Combating P-glycoprotein-mediated multidrug resistance using therapeutic nanoparticles

Current Pharmaceutical Design

Volumn 19, Issue 37, 2013, Pages 6655-6666

  Zhang, Qiu ^a   Li, Fei ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Cancer chemotherapy; Drug delivery; Multidrug resistance; Nanotechnology; P glycoprotein; Therapeutic nanoparticles

Indexed keywords

ALBUMIN; ANTHRACYCLINE; CYCLOPHOSPHAMIDE; DENDRIMER; DOCETAXEL; DOXORUBICIN; EPIPODOPHYLLOTOXIN; ETOPOSIDE; GOLD NANOPARTICLE; IMMUNOLIPOSOME; IRINOTECAN; LIPID; LIPOSOME; MACROGOL; MITOMYCIN; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; NANOCAPSULE; NANOCARRIER; NANOPARTICLE; PACLITAXEL; POLOXAMER; POLYMER; SINGLE WALLED NANOTUBE; STYRENE MALEIC ANHYDRIDE COPOLYMER; SURFACTANT; UNINDEXED DRUG; VINBLASTINE; VINCRISTINE;

ACTIVE TRANSPORT; ANTINEOPLASTIC ACTIVITY; BREAST CANCER; BREAST METASTASIS; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CONTROLLED DRUG RELEASE; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG FORMULATION; DRUG SAFETY; DRUG SOLUBILITY; DRUG TARGETING; ENDOCYTOSIS; ENERGY; GLIOMA; HUMAN; HYPERTHERMIC THERAPY; INTERNALIZATION; KAPOSI SARCOMA; LEUKEMIA; LIVER CELL CARCINOMA; LUNG CANCER; MICELLE; MOUTH CANCER; MULTIDRUG RESISTANCE; NANOEMULSION; NONHODGKIN LYMPHOMA; NONHUMAN; OVARY CANCER; OVARY TUMOR; OXIDATION REDUCTION POTENTIAL; PASSIVE TRANSPORT; PH; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PHASE 4 CLINICAL TRIAL (TOPIC); PHOTOCHEMISTRY; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RECURRENT CANCER; REVIEW; SOLID TUMOR; STIMULUS RESPONSE; ULTRASOUND; UTERINE CERVIX CANCER; UTERUS CANCER;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; NANOPARTICLES; NEOPLASMS; P-GLYCOPROTEINS;

EID: 84887884596     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811319370009     Document Type: Review

References (143)

1. Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev 2010; 19: 1893-907.
2. Longley D, Johnston P. Molecular mechanisms of drug resistance. J Pathol 2005; 205: 275-92.
3. Stein W, Bates S, Fojo T. Intractable cancers: the many faces of multidrug resistance and the many targets it presents for therapeutic attack. Curr Drug Targets 2004; 5: 333-46.
4. Shabbits JA, Krishna R, Mayer LD. Molecular and pharmacological strategies to overcome multidrug resistance. Expert Rev Anticancer Ther 2001; 1: 585-94.
5. Eckford PDW, Sharom FJ. ABC efflux pump-based resistance to chemotherapy drugs. Chem Rev 2009; 109: 2989-3011.
6. Ozben T. Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Lett 2006; 580: 2903-9.
7. Hu C-MJ, Zhang L. Therapeutic nanoparticles to combat cancer drug resistance. Curr Drug Metab 2009; 10: 836-41.
8. Gottesman MM. Mechanisms of cancer drug resistance. Annu Rev Med 2002; 53: 615-27.
9. Gillet JP, Gottesman MM. Mechanisms of multidrug resistance in cancer. Methods Mol Biol 2010; 596: 47-76.
10. Constantinides PP, Wasan KM. Lipid formulation strategies for enhancing intestinal transport and absorption of Pglycoprotein (P-gp) substrate drugs: In vitro/In vivo case studies. J Pharm Sci 2007; 96: 235-48.
11. Couvreur P, Roblot-Treupel L, Poupon M, Brasseur F, Puisieux F. Nanoparticles as microcarriers for anticancer drugs. Adv Drug Deliv Rev 1990; 5: 209-30.
