In vivo delivery of miRNAs for cancer therapy: Challenges and strategies

Advanced Drug Delivery Reviews

Volumn 81, Issue , 2015, Pages 128-141

  Chen, Yunching ^a   Gao, Dong Yu ^a   Huang, Leaf ^b  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b UNC Hamner Institute for Drug Safety Sciences   (United States)

Author keywords

Cancer therapy; Gene delivery; In vivo delivery; MiRNA; Nanotechnology

Indexed keywords

CELL DEATH; CELL SIGNALING; DIAGNOSIS; DISEASES; GENE EXPRESSION; GENE TRANSFER; NANOTECHNOLOGY; ONCOGENIC VIRUSES; ONCOLOGY;

CANCER THERAPY; CELL-CYCLE PROGRESSION; GENE DELIVERY; IN-VIVO; MIRNA; POST-TRANSCRIPTIONAL; THERAPEUTIC TARGETS; TUMOR SUPPRESSOR GENES;

RNA;

DOUBLE STRANDED RNA; DRUG CARRIER; MICRORNA; NANOPARTICLE; POLYMER; SINGLE STRANDED RNA;

CANCER DIAGNOSIS; CANCER THERAPY; CELL DEATH; CELL METABOLISM; CELL PROLIFERATION; CHEMICAL MODIFICATION; DRUG CLEARANCE; DRUG DECOMPOSITION; DRUG DELIVERY SYSTEM; DRUG PENETRATION; DRUG TARGETING; ENDOSOME; GENE SILENCING; HUMAN; IMMUNOTOXICITY; LIPOSOMAL DELIVERY; LIPOSOMAL GENE DELIVERY SYSTEM; METASTASIS; NEUROTOXICITY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PHARMACODYNAMICS; REVIEW; RNA DEGRADATION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; VIRAL GENE DELIVERY SYSTEM; ANIMAL; DISEASE COURSE; GENE EXPRESSION REGULATION; GENE TRANSFER; GENETICS; NEOPLASMS; RNA PROCESSING;

ANIMALS; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENE TRANSFER TECHNIQUES; HUMANS; MICRORNAS; NEOPLASMS; RNA PROCESSING, POST-TRANSCRIPTIONAL; SIGNAL TRANSDUCTION;

EID: 84922273505     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.05.009     Document Type: Review

References (153)

