Recent progress in microRNA delivery for cancer therapy by non-viral synthetic vectors

Advanced Drug Delivery Reviews

Volumn 81, Issue , 2015, Pages 142-160

  Wang, Huiyuan ^a   Jiang, Yifan ^a   Peng, Huige ^a   Chen, Yingzhi ^a   Zhu, Peizhi ^b   Huang, Yongzhuo ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^b YANGZHOU UNIVERSITY   (China)

Author keywords

Cancer therapy; Drug delivery; MicroRNA; Non viral vector; Synthetic vector

Indexed keywords

DESIGN; DISEASES; DRUG DELIVERY; DRUG INTERACTIONS; DRUG THERAPY; GENE EXPRESSION; ONCOLOGY; VECTORS;

ANTI-CANCER THERAPIES; CANCER THERAPY; DESIGN AND APPLICATION; MICRORNAS; NON-VIRAL DELIVERY SYSTEMS; NONVIRAL VECTORS; SYNTHETIC VECTOR; THERAPEUTIC APPLICATION;

RNA;

ANTIBODY; ANTINEOPLASTIC AGENT; APTAMER; ATELOCOLLAGEN; COPOLYMER; DENDRIMER; LIGAND; LIPID NANOPARTICLE; MAGNETIC NANOPARTICLE; MICRORNA; MRX 34; NANOPARTICLE; POLYAMIDOAMINE; POLYETHYLENEIMINE; POLYGLACTIN; UNCLASSIFIED DRUG;

CANCER THERAPY; CLINICAL EFFECTIVENESS; DRUG CYTOTOXICITY; DRUG DESIGN; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; GENE FUNCTION; GENE IDENTIFICATION; GENE SILENCING; GENE VECTOR; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR DYNAMICS; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL SYNTHETIC VECTOR; REVIEW; ADMINISTRATION AND DOSAGE; ANIMAL; GENE EXPRESSION REGULATION; GENE TRANSFER; GENETICS; NEOPLASMS;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; MICRORNAS; NEOPLASMS;

EID: 84922181105     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.10.031     Document Type: Review

References (150)

1. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
2. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
3. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
4. Kozomara A., Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011, 39:152-157.
5. Friedman R.C., Farh K.K.H., Burge C.B., Bartel D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19:92-105.
6. Berezikov E., Guryev V., van de Belt J., Wienholds E., Plasterk R.H., Cuppen E. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 2005, 120:21-24.
7. Jakob P., Landmesser U. Role of microRNAs in stem/progenitor cells and cardiovascular repair. Cardiovasc. Res. 2012, 93:614-622.
8. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
9. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Radmark O., Kim S., Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
10. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
11. Esau C.C., Monia B.P. Therapeutic potential for microRNAs. Adv. Drug Deliv. Rev. 2007, 59:101-114.
12. Singh R.P., Massachi I., Manickavel S., Singh S., Rao N.P., Hasan S., Mc Curdy D.K., Sharma S., Wong D., Hahn B.H., Rehimi H. The role of miRNA in inflammation and autoimmunity. Autoimmun. Rev. 2013, 12:1160-1165.
13. Frangou E.A., Bertsias G.K., Boumpas D.T. Gene expression and regulation in systemic lupus erythematosus. Eur. J. Clin. Invest. 2013, 43:1084-1096.
14. Tandon M., Gallo A., Jang S.I., Illei G.G., Alevizos I. Deep sequencing of short RNAs reveals novel microRNAs in minor salivary glands of patients with Sjogren's syndrome. Oral Dis. 2012, 18:127-131.
15. Thamilarasan M., Koczan D., Hecker M., Paap B., Zettl U.K. MicroRNAs in multiple sclerosis and experimental autoimmune encephalomyelitis. Autoimmun. Rev. 2012, 11:174-179.
16. Bader A.G., Brown D., Stoudemire J., Lammers P. Developing therapeutic microRNAs for cancer. Gene Ther. 2011, 18:1121-1126.
17. Garzon R., Marcucci G., Croce C.M. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat. Rev. Drug Discov. 2010, 9:775-789.
18. Calin G.A., Sevignani C., Dan Dumitru C., Hyslop T., Noch E., Yendamuri S., Shimizu M., Rattan S., Bullrich F., Negrini M., Croce C.M. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2999-3004.
19. Yang S., Li Y. MicroRNAs: novel factors in clinical diagnosis and prognosis for nasopharyngeal carcinoma. Acta Pharmacol. Sin. 2012, 33:981-982.
