Nanoparticle-mediated delivery of siRNA for effective lung cancer therapy

Nanomedicine

Volumn 10, Issue 7, 2015, Pages 1165-1188

  Kim, Young Dong ^a   Park, Tae Eun ^a   Singh, Bijay ^a   Maharjan, Sushila ^a   Choi, Yun Jaie ^a   Choung, Pill Hoon ^a   Arote, Rohidas B ^a   Cho, Chong Su ^a  

^a Seoul National University   (South Korea)

Author keywords

codelivery system; lung cancer; nanoparticle; RNA interference; siRNA delivery system

Indexed keywords

ANTIBODY; ANTINEOPLASTIC AGENT; ARGINYLGLYCYLASPARTIC ACID; BIOLOGICAL FACTOR; CARBON NANOTUBE; DRUG CARRIER; FOLIC ACID; GOLD NANOPARTICLE; HYALURONIC ACID; LIPID; NANOPARTICLE; POLYMER; SMALL INTERFERING RNA; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ARTICLE; CANCER GENE THERAPY; CANCER RESISTANCE; CLINICAL TRIAL (TOPIC); HETEROZYGOTE; HUMAN; LUNG CANCER; MULTIDRUG RESISTANCE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); POLYMERIZATION; PRIORITY JOURNAL; ANIMAL; CHEMISTRY; GENETICS; LUNG; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; PROCEDURES; RNA INTERFERENCE; RNAI THERAPEUTICS;

ANIMALS; HUMANS; LIPIDS; LUNG; LUNG NEOPLASMS; NANOPARTICLES; POLYMERS; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNAI THERAPEUTICS;

EID: 84929091507     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.14.214     Document Type: Article

References (143)

1. Ferlay J, Soerjomataram I, Ervik M et al. GLOBOCAN 2012: estimated cancer incidence, mortality and prevalence worldwide in 2012. http://globocan.iarc.fr/Default.aspx
2. Ramalingam SS, Owonikoko TK, Khuri FR. Lung cancer: new biological insights and recent therapeutic advances. CA Cancer J. Clin. 61(2), 91-112 (2011).
3. Ferlay J, Autier P, Boniol M, Heanue M, Colombet M, Boyle P. Estimates of the cancer incidence and mortality in Europe in 2006. Ann. Oncol. 18(3), 581-592 (2007).
4. Oh YK, Park TG. siRNA delivery systems for cancer treatment. Adv. Drug Deliv. Rev. 61(10), 850-862 (2009).
5. Bareschino MA, Schettino C, Rossi A et al. Treatment of advanced non small cell lung cancer. J. Thorac. Dis. 3(2), 122-133 (2011).
6. Klasa RJ, Murray N, Coldman AJ. Dose-intensity meta-analysis of chemotherapy regimens in small-cell carcinoma of the lung. J. Clin. Oncol. 9(3), 499-508 (1991).
7. Yu J, Li WD, Zhang Z, Yu TL, Li D. Prediction of early response to chemotherapy in lung cancer by using diffusion-weighted MR imaging. Sci. World J. 2014, 7 (2014).
8. Diaz MR, Vivas-Mejia PE. Nanoparticles as drug delivery systems in cancer medicine: emphasis on RNAi-containing nanoliposomes. Pharmaceuticals (Basel) 6(11), 1361-1380 (2013).
9. Matsumura Y, Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 46(12 Pt 1), 6387-6392 (1986).
10. Wang AZ, Langer R, Farokhzad OC. Nanoparticle delivery of cancer drugs. Annu. Rev. Med. 63, 185-198 (2012).
11. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411(6836), 494-498 (2001).
12. Zamore PD, Tuschl T, Sharp PA, Bartel DP. RNAi: doublestranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101(1), 25-33 (2000).
13. Elbashir SM, Lendeckel W, Tuschl T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 15(2), 188-200 (2001).
14. Hutvagner G, Zamore PD. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297(5589), 2056-2060 (2002).
15. Salem AK, Patil SD, Burgess DJ. Recent progress in non-viral nucleic acids delivery. Int. J. Pharm. 427(1), 1-2 (2012).