1. 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.
2. Arora A., Scholar E.M. Role of tyrosine kinase inhibitors in cancer therapy. J. Pharmacol. Exp. Ther. 2005, 315:971-979.
3. Kris M.G., Natale R.B., Herbst R.S., Lynch T.J., Prager D., Belani C.P., Schiller J.H., Kelly K., Spiridonidis H., Sandler A., Albain K.S., Cella D., Wolf M.K., Averbuch S.D., Ochs J.J., Kay A.C. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. JAMA 2003, 290:2149-2158.
4. Druker B.J., Lydon N.B. Lessons learned from the development of an abl tyrosine kinase inhibitor for chronic myelogenous leukemia. J. Clin. Invest. 2000, 105:3-7.
5. Scott A.M., Wolchok J.D., Old L.J. Antibody therapy of cancer. Nat. Rev. Cancer 2012, 12:278-287.
6. Amado R.G., Wolf M., Peeters M., Van Cutsem E., Siena S., Freeman D.J., Juan T., Sikorski R., Suggs S., Radinsky R., Patterson S.D., Chang D.D. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J. Clin. Oncol. 2008, 26:1626-1634.
7. Karapetis C.S., Khambata-Ford S., Jonker D.J., O'Callaghan C.J., Tu D., Tebbutt N.C., Simes R.J., Chalchal H., Shapiro J.D., Robitaille S., Price T.J., Shepherd L., Au H.J., Langer C., Moore M.J., Zalcberg J.R. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N. Engl. J. Med. 2008, 359:1757-1765.
8. Lievre A., Bachet J.B., Boige V., Cayre A., Le Corre D., Buc E., Ychou M., Bouche O., Landi B., Louvet C., Andre T., Bibeau F., Diebold M.D., Rougier P., Ducreux M., Tomasic G., Emile J.F., Penault-Llorca F., Laurent-Puig P. KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. J. Clin. Oncol. 2008, 26:374-379.
9. Pillay V., Gan H.K., Scott A.M. Antibodies in oncology. N. Biotechnol. 2011, 28:518-529.
10. Weiner L.M., Surana R., Wang S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat. Rev. Immunol. 2010, 10:317-327.
11. Hu W., Jin L., Jiang C.C., Long G.V., Scolyer R.A., Wu Q., Zhang X.D., Mei Y., Wu M. AEBP1 upregulation confers acquired resistance to BRAF (V600E) inhibition in melanoma. Cell Death Dis. 2013, 4:e914.
12. Zhu A.X., Duda D.G., Sahani D.V., Jain R.K. HCC and angiogenesis: possible targets and future directions. Nat. Rev. Clin. Oncol. 2011, 8:292-301.
13. Suarez Y., Sessa W.C. MicroRNAs as novel regulators of angiogenesis. Circ. Res. 2009, 104:442-454.
14. Plummer P.N., Freeman R., Taft R.J., Vider J., Sax M., Umer B.A., Gao D., Johns C., Mattick J.S., Wilton S.D., Ferro V., McMillan N.A., Swarbrick A., Mittal V., Mellick A.S. MicroRNAs regulate tumor angiogenesis modulated by endothelial progenitor cells. Cancer Res. 2013, 73:341-352.
15. Enkelmann A., Heinzelmann J., von Eggeling F., Walter M., Berndt A., Wunderlich H., Junker K. Specific protein and miRNA patterns characterise tumour-associated fibroblasts in bladder cancer. J. Cancer Res. Clin. Oncol. 2011, 137:751-759.
16. Nielsen B.S., Jorgensen S., Fog J.U., Sokilde R., Christensen I.J., Hansen U., Brunner N., Baker A., Moller S., Nielsen H.J. High levels of microRNA-21 in the stroma of colorectal cancers predict short disease-free survival in stage II colon cancer patients. Clin. Exp. Metastasis 2011, 28:27-38.
17. Stenvang J., Petri A., Lindow M., Obad S., Kauppinen S. Inhibition of microRNA function by antimiR oligonucleotides. Silence 2012, 3:1.
18. Hansen T.F., Christensen R., Andersen R.F., Sorensen F.B., Johnsson A., Jakobsen A. MicroRNA-126 and epidermal growth factor-like domain 7-an angiogenic couple of importance in metastatic colorectal cancer. Results from the Nordic ACT trial. Br. J. Cancer 2013, 109:1243-1251.
19. Valencia-Sanchez M.A., Liu J., Hannon G.J., Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006, 20:515-524.
20. Lewis B.P., Burge C.B., Bartel D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
21. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
22. Yekta S., Shih I.H., Bartel D.P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 2004, 304:594-596.
