Lipoplex formulation of superior efficacy exhibits high surface activity and fusogenicity, and readily releases DNA

Biochimica et Biophysica Acta - Biomembranes

Volumn 1768, Issue 2, 2007, Pages 375-386

  Koynova, Rumiana ^a   Tarahovsky, Yury S ^a,b   Wang, Li ^a   MacDonald, Robert C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

Author keywords

Cationic lipid; DNA unbinding; Gene therapy; Lipofection; Membrane fusion; Surface tension

Indexed keywords

DILAUROYLETHYLPHOSPHATIDYLCHOLINE; DIOLEOYLETHYLPHOSPHATIDYLCHOLINE; DNA; LIPOPLEX; PHOSPHATIDYLCHOLINE; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DNA TRANSFER; DRUG FORMULATION; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; UMBILICAL ARTERY;

CELL MEMBRANE; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; DNA; ENDOPLASMIC RETICULUM; ENDOTHELIUM, VASCULAR; HUMANS; LIPOSOMES; MICROSCOPY, ELECTRON; MITOCHONDRIA; OLEIC ACIDS; PHOSPHATIDYLCHOLINES; TRANSFECTION; UMBILICAL ARTERIES;

EID: 33846390694     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2006.10.016     Document Type: Article

References (65)

1. Tachibana R., Harashima H., Ide N., Ukitsu S., Ohta Y., Suzuki N., Kikuchi H., Shinohara Y., and Kiwada H. Quantitative analysis of correlation between number of nuclear plasmids and gene expression activity after transfection with cationic liposomes. Pharm. Res. 19 (2002) 377-381
2. Pozharski E., and MacDonald R.C. Lipoplex thermodynamics: determination of DNA-cationic lipoid interaction energies. Biophys. J. 85 (2003) 3969-3978
3. Xu Y.H., and Szoka F.C. Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection. Biochemistry 35 (1996) 5616-5623
4. Zelphati O., and Szoka F.C. Mechanism of oligonucleotide release from cationic liposomes. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 11493-11498
5. Szoka F.C., Xu Y.H., and Zelphati O. How are nucleic acids released in cells from cationic lipid-nucleic acid complexes?. Adv. Drug Delivery Rev. 24 (1997) 291
6. Bhattacharya S., and Mandal S.S. Evidence of interlipidic ion-pairing in anion-induced DNA release from cationic amphiphile-DNA complexes, mechanistic implications in transfection. Biochemistry 37 (1998) 7764-7777
7. Harvie P., Wong F.M.P., and Bally M.B. Characterization of lipid DNA interactions. I. Destabilization of bound lipids and DNA dissociation. Biophys. J. 75 (1998) 1040-1051
8. Wrobel I., and Collins D. Fusion of cationic liposomes with mammalian-cells occurs after endocytosis. Biochim. Biophys. Acta, Biomembr. 1235 (1995) 296-304
9. Noguchi A., Furuno T., Kawaura C., and Nakanishi M. Membrane fusion plays an important role in gene transfection mediated by cationic liposomes. FEBS Lett. 433 (1998) 169-173
10. Nakanishi M., and Noguchi A. Confocal and probe microscopy to study gene transfection mediated by cationic liposomes with a cationic cholesterol derivative. Adv. Drug Delivery Rev. 52 (2001) 197-207
11. Wang L., and MacDonald R.C. New strategy for transfection: mixtures of medium-chain and long-chain cationic lipids synergistically enhance transfection. Gene Ther. 11 (2004) 1358-1362
12. Teifel M., Heine L.T., Milbredt S., and Friedl P. Optimization of transfection of human endothelial cells. Endothelium (New York) 5 (1997) 21-35