20. Rosenfeld N., Aharonov R., Meiri E., Rosenwald S., Spector Y., Zepeniuk M., Benjamin H., Shabes N., Tabak S., Levy A., Lebanony D., Goren Y., Silberschein E., Targan N., Ben-Ari A., Gilad S., Sion-Vardy N., Tobar A., Feinmesser M., Kharenko O., Nativ O., Nass D., Perelman M., Yosepovich A., Shalmon B., Polak-Charcon S., Fridman E., Avniel A., Bentwich I., Bentwich Z., Cohen D., Chajut A., Barshack I. MicroRNAs accurately identify cancer tissue origin. Nat. Biotechnol. 2008, 26:462-469.
21. Broderick J.A., Zamore P.D. MicroRNA therapeutics. Gene Ther. 2011, 18:1104-1110.
22. Kong Y.W., Ferland-McCollough D., Jackson T.J., Bushell M. MicroRNAs in cancer management. Lancet Oncol. 2012, 13:249-258.
23. Croce C.M. Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 2009, 10:704-714.
24. Esquela-Kerscher A., Slack F.J. Oncomirs - microRNAs with a role in cancer. Nat. Rev. Cancer 2006, 6:259-269.
25. Bonci D., Coppola V., Musumeci M., Addario A., Giuffrida R., Memeo L., D'Urso L., Pagliuca A., Biffoni M., Labbaye C., Bartucci M., Muto G., Peschle C., De Maria R. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat. Med. 2008, 14:1271-1277.
26. Osaki M., Takeshita F., Sugimoto Y., Kosaka N., Yamamoto Y., Yoshioka Y., Kobayashi E., Yamada T., Kawai A., Inoue T., Ito H., Oshimura M., Ochiya T. MicroRNA-143 regulates human osteosarcoma metastasis by regulating matrix metalloprotease-13 expression. Mol. Ther. 2011, 19:1123-1130.
27. Bader A.G., Brown D., Winkler M. The promise of microRNA replacement therapy. Cancer Res. 2010, 70:7027-7030.
28. Henry J.C., Azevedo-Pouly A.C., Schmittgen T.D. MicroRNA replacement therapy for cancer. Pharm. Res. 2011, 28:3030-3042.
29. Li H.R., Yang B.B. Friend or foe: the role of microRNA in chemotherapy resistance. Acta Pharmacol. Sin. 2013, 34:870-879.
30. Garofalo M., Croce C.M. MicroRNAs as therapeutic targets in chemoresistance. Drug Resist. Updat. 2013, 16:47-59.
31. Li Z.M., Hu S., Wang J., Cai J., Xiao L., Yu L.L., Wang Z.H. MiR-27a modulates MDR1/P-glycoprotein expression by targeting HIPK2 in human ovarian cancer cells. Gynecol. Oncol. 2010, 119:125-130.
32. Chen C.F., He X., Arslan A.D., Mo Y.Y., Reinhold W.C., Pommier Y., Beck W.T. Novel regulation of nuclear factor-YB by miR-485-3p affects the expression of DNA topoisomerase IIalpha and drug responsiveness. Mol. Pharmacol. 2011, 79:735-741.
33. Arora H., Qureshi R., Jin S., Park A.K., Park W.Y. miR-9 and let-7g enhance the sensitivity to ionizing radiation by suppression of NFkappaB1. Exp. Mol. Med. 2011, 43:298-304.
34. Zhang Y., Wang Z., Gemeinhart R.A. Progress in microRNA delivery. J. Control. Release 2013, 172:962-974.
35. Bravo V., Rosero S., Ricordi C., Pastori R.L. Instability of miRNA and cDNAs derivatives in RNA preparations. Biochem. Biophys. Res. Commun. 2007, 353:1052-1055.
36. Cho W.C.S. Role of miRNAs in lung cancer. Expert. Rev. Mol. Diagn. 2009, 9:773-776.
37. Pecot C.V., Calin G.A., Coleman R.L., Lopez-Berestein G., Sood A.K. RNA interference in the clinic: challenges and future directions. Nat. Rev. Cancer 2011, 11:59-67.
38. Grimm D., Streetz K.L., Jopling C.L., Storm T.A., Pandey K., Davis C.R., Marion P., Salazar F., Kay M.A. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 2006, 441:537-541.
39. Wang X., Yu B., Ren W., Mo X., Zhou C., He H., Jia H., Wang L., Jacob S.T., Lee R.J., Ghoshal K., Lee L.J. Enhanced hepatic delivery of siRNA and microRNA using oleic acid based lipid nanoparticle formulations. J. Control. Release 2013, 172:690-698.
40. Aagaard L., Rossi J.J. RNAi therapeutics: principles, prospects and challenges. Adv. Drug Deliv. Rev. 2007, 59:75-86.
