Lipoplex Formulation of Superior Efficacy Exhibits High Surface Activity and Fusogenicity, and Readily Releases DNA

Overview

Journal Biochim Biophys Acta

Specialties Biochemistry
Biophysics

Date 2006 Dec 13

PMID 17156744

Citations 16

Authors

Rumiana Koynova

Yury S Tarahovsky

Li Wang

Robert C MacDonald

Affiliations

Soon will be listed here.

Abstract

Lipoplexes containing a mixture of cationic phospholipids dioleoylethylphosphatidylcholine (EDOPC) and dilauroylethylphosphatidylcholine (EDLPC) are known to be far more efficient agents in transfection of cultured primary endothelial cells than are lipoplexes containing either lipid alone. The large magnitude of the synergy permits comparison of the physical and physico-chemical properties of lipoplexes that have very different transfection efficiencies, but minor chemical differences. Here we report that the superior transfection efficiency of the EDLPC/EDOPC lipoplexes correlates with higher surface activity, higher affinity to interact and mix with negatively charged membrane-mimicking liposomes, and with considerably more efficient DNA release relative to the EDOPC lipoplexes. Observations on cultured cells agree with the results obtained with model systems; confocal microscopy of transfected human umbilical artery endothelial cells (HUAEC) demonstrated more extensive DNA release into the cytoplasm and nucleoplasm for the EDLPC/EDOPC lipoplexes than for EDOPC lipoplexes; electron microscopy of cells fixed and embedded directly on the culture dish revealed contact of EDLPC/EDOPC lipoplexes with various cellular membranes, including those of the endoplasmic reticulum, mitochondria and nucleus. The sequence of events outlining efficient lipofection is discussed based on the presented data.

Citing Articles

Looking Back, Moving Forward: Lipid Nanoparticles as a Promising Frontier in Gene Delivery.

Pozzi D, Caracciolo G ACS Pharmacol Transl Sci. 2023; 6(11):1561-1573.

PMID: 37974625 PMC: 10644400. DOI: 10.1021/acsptsci.3c00185.

Preparation of cationic proteoliposomes using cell-free membrane protein synthesis: the chaperoning effect of cationic liposomes.

Ando M, Sasaki Y, Akiyoshi K RSC Adv. 2022; 10(48):28741-28745.

PMID: 35520093 PMC: 9055869. DOI: 10.1039/d0ra05825d.

Overcoming barriers in non-viral gene delivery for neurological applications.

Tasset A, Bellamkonda A, Wang W, Pyatnitskiy I, Ward D, Peppas N Nanoscale. 2022; 14(10):3698-3719.

PMID: 35195645 PMC: 9036591. DOI: 10.1039/d1nr06939j.

The Process of Binding and Releasing of Genetic Material from Lipoplexes Based on Trimeric Surfactants and Phospholipids.

Polanska Z, Pietralik-Molinska Z, Wojciechowska D, Molinski A, Weiss M, Skrzypczak A Int J Mol Sci. 2021; 22(14).

PMID: 34299360 PMC: 8303235. DOI: 10.3390/ijms22147744.

Effect of white mange mixture in a murine model of psoriasis.

Guo J, Liu J Exp Ther Med. 2019; 18(2):881-887.

PMID: 31384318 PMC: 6639981. DOI: 10.3892/etm.2019.7641.

References

Macdonald R, Ashley G, Shida M, Rakhmanova V, Tarahovsky Y, Pantazatos D . Physical and biological properties of cationic triesters of phosphatidylcholine. Biophys J. 1999; 77(5):2612-29. PMC: 1300535. DOI: 10.1016/S0006-3495(99)77095-5. View

Pantazatos S, Macdonald R . Real-time observation of lipoplex formation and interaction with anionic bilayer vesicles. J Membr Biol. 2003; 191(2):99-112. DOI: 10.1007/s00232-002-1050-4. View

Zabner J, Fasbender A, Moninger T, Poellinger K, Welsh M . Cellular and molecular barriers to gene transfer by a cationic lipid. J Biol Chem. 1995; 270(32):18997-9007. DOI: 10.1074/jbc.270.32.18997. View

Hovius R, Thijssen J, Van Der Linden P, Nicolay K, de Kruijff 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. 1993; 330(1):71-6. DOI: 10.1016/0014-5793(93)80922-h. View