13. Wang L., Koynova R., Parikh H., and MacDonald R.C. Transfection Activity of Binary Mixtures of Cationic O-Substituted Phosphatidylcholine Derivatives: The Hydrophobic Core Strongly Modulates Their Physical Properties and DNA Delivery Efficacy. Biophys. J. 91 (2006) 3692-3706
14. MacDonald R.C., Rakhmanova V.A., Choi K.L., Rosenzweig H.S., and Lahiri M.K. O-Ethylphosphatidylcholine: a metabolizable cationic phospholipid which is a serum-compatible DNA transfection agent. J. Pharm. Sci. 88 (1999) 896-904
15. Koynova R., and MacDonald R.C. Mixtures of cationic lipid o-ethylphosphatidylcholine with membrane lipids and DNA: phase diagrams. Biophys. J. 85 (2003) 2449-2465
16. MacDonald R.C., and Simon S.A. Lipid monolayer states and their relationships to bilayers. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 4089-4093
17. MacDonald R.C., Gorbonos A., Mornsen M.M., and Brockman H.L. Surface properties of dioleoyl-sn-glycerol-3-ethylphosphocholine, a cationic phosphatidylcholine transfection agent, alone and in combination with lipids or DNA. Langmuir 22 (2006) 2770-2779
18. Qiu R.Z., and MacDonald R.C. A metastable state of high surface-activity produced by sonication of phospholipids. Biochim. Biophys. Acta, Biomembr. 1191 (1994) 343-353
19. Jordanova A., Lalchev Z., and Tenchov B. Formation of monolayers and bilayer foam films from lamellar, inverted hexagonal and cubic lipid phases. Eur. Biophys. J. 31 (2003) 626-632
20. Pozharski E., and MacDonald R.C. Analysis of the structure and composition of individual lipoplex particles by flow fluorometry. Anal. Biochem. 341 (2005) 230-240
21. Pozharski E., and MacDonald R.C. Single lipoplex study of cationic lipid-DNA self-assembled complex: flow cytometric approach. Biophys. J. 80 (2001) 427A
22. MacDonald R.C., Ashley G.W., Shida M.M., Rakhmanova V.A., Tarahovsky Y.S., Pantazatos D.P., Kennedy M.T., Pozharski E.V., Baker K.A., Jones R.D., Rosenzweig H.S., Choi K.L., Qiu R.Z., and McIntosh T.J. Physical and biological properties of cationic triesters of phosphatidylcholine. Biophys. J. 77 (1999) 2612-2629
23. Ouedraogo G., Morliere P., Maziere C., Maziere J.C., and Santus R. Alteration of the endocytotic pathway by photosensitization with fluoroquinolones. Photochem. Photobiol. 72 (2000) 458-463
24. Traore M., Sun R.J., Fawzi-Grancher S., Dumas D., Qing X., Santus R., Stoltz J.F., and Muller S. Kinetics of the endocytotic pathway of low density lipoprotein (LDL) in human endothelial cells line under shear stress: an in vitro confocal microscopy study. Clin. Hemorheol. Microcirc. 33 (2005) 243-251
25. Mosmann T. Rapid colorimetric assay for cellular growth and survival-Application to proliferation and cyto-toxicity assays. J. Immunol. Methods 65 (1983) 55-63
26. Koynova R., and MacDonald R.C. Cationic o-ethylphosphatidylcholines and their lipoplexes: phase behavior aspects, structural organization and morphology. Biochim. Biophys. Acta, Biomembr. 1613 (2003) 39-48
27. Koynova R., and MacDonald R.C. Columnar DNA superlattices in lamellar o-ethylphosphatidylcholine lipoplexes: mechanism of the gel-liquid crystalline lipid phase transition. Nano Lett. 4 (2004) 1475-1479
28. Koynova R., Wang L., and MacDonald R.C. An intracellular lamellar-nonlamellar phase transition rationalizes the superior performance of some cationic lipid transfection agents. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 14373-14378
