Application of membrane-active peptides for drug and gene delivery across cellular membranes

Advanced Drug Delivery Reviews

Volumn 34, Issue 1, 1998, Pages 21-35

  Plank, Christian ^a   Zauner, Wolfgang ^a   Wagner, Ernst ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

Amphipathic peptides; Cytosolic delivery; DNA transfection; Endosome disruption; Membrane fusion

Indexed keywords

BIOLOGICAL MEMBRANES; DNA; GENES; LIPIDS; OLIGOMERS; PHYSIOLOGY; PROTEINS;

AMPHIPATHIC PEPTIDES; CYTOSOLIC DELIVERY;

CONTROLLED DRUG DELIVERY;

EXOTOXIN; HYBRID PROTEIN; MEMBRANE PROTEIN; OLIGONUCLEOTIDE; PLASMID DNA; SYNTHETIC PEPTIDE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CYTOPLASM; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; GENE TRANSFER; HUMAN; LIPID MEMBRANE; MEMBRANE FUSION; MEMBRANE STABILIZATION; MEMBRANE STRUCTURE; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW;

EID: 0032487377     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-409X(98)00005-2     Document Type: Review

References (115)

1. Wagner E., Curiel D., Cotten M. Delivery of drugs, proteins and genes into cells using transferrin as a ligand for receptor-mediated endocytosis. Adv. Drug Del. Rev. 14:1994;113-136.
2. Rothman J.E., Wieland F.T. Protein sorting by transport vesicles. Science. 272:1996;227-234.
3. White J.M. Membrane fusion. Science. 258:1992;917-924.
4. Blobel C.P., Wolfsberg T.G., Turuck C.W., Myles D.G., Primakoff P., White J.M. A potential fusion peptide and an integrin domain in a protein active in sperm-egg fusion. Nature. 356:1992;248.
5. Muga A., Neugebauer W., Hirama T., Surewicz W.K. Membrane interaction and conformational properties of the putative fusion peptide of PH-30, a protein active in sperm-egg fusion. Biochemistry. 33:1994;4444-4448.
6. Bhakdi S., Tranum-Jensen J. Complement lysis: a hole is a hole. Immunol. Today. 12:1991;318.
7. Esser A.F. Big MAC attack: complement proteins cause leaky patches. Immunol. Today. 12:1991;316.
8. Esser A.F. The membrane attack complex of complement. Assembly, structure and cytotoxic activity. Toxicology. 87:1994;229-247.
9. Liu C.C., Persechini P.M., Young J.D. Perforin and lymphocyte-mediated cytolysis. Immunol. Rev. 146:1995;145-175.
10. Plank C., Zatloukal K., Cotten M., Mechtler K., Wagner E. Gene transfer into hepatocytes using asialoglycoprotein receptor mediated endocytosis of DNA complexed with an artificial tetra-antennary galactose ligand. Bioconjugate Chem. 3:1992;533-539.
11. Plank C., Oberhauser B., Mechtler K., Koch C., Wagner E. The influence of endosome-disruptive peptides on gene transfer using synthetic virus-like gene transfer systems. J. Biol. Chem. 269:1994;12918-12924.
12. Fernandez-Puentes C., Carrasco L. Viral infection permeabilizes mammalian cells to protein toxins. Cell. 20:1980;769-775.
13. Otero M.J., Carrasco L. Proteins are cointernalized with virion particles during early infection. Virology. 160:1987;75-80.
14. Carrasco L. Entry of animal viruses and macromolecules into cells. FEBS Lett. 350:1994;151-154.
15. Carrasco L. Modification of membrane permeability by animal viruses. Adv. Virus Res. 45:1995;61-112.
16. FitzGerald D.J.P., Padmanabhan R., Pastan I., Willingham M.C. Adenovirus-induced release of epidermal growth factor and Pseudomonas toxin into the cytosol of KB cells during receptor-mediated endocytosis. Cell. 32:1983;607-617.