16. Nie S. Understanding and overcoming major barriers in cancer nanomedicine. Nanomedicine 5(4), 523-528 (2010).
17. Kirtane AR, Panyam J. Polymer nanoparticles: weighing up gene delivery. Nat. Nanotechnol. 8(11), 805-806 (2013).
18. Yu MK, Park J, Jon S. Targeting strategies for multifunctional nanoparticles in cancer imaging and therapy. Theranostics 2(1), 3-44 (2012).
19. Khalil IA, Kogure K, Akita H, Harashima H. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol. Rev. 58(1), 32-45 (2006).
20. Ziello JE, Huang Y, Jovin IS. Cellular endocytosis and gene delivery. Mol. Med. 16(5-6), 222-229 (2010).
21. Hillaireau H, Couvreur P. Nanocarriers' entry into the cell: relevance to drug delivery. Cell. Mol. Life Sci. 66(17), 2873-2896 (2009).
22. Goncalves C, Mennesson E, Fuchs R, Gorvel JP, Midoux P, Pichon C. Macropinocytosis of polyplexes and recycling of plasmid via the clathrin-dependent pathway impair the transfection efficiency of human hepatocarcinoma cells. Mol. Ther. 10(2), 373-385 (2004).
23. Kiss AL, Botos E. Endocytosis via caveolae: alternative pathway with distinct cellular compartments to avoid lysosomal degradation? J. Cell. Mol. Med. 13(7), 1228-1237 (2009).
24. Felgner PL, Gadek TR, Holm M et al. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl Acad. Sci. USA 84(21), 7413-7417 (1987).
25. Zhi D, Zhang S, Wang B, Zhao Y, Yang B, Yu S. Transfection efficiency of cationic lipids with different hydrophobic domains in gene delivery. Bioconjug. Chem. 21(4), 563-577 (2010).
26. Kanasty R, Dorkin JR, Vegas A, Anderson D. Delivery materials for siRNA therapeutics. Nat. Mater. 12(11), 967-977 (2013).
27. Amarzguioui M, Peng Q, Wiiger MT et al. Ex vivo and in vivo delivery of anti-tissue factor short interfering RNA inhibits mouse pulmonary metastasis of B16 melanoma cells. Clin. Cancer Res. 12(13), 4055-4061 (2006).
28. Amirkhosravi A, Meyer T, Chang JY et al. Tissue factor pathway inhibitor reduces experimental lung metastasis of B16 melanoma. Thromb. Haemost. 87(6), 930-936 (2002).
29. Zhang CL, Tang N, Liu XJ, Liang W, Xu W, Torchilin VP. siRNA-containing liposomes modified with polyarginine effectively silence the targeted gene. J. Control. Release 112(2), 229-239 (2006).
30. Unnamalai N, Kang BG, Lee WS. Cationic oligopeptide-mediated delivery of dsRNA for post-transcriptional gene silencing in plant cells. FEBS Lett. 566(1-3), 307-310 (2004).
31. Niculescu-Duvaz D, Heyes J, Springer CJ. Structure-activity relationship in cationic lipid mediated gene transfection. Curr. Med. Chem. 10(14), 1233-1261 (2003).
32. Ewert K, Slack NL, Ahmad A et al. Cationic lipid-DNA complexes for gene therapy: understanding the relationship between complex structure and gene delivery pathways at the molecular level. Curr. Med. Chem. 11(2), 133-149 (2004).
33. Fraix A, Montier T, Carmoy N et al. Cationic lipothiophosphoramidates for gene delivery: synthesis, physicochemical characterization and gene transfection activity - comparison with lipo-phosphoramidates. Org. Biomol. Chem. 9(7), 2422-2432 (2011).
34. Biswas S, Knipp RJ, Gordon LE et al. Hydrophobic oxime ethers: a versatile class of pDNA and siRNA transfection lipids. Chem. Med. Chem. 6(11), 2063-2069 (2011).
35. Cun D, Jensen DK, Maltesen MJ et al. High loading efficiency and sustained release of siRNA encapsulated in PLGA nanoparticles: quality by design optimization and characterization. Eur. J. Pharm. Biopharm. 77(1), 26-35 (2011).
