An aptamer-siRNA chimera silences the eukaryotic elongation factor 2 gene and induces apoptosis in cancers expressing αvβ3 integrin

Nucleic Acid Therapeutics

Volumn 23, Issue 3, 2013, Pages 203-212

  Hussain, Ahmad Fawzi ^a   Tur, Mehmet Kemal ^b   Barth, Stefan ^a,c  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL GIESSEN   (Germany)

^c FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; APTAMER VITRONECTIN RECEPTOR; APTAMER VITRONECTIN RECEPTOR SIRNA EUKARYOTIC ELONGATION FACTOR 2; BETA INTERFERON; ELONGATION FACTOR 2; EUKARYOTIC ELONGATION FACTOR 2; MESSENGER RNA; SMALL INTERFERING RNA; TUMOR ANTIGEN; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ANTIGEN BINDING; APOPTOSIS; ARTICLE; CANCER CELL; CANCER GENETICS; CELL PROLIFERATION; CELL VIABILITY; CHIMERA; CONTROLLED STUDY; CYTOTOXICITY; EMBRYO; EUKARYOTE; FEMALE; FLOW CYTOMETRY; GENE DELIVERY SYSTEM; GENE INDUCTION; GENE SEQUENCE; GENE SILENCING; GENE TARGETING; GLIOBLASTOMA; HUMAN; HUMAN CELL; IMMUNOGENICITY; INTERFERON INDUCTION; MALE; PRIORITY JOURNAL; PROSTATE CANCER; RNA DEGRADATION; RNA SEQUENCE; RNA SYNTHESIS; RNA TRANSCRIPTION; TUMOR CELL; UTERINE CERVIX CANCER;

APOPTOSIS; APTAMERS, NUCLEOTIDE; BASE SEQUENCE; CELL LINE, TUMOR; GENE EXPRESSION; GENE SILENCING; HUMANS; INTEGRIN ALPHAVBETA3; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDE ELONGATION FACTOR 2; RNA, SMALL INTERFERING;

EID: 84878226716     PISSN: 21593337     EISSN: None     Source Type: Journal    
DOI: 10.1089/nat.2012.0408     Document Type: Article

References (58)