17. Fitzgerald D.J.P., Trowbridge I.S., Pastan I., Willingham M.C. Enhancement of toxicity of an anti-transferrin receptor antibody Pseudomonas exotoxin conjugates by adenovirus. Proc. Natl. Acad. Sci. USA. 80:1983;4134-4138.
18. Seth P., FitzGerald D., Ginsberg H., Willingham M., Pastan I. Evidence that the penton base is involved in potentiation of toxicity of pseudomonas exotoxin conjugated to epidermal growth factor. Mol. Cell. Biol. 4:1984;1528-1533.
19. Wagner E., Zenke M., Cotten M., Beug H., Birnstiel M.L. Transferrin-polycation conjugates as carriers for DNA uptake into cells. Proc. Natl. Acad. Sci. USA. 87:1990;3410-3414.
20. Cotten M., Laengle-Rouault F., Kirlappos H., Wagner E., Mechtler K., Zenke M., Beug H., Birnstiel M.L. Transferrin-polycation-mediated introduction of DNA into human leukemic cells: stimulation by agents that affect the survival of transfected DNA or modulate transferrin receptor levels. Proc. Natl. Acad. Sci. USA. 87:1990;4033-4037.
21. Curiel D.T., Agarwal S., Wagner E., Cotten M. Adenovirus enhancement of transferrin-polylysine-mediated gene delivery. Proc. Natl. Acad. Sci. USA. 88:1991;8850-8854.
22. Cotten M., Wagner E., Zatloukal K., Phillips S., Curiel D.T., Birnstiel M.L. High-efficiency receptor-mediated delivery of small and large (48kb) gene constructs using the endosome disruption activity of defective or chemically inactivated adenovirus particles. Proc. Natl. Acad. Sci. USA. 89:1992;6094-6098.
23. Curiel D.T., Wagner E., Cotten M., Birnstiel M.L., Agarwal S., Li C.-M., Loechel S., Hu P.-C. High-efficiency gene transfer by adenovirus coupled to DNA-polylysine complexes. Hum. Gene Ther. 3:1992;147-154.
24. Cristiano R.J., Smith L.J., Kay M.A., Brinkley B.R., Woo S.L.C. Hepatic gene therapy: Efficient gene delivery and expression in primary hepatocytes utilizing a conjugated adenovirus-DNA complex. Proc. Natl. Acad. Sci. USA. 90:1993;11548-11552.
25. Wagner E., Zatloukal K., Cotten M., Kirlappos H., Mechtler K., Curiel D.T., Birnstiel M.L. Coupling of adenovirus to transferrin-polylysine/DNA complexes greatly enhances receptor-mediated gene delivery and expression of transfected genes. Proc. Natl. Acad. Sci. USA. 89:1992;6099-6103.
26. Zatloukal K., Wagner E., Cotten M., Phillips S., Plank C., Steinlein P., Curiel D., Birnstiel M.L. Transferrinfection: A highly efficient way to express gene constructs in eukariotic cells. Ann. NY Acad. Sci. 660:1992;136-153.
27. Wu G.Y., Zhan P., Sze L.L., Rosenberg A.R., Wu C.H. Incorporation of adenovirus into a ligand-based DNA carrier system results in retention of original receptor specificity and enhances targeted gene expression. J. Biol. Chem. 269:1994;11542-11546.
28. Fisher K.J., Wilson J.M. Biochemical and functional analysis of an adenovirus-based ligand complex for gene transfer. Biochem. J. 299:1994;49-58.
29. Cotten M., Saltik M., Kursa M., Wagner E., Maass G., Birnstiel M.L. Psoralen treatment of adenovirus particles eliminates virus replication and transcription while maintaining the endosomolytic activity of the virus capsid. Virology. 205:1994;254-261.
30. Cotten M., Wagner E., Zatloukal K., Birnstiel M.L. Chicken adenovirus (CELO virus) particles augment receptor-mediated DNA delivery to mammalian cells and yield exceptional levels of stable transformants. J. Virol. 67:1993;3777-3785.