12. Banerjee D, Sengupta S. Nanoparticles in cancer chemotherapy. Prog Mol Biol Transl Sci 2011; 104: 489-507.
13. Kubiak C, Couvreur P, Manil L, Clausse B. Increased eytotoxicity of nanoparticle-carried Adriamycin in vitro and potentiation by verapamil and amiodarone. Biomaterials 1989; 10: 553-6.
14. Cuvier C, Roblot-Treupel L, Millot J, et al. Doxorubicin-loaded nanospheres bypass tumor cell multidrug resistance. Biochem Pharmacol 1992; 44: 509-17.
15. Chinn L, Kroetz D. ABCB1 pharmacogenetics: progress, pitfalls, and promise. Clin Pharmacol Ther 2007; 81: 265-9.
16. Azzaria M, Schurr E, Gros P. Discrete mutations introduced in the predicted nucleotide-binding sites of the mdr1 gene abolish its ability to confer multidrug resistance. Mol Cell Biol 1989; 9: 5289-97.
17. Ambudkar SV, Lelong IH, Zhang J, Cardarelli CO, Gottesman MM, Pastan I. Partial purification and reconstitution of the human multidrug-resistance pump: characterization of the drugstimulatable ATP hydrolysis. Proc Natl Acad Sci USA 1992; 89: 8472-6.
18. Endicott JA, Ling V. The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu Rev Biochem 1989; 58: 137-71.
19. Gottesman MM, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 1993; 62: 385-427.
20. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002; 2: 48-58.
21. van Helvoort A, Smith AJ, Sprong H, et al. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 Pglycoprotein specifically translocates phosphatidylcholine. Cell 1996; 87: 507-17.
22. De Graaf D, Sharma RC, Mechetner EB, Schimke RT, Roninson IB. P-glycoprotein confers methotrexate resistance in 3T6 cells with deficient carrier-mediated methotrexate uptake. Proc Natl Acad Sci USA 1996; 93: 1238-42.
23. Seelig A. A general pattern for substrate recognition by P-glycoprotein. Eur J Biochem 1998; 251: 252-61.
24. Ambudkar SV, Dey S, Hrycyna CA, Ramachandra M, Pastan I, Gottesman MM. Biochemical, cellular, and pharmacological aspects of the multidrug transporter 1. Annu Rev Pharmacol Toxicol 1999; 39: 361-98.
25. Zhang Y, Tang L, Sun L, et al. A novel paclitaxel-loaded poly(β-caprolactone)/Poloxamer 188 blend nanoparticle overcoming multidrug resistance for cancer treatment. Acta Biomater 2010; 6: 2045-52.
26. Zhang XG, Miao J, Dai YQ, Du YZ, Yuan H, Hu FQ. Reversal activity of nanostructured lipid carriers loading cytotoxic drug in multi-drug resistant cancer cells. Int J Pharm 2008; 361: 239-44.
27. Mei L, Zhang Y, Zheng Y, et al. A novel docetaxel-loaded poly (β-caprolactone)/pluronic F68 nanoparticle overcoming multidrug resistance for breast cancer treatment. Nanoscale Res Lett 2009; 4: 1530-9.
28. Li Y, Chen Y, Cuong N, Hsieh M, Preparation of Nanoparticles of AB 2 Triblock Copolymers for Doxorubicin Delivery, 6th World Congress of Biomechanics (WCB 2010), Singapore, 2010, pp. 1242-5.
29. Gu Y-J, Cheng J, Man CW-Y, Wong W-T, Cheng SH. Golddoxorubicin nanoconjugates for overcoming multidrug resistance. Nanomedicine 2012; 8: 204-11.
30. Michiro S, Arun I, Keinosuke R, et al. Doxorubicin loaded Polymeric Nanoparticulate Delivery System to overcome drug resistance in osteosarcoma. BMC Cancer 2009; 9: 399.
31. 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 2007; 10: 350-7.
