Synthetic viruslike particles for targeted gene delivery to αvβ3 integrin-presenting endothelial cells

Molecular Pharmaceutics

Volumn 6, Issue 5, 2009, Pages 1544-1552

  Zuber, Guy ^a   Dontenwill, Monique ^a   Behr, Jean Paul ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

DNA condensation; Gene delivery; Integrin; RGD peptide; Synthetic virus; Transfection

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; CHLOROQUINE; DIOLEOYLPHOSPHATIDYLETHANOLAMINE; INTEGRIN; LIGAND; LIPID; LUCIFERASE; NANOPARTICLE; PLASMID DNA; VITRONECTIN RECEPTOR;

AGAR GEL ELECTROPHORESIS; AMINO ACID SUBSTITUTION; BINDING AFFINITY; CANCER CELL CULTURE; CANCER GENE THERAPY; COMPLEX FORMATION; CONFERENCE PAPER; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG CONJUGATION; ENDOTHELIUM CELL; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR INTERACTION; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REPORTER GENE; SYNTHESIS; SYNTHETIC VIRUS; TRANSMISSION ELECTRON MICROSCOPY; VIRUS LIKE AGENT;

ANTIGEN PRESENTATION; DNA, RECOMBINANT; ENDOTHELIAL CELLS; GENE THERAPY; GENETIC VECTORS; HUMANS; INTEGRIN ALPHAVBETA3; KB CELLS; LIGANDS; MICROSCOPY, ELECTRON, TRANSMISSION; NANOPARTICLES; NANOTECHNOLOGY; OLIGOPEPTIDES; VIRUSES;

EID: 70350077962     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp900105q     Document Type: Conference Paper

References (47)

