Virus-like particle-mediated intracellular delivery of mRNA cap analog with in vivo activity against hepatocellular carcinoma

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 11, Issue 1, 2015, Pages 67-76

  Zochowska, Monika ^a   Piguet, Anne Christine ^b   Jemielity, Jacek ^c,d   Kowalska, Joanna ^c   Szolajska, Ewa ^a   Dufour, Jean François ^e   Chroboczek, Jadwiga ^a,f  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF WARSAW   (Poland)

^d UNIVERSITY OF WARSAW   (Poland)

^e UNIVERSITY OF BERN   (Switzerland)

^f CNRS   (France)

Author keywords

Adenoviral dodecahedron; Cap structure analogs; Doxorubicin; Drug delivery vector; EIF4E inhibitor; Hepatocellular carcinoma; Oncogene eIF4E; Virus like particle

Indexed keywords

CELL CULTURE; DISEASES; DRUG DELIVERY; ONCOGENIC VIRUSES; RATS;

ADENOVIRAL DODECAHEDRON; CAP STRUCTURE; DELIVERY VECTOR; DOXORUBICIN; EIF4E INHIBITOR; HEPATOCELLULAR CARCINOMA; ONCOGENE EIF4E; VIRUS-LIKE PARTICLES;

TUMORS;

ADENOVIRUS DODECAHEDRON VECTOR; ADENOVIRUS VECTOR; DOXORUBICIN; INITIATION FACTOR 4E; MESSENGER RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; MYC PROTEIN; VIRUS LIKE PARTICLE VACCINE;

ADENOVIRIDAE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER GENE THERAPY; CANCER INHIBITION; CONTROLLED STUDY; DRUG CYTOTOXICITY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; NONHUMAN; ONCOGENE C MYC; RAT; VIRAL GENE DELIVERY SYSTEM; VIRUS LIKE AGENT; ANIMAL; CANCER TRANSPLANTATION; CARCINOMA, HEPATOCELLULAR; CELL NUCLEUS; CELL PROLIFERATION; CHEMISTRY; CYTOPLASM; ENDOCYTOSIS; GENE VECTOR; HELA CELL LINE; LIVER NEOPLASMS; METABOLISM; NANOMEDICINE; PROCEDURES; TUMOR CELL LINE;

ADENOVIRIDAE; ANIMALIA; RATTUS;

ADENOVIRIDAE; ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; CYTOPLASM; DOXORUBICIN; ENDOCYTOSIS; EUKARYOTIC INITIATION FACTOR-4E; GENETIC VECTORS; HELA CELLS; HUMANS; LIVER NEOPLASMS; NANOMEDICINE; NEOPLASM TRANSPLANTATION; PROTO-ONCOGENE PROTEINS C-MYC; RATS; RNA, MESSENGER; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84919614677     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2014.07.009     Document Type: Article

References (45)