41. Yang H.W., Huang C.Y., Lin C.W., Liu H.L., Huang C.W., Liao S.S., Chen P.Y., Lu Y.J., Wei K.C., Ma C.C. Gadolinium-functionalized nanographene oxide for combined drug and microRNA delivery and magnetic resonance imaging. Biomaterials 2014, 35:6534-6542.
42. Liu J., Valencia-Sanchez M.A., Hannon G.J., Parker R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 2005, 7:719-723.
43. Scholz C., Wagner E. Therapeutic plasmid DNA versus siRNA delivery: common and different tasks for synthetic carriers. J. Control. Release 2012, 161:554-565.
44. Whitehead K.A., Langer R., Anderson D.G. Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 2009, 8:129-138.
45. Gibbings D.J., Ciaudo C., Erhardt M., Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat. Cell Biol. 2009, 11:1143-1149.
46. Hatakeyama H., Murata M., Sato Y., Takahashi M., Minakawa N., Matsuda A., Harashima H. The systemic administration of an anti-miRNA oligonucleotide encapsulated pH-sensitive liposome results in reduced level of hepatic microRNA-122 in mice. J. Control. Release 2014, 173:43-50.
47. Anand S., Majeti B.K., Acevedo L.M., Murphy E.A., Mukthavaram R., Scheppke L., Huang M., Shields D.J., Lindquist J.N., Lapinski P.E., King P.D., Weis S.M., Cheresh D.A. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat. Med. 2010, 16:909-914.
48. Dai F.R., Zhang Y., Zhu X., Shan N.C., Chen Y.X. Anticancer role of MUC1 aptamer-miR-29b chimera in epithelial ovarian carcinoma cells through regulation of PTEN methylation. Target. Oncol. 2012, 7:217-225.
49. Wu Y., Crawford M., Mao Y., Lee R.J., Davis I.C., Elton T.S., Lee L.J., Nana-Sinkam S.P. Therapeutic delivery of microRNA-29b by cationic lipoplexes for lung cancer. Mol. Ther. Nucleic Acids 2013, 2:e84.
50. Wu Y., Crawford M., Yu B., Mao Y., Nana-Sinkam S.P., Lee L.J. MicroRNA delivery by cationic lipoplexes for lung cancer therapy. Mol. Pharm. 2011, 8:1381-1389.
51. Rai K., Takigawa N., Ito S., Kashihara H., Ichihara E., Yasuda T., Shimizu K., Tanimoto M., Kiura K. Liposomal delivery of microRNA-7-expressing plasmid overcomes epidermal growth factor receptor tyrosine kinase inhibitor-resistance in lung cancer cells. Mol. Cancer Ther. 2011, 10:1720-1727.
52. Piao L., Zhang M., Datta J., Xie X., Su T., Li H., Teknos T.N., Pan Q. Lipid-based nanoparticle delivery of pre-miR-107 inhibits the tumorigenicity of head and neck squamous cell carcinoma. Mol. Ther. 2012, 20:1261-1269.
53. de Antonellis P., Medaglia C., Cusanelli E., Andolfo I., Liguori L., De Vita G., Carotenuto M., Bello A., Formiggini F., Galeone A., De Rosa G., Virgilio A., Scognamiglio I., Sciro M., Basso G., Schulte J.H., Cinalli G., Iolascon A., Zollo M. MiR-34a targeting of Notch ligand delta-like 1 impairs CD15+/CD133+ tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS One 2011, 6:e24584.
54. Kamaly N., Xiao Z., Valencia P.M., Radovic-Moreno A.F., Farokhzad O.C. Targeted polymeric therapeutic nanoparticles: design, development and clinical translation. Chem. Soc. Rev. 2012, 41:2971-3010.
55. Zuhorn I.S., Engberts J.B., Hoekstra D. Gene delivery by cationic lipid vectors: overcoming cellular barriers. Eur. Biophys. J. 2007, 36:349-362.
56. Wiggins J.F., Ruffino L., Kelnar K., Omotola M., Patrawala L., Brown D., Bader A.G. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res. 2010, 70:5923-5930.
57. Trang P., Wiggins J.F., Daige C.L., Cho C., Omotola M., Brown D., Weidhaas J.B., Bader A.G., Slack F.J. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol. Ther. 2011, 19:1116-1122.
58. Bikram M., Lee M., Chang C.W., Janat-Amsbury M.M., Kern S.E., Kim S.W. Long-circulating DNA-complexed biodegradable multiblock copolymers for gene delivery: degradation profiles and evidence of dysopsonization. J. Control. Release 2005, 103:221-233.
59. Pramanik D., Campbell N.R., Karikari C., Chivukula R., Kent O.A., Mendell J.T., Maitra A. Restitution of tumor suppressor microRNAs using a systemic nanovector inhibits pancreatic cancer growth in mice. Mol. Cancer Ther. 2011, 10:1470-1480.