32. Jiang J, Yang S-j, Wang J-c, et al. Sequential treatment of drugresistant tumors with RGD-modified liposomes containing siRNA or doxorubicin. European Journal of Pharmaceutics and Biopharmaceutics 2010; 76: 170-8.
33. Dong X, Mattingly CA, Tseng MT, et al. Doxorubicin and Paclitaxel-Loaded Lipid-Based Nanoparticles Overcome Multidrug Resistance by Inhibiting P-Glycoprotein and Depleting ATP. Cancer Res 2009; 69: 3918-26.
34. 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 2010; 31: 358-65.
35. Song XR, Cai Z, Zheng Y, et al. Reversion of multidrug resistance by co-encapsulation of vincristine and verapamil in PLGA nanoparticles. Eur J Pharm Sci 2009; 37: 300-5.
36. Khdair A, Di C, Patil Y, et al. Nanoparticle-mediated combination chemotherapy and photodynamic therapy overcomes tumor drug resistance. J Control Release 2010; 141: 137-44.
37. Kim D, Lee ES, Oh KT, Gao ZG, Bae YH. Doxorubicin-Loaded Polymeric Micelle Overcomes Multidrug Resistance of Cancer by DoubléTargeting Folate Receptor and Early Endosomal pH. Small 2008; 4: 2043-50.
38. Wang X, Li J, Wang Y, et al. A Folate Receptor-Targeting Nanoparticle Minimizes Drug Resistance in a Human Cancer Model. ACS Nano 2011; 5: 6184-94.
39. Yang X, Deng W, Fu L, et al. Folate-functionalized polymeric micelles for tumor targeted delivery of a potent multidrugresistance modulator FG020326. J Biomed Mater Res Part A 2008; 86A: 48-60.
40. Quintana A, Raczka E, Piehler L, et al. Design and function of a dendrimer-based therapeutic nanodevice targeted to tumor cells through the folate receptor. Pharm Res 2002; 19: 1310-6.
41. Gao Y, Chen Y, Ji X, et al. Controlled Intracellular Release of Doxorubicin in Multidrug-Resistant Cancer Cells by Tuning the Shell-Pore Sizes of Mesoporous Silica Nanoparticles. Acs Nano 2011; 5: 9788-98.
42. Li R, Wu R, Zhao L, Wu M, Yang L, Zou H. P-glycoprotein antibody functionalized carbon nanotube overcomes the multidrug resistance of human leukemia cells. Acs Nano 2010; 4: 1399-408.
43. Gu Y-J, Cheng J, Man CWY, Wong WT, Cheng SH. Golddoxorubicin nanoconjugates for overcoming multidrug resistance. Nanomedicine: Nanotechnol Biol Med 2012; 8: 204-11.
44. Hu CMJ, Zhang L. Nanoparticle-based combination therapy toward overcoming drug resistance in cancer. Biochem Pharmacol 2012; 83: 1104-11.
45. Dong X, Mumper RJ. Nanomedicinal strategies to treat multidrugresistant tumors: current progress. Nanomedicine 2010; 5: 597-615.
46. Cho K, Wang X, Nie S, Shin DM. Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer Res 2008; 14: 1310-6.
47. NCT01463072. Paclitaxel Albumin-Stabilized Nanoparticle Formulation in Treating Older Patients With Metastatic Breast Cancer. Available at http://clinicaltrials. gov/ct2/show/NCT01463072. [Accessed December 2012].
48. NCT00629499. Nanoparticle Albumin-Bound (Nab) Paclitaxel/Cyclophosphamide in Early-Stage Breast Cancer (With Trastuzumab in HER2 + Patients). Available at http://clinicaltrials. gov/ct2/show/NCT00629499. [Accessed May 2011].
49. NCT01702129. Anti-EGFR Immunoliposomes in Solid Tumors. Available at http://clinicaltrials. gov/ct2/show/NCT01702129. [Accessed October 2012].
50. NCT00734682. A Phase I Trial of Nanoliposomal CPT-11 (NL CPT-11) in Patients With Recurrent High-Grade Gliomas. Available at http://clinicaltrials. gov/ct2/show/NCT00734682. [Accessed May 2012].