23. Macfarlane L.A., Murphy P.R. MicroRNA: biogenesis, function and role in cancer. Curr. Genomics 2010, 11:537-561.
24. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
25. Arroyo J.D., Chevillet J.R., Kroh E.M., Ruf I.K., Pritchard C.C., Gibson D.F., Mitchell P.S., Bennett C.F., Pogosova-Agadjanyan E.L., Stirewalt D.L., Tait J.F., Tewari M. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5003-5008.
26. Vickers K.C., Palmisano B.T., Shoucri B.M., Shamburek R.D., Remaley A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 2011, 13:423-433.
27. Lawrie C.H., Gal S., Dunlop H.M., Pushkaran B., Liggins A.P., Pulford K., Banham A.H., Pezzella F., Boultwood J., Wainscoat J.S., Hatton C.S., Harris A.L. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br. J. Haematol. 2008, 141:672-675.
28. Chen X., Ba Y., Ma L., Cai X., Yin Y., Wang K., Guo J., Zhang Y., Chen J., Guo X., Li Q., Li X., Wang W., Zhang Y., Wang J., Jiang X., Xiang Y., Xu C., Zheng P., Zhang J., Li R., Zhang H., Shang X., Gong T., Ning G., Wang J., Zen K., Zhang J., Zhang C.Y. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008, 18:997-1006.
29. Pritchard C.C., Kroh E., Wood B., Arroyo J.D., Dougherty K.J., Miyaji M.M., Tait J.F., Tewari M. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev. Res. (Phila.) 2012, 5:492-497.
30. Yu Z., Baserga R., Chen L., Wang C., Lisanti M.P., Pestell R.G. microRNA, cell cycle, and human breast cancer. Am. J. Pathol. 2010, 176:1058-1064.
31. Garofalo M., Quintavalle C., Di Leva G., Zanca C., Romano G., Taccioli C., Liu C.G., Croce C.M., Condorelli G. MicroRNA signatures of TRAIL resistance in human non-small cell lung cancer. Oncogene 2008, 27:3845-3855.
32. Xiao C., Srinivasan L., Calado D.P., Patterson H.C., Zhang B., Wang J., Henderson J.M., Kutok J.L., Rajewsky K. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol. 2008, 9:405-414.
33. Lima R.T., Busacca S., Almeida G.M., Gaudino G., Fennell D.A., Vasconcelos M.H. MicroRNA regulation of core apoptosis pathways in cancer. Eur. J. Cancer 2011, 47:163-174.
34. Cimmino A., Calin G.A., Fabbri M., Iorio M.V., Ferracin M., Shimizu M., Wojcik S.E., Aqeilan R.I., Zupo S., Dono M., Rassenti L., Alder H., Volinia S., Liu C.G., Kipps T.J., Negrini M., Croce C.M. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13944-13949.
35. Chen B., Li H., Zeng X., Yang P., Liu X., Zhao X., Liang S. Roles of microRNA on cancer cell metabolism. J. Transl. Med. 2012, 10:228.
36. Horie T., Ono K., Nishi H., Iwanaga Y., Nagao K., Kinoshita M., Kuwabara Y., Takanabe R., Hasegawa K., Kita T., Kimura T. MicroRNA-133 regulates the expression of GLUT4 by targeting KLF15 and is involved in metabolic control in cardiac myocytes. Biochem. Biophys. Res. Commun. 2009, 389:315-320.
37. Koh H.J., Toyoda T., Fujii N., Jung M.M., Rathod A., Middelbeek R.J., Lessard S.J., Treebak J.T., Tsuchihara K., Esumi H., Richter E.A., Wojtaszewski J.F., Hirshman M.F., Goodyear L.J. Sucrose nonfermenting AMPK-related kinase (SNARK) mediates contraction-stimulated glucose transport in mouse skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15541-15546.
38. Davalos A., Goedeke L., Smibert P., Ramirez C.M., Warrier N.P., Andreo U., Cirera-Salinas D., Rayner K., Suresh U., Pastor-Pareja J.C., Esplugues E., Fisher E.A., Penalva L.O., Moore K.J., Suarez Y., Lai E.C., Fernandez-Hernando C. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9232-9237.
39. Mersey B.D., Jin P., Danner D.J. Human microRNA (miR29b) expression controls the amount of branched chain alpha-ketoacid dehydrogenase complex in a cell. Hum. Mol. Genet. 2005, 14:3371-3377.
40. Zhang Y., Yang P., Wang X.F. Microenvironmental regulation of cancer metastasis by miRNAs. Trends Cell Biol. 2014, 24:153-160.
41. Ghosh G., Subramanian I.V., Adhikari N., Zhang X., Joshi H.P., Basi D., Chandrashekhar Y.S., Hall J.L., Roy S., Zeng Y., Ramakrishnan S. Hypoxia-induced microRNA-424 expression in human endothelial cells regulates HIF-alpha isoforms and promotes angiogenesis. J. Clin. Invest. 2010, 120:4141-4154.
