Probing the in vitro mechanism of action of cationic lipid/DNA lipoplexes at a nanometric scale

Nucleic Acids Research

Volumn 39, Issue 4, 2011, Pages 1595-1609

  Le Bihan, Olivier ^a   Chèvre, Raphaël ^b,c   Mornet, Stéphane ^a   Garnier, Boris ^a   Pitard, Bruno ^b,c,d   Lambert, Olivier ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d IN CELL ART   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIS(GUANIDINIUM) TRIS (2 AMINOETHYL)AMINE CHOLESTEROL; DIOLEYLSUCCINYLPARAMOMYCIN; LIPID; LIPOPLEX; NANOPARTICLE; PLASMID DNA; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL INTERACTION; CONTROLLED STUDY; DISSOCIATION; DNA BINDING; DNA TRANSFER; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; LIPID DNA INTERACTION; LIPID MEMBRANE; MEMBRANE RUPTURE; MEMBRANE STRUCTURE; PRIORITY JOURNAL;

EID: 79952318104     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq921     Document Type: Article

References (57)

1. Felgner, P.L., Barenholz, Y., Behr, J.P., Cheng, S.H., Cullis, P., Huang, L., Jessee, J.A., Seymour, L., Szoka, F., Thierry, A.R. et al. (1997) Nomenclature for synthetic gene delivery systems. Hum. Gene Ther., 8, 511-512. (Pubitemid 27202042)
2. Barteau, B., Chevre, R., Letrou-Bonneval, E., Labas, R., Lambert, O. and Pitard, B. (2008) Physicochemical parameters of non-viral vectors that govern transfection efficiency. Curr. Gene Ther., 8, 313-323.
3. Khalil, I.A., Kogure, K., Akita, H. and Harashima, H. (2006) Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol. Rev., 58, 32-45.
4. Hoekstra, D., Rejman, J., Wasungu, L., Shi, F. and Zuhorn, I. (2007) Gene delivery by cationic lipids: in and out of an endosome. Biochem. Soc. Trans., 35, 68-71.
5. Midoux, P., Breuzard, G., Gomez, J.P. and Pichon, C. (2008) Polymer-based gene delivery: a current review on the uptake and intracellular trafficking of polyplexes. Curr. Gene Ther., 8, 335-352.
6. van der Aa, M.A.E.M., Mastrobattista, E., Oosting, R.S., Hennink, W.E., Koning, G.A. and Crommelin, D.J.A. (2006) The nuclear pore complex: the gateway to successful nonviral gene delivery. Pharm. Res., 23, 447-459.
7. Braun, S. (2008) Muscular gene transfer using nonviral vectors. Curr. Gene Ther., 8, 391-405.
8. Elouahabi, A. and Ruysschaert, J. (2005) Formation and intracellular trafficking of lipoplexes and polyplexes. Mol. Ther., 11, 336-347. (Pubitemid 40277310)
9. Godbey, W.T., Wu, K.K. and Mikos, A.G. (1999) Tracking the intracellular path of poly(ethylenimine)/DNA complexes for gene delivery. Proc. Natl Acad. Sci. USA, 96, 5177-5181. (Pubitemid 29214556)
10. Suh, J., Wirtz, D. and Hanes, J. (2003) Efficient active transport of gene nanocarriers to the cell nucleus. Proc. Natl Acad. Sci. USA, 100, 3878-3882. (Pubitemid 36418125)
11. Chen, H.H., Ho, Y., Jiang, X., Mao, H., Wang, T. and Leong, K.W. (2008) Quantitative comparison of intracellular unpacking kinetics of polyplexes by a model constructed from quantum dot-FRET. Mol. Ther., 16, 324-332. (Pubitemid 351168042)
12. Schneider, S., Lenz, D., Holzer, M., Palme, K. and Suss, R. (2010) Intracellular FRET analysis of lipid/DNA complexes using flow cytometry and fluorescence imaging techniques. J. Control Rel., 145, 289-296.