36. Jensen DK, Jensen LB, Koocheki S et al. Design of an inhalable dry powder formulation of DOTAP-modified PLGA nanoparticles loaded with siRNA. J. Control. Release 157(1), 141-148 (2012).
37. Shim G, Choi HW, Lee S et al. Enhanced intrapulmonary delivery of anticancer siRNA for lung cancer therapy using cationic ethylphosphocholine-based nanolipoplexes. Mol. Ther. 21(4), 816-824 (2013).
38. Garbuzenko OB, Saad M, Betigeri S et al. Intratracheal versus intravenous liposomal delivery of siRNA, antisense oligonucleotides and anticancer drug. Pharm. Res. 26(2), 382-394 (2009).
39. Shen S, Mao CQ, Yang XZ et al. Cationic lipid-assisted polymeric nanoparticle mediated GATA2 siRNA delivery for synthetic lethal therapy of KRAS mutant non-small-cell lung carcinoma. Mol. Pharm. 1111(8), 2612-2622 (2014).
40. Fehring V, Schaeper U, Ahrens K et al. Delivery of therapeutic siRNA to the lung endothelium via novel lipoplex formulation DACC. Mol. Ther. 22(4), 811-820 (2014).
41. Demeneix B, Behr JP. Polyethylenimine (PEI). In: Non-Viral Vectors for Gene Therapy (53) (2nd Edition; Part 1) . Huang L, Hung MC, Wagner E (Eds). Elsevier Academic Press Inc., CA, USA, 217-230 (2005).
42. Zamora-Avila DE, Zapata-Benavides P, Franco-Molina MA et al. WT1 gene silencing by aerosol delivery of PEI-RNAi complexes inhibits B16-F10 lung metastases growth. Cancer Gene Ther. 16(12), 892-899 (2009).
43. Kamlah F, Eul BG, Li S et al. Intravenous injection of siRNA directed against hypoxia-inducible factors prolongs survival in a Lewis lung carcinoma cancer model. Cancer Gene Ther. 16(3), 195-205 (2009).
44. Bonnet ME, Gossart JB, Benoit E et al. Systemic delivery of sticky siRNAs targeting the cell cycle for lung tumor metastasis inhibition. J. Control. Release 170(2), 183-190 (2013).
45. Thomas M, Lu JJ, Ge Q, Zhang CC, Chen JZ, Klibanov AM. Full deacylation of polyethylenimine dramatically boosts its gene delivery efficiency and specificity to mouse lung. Proc. Natl Acad. Sci. USA 102(16), 5679-5684 (2005).
46. Jere D, Xu CX, Arote R, Yun CH, Cho MH, Cho CS. Poly(beta-amino ester) as a carrier for si/shRNA delivery in lung cancer cells. Biomaterials 29(16), 2535-2547 (2008).
47. Park MR, Han KO, Han IK et al. Degradable polyethylenimine-alt-poly(ethylene glycol) copolymers as novel gene carriers. J. Control. Release 105(3), 367-380 (2005).
48. Testa JR, Bellacosa A. AKT plays a central role in tumorigenesis. Proc. Natl Acad. Sci. USA 98(20), 10983-10985 (2001).
49. Xu CX, Jere D, Jin H et al. Poly(ester amine)-mediated, aerosol-delivered Akt1 small interfering RNA suppresses lung tumorigenesis. Am. J. Respir. Crit. Care Med. 178(1), 60-73 (2008).
50. Jere D, Kim JE, Arote R et al. Akt1 silencing efficiencies in lung cancer cells by sh/si/ssiRNA transfection using a reductable polyspermine carrier. Biomaterials 30(8), 1635-1647 (2009).
51. Hong SH, Kim JE, Kim YK et al. Suppression of lung cancer progression by biocompatible glycerol triacrylate-sperminemediated delivery of shAkt1. Int. J. Nanomedicine 7, 2293-2306 (2012).
52. Jiang HL, Hong SH, Kim YK et al. Aerosol delivery of spermine-based poly(amino ester)/Akt1 shRNA complexes for lung cancer gene therapy. Int. J. Pharm. 420(2), 256-265 (2011).