1. BOYCE, M., PY B.F., RYAZANOV A.G., MINDEN J.S., LONG K., MA D., and YUAN J. (2008). A pharmacoproteomic approach implicates eukaryotic elongation factor 2 kinase in ER stress-induced cell death. Cell Death Differ. 15, 589-599.
2. BRETSCHER, M.S. (1992). Circulating integrins: alpha 5 beta 1, alpha 6 beta 4 and Mac-1, but not alpha 3 beta 1, alpha 4 beta 1 or LFA-1. EMBO J 11, 405-410.
3. CASWELL, P.T., and NORMAN J.C. (2006). Integrin trafficking and the control of cell migration. Traffic 7, 14-21.
4. CHATTOPADHYAY, N., and CHATTERJEE A. (2001). Studies on the expression of alpha(v)beta3 integrin receptors in non-malignant and malignant human cervical tumor tissues. J. Exp. Clin. Cancer Res. 20, 269-275.
5. CHEN, K., and CHEN X. (2011). Integrin targeted delivery of chemotherapeutics. Theranostics 1, 189-200.
6. CHEN, M., DU Q., ZHANG H.Y., WAHLESTEDT C., and LIANG Z. (2005). Vector-based siRNA delivery strategies for high-throughput screening of novel target genes. J. RNAi Gene Silencing 1, 5-11.
7. CHU, T.C., TWU K.Y., ELLINGTON A.D., and LEVY M. (2006). Aptamer mediated siRNA delivery. Nucleic Acids Res. 34, e73.
8. DASSIE, J.P., LIU X.Y., THOMAS G.S., WHITAKER R.M., THIEL K.W., STOCKDALE K.R., MEYERHOLZ D.K., MCCAFFREY A.P., MCNAMARA J.O., 2ND, and GIAN-GRANDE P.H. (2009). Systemic administration of optimized aptamer-siRNA chimeras promotes regression of PSMA-expressing tumors. Nat. Biotechnol. 27, 839-849.
9. DHAR, S., GU F.X., LANGER R., FAROKHZAD O.C., and LIPPARD S.J. (2008). Targeted delivery of cisplatin to prostate cancer cells by aptamer functionalized Pt(IV) prodrug-PLGA-PEG nanoparticles. Proc. Natl. Acad. Sci. U. S. A. 105, 17356-17361.
10. DIEBOLD, S.S., MASSACRIER C., AKIRA S., PATUREL C., MOREL Y., and REIS E SOUSA C. (2006). Nucleic acid agonists for Toll-like receptor 7 are defined by the presence of uridine ribonucleotides. Eur. J. Immunol. 36, 3256-3267.
11. ELBAKRY, A., ZAKY A., LIEBL R., RACHEL R., GOEPFERICH A., and BREUNIG M. (2009). Layer-by-layer assembled gold nanoparticles for siRNA delivery. Nano Lett 9, 2059-2064.
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. FERREIRA, C.S., CHEUNG M.C., MISSAILIDIS S., BISLAND S., and GARIEPY J. (2009). Phototoxic aptamers selectively enter and kill epithelial cancer cells. Nucleic Acids Res. 37, 866-876.
14. FIRE, A., XU S., MONTGOMERY M.K., KOSTAS S.A., DRIVER S.E., and MELLO C.C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis ele-gans. Nature 391, 806-811.
15. FUKUDA, K., VISHNUVARDHAN D., SEKIYA S., HWANG J., KAKIUCHI N., TAIRA K., SHIMOTOHNO K., KUMAR P.K., and NISHIKAWA S. (2000). Isolation and characterization of RNA aptamers specific for the hepatitis C virus nonstructural protein 3 protease. Eur. J. Biochem. 267, 3685-3694.
16. GARCIA-SASTRE, A., and BIRON C.A. (2006). Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312, 879-882.
17. GOEL, H.L., LI J., KOGAN S., and LANGUINO L.R. (2008). Integrins in prostate cancer progression. Endocr. Relat. Cancer 15, 657-664.
18. GUO, S., HUANG Y., JIANG Q., SUN Y., DENG L., LIANG Z., DU Q., XING J., ZHAO Y., WANG P.C., et al. (2010). Enhanced gene delivery and siRNA silencing by gold nano-particles coated with charge-reversal polyelectrolyte. ACS Nano. 4, 5505-5511.
19. GUO, W., and GIANCOTTI F.G. (2004). Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5, 816-826.
20. HAUSER, P.V., PIPPIN J.W., KAISER C., KROFFT R.D., BRINKKOETTER P.T., HUDKINS K.L., KERJASCHKI D., REISER J., ALPERS C.E., and SHANKLAND S.J. (2010). Novel siRNA delivery system to target podocytes in vivo. PLoS One 5, e9463.
