Oncogene Knockdown via Active Loading of Small RNAs into Extracellular Vesicles by Sonication

Cellular and Molecular Bioengineering

Volumn 9, Issue 3, 2016, Pages 315-324

  Lamichhane, Tek N ^a   Jeyaram, Anjana ^a   Patel, Divya B ^a   Parajuli, Babita ^a   Livingston, Natalie K ^a   Arumugasaamy, Navein ^a   Schardt, John S ^a   Jay, Steven M ^a,b,c  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Biopharmaceutical; Biotherapeutic; Cancer nanoparticle; Exosomes; HER2; microRNA; Nanobiotechnology; siRNA delivery

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; MESSENGER RNA; MICRORNA; RNA; SINGLE STRANDED DNA; SMALL INTERFERING RNA; SMALL RNA; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CELL TRANSPORT; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; EXOSOME; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ULTRASOUND;

EID: 84978054068     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-016-0457-4     Document Type: Article

References (36)

1. Alvarez-Erviti, L., Y. Seow, H. Yin, C. Betts, S. Lakhal, and M. J. Wood. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 29:341–345, 2011.
2. Andaloussi, E. L., I. Mager, X. O. Breakefield, and M. J. Wood. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat. Rev. Drug Discov. 12:347–357, 2013.
3. Arteaga, C. L., M. X. Sliwkowski, C. K. Osborne, E. A. Perez, F. Puglisi, and L. Gianni. Treatment of HER2-positive breast cancer: current status and future perspectives. Nat. Rev. Clin. Oncol. 9:16–32, 2012.
4. Baselga, J., and S. M. Swain. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat. Rev. Cancer. 9:463–475, 2009.
5. Blenkiron, C., and E. A. Miska. miRNAs in cancer: approaches, aetiology, diagnostics and therapy. Hum. Mol. Genet. 16(Spec No 1):R106–R113, 2007.
6. Bumcrot, D., M. Manoharan, V. Koteliansky, and D. W. Sah. RNAi therapeutics: a potential new class of pharmaceutical drugs. Nat. Chem. Biol. 2:711–719, 2006.
7. Choudhury, A., J. Charo, S. K. Parapuram, R. C. Hunt, D. M. Hunt, B. Seliger, and R. Kiessling. Small interfering RNA (siRNA) inhibits the expression of the Her2/neu gene, upregulates HLA class I and induces apoptosis of Her2/neu positive tumor cell lines. Int. J. Cancer. 108:71–77, 2004.
8. Coelho, T., D. Adams, A. Silva, P. Lozeron, P. N. Hawkins, T. Mant, J. Perez, J. Chiesa, S. Warrington, E. Tranter, M. Munisamy, R. Falzone, J. Harrop, J. Cehelsky, B. R. Bettencourt, M. Geissler, J. S. Butler, A. Sehgal, R. E. Meyers, Q. Chen, T. Borland, R. M. Hutabarat, V. A. Clausen, R. Alvarez, K. Fitzgerald, C. Gamba-Vitalo, S. V. Nochur, A. K. Vaishnaw, D. W. Sah, J. A. Gollob, and O. B. Suhr. Safety and efficacy of RNAi therapy for transthyretin amyloidosis. N. Engl. J. Med. 369:819–829, 2013.
9. Cooper, J. M., P. B. Wiklander, J. Z. Nordin, R. Al-Shawi, M. J. Wood, M. Vithlani, A. H. Schapira, J. P. Simons, S. El-Andaloussi, and L. Alvarez-Erviti. Systemic exosomal siRNA delivery reduced alpha-synuclein aggregates in brains of transgenic mice. Mov. Disord. 29:1476–1485, 2014.
10. De Jong, W. H., and P. J. Borm. Drug delivery and nanoparticles: applications and hazards. Int. J. Nanomed. 3:133–149, 2008.
11. El-Andaloussi, S., Y. Lee, S. Lakhal-Littleton, J. Li, Y. Seow, C. Gardiner, L. Alvarez-Erviti, I. L. Sargent, and M. J. Wood. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat. Protoc. 7:2112–2126, 2012.
12. Esmaeilzadeh-Gharehdaghi, E., A. Amani, M. R. Khoshayand, M. Banan, E. Esmaeilzadeh-Gharehdaghi, M. A. Amini, and M. A. Faramarzi. Chitosan nanoparticles for siRNA delivery: optimization of processing/formulation parameters. Nucleic Acid Ther. 24:420–427, 2014.
13. Faltus, T., J. Yuan, B. Zimmer, A. Kramer, S. Loibl, M. Kaufmann, and K. Strebhardt. Silencing of the HER2/neu gene by siRNA inhibits proliferation and induces apoptosis in HER2/neu-overexpressing breast cancer cells. Neoplasia 6:786–795, 2004.
14. Farooqi, A. A., Z. U. Rehman, and J. Muntane. Antisense therapeutics in oncology: current status. Onco Targets Ther. 7:2035–2042, 2014.
15. Gavrilov, K., and W. M. Saltzman. Therapeutic siRNA: principles, challenges, and strategies. Yale J. Biol. Med. 85:187–200, 2012.