51. NCT00912639. A Clinical Trial of Paclitaxel Loaded Polymeric Micelle in Patients With Taxane-Pretreated Recurrent Breast Cancer. Available at http://clinicaltrials. gov/ct2/show/NCT00912639. [Accessed June 2009].
52. NCT00350948. Ph 3 Randomized Study of Telcyta® + Liposomal Doxorubicin Vs Liposomal Doxorubicin in Platinum Refractory or Resistant Ovarian Cancer. Available at http://clinicaltrials. gov/ct2/show/NCT00350948. [Accessed June 2011].
53. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007; 2: 751-60.
54. Wang F, Zhang D, Zhang Q, et al. Synergistic effect of folatemediated targeting and verapamil-mediated P-gp inhibition with paclitaxel-polymer micelles to overcome multi-drug resistance. Biomaterials 2011; 32: 9444-56.
55. Patil Y, Sadhukha T, Ma L, Panyam J. Nanoparticle-mediated simultaneous and targeted delivery of paclitaxel and tariquidar overcomes tumor drug resistance. J Control Release 2009; 136: 21-9.
56. MacDiarmid JA, Amaro-Mugridge NB, Madrid-Weiss J, et al. Sequential treatment of drug-resistant tumors with targeted minicells containing siRNA or a cytotoxic drug. Nat Biotechnol 2009; 27: 643-51.
57. Hede S, Huilgol N. " Nano": The new nemesis of cancer. J Cancer Res Ther 2006; 2: 186-95.
58. Moghimi SM, Hunter AC, Murray JC. Nanomedicine: current status and future prospects. FASEB J 2005; 19: 311-30.
59. Jabr-Milane LS, van Vlerken LE, Yadav S, Amiji MM. Multifunctional nanocarriers to overcome tumor drug resistance. Cancer Treat Rev 2008; 34: 592-602.
60. Thornton G. Watching nanoparticles grow. Science 2003; 300: 1378-9.
61. Kim JS, Yoon TJ, Yu KN, et al. Cellular uptake of magnetic nanoparticle is mediated through energy-dependent endocytosis in A549 cells. J Vet Sci 2006; 7: 321-6.
62. de Verdiã A. Reversion of multidrug resistance with polyalkylcyanoacrylate nanoparticles: towards a mechanism of action. Br J Cancer 1997; 76: 198-205.
63. Chen B, Cheng J, Wu Y, et al. Reversal of multidrug resistance by magnetic Fe3O4 nanoparticle copolymerizating daunorubicin and 5-bromotetrandrine in xenograft nude-mice. Int J Nanomedicine 2009; 4: 73-8.
64. Astier A, Doat B, Ferrer MJ, et al. Enhancement of adriamycin antitumor activity by its binding with an intracellular sustainedrelease form, polymethacrylate nanospheres, in U-937 cells. Cancer Res 1988; 48: 1835-41.
65. Ren F, Chen R, Wang Y, Sun Y, Jiang Y, Li G. Paclitaxel-loaded poly (n-butylcyanoacrylate) nanoparticle delivery system to overcome multidrug resistance in ovarian cancer. Pharm Res 2011; 28: 897-906.
66. Collnot EM, Baldes C, Wempe MF, et al. Mechanism of inhibition of P-glycoprotein mediated efflux by vitamin E TPGS: influence on ATPase activity and membrane fluidity. Mol Pharm 2007; 4: 465-74.
67. Dintaman JM, Silverman JA. Inhibition of P-glycoprotein by D-β-tocopheryl polyethylene glycol 1000 succinate (TPGS). Pharm Res 1999; 16: 1550-6.
68. Xiao L, Xiong X, Sun X, et al. Role of cellular uptake in the reversal of multidrug resistance by PEG-b-PLA polymeric micelles. Biomaterials 2011; 32: 5148-57.
69. 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 2001; 299: 483-93.