Siakotos A, Rouser G . Isolation of highly purified human and bovine brain endothelial cells and nuclei and their phospholipid composition. Lipids. 1969; 4(3):234-9. DOI: 10.1007/BF02532638. View

Boukhnikachvili T, Airiau M, Lesieur S, Ollivon M, Vacus J . Structure of in-serum transfecting DNA-cationic lipid complexes. FEBS Lett. 1997; 409(2):188-94. DOI: 10.1016/s0014-5793(97)00505-x. View

Bally , Harvie , Wong , Kong , Wasan , REIMER . Biological barriers to cellular delivery of lipid-based DNA carriers. Adv Drug Deliv Rev. 2000; 38(3):291-315. DOI: 10.1016/s0169-409x(99)00034-4. View

Tachibana R, Harashima H, Ide N, Ukitsu S, Ohta Y, Suzuki N . Quantitative analysis of correlation between number of nuclear plasmids and gene expression activity after transfection with cationic liposomes. Pharm Res. 2002; 19(4):377-81. DOI: 10.1023/a:1015162722295. View

Siegel D, Epand R . The mechanism of lamellar-to-inverted hexagonal phase transitions in phosphatidylethanolamine: implications for membrane fusion mechanisms. Biophys J. 1997; 73(6):3089-111. PMC: 1181213. DOI: 10.1016/S0006-3495(97)78336-X. View

10.

Jordanova A, Lalchev Z, Tenchov B . Formation of monolayers and bilayer foam films from lamellar, inverted hexagonal and cubic lipid phases. Eur Biophys J. 2003; 31(8):626-32. DOI: 10.1007/s00249-002-0263-x. View

11.

Lei G, MacDonald R . Lipid bilayer vesicle fusion: intermediates captured by high-speed microfluorescence spectroscopy. Biophys J. 2003; 85(3):1585-99. PMC: 1303334. DOI: 10.1016/S0006-3495(03)74590-1. View

12.

Friend D, Papahadjopoulos D, Debs R . Endocytosis and intracellular processing accompanying transfection mediated by cationic liposomes. Biochim Biophys Acta. 1996; 1278(1):41-50. DOI: 10.1016/0005-2736(95)00219-7. View

13.

Bhattacharya S, Mandal S . Evidence of interlipidic ion-pairing in anion-induced DNA release from cationic amphiphile-DNA complexes. Mechanistic implications in transfection. Biochemistry. 1998; 37(21):7764-77. DOI: 10.1021/bi971772j. View

14.

Leventis R, Silvius J . Interactions of mammalian cells with lipid dispersions containing novel metabolizable cationic amphiphiles. Biochim Biophys Acta. 1990; 1023(1):124-32. DOI: 10.1016/0005-2736(90)90017-i. View

15.

Radler J, Koltover I, Salditt T, Safinya C . Structure of DNA-cationic liposome complexes: DNA intercalation in multilamellar membranes in distinct interhelical packing regimes. Science. 1997; 275(5301):810-4. DOI: 10.1126/science.275.5301.810. View

16.

Koynova R, MacDonald R . Lipid transfer between cationic vesicles and lipid-DNA lipoplexes: effect of serum. Biochim Biophys Acta. 2005; 1714(1):63-70. DOI: 10.1016/j.bbamem.2005.05.009. View

17.

McMurray W, Dawson R . Phospholipid exchange reactions within the liver cell. Biochem J. 1969; 112(1):91-108. PMC: 1187645. DOI: 10.1042/bj1120091. View

18.

Macdonald R, Rakhmanova V, Choi K, Rosenzweig H, Lahiri M . O-ethylphosphatidylcholine: A metabolizable cationic phospholipid which is a serum-compatible DNA transfection agent. J Pharm Sci. 1999; 88(9):896-904. DOI: 10.1021/js990006q. View

19.

Nakanishi M, Noguchi A . Confocal and probe microscopy to study gene transfection mediated by cationic liposomes with a cationic cholesterol derivative. Adv Drug Deliv Rev. 2001; 52(3):197-207. DOI: 10.1016/s0169-409x(01)00207-1. View

20.

Pires P, Simoes S, Nir S, Gaspar R, Duzgunes N, Pedroso de Lima M . Interaction of cationic liposomes and their DNA complexes with monocytic leukemia cells. Biochim Biophys Acta. 1999; 1418(1):71-84. DOI: 10.1016/s0005-2736(99)00023-1. View