42. Zhou B., Ma R., Si W., Li S., Xu Y., Tu X., Wang Q. MicroRNA-503 targets FGF2 and VEGFA and inhibits tumor angiogenesis and growth. Cancer Lett. 2013, 333:159-169.
43. Iorio M.V., Croce C.M. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med. 2012, 4:143-159.
44. Yanaihara N., Caplen N., Bowman E., Seike M., Kumamoto K., Yi M., Stephens R.M., Okamoto A., Yokota J., Tanaka T., Calin G.A., Liu C.G., Croce C.M., Harris C.C. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 2006, 9:189-198.
45. Rao X., Di Leva G., Li M., Fang F., Devlin C., Hartman-Frey C., Burow M.E., Ivan M., Croce C.M., Nephew K.P. MicroRNA-221/222 confers breast cancer fulvestrant resistance by regulating multiple signaling pathways. Oncogene 2011, 30:1082-1097.
46. Miller T.E., Ghoshal K., Ramaswamy B., Roy S., Datta J., Shapiro C.L., Jacob S., Majumder S. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J. Biol. Chem. 2008, 283:29897-29903.
47. Iorio M.V., Casalini P., Piovan C., Di Leva G., Merlo A., Triulzi T., Menard S., Croce C.M., Tagliabue E. microRNA-205 regulates HER3 in human breast cancer. Cancer Res. 2009, 69:2195-2200.
48. Bader A.G., Brown D., Stoudemire J., Lammers P. Developing therapeutic microRNAs for cancer. Gene Ther. 2011, 18:1121-1126.
49. Han M., Liu M., Wang Y., Chen X., Xu J., Sun Y., Zhao L., Qu H., Fan Y., Wu C. Antagonism of miR-21 reverses epithelial-mesenchymal transition and cancer stem cell phenotype through AKT/ERK1/2 inactivation by targeting PTEN. PLoS One 2012, 7:e39520.
50. Liu L.Z., Li C., Chen Q., Jing Y., Carpenter R., Jiang Y., Kung H.F., Lai L., Jiang B.H. MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1alpha expression. PLoS One 2011, 6:e19139.
51. Wong M.Y., Yu Y., Walsh W.R., Yang J.L. microRNA-34 family and treatment of cancers with mutant or wild-type p53. Int. J. Oncol. 2011, 38:1189-1195. (Review).
52. Jansson M.D., Lund A.H. MicroRNA and cancer. Mol. Oncol. 2012, 6:590-610.
53. Wang H., Chiu M., Xie Z., Chiu M., Liu Z., Chen P., Liu S., Byrd J.C., Muthusamy N., Garzon R., Croce C.M., Marcucci G., Chan K.K. Synthetic microRNA cassette dosing: pharmacokinetics, tissue distribution and bioactivity. Mol. Pharm. 2012, 9:1638-1644.
54. Weiler J., Hunziker J., Hall J. Anti-miRNA oligonucleotides (AMOs): ammunition to target miRNAs implicated in human disease?. Gene Ther. 2006, 13:496-502.
55. Montgomery R.L., Hullinger T.G., Semus H.M., Dickinson B.A., Seto A.G., Lynch J.M., Stack C., Latimer P.A., Olson E.N., van Rooij E. Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation 2011, 124:1537-1547.
56. van Rooij E., Purcell A.L., Levin A.A. Developing microRNA therapeutics. Circ. Res. 2012, 110:496-507.
57. 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.
58. Pereira D.M., Rodrigues P.M., Borralho P.M., Rodrigues C.M. Delivering the promise of miRNA cancer therapeutics. Drug Discov. Today 2013, 18:282-289.
59. Gondi C.S., Rao J.S. Concepts in in vivo siRNA delivery for cancer therapy. J. Cell. Physiol. 2009, 220:285-291.
60. Petrocca F., Lieberman J. Promise and challenge of RNA interference-based therapy for cancer. J. Clin. Oncol. 2011, 29:747-754.
61. Stylianopoulos T., Jain R.K. Combining two strategies to improve perfusion and drug delivery in solid tumors. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:18632-18637.
62. Li C., Li L., Keates A.C. Targeting cancer gene therapy with magnetic nanoparticles. Oncotarget 2012, 3:365-370.
63. Phillips P. Pancreatic stellate cells and fibrosis. Pancreatic Cancer and Tumor Microenvironment, Trivandrum (India) 2012, P.J. Grippo, H.G. Munshi (Eds.).
64. Kleger A., Perkhofer L., Seufferlein T. Smarter drugs emerging in pancreatic cancer therapy. Ann. Oncol. 2014, 10.1093/annonc/mdu013.
65. Castelli D.D., Terreno E., Cabella C., Chaabane L., Lanzardo S., Tei L., Visigalli M., Aime S. Evidence for in vivo macrophage mediated tumor uptake of paramagnetic/fluorescent liposomes. NMR Biomed. 2009, 22:1084-1092.