70. Batrakova EV, Li S, Li Y, Alakhov VY, Kabanov AV. Effect of pluronic P85 on ATPase activity of drug efflux transporters. Pharm Res 2004; 21: 2226-33.
71. Yao HJ, Ju RJ, Wang XX, et al. The antitumor efficacy of functional paclitaxel nanomicelles in treating resistant breast cancers by oral delivery. Biomaterials 2011; 32: 3285-302.
72. Koziara JM, Lockman PR, Allen DD, Mumper RJ. Paclitaxel nanoparticles for the potential treatment of brain tumors. J Control Release 2004; 99: 259-69.
73. Murthy R, Shah NM. Strategies for Inhibition of P-Glycoproteins for Effective Treatment of Multidrug Resistance Tumors. J Biomed Nanotechnol 2007; 3: 1-17.
74. Jain TK, Morales MA, Sahoo SK, Leslie-Pelecky DL, Labhasetwar V. Iron oxide nanoparticles for sustained delivery of anticancer agents. Mol Pharm 2005; 2: 194-205.
75. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006; 25: 9-34.
76. Wang X, Yang L, Chen ZG, Shin DM. Application of nanotechnology in cancer therapy and imaging. CA Cancer J Clin 2008; 58: 97-110.
77. Brannon-Peppas L, Blanchette JO. Nanoparticle and targeted systems for cancer therapy. Adv Drug Deliv Rev 2004; 56: 1649-59.
78. Wang X, Li J, Wang Y, et al. A folate receptor-targeting nanoparticle minimizes drug resistance in a human cancer model. Acs Nano 2011; 5: 6184-94.
79. Yang X, Deng W, Fu L, et al. Folatéfunctionalized polymeric micelles for tumor targeted delivery of a potent multidrug resistance modulator FG020326. J Biomed Mater Res A 2008; 86: 48-60.
80. Tahara K, Kato Y, Yamamoto H, Kreuter J, Kawashima Y. Intracellular drug delivery using polysorbate 80-modified poly(D, L-lactide-co-glycolide) nanospheres to glioblastoma cells. J Microencapsul 2011; 28: 29-36.
81. Jiang J, Yang S, Wang J, et al. Sequential treatment of drugresistant tumors with RGD-modified liposomes containing siRNA or doxorubicin. Eur J Pharm Biopharm 2010; 76: 170-8.
82. Önyüksel H, Jeon E, Rubinstein I. Nanomicellar paclitaxel increases cytotoxicity of multidrug resistant breast cancer cells. Cancer Lett 2009; 274: 327-30.
83. Wang X, Yang L, Chen ZG, Shin DM. Application of nanotechnology in cancer therapy and imaging. CA Cancer J Clin 2008; 58: 97-110.
84. Sapra P, Tyagi P, Allen TM. Ligand-targeted liposomes for cancer treatment. Current drug delivery 2005; 2: 369-81.
85. Sapra P, Moase EH, Ma J, Allen TM. Improved therapeutic responses in a xenograft model of human B lymphoma (Namalwa) for liposomal vincristine versus liposomal doxorubicin targeted via anti-CD19 IgG2a or Fab-fragments. Clin Cancer Res 2004; 10: 1100-11.
86. Xiong XB, 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: 757-68.
87. Delbaldo C, Michiels S, Syz N, Soria JC, Le Chevalier T, Pignon JP. Benefits of Adding a Drug to a Single-Agent or a 2-Agent Chemotherapy Regimen in Advanced Non-Small-Cell Lung Cancer: a meta-analysis. JAMA 2004; 292: 470-84.
88. Di Maio M, Chiodini P, Georgoulias V, et al. Meta-Analysis of Single-Agent Chemotherapy Compared With Combination Chemotherapy As Second-Line Treatment of Advanced Non-Small-Cell Lung Cancer. J Clin Oncol 2009; 27: 1836-43.
89. Klopman G, Shi LM, Ramu A. Quantitative structure-activity relationship of multidrug resistance reversal agents. Mol Pharmacol 1997; 52: 323-34.