1. Fender P., Ruigrok R.W., Gout E., Buffet, Chroboczek J. Adenovirus dodecahedron, a novel vector for human gene transfer. Nat Biotechnol 1997, 15:52-56.
2. Garcel A., Gout E., Timmins J., Chroboczek J., Fender P. Protein transduction into human cells by adenovirus dodecahedron using WW domains as universal adaptors. J Gene Med 2006, 8:524-531.
3. Wickham T.J., Mathias P., Cheresh D.A., Nemerow G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 23:309-319.
4. Eliceiri B.P., Cheresh D.A. The role of alpha v integrins during angiogenesis: insights into potential mechanisms of action and clinical development. J Clin Invest 1999, 103:1227-1230. [Review].
5. Pasqualini R., Koivunen E., Ruoslahti E. Alpha v integrins as receptors for tumor targeting by circulating ligands. Nat Biotechnol 1997, 15:542-546.
6. Vivès R.R., Lortat-Jacob H., Chroboczek J., Fender P. Heparan sulfate proteoglycan mediates the selective attachment and internalization of serotype 3 human adenovirus dodecahedron. Virology 2004, 321:332-340.
7. Fender P., Schoehn G., Perron-Sierra F., Tucker G.C., Lortat-Jacob H. Adenovirus dodecahedron cell attachment and entry are mediated by heparan sulfate and integrins and vary along the cell cycle. Virology 2008, 371:155-164.
8. Nakamura N., Hurst R.E., West S.S. Biochemical composition and heterogeneity of heparan sulfates isolated from AH-130 ascites hepatoma cells and fluid. Biochim Biophys Acta 1978, 538:445-457.
9. Kojima J., Nakamura N., Kanatani M., Ohmori K. The glycosaminoglycans in human hepatic cancer. Cancer Res 1975, 3:542-547.
10. Maluccio M., Covey A. Recent progress in understanding, diagnosing, and treating hepatocellular carcinoma. CA Cancer J Clin 2012, 62:394-399.
11. Sonenberg N., Gingras A.C. The mRNA 5' cap-binding protein eIF4E and control of cell growth. Curr Opin Cell Biol 1998, 10:268-275.
12. De Benedetti A., Graff J.R. eIF4E expression and its role in malignancies and metastases. Oncogene 2004, 23:3189-3199.
13. Lejbkowicz F., Goyer C., Darveau A., Neron S., Lemieux R., Sonenberg N. A fraction of the mRNA 5' cap-binding protein, eukaryotic initiation factor 4E, localizes to the nucleus. Proc Natl Acad Sci U S A 1992, 89:9612-9616.
14. Culjkovic B., Topisirovic I., Skrabanek L., Ruiz-Gutierrez M., Borden K.L. eIF4E is a central node of an RNA regulon that governs cellular proliferation. J Cell Biol 2006, 175:415-426.
15. Culjkovic B., Topisirovic I., Borden K.L. Controlling gene expression through RNA regulons: the role of the eukaryotic translation initiation factor eIF4E. Cell Cycle 2007, 6:65-69.
16. Jia Y., Polunovsky V., Bitterman P.B., Wagner C.R. Cap-dependent translation initiation factor eIF4E: an emerging anticancer drug target. Med Res Rev 2012, 32:786-814.
17. Cai A.L., Jankowska-Anyszka M., Centers A., Chlebicka L., Stepinski J., Stolarski R., et al. Quantitative assessment of mRNA cap analogs as inhibitors of cell-free translation. Biochemistry 1999, 38:8538-8547.
18. Li S., Jia Y., Jacobson B., McCauley J., Kratzke R., Bitterman P., et al. Treatment of breast and lung cancer cells with a N-7 benzyl guanosine monophosphate tryptamine phosphoramidate pronucleotide (4Ei-1) results in chemosensitization to gemcitabine and induced eIF4E proteasomal degradation. Mol Pharm 2013, 10:523-531.
19. Jemielity J., Fowler T., Zuberek J., Stepinski J., Lewdorowicz M., Niedzwiecka A. Novel "anti-reverse" cap analogs with superior translational properties. RNA 2003, 9:1108-1122.
20. Dewhirst M.W., Landon C.D., Hofmann C.L., Stauffer P.R. Novel approaches to treatment of hepatocellular carcinoma and hepatic metastases using thermal ablation and thermosensitive liposomes. Surg Oncol Clin N Am 2013, 22:545-561.
21. Gabizon A., Shmeeda H., Barenholz Y. Pharmacokinetics of pegylated liposomal doxorubicin: review of animal and human studies. Clin Pharmacokinet 2003, 42:419-436.
22. Zochowska M., Paca A., Schoehn G., Andrieu J.P., Chroboczek J., Dublet B., et al. Adenovirus dodecahedron, as a drug delivery vector. PLoS One 2009, 4:e5569.
23. Sebestik J., Niederhafner P., Jezek J. Peptide and glycopeptide dendrimers and analogous dendrimeric structures and their biomedical applications. Amino Acids 2011, 40:301-370.
24. Jian F., Zhang Y., Wang J., Ba K., Mao R., Lai W., et al. Toxicity of biodegradable nanoscale preparations. Curr Drug Metab 2012, 13:440-446.
25. van den Berg A., Dowdy S.F. Protein transduction domain delivery of therapeutic macromolecules. Curr Opin Biotechnol 2011, 22:888-893.