13. Sonawane, N.D., Szoka, F.C. and Verkman, A.S. (2003) Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes. J. Biol. Chem., 278, 44826-44831. (Pubitemid 37377241)
14. Felgner, P.L., Gadek, T.R., Holm, M., Roman, R., Chan, H.W., Wenz, M., Northrop, J.P., Ringold, G.M. and Danielsen, M. (1987) Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl Acad. Sci. USA, 84, 7413-7417.
15. Labat-Moleur, F., Steffan, A.M., Brisson, C., Perron, H., Feugeas, O., Furstenberger, P., Oberling, F., Brambilla, E. and Behr, J.P. (1996) An electron microscopy study into the mechanism of gene transfer with lipopolyamines. Gene Ther., 3, 1010-1017. (Pubitemid 26397476)
16. Zabner, J., Fasbender, A.J., Moninger, T., Poellinger, K.A. and Welsh, M.J. (1995) Cellular and molecular barriers to gene transfer by a cationic lipid. J. Biol. Chem., 270, 18997-19007.
17. Zhou, X. and Huang, L. (1994) DNA transfection mediated by cationic liposomes containing lipopolylysine: characterization and mechanism of action. Biochim. Biophys. Acta, 1189, 195-203. (Pubitemid 24042719)
18. Pitard, B., Oudrhiri, N., Vigneron, J.P., Hauchecorne, M., Aguerre, O., Toury, R., Airiau, M., Ramasawmy, R., Scherman, D., Crouzet, J. et al. (1999) Structural characteristics of supramolecular assemblies formed by guanidinium-cholesterol reagents for gene transfection. Proc. Natl Acad. Sci. USA, 96, 2621-2626. (Pubitemid 29148767)
19. Goncalves, C., Mennesson, E., Fuchs, R., Gorvel, J., Midoux, P. and Pichon, C. (2004) Macropinocytosis of polyplexes and recycling of plasmid via the clathrin-dependent pathway impair the transfection efficiency of human hepatocarcinoma cells. Mol. Ther., 10, 373-385. (Pubitemid 39117882)
20. Kopatz, I., Remy, J. and Behr, J. (2004) A model for non-viral gene delivery: through syndecan adhesion molecules and powered by actin. J. Gene Med., 6, 769-776. (Pubitemid 40228093)
21. Lappalainen, K., Miettinen, R., Kellokoski, J., Jaaskelainen, I. and Syrjanen, S. (1997) Intracellular distribution of oligonucleotides delivered by cationic liposomes: light and electron microscopic study. J. Histochem. Cytochem., 45, 265-274. (Pubitemid 27114496)
22. Akhtar, S., Hughes, M.D., Khan, A., Bibby, M., Hussain, M., Nawaz, Q., Double, J. and Sayyed, P. (2000) The delivery of antisense therapeutics. Adv. Drug Deliv. Rev., 44, 3-21.
23. Friend, D.S., Papahadjopoulos, D. and Debs, R.J. (1996) Endocytosis and intracellular processing accompanying transfection mediated by cationic liposomes. Biochim. Biophys. Acta, 1278, 41-50. (Pubitemid 26042269)
24. Thomas, M. and Klibanov, A.M. (2003) Conjugation to gold nanoparticles enhances polyethylenimine's transfer of plasmid DNA into mammalian cells. Proc. Natl Acad. Sci. USA, 100, 9138-9143. (Pubitemid 37033896)
25. Koynova, R., Tarahovsky, Y.S., Wang, L. and MacDonald, R.C. (2007) Lipoplex formulation of superior efficacy exhibits high surface activity and fusogenicity, and readily releases DNA. Biochim. Biophys. Acta, 1768, 375-386. (Pubitemid 46136190)
26. Vigneron, J.P., Oudrhiri, N., Fauquet, M., Vergely, L., Bradley, J.C., Basseville, M., Lehn, P. and Lehn, J.M. (1996) Guanidinium-cholesterol cationic lipids: efficient vectors for the transfection of eukaryotic cells. Proc. Natl Acad. Sci. USA, 93, 9682-9686. (Pubitemid 26296669)
