Aptamer-mediated delivery of splice-switching oligonucleotides to the nuclei of cancer cells

Nucleic Acid Therapeutics

Volumn 22, Issue 3, 2012, Pages 187-195

  Kotula, Jonathan W ^a   Pratico, Elizabeth D ^a   Ming, Xin ^b   Nakagawa, Osamu ^b   Juliano, Rudolph L ^b   Sullenger, Bruce A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b University of North Carolina   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; CELL SURFACE RECEPTOR; NUCLEOLIN; OLIGONUCLEOTIDE; SPLICE SWITCHING OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL MIGRATION; CELL NUCLEUS; CELL TYPE; CHIMERA; CONTROLLED STUDY; CYTOPLASM; ENDOSOME; GENE DELIVERY SYSTEM; GENETIC ENGINEERING; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; RNA SPLICING;

APTAMERS, NUCLEOTIDE; CELL LINE, TUMOR; CELL NUCLEUS; ENDOCYTOSIS; FLOW CYTOMETRY; HUMANS; NEOPLASMS; OLIGONUCLEOTIDES; PHOSPHOPROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA INTERFERENCE; RNA SPLICING; RNA-BINDING PROTEINS;

EID: 84862319255     PISSN: 21593337     EISSN: None     Source Type: Journal    
DOI: 10.1089/nat.2012.0347     Document Type: Article

References (46)