66. Caffo M., Barresi V., Caruso G., Cutugno M., La Fata G., Venza M., Alafaci C., Tomasello F. Innovative therapeutic strategies in the treatment of brain metastases. Int. J. Mol. Sci. 2013, 14:2135-2174.
67. Raemdonck K., Vandenbroucke R.E., Demeester J., Sanders N.N., De Smedt S.C. Maintaining the silence: reflections on long-term RNAi. Drug Discov. Today 2008, 13:917-931.
68. Yu B., Zhao X., Lee L.J., Lee R.J. Targeted delivery systems for oligonucleotide therapeutics. AAPS J. 2009, 11:195-203.
69. Garzon R., Marcucci G., Croce C.M. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat. Rev. Drug Discov. 2010, 9:775-789.
70. Kabilova T.O., Meschaninova M.I., Venyaminova A.G., Nikolin V.P., Zenkova M.A., Vlassov V.V., Chernolovskaya E.L. Short double-stranded RNA with immunostimulatory activity: sequence dependence. Nucleic Acid Ther. 2012, 22:196-204.
71. Judge A.D., Sood V., Shaw J.R., Fang D., McClintock K., MacLachlan I. Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 2005, 23:457-462.
72. Villanueva A.I., Kulkarni R.R., Sharif S. Synthetic double-stranded RNA oligonucleotides are immunostimulatory for chicken spleen cells. Dev. Comp. Immunol. 2011, 35:28-34.
73. Benwell R.K., Hruska J.E., Fritsche K.L., Lee D.R. Double stranded RNA- relative to other TLR ligand-activated dendritic cells induce extremely polarized human Th1 responses. Cell. Immunol. 2010, 264:119-126.
74. Fabbri M., Paone A., Calore F., Galli R., Gaudio E., Santhanam R., Lovat F., Fadda P., Mao C., Nuovo G.J., Zanesi N., Crawford M., Ozer G.H., Wernicke D., Alder H., Caligiuri M.A., Nana-Sinkam P., Perrotti D., Croce C.M. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E2110-E2116.
75. Chen X., Liang H., Zhang J., Zen K., Zhang C.Y. microRNAs are ligands of Toll-like receptors. RNA 2013, 19:737-739.
76. Fabbri M., Paone A., Calore F., Galli R., Croce C.M. A new role for microRNAs, as ligands of Toll-like receptors. RNA Biol. 2013, 10:169-174.
77. Ceppi M., Pereira P.M., Dunand-Sauthier I., Barras E., Reith W., Santos M.A., Pierre P. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2735-2740.
78. Lu F., Weidmer A., Liu C.G., Volinia S., Croce C.M., Lieberman P.M. Epstein-Barr virus-induced miR-155 attenuates NF-kappaB signaling and stabilizes latent virus persistence. J. Virol. 2008, 82:10436-10443.
79. Lehmann S.M., Kruger C., Park B., Derkow K., Rosenberger K., Baumgart J., Trimbuch T., Eom G., Hinz M., Kaul D., Habbel P., Kalin R., Franzoni E., Rybak A., Nguyen D., Veh R., Ninnemann O., Peters O., Nitsch R., Heppner F.L., Golenbock D., Schott E., Ploegh H.L., Wulczyn F.G., Lehnardt S. An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat. Neurosci. 2012, 15:827-835.
80. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H., Bauer S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
81. van Dongen S., Abreu-Goodger C., Enright A.J. Detecting microRNA binding and siRNA off-target effects from expression data. Nat. Methods 2008, 5:1023-1025.
82. Ho J.J., Metcalf J.L., Yan M.S., Turgeon P.J., Wang J.J., Chalsev M., Petruzziello-Pellegrini T.N., Tsui A.K., He J.Z., Dhamko H., Man H.S., Robb G.B., Teh B.T., Ohh M., Marsden P.A. Functional importance of Dicer protein in the adaptive cellular response to hypoxia. J. Biol. Chem. 2012, 287:29003-29020.
83. Sarkar S., Horn G., Moulton K., Oza A., Byler S., Kokolus S., Longacre M. Cancer development, progression, and therapy: an epigenetic overview. Int. J. Mol. Sci. 2013, 14:21087-21113.
84. Di Leva G., Croce C.M. The role of microRNAs in the tumorigenesis of ovarian cancer. Front. Oncol. 2013, 3:153.
85. Rao D.D., Vorhies J.S., Senzer N., Nemunaitis J. siRNA vs. shRNA: similarities and differences. Adv. Drug Deliv. Rev. 2009, 61:746-759.