60. Li S.D., Huang L. Stealth nanoparticles: high density but sheddable PEG is a key for tumor targeting. J. Control. Release 2010, 145:178-181.
61. Maeda H. The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. Adv. Enzym. Regul. 2001, 41:189-207.
62. Boussif O., Lezoualch F., Zanta M.A., Mergny M.D., Scherman D., Demeneix B., Behr J.P. A versatile vector for gene and oligonucleotide transfer into cells in culture and in-vivo - polyethylenimine. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7297-7301.
63. Rodl W., Schaffert D., Wagner E., Ogris M. Synthesis of polyethylenimine-based nanocarriers for systemic tumor targeting of nucleic acids. Methods Mol. Biol. 2013, 948:105-120.
64. Kunath K., von Harpe A., Fischer D., Peterson H., Bickel U., Voigt K., Kissel T. Low-molecular-weight polyethylenimine as a non-viral vector for DNA delivery: comparison of physicochemical properties, transfection efficiency and in vivo distribution with high-molecular-weight polyethylenimine. J. Control. Release 2003, 89:113-125.
65. Bieber T., Elsasser H.P. Preparation of a low molecular weight polyethylenimine for efficient cell transfection. Biotechniques 2001, 30. (74-+).
66. Gebhart C.L., Kabanov A.V. Evaluation of polyplexes as gene transfer agents. J. Control. Release 2001, 73:401-416.
67. Ibrahim A.F., Weirauch U., Thomas M., Grunweller A., Hartmann R.K., Aigner A. MicroRNA replacement therapy for miR-145 and miR-33a is efficacious in a model of colon carcinoma. Cancer Res. 2011, 71:5214-5224.
68. Chiou G.Y., Cherng J.Y., Hsu H.S., Wang M.L., Tsai C.M., Lu K.H., Chien Y., Hung S.C., Chen Y.W., Wong C.I., Tseng L.M., Huang P.I., Yu C.C., Hsu W.H., Chiou S.H. Cationic polyurethanes-short branch PEI-mediated delivery of Mir145 inhibited epithelial-mesenchymal transdifferentiation and cancer stem-like properties and in lung adenocarcinoma. J. Control. Release 2012, 159:240-250.
69. Yang Y.P., Chien Y., Chiou G.Y., Cherng J.Y., Wang M.L., Lo W.L., Chang Y.L., Huang P.I., Chen Y.W., Shih Y.H., Chen M.T., Chiou S.H. Inhibition of cancer stem cell-like properties and reduced chemoradioresistance of glioblastoma using microRNA145 with cationic polyurethane-short branch PEI. Biomaterials 2012, 33:1462-1476.
70. Ochiya T., Nagahara S., Sano A., Itoh H., Terada M. Biomaterials for gene delivery: atelocollagen-mediated controlled release of molecular medicines. Curr. Gene Ther. 2001, 1:31-52.
71. Minakuchi Y., Takeshita F., Kosaka N., Sasaki H., Yamamoto Y., Kouno M., Honma K., Nagahara S., Hanai K., Sano A., Kato T., Terada M., Ochiya T. Atelocollagen-mediated synthetic small interfering RNA delivery for effective gene silencing in vitro and in vivo. Nucleic Acids Res. 2004, 32:e109.
72. Takeshita F., Minakuchi Y., Nagahara S., Honma K., Sasaki H., Hirai K., Teratani T., Namatame N., Yamamoto Y., Hanai K., Kato T., Sano A., Ochiya T. Efficient delivery of small interfering RNA to bone-metastatic tumors by using atelocollagen in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12177-12182.
73. Tazawa H., Tsuchiya N., Izumiya M., Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:15472-15477.
74. Matsuyama H., Suzuki H.I., Nishimori H., Noguchi M., Yao T., Komatsu N., Mano H., Sugimoto K., Miyazono K. miR-135b mediates NPM-ALK-driven oncogenicity and renders IL-17-producing immunophenotype to anaplastic large cell lymphoma. Blood 2011, 118:6881-6892.
75. Takei Y., Takigahira M., Mihara K., Tarumi Y., Yanagihara K. The metastasis-associated microRNA miR-516a-3p is a novel therapeutic target for inhibiting peritoneal dissemination of human scirrhous gastric cancer. Cancer Res. 2011, 71:1442-1453.
76. Takeshita F., Patrawala L., Osaki M., Takahashi R.U., Yamamoto Y., Kosaka N., Kawamata M., Kelnar K., Bader A.G., Brown D., Ochiya T. Systemic delivery of synthetic microRNA-16 inhibits the growth of metastatic prostate tumors via downregulation of multiple cell-cycle genes. Mol. Ther. 2010, 18:181-187.