53. Kawata E, Ashihara E, Kimura S et al. Administration of PLK-1 small interfering RNA with atelocollagen prevents the growth of liver metastases of lung cancer. Mol. Cancer Ther. 7(9), 2904-2912 (2008).
54. Weichert W, Denkert C, Schmidt M et al. Polo-like kinase isoform expression is a prognostic factor in ovarian carcinoma. Br. J. Cancer 90(4), 815-821 (2004).
55. Jere D, Jiang HL, Kim YK et al. Chitosan-graft-polyethylenimine for Akt1 siRNA delivery to lung cancer cells. Int. J. Pharm. 378(1-2), 194-200 (2009).
56. Varkouhi AK, Verheul RJ, Schiffelers RM, Lammers T, Storm G, Hennink WE. Gene silencing activity of siRNA polyplexes based on thiolated N,N,N-trimethylated chitosan. Bioconjug. Chem. 21(12), 2339-2346 (2010).
57. Okuda T, Kito D, Oiwa A, Fukushima M, Hira D, Okamoto H. Gene silencing in a mouse lung metastasis model by an inhalable dry small interfering RNA powder prepared using the supercritical carbon dioxide technique. Biol. Pharm. Bull. 36(7), 1183-1191 (2013).
58. Han J, Wang Q, Zhang Z, Gong T, Sun X. Cationic bovine serum albumin based self-assembled nanoparticles as siRNA delivery vector for treating lung metastatic cancer. Small 10(3), 524-535 (2014).
59. Nguyen J, Steele TW, Merkel O, Reul R, Kissel T. Fast degrading polyesters as siRNA nano-carriers for pulmonary gene therapy. J. Control. Release 132(3), 243-251 (2008).
60. Itaka K, Kataoka K. Progress and prospects of polyplex nanomicelles for plasmid DNA delivery. Curr. Gene Ther. 11(6), 457-465 (2011).
61. Du J, Sun Y, Shi QS et al. Biodegradable nanoparticles of mPEG-PLGA-PLL triblock copolymers as novel non-viral vectors for improving siRNA delivery and gene silencing. Int. J. Mol. Sci. 13(1), 516-533 (2012).
62. Yu H, Zou Y, Jiang L et al. Induction of apoptosis in non-small cell lung cancer by downregulation of MDM2 using pH-responsive PMPC-b-PDPA/siRNA complex nanoparticles. Biomaterials 34(11), 2738-2747 (2013).
63. Mao CQ, Xiong MH, Liu Y et al. Synthetic lethal therapy for KRAS mutant non-small-cell lung carcinoma with nanoparticle-mediated CDK4 siRNA delivery. Mol. Ther. 22(5), 964-973 (2014).
64. Boyer C, Teo J, Phillips P et al. Effective delivery of siRNA into cancer cells and tumors using well-defined biodegradable cationic star polymers. Mol. Pharm. 10(6), 2435-2444 (2013).
65. Conti DS, Brewer D, Grashik J, Avasarala S, Da Rocha SR. Poly(amidoamine) dendrimer nanocarriers and their aerosol formulations for siRNA delivery to the lung epithelium. Mol. Pharm. 11(6), 1808-1822 (2014).
66. Durcan N, Murphy C, Cryan SA. Inhalable siRNA: potential as a therapeutic agent in the lungs. Mol. Pharm. 5(4), 559-566 (2008).
67. Wang Z, Liu G, Zheng H, Chen X. Rigid nanoparticle-based delivery of anti-cancer siRNA: challenges and opportunities. Biotechnol. Adv. 32(4), 831-843 (2013).
68. Wang C, Ding C, Kong M et al. Tumor-targeting magnetic lipoplex delivery of short hairpin RNA suppresses IGF-1R overexpression of lung adenocarcinoma A549 cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 410(3), 537-542 (2011).
69. Podesta JE, Al-Jamal KT, Herrero MA et al. Antitumor activity and prolonged survival by carbon-nanotubemediated therapeutic siRNA silencing in a human lung xenograft model. Small 5(10), 1176-1185 (2009).