1. ALAM, M., MING, X., DIXIT, V., FISHER, M., CHEN, X., and JULIANO, R. (2010). The biological effect of an antisense oligonucleotide depends on its route of endocytosis and trafficking. Oligonucleotides 20, 103-109.
2. BATES, P., CHOI, E., and NAYAK, L. (2009a). G-rich oligonucleotides for cancer treatment. Methods Mol. Biol. 542, 379-392.
3. BATES, P.J., LABER, D.A., MILLER, D.M., THOMAS, S.D., and TRENT, J.O. (2009b). Discovery and development of the G-rich oligonucleotide AS1411 as a novel treatment for cancer. Exp. Mol. Pathol. 86, 151-164.
4. BAUMAN, J., JEARAWIRIYAPAISARN, N., and KOLE, R. (2009). Therapeutic potential of splice-switching oligonucleotides. Oligonucleotides 19, 1-13.
5. BAUMAN, J.A., and KOLE, R. (2011). Modulation of RNA splicing as a potential treatment for cancer. Bioeng. Bugs 2, 125-128.
6. BAUMAN, J.A., LI, S.D., YANG, A., HUANG, L., and KOLE, R. (2010). Anti-tumor activity of splice-switching oligonucleotides. Nucleic Acids Res. 38, 8348-8356.
7. CHU, T., MARKS, J.R., LAVERY, L., FAULKNER, S., ROSENBLUM, M., ELLINGTON, A., and LEVY, M. (2006a). Aptamer: toxin conjugates that specifically target prostate tumor cells. Cancer Res. 66, 5989-5992.
8. CHU, T., TWU, K., ELLINGTON, A., and LEVY M. (2006b). Aptamer mediated siRNA delivery. Nucleic Acids Res. 34, e73.
9. DASSIE, J., LIU, X., THOMAS, G., WHITAKER, R., THIEL, K., STOCKDALE, K., MEYERHOLZ, D., MCCAFFREY, A., MCNAMARA, J.N., and GIANGRANDE, P. (2009). Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors. Nat. Biotechnol. 27, 839-849.
10. DOLLINS, C., NAIR, S., BOCZKOWSKI, D., LEE, J., LAYZER, J., GILBOA, E., and SULLENGER B. (2008a). Assembling OX40 aptamers on a molecular scaffold to create a receptor-activating aptamer. Chem. Biol. 15, 675-682.
11. DOLLINS, C., NAIR, S., SULLENGER, B. (2008b). Aptamers in immunotherapy. Hum. Gene Ther. 19, 443-450.
12. FAROKHZAD, O.C., CHENG, J., TEPLY, B.A., SHERIFI, I., JON, S., KANTOFF, P.W., RICHIE, J.P., and LANGER, R. (2006). Targeted nanoparticle-aptamer bioconjugates for cancer chemotherapy in vivo. Proc. Natl. Acad. Sci. U. S. A. 103, 6315-6320.
13. GINISTY, H., AMALRIC, F., and BOUVET, P. (1998). Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17, 1476-1486.
14. GINISTY, H., SICARD, H., ROGER, B., and BOUVET, P. (1999). Structure and functions of nucleolin. J. Cell Sci. 112(6), 761-772.
15. GIRVAN, A., TENG, Y., CASSON, L., THOMAS, S., JÜLIGER, S., BALL, M., KLEIN, J., PIERCE, W.J., BARVE, S., and BATES, P. (2006). AGRO100 inhibits activation of nuclear factor-kappaB (NF-kappaB) by forming a complex with NF-kappaB essential modulator (NEMO) and nucleolin. Mol. Cancer Ther. 5, 1790-1799.
16. HOVANESSIAN, A.G., SOUNDARAMOURTY, C., EL KHOURY, D., NONDIER, I., SVAB, J., and KRUST, B. (2010). Surface expressed nucleolin is constantly induced in tumor cells to mediate calcium-dependent ligand internalization. PLoS One 5, e15787.
17. HUANG, Y., SHI, H., ZHOU, H., SONG, X., YUAN, S., and LUO, Y. (2006). The angiogenic function of nucleolin is mediated by vascular endothelial growth factor and nonmuscle myosin. Blood 107, 3564-3571.
18. IRESON, C., and KELLAND, L. (2006). Discovery and development of anticancer aptamers. Mol. Cancer Ther. 5, 2957-2962.
19. IVANOV, A.I., NUSRAT, A., and PARKOS, C.A. (2004). Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol. Biol. Cell 15, 176-188.
20. KANG, S.H., CHO, M.J., and KOLE, R. (1998). Up-regulation of luciferase gene expression with antisense oligonucleotides: implications and applications in functional assay development. Biochemistry 37, 6235-6239.
21. KIM, E., JUNG, Y., CHOI, H., YANG, J., SUH, J.S., HUH, Y.M., KIM, K., and HAAM, S. (2010). Prostate cancer cell death produced by the co-delivery of Bcl-xL shRNA and doxorubicin using an aptamer-conjugated polyplex. Biomaterials 31, 4592-9.
22. KOIVUSALO, M., WELCH, C., HAYASHI, H., SCOTT, C.C., KIM, M., ALEXANDER, T., TOURET, N., HAHN, K.M., and GRINSTEIN, S. (2010). Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J. Cell Biol. 188, 547-563.
23. KOLE, R., VACEK, M., and WILLIAMS, T. (2004a). Modification of alternative splicing by antisense therapeutics. Oligonucleotides 14, 65-74.