77. Zhou Y., Zhang L., Zhao W., Wu Y., Zhu C., Yang Y. Nanoparticle-mediated delivery of TGF-beta1 miRNA plasmid for preventing flexor tendon adhesion formation. Biomaterials 2013, 34:8269-8278.
78. Cheng C.J., Saltzman W.M. Polymer nanoparticle-mediated delivery of microRNA inhibition and alternative splicing. Mol. Pharm. 2012, 9:1481-1488.
79. Tinsley-Bown A.M., Fretwell R., Dowsett A.B., Davis S.L., Farrar G.H. Formulation of poly(D,L-lactic-co-glycolic acid) microparticles for rapid plasmid DNA delivery. J. Control. Release 2000, 66:229-241.
80. Otten G., Schaefer M., Greer C., Calderon-Cacia M., Coit D., Kazzaz J., Medina-Selby A., Selby M., Singh M., Ugozzoli M., zur Megede J., Barnett S.W., O'Hagan D., Donnelly J., Ulmer J. Induction of broad and potent anti-human immunodeficiency virus immune responses in rhesus macaques by priming with a DNA vaccine and boosting with protein-adsorbed polylactide coglycolide microparticles. J. Virol. 2003, 77:6087-6092.
81. Dailey L.A., Wittmar M., Kissel T. The role of branched polyesters and their modifications in the development of modern drug delivery vehicles. J. Control. Release 2005, 101:137-149.
82. Duncan R., Izzo L. Dendrimer biocompatibility and toxicity. Adv. Drug Deliv. Rev. 2005, 57:2215-2237.
83. Ren Y., Kang C.S., Yuan X.B., Zhou X., Xu P., Han L., Wang G.X., Jia Z., Zhong Y., Yu S., Sheng J., Pu P.Y. Co-delivery of as-miR-21 and 5-FU by poly(amidoamine) dendrimer attenuates human glioma cell growth in vitro, Journal of biomaterials science. J. Biomater. Sci. Polym. Ed. 2010, 21:303-314.
84. Li X., Xin S., He Z., Che X., Wang J., Xiao X., Chen J., Song X. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor PDCD4 and promotes cell transformation, proliferation, and metastasis in renal cell carcinoma. Cell. Physiol. Biochem. 2014, 33:1631-1642.
85. Ren Y., Zhou X., Mei M., Yuan X.B., Han L., Wang G.X., Jia Z.F., Xu P., Pu P.Y., Kang C.S. MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC Cancer 2010, 10:27.
86. Labieniec-Watala M., Karolczak K., Siewiera K., Watala C. The janus face of PAMAM dendrimers used to potentially cure nonenzymatic modifications of biomacromolecules in metabolic disorders-a critical review of the pros and cons. Molecules 2013, 18:13769-13811.
87. Jiang Y.Y., Tang G.T., Zhang L.H., Kong S.Y., Zhu S.J., Pei Y.Y. PEGylated PAMAM dendrimers as a potential drug delivery carrier: in vitro and in vivo comparative evaluation of covalently conjugated drug and noncovalent drug inclusion complex. J. Drug Target. 2010, 18:389-403.
88. Bhadra D., Bhadra S., Jain S., Jain N.K. A PEGylated dendritic nanoparticulate carrier of fluorouracil. Int. J. Pharm. 2003, 257:111-124.
89. Jevprasesphant R., Penny J., Jalal R., Attwood D., McKeown N.B., D'Emanuele A. The influence of surface modification on the cytotoxicity of PAMAM dendrimers. Int. J. Pharm. 2003, 252:263-266.
90. Cho H.Y., Srinivasan A., Hong J., Hsu E., Liu S., Shrivats A., Kwak D., Bohaty A.K., Paik H.J., Hollinger J.O., Matyjaszewski K. Synthesis of biocompatible PEG-based star polymers with cationic and degradable core for siRNA delivery. Biomacromolecules 2011, 12:3478-3486.
91. Qian X., Long L., Shi Z., Liu C., Qiu M., Sheng J., Pu P., Yuan X., Ren Y., Kang C. Star-branched amphiphilic PLA-b-PDMAEMA copolymers for co-delivery of miR-21 inhibitor and doxorubicin to treat glioma. Biomaterials 2014, 35:2322-2335.
92. Cao M.J., Deng X.W., Su S.S., Zhang F., Xiao X.Q., Hu Q., Fu Y.W., Yang B.B., Wu Y., Sheng W., Zeng Y. Protamine sulfate-nanodiamond hybrid nanoparticles as a vector for MiR-203 restoration in esophageal carcinoma cells. Nanoscale 2013, 5:12120-12125.