70. Al-Jamal KT, Toma FM, Yilmazer A et al. Enhanced cellular internalization and gene silencing with a series of cationic dendron-multiwalled carbon nanotube: siRNA complexes. FASEB J. 24(11), 4354-4365 (2010).
71. Zhang Z, Yang X, Zhang Y et al. Delivery of telomerase reverse transcriptase small interfering RNA in complex with positively charged single-walled carbon nanotubes suppresses tumor growth. Clin. Cancer Res. 12(16), 4933-4939 (2006).
72. Huschka R, Barhoumi A, Liu Q, Roth JA, Ji L, Halas NJ. Gene silencing by gold nanoshell-mediated delivery and lasertriggered release of antisense oligonucleotide and siRNA. ACS Nano 6(9), 7681-7691 (2012).
73. Vilner BJ, John CS, Bowen WD. Sigma-1 and sigma-2 receptors are expressed in a wide variety of human and rodent tumor cell lines. Cancer Res. 55(2), 408-413 (1995).
74. Li SD, Huang L. Targeted delivery of antisense oligodeoxynucleotide and small interference RNA into lung cancer cells. Mol. Pharm. 3(5), 579-588 (2006).
75. Chono S, Li SD, Conwell CC, Huang L. An efficient and low immunostimulatory nanoparticle formulation for systemic siRNA delivery to the tumor. J. Control. Release 131(1), 64-69 (2008).
76. Li SD, Chono S, Huang L. Efficient oncogene silencing and metastasis inhibition via systemic delivery of siRNA. Mol. Ther. 16(5), 942-946 (2008).
77. Li J, Yang Y, Huang L. Calcium phosphate nanoparticles with an asymmetric lipid bilayer coating for siRNA delivery to the tumor. J. Control. Release 158(1), 108-114 (2012).
78. Yang Y, Li J, Liu F, Huang L. Systemic delivery of siRNA via LCP nanoparticle efficiently inhibits lung metastasis. Mol. Ther. 20(3), 609-615 (2012).
79. Yang Y, Hu Y, Wang Y, Li J, Liu F, Huang L. Nanoparticle delivery of pooled siRNA for effective treatment of non-small cell lung cancer. Mol. Pharm. 9(8), 2280-2289 (2012).
80. Platt VM, Szoka FC Jr. Anticancer therapeutics: targeting macromolecules and nanocarriers to hyaluronan or CD44, a hyaluronan receptor. Mol. Pharm. 5(4), 474-486 (2008).
81. Coradini D, Pellizzaro C, Abolafio G et al. Hyaluronic-acid butyric esters as promising antineoplastic agents in human lung carcinoma: a preclinical study. Invest. New Drugs 22(3), 207-217 (2004).
82. Ganesh S, Iyer AK, Morrissey DV, Amiji MM. Hyaluronic acid based self-assembling nanosystems for CD44 target mediated siRNA delivery to solid tumors. Biomaterials 34(13), 3489-3502 (2013).
83. Taetz S, Bochot A, Surace C et al. Hyaluronic acid-modified DOTAP/DOPE liposomes for the targeted delivery of anti-telomerase siRNA to CD44-expressing lung cancer cells. Oligonucleotides 19(2), 103-116 (2009).
84. Wang Y, Xu Z, Guo S et al. Intravenous delivery of siRNA targeting CD47 effectively inhibits melanoma tumor growth and lung metastasis. Mol. Ther. 21(10), 1919-1929 (2013).
85. Chen G, Chen W, Wu Z et al. MRI-visible polymeric vector bearing CD3 single chain antibody for gene delivery to T cells for immunosuppression. Biomaterials 30(10), 1962-1970 (2009).
86. Chen Y, Zhu X, Zhang X, Liu B, Huang L. Nanoparticles modified with tumor-targeting scFv deliver siRNA and miRNA for cancer therapy. Mol. Ther. 18(9), 1650-1656 (2010).
87. Mokhtarieh AA, Cheong S, Kim S, Chung BH, Lee MK. Asymmetric liposome particles with highly efficient encapsulation of siRNA and without nonspecific cell penetration suitable for target-specific delivery. Biochim. Biophys. Acta 1818(7), 1633-1641 (2012).