16. Gyorgy, B., M. E. Hung, X. O. Breakefield, and J. N. Leonard. Therapeutic applications of extracellular vesicles: clinical promise and open questions. Annu. Rev. Pharmacol. Toxicol. 55:439–464, 2015.
17. Haney, M. J., N. L. Klyachko, Y. Zhao, R. Gupta, E. G. Plotnikova, Z. He, T. Patel, A. Piroyan, M. Sokolsky, A. V. Kabanov, and E. V. Batrakova. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J. Control Release 207:18–30, 2015.
18. Kim, M. S., M. J. Haney, Y. Zhao, V. Mahajan, I. Deygen, N. L. Klyachko, E. Inskoe, A. Piroyan, M. Sokolsky, O. Okolie, S. D. Hingtgen, A. V. Kabanov, and E. V. Batrakova. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine 12(3):655–664, 2016.
19. Kooijmans, S. A., S. Stremersch, K. Braeckmans, S. C. de Smedt, A. Hendrix, M. J. Wood, R. M. Schiffelers, K. Raemdonck, and P. Vader. Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles. J. Control Release 172:229–238, 2013.
20. Kundu, A. K., P. K. Chandra, S. Hazari, Y. V. Pramar, S. Dash, and T. K. Mandal. Development and optimization of nanosomal formulations for siRNA delivery to the liver. Eur. J. Pharm. Biopharm. 80:257–267, 2012.
21. Lamichhane, T. N., R. S. Raiker, and S. M. Jay. Exogenous DNA loading into extracellular vesicles via electroporation is size-dependent and enables limited gene delivery. Mol. Pharm. 12:3650–3657, 2015.
22. Lamichhane, T. N., S. Sokic, J. S. Schardt, R. S. Raiker, J. W. Lin, and S. M. Jay. Emerging roles for extracellular vesicles in tissue engineering and regenerative medicine. Tissue Eng. Part B Rev. 21:45–54, 2015.
23. McClorey, G., and M. J. Wood. An overview of the clinical application of antisense oligonucleotides for RNA-targeting therapies. Curr. Opin. Pharmacol. 24:52–58, 2015.
24. Moasser, M. M. The oncogene HER2: its signaling and transforming functions and its role in human cancer pathogenesis. Oncogene 26:6469–6487, 2007.
25. Munoz, J. L., S. A. Bliss, S. J. Greco, S. H. Ramkissoon, K. L. Ligon, and P. Rameshwar. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol. Ther. Nucleic Acids 2:e126, 2013.
26. Ohno, S., M. Takanashi, K. Sudo, S. Ueda, A. Ishikawa, N. Matsuyama, K. Fujita, T. Mizutani, T. Ohgi, T. Ochiya, N. Gotoh, and M. Kuroda. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol. Ther. 21:185–191, 2013.
27. Peer, D., and J. Lieberman. Special delivery: targeted therapy with small RNAs. Gene Ther. 18:1127–1133, 2011.
28. Smyth, T., M. Kullberg, N. Malik, P. Smith-Jones, M. W. Graner, and T. J. Anchordoquy. Biodistribution and delivery efficiency of unmodified tumor-derived exosomes. J. Control Release. 199:145–155, 2015.
29. Tan, W. B., S. Jiang, and Y. Zhang. Quantum-dot based nanoparticles for targeted silencing of HER2/neu gene via RNA interference. Biomaterials 28:1565–1571, 2007.
30. Thiel, K. W., L. I. Hernandez, J. P. Dassie, W. H. Thiel, X. Liu, K. R. Stockdale, A. M. Rothman, F. J. Hernandez, J. O. McNamara, 2nd, and P. H. Giangrande. Delivery of chemo-sensitizing siRNAs to HER2 + -breast cancer cells using RNA aptamers. Nucleic Acids Res. 40:6319–6337, 2012.
31. Valadi, H., K. Ekstrom, A. Bossios, M. Sjostrand, J. J. Lee, and J. O. Lotvall. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9:654–659, 2007.
32. Whitehead, K. A., R. Langer, and D. G. Anderson. Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 8:129–138, 2009.
33. Wichmann, H., A. Guttler, M. Bache, H. Taubert, S. Rot, J. Kessler, A. W. Eckert, M. Kappler, and D. Vordermark. Targeting of EGFR and HER2 with therapeutic antibodies and siRNA: a comparative study in glioblastoma cells. Strahlenther. Onkol. 191:180–191, 2015.
34. Wiklander, O. P., J. Z. Nordin, A. O’Loughlin, Y. Gustafsson, G. Corso, I. Mager, P. Vader, Y. Lee, H. Sork, Y. Seow, N. Heldring, L. Alvarez-Erviti, C. E. Smith, K. Le Blanc, P. Macchiarini, P. Jungebluth, M. J. Wood, and S. E. Andaloussi. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J. Extracell. Vesicles. 4:26316, 2015.
35. Wittrup, A., and J. Lieberman. Knocking down disease: a progress report on siRNA therapeutics. Nat. Rev. Genet. 16:543–552, 2015.
36. Zhao, D., Y. Sui, and X. Zheng. miR-331-3p inhibits proliferation and promotes apoptosis by targeting HER2 through the PI3K/Akt and ERK1/2 pathways in colorectal cancer. Oncol. Rep. 35:1075–1082, 2016.