90. Sikic BI, Fisher GA, Lum BL, Halsey J, Beketic-Oreskovic L, Chen G. Modulation and prevention of multidrug resistance by inhibitors of P-glycoprotein. Cancer Chemother Pharmacol 1997; 40: 13-9.
91. Kolitz JE, George SL, Marcucci G, et al. P-glycoprotein inhibition using valspodar (PSC-833) does not improve outcomes for patients younger than age 60 years with newly diagnosed acute myeloid leukemia: Cancer and Leukemia Group B study 19808. Blood 2010; 116: 1413-21.
92. Abraham J, Edgerly M, Wilson R, et al. A phase I study of the Pglycoprotein antagonist tariquidar in combination with vinorelbine. Clin Cancer Res 2009; 15: 3574-82.
93. Ruff P, Vorobiof D, Jordaan J, et al. A randomized, placebocontrolled, double-blind phase 2 study of docetaxel compared to docetaxel plus zosuquidar (LY335979) in women with metastatic or locally recurrent breast cancer who have received one prior chemotherapy regimen. Cancer Chemother Pharmacol 2009; 64: 763-8.
94. Kerr D, Graham J, Cummings J, et al. The effect of verapamil on the pharmacokinetics of adriamycin. Cancer Chemother Pharmacol 1986; 18: 239-42.
95. Advani R, Fisher GA, Lum BL, et al. A phase I trial of doxorubicin, paclitaxel, and valspodar (PSC 833), a modulator of multidrug resistance. Clin Cancer Res 2001; 7: 1221-9.
96. Fracasso PM, Brady MF, Moore DH, et al. Phase II Study of Paclitaxel and Valspodar (PSC 833) in Refractory Ovarian Carcinoma: A Gynecologic Oncology Group Study. J Clin Oncol 2001; 19: 2975-82.
97. Emilienne Soma C, Dubernet C, Bentolila D, Benita S, Couvreur P. Reversion of multidrug resistance by co-encapsulation of doxorubicin and cyclosporin A in polyalkylcyanoacrylate nanoparticles. Biomaterials 2000; 21: 1-7.
98. Patel NR, Rathi A, Mongayt D, Torchilin VP. Reversal of multidrug resistance by co-delivery of tariquidar (XR9576) and paclitaxel using long-circulating liposomes. Int J Pharm 2011; 416: 296-9.
99. Liang GW, Lu WL, Wu JW, et al. Enhanced therapeutic effects on the multi-drug resistant human leukemia cells in vitro and xenograft in mice using the stealthy liposomal vincristine plus quinacrine. Fundam Clin Pharmacol 2008; 22: 429-37.
100. Li X, Lu W, Liang G, 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 2006; 36: 409-18.
101. Song XR, Cai Z, Zheng Y, et al. Reversion of multidrug resistance by co-encapsulation of vincristine and verapamil in PLGA nanoparticles. Eur J Pharm Sci 2009; 37: 300-5.
102. Ganta S, Amiji M. Coadministration of Paclitaxel and curcumin in nanoemulsion formulations to overcome multidrug resistance in tumor cells. Mol Pharm 2009; 6: 928-39.
103. De Fougerolles A, Vornlocher HP, Maraganore J, Lieberman J. Interfering with disease: a progress report on siRNA-based therapeutics. Nat Rev Drug Discov 2007; 6: 443-53.
104. Bartsch M, Weeke-Klimp AH, Meijer DKF, Scherphof GL, Kamps JAAM. Cell-specific targeting of lipid-based carriers for ODN and DNA. J Liposome Res 2005; 15: 59-92.
105. Gao S, Dagnaes-Hansen F, Nielsen EJB, et al. The effect of chemical modification and nanoparticle formulation on stability and biodistribution of siRNA in mice. Mol Ther 2009; 17: 1225-33.
106. Di Paolo D, Brignole C, Pastorino F, et al. Neuroblastoma-targeted nanoparticles entrapping siRNA specifically knockdown ALK. Mol Ther 2011; 19: 1131-40.
107. Banerjee R, Tyagi P, Li S, Huang L. AnisamideStargeted stealth liposomes: A potent carrier for targeting doxorubicin to human prostate cancer cells. Int J Cancer 2004; 112: 693-700.