88. Nascimento AV, Singh A, Bousbaa H, Ferreira D, Sarmento B, Amiji MM. Mad2 checkpoint gene silencing using epidermal growth factor receptor-targeted chitosan nanoparticles in non-small cell lung cancer model. Mol. Pharm. 11(10), 3515-3527 (2014).
89. Barbosa J, Nascimento AV, Faria J, Silva P, Bousbaa H. The spindle assembly checkpoint: perspectives in tumorigenesis and cancer therapy. Front. Biol. 6(2), 147-155 (2011).
90. Antony AC. Folate receptors. Annu. Rev. Nutr. 16, 501-521 (1996).
91. Jiang HL, Xu CX, Kim YK et al. The suppression of lung tumorigenesis by aerosol-delivered folate-chitosan-graft-polyethylenimine/Akt1 shRNA complexes through the Akt signaling pathway. Biomaterials 30(29), 5844-5852 (2009).
92. Kim J, Nam HY, Kim TI et al. Active targeting of RGDconjugated bioreducible polymer for delivery of oncolytic adenovirus expressing shRNA against IL-8 mRNA. Biomaterials 32(22), 5158-5166 (2011).
93. Yonenaga N, Kenjo E, Asai T et al. RGD-based active targeting of novel polycation liposomes bearing siRNA for cancer treatment. J. Control. Release 160(2), 177-181 (2012).
94. Conde J, Tian F, Hernandez Y et al. In vivo tumor targeting via nanoparticle-mediated therapeutic siRNA coupled to inflammatory response in lung cancer mouse models. Biomaterials 34(31), 7744-7753 (2013).
95. Pauwels EK, Erba P, Mariani G, Gomes CM. Multidrug resistance in cancer: its mechanism and its modulation. Drug News Perspect. 20(6), 371-377 (2007).
96. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2(1), 48-58 (2002).
97. Triller N, Korosec P, Kern I, Kosnik M, Debeljak A. Multidrug resistance in small cell lung cancer: expression of P-glycoprotein, multidrug resistance protein 1 and lung resistance protein in chemo-naive patients and in relapsed disease. Lung Cancer 54(2), 235-240 (2006).
98. Loo TW, Clarke DM. The transmembrane domains of the human multidrug resistance P-glycoprotein are sufficient to mediate drug binding and trafficking to the cell surface. J. Biol. Chem. 274(35), 24759-24765 (1999).
99. Chen ZS, Tiwari AK. Multidrug resistance proteins (MRPs/ ABCCs) in cancer chemotherapy and genetic diseases. FEBS J. 278(18), 3226-3245 (2011).
100. Scagliotti GV, Novello S, Selvaggi G. Multidrug resistance in non-small-cell lung cancer. Ann. Oncol. 10(Suppl. 5), S83-S86 (1999).
101. Lagas JS, Sparidans RW, Van Waterschoot RA, Wagenaar E, Beijnen JH, Schinkel AH. P-glycoprotein limits oral availability, brain penetration, and toxicity of an anionic drug, the antibiotic salinomycin. Antimicrob. Agents Chemother. 52(3), 1034-1039 (2008).
102. Jaeger W. Classical resistance mechanisms. Int. J. Clin. Pharmacol. Ther. 47(1), 46-48 (2009).
103. 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).
104. Borst P, Evers R, Kool M, Wijnholds J. A family of drug transporters: the multidrug resistance-associated proteins. J. Natl Cancer Inst. 92(16), 1295-1302 (2000).
105. Zou S, Cao N, Cheng D et al. Enhanced apoptosis of ovarian cancer cells via nanocarrier-mediated codelivery of siRNA and doxorubicin. Int. J. Nanomedicine 7, 3823-3835 (2012).
106. Kim HO, Kim E, An Y et al. A biodegradable polymersome containing Bcl-xL siRNA and doxorubicin as a dual delivery vehicle for a synergistic anticancer effect. Macromol. Biosci. 13(6), 745-754 (2013).
107. Cao N, Cheng D, Zou SY, Ai H, Gao JM, Shuai XT. The synergistic effect of hierarchical assemblies of siRNA and chemotherapeutic drugs co-delivered into hepatic cancer cells. Biomaterials 32(8), 2222-2232 (2011).
