Gene delivery to vascular endothelium using chemical vectors: Implications for cardiovascular gene therapy

Expert Opinion on Biological Therapy

Volumn 7, Issue 5, 2007, Pages 627-643

  Theoharis, Stefanos ^a   Manunta, Maria ^a,b   Tan, Peng H ^a,c,d  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d Kettering General Hospital NHS Trust   (United Kingdom)

Author keywords

Chemical vectors; Endothelial cells; Gene transfer; Liposomes; Molecular conjugates; Polymers

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; ANGIOPOIETIN 1; ANGIOPOIETIN 2; ANTIBODY CONJUGATE; BASIC FIBROBLAST GROWTH FACTOR; CLONFECTIN; DENDRIMER; EFFECTENE; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 4; FIBROBLAST GROWTH FACTOR 5; FUGENE; GROWTH FACTOR; IMMUNOLIPOSOME; LIPOFECTAMINE 2000; LIPOFECTIN; LIPOSOME; MONOCYTE CHEMOTACTIC PROTEIN 1; NAKED DNA; PEPTIDE DERIVATIVE; PLASMID DNA; PLATELET DERIVED GROWTH FACTOR BB; POLYAMIDOAMINE; POLYETHYLENEIMINE; POLYMER; SCATTER FACTOR; TFX 50; TRANSFERRIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VIRUS VECTOR;

ANEURYSM; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR GENE THERAPY; CELL HYPERPLASIA; CLINICAL TRIAL; DRUG MECHANISM; ENDOCYTOSIS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; GENE EXPRESSION; GENE REPLACEMENT THERAPY; GENE TARGETING; GENE TRANSFER; GENETIC MANIPULATION; GENETIC TRANSFECTION; HUMAN; IMMUNOGENICITY; INTRACELLULAR TRANSPORT; ISCHEMIA; NONVIRAL GENE DELIVERY SYSTEM; NUCLEAR LOCALIZATION SIGNAL; PATHOGENICITY; PHAGE DISPLAY; REVIEW; RNA TRANSPORT; SMOOTH MUSCLE FIBER; THROMBOSIS; VASCULAR ENDOTHELIUM;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CARDIOVASCULAR DISEASES; CELL MEMBRANE; CELL NUCLEUS; DNA; ENDOCYTOSIS; ENDOSOMES; ENDOTHELIUM, VASCULAR; GENE EXPRESSION; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; LIPIDS; LIPOSOMES; POLYMERS;

EID: 34248142251     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.7.5.627     Document Type: Review

References (117)

1. TAN PH, CHAN CL, CHAN C, GEORGE AJ: The evolving role of gene-based treatment in surgery. Br. J. Surg. (2005) 92(12):1466-1480.
2. TAN PH, XUE SA, MANUNTA M et al.: Effect of vectors on human endothelial cell signal transducrion: implications for cardiovascular gene therapy. Arterioscler. Thromb. Vasc. Biol. (2006) 26(3):462-467. • Using an endothelial cell model, the authors dissect the mechanism of viral vector-induced activation on the PI3K and the PKR pathways. Both the PKR and the PI3K pathways are associated with cytokine production (IFN-α/β for PKR, and TNF-α/IL-1α/β for PI3K), serving as positive feedback loops that may help 'lock' the endothelial cells into an activated phenotype. In addition, this study also demonstrated potential strategies that might prevent nonspecific endothelial cell activation by viral vectors.
3. NICKLIN SA, BUENING H, DISHART KL et al.: Efficient and selective AAV2-mediated gene transfer directed to human vascular endothelial cells. Mol. Ther. (2001) 4(3):174-181. • An interesting study to demonstrate the feasibility of an adeno-associated vector to mediate gene transfer to vascular endothelium.
4. MULLER OJ, KAUL F, WEITZMAN MD et al.: Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat. Biotechnol. (2003) 21(9):1040-1046.
5. SKELLY CL, CURI MA, MEYERSON SL et al.: Prevention of restenosis by a herpes simplex virus mutant capable of controlled long-term expression in vascular tissue in vivo. Gene Ther. (2001) 8(24):1840-1846.
6. DZAU VJ, MANN MJ, MORISHITA R, KANEDA Y: Fusigenic viral liposome for gene therapy in cardiovascular diseases. Proc. Natl. Acad. Sci. USA (1996) 93(21):11421-11425.