93. Bitar A., Ahmad N.M., Fessi H., Elaissari A. Silica-based nanoparticles for biomedical applications. Drug Discov. Today 2012, 17:1147-1154.
94. Schade A., Delyagina E., Scharfenberg D., Skorska A., Lux C., David R., Steinhoff G. Innovative strategy for microRNA delivery in human mesenchymal stem cells via magnetic nanoparticles. Int. J. Mol. Sci. 2013, 14:10710-10726.
95. Vigderman L., Zubarev E.R. Therapeutic platforms based on gold nanoparticles and their covalent conjugates with drug molecules. Adv. Drug Deliv. Rev. 2013, 65:663-676.
96. Crew E., Tessel M.A., Rahman S., Razzak-Jaffar A., Mott D., Kamundi M., Yu G., Tchah N., Lee J., Bellavia M., Zhong C.J. MicroRNA conjugated gold nanoparticles and cell transfection. Anal. Chem. 2012, 84:10147.
97. Ghosh R., Singh L.C., Shohet J.M., Gunaratne P.H. A gold nanoparticle platform for the delivery of functional microRNAs into cancer cells. Biomaterials 2013, 34:807-816.
98. Kim J.H., Yeom J.H., Ko J.J., Han M.S., Lee K., Na S.Y., Bae J. Effective delivery of anti-miRNA DNA oligonucleotides by functionalized gold nanoparticles. J. Biotechnol. 2011, 155:287-292.
99. Trang P., Medina P.P., Wiggins J.F., Ruffino L., Kelnar K., Omotola M., Homer R., Brown D., Bader A.G., Weidhaas J.B., Slack F.J. Regression of murine lung tumors by the let-7 microRNA. Oncogene 2010, 29:1580-1587.
100. Saini S., Yamamura S., Majid S., Shahryari V., Hirata H., Tanaka Y., Dahiya R. MicroRNA-708 induces apoptosis and suppresses tumorigenicity in renal cancer cells. Cancer Res. 2011, 71:6208-6219.
101. Shi S., Han L., Gong T., Zhang Z., Sun X. Systemic delivery of microRNA-34a for cancer stem cell therapy. Angew. Chem. Int. Engl. 2013, 52:3901-3905.
102. Craig V.J., Tzankov A., Flori M., Schmid C.A., Bader A.G., Muller A. Systemic microRNA-34a delivery induces apoptosis and abrogates growth of diffuse large B-cell lymphoma in vivo. Leukemia 2012, 26:2421-2424.
103. Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv. Drug Deliv. Rev. 2011, 63:131-135.
104. Maruyama K. Intracellular targeting delivery of liposomal drugs to solid tumors based on EPR effects. Adv. Drug Deliv. Rev. 2011, 63:161-169.
105. Brannon-Peppas L., Blanchette J.O. Nanoparticle and targeted systems for cancer therapy. Adv. Drug Deliv. Rev. 2004, 56:1649-1659.
106. Schmidt M.M., Wittrup K.D. A modeling analysis of the effects of molecular size and binding affinity on tumor targeting. Mol. Cancer Ther. 2009, 8:2861-2871.
107. Babar I.A., Cheng C.J., Booth C.J., Liang X.P., Weidhaas J.B., Saltzman W.M., Slack F.J. Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1695-E1704.
108. Shi S.J., Han L., Gong T., Zhang Z.R., Sun X. Systemic delivery of microRNA-34a for cancer stem cell therapy. Angew. Chem. Int. Ed. Engl. 2013, 52:3901-3905.
109. Bae Y.H. Drug targeting and tumor heterogeneity. J. Control. Release 2009, 133:2-3.
110. Singh S.R., Grossniklaus H.E., Kang S.J., Edelhauser H.F., Ambati B.K., Kompella U.B. Intravenous transferrin, RGD peptide and dual-targeted nanoparticles enhance anti-VEGF intraceptor gene delivery to laser-induced CNV. Gene Ther. 2009, 16:645-659.
111. Nasongkla N., Shuai X., Ai H., Weinberg B.D., Pink J., Boothman D.A., Gao J. cRGD-functionalized polymer micelles for targeted doxorubicin delivery. Angew. Chem. Int. Ed. Engl. 2004, 43:6323-6327.
112. Liu X.Q., Song W.J., Sun T.M., Zhang P.Z., Wang J. Targeted delivery of antisense inhibitor of miRNA for antiangiogenesis therapy using cRGD-functionalized nanoparticles. Mol. Pharm. 2011, 8:250-259.
113. Sugahara K.N., Teesalu T., Karmali P.P., Kotamraju V.R., Agemy L., Greenwald D.R., Ruoslahti E. Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 2010, 328:1031-1035.
