Ultrasound-guided delivery of microRNA loaded nanoparticles into cancer

Journal of Controlled Release

Volumn 203, Issue , 2015, Pages 99-108

  Wang, Tzu Yin ^a   Choe, Jung Woo ^b   Pu, Kanyi ^a   Devulapally, Rammohan ^a   Bachawal, Sunitha ^a   Machtaler, Steven ^a   Chowdhury, Sayan Mullick ^a   Luong, Richard ^c   Tian, Lu ^c   Khuri Yakub, Butrus ^b   Rao, Jianghong ^a   Paulmurugan, Ramasamy ^a   Willmann, Jürgen K ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Stanford University   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Cancer; Drug delivery; Image guidance; Nanocarriers; Therapy; Ultrasound

Indexed keywords

BIOLOGICAL MATERIALS; CARDIOVASCULAR SYSTEM; CAVITATION; CELL MEMBRANES; COPOLYMERS; DISEASES; DRUG DELIVERY; DRUG THERAPY; ELASTIC WAVES; HIGH PRESSURE EFFECTS; MOBILE SECURITY; NANOPARTICLES; RNA; TISSUE; TUMORS;

CANCER; ENHANCED PERMEABILITY; IMAGE GUIDANCES; NANO-CARRIERS; POLY LACTIC-CO-GLYCOLIC ACID; PULSE REPETITION FREQUENCIES; THERAPY; TISSUE MIMICKING PHANTOM;

ULTRASONICS;

MICRORNA 122; NANOCARRIER; POLYGLACTIN; SEMICONDUCTING POLYMER NANOPARTICLE; UNCLASSIFIED DRUG; LACTIC ACID; MACROGOL DERIVATIVE; MICRORNA; MIRN122 MICRORNA, HUMAN; NANOPARTICLE; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER;

ACOUSTICS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER TISSUE; COLON CANCER; CONCENTRATION RESPONSE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG PENETRATION; ECHOGRAPHY; EXPERIMENTAL NEOPLASM; HUMAN; HUMAN CELL; IMAGING PHANTOM; IN VIVO STUDY; MICROBUBBLE; MOUSE; NANOENCAPSULATION; NANOPHARMACEUTICS; NONHUMAN; PRESSURE; PRIORITY JOURNAL; PULSE LENGTH; PULSE REPETITION FREQUENCY; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; THREE DIMENSIONAL IMAGING; TISSUE INJURY; TUMOR XENOGRAFT; ULTRASOUND TRANSDUCER; ANIMAL; CHEMISTRY; COLON; COLONIC NEOPLASMS; DEVICES; EQUIPMENT DESIGN; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE; ULTRASOUND;

ANIMALS; CELL LINE, TUMOR; COLON; COLONIC NEOPLASMS; DRUG DELIVERY SYSTEMS; EQUIPMENT DESIGN; HUMANS; LACTIC ACID; MICE; MICE, NUDE; MICROBUBBLES; MICRORNAS; NANOPARTICLES; POLYETHYLENE GLYCOLS; POLYGLYCOLIC ACID; SONICATION; ULTRASONICS;

EID: 84923284952     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.02.018     Document Type: Article

References (46)