31. Zauner W., Blaas D., Küchler E., Wagner E. Rhinovirus mediated endosomal release of transfection complexes. J. Virol. 69:1995;1085-1092.
32. Prchla E., Plank C., Wagner E., Blaas D., Fuchs R. Virus-mediated release of endosomal content in vitro: Different behaviour of adenovirus and rhinovirus serotype 2. J. Cell Biol. 131:1995;111-123.
33. Bron R., Ortiz A., Wilschut J. Cellular cytoplasmic delivery of a polypeptide toxin by reconstituted influenza virus envelopes (virosomes). Biochemistry. 33:1994;9110-9117.
34. Hug P., Sleight R.G. Fusogenic virosomes prepared by partitioning of vesicular stomatitis virus G protein into preformed vesicles. J. Biol. Chem. 269:1994;4050-4056.
35. Kaneda Y., Iwai K., Uchida T. Increased expression of DNA cointroduced with nuclear protein in adult rat liver. Science. 243:1989;375-378.
36. Mizuguchi H., Nakagawa T., Nakanishi M., Imazu S., Nakagawa S., Mayumi T. Efficient gene transfer into mammalian cells using fusogenic liposomes. Biochem. Biophys. Res. Commun. 218:1996;402-407.
37. von der Leyen H.E., Gibbons G.H., Morishita R., Lewis N.P., Zhang L., Nakajima M., Kaneda Y., Cooke J.P., Dzau V.J. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc. Natl. Acad. Sci. USA. 92:1995;1137-1141.
38. Gluck R., Mischler R., Finkel B., Que J.U., Scarpa B., Cryz S.J. Immunogenicity of new virosome influenza vaccine in elderly people. Lancet. 344:1994;160-163.
39. Poovorawan Y., Theamboonlers A., Chumdermpadetsuk S., Gluck R., Cryz S.J. Safety, immunogenicity, and kinetics of the immune response to a single dose of virosome-formulated hepatitis A vaccine in Thais. Vaccine. 13:1995;891-893.
40. Moskaug J.O., Sletten K., Sandvig K., Olsnes S. Translocation of diphteria toxin A-fragment to the cytosol. J. Biol. Chem. 264:1989;15709-15713.
41. Defrise-Quertain F.D., Cabiaux V., Vandenbranden M., Wattiez R., Falmagne P., Ruysschaert J.-M. pH-dependent bilayer destabilization and fusion of phospholipidic large unilamellar vesicles induced by diphtheria toxin and its fragments A and B. Biochemistry. 28:1989;3406-3413.
42. Mindell J.A., Silverman J.A., Collier R.J., Finkelstein A. Structure function relationships in diphtheria toxin channels: II. A residue responsible for the channel's dependence on trans pH. J. Membr. Biol. 137:1994;29-44.
43. Mindell J.A., Silverman J.A., Collier R.J., Finkelstein A. Structure-function relationships in diphtheria toxin channels: III. Residues which affect the cis pH dependence of channel conductance. J. Membr. Biol. 137:1994;45-57.
44. Silverman J.A., Mindell J.A., Finkelstein A., Shen W.H., Collier R.J. Mutational analysis of the helical hairpin region of diphtheria toxin transmembrane domain. J. Biol. Chem. 269:1994;22524-22532.
45. Silverman J.A., Mindell J.A., Zhan H., Finkelstein A., Collier R.J. Structure-function relationships in diphtheria toxin channels: I. Determining a minimal channel-forming domain. J. Membr. Biol. 137:1994;17-28.
46. Madshus I.H. The N-terminal alpha-helix of fragment B of diphtheria toxin promotes translocation of fragment A into the cytoplasm of eukaryotic cells. J. Biol. Chem. 269:1994;17723-17729.