114. Hu Q.L., Jiang Q.Y., Jin X., Shen J., Wang K., Li Y.B., Xu F.J., Tang G.P., Li Z.H. Cationic microRNA-delivering nanovectors with bifunctional peptides for efficient treatment of PANC-1 xenograft model. Biomaterials 2013, 34:2265-2276.
115. Lee H.J., Namgung R., Kim W.J., Kim J.I., Park I.K. Targeted delivery of microRNA-145 to metastatic breast cancer by peptide conjugated branched PEI gene carrier. Macromol. Res. 2013, 21:1201-1209.
116. Klutz K., Schaffert D., Willhauck M.J., Grunwald G.K., Haase R., Wunderlich N., Zach C., Gildehaus F.J., Senekowitsch-Schmidtke R., Goke B., Wagner E., Ogris M., Spitzweg C. Epidermal growth factor receptor-targeted I-131-therapy of liver cancer following systemic delivery of the sodium iodide symporter gene. Mol. Ther. 2011, 19:676-685.
117. Ohno S., Takanashi M., Sudo K., Ueda S., Ishikawa A., Matsuyama N., Fujita K., Mizutani T., Ohgi T., Ochiya T., Gotoh N., Kuroda M. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol. Ther. 2013, 21:185-191.
118. Hwang D.W., Son S., Jang J., Youn H., Lee S., Lee D., Lee Y.S., Jeong J.M., Kim W.J., Lee D.S. A brain-targeted rabies virus glycoprotein-disulfide linked PEI nanocarrier for delivery of neurogenic microRNA. Biomaterials 2011, 32:4968-4975.
119. Maiorano N.A., Mallamaci A. Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev. 2009, 4:40.
120. Kumar P., Wu H., McBride J.L., Jung K.E., Kim M.H., Davidson B.L., Lee S.K., Shankar P., Manjunath N. Transvascular delivery of small interfering RNA to the central nervous system. Nature 2007, 448:39-43.
121. Yi X., Yuan D., Farr S.A., Banks W.A., Poon C.D., Kabanov A.V. Pluronic modified leptin with increased systemic circulation, brain uptake and efficacy for treatment of obesity. J. Control. Release 2014, 191:34-46.
122. Price T.O., Farr S.A., Yi X., Vinogradov S., Batrakova E., Banks W.A., Kabanov A.V. Transport across the blood-brain barrier of pluronic leptin. J. Pharmacol. Exp. Ther. 2010, 333:253-263.
123. Zhang X., Koh C.G., Yu B., Liu S., Piao L., Marcucci G., Lee R.J., Lee L.J. Transferrin receptor targeted lipopolyplexes for delivery of antisense oligonucleotide g3139 in a murine k562 xenograft model. Pharm. Res. 2009, 26:1516-1524.
124. Pardridge W.M. Blood-brain barrier drug delivery of IgG fusion proteins with a transferrin receptor monoclonal antibody. Expert Opin. Drug Deliv. 2014, 1-16.
125. Zhou Q.H., Boado R.J., Hui E.K., Lu J.Z., Pardridge W.M. Chronic dosing of mice with a transferrin receptor monoclonal antibody-glial-derived neurotrophic factor fusion protein. Drug Metab. Dispos. 2011, 39:1149-1154.
126. Huang X., Schwind S., Yu B., Santhanam R., Wang H., Hoellerbauer P., Mims A., Klisovic R., Walker A.R., Chan K.K., Blum W., Perrotti D., Byrd J.C., Bloomfield C.D., Caligiuri M.A., Lee R.J., Garzon R., Muthusamy N., Lee L.J., Marcucci G. Targeted delivery of microRNA-29b by transferrin-conjugated anionic lipopolyplex nanoparticles: a novel therapeutic strategy in acute myeloid leukemia. Clin. Cancer Res. 2013, 19:2355-2367.
127. Ahmad Z.A., Yeap S.K., Ali A.M., Ho W.Y., Alitheen N.B., Hamid M. scFv antibody: principles and clinical application. Clin. Dev. Immunol. 2012, (2012):980250.
128. 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. 2010, 18:1650-1656.
129. Tivnan A., Orr W.S., Gubala V., Nooney R., Williams D.E., McDonagh C., Prenter S., Harvey H., Domingo-Fernandez R., Bray I.M., Piskareva O., Ng C.Y., Lode H.N., Davidoff A.M., Stallings R.L. Inhibition of neuroblastoma tumor growth by targeted delivery of microRNA-34a using anti-disialoganglioside GD2 coated nanoparticles. PLoS One 2012, 7:e38129.
