKC-LIF: liposomal carrier for enhanced drug delivery. Talanta 2012, 99:683-688.
141. Burke A.C., Giles F.J. Elacytarabine - lipid vector technology overcoming drug resistance in acute myeloid leukemia. Expert Opin. Investig. Drugs 2011, 20:1707-1715.
142. Chaurasiya A., Singh A.K., Jain G.K., Warsi M.H., Sublet E., Ahmad F.J., Borchard G., Khar R.K. Dual approach utilizing self microemulsifying technique and novel P-gp inhibitor for effective delivery of taxanes. J. Microencapsul. 2012, 29:583-595.
143. Kang K.W., Chun M.K., Kim O., Subedi R.K., Ahn S.G., Yoon J.H., Choi H.K. Doxorubicin-loaded solid lipid nanoparticles to overcome multidrug resistance in cancer therapy. Nanomedicine 2010, 6:210-213.
144. Mahmood M., Xu Y., Dantuluri V., Mustafa T., Zhang Y., Karmakar A., Casciano D., Ali S., Biris A. Carbon nanotubes enhance the internalization of drugs by cancer cells and decrease their chemoresistance to cytostatics. Nanotechnology 2013, 24.
145. Xu X., Li R.B., Ma M., Wang X., Wang Y.H., Zou H.F. Multidrug resistance protein P-glycoprotein does not recognize nanoparticle C-60: experiment and modeling. Soft Matter 2012, 8:2915-2923.
146. Wu J., Wang Y.S., Yang X.Y., Liu Y.Y., Yang J.R., Yang R., Zhang N. Graphene oxide used as a carrier for adriamycin can reverse drug resistance in breast cancer cells. Nanotechnology 2012, 23.
147. Gao Y., Chen Y., Ji X.F., He X.Y., Yin Q., Zhang Z.W., Shi J.L., Li Y.P. Controlled intracellular release of doxorubicin in multidrug-resistant cancer cells by tuning the shell-pore sizes of mesoporous silica nanoparticles. ACS Nano 2011, 5:9788-9798.
148. Meng H., Mai W.X., Zhang H.Y., Xue M., Xia T., Lin S.J., Wang X., Zhao Y., Ji Z.X., Zink J.I., Nel A.E. Codelivery of an optimal drug/siRNA combination using mesoporous silica nanoparticles to overcome drug resistance in breast cancer in vitro and in vivo. ACS Nano 2013, 7:994-1005.
149. Gu Y.J., Cheng J.P., Man C.W.Y., Wong W.T., Cheng S.H. Gold-doxorubicin nanoconjugates for overcoming multidrug resistance. Nanomedicine 2012, 8:204-211.
150. Tomuleasa C., Soritau O., Orza A., Dudea M., Petrushev B., Mosteanu O., Susman S., Florea A., Pall E., Aldea M., Kacso G., Cristea V., Berindan-Neagoe I., Irimie A. Gold nanoparticles conjugated with cisplatin/doxorubicin/capecitabine lower the chemoresistance of hepatocellular carcinoma-derived cancer cells. J. Gastrointest. Liver Dis. 2012, 21:187-196.
151. Liu J.H., Zhao Y.X., Guo Q.Q., Wang Z., Wang H.Y., Yang Y.X., Huang Y.Z. TAT-modified nanosilver for combating multidrug-resistant cancer. Biomaterials 2012, 33:6155-6161.
152. Wagstaff K.M., Jans D.A. Protein transduction: cell penetrating peptides and their therapeutic applications. Curr. Med. Chem. 2006, 13:1371-1387.
153. Beljanski V., Hiscott J. The use of oncolytic viruses to overcome lung cancer drug resistance. Curr. Opin. Virol. 2012, 2:629-635.
154. Xiong X.B., Lavasanifar A. Traceable multifunctional micellar nanocarriers for cancer-targeted co-delivery of MDR-1 siRNA and doxorubicin. ACS Nano 2011, 5:5202-5213.