47. Olsnes S., Sandvig K., Petersen O.W., van Deurs B. Immunotoxins-entry into cells and mechanisms of action. Immunol. Today. 10:1989;291-295.
48. Pastan I.H., Pai L.H., Brinkmann U., Fitzgerald D.J. Recombinant toxins: new therapeutic agents for cancer. Ann. NY Acad. Sci. 758:1995;345-354.
49. Chaudhary V.K., Gallo M.G., FitzGerald D.J., Pastan I. A recombinant single-chain immunotoxin composed of anti-Tac variable regions and a truncated diphtheria toxin. Proc. Natl. Acad. Sci. USA. 87:1990;9491-9494.
50. Wiedlocha A., Falnes P.O., Madshus I.H., Sandvig K., Olsnes S. Dual mode of signal transduction by externally added acidic fibroblast growth factor. Cell. 76:1994;1039-1051.
51. Bhakdi S., Bayley H., Valeva A., Walev I., Walker B., Kehoe M., Palmer M. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch. Microbiol. 165:1996;73-79.
52. Bielecki J., Youngman P., Connelly P., Portnoy D.A. Bacillus subtilis expressing a haemolysin gene from can grow in mammalian cells. Nature. 345:1990;175-176.
53. Tilney L.G., Portnoy D.A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1989;1597-1608.
54. Ahnert-Hilger G., Mach W., Föhr K.J., Gratzl M. Poration by alpha-toxin and streptolysin O: an approach to analyze intracellular processes. Methods Cell Biol. 31:1989;63-90.
55. Barry E.L.R., Gesek F.A., Friedman P.A. Introduction of antisense oligonucleotides into cells by permeabilization with streptolysin O. Biotechniques. 15:1993;1016-1020.
56. Gottschalk S., Tweten R.K., Smith L.C., Woo S.L.C. Efficient gene delivery and expression in mammalian cells using DNA coupled with perfringolysin O. Gene Ther. 2:1995;498-503.
57. Dempsey C.E. The actions of melittin on membranes. Biochim. Biophys. Acta. 1031:1990;143-161.
58. Gazit E., Boman A., Boman H.G., Shai Y. Interaction of the mammalian antibacterial peptide cecropin P1 with phospholipid vesicles. Biochemistry. 34:1995;11479-11488.
59. Fujii G., Selsted M.E., Eisenberg D. Defensins promote fusion and lysis of negatively charged membranes. Protein Sci. 2:1993;1301-1312.
60. Haimovich B., Tanaka J.C. Magainin-induced cytotoxicity in eukaryotic cells: kinetics, dose-response and channel characteristics. Biochim. Biophys. Acta. 1240:1995;149-158.
61. Benachir T., Lafleur M. Study of vesicle leakage induced by melittin. Biochim. Biophys. Acta. 1235:1995;452-460.
62. Shai Y. Pardaxin: channel formation by a shark repellant peptide from fish. Toxicology. 87:1994;109-129.
63. Epand R.M., Shai Y., Segrest J.P., Anantharamaiah G.M. Mechanisms for the modulation of membrane bilayer properties by amphipathic helical peptides. Biopolymers. 17:1995;319-338.
64. Epand R.M., Cheetham J.J., Epand R.F., Yeagle P.L., Richardson C.D., Rockwell A., DeGrado W.F. Peptide models for the membrane destabilizing action of viral fusion proteins. Biopolymers. 32:1992;309-314.
65. Colotto A., Martin I., Ruysschaert J.M., Sen A., Hui S.W., Epand R.M. Structural study of the interaction between the SIV fusion peptide and model membranes. Biochemistry. 35:1996;980-989.
66. Tytler E.M., Segrest J.P., Epand R.M., Nie S.-Q., Epand R.F., Mishra V.K., Venkatachalapathi Y.V., Anatharamaiah G.M. Reciprocal effects of apolipoprotein and lytic peptide analogs on membrane. Cross-sectional molecular shapes of amphipathic alpha helices control membrane stability. J. Biol. Chem. 268:1993;22112-22118.