27. Pitard, B., Oudrhiri, N., Lambert, O., Vivien, E., Masson, C., Wetzer, B., Hauchecorne, M., Scherman, D., Rigaud, J.L., Vigneron, J.P. et al. (2001) Sterically stabilized BGTC-based lipoplexes: structural features and gene transfection into the mouse airways in vivo. J. Gene Med., 3, 478-487. (Pubitemid 33684784)
28. Desigaux, L., Sainlos, M., Lambert, O., Chevre, R., Letrou-Bonneval, E., Vigneron, J., Lehn, P., Lehn, J. and Pitard, B. (2007) Self-assembled lamellar complexes of siRNA with lipidic aminoglycoside derivatives promote efficient siRNA delivery and interference. Proc. Natl Acad. Sci. USA, 104, 16534-16539. (Pubitemid 350211053)
29. Pitard, B., Pollard, H., Agbulut, O., Lambert, O., Vilquin, J., Cherel, Y., Abadie, J., Samuel, J., Rigaud, J., Menoret, S. et al. (2002) A nonionic amphiphile agent promotes gene delivery in vivo to skeletal and cardiac muscles. Hum. Gene Ther., 13, 1767-1775. (Pubitemid 35191750)
30. Letrou-Bonneval, E., Chevre, R., Lambert, O., Costet, P., Andre, C., Tellier, C. and Pitard, B. (2008) Galactosylated multimodular lipoplexes for specific gene transfer into primary hepatocytes. J. Gene Med., 10, 1198-1209.
31. Massart, R. (1981) Preparation of aqueous magnetic liquids in alkaline and acidic media. IEEE Trans. Magn., 17, 1244-1245.
32. Stober, W., Fink, A. and Bohn, E. (1968) Controlled growth of monodisperse silica spheres in the micron size range. J. Colloid Int. Sci., 26, 62-69.
33. Mornet, S., Lambert, O., Duguet, E. and Brisson, A. (2005) The formation of supported lipid bilayers on silica nanoparticles revealed by cryoelectron microscopy. Nano Lett., 5, 281-285. (Pubitemid 40308285)
34. Trepout, S., Mornet, S., Benabdelhak, H., Ducruix, A., Brisson, A.R. and Lambert, O. (2007) Membrane protein selectively oriented on solid support and reconstituted into a lipid membrane. Langmuir, 23, 2647-2654. (Pubitemid 46383683)
35. Kneuer, C., Sameti, M., Haltner, E.G., Schiestel, T., Schirra, H., Schmidt, H. and Lehr, C.M. (2000) Silica nanoparticles modified with aminosilanes as carriers for plasmid DNA. Int. J. Pharm., 196, 257-261. (Pubitemid 30105756)
36. Ravi Kumar, M.N.V., Sameti, M., Mohapatra, S.S., Kong, X., Lockey, R.F., Bakowsky, U., Lindenblatt, G., Schmidt, H. and Lehr, C.M. (2004) Cationic silica nanoparticles as gene carriers: synthesis, characterization and transfection efficiency in vitro and in vivo. J. Nanosci. Nanotechnol., 4, 876-881.
37. Paulson, J.R. and Laemmli, U.K. (1977) The structure of histone-depleted metaphase chromosomes. Cell, 12, 817-828.
38. Pichon, C., Goncalves, C. and Midoux, P. (2001) Histidine-rich peptides and polymers for nucleic acids delivery. Adv. Drug Deliv. Rev., 53, 75-94. (Pubitemid 33152834)
39. Gemeinhart, R.A., Luo, D. and Saltzman, W.M. (2005) Cellular fate of a modular DNA delivery system mediated by silica nanoparticles. Biotechnol. Prog., 21, 532-537. (Pubitemid 40466426)
40. Turek, J., Dubertret, C., Jaslin, G., Antonakis, K., Scherman, D. and Pitard, B. (2000) Formulations which increase the size of lipoplexes prevent serum-associated inhibition of transfection. J. Gene Med., 2, 32-40.