29. Rakhmanova V.A., McIntosh T.J., and MacDonald R.C. Effects of dioleoylphosphatidylethanolamine on the activity and structure of o-alkyl phosphatidylcholine-DNA transfection complexes. Cell. Mol. Biol. Lett. 5 (2000) 51-65
30. Lasic D.D., Strey H., Stuart M.C.A., Podgornik R., and Frederik P.M. The structure of DNA-liposome complexes. J. Am. Chem. Soc. 119 (1997) 832-833
31. Radler J.O., Koltover I., Salditt T., and Safinya C.R. Structure of DNA-cationic liposome complexes: DNA intercalation in multilamellar membranes in distinct interhelical packing regimes. Science 275 (1997) 810-814
32. Koltover I., Salditt T., and Safinya C.R. Phase diagram, stability, and overcharging of lamellar cationic lipid-DNA self-assembled complexes. Biophys. J. 77 (1999) 915-924
33. Daum G. Lipids of mitochondria. Biochim. Biophys. Acta 822 (1985) 1-42
34. Siakotos A.N., Rouser G., and Fleische S. Isolation of highly purified human and bovine brain endothelial cells and nuclei and their phospholipid composition. Lipids 4 (1969) 234-239
35. Tarahovsky Y.S., Koynova R., and MacDonald R.C. DNA release from lipoplexes by anionic lipids: correlation with lipid mesomorphism, interfacial curvature, and membrane fusion. Biophys. J. 87 (2004) 1054-1064
36. Gennis R.B. Biomembranes. Molecular Structure and Function. (1989), Springer-Verlag, New York
37. Friend D.S., Papahadjopoulos D., and Debs R.J. Endocytosis and intracellular processing accompanying transfection mediated by cationic liposomes. Biochim. Biophys. Acta, Biomembr. 1278 (1996) 41-50
38. Zabner J., Fasbender A.J., Moninger T., Poellinger K.A., and Welsh M.J. Cellular and molecular barriers to gene-transfer by a cationic lipid. J. Biol. Chem. 270 (1995) 18997-19007
39. Zhou X.H., and Huang L. DNA transfection mediated by cationic liposomes containing lipopolylysine-Characterization and mechanism of action. Biochim. Biophys. Acta, Biomembr. 1189 (1994) 195-203
40. Koynova R., Wang L., Tarahovsky Y., and MacDonald R.C. Lipid phase control of DNA delivery. Bioconjugate Chem. 16 (2005) 1335-1339
41. Boukhnikachvili T., Aguerre-Chariol O., Airiau M., Lesieur S., Ollivon M., and Vacus J. Structure of in-serum transfecting DNA-cationic lipid complexes. FEBS Lett. 409 (1997) 188-194
42. Marsh D. Handbook of Lipid Bilayers (1990), CRC Press
43. Ashley G.W., Shida M.M., Qiu R., Lahiri M.K., Levisay P.C., Jones R.D., Baker K.A., and MacDonald R.C. Phosphatidylcholinium compounds: a new class of cationic phospholipids with transfection activin and unusual physical properties (Abstract). Biophys. J. 70 (1996) 88A
44. Pantazatos D.P., and MacDonald R.C. Directly observed membrane fusion between oppositely charged phospholipid bilayers. J. Membr. Biol. 170 (1999) 27-38
45. Stegmann T., and Legendre J.Y. Gene transfer mediated by cationic lipids: lack of a correlation between lipid mixing and transfection1. Biochim. Biophys. Acta, Biomembr. 1325 (1997) 71-79
46. Mui B., Ahkong Q.F., Chow L., and Hope M.J. Membrane perturbation and the mechanism of lipid-mediated transfer of DNA into cells. Biochim. Biophys. Acta, Biomembr. 1467 (2000) 281-292
47. Pires P., Simoes S., Nir S., Gaspar R., Duzgunes N., and de Lima M.C.P. Interaction of cationic liposomes and their DNA complexes with monocytic leukemia cells. Biochim. Biophys. Acta, Biomembr. 1418 (1999) 71-84