67. Wilson I.A., Skehel J.J., Wiley D.C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3A resolution. Nature. 289:1981;366-373.
68. Bullough P.A., Hughson F.M., Skehel J.J., Wiley D.C. The structure of influenza haemagglutinin at the pH of membrane fusion. Nature. 371:1994;37-43.
69. Lear J.D., Grado W.F. Membrane binding and conformational properties of peptides representing the NH2 terminus of influenza HA-2. J. Biol. Chem. 262:1987;6500-6505.
70. Wharton S.A., Martin S.R., Ruigrok R.W.H., Skehel J.J., Wiley D.C. Membrane fusion by peptide analogues of influenza virus haemagglutinin. J. Gen. Virol. 69:1988;1847-1857.
71. Rafalski M., Ortiz A., Rockwell A., van Gickel L.C., Lear J.D., DeGrado W.F., Wilschut J. Membrane fusion activity of the influenza virus hemagglutinin: interaction of HA2 N-terminal peptides with phospholipid vesicles. Biochemistry. 30:1991;10211-10220.
72. Takahashi S. Conformation of membrane fusion active 20-residue peptides with or without lipid bilayers. Implication of alpha-helix formation for membrane fusion. Biochemistry. 29:1990;6257-6264.
73. Lüneberg J., Martin I., Nüßler F., Ruysschaert J.-M., Herrmann A. Structure and topology of the influenza virus fusion peptide in lipid bilayers. J. Biol. Chem. 270:1995;27606-27614.
74. Martin I., Defrise-Quertain F., Mandieau V., Nielsen N.M., Saermark T., Burny A., Brasseur R., Ruysschaert J.-M., Vandenbranden M. Fusogenic activity of SIV (simian immunodeficiency virus) peptides located in the gp32 N-terminal domain. Biochem. Biophys. Res. Commun. 175:1991;872-879.
75. Epand R.F., Martin I., Ruysschaert J.M., Epand R.M. Membrane orientation of the SIV fusion peptide determines its effect on bilayer stability and ability to promote membrane fusion. Biochem. Biophys. Res. Commun. 205:1994;1938-1943.
76. Martin I., Schaal H., Scheid A., Ruysschaert J.M. Lipid membrane fusion induced by the human immunodeficiency virus type 1 gp41 N-terminal extremity is determined by its orientation in the lipid bilayer. J. Virol. 70:1996;298-304.
77. Murata M., Sugahara Y., Takahashi S., Ohnishi S.-i. pH-dependent membrane fusion activity of a synthetic twenty amino acid peptide with the same sequence as that of the hydrophobic segment of influenza virus hemagglutinin. J. Biochem. 102:1987;957-962.
78. Steinhauer D.A., Wharton S.A., Skehel J.J., Wiley D.C. Studies of the membrane fusion activities of fusion peptide mutants of influenza virus hemagglutinin. J. Virol. 69:1995;6643-6651.
79. Mechtler K., Wagner E. Influenza peptide enhanced gene transfer: The role of peptide sequences. New J. Chem. 21:1997;105-111.
80. Parente R.A., Nir S., Szoka F.C. pH-dependent fusion of phosphatidylcholine small vesicles. Induction by a synthetic amphipathic peptide. J. Biol. Chem. 263:1988;4724-4730.
81. Subbarao N.K., Parente R.A., Szoka F.C., Nadasdi L., Pongracz K. pH-dependent bilayer destabilization by an amphipathic peptide. Biochemistry. 26:1987;2964-2972.
82. Gottschalk S., Sparrow J.T., Hauer J., Mims M.P., Leland F.E., Woo S.L.C., Smith L.C. A novel DNA-peptide complex for efficient gene transfer and expression in mammalian cells. Gene Ther. 3:1996;448-457.
83. Rapaport D., Nir S., Shai Y. Capacities of pardaxin analogues to induce fusion and leakage of negatively charged phospholipid vesicles are not necessarily correlated. Biochemistry. 33:1994;12615-12624.