7. HARDY S, KITAMURA M, HARRIS-STANSIL T, DAI Y, PHIPPS ML: Construction of adenovirus vectors through Cre-lox recombination. J. Virol. (1997) 71(3):1842-1849.
8. LOGVINOFF C, EPSTEIN AL: A novel approach for herpes simplex virus Type 1 amplicon vector production, using the Cre-loxP recombination system to remove helper virus. Hum. Gene Ther. (2001) 12(2):161-167.
9. TAN PH, BEUTELSPACHER SC, WANG YH et al.: Immunolipoplexes: an efficient, nonviral alternative for transfection of human dendritic cells with potential for clinical vaccination. Mol. Ther. (2005) 11(5):790-800.
10. MANN MJ, GIBBONS GH, HUTCHINSON H et al.: Pressure-mediated oligonucleotide transfection of rat and human cardiovascular tissues. Proc. Natl. Acad. Sci. USA (1999) 96(11):6411-6416.
11. HODGES BL, SCHEULE RK: Hydrodynamic delivery of DNA. Expert Opin. Biol. Ther. (2003) 3(6):911-918.
12. HAGSTROM JE: Plasmid-based gene delivery to target tissues in vivo: the intravascular approach. Curr. Opin. Mol. Ther. (2003) 5(4):338-344.
13. YANG NS, BURKHOLDER J, ROBERTS B, MARTINELL B, MCCABE D: In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment. Proc. Natl. Acad. Sci. USA (1990) 87(24):9568-9572.
14. KODAMA T, TAN PH, OFFIAH I et al.: Delivery of oligodeoxynucleotides into human saphenous veins: the adjunct effect of ultrasound and microbubbles. Ultrasound Med. Biol. (2005) 31(12):1683-1691.
15. OSHIMA Y, SAKAMOTO T, YAMANAKA I et al.: Targeted gene transfer to corneal endothelium in vivo by electric pulse. Gene Ther. (1998) 5(10):1347-1354.
16. MANN MJ, WHITTEMORE AD, DONALDSON MC et al.: Ex-vivo gene therapy of human vascular bypass grafts with E2F decoy: the PREVENT single-centre, randomised, controlled trial. Lancet (1999) 354(9189):1493-1498. •• This is an important clinical trial demonstrating that the modification of bypass graft with E2F decoy can delay graft failure.
17. TAN PH, CHAN CL, GEORGE AJ: Strategies to improve non-viral vectors - potential applications in clinical transplantation. Expert Opin. Biol. Ther. (2006) 6(6):619-630.
18. FELGNER PL, GADEK TR, HOLM M et al.: Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc. Natl. Acad. Sci. USA (1987) 84(21):7413-7417.
19. FELGNER PL, RINGOLD GM: Cationic liposome-mediated transfection. Nature (1989) 337(6205):387-388. •• A landmark paper to illustrate the feasibility of cationic lipids to transfect cells.
20. FELGNER JH, KUMAR R, SRIDHAR CN et al.: Enhanced gene delivery and mechanism studies with a novel series of cationic lipid formulations. J. Biol. Chem. (1994) 269(4):2550-2561.
21. NABEL EG, PLAUTZ G, NABEL GJ: Site-specific gene expression in vivo by direct gene transfer into the arterial wall. Science (1990) 249(4974):1285-1288. •• A landmark work illustrating site-specific gene expression in vivo to vascular endothelium.
22. STERNBERG B, SORGI FL, HUANG L: New structures in complex formation between DNA and cationic liposomes visualized by freeze-fracture electron microscopy. FEBS Lett. (1994) 356(2-3):361-366.
23. ZABNER J, FASBENDER AJ, MONINGER T, POELLINGER KA, WELSH MJ: Cellular and molecular barriers to gene transfer by a cationic lipid. J. Biol. Chem. (1995) 270(32):18997-19007.
24. CHABAUD P, CAMPLO M, PAYET D et al.: Cationic nucleoside lipids for gene delivery. Bioconjug. Chem. (2006) 17(2):466-472.
25. PIGNATELLO R, INTRAVAIA VD, PUGLISI G: A calorimetric evaluation of the interaction of amphiphilic prodrugs of idebenone with a biomembrane model. J. Colloid Interface Sci. (2006) 299(2):626-635.
26. SEGOTA S, TEZAK D: Spontaneous formation of vesicles. Adv. Colloid Interface Sci. (2006) 121(1-3):51-75.
27. GERSHON H, GHIRLANDO R, GUTTMAN SB, MINSKY A: Mode of formation and structural features of DNA-cationic liposome complexes used for transfection. Biochemistry (1993) 32(28):7143-7151.