48. Leventis R., and Silvius J.R. Interactions of mammalian-cells with lipid dispersions containing novel metabolizable cationic amphiphiles. Biochim. Biophys. Acta 1023 (1990) 124-132
49. Harvie P., Wong F.M.P., and Bally M.B. Characterization of lipid DNA interactions. I. Destabilization of bound lipids and DNA dissociation. Biophys. J. 75 (1998) 1040-1051
50. Papahadjopoulos D., Nir S., and Duzgunes N. Molecular mechanisms of calcium-induced membrane-fusion. J. Bioenerg. Biomembr. 22 (1990) 157-179
51. Bergstrom M. Thermodynamics of unilamellar vesicles: influence of mixing on the curvature free energy of a vesicle bilayer. J. Colloid Interface Sci. 240 (2001) 294-306
52. Lei G.H., and MacDonald R.C. Lipid bilayer vesicle fusion: intermediates captured by high-speed microfluorescence spectroscopy. Biophys. J. 85 (2003) 1585-1599
53. Pantazatos D.P., Pantazatos S.P., and MacDonald R.C. Bilayer mixing, fusion, and lysis following the interaction of populations of cationic and anionic phospholipid bilayer vesicles. J. Membr. Biol. 194 (2003) 129-139
54. Pantazatos S.P., and MacDonald R.C. Real-time observation of lipoplex formation and interaction with anionic bilayer vesicles. J. Membr. Biol. 191 (2003) 99-112
55. Smith R., and Tanford C. Critical micelle concentration of l-alpha-dipalmitoylphosphatidylcholine in water and water/methanol solutions. J. Mol. Biol. 67 (1972) 75-83
56. Koynova R., and MacDonald R.C. Lipid transfer between cationic vesicles and lipid-DNA lipoplexes. Effect of Serum. Biochim. Biophys. Acta, Biomembr. 1714 (2005) 63-70
57. Tarahovsky Y.S., Arsenault A.L., MacDonald R.C., McIntosh T.J., and Epand R.M. Electrostatic control of phospholipid polymorphism. Biophys. J. 79 (2000) 3193-3200
58. Lewis R.N.A.H., and McElhaney R.N. Surface charge markedly attenuates the nonlamellar phase-forming propensities of lipid bilayer membranes: calorimetric and P-31-nuclear magnetic resonance studies of mixtures of cationic, anionic, and zwitterionic lipids. Biophys. J. 79 (2000) 1455-1464
59. Ellens H., Siegel D.P., Alford D., Yeagle P.L., Boni L., Lis L.J., Quinn P.J., and Bentz J. Membrane-fusion and inverted phases. Biochemistry 28 (1989) 3692-3703
60. Siegel D.P., and Epand R.M. The mechanism of lamellar-to-inverted hexagonal phase transitions in phosphatidylethanolamine: implications for membrane fusion mechanisms. Biophys. J. 73 (1997) 3089-3111
61. Tarahovsky Y., Koynova R., and MacDonald R.C. Efficiency of anionic lipids to release DNA from lipoplexes correlates with the interfacial curvature of the mesomorphic phases of cationic/anionic lipid mixtures. Biophys. J. 86 (2004) 37A
62. Bally M.B., Harvie P., Wong F.M.P., Kong S., Wasan E.K., and Reimer D.L. Biological barriers to cellular delivery of lipid-based DNA carriers. Adv. Drug Delivery Rev. 38 (1999) 291-315
63. Lechardeur D., Sohn K.J., Haardt M., Joshi P.B., Monck M., Graham R.W., Beatty B., Squire J., O'Brodovich H., and Lukacs G.L. Metabolic instability of plasmid DNA in the cytosol: a potential barrier to gene transfer. Gene Ther. 6 (1999) 482-497
64. Hovius R., Thijssen J., Vanderlinden P., Nicolay K., and Dekruijff B. Phospholipid asymmetry of the outer-membrane of rat-liver mitochondria-Evidence for the presence of cardiolipin on the outside of the outer-membrane. FEBS Lett. 330 (1993) 71-76
65. Mcmurray W.C., and Dawson R.M.C. Phospholipid exchange reactions within liver cell. Biochem. J. 112 (1969) 91-108