84. Nieva J.L., Nir S., Muga A., Goni F.M., Wilschut J. Interaction of the HIV-1 fusion peptide with phospholipid vesicles: different structural requirements for fusion and leakage. Biochemistry. 33:1994;3201-3209.
85. Ono S., Lee S., Mihara H., Aoyagi H., Kato T., Yamasaki N. Design and synthesis of basic peptides having amphipathic beta-structures and their interaction with phospholipid membranes. Biochim. Biophys. Acta. 1022:1990;237-244.
86. Parente R.A., Nir S., Szoka F.C. Mechanism of leakage of phospholipid vesicle contents induced by the peptide GALA. Biochemistry. 29:1990;8720-8728.
87. Fattal E., Nir S., Parente R.A., Szoka F.C. Pore-forming peptides induce rapid phospholipid flip-flop in membranes. Biochemistry. 33:1994;6721-6731.
88. Puyal C., Maurin L., Miquel G., Bienvenue A., Philippot J. Design of a short membrane-destabilizing peptide covalently bound to liposomes. Biochim. Biophys. Acta. 1195:1994;259-266.
89. Nicol F., Nir S., Szoka F.C. Effect of cholesterol and charge on pore formation in bilayer vesicles by a pH-sensitive peptide. Biophys. Res. 71(6):1997;3288-3301.
90. B. Oberhauser, C. Plank, E. Wagner, Enhancing endosomal exit of nucleic acids using pH-sensitive viral fusion peptides, in: S. Akhtar (Ed.), Delivery Strategies for Antisense Oligonucleotide Therapeutics, ch. 16, CRC Press, FL, 1995, pp. 247-268.
91. Midoux P., Mayer R., Monsigny M. Membrane permeabilization by alpha-helical peptides: a flow cytometry study. Biochim. Biophys. Acta. 1239:1995;249-256.
92. Liang W.W., Shi X., Deshpande D., Malanga C.J., Rojanasakul Y. Oligonucleotide targeting to alveolar macrophages by mannose receptor-mediated endocytosis. Biochim. Biophys. Acta. 1279:1996;227-234.
93. Bongartz J.P., Aubertin A.M., Milhaud P.G., Lebleu B. Improved biological activity of antisense oligonucleotides conjugated to a fusogenic peptide. Nucleic Acids Res. 22:1994;4681-4688.
94. Partidos C.D., Vohra P., Steward M.W. Priming of measles virus-specific CTL responses after immunization with a CTL epitope linked to a fusogenic peptide. Virology. 215:1996;107-110.
95. Chignola R., Anselmi C., Dalla-Serra M., Franceschi A., Fracasso G., Pasti M., Chiesa E., Lord J.M., Tridente G., Colombatti M. Self-potentiation of ligand-toxin conjugates containing ricin A chain fused with viral structures. J. Biol. Chem. 270:1995;23345-23351.
96. Murata M., Kagiwada S., Takahashi S., Ohnishi S.-I. Membrane fusion induced by mutual interaction of the two charge-reversed amphiphilic peptides at neutral pH. J. Biol. Chem. 266:1991;14353-14358.
97. Wu G.Y., Wu C.H. Receptor-mediated in vitro gene transformation by a soluble DNA carrier system. J. Biol. Chem. 262:1987;4429-4432.
98. Cotten M., Wagner E., Birnstiel M.L. Receptor mediated transport of DNA into eukariotic cells. Methods Enzymol. 217:1993;618-644.
99. Huckett B., Ariatti M., Hawtrey A.O. Evidence for targeted gene transfer by receptor-mediated endocytosis: Stable expression following insulin-directed entry of neo into HepG2 cells. Biochem. Pharmacol. 40:1990;253-263.