108. Shim G, Han SE, Yu YH et al. Trilysinoyl oleylamide-based cationic liposomes for systemic co-delivery of siRNA and an anticancer drug. J. Control. Release 155(1), 60-66 (2011).
109. Adams JM, Cory S. Bcl-2-regulated apoptosis: mechanism and therapeutic potential. Curr. Opin. Immunol. 19(5), 488-496 (2007).
110. Shen J, Yin Q, Chen L, Zhang Z, Li Y. Co-delivery of paclitaxel and survivin shRNA by pluronic P85-PEI/TPGS complex nanoparticles to overcome drug resistance in lung cancer. Biomaterials 33(33), 8613-8624 (2012).
111. Shen J, Meng Q, Sui H et al. iRGD conjugated TPGS mediates codelivery of Paclitaxel and survivin shRNA for the reversal of lung cancer resistance. Mol. Pharm. 11(8), 2579-2591 (2013).
112. Zhu L, Perche F, Wang T, Torchilin VP. Matrix metalloproteinase 2-sensitive multifunctional polymeric micelles for tumor-specific co-delivery of siRNA and hydrophobic drugs. Biomaterials 35(13), 4213-4222 (2014).
113. Ma YP, Yang Y, Zhang S et al. Efficient inhibition of lung cancer in murine model by plasmid-encoding VEGF short hairpin RNA in combination with low-dose DDP. J. Exp. Clin. Cancer. Res. 29, 56 (2010).
114. Zhang Y, Schwerbrock NM, Rogers AB, Kim WY, Huang L. Codelivery of VEGF siRNA and gemcitabine monophosphate in a single nanoparticle formulation for effective treatment of NSCLC. Mol. Ther. 21(8), 1559-1569 (2013).
115. Garbuzenko OB, Saad M, Pozharov VP, Reuhl KR, Mainelis G, Minko T. Inhibition of lung tumor growth by complex pulmonary delivery of drugs with oligonucleotides as suppressors of cellular resistance. Proc. Natl Acad. Sci. USA 107(23), 10737-10742 (2010).
116. Taratula O, Garbuzenko OB, Chen AM, Minko T. Innovative strategy for treatment of lung cancer: targeted nanotechnology-based inhalation co-delivery of anticancer drugs and siRNA. J. Drug Target. 19(10), 900-914 (2011).
117. Taratula O, Kuzmov A, Shah M, Garbuzenko OB, Minko T. Nanostructured lipid carriers as multifunctional nanomedicine platform for pulmonary co-delivery of anticancer drugs and siRNA. J. Control. Release 171(3), 349-357 (2013).
118. Ganesh S, Iyer AK, Weiler J, Morrissey DV, Amiji MM. Combination of siRNA-directed gene silencing with cisplatin reverses drug resistance in human non-small cell lung cancer. Mol. Ther. Nucl. Acids 2, e110 (2013).
119. Altieri DC. Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 22(53), 8581-8589 (2003).
120. Salvesen GS, Duckett CS. IAP proteins: blocking the road to death's door. Nat. Rev. Mol. Cell. Biol. 3(6), 401-410 (2002).
121. Lu J, Tan M, Huang WC et al. Mitotic deregulation by survivin in ErbB2-overexpressing breast cancer cells contributes to Taxol resistance. Clin. Cancer Res. 15(4), 1326-1334 (2009).
122. Zaffaroni N, Pennati M, Daidone MG. Survivin as a target for new anticancer interventions. J. Cell. Mol. Med. 9(2), 360-372 (2005).
123. Tew KD, Manevich Y, Grek C, Xiong Y, Uys J, Townsend DM. The role of glutathione S-transferase P in signaling pathways and S-glutathionylation in cancer. Free Radic. Biol. Med. 51(2), 299-313 (2011).
124. Shuai X, Merdan T, Unger F, Kissel T. Supramolecular gene delivery vectors showing enhanced transgene expression and good biocompatibility. Bioconjug. Chem. 16(2), 322-329 (2005).