24. KOLE, R., WILLIAMS, T., and COHEN, L. (2004b). RNA modulation, repair and remodeling by splice switching oligonucleotides. Acta Biochim. Pol. 51, 373-378.
25. LI, N., LARSON, T., NGUYEN, H., SOKOLOV, K., and ELLINGTON, A. (2010). Directed evolution of gold nanoparticle delivery to cells. Chem. Commun. (Camb.) 46, 392-394.
26. LI, N., NGUYEN, H.H., BYROM, M., and ELLINGTON, A.D. (2011). Inhibition of cell proliferation by an anti-EGFR aptamer. PLoS One 6, e20299.
27. LUNDIN, P., JOHANSSON, H., GUTERSTAM, P., HOLM, T., HANSEN, M., LANGEL, U., and EL ANDALOUSSI, S. (2008). Distinct uptake routes of cell-penetrating peptide conjugates. Bioconjug. Chem. 19, 2535-2542.
28. MCNAMARA, J.N., ANDRECHEK, E., WANG, Y., VILES, K., REMPEL, R., GILBOA, E., SULLENGER, B., and GIANGRANDE, P. (2006). Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras. Nat Biotechnol 24, 1005-1015.
29. MERCER, J., and HELENIUS, A. (2009). Virus entry by macropinocytosis. Nat. Cell Biol. 11, 510-520.
30. MERCER, J., SCHELHAAS, M., and HELENIUS, A. (2010). Virus entry by endocytosis. Annu. Rev. Biochem. 79, 803-833.
31. MIN, K., JO, H., SONG, K., CHO, M., CHUN, Y.S., JON, S., KIM, W.J., and BAN, C. (2011). Dual-aptamer-based delivery vehicle of doxorubicin to both PSMA (+) and PSMA (-) prostate cancers. Biomaterials 32, 2124-2132.
32. MING, X., ALAM, M., FISHER, M., YAN, Y., CHEN, X., and JULIANO, R. (2010). Intracellular delivery of an antisense oligonucleotide via endocytosis of a G protein-coupled receptor. Nucleic Acids Res. 38, 6567-6576.
33. PARTON, R.G., JOGGERST, B., and SIMONS, K. (1994). Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215.
34. POLLICE, A., ZIBELLA, M., BILAUD, T., LAROCHE, T., PULITZER, J., and GILSON, E. (2000). In vitro binding of nucleolin to double-stranded telomeric DNA. Biochem. Biophys. Res. Commun. 268, 909-915.
35. REYES-REYES, E.M., TENG, Y., and BATES, P.J. (2010). A new paradigm for aptamer therapeutic AS1411 action: uptake by macropinocytosis and its stimulation by a nucleolin-dependent mechanism. Cancer Res. 70, 8617-8629.
36. SIECZKARSKI, S.B., and WHITTAKER, G.R. (2002). Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 76, 10455-10464.
37. SOUNDARARAJAN, S., CHEN, W., SPICER, E., COURTENAYLUCK, N., and FERNANDES, D. (2008). The nucleolin targeting aptamer AS1411 destabilizes Bcl-2 messenger RNA in human breast cancer cells. Cancer Res. 68, 2358-2365.
38. TENG, Y., GIRVAN, A., CASSON, L., PIERCE, W.J., QIAN, M., THOMAS, S., and BATES, P. (2007). AS1411 alters the localization of a complex containing protein arginine methyltransferase 5 and nucleolin. Cancer Res. 67, 10491-10500.
39. TIEMANN, K., and ROSSI, J. (2009). RNAi-based therapeutics-current status, challenges and prospects. EMBO Mol. Med. 1, 142-151.
40. VALLEE, R.B., HERSKOVITS, J.S., AGHAJANIAN, J.G., BURGESS, C.C., and SHPETNER, H.S. (1993). Dynamin, a GTPase involved in the initial stages of endocytosis. Ciba Found. Symp. 176, 185-193; discussion 193-197.
41. WADIA, J.S., STAN, R.V., and DOWDY, S.F. (2004). Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10, 310-315.
42. WAN, J., SAZANI, P., and KOLE, R. (2009). Modification of HER2 pre-mRNA alternative splicing and its effects on breast cancer cells. Int. J. Cancer 124, 772-777.
43. WU, X., DING, B., GAO, J., WANG, H., FAN, W., WANG, X., ZHANG, W., YE, L., ZHANG, M., DING, X. et al. (2011). Second-generation aptamer-conjugated PSMA-targeted delivery system for prostate cancer therapy. Int. J. Nanomedicine 6, 1747-1756.
44. WULLNER, U., NEEF, I., ELLER, A., KLEINES, M., TUR, M.K., and BARTH, S. (2008). Cell-specific induction of apoptosis by rationally designed bivalent aptamer-siRNA transcripts silencing eukaryotic elongation factor 2. Curr. Cancer Drug Targets 8, 554-565.
45. ZHANG, N., PEAIRS, J.J., YANG, P., TYRRELL, J., ROBERTS, J., KOLE, R., and JAFFE, G.J. (2007). The importance of Bcl-xL in the survival of human RPE cells. Invest. Ophthalmol. Vis. Sci. 48, 3846-3853.
46. ZHOU, J., and ROSSI, J. (2010). Aptamer-targeted cell-specific RNA interference. Silence 1, 4.