41. Xu, Y. and Szoka, F.C. (1996) Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection. Biochemistry, 35, 5616-5623. (Pubitemid 26143656)
42. Ross, G.F., Bruno, M.D., Uyeda, M., Suzuki, K., Nagao, K., Whitsett, J.A. and Korfhagen, T.R. (1998) Enhanced reporter gene expression in cells transfected in the presence of DMI-2, an acid nuclease inhibitor. Gene Ther., 5, 1244-1250. (Pubitemid 28448433)
43. Wattiaux, R., Laurent, N., Wattiaux-De Coninck, S. and Jadot, M. (2000) Endosomes, lysosomes: their implication in gene transfer. Adv. Drug Deliv. Rev., 41, 201-208. (Pubitemid 30122959)
44. Lechardeur, D., Verkman, A.S. and Lukacs, G.L. (2005) Intracellular routing of plasmid DNA during non-viral gene transfer. Adv. Drug Deliv. Rev., 57, 755-767. (Pubitemid 40332601)
45. Varga, C.M., Tedford, N.C., Thomas, M., Klibanov, A.M., Griffith, L.G. and Lauffenburger, D.A. (2005) Quantitative comparison of polyethylenimine formulations and adenoviral vectors in terms of intracellular gene delivery processes. Gene Ther., 12, 1023-1032. (Pubitemid 40946144)
46. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787. (Pubitemid 27181245)
47. Cohen, R.N., van der Aa, M.A.E.M., Macaraeg, N., Lee, A.P. and Szoka, F.C. (2009) Quantification of plasmid DNA copies in the nucleus after lipoplex and polyplex transfection. J. Control. Release, 135, 166-174.
48. Capecchi, M.R. (1980) High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell, 22, 479-488. (Pubitemid 11199905)
49. Ochiai, H., Fujimuro, M., Yokosawa, H., Harashima, H. and Kamiya, H. (2007) Transient activation of transgene expression by hydrodynamics-based injection may cause rapid decrease in plasmid DNA expression. Gene Ther., 14, 1152-1159. (Pubitemid 47086745)
50. Wrobel, I. and Collins, D. (1995) Fusion of cationic liposomes with mammalian cells occurs after endocytosis. Biochim. Biophys. Acta, 1235, 296-304.
51. Duzgunes, N., Goldstein, J.A., Friend, D.S. and Felgner, P.L. (1989) Fusion of liposomes containing a novel cationic lipid, N-[2, 3-(dioleyloxy)propyl]-N, N, N-trimethylammonium: induction by multivalent anions and asymmetric fusion with acidic phospholipid vesicles. Biochemistry, 28, 9179-9184. (Pubitemid 19283488)
52. Hafez, I.M., Maurer, N. and Cullis, P.R. (2001) On the mechanism whereby cationic lipids promote intracellular delivery of polynucleic acids. Gene Ther., 8, 1188-1196. (Pubitemid 32776393)
53. Stratton, C.J. (1978) The ultrastructure of multilamellar bodies and surfactant in the human lung. Cell Tissue Res., 193, 219-229. (Pubitemid 9028657)
54. Weaver, T.E., Na, C. and Stahlman, M. (2002) Biogenesis of lamellar bodies, lysosome-related organelles involved in storage and secretion of pulmonary surfactant. Semin. Cell Dev. Biol., 13, 263-270. (Pubitemid 35304511)
55. Kolleck, I., Guthmann, F., Ladhoff, A., Tandon, N.N., Schlame, M. and Rustow, B. (2002) Cellular cholesterol stimulates acute uptake of palmitate by redistribution of fatty acid translocase in type II pneumocytes. Biochemistry, 41, 6369-6375. (Pubitemid 34526001)
56. Yang, Z., Zhu, J., Sriadibhatla, S., Gebhart, C., Alakhov, V. and Kabanov, A. (2005) Promoter- and strain-selective enhancement of gene expression in a mouse skeletal muscle by a polymer excipient Pluronic P85. J. Control. Release, 108, 496-512. (Pubitemid 41608680)
57. Wang, L., Dean, D.A. and Macdonald, R.C. (2005) Effect of vinblastine on transfection: influence of cell types, cationic lipids and promoters. Curr. Drug Deliv., 2, 93-96. (Pubitemid 40590924)