1. S. Ganta, H. Devalapally, A. Shahiwala, and M. Amiji A review of stimuli-responsive nanocarriers for drug and gene delivery J. Control. Release 126 2008 187 204
2. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review J. Control. Release 65 2000 271 284
3. Y.H. Bae, and K. Park Targeted drug delivery to tumors: myths, reality and possibility J. Control. Release 153 2011 198 205
4. U. Prabhakar, H. Maeda, R.K. Jain, E.M. Sevick-Muraca, W. Zamboni, O.C. Farokhzad, S.T. Barry, A. Gabizon, P. Grodzinski, and D.C. Blakey Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology Cancer Res. 73 2013 2412 2417
5. F. Yuan, H.A. Salehi, Y. Boucher, U.S. Vasthare, R.F. Tuma, and R.K. Jain Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows Cancer Res. 54 1994 4564 4568
6. K.J. Harrington, S. Mohammadtaghi, P.S. Uster, D. Glass, A.M. Peters, R.G. Vile, and J.S. Stewart Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes Clin. Cancer Res. 7 2001 243 254
7. W.L. Nyborg Ultrasonic microstreaming and related phenomena Br. J. Cancer Suppl. 5 1982 156 160
8. M. Postema, S. Kotopoulis, A. Delalande, and O.H. Gilja Invited editorial - Sonoporation: why microbubbles create pores Ultraschall Med. 33 2012 97 98
9. N. Hosseinkhah, H. Chen, T.J. Matula, P.N. Burns, and K. Hynynen Mechanisms of microbubble-vessel interactions and induced stresses: a numerical study J. Acoust. Soc. Am. 134 2013 1875 1885
10. J. Collis, R. Manasseh, P. Liovic, P. Tho, A. Ooi, K. Petkovic-Duran, and Y. Zhu Cavitation microstreaming and stress fields created by microbubbles Ultrasonics 50 2010 273 279
11. P. Marmottant, and S. Hilgenfeldt Controlled vesicle deformation and lysis by single oscillating bubbles Nature 423 2003 153 156
12. P. Prentice, A. Cuschieri, K. Dholakia, M. Prausnitz, and P. Campbell Membrane disruption by optically controlled microbubble cavitation Nat. Phys. 1 2005 107 110
13. L.H. Treat, N. McDannold, Y. Zhang, N. Vykhodtseva, and K. Hynynen Improved anti-tumor effect of liposomal doxorubicin after targeted blood-brain barrier disruption by MRI-guided focused ultrasound in rat glioma Ultrasound Med. Biol. 38 2012 1716 1725
14. Z.K. Liao, K.C. Tsai, H.T. Wang, S.H. Tseng, W.P. Deng, W.S. Chen, and L.H. Hwang Sonoporation-mediated anti-angiogenic gene transfer into muscle effectively regresses distant orthotopic tumors Cancer Gene Ther. 19 2011 171 180
15. S. Kotopoulis, A. Delalande, M. Popa, V. Mamaeva, G. Dimcevski, O.H. Gilja, M. Postema, B.T. Gjertsen, and E. McCormack Sonoporation-enhanced chemotherapy significantly reduces primary tumour burden in an orthotopic pancreatic cancer xenograft Mol. Imaging Biol. 16 2013 53 62
16. F. Yan, L. Li, Z. Deng, Q. Jin, J. Chen, W. Yang, C.K. Yeh, J. Wu, R. Shandas, X. Liu, and H. Zheng Paclitaxel-liposome-microbubble complexes as ultrasound-triggered therapeutic drug delivery carriers J. Control. Release 166 2013 246 255
17. N.Y. Rapoport, A.M. Kennedy, J.E. Shea, C.L. Scaife, and K.H. Nam Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles J. Control. Release 138 2009 268 276
18. S. Kotopoulis, G. Dimcevski, O.H. Gilja, D. Hoem, and M. Postema Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study Med. Phys. 40 2013 072902
19. M. Aryal, C.D. Arvanitis, P.M. Alexander, and N. McDannold Ultrasound-mediated blood-brain barrier disruption for targeted drug delivery in the central nervous system Adv. Drug Deliv. Rev. 72 2014 94 109
20. H. Chen, and E.E. Konofagou The size of blood-brain barrier opening induced by focused ultrasound is dictated by the acoustic pressure J. Cereb. Blood Flow Metab. 34 2014 1197 1204
21. A. Bao, B. Goins, R. Klipper, G. Negrete, and W.T. Phillips Direct 99mTc labeling of pegylated liposomal doxorubicin (Doxil) for pharmacokinetic and non-invasive imaging studies J. Pharmacol. Exp. Ther. 308 2004 419 425
22. R. Gluck, and E. Walti Biophysical validation of Epaxal Berna, a hepatitis A vaccine adjuvanted with immunopotentiating reconstituted influenza virosomes (IRIV) Dev. Biol. (Basel) 103 2000 189 197
23. A. Fahr, P. van Hoogevest, S. May, N. Bergstrand, and M.L.S. Leigh Transfer of lipophilic drugs between liposomal membranes and biological interfaces: consequences for drug delivery Eur. J. Pharm. Sci. 26 2005 251 265
24. R. Garzon, G.A. Calin, and C.M. Croce MicroRNAs in cancer Annu. Rev. Med. 60 2009 167 179
25. Y. Saito, H. Suzuki, M. Matsuura, A. Sato, Y. Kasai, K. Yamada, H. Saito, and T. Hibi MicroRNAs in hepatobiliary and pancreatic cancers Front. Genet. 2 2011 66