1. Pitard, B.; Oudrhiri, N.; Vigneron, J. P.; Hauchecorne, M.; Aguerre, O.; Toury, R.; Airiau, M.; Ramasawmy, R.; Scherman, D.; Crouzet, J.; Lehn, J. M.; Lehn, P. Structural characteristics of supramolecular assemblies formed by guanidinium-cholesterol reagents for gene transfection. Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (6), 2621-2626. (Pubitemid 29148767)
2. Kopatz, I.; Remy, J. S.; Behr, J. P. A model for non-viral gene delivery: through syndecan adhesion molecules and powered by actin. J. Gene Med. 2004, 6 (7), 769-776.
3. Payne, C. K.; Jones, A. S.; Chen, C.; Zhuang, X. Internalization and trafficking of cell surface proteoglycans and proteoglycan-binding ligands. Traffic 2007, 8 (4), 389-401. (Pubitemid 46421621)
4. Zou, S. M.; Erbacher, P.; Remy, J. S.; Behr, J. P. Systemic linear polyethylenimine (L-PEI)-mediated gene delivery in the mouse. J. Gene Med. 2000, 2 (2), 128-134.
5. Lemkine, G. F.; Mantero, S.; Migne, C.; Raji, A.; Goula, D.; Normandie, P.; Levi, G.; Demeneix, B. A. Preferential transfection of adult mouse neural stem cells and their immediate progeny in vivo with polyethylenimine. Mol. Cell. Neurosci. 2002, 165-174.
6. Ohana, P.; Gofrit, O.; Ayesh, S.; Al-Sharef, W.; Mizrahi, A.; Birman, T.; Schneider, T.; Matouk, I.; de Groot, N.; Tavdy, E.; Sidi, A. A.; Hochberg, A. Regulatory sequences of the H19 gene in DNA-based therapy of bladder cancer. Gene Ther. Mol. Biol. 2004, 8, 181-192.
7. Brower, V. Tumor angiogenesis - new drugs on the block. Nat. Biotechnol. 1999, 17 (10), 963-968. (Pubitemid 29474850)
8. Medarova, Z.; Pham, W.; Farrar, C.; Petkova, V.; Moore, A. In vivo imaging of siRNA delivery and silencing in tumors. Nat. Med. 2007, 13 (3), 372-377. (Pubitemid 46376679)
9. Hood, J. D.; Bednarski, M.; Frausto, R.; Guccione, S.; Reisfeld, R. A.; Xiang, R.; Cheresh, D. A. Tumor regression by targeted gene delivery to the neovasculature. Science 2002, 296 (5577), 2404-2407. (Pubitemid 34734217)
10. Kircheis, R.; Blessing, T.; Brunner, S.; Wightman, L.; Wagner, E. Tumor targeting with surface-shielded ligand - polycation DNA complexes. J. Controlled Release 2001, 72 (1-3), 165-170. (Pubitemid 32522354)
11. Barron, L. G.; Meyer, K. B.; Szoka, F. C., Jr. Effects of complement depletion on the pharmacokinetics and gene delivery mediated by cationic lipid-DNA complexes. Hum. Gene Ther. 1998, 9 (3), 315-323.
12. Chollet, P.; Favrot, M. C.; Hurbin, A.; Coll, J. L. Side-effects of a systemic injection of linear polyethylenimine-DNA complexes. J. Gene Med. 2002, 4 (1), 84-91.
13. Oupicky, D.; Parker, A. L.; Seymour, L. W. Laterally stabilized complexes of DNA with linear reducible polycations: strategy for triggered intracellular activation of DNA delivery vectors. J. Am. Chem. Soc. 2002, 124 (1), 8-9.
14. Pun, S. H.; Bellocq, N. C.; Liu, A.; Jensen, G.; Machemer, T.; Quijano, E.; Schluep, T.; Wen, S.; Engler, H.; Heidel, J.; Davis, M. E. Cyclodextrin-modified polyethylenimine polymers for gene delivery. Bioconjugate Chem. 2004, 15 (4), 831-840. (Pubitemid 38981958)
15. Kunath, K.; Merdan, T.; Hegener, O.; Haberlein, H.; Kissel, T. Integrin targeting using RGD-PEI conjugates for in vitro gene transfer. J. Gene Med. 2003, 5 (7), 588-599. (Pubitemid 40310402)
16. Chen, Y.; Sen, J.; Bathula, S. R.; Yang, Q.; Fittipaldi, R.; Huang, L. Novel Cationic Lipid That Delivers siRNA and Enhances Therapeutic Effect in Lung Cancer Cells. Mol. Pharmaceutics 2009, 6, 696-705.
17. Chittimalla, C.; Zammut-Italiano, L.; Zuber, G.; Behr, J. P. Monomolecular DNA nanoparticles for intravenous delivery of genes. J. Am. Chem. Soc. 2005, 127 (32), 11436-11441. (Pubitemid 41176904)
18. Dauty, E.; Remy, J. S.; Blessing, T.; Behr, J. P. Dimerizable Cationic Detergents with a Low cmc Condense Plasmid DNA into Nanometric Particles and Transfect Cells in Culture. J. Am. Chem. Soc. 2001, 123 (38), 9227-9234.
19. Blessing, T.; Remy, J.-S.; Behr, J.-P. Template Oligomerization of DNA-Bound Cations Produces Calibrated Nanometric Particles. J. Am. Chem. Soc. 1998, 120 (33), 8519-8520.
20. Dauty, E.; Remy, J.-S.; Zuber, G.; Behr, J.-P. Intracellular delivery of nanometric DNA particles via the folate receptor. Bioconjugate Chem. 2002, 831-839.
21. Zuber, G.; Zammut-Italiano, L.; Dauty, E.; Behr, J. P. Targeted gene delivery to cancer cells: Directed assembly of nanometric DNA particles coated with folic acid. Angew. Chem., Int. Ed. 2003, 42 (23), 2666-2669.
22. Zuber, G.; Muller, C. D.; Behr, J. P. Targeted gene delivery to cancer cells with nanometric DNA particles enveloped with folic acid using a polymerisable anchor. Technol. Cancer Res. Treat. 2005, 4 (6), 637-643.
23. Mishra, S.; Webster, P.; Davis, M. E. PEGylation significantly affects cellular uptake and intracellular trafficking of non-viral gene delivery particles. Eur. J. Cell Biol. 2004, 83 (3), 97-111.