108. Yadav S, van Vlerken LE, Little SR, Amiji MM. Evaluations of combination MDR-1 gene silencing and paclitaxel administration in biodegradable polymeric nanoparticle formulations to overcome multidrug resistance in cancer cells. Cancer Chemother Pharmacol 2009; 63: 711-22.
109. Meng H, Liong M, Xia T, et al. Engineered design of mesoporous silica nanoparticles to deliver doxorubicin and P-glycoprotein siRNA to overcome drug resistance in a cancer cell line. Acs Nano 2010; 4: 4539-50.
110. Chen Y, Bathula SR, Li J, Huang L. Multifunctional nanoparticles delivering small interfering RNA and doxorubicin overcome drug resistance in cancer. J Biol Chem 2010; 285: 22639-50.
111. Wong HL, Bendayan R, Rauth AM, Wu XY. Simultaneous delivery of doxorubicin and GG918 (Elacridar) by new polymerlipid hybrid nanoparticles (PLN) for enhanced treatment of multidrug-resistant breast cancer. J Control Release 2006; 116: 275-84.
112. Khdair A, Handa H, Mao G, Panyam J. Nanoparticle-mediated combination chemotherapy and photodynamic therapy overcomes tumor drug resistance in vitro. Eur J Pharm Biopharm 2009; 71: 214-22.
113. Shuhendler AJ, Cheung RY, Manias J, Connor A, Rauth AM, Wu XY. A novel doxorubicin-mitomycin C co-encapsulated nanoparticle formulation exhibits anti-cancer synergy in multidrug resistant human breast cancer cells. Breast Cancer Res Treat 2010; 119: 255-69.
114. Milane L, Ganesh S, Shah S, Duan Z, Amiji M. Multi-modal strategies for overcoming tumor drug resistance: Hypoxia, the Warburg effect, stem cells, and multifunctional nanotechnology. J Control Release 2011; 155: 237-47.
115. Kobayashi T, Ishida T, Okada Y, Ise S, Harashima H, Kiwada H. Effect of transferrin receptor-targeted liposomal doxorubicin in Pglycoprotein-mediated drug resistant tumor cells. Int J Pharm 2007; 329: 94-102.
116. Mohajer G, Lee ES, Bae YH. Enhanced intercellular retention activity of novel pH-sensitive polymeric micelles in wild and multidrug resistant MCF-7 cells. Pharm Res 2007; 24: 1618-27.
117. Kraus M, Wolf B. Implications of acidic tumor microenvironment for neoplastic growth and cancer treatment: a computer analysis. Tumour Biol 1996; 17: 133-54.
118. Modi S, Swetha M, Goswami D, Gupta GD, Mayor S, Krishnan Y. A DNA nanomachine that maps spatial and temporal pH changes inside living cells. Nat Nanotechnol 2009; 4: 325-30.
119. Simon S, Roy D, Schindler M. Intracellular pH and the control of multidrug resistance. Proc Natl Acad Sci USA 1994; 91: 1128-32.
120. Kievit FM, Wang FY, Fang C, et al. Doxorubicin loaded iron oxide nanoparticles overcome multidrug resistance in cancer in vitro. J Control Release 2011; 152 76-83.
121. He Q, Gao Y, Zhang L, et al. A pH-responsive mesoporous silica nanoparticles-based multi-drug delivery system for overcoming multi-drug resistance. Biomaterials 2011; 32: 7711-20.
122. Lee ES, Na K, Bae YH. Doxorubicin loaded pH-sensitive polymeric micelles for reversal of resistant MCF-7 tumor. J Control Release 2005; 103: 405-18.
123. Lee ES, Gao Z, Bae YH. Recent progress in tumor pH targeting nanotechnology. J Control Release 2008; 132: 164-70.
124. Benns JM, Choi JS, Mahato RI, Park JS, Kim SW. pH-sensitive cationic polymer gene delivery vehicle: N-Ac-poly (L-histidine)-graft-poly (L-lysine) comb shaped polymer. Bioconjug Chem 2000; 11: 637-45.