26. L. Ma, J. Liu, J. Shen, L. Liu, J. Wu, W. Li, J. Luo, Q. Chen, and C. Qian Expression of miR-122 mediated by adenoviral vector induces apoptosis and cell cycle arrest of cancer cells Cancer Biol. Ther. 9 2010 554 561
27. W.C. Tsai, P.W. Hsu, T.C. Lai, G.Y. Chau, C.W. Lin, C.M. Chen, C.D. Lin, Y.L. Liao, J.L. Wang, Y.P. Chau, M.T. Hsu, M. Hsiao, H.D. Huang, and A.P. Tsou MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma Hepatology 49 2009 1571 1582
28. J. He, G. Xie, J. Tong, Y. Peng, H. Huang, J. Li, N. Wang, and H. Liang Overexpression of microRNA-122 re-sensitizes 5-FU-resistant colon cancer cells to 5-FU through the inhibition of PKM2 in vitro and in vivo Cell Biochem. Biophys. 70 2014 1343 1350
29. S. Bai, M.W. Nasser, B. Wang, S.H. Hsu, J. Datta, H. Kutay, A. Yadav, G. Nuovo, P. Kumar, and K. Ghoshal MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib J. Biol. Chem. 284 2009 32015 32027
30. C. Wu, and D.T. Chiu Highly fluorescent semiconducting polymer dots for biology and medicine Angew. Chem. Int. Ed. Engl. 52 2013 3086 3109
31. K. Pu, A.J. Shuhendler, M.P. Valta, L. Cui, M. Saar, D.M. Peehl, and J. Rao Phosphorylcholine-coated semiconducting polymer nanoparticles as rapid and efficient labeling agents for in vivo cell tracking Adv. Healthc. Mater. 3 2014 1292 1298
32. R. Devulapally, and R. Paulmurugan Polymer nanoparticles for drug and small silencing RNA delivery to treat cancers of different phenotypes Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 6 2013 40 60
33. B. Wang, H. Wang, and Z. Yang MiR-122 inhibits cell proliferation and tumorigenesis of breast cancer by targeting IGF1R PLoS One 7 2012 e47053
34. M. Schneider, B. Anantharam, M. Arditi, D. Bokor, A. Broillet, P. Bussat, X. Fouillet, P. Frinking, I. Tardy, J. Terrettaz, R. Senior, and F. Tranquart BR38, a new ultrasound blood pool agent Investig. Radiol. 46 2011 486 494
35. R. Bekeredjian, S. Chen, P.A. Frenkel, P.A. Grayburn, and R.V. Shohet Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart Circulation 108 2003 1022 1026
36. A.C. Riches, J.G. Sharp, D.B. Thomas, and S.V. Smith Blood volume determination in the mouse J. Physiol. 228 1973 279 284
37. C.M. Panje, D.S. Wang, M.A. Pysz, R. Paulmurugan, Y. Ren, F. Tranquart, L. Tian, and J.K. Willmann Ultrasound-mediated gene delivery with cationic versus neutral microbubbles: effect of DNA and microbubble dose on in vivo transfection efficiency Theranostics 2 2012 1078 1091
38. A. Needles, M. Arditi, N.G. Rognin, J. Mehi, T. Coulthard, C. Bilan-Tracey, E. Gaud, P. Frinking, D. Hirson, and F.S. Foster Nonlinear contrast imaging with an array-based micro-ultrasound system Ultrasound Med. Biol. 36 2010 2097 2106
39. S. Eggen, M. Afadzi, E.A. Nilssen, S.B. Haugstad, B. Angelsen, and L. Davies Cde Ultrasound improves the uptake and distribution of liposomal Doxorubicin in prostate cancer xenografts Ultrasound Med. Biol. 39 2013 1255 1266
40. R.D. Lillie Histopathologic Technic and Practical Histochemistry 1954 The Blackiston Company, Inc. New York
41. H. Cabral, Y. Matsumoto, K. Mizuno, Q. Chen, M. Murakami, M. Kimura, Y. Terada, M.R. Kano, K. Miyazono, M. Uesaka, N. Nishiyama, and K. Kataoka Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size Nat. Nanotechnol. 6 2011 815 823
42. A. Xie, T. Belcik, Y. Qi, T.K. Morgan, S.A. Champaneri, S. Taylor, B.P. Davidson, Y. Zhao, A.L. Klibanov, M.A. Kuliszewski, H. Leong-Poi, A. Ammi, and J.R. Lindner Ultrasound-mediated vascular gene transfection by cavitation of endothelial-targeted cationic microbubbles JACC Cardiovasc Imaging 5 2012 1253 1262
43. J.H. Hwang, A.A. Brayman, M.A. Reidy, T.J. Matula, M.B. Kimmey, and L.A. Crum Vascular effects induced by combined 1-MHz ultrasound and microbubble contrast agent treatments in vivo Ultrasound Med. Biol. 31 2005 553 564
44. J. Holash, P.C. Maisonpierre, D. Compton, P. Boland, C.R. Alexander, D. Zagzag, G.D. Yancopoulos, and S.J. Wiegand Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF Science 284 1999 1994 1998
45. L.A. Frizzell Threshold dosages for damage to mammalian liver by high intensity focused ultrasound IEEE Trans. Ultrason. Ferroelectr. Freq. Control 35 1988 578 581
46. M.A. Borden, D.E. Kruse, C.F. Caskey, S. Zhao, P.A. Dayton, and K.W. Ferrara Influence of lipid shell physicochemical properties on ultrasound-induced microbubble destruction IEEE Trans. Ultrason. Ferroelectr. Freq. Control 52 2005 1992 2002