100. Chowdhury N.R., Wu C.H., Wu G.Y., Yerneni P.C., Bommineni V.R., Chowdhury J.R. Fate of DNA targeted to the liver by asialoglycoprotein receptor mediated endocytosis in vivo: prolonged persistence in cytoplasmic vesicles after partial hepatectomy. J. Biol. Chem. 268:1993;11265-11271.
101. Baatz J.E., Bruno M.D., Ciraolo P.J., Glasser S.W., Stripp B.R., Smyth K.L., Korfhagen T.R. Utilization of modified surfactant-associated protein B for delivery of DNA to airway cells in culture. Proc. Natl. Acad. Sci. USA. 91:1994;2547-2551.
102. Buschle M., Cotten M., Mechtler K., Birnstiel M.L., Wagner E. Receptor-mediated gene transfer into T-lymphocytes via binding of DNA/CD3 antibody particles to the CD3 T cell receptor complex. Hum. Gene Ther. 6:1995;753-761.
103. Ferkol T., Perales J.C., Eckman E., Kaetzel C.S., Hanson R.W., Davis P.B. Gene transfer into the airway epithelium of animals by targeting the polymeric immunoglobulin receptor. J. Clin. Invest. 95:1995;493-502.
104. Perales J.C., Ferkol T., Molas M., Hanson R.W. An evaluation of receptor-mediated gene transfer using synthetic DNA-ligand complexes. Eur. J. Biochem. 226:1994;255-266.
105. Zauner W., Kichler A., Schmidt W., Sinski A., Wagner E. Glycerol enhancement of ligand-polylysine/DNA transfection. Biotechniques. 20:1996;905-913.
106. Wagner E., Plank C., Zatloukal K., Cotten M., Birnstiel M.L. Influenza virus hemagglutinin HA-2 N-terminal fusogenic peptides augment gene transfer by transferrin-polylysine/DNA complexes: Towards a synthetic virus-like gene transfer vehicle. Proc. Natl. Acad. Sci. USA. 89:1992;7934-7938.
107. Midoux P., Mendes C., Legrand A., Raimond J., Mayer R., Monsigny M., Roche A.C. Specific gene transfer mediated by lactosylated poly-L-lysine into hepatoma cells. Nucleic Acids Res. 21:1993;871-878.
108. Haensler J., Szoka F.C. Polyamidoamine cascade polymers mediate efficient transfection of cells in culture. Bioconjugate Chem. 4:1993;372-379.
109. Wyman T.B., Nicol F., Zelphati O., Scaria P.V., Plank C., Szoka F.C. Design, synthesis and characterization of a cationic peptide that binds to nucleic acids and permeabilizes bilayers. Biochemistry. 36:1977;3008-3117.
110. Legendre J.Y., Szoka F.C. Cyclic amphipathic peptide-DNA complexes mediate high-efficiency transfection of adherent cells. Proc. Natl. Acad. Sci. USA. 90:1993;893.
111. Legendre J.Y., Supersaxo A. Short-chain phospholipids enhance amphipathic peptide-mediated gene transfer. Biochem. Biophys. Res. Commun. 217:1995;179-185.
112. Hara T., Kuwasawa H., Aramaki Y., Takada S., Koike K., Ishidate K., Kato H., Tsuchiya S. Effects of fusogenic and DNA-binding amphiphilic compounds on the receptor-mediated gene transfer into hepatic cells by asialofetuin-labeled liposomes. Biochim. Biophys. Acta. 1278:1996;51-58.
113. Kichler A., Mechtler K., Behr J.-P., Wagner E. The influence of membrane-active peptides and helper lipids on lipospermine/DNA complex mediated gene transfer. Bioconjug. Chem. 8:1997;213-221.
114. Kamata H., Yagisawa H., Takahashi S., Hirata H. Amphiphilic peptides enhance the efficiency of liposome-mediated DNA transfection. Nucleic Acids Res. 22:1994;536-537.
115. Li S., Huang L. Lipidic supramolecular assemblies for gene transfer. J. Liposome Res. 6:1996;589-608.