24. Conner, S. D.; Schmid, S. L. Regulated portals of entry into the cell. Nature 2003, 422 (6927), 37-44.
25. Rejman, J.; Conese, M.; Hoekstra, D. Gene transfer by means of lipo- and polyplexes: role of clathrin and caveolae-mediated endocytosis. J. Liposome Res. 2006, 16 (3), 237-247. (Pubitemid 44358997)
26. von Gersdorff, K.; Sanders, N. N.; Vandenbroucke, R.; De Smedt, S. C.; Wagner, E.; Ogris, M. The Internalization Route Resulting in Successful Gene Expression Depends on both Cell Line and Polyethylenimine Polyplex Type. Mol. Ther. 2006, 14 (5), 745-753. (Pubitemid 44480760)
27. Luhmann, T.; Rimann, M.; Bittermann, A. G.; Hall, H. Cellular uptake and intracellular pathways of PLL-g-PEG-DNA nanoparticles. Bioconjugate Chem. 2008, 19 (9), 1907-1916.
28. Sandoval, R. M.; Kennedy, M. D.; Low, P. S.; Molitoris, B. A. Uptake and trafficking of fluorescent conjugates of folic acid in intact kidney determined using intravital two-photon microscopy. Am. J. Physiol. 2004, 287 (2), C517-C526.
29. O'Donnell, V.; LaRocco, M.; Baxt, B. Heparan sulfate-binding foot-and-mouth disease virus enters cells via caveola-mediated endocytosis. J. Virol. 2008, 82 (18), 9075-9085.
30. Hoekstra, D.; Rejman, J.; Wasungu, L.; Shi, F.; Zuhorn, I. Gene delivery by cationic lipids: in and out of an endosome. Biochem. Soc. Trans. 2007, 35 (Part 1), 68-71. (Pubitemid 46271811)
31. Temming, K.; Schiffelers, R. M.; Molema, G.; Kok, R. J. RGD-based strategies for selective delivery of therapeutics and imaging agents to the tumour vasculature. Drug Resist. Updates 2005, 8 (6), 381-402.
32. Hafez, I. M.; Maurer, N.; Cullis, P. R. On the mechanism whereby cationic lipids promote intracellular delivery of polynucleic acids. Gene Ther. 2001, 8 (15), 1188-1196.
33. Erbacher, P.; Roche, A. C.; Monsigny, M.; Midoux, P. Putative role of chloroquine in gene transfer into a human hepatoma cell line by DNA/lactosylated polylysine complexes. Exp. Cell Res. 1996, 225 (1), 186-194. (Pubitemid 26158468)
34. Feuston, B. P.; Culberson, J. C.; Duggan, M. E.; Hartman, G. D.; Leu, C. T.; Rodan, S. B. Binding model for nonpeptide antagonists of alpha(v)beta(3) integrin. J. Med. Chem. 2002, 45 (26), 5640-5648.
35. Goodman, S. L.; Holzemann, G.; Sulyok, G. A.; Kessler, H. Nanomolar small molecule inhibitors for alphav(beta)6, alphav-(beta)5, and alphav(beta)3 integrins. J. Med. Chem. 2002, 45 (5), 1045-1051.
36. 3 antagonists. J. Am. Chem. Soc. 1996, 118, 7461-7472.
37. Oba, M.; Fukushima, S.; Kanayama, N.; Aoyagi, K.; Nishiyama, N.; Koyama, H.; Kataoka, K. Cyclic RGD peptide-conjugated polyplex micelles as a targetable gene delivery system directed to cells possessing alphavbeta3 and alphavbeta5 integrins. Bioconjugate Chem. 2007, 18 (5), 1415-1423.
38. Marchi-Artzner, V.; Lorz, B.; Hellerer, U.; Kantlehner, M.; Kessler, H.; Sackmann, E. Selective adhesion of endothelial cells to artificial membranes with a synthetic RGD-lipopeptide. Chemistry 2001, 7 (5), 1095-1101.
39. Ishikawa, A.; Zhou, Y. M.; Kambe, N.; Nakayama, Y. Enhancement of star vector-based gene delivery to endothelial cells by addition of RGD-peptide. Bioconjuguate Chem. 2008, 19 (2), 558-561. (Pubitemid 351294929)
40. Kok, R. J.; Schraa, A. J.; Bos, E. J.; Moorlag, H. E.; Asgeirsdottir, S. A.; Everts, M.; Meijer, D. K.; Molema, G. Preparation and functional evaluation of RGD-modified proteins as alpha(v)beta(3) integrin directed therapeutics. Bioconjugate Chem. 2002, 13 (1), 128-135.
41. Xiong, J. P.; Stehle, T.; Zhang, R.; Joachimiak, A.; Frech, M.; Goodman, S. L.; Arnaout, M. A. Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand. Science 2002, 296 (5565), 151-155.
42. Aumailley, M.; Gurrath, M.; Muller, G.; Calvete, J.; Timpl, R.; Kessler, H. Arg-Gly-Asp constrained within cyclic pentapeptides. Strong and selective inhibitors of cell adhesion to vitronectin and laminin fragment P1. FEBS Lett. 1991, 291 (1), 50-54.
43. Schraa, A. J.; Kok, R. J.; Berendsen, A. D.; Moorlag, H. E.; Bos, E. J.; Meijer, D. K.; de Leij, L. F.; Molema, G. Endothelial cells internalize and degrade RGD-modified proteins developed for tumor vasculature targeting. J. Controlled Release 2002, 83 (2), 241-251. (Pubitemid 35279469)
44. Allman, R.; Cowburn, P.; Mason, M. In vitro and in vivo effects of a cyclic peptide with affinity for the alpha(nu)beta3 integrin in human melanoma cells. Eur. J. Cancer 2000, 36 (3), 410-422. (Pubitemid 30116739)
45. Zhang, X.; Sawyer, G. J.; Dong, X.; Qiu, Y.; Collins, L.; Fabre, J. W. The in vivo use of chloroquine to promote non-viral gene delivery to the liver via the portal vein and bile duct. J. Gene Med. 2003, 5 (3), 209-218.
46. Riddles, P. W.; Blakeley, R. L.; Zerner, B. Ellman's reagent: 5,5′-dithiobis(2-nitrobenzoic acid) - a reexamination. Anal. Biochem. 1979, 94, 75-81. (Pubitemid 9170207)
47. Figure S3 in the Supporting Information confirms that cRAD motifs protect the particles from unspecific binding to HUVEC.