28. SIMBERG D, DANINO D, TALMON Y et al.: Phase behavior, DNA ordering, and size instability of cationic lipoplexes. Relevance to optimal transfection activity. J. Biol. Chem. (2001) 276(50):47453-47459.
29. BOUSSIF O, GAUCHERON J, BOULANGER C et al.: Enhanced in vitro and in vivo cationic lipid-mediated gene delivery with a fluorinated glycerophosphoethanolamine helper lipid. J. Gene Med. (2001) 3(2):109-114.
30. FARHOOD H, SERBINA N, HUANG L: The role of dioleoyl phosphatidylethanolamine in cationic liposome mediated gene transfer. Biochim. Biophys. Acta (1995) 1235(2):289-295.
31. KUPATT C, DESSY C, HINKEL R et al.: Heat shock protein 90 transfection reduces ischemia-reperfusion-induced myocardial dysfunction via reciprocal endothelial NO synthase serine 1177 phosphorylation and threonine 495 dephosphotylation. Arterioscler. Thromb. Vasc. Biol. (2004) 24(8):1435-1441.
32. KHURANA R, SHAFI S, MARTIN J, ZACHARY I: Vascular endothelial growth factor gene transfer inhibits neointimal macrophage accumulation in hypercholesterolemic rabbits. Arterioscler. Thromb. Vasc. Biol. (2004) 24(6):1074-1080.
33. KIM SI, KIM KS, KIM HS et al.: Inhibitory effect of the salmosin gene transferred by cationic liposomes on the progression of B16BL6 tumors. Cancer Res. (2003) 63(19):6458-6462.
34. KAISER S, TOBOREK M: Liposome-mediated high-efficiency transfection of human endothelial cells. J. Vasc. Res. (2001) 38(2):133-143.
35. LAITINEN M, HARTIKAINEN J, HILTUNEN MO et al.: Catheter-mediated vascular endothelial growth factor gene transfer to human coronary arteries after angioplasty. Hum. Gene Ther. (2000) 11(2):263-270.
36. SLEPUSHKIN VA, SIMOES S, DAZIN P et al.: Sterically stabilized pH-sensitive liposomes. Intracellular delivery of aqueous contents and prolonged circulation in vivo. J. Biol. Chem. (1997) 272(4):2382-2388.
37. WOODLE MC, ENGBERS CM, ZALIPSKY S: New amphipatic polymer-lipid conjugates forming long-circulating reticuloendothelial system-evading liposomes. Bioconjug. Chem. (1994) 5(6):493-496.
38. KUKOWSKA-LATALLO JF, BIELINSKA AU, JOHNSON J et al.: Efficient transfer of genetic material into mammalian cells using Starburst polyamidoamine dendrimers. Proc. Natl. Acad. Sci. USA (1996) 93(10):4897-4902.
39. SU JC, LIU YC, CHEN HL et al.: Two-dimensional densely packed DNA nanostructure derived from DNA complexation with a low-generation poly(amidoamine) dendrimer. Langmuir (2007) 23(3):975-978.
40. HAENSLER J, SZOKA FC JR: Polyamidoamine cascade polymers mediate efficient transfection of cells in culture. Bioconjug. Chem. (1993) 4(5):372-379.
41. TANG MX, REDEMANN CT, SZOKA FC JR: In vitro gene delivery by degraded polyamidoamine dendrimers. Bioconjug. Chem. (1996) 7(6):703-714.
42. ROBERTS JC, BHALGAT MK, ZERA RT: Preliminary biological evaluation of polyamidoamine (PAMAM) Starburst dendrimers. J. Biomed. Mater. Res. (1996) 30(1):53-65.
43. PLANK C, MECHTLER K, SZOKA FC JR, WAGNER E: Activation of the complement system by synthetic DNA complexes: a potential barrier for intravenous gene delivery. Hum. Gene Ther. (1996) 7(12):1437-1446.
44. WANG Y, BOROS P, LIU J et al.: DNA/dendrimer complexes mediate gene transfer into murine cardiac transplants ex vivo. Mol. Ther. (2000) 2(6):602-608. •• A interesting work illustrating the feasibility of dendrimers to mediate gene transfer to vascular endothelium.
45. QIN L, PAHUD DR, DING Y et al.: Efficient transfer of genes into murine cardiac grafts by Starburst polyamidoamine dendrimers. Hum. Gene Ther. (1998) 9(4):553-560.