86. Formstecher E., Reverdy C., Cholay M., Planquette C., Trouplin V., Lehrmann H., Aresta S., Calabrese A., Arar K., Daviet L., Colland F. Combination of active and inactive siRNA targeting the mitotic kinesin Eg5 impairs silencing efficiency in several cancer cell lines. Oligonucleotides 2006, 16:387-394.
87. Loinger A., Shemla Y., Simon I., Margalit H., Biham O. Competition between small RNAs: a quantitative view. Biophys. J. 2012, 102:1712-1721.
88. Vicentini F.T., Borgheti-Cardoso L.N., Depieri L.V., de Macedo Mano D., Abelha T.F., Petrilli R., Bentley M.V. Delivery systems and local administration routes for therapeutic siRNA. Pharm. Res. 2013, 30:915-931.
89. Xie J., Xie Q., Zhang H., Ameres S.L., Hung J.H., Su Q., He R., Mu X., Seher Ahmed S., Park S., Kato H., Li C., Mueller C., Mello C.C., Weng Z., Flotte T.R., Zamore P.D., Gao G. MicroRNA-regulated, systemically delivered rAAV9: a step closer to CNS-restricted transgene expression. Mol. Ther. 2011, 19:526-535.
90. Moller H.G., Rasmussen A.P., Andersen H.H., Johnsen K.B., Henriksen M., Duroux M. A systematic review of microRNA in glioblastoma multiforme: micro-modulators in the mesenchymal mode of migration and invasion. Mol. Neurobiol. 2013, 47:131-144.
91. Schneider M.R. MicroRNAs as novel players in skin development, homeostasis and disease. Br. J. Dermatol. 2012, 166:22-28.
92. Inoue T., Sugimoto M., Sakurai T., Saito R., Futaki N., Hashimoto Y., Honma Y., Arai I., Nakaike S. Modulation of scratching behavior by silencing an endogenous cyclooxygenase-1 gene in the skin through the administration of siRNA. J. Gene Med. 2007, 9:994-1001.
93. Zheng D., Giljohann D.A., Chen D.L., Massich M.D., Wang X.Q., Iordanov H., Mirkin C.A., Paller A.S. Topical delivery of siRNA-based spherical nucleic acid nanoparticle conjugates for gene regulation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:11975-11980.
94. He X.X., Chang Y., Meng F.Y., Wang M.Y., Xie Q.H., Tang F., Li P.Y., Song Y.H., Lin J.S. MicroRNA-375 targets AEG-1 in hepatocellular carcinoma and suppresses liver cancer cell growth in vitro and in vivo. Oncogene 2012, 31:3357-3369.
95. 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.
96. 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.
97. Sureban S.M., May R., Mondalek F.G., Qu D., Ponnurangam S., Pantazis P., Anant S., Ramanujam R.P., Houchen C.W. Nanoparticle-based delivery of siDCAMKL-1 increases microRNA-144 and inhibits colorectal cancer tumor growth via a Notch-1 dependent mechanism. J. Nanobiotechnol. 2011, 9:40.
98. Lennox K.A., Behlke M.A. Chemical modification and design of anti-miRNA oligonucleotides. Gene Ther. 2011, 18:1111-1120.
99. Prabhakar U., Maeda H., Jain R.K., Sevick-Muraca E.M., Zamboni W., Farokhzad O.C., Barry S.T., Gabizon A., Grodzinski P., Blakey D.C. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res. 2013, 73:2412-2417.
100. Maeda H., Wu J., Sawa T., Matsumura Y., Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J. Control. Release 2000, 65:271-284.
101. 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.
102. 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.
103. Davis S., Lollo B., Freier S., Esau C. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res. 2006, 34:2294-2304.
104. Krutzfeldt J., Rajewsky N., Braich R., Rajeev K.G., Tuschl T., Manoharan M., Stoffel M. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005, 438:685-689.
105. Elmen J., Lindow M., Silahtaroglu A., Bak M., Christensen M., Lind-Thomsen A., Hedtjarn M., Hansen J.B., Hansen H.F., Straarup E.M., McCullagh K., Kearney P., Kauppinen S. Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res. 2008, 36:1153-1162.
106. 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.
107. Peacock H., Fucini R.V., Jayalath P., Ibarra-Soza J.M., Haringsma H.J., Flanagan W.M., Willingham A., Beal P.A. Nucleobase and ribose modifications control immunostimulation by a microRNA-122-mimetic RNA. J. Am. Chem. Soc. 2011, 133:9200-9203.
108. Henry J.C., Azevedo-Pouly A.C., Schmittgen T.D. MicroRNA replacement therapy for cancer. Pharm. Res. 2011, 28:3030-3042.
