Proton sponge trick for ph-sensitive disassembly of polyethylenimine-based sirna delivery systems

Bioconjugate Chemistry

Volumn 21, Issue 5, 2010, Pages 994-1002

  Creusat, Gaelle ^a   Rinaldi, Anne Sophie ^a   Weiss, Etienne ^a   Elbaghdadi, Rkia ^a   Remy, Jean Serge ^a   Mulherkar, Rita ^b   Zuber, Guy ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b TATA MEMORIAL HOSPITAL   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; GENE EXPRESSION; MAMMALS; RNA;

CYTOSOLIC; DELIVERY SYSTEMS; DNA TRANSFECTION; GENES EXPRESSION; PH SENSITIVE; PLASMID DNA; POLY(ETHYLENIMINE); PROTON SPONGE; SIRNA DELIVERY; SMALL INTERFERING RNA;

PH SENSORS;

POLYETHYLENEIMINE; POLYMER; PROTON; SMALL INTERFERING RNA; TYROSINE;

ARTICLE; CONJUGATION; DRUG DELIVERY SYSTEM; HUMAN; HUMAN CELL; HYDROPHOBICITY; MEDICAL RESEARCH; PH; PROTON TRANSPORT;

MAMMALIA;

EID: 77952555362     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc100010k     Document Type: Article

References (40)

1. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells Nature 411, 494-498
2. Kim, D. H. and Rossi, J. J. (2007) Strategies for silencing human disease using RNA interference Nat. Rev. Genet. 8, 173-184
3. Wolfrum, C., Shi, S., Jayaprakash, K. N., Jayaraman, M., Wang, G., Pandey, R. K., Rajeev, K. G., Nakayama, T., Charrise, K., Ndungo, E. M., Zimmermann, T., Koteliansky, V., Manoharan, M., and Stoffel, M. (2007) Mechanisms and optimization of in vivo delivery of lipophilic siRNAs Nat. Biotechnol. 25, 1149-1157
4. Juliano, R., Alam, M. R., Dixit, V., and Kang, H. (2008) Mechanisms and strategies for effective delivery of antisense and siRNA oligonucleotides Nucleic Acids Res. 36, 4158-4171
5. Felgner, P. L. (1999) Prospects for synthetic self-assembling systems in gene delivery J. Gene Med. 1, 290-292
6. Neu, M., Fischer, D., and Kissel, T. (2005) Recent advances in rational gene transfer vector design based on poly(ethylene imine) and its derivatives J. Gene Med. 7, 992-1009
7. Lleres, D., Weibel, J. M., Heissler, D., Zuber, G., Duportail, G., and Mely, Y. (2004) Dependence of the cellular internalization and transfection efficiency on the structure and physicochemical properties of cationic detergent/DNA/liposomes J. Gene Med. 6, 415-428
8. Itaka, K. and Kataoka, K. (2009) Recent development of nonviral gene delivery systems with virus-like structures and mechanisms Eur. J. Pharm. Biopharm. 71, 475-483
9. Boussif, O., Lezoualch, F., Zanta, M. A., Mergny, M. D., Scherman, D., Demeneix, B., and Behr, J. P. (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: Polyethylenimine Proc. Natl. Acad. Sci. U.S.A. 92, 7297-7301
10. Kichler, A., Leborgne, C., Coeytaux, E., and Danos, O. (2001) Polyethylenimine-mediated gene delivery: a mechanistic study J. Gene Med. 3, 135-44
11. Grayson, A. C., Doody, A. M., and Putnam, D. (2006) Biophysical and structural characterization of polyethylenimine-mediated siRNA delivery in vitro Pharm. Res. 23, 1868-1876
12. Spagnou, S., Miller, A. D., and Keller, M. (2004) Lipidic carriers of siRNA: differences in the formulation, cellular uptake, and delivery with plasmid DNA Biochemistry 43, 13348-13356
13. van der Gun, B. T., Monami, A., Laarmann, S., Rasko, T., Slaska-Kiss, K., Weinhold, E., Wasserkort, R., de Leij, L. F., Ruiters, M. H., Kiss, A., and McLaughlin, P. M. (2007) Serum insensitive, intranuclear protein delivery by the multipurpose cationic lipid SAINT-2 J. Controlled Release 123, 228-238
14. Meyer, M., Dohmen, C., Philipp, A., Kiener, D., Maiwald, G., Scheu, C., Ogris, M., and Wagner, E. (2009) Synthesis and biological evaluation of a bioresponsive and endosomolytic siRNA-polymer conjugate Mol. Pharm. 6, 752-762
15. Baigude, H., McCarroll, J., Yang, C. S., Swain, P. M., and Rana, T. M. (2007) Design and creation of new nanomaterials for therapeutic RNAi ACS Chem. Biol. 2, 237-41
16. Davis, M. E. (2009) The first targeted delivery of siRNA in humans via a self-assembling, cyclodextrin polymer-based nanoparticle: from concept to clinic Mol. Pharm. 6, 659-668
17. Lim, Y. B., Lee, E., Yoon, Y. R., Lee, M. S., and Lee, M. (2008) Filamentous artificial virus from a self-assembled discrete nanoribbon Angew. Chem., Int. Ed. Engl. 47, 4525-4528
18. Zintchenko, A., Philipp, A., Dehshahri, A., and Wagner, E. (2008) Simple modifications of branched PEI lead to highly efficient siRNA carriers with low toxicity Bioconjugate Chem. 19, 1448-1455
19. Brus, C., Petersen, H., Aigner, A., Czubayko, F., and Kissel, T. (2004) Physicochemical and biological characterization of polyethylenimine-graft- poly(ethylene glycol) block copolymers as a delivery system for oligonucleotides and ribozymes Bioconjugate Chem. 15, 677-684
20. Dufresne, M. H., Elsabahy, M., and Leroux, J. C. (2008) Characterization of polyion complex micelles designed to address the challenges of oligonucleotide delivery Pharm. Res. 25, 2083-2093
21. Kim, Y., Tewari, M., Pajerowski, J. D., Cai, S., Sen, S., Williams, J., Sirsi, S., Lutz, G., and Discher, D. E. (2009) Polymersome delivery of siRNA and antisense oligonucleotides J. Controlled Release 134, 132-140
22. Bolcato-Bellemin, A. L., Bonnet, M. E., Creusat, G., Erbacher, P., and Behr, J. P. (2007) Sticky overhangs enhance siRNA-mediated gene silencing Proc. Natl. Acad. Sci. U.S.A. 104, 16050-16055
23. Zimmermann, T. S., Lee, A. C., Akinc, A., Bramlage, B., Bumcrot, D., Fedoruk, M. N., Harborth, J., Heyes, J. A., Jeffs, L. B., John, M., Judge, A. D., Lam, K., McClintock, K., Nechev, L. V., Palmer, L. R., Racie, T., Rohl, I., Seiffert, S., Shanmugam, S., Sood, V., Soutschek, J., Toudjarska, I., Wheat, A. J., Yaworski, E., Zedalis, W., Koteliansky, V., Manoharan, M., Vornlocher, H. P., and MacLachlan, I. (2006) RNAi-mediated gene silencing in non-human primates Nature 441, 111-114
24. Fraley, A. W., Pons, B., Dalkara, D., Nullans, G., Behr, J. P., and Zuber, G. (2006) Cationic oligonucleotide-peptide conjugates with aggregating properties enter efficiently into cells while maintaining hybridization properties and enzymatic recognition J. Am. Chem. Soc. 128, 10763-10771
25. Creusat, G. and Zuber, G. (2008) Self-assembling polyethylenimine derivatives mediate efficient siRNA delivery in mammalian cells ChemBioChem 9, 2787-2789
26. Hendriks, J., Gensch, T., Hviid, L., van Der Horst, M. A., Hellingwerf, K. J., and van Thor, J. J. (2002) Transient exposure of hydrophobic surface in the photoactive yellow protein monitored with Nile Red Biophys. J. 82, 1632-1643
27. Ercelen, S., Zhang, X., Duportail, G., Grandfils, C., Desbrieres, J., Karaeva, S., Tikhonov, V., Mely, Y., and Babak, V. (2006) Physicochemical properties of low molecular weight alkylated chitosans: a new class of potential nonviral vectors for gene delivery Colloids Surf., B: Biointerfaces 51, 140-148
28. Rathinakumar, R., Walkenhorst, W. F., and Wimley, W. C. (2009) Broad-spectrum antimicrobial peptides by rational combinatorial design and high-throughput screening: the importance of interfacial activity J. Am. Chem. Soc. 131, 7609-7617
29. Kopatz, I., Remy, J. S., and Behr, J. P. (2004) A model for non-viral gene delivery: through syndecan adhesion molecules and powered by actin J. Gene Med. 6, 769-776
30. Verkman, A. S. (2002) Solute and macromolecule diffusion in cellular aqueous compartments Trends Biochem. Sci. 27, 27-33
31. Sonawane, N. D., Szoka, F. C., Jr., and Verkman, A. S. (2003) Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes J. Biol. Chem. 278, 44826-44831
32. Akinc, A., Thomas, M., Klibanov, A. M., and Langer, R. (2005) Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis J. Gene Med. 7, 657-663
33. Yang, S. and May, S. (2008) Release of cationic polymer-DNA complexes from the endosome: A theoretical investigation of the proton sponge hypothesis J. Chem. Phys. 129, 185105
34. Wightman, L., Kircheis, R., Rossler, V., Carotta, S., Ruzicka, R., Kursa, M., and Wagner, E. (2001) Different behavior of branched and linear polyethylenimine for gene delivery in vitro and in vivo J. Gene Med. 3, 362-372
35. Ogris, M., Steinlein, P., Kursa, M., Mechtler, K., Kircheis, R., and Wagner, E. (1998) The size of DNA/transferrin-PEI complexes is an important factor for gene expression in cultured cells Gene Ther. 5, 1425-1433
36. Williams, J. H., Sirsi, S. R., Latta, D. R., and Lutz, G. J. (2006) Induction of dystrophin expression by exon skipping in mdx mice following intramuscular injection of antisense oligonucleotides complexed with PEG-PEI copolymers Mol. Ther. 14, 88-96
37. Zuber, G., Dontenwill, M., and Behr, J. P. (2009) Synthetic viruslike particles for targeted gene delivery to alpha(v)beta(3) integrin-presenting endothelial cells Mol. Pharm. 6, 1544-1552
38. Courtete, J., Sibler, A. P., Zeder-Lutz, G., Dalkara, D., Oulad-Abdelghani, M., Zuber, G., and Weiss, E. (2007) Suppression of cervical carcinoma cell growth by intracytoplasmic codelivery of anti-oncoprotein E6 antibody and small interfering RNA Mol. Cancer Ther. 6, 1728-1735
39. Hobbs, S. K., Monsky, W. L., Yuan, F., Roberts, W. G., Griffith, L., Torchilin, V. P., and Jain, R. K. (1998) Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment Proc. Natl. Acad. Sci. U.S.A. 95, 4607-4612
40. Kyte, J. and Doolite, A. (1998) A simple method for displaying the hydropathy character of protein. J. Mol. Biol. 157, 105-132