21. HEIL, F., HEMMI H., HOCHREIN H., AMPENBERGER F., KIRSCHNING C., AKIRA S., LIPFORD G., WAGNER H., and BAUER S. (2004). Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303, 1526-1529.
22. HUANG, Y.F., SHANGGUAN D., LIU H., PHILLIPS J.A., ZHANG X., CHEN Y., and TAN W. (2009). Molecular assembly of an aptamer-drug conjugate for targeted drug delivery to tumor cells. Chembiochem 10, 862-868.
23. JEONG, J.H., MOK H., OH Y.K., and PARK T.G. (2009). siRNA conjugate delivery systems. Bioconjug. Chem. 20, 5-14.
24. JEONG, S., EOM T., KIM S., LEE S., and YU J. (2001). In vitro selection of the RNA aptamer against the Sialyl Lewis X and its inhibition of the cell adhesion. Biochem Biophys Res Commun 281, 237-43.
25. JUDGE, A.D., SOOD V., SHAW J.R., FANG D., MCCLINTOCK K., and MACLACHLAN I. (2005). Sequence-dependent stimulation of the mammalian innate immune response by synthetic siRNA. Nat. Biotechnol. 23, 457-462.
26. KAUL, G., PATTAN G., and RAFEEQUI T. (2011). Eukaryotic elongation factor-2 (eEF2): its regulation and peptide chain elongation. Cell Biochem. Funct. 29, 227-234.
27. KIM, H.K., DAVAA E., MYUNG C.S., and PARK J.S. (2010). Enhanced siRNA delivery using cationic liposomes with new polyarginine-conjugated PEG-lipid. Int. J. Pharm. 392, 141-147.
28. LENG, Q., WOODLE M.C., LU P.Y., and MIXSON A.J. (2009). Advances in Systemic siRNA Delivery. Drugs Future 34, 721.
29. LI, N., NGUYEN H.H., BYROM M., and ELLINGTON A.D. (2011). Inhibition of cell proliferation by an anti-EGFR apta-mer. PLoS ONE 6, e20299.
30. LUO, B.H., CARMAN C.V., and SPRINGER T.A. (2007). Structural basis of integrin regulation and signaling. Annu. Rev. Immunol. 25, 619-647.
31. MALLIKARATCHY, P., TANG Z., and TAN W. (2008). Cell specific aptamer-photosensitizer conjugates as a molecular tool in photodynamic therapy. ChemMedChem 3, 425-428.
32. MCNAMARA, J.O., 2ND, ANDRECHEK E.R., WANG Y., VILES K.D., REMPEL R.E., GILBOA E., SULLENGER B.A., and GIANGRANDE P.H. (2006). Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras. Nat. Biotechnol. 24, 1005-1015.
33. MI, J., ZHANG X., GIANGRANDE P.H., MCNAMARA J.O., 2ND, NIMJEE S.M., SARRAF-YAZDI S., SULLENGER B.A., and CLARY B.M. (2005). Targeted inhibition of al-phavbeta3 integrin with an RNA aptamer impairs endothelial cell growth and survival. Biochem. Biophys. Res. Commun. 338, 956-363.
34. MOSCHOS, S.A., JONES S.W., PERRY M.M., WILLIAMS A.E., ERJEFALT J.S., TURNER J.J., BARNES P.J., SPROAT B.S., GAIT M.J., and LINDSAY M.A. (2007). Lung delivery studies using siRNA conjugated to TAT(48-60) and penetratin reveal peptide induced reduction in gene expression and induction of innate immunity. Bioconjug. Chem. 18, 1450-1459.
35. NEFF, C.P., ZHOU J., REMLING L., KURUVILLA J., ZHANG J., LI H., SMITH D.D., SWIDERSKI P., ROSSI J.J., and AKKINA R. (2011). An aptamer-siRNA chimera suppresses HIV-1 viral loads and protects from helper CD4(+) T cell decline in humanized mice. Sci. Transl. Med. 3, 66ra6.
36. NG, E.W., SHIMA D.T., CALIAS P., CUNNINGHAM E.T., JR., GUYER D.R., and ADAMIS A.P. (2006). Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat. Rev. Drug Discov. 5, 123-132.
37. NGUYEN, T., MENOCAL E.M., HARBORTH J., and FRUE-HAUF J.H. (2008). RNAi therapeutics: an update on delivery. Curr. Opin. Mol. Ther. 10, 158-167.
38. NI, X., ZHANG Y., RIBAS J., CHOWDHURY W.H., CASTA-NARES M., ZHANG Z., LAIHO M., DEWEESE T.L., and LUPOLD S.E. (2011). Prostate-targeted radiosensitization via aptamer-shRNA chimeras in human tumor xenografts. J. Clin. Invest. 121, 2383-2890.
39. PASTOR, F., KOLONIAS D., GIANGRANDE P.H., and GILBOA E. (2010). Induction of tumour immunity by targeted inhibition of nonsense-mediated mRNA decay. Nature 465, 227-230.