26. Storm G., van Hoesel Q.G., de Groot G., Kop W., Steerenberg P.A., Hillen F.C. A comparative study on the antitumor effect, cardiotoxicity and nephrotoxicity of doxorubicin given as a bolus, continuous infusion or entrapped in liposomes in the Lou/M Wsl rat. Cancer Chemother Pharmacol 1989, 24:341-348.
27. Fender P., Schoehn G., Foucaud-Gamen J., Gout E., Garcel A., Drouet E., et al. Adenovirus dodecahedron allows large multimeric protein transduction in human cells. J Virol 2003, 77:4960-4964.
28. Kowalska J., Lukaszewicz M., Zuberek J., Ziemniak M., Darzynkiewicz E., Jemielity J. Phosphorothioate analogs of m7GTP are enzymatically stable inhibitors of cap-dependent translation. Bioorg Med Chem Lett 2009, 19:1921-1925.
29. Kalek M., Jemielity J., Darzynkiewicz Z.M., Bojarska E., Stepinski J., Stolarski R., et al. Enzymatically stable 5' mRNA cap analogs: synthesis and binding studies with human DcpS decapping enzyme. Bioorg Med Chem 2006, 14:3223-3230.
30. Rydzik A.M., Lukaszewicz M., Zuberek J., Kowalska J., Darzynkiewicz Z.M., Darzynkiewicz E., et al. Synthetic dinucleotide mRNA cap analogs with tetraphosphate 5,5 bridge containing methylenebis(phosphonate) modification. Org Biomol Chem 2009, 7:4763-4776.
31. Kalek M., Jemielity J., Zuberek J., Grudzien E., Bojarska E., Cohen L.S., et al. Synthesis and biochemical properties of novel mRNA 5' cap analogs resistant to enzymatic hydrolysis. Nucleosides Nucleotides Nucleic Acids 2005, 24:615-621.
32. Beyer U., Rothern-Rutishauser B., Unger C., Wunderli-Allenspach H., Kratz F. Differences in the intracellular distribution of acid-sensitive doxorubicin-protein conjugates in comparison to free and liposomal formulated doxorubicin as shown by confocal microscopy. Pharm Res 2001, 1:29-38.
33. Alberici L., Roth L., Sugahara K.N., Agemy L., Kotamraju V.R., Teesalu T., et al. De novo design of a tumor-penetrating peptide. Cancer Res 2013, 73:804-812.
34. El Hage T., Decottignies P., Authier F. Endosomal proteolysis of diphtheria toxin without toxin translocation into the cytosol of rat liver in vivo. FEBS J 2008, 275:1708-1722.
35. El Hage T., Lorin S., Decottignies P., Djavaheri-Mergny M., Authier F. Proteolysis of Pseudomonas exotoxin A within hepatic endosomes by cathepsins B and D produces fragments displaying in vitro ADP-ribosylating and apoptotic effects. FEBS J 2010, 277:3735-3749.
36. Assouline S., Culjkovic B., Cocolakis E., Rousseau C., Beslu N., Amri A., et al. Molecular targeting of the oncogene eIF4E in acute myeloid leukemia (AML): a proof-of-principle clinical trial with ribavirin. Blood 2009, 114:257-260.
37. Westman B., Beeren L., Grudzien E., Stepinski J., Worch R., Zuberek J., et al. The antiviral drug ribavirin does not mimic the 7-methylguanosine moiety of the mRNA cap structure in vitro. RNA 2005, 11:1505-1513.
38. Murakami H., Sanderson N.D., Nagy P., Marino P.A., Merlino G., Thorgeirsson S.S. Transgenic mouse model for synergistic effects of nuclear oncogenes and growth factors in tumorigenesis: interaction of c-myc and transforming growth factor-α in hepatic oncogenesis. Cancer Res 1993, 53:1719-1723.
39. Pelengaris S., Rudolph B., Littlewood T. Action of Myc in vivo-proliferation and apoptosis. Curr Opin Genet Dev 2000, 10:100-105. [Review].
40. Kawate S., Fukusato T., Ohwada S., Watanuki A., Morishita Y. Amplification of c-myc in hepatocellular carcinoma: correlation with clinicopathologic features, proliferative activity and p53 overexpression. Oncology 1999, 57:157-163.
41. Abou-Elella A.G.T., Fritsch C., Gansler T. c-myc amplification in hepatocellular carcinoma predicts unfavorable prognosis. Mod Pathol 1996, 9:95-98.
42. Shachaf C.M., Kopelman A.M., Arvanitis C., Karlsson A., Beer S., Mandl S., et al. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 2004, 431:1112-1117.
43. Fender P., Hall K., Schoehn G., Blair G.E. Impact of human adenovirus type 3 dodecahedron on host cells and its potential role in viral infection. J Virol 2012, 86:5380-5385.
44. Roth P., Hammer C., Piguet A.C., Ledermann M., Dufour J.F., Waelti E. Effects on hepatocellular carcinoma of doxorubicin-loaded immunoliposomes designed to target the VEGFR-2. J Drug Target 2007, 15:623-631.
45. Jones A.L., Aggeler J. Structure of the liver. Gastroenterology 1995, 3:1813-1831. Saunders, Philadelphia. 5th ed. W. Haubrich, F. Schaffner, J.E. Berk (Eds.).