109. Akao Y., Nakagawa Y., Hirata I., Iio A., Itoh T., Kojima K., Nakashima R., Kitade Y., Naoe T. Role of anti-oncomirs miR-143 and -145 in human colorectal tumors. Cancer Gene Ther. 2010, 17:398-408.
110. Kasar S., Salerno E., Yuan Y., Underbayev C., Vollenweider D., Laurindo M.F., Fernandes H., Bonci D., Addario A., Mazzella F., Raveche E. Systemic in vivo lentiviral delivery of miR-15a/16 reduces malignancy in the NZB de novo mouse model of chronic lymphocytic leukemia. Genes Immun. 2012, 13:109-119.
111. Liu Y., Lai L., Chen Q., Song Y., Xu S., Ma F., Wang X., Wang J., Yu H., Cao X., Wang Q. MicroRNA-494 is required for the accumulation and functions of tumor-expanded myeloid-derived suppressor cells via targeting of PTEN. J. Immunol. 2012, 188:5500-5510.
112. Kota J., Chivukula R.R., O'Donnell K.A., Wentzel E.A., Montgomery C.L., Hwang H.W., Chang T.C., Vivekanandan P., Torbenson M., Clark K.R., Mendell J.R., Mendell J.T. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009, 137:1005-1017.
113. Pegtel D.M., Cosmopoulos K., Thorley-Lawson D.A., van Eijndhoven M.A., Hopmans E.S., Lindenberg J.L., de Gruijl T.D., Wurdinger T., Middeldorp J.M. Functional delivery of viral miRNAs via exosomes. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6328-6333.
114. Zomer A., Vendrig T., Hopmans E.S., van Eijndhoven M., Middeldorp J.M., Pegtel D.M. Exosomes: fit to deliver small RNA. Commun. Integr. Biol. 2010, 3:447-450.
115. Koppers-Lalic D., Hogenboom M.M., Middeldorp J.M., Pegtel D.M. Virus-modified exosomes for targeted RNA delivery; a new approach in nanomedicine. Adv. Drug Deliv. Rev. 2013, 65:348-356.
116. Gardner M.B., Henderson B.E., Officer J.E., Rongey R.W., Parker J.C., Oliver C., Estes J.D., Huebner R.J. A spontaneous lower motor neuron disease apparently caused by indigenous type-C RNA virus in wild mice. J. Natl. Cancer Inst. 1973, 51:1243-1254.
117. Anson D.S. The use of retroviral vectors for gene therapy-what are the risks? A review of retroviral pathogenesis and its relevance to retroviral vector-mediated gene delivery. Genet. Vaccines Ther. 2004, 2:9.
118. Selten G., Cuypers H.T., Berns A. Proviral activation of the putative oncogene Pim-1 in MuLV induced T-cell lymphomas. EMBO J. 1985, 4:1793-1798.
119. 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.
120. Panyam J., Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev. 2007, 59(8):718-728.
121. Kulkarni R., Moore E., Hegyeli A., Leonard F. Biodegradable poly (lactic acid) polymers. J. Biomed. Mater. Res. 1971, 5:169-181.
122. Panyam J., Zhou W.-Z., Prabha S., Sahoo S.K., Labhasetwar V. Rapid endo-lysosomal escape of poly (DL-lactide-co-glycolide) nanoparticles: implications for drug and gene delivery. FASEB J. 2002, 16:1217-1226.
123. Vasir J.K., Labhasetwar V. Biodegradable nanoparticles for cytosolic delivery of therapeutics. Adv. Drug Deliv. Rev. 2007, 59:718-728.
124. van Vlerken L.E., Vyas T.K., Amiji M.M. Poly (ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery. Pharm. Res. 2007, 24:1405-1414.
125. Paulmurugan R., Sekar N.M., Sekar T.V. Biodegradable polymer nanocarriers for therapeutic antisense microRNA delivery in living animals. SPIE BiOS 2012, 823208-823213. International Society for Optics and Photonics.
126. Babar I.A., Cheng C.J., Booth C.J., Liang X., 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. 2012, 109:E1695-E1704.
127. Boussif O., Lezoualc'h 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. 1995, 92:7297-7301.
128. Park T.G., Jeong J.H., Kim S.W. Current status of polymeric gene delivery systems. Adv. Drug Deliv. Rev. 2006, 58:467-486.
129. Akinc A., Thomas M., Klibanov A.M., Langer R. Exploring polyethylenimine mediated DNA transfection and the proton sponge hypothesis. J. Gene Med. 2005, 7:657-663.
130. 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. 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.