125. Bolcato-Bellemin AL, Bonnet ME, Creusat G, Erbacher P, Behr JP. Sticky overhangs enhance siRNA-mediated gene silencing. Proc. Natl Acad. Sci. USA 104(41), 16050-16055 (2007).
126. Yuan J, Yan R, Kramer A et al. Cyclin B1 depletion inhibits proliferation and induces apoptosis in human tumor cells. Oncogene 23(34), 5843-5852 (2004).
127. Rosen LS. VEGF-targeted therapy: therapeutic potential and recent advances. Oncologist 10(6), 382-391 (2005).
128. Tran J, Rak J, Sheehan C et al. Marked induction of the IAP family antiapoptotic proteins survivin and XIAP by VEGF in vascular endothelial cells. Biochem. Biophys. Res. Commun. 264(3), 781-788 (1999).
129. Lee JK, Hong YJ, Han CJ, Hwang DY, Hong SI. Clinical usefulness of serum and plasma vascular endothelial growth factor in cancer patients: which is the optimal specimen? Int. J. Oncol. 17(1), 149-152 (2000).
130. Xiong XB, Lavasanifar A. Traceable multifunctional micellar nanocarriers for cancer-targeted co-delivery of MDR-1 siRNA and doxorubicin. ACS Nano 5(6), 5202-5213 (2011).
131. Patil YB, Swaminathan SK, Sadhukha T, Ma LA, Panyam J. The use of nanoparticle-mediated targeted gene silencing and drug delivery to overcome tumor drug resistance. Biomaterials 31(2), 358-365 (2010).
132. Yu YH, Kim E, Park DE et al. Cationic solid lipid nanoparticles for co-delivery of paclitaxel and siRNA. Eur. J. Pharm. Biopharm. 80(2), 268-273 (2012).
133. Meng H, Mai WX, Zhang H et al. 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 7(2), 994-1005 (2013).
134. Hong H, Zhang Y, Cai W. In vivo imaging of RNA interference. J. Nucl. Med. 51(2), 169-172 (2010).
135. Kami D, Takeda S, Itakura Y, Gojo S, Watanabe M, Toyoda M. Application of magnetic nanoparticles to gene delivery. Int. J. Mol. Sci. 12(6), 3705-3722 (2011).
136. Issa B, Obaidat IM, Albiss BA, Haik Y. Magnetic nanoparticles: surface effects and properties related to biomedicine applications. Int. J. Mol. Sci. 14(11), 21266-21305 (2013).
137. Taratula O, Garbuzenko O, Savla R, Wang YA, He HX, Minko T. Multifunctional nanomedicine platform for cancer specific delivery of siRNA by superparamagnetic iron oxide nanoparticles-dendrimer complexes. Curr. Drug Deliv. 8(1), 59-69 (2011).
138. Chen Y, Gu H, Zhang DS, Li F, Liu T, Xia W. Highly effective inhibition of lung cancer growth and metastasis by systemic delivery of siRNA via multimodal mesoporous silica-based nanocarrier. Biomaterials 35(38), 10058-10069 (2014).
139. Liu G, Swierczewska M, Lee S, Chen X. Functional nanoparticles for molecular imaging guided gene delivery. Nano Today 5(6), 524-539 (2010).
140. Thakor AS, Gambhir SS. Nanooncology: the future of cancer diagnosis and therapy. Ca-Cancer J. Clin. 63(6), 395-418 (2013).
141. Biffi S, Garrovo C, Macor P et al. In vivo Biodistribution and lifetime analysis of Cy5.5-conjugated rituximab in mice bearing lymphoid tumor xenograft using time-domain near-infrared optical imaging. Mol. Imaging 7(6), 272-282 (2008).
142. Wei W, Lv PP, Chen XM et al. Codelivery of mTERT siRNA and paclitaxel by chitosan-based nanoparticles promoted synergistic tumor suppression. Biomaterials 34(15), 3912-3923 (2013).
143. Liu L, Liu X, Xu Q et al. Self-assembled nanoparticles based on the c(RGDfk) peptide for the delivery of siRNA targeting the VEGFR2 gene for tumor therapy. Int. J. Nanomed. 9, 3509-3526 (2014).