125. Lee ES. A Virus-Mimetic Nanogel Vehicle. Angew Chem Int Ed Engl 2008; 47 2418-21.
126. Gao GH, Li Y, Lee DS. Environmental pH-sensitive polymeric micelles for cancer diagnosis and targeted therapy. J Control Release 2012.
127. Balendiran GK, Dabur R, Fraser D. The role of glutathione in cancer. Cell Biochem Funct 2004; 22: 343-52.
128. Saito G, Swanson JA, Lee KD. Drug delivery strategy utilizing conjugation via reversible disulfide linkages: role and site of cellular reducing activities. Adv Drug Deliv Rev 2003; 55: 199-215.
129. Wang J, Wang YC, Wang F, Sun TM. Redox-Responsive Nanoparticles from the Single Disulfide Bond-Bridged Block Copolymer as Drug Carriers for Overcoming Multi-Drug Resistance in Cancer Cells. Bioconjug Chem 2011; 22: 1939-45.
130. Gao Y, Chen L, Zhang Z, Chen Y, Li Y. Reversal of multidrug resistance by reduction-sensitive linear cationic click polymer/iMDR1-pDNA complex nanoparticles. Biomaterials 2011; 32: 1738-47.
131. Miyajima Y, Nakamura H, Kuwata Y, et al. Transferrin-loaded nido-carborane liposomes: tumor-targeting boron delivery system for neutron capture therapy. Bioconjug Chem 2006; 17: 1314-20.
132. Saito G, Swanson JA, Lee KD. Drug delivery strategy utilizing conjugation via reversible disulfide linkages: role and site of cellular reducing activities. Adv Drug Deliv Rev 2003; 55: 199-215.
133. Rapoport N. Combined cancer therapy by micellar-encapsulated drug and ultrasound. Int J Pharm 2004; 277: 155-62.
134. Marin A, Sun H, Husseini GA, Pitt WG, Christensen DA, Rapoport NY. Drug delivery in pluronic micelles: effect of high-frequency ultrasound on drug release from micelles and intracellular uptake. J Control Release 2002; 84: 39-47.
135. Gaber MH. Modulation of doxorubicin resistance in multidrugresistance cells by targeted liposomes combined with hyperthermia. J Biochem Mol Biol Biophys 2002; 6: 309-14.
136. Shieh MJ, Hsu CY, Huang LY, Chen HY, Huang FH, Lai PS. Reversal of doxorubicin-resistance by multifunctional nanoparticles in MCF-7/ADR cells. J Control Release 2011; 152: 418-25.
137. Khdair A, Di C, Patil Y, et al. Nanoparticle-mediated combination chemotherapy and photodynamic therapy overcomes tumor drug resistance. J Control Release 2010; 141: 137-44.
138. Ng K, Liu Y. Therapeutic ultrasound: its application in drug delivery. Med Res Rev 2002; 22: 204-23.
139. Diederich CJ, Hynynen K. Ultrasound technology for hyperthermia. Ultrasound Med Biol 1999; 25: 871-87.
140. Desmettre T, Devoisselle J, Mordon S. Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography. Surv Ophthalmol 2000; 45: 15-27.
141. Berg K, Dietze A, Kaalhus O, Høgset A. Site-specific drug delivery by photochemical internalization enhances the antitumor effect of bleomycin. Clin Cancer Res 2005; 11: 8476-85.
142. Tacelosky D, Creecy A, Shanmugavelandy S, et al. Calcium phosphosilicate nanoparticles for imaging and photodynamic therapy of cancer. Discov Med 2012; 13: 275.
143. Manchanda R, Lei T, Tang Y, Fernandez-Fernandez A, McGoron AJ. Cellular Uptake and Cytotoxicity of a Novel ICG-DOX-PLGA Dual Agent Polymer Nanoparticle Delivery System. 26th Southern Biomedical Engineering Conference SBEC, Maryland, USA, Apr. 30-May 2, 2010; pp. 228-31.