40. PICKFORD, A.S., and COGONI C. (2003). RNA-mediated gene silencing. Cell Mol. Life Sci. 60, 871-882.
41. PIETRAS, K., OSTMAN A., SJOQUIST M., BUCHDUNGER E., REED R.K., HELDIN C.H., and RUBIN K. (2001). Inhibition of platelet-derived growth factor receptors reduces interstitial hypertension and increases transcapillary transport in tumors. Cancer Res. 61, 2929-2934.
42. PROSKE, D., GILCH S., WOPFNER F., SCHATZL H.M., WINNACKER E.L., and FAMULOK M. (2002). Prion-protein-specific aptamer reduces PrPSc formation. Chembiochem 3, 717-7125.
43. ROBERTS, M.S., WOODS A.J., DALE T.C., VAN DER SLUIJS P., and NORMAN J.C. (2004). Protein kinase B/Akt acts via glycogen synthase kinase 3 to regulate recycling of alpha v beta 3 and alpha 5 beta 1 integrins. Mol. Cell Biol. 24, 1505-1515.
44. RUSCONI, C.P., SCARDINO E., LAYZER J., PITOC G.A., OR-TEL T.L., MONROE D., and SULLENGER B.A. (2002). RNA aptamers as reversible antagonists of coagulation factor IXa. Nature 419, 90-94.
45. RYDZANICZ, R., ZHAO X.S., and JOHNSON P.E. (2005). Assembly PCR oligo maker: a tool for designing oligodeox-ynucleotides for constructing long DNA molecules for RNA production. Nucleic Acids Res. 33, W521-525.
46. SIOUD, M. (2005). Induction of inflammatory cytokines and interferon responses by double-stranded and single-stranded siRNAs is sequence-dependent and requires endosomal localization. J. Mol. Biol. 348, 1079-1090.
47. SONG, E., ZHU P., LEE S.K., CHOWDHURY D., KUSSMAN S., DYKXHOORN D.M., FENG Y., PALLISER D., WEINER D.B., SHANKAR P., et al. (2005). Antibody mediated in vivo delivery of small interfering RNAs via cell-surface receptors. Nat. Biotechnol. 23, 709-717.
48. SOUTSCHEK, J., AKINC A., BRAMLAGE B., CHARISSE K., CONSTIEN R., DONOGHUE M., ELBASHIR S., GEICK A., HADWIGER P., HARBORTH J., et al. (2004). Therapeutic silencing of an endogenous gene by systemic administration of modified-17siRNAs. Nature 432, 173-8.
49. TAHERIAN, A., LI X., LIU Y., and HAAS T.A. (2011). Differences in integrin expression and signaling within human breast cancer cells. BMC Cancer 11, 293.
50. TAKANO, S., TSUBOI K., TOMONO Y., MITSUI Y., and NOSE T. (2000). Tissue factor, osteopontin, alphavbeta3 integrin expression in microvasculature of gliomas associated with vascular endothelial growth factor expression. Br. J. Cancer 82, 1967-1973.
51. WHITE, D.P., CASWELL P.T., and NORMAN J.C. (2007). Alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J. Cell Biol. 177, 515-525.
52. WHITEHEAD, K.A., DAHLMAN J.E., LANGER R.S., and ANDERSON D.G. (2011). Silencing or stimulation? siRNA delivery and the immune system. Annu. Rev. Chem. and Biomol. Eng. 2, 77-96.
53. WOODS, A.J., WHITE D.P., CASWELL P.T., and NORMAN J.C. (2004). PKD1/PKCmu promotes alphavbeta3 integrin recycling and delivery to nascent focal adhesions. EMBO J. 23, 2531-2543.
54. 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.
55. YOSHIMOTO, M., OGAWA K., WASHIYAMA K., SHIKANO N., MORI H., AMANO R., and KAWAI K. (2008). al-pha(v)beta(3) Integrin-targeting radionuclide therapy and imaging with monomeric RGD peptide. Int. J. Cancer 123, 709-15.
56. ZHOU, J., LI H., LI S., ZAIA J., and ROSSI J.J. (2008). Novel dual inhibitory function aptamer-siRNA delivery system for HIV-1 therapy. Mol. Ther. 16, 1481-1489.
57. ZHOU, J., SHU Y., GUO P., SMITH D.D., and ROSSI J.J. (2011). Dual functional RNA nanoparticles containing phi29 motor pRNA and anti-gp120 aptamer for cell-type specific delivery and HIV-1 inhibition. Methods 54, 284-294.
58. ZUKER, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415.