46. VINCENT L, VARET J, PILLE JY et al.: Efficacy of dendrimer-mediated angiostatin and TIMP-2 gene delivery on inhibition of tumor growth and angiogenesis: in vitro and in vivo studies. Int. J. Cancer (2003) 105(3):419-429.
47. GODBEY WT, WU KK, MIKOS AG: Size matters: molecular weight affects the efficiency of poly(ethylenimine) as a gene delivery vehicle. J. Biomed. Mater. Res. (1999) 45(3):268-275.
48. TANG MX, SZOKA FC: The influence of polymer structure on the interactions of cationic polymers with DNA and morphology of the resulting complexes. Gene Ther. (1997) 4(8):823-832.
49. GOULA D, REMY JS, ERBACHER P et al.: Size, diffusibility and transfection performance of linear PEI/DNA complexes in the mouse central nervous system. Gene Ther. (1998) 5(5):712-717.
50. OGRIS M, BRUNNER S, SCHULLER S, KIRCHEIS R, WAGNER E: PEGylated DNA/transferrin-PEI complexes: reduced interaction with blood components, extended circulation in blood and potential for systemic gene delivery. Gene Ther. (1999) 6(4):595-605.
51. TAN PH, MANUNTA M, ARDJOMAND N et al.: Antibody targeted gene transfer to endothelium. J. Gene Med. (2003) 5(4):311-323.
52. TAN PH, KING WJ, CHEN D et al.: Transferrin receptor-mediated gene transfer to the corneal endothelium. Transplantation (2001) 71(4):552-560.
53. HART SL, COLLINS L, GUSTAFSSON K, FABRE JW: Integrin-mediated transfection with peptides containing arginine-glycine-aspartic acid domains. Gene Ther. (1997) 4(11):1225-1230. •• An important study illustrating the role of peptide-mediated gene transfer.
54. WHITE SJ, NICKLIN SA, SAWAMURA T, BAKER AH: Identification of peptides that target the endothelial cell-specific LOX-1 teceptor. Hypertension (2001) 37(2 Part 2):449-455. •• Using a specific peptide to target LOX-1 receptor, the authors illustrate a novel approach to mediate gene transfer to vascular endothelium.
55. FISHER KD, ULBRICH K, SUBR V et al.: A versatile system for receptor-mediated gene delivery permits increased entry of DNA into target cells, enhanced delivery to the nucleus and elevated rates of transgene expression. Gene Ther. (2000) 7(15):1337-1343.
56. SUTHERLAND R, DELIA D, SCHNEIDER C et al.: Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin. Proc. Natl. Acad. Sci. USA (1981) 78(7):4515-4519.
57. WAGNER E, COTTEN M, FOISNER R, BIRNSTIEL ML: Transferrin-polycation-DNA complexes: the effect of polycations on the strucrure of the complex and DNA delivery to cells. Proc. Natl. Acad. Sci. USA (1991) 88(10):4255- 4259.
58. LIANG KW, HOFFMAN EP, HUANG L: Targeted delivery of plasmid DNA to myogenic cells via transferrin-conjugated peptide nucleic acid. Mol. Ther. (2000) 1(3):236-243.
59. ZHANG Y, ZHU C, PARDRIDGE WM: Antisense gene therapy of brain cancer with an artificial virus gene delivery system. Mol. Ther. (2002) 6(1):67-72.
60. HYNES RO: Integrins: versatility, modulation, and signaling in cell adhesion. Cell (1992) 69(1):11-25.
61. KOIVUNEN E, WANG B, RUOSLAHTI E: Phage libraries displaying cyclic peptides with different ring sizes: ligand specificities of the RGD-directed integrins. Biotechnology (NY) (1995) 13(3):265-270.
62. HART SL, HARBOTTLE RP, COOPER R et al.: Gene delivery and expression mediated by an integrin-binding peptide. Gene Ther. (1995) 2(8):552-554. •• Using an integrin-binding peptide, the authors highlight the potentials of peptide-mediated gene transfer.
63. HART SL, ARANCIBIA-CARCAMO CV, WOLFERT MA et al.: Lipid-mediated enhancement of transfection by a nonviral integrin-targeting vector. Hum. Gene Ther. (1998) 9(4):575-585.
64. SHEWRING L, COLLINS L, LIGHTMAN SL et al.: A nonviral vector system for efficient gene transfer to corneal endothelial cells via membrane integrins. Transplantation (1997) 64(5):763-769. •• Using corneal endothelial cell as a model, the authors illustrate an endothelial-specific approach to target cells. This method can also be applied to vascular endothelial cells.