130. Wu X., Ding B., Gao J., Wang H., Fan W., Wang X., Zhang W., Wang X., Ye L., Zhang M., Ding X., Liu J., Zhu Q., Gao S. Second-generation aptamer-conjugated PSMA-targeted delivery system for prostate cancer therapy. Int. J. Nanomedicine 2011, 6:1747-1756.
131. Kim J.K., Choi K.J., Lee M., Jo M.H., Kim S. Molecular imaging of a cancer-targeting theragnostics probe using a nucleolin aptamer- and microRNA-221 molecular beacon-conjugated nanoparticle. Biomaterials 2012, 33:207-217.
132. Deng X., Cao M., Zhang J., Hu K., Yin Z., Zhou Z., Xiao X., Yang Y., Sheng W., Wu Y., Zeng Y. Hyaluronic acid-chitosan nanoparticles for co-delivery of MiR-34a and doxorubicin in therapy against triple negative breast cancer. Biomaterials 2014, 35:4333-4344.
133. Ye X., Liu Z., Hemida M.G., Yang D. Targeted delivery of mutant tolerant anti-coxsackievirus artificial microRNAs using folate conjugated bacteriophage Phi29 pRNA. PLoS One 2011, 6:e21215.
134. Orian-Rousseau V. CD44, a therapeutic target for metastasising tumours. Eur. J. Cancer 2010, 46:1271-1277.
135. Veiseh O., Gunn J.W., Zhang M. Design and fabrication of magnetic nanoparticles for targeted drug delivery and imaging. Adv. Drug Deliv. Rev. 2010, 62:284-304.
136. Li W., Ma N., Ong L.L., Kaminski A., Skrabal C., Ugurlucan M., Lorenz P., Gatzen H.H., Lutzow K., Lendlein A., Putzer B.M., Li R.K., Steinhoff G. Enhanced thoracic gene delivery by magnetic nanobead-mediated vector. J. Gene Med. 2008, 10:897-909.
137. 4@polydopamine core-shell nanocomposites for intracellular mRNA detection and imaging-guided photothermal therapy. ACS Nano 2014, 8:3876-3883.
138. Schade A., Muller P., Delyagina E., Voronina N., Skorska A., Lux C., Steinhoff G., David R. Magnetic nanoparticle based nonviral microRNA delivery into freshly isolated CD105(+) hMSCs. Stem Cells Int. 2014, 2014:197154.
139. Yigit M.V., Ghosh S.K., Kumar M., Petkova V., Kavishwar A., Moore A., Medarova Z. Context-dependent differences in miR-10b breast oncogenesis can be targeted for the prevention and arrest of lymph node metastasis. Oncogene 2013, 32:1530-1538.
140. Li F., Mahato R.I. MicroRNAs and drug resistance in prostate cancers. Mol. Pharm. 2014, 11:2539-2552.
141. Choi K.M., Choi S.H., Jeon H., Kim I.S., Ahn H.J. Chimeric capsid protein as a nanocarrier for siRNA delivery: stability and cellular uptake of encapsulated siRNA. ACS Nano 2011, 5:8690-8699.
142. Ledford H. Drug giants turn their backs on RNA interference. Nature 2010, 468:487.
143. Zeng X., Sun Y.X., Qu W., Zhang X.Z., Zhuo R.X. Biotinylated transferrin/avidin/biotinylated disulfide containing PEI bioconjugates mediated p53 gene delivery system for tumor targeted transfection. Biomaterials 2010, 31:4771-4780.
144. Batrakova E.V., Kabanov A.V. Pluronic block copolymers: evolution of drug delivery concept from inert nanocarriers to biological response modifiers. J. Control. Release 2008, 130:98-106.
145. Panyam J., Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev. 2012, 64:61-71.
146. Obad S., dos Santos C.O., Petri A., Heidenblad M., Broom O., Ruse C., Fu C., Lindow M., Stenvang J., Straarup E.M., Hansen H.F., Koch T., Pappin D., Hannon G.J., Kauppinen S. Silencing of microRNA families by seed-targeting tiny LNAs. Nat. Genet. 2011, 43:371-378.
147. Guo J., Evans J.C., O'Driscoll C.M. Delivering RNAi therapeutics with non-viral technology: a promising strategy for prostate cancer?. Trends Mol. Med. 2013, 19:250-261.
148. Bouchie A. First microRNA mimic enters clinic. Nat. Biotechnol. 2013, 31:577.
149. Khan S., Ansarullah, Kumar D., Jaggi M., Chauhan S.C. Targeting microRNAs in pancreatic cancer: microplayers in the big game. Cancer Res. 2013, 73:6541-6547.
150. van Rooij E., Purcell A.L., Levin A.A. Developing microRNA therapeutics. Circ. Res. 2012, 110:496-507.