131. Jones C.H., Chen C.-K., Ravikrishnan A., Rane S., Pfeifer B.A. Overcoming nonviral gene delivery barriers: perspective and future. Mol. Pharm. 2013, 10(11):4082-4098.
132. Hsu S.H., Yu B., Wang X., Lu Y., Schmidt C.R., Lee R.J., Lee L.J., Jacob S.T., Ghoshal K. Cationic lipid nanoparticles for therapeutic delivery of siRNA and miRNA to murine liver tumor. Nanomedicine 2013, 9:1169-1180.
133. 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.
134. 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.
135. Shi S., Han L., Gong T., Zhang Z., Sun X. Systemic delivery of microRNA-34a for cancer stem cell therapy. Angew. Chem. Int. Ed. Engl. 2013, 52:3901-3905.
136. 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.
137. 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.
138. Liu X., Chen Y., Li H., Huang N., Jin Q., Ren K., Ji J. Enhanced retention and cellular uptake of nanoparticles in tumors by controlling their aggregation behavior. ACS Nano 2013, 7:6244-6257.
139. Shenoy D., Little S., Langer R., Amiji M. Poly(ethylene oxide)-modified poly(beta-amino ester) nanoparticles as a pH-sensitive system for tumor-targeted delivery of hydrophobic drugs. 1. In vitro evaluations. Mol. Pharm. 2005, 2:357-366.
140. Wong C., Stylianopoulos T., Cui J., Martin J., Chauhan V.P., Jiang W., Popovic Z., Jain R.K., Bawendi M.G., Fukumura D. Multistage nanoparticle delivery system for deep penetration into tumor tissue. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2426-2431.
141. Mitra A.K., Zillhardt M., Hua Y., Tiwari P., Murmann A.E., Peter M.E., Lengyel E. MicroRNAs reprogram normal fibroblasts into cancer-associated fibroblasts in ovarian cancer. Cancer Discov. 2012, 2:1100-1108.
142. Aprelikova O., Green J.E. MicroRNA regulation in cancer-associated fibroblasts. Cancer Immunol. Immunother. 2012, 61:231-237.
143. Chou J., Werb Z. MicroRNAs play a big role in regulating ovarian cancer-associated fibroblasts and the tumor microenvironment. Cancer Discov. 2012, 2:1078-1080.
144. Neesse A., Frese K.K., Chan D.S., Bapiro T.E., Howat W.J., Richards F.M., Ellenrieder V., Jodrell D.I., Tuveson D.A. SPARC independent drug delivery and antitumour effects of nab-paclitaxel in genetically engineered mice. Gut 2014, 63(6):974-983.
145. Kotowski A., Ma W.W. Emerging therapies in pancreas cancer. J. Gastrointest. Oncol. 2011, 2:93-103.
146. Neuzillet C., Tijeras-Raballand A., Cros J., Faivre S., Hammel P., Raymond E. Stromal expression of SPARC in pancreatic adenocarcinoma. Cancer Metastasis Rev. 2013, 32:585-602.
147. Zhang J., Miao L., Guo S., Zhang Y., Zhang L., Satterlee A., Kim W.Y., Huang L. Synergistic anti-tumor effects of combined gemcitabine and cisplatin nanoparticles in a stroma-rich bladder carcinoma model. J. Control. Release 2014, 182:90-96.
148. Auffinger B., Thaci B., Nigam P., Rincon E., Cheng Y., Lesniak M.S. New therapeutic approaches for malignant glioma: in search of the Rosetta stone. F1000 Med. Rep. 2012, 4:18.
149. Forbes G.M., Sturm M.J., Leong R.W., Sparrow M.P., Segarajasingam D., Cummins A.G., Phillips M., Herrmann R.P. A phase 2 study of allogeneic mesenchymal stromal cells for luminal Crohn's disease refractory to biologic therapy. Clin. Gastroenterol. Hepatol. 2014, 12:64-71.
150. Rameshwar P. Casting doubt on the safety of "off-the-shelf" mesenchymal stem cells for cell therapy. Mol. Ther. 2009, 17:216-218.
151. Greco S.J., Rameshwar P. Mesenchymal stem cells in drug/gene delivery: implications for cell therapy. Ther. Deliv. 2012, 3:997-1004.
152. Matuskova M., Hlubinova K., Pastorakova A., Hunakova L., Altanerova V., Altaner C., Kucerova L. HSV-tk expressing mesenchymal stem cells exert bystander effect on human glioblastoma cells. Cancer Lett. 2010, 290:58-67.
153. Munoz J.L., Bliss S.A., Greco S.J., Ramkissoon S.H., Ligon K.L., Rameshwar P. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol. Ther. Nucleic Acids 2013, 2:e126.