65. GEORGE AJ, LEE L, PITZALIS C: Isolating ligands specific for human vasculature using in vivo phage selection. Trends Biotechnol. (2003) 21(5):199-203.
66. NICKLIN SA, WHITE SJ, WATKINS SJ, HAWKINS RE, BAKER AH: Selective targeting of gene transfer to vascular endothelial cells by use of peptides isolated by phage display. Circulation (2000) 102(2):231-237. •• An important work illustrating the phage display technology to be utilised to generate endothelial-specific peptides to target vascular endothelium.
67. WHITE SJ, NICKLIN SA, BUNING H et al.: Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation (2004) 109(4):513-519. •• Changing the tropism of adeno-associated vectors can generate a novel vector that is specific for vascular endothelium. This is the first in vivo demonstration of this novel approach.
68. MORPURGO M, KIRSCHNER M, RADU A: An approach to increased polyplex gene delivery by peptides selected from a phage display library. J. Biochem. Biophys. Methods (2002) 52(1):31-43.
69. JOST PJ, HARBOTTLE RP, KNIGHT A et al.: A novel peptide, THALWHT, for the targeting of human airway epithelia. FEBS Lett. (2001) 489(2-3):263-269.
70. GUPTA S, EASTMAN J, SILSKI C, FERKOL T, DAVIS PB: Single chain Fv: a ligand in receptor-mediated gene delivery. Gene Ther. (2001) 8(8):586-592.
71. SUH W, CHUNG JK, PARK SH, KIM SW: Anti-JL1 antibody-conjugated poly (L-lysine) for targeted gene delivery to leukemia T cells. J. Control. Release (2001) 72(1-3):171-178.
72. KIRCHEIS R, KICHLER A, WALLNER G et al.: Coupling of cell-binding ligands to polyethylenimine for targeted gene delivety. Gene Ther. (1997) 4(5):409-418.
73. VAN ZANTEN J, DOORNBOS-VAN DER MEER B, AUDOUY S, KOK RJ, DE LEIJ L: A nonviral carrier for targeted gene delivery to tumor cells. Cancer Gene Ther. (2004) 11(2):156-164.
74. FERKOL T, KAETZEL CS, DAVIS PB: Gene transfer into respiratory epithelial cells by targeting the polymeric immunoglobulin receptor. J. Clin. Invest. (1993) 92(5):2394-2400.
75. CHEN J, GAMOU S, TAKAYANAGI A et al.: Receptor-mediated gene delivery using the Fab fragments of anti-epidermal growth factor receptor antibodies: improved immunogene approach. Cancer Gene Ther. (1998) 5(6):357-364.
76. SUZUKI M, TAKAYANAGI A, SHIMIZU N: Recombinant single-chain antibodies with various oligopeptide tails for targeted gene delivery. Gene Ther. (2003) 10(9):781-788.
77. LI X, STUCKERT P, BOSCH I, MARKS JD, MARASCO WA: Single-chain antibody-mediated gene delivery into ErbB2-positive human breast cancer cells. Cancer Gene Ther. (2001) 8(8):555-565.
78. RAPPOPORT JZ, SIMON SM, BENMERAH A: Understanding living clathrin-coated pits. Traffic (2004) 5(5):327-333.
79. PARTON RG, SIMONS K: The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. (2007) 8(3):185-194.
80. BAR-SAGI D, FERAMISCO JR: Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science (1986) 233(4768):1061-1068.
81. GAO X, HUANG L: Cationic liposome-mediated gene transfer. Gene Ther. (1995) 2(10):710-722.
82. MISLICK KA, BALDESCHWIELER JD: Evidence for the role of proteoglycans in cation-mediated gene transfer. Proc. Natl. Acad. Sci. USA (1996) 93(22):12349-12354.
83. RUPONEN M, RONKKO S, HONKAKOSKI P, PELKONEN J, TAMMI M, URTTI A: Extracellular glycosaminoglycans modify cellular trafficking of lipoplexes and polyplexes. J. Biol. Chem. (2001) 276(36):33875-33880.
84. ZUHORN IS, HOEKSTRA D: On the mechanism of cationic amphiphile-mediated transfection. To fuse or nor to fuse: is that the question? J. Membr. Biol. (2002) 189(3):167-179.
85. ZUHORN IS, KALICHARAN R, HOEKSTRA D: Lipoplex-mediated transfection of mammalian cells occurs through the cholesterol-dependent clathrin-mediated pathway of endocytosis. J. Biol. Chem. (2002) 277(20):18021-18028.
86. ZELPHATI O, SZOKA FC JR: Mechanism of oligonucleotide release from cationic liposomes. Proc. Natl. Acad. Sci. USA (1996) 93(21):11493-11498.
87. 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(Pt 1):68-71.
88. ZUHORN IS, OBERLE V, VISSER WH et al.: Phase behavior of cationic amphiphiles and their mixtures with helper lipid influences lipoplex shape, DNA translocation, and transfection efficiency. Biophys. J. (2002) 83(4):2096-2108.
89. ROCHA A, RUIZ S, COLL JM: Improvement of DNA transfection with cationic liposomes. J. Physiol. Biochem. (2002) 58(1):45-56.
90. MARALDI NM, GALANZI A, CARAMELLI E et al.: Changes in ribonucleoprotein particle and chromatin organization induced by liposomes in isolated nuclei. Cell Biochem. Funct. (1988) 6(3):165-173.
91. ZHANG ZY, SMITH BD: High-generation polycationic dendrimers are unusually effective at disrupting anionic vesicles: membrane bending model. Bioconjug. Chem. (2000) 11(6):805-814.
92. MANUNTA M, TAN PH, SAGOO P, KASHEFI K, GEORGE AJ: Gene delivery by dendrimers operates via a cholesterol dependent pathway. Nucleic Acids Res. (2004) 32(9):2730-2739.
93. REJMAN J, OBERLE V, ZUHORN IS, HOEKSTRA D: Size-dependent internalization of panicles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem. J. (2004) 377(Pt 1):159-169.
94. MANUNTA M, NICHOLS BJ, TAN PH et al.: Gene delivery by dendrimers operates via different pathways in different cells, but is enhanced by the presence of caveolin. J. Immunol. Methods (2006) 314(1-2):134-146.
95. JOHANNES L, LAMAZE C: Clathrin-dependent or not: is it still the question? Traffic (2002) 3(7):443-451.
96. WATTIAUX R, LAURENT N, WATTIAUX-DE CONINCK S, JADOT M: Endosomes, lysosomes: their implication in gene transfer. Adv. Drug Deliv. Rev. (2000) 41(2):201-208.
97. XU Y, SZOKA FC JR: Mechanism of DNA release from cationic liposome/DNA complexes used in cell transfection. Biochemistry (1996) 35(18):5616-5623.
98. WIETHOFF CM, SMITH JG, KOE GS, MIDDAUGH CR: The potential role of proteoglycans in cationic lipid-mediated gene delivery. Studies of the interaction of cationic lipid-DNA complexes with model glycosaminoglycans. J. Biol. Chem. (2001) 276(35):32806-32813.
99. BOUSSIF O, ZANTA MA, BEHR JP: Optimized galenics improve in vitro gene transfer with cationic molecules up to 1000-fold. Gene Ther. (1996) 3(12):1074-1080.
100. KANEDA Y, SAEKI Y, NAKABAYASHI M et al.: Enhancement of transgene expression by cotransfection of oriP plasmid with EBNA-1 expression vector. Hum. Gene Ther. (2000) 11(3):471-479.
101. ZHANG X, COLLINS L, FABRE JW: A powerful cooperative interaction between a fusogenic peptide and lipofectamine for the enhancement of receptor-targeted, non-viral gene delivery via integrin receptors. J. Gene Med. (2001) 3(6):560-568.
102. COLIN M, MAURICE M, TRUGNAN G et al.: Cell delivery, intracellular trafficking and expression of an integrin-mediated gene transfer vector in tracheal epithelial cells. Gene Ther. (2000) 7(2):139-152.
103. VAYSSE L, BURGELIN I, MERLIO JP, ARVEILER B: Improved transfection using epithelial cell line-selected ligands and fusogenic peptides. Biochem. Biophys. Acta (2000) 1475(3):369-376.
104. ARANCIBIA-CARCAMO CV, ORAL HB, HASKARD DO, LARKIN DF, GEORGE AJ: Lipoadenofection-mediated gene delivery to the corneal endothelium: prospects for modulating graft rejection. Transplantation (1998) 65(1):62-67.
105. KLINK DT, CHAO S, GLICK MC, SCANLIN TF: Nuclear translocation of lactosylated poly-L-lysine/cDNA complex in cystic fibrosis airway epithelial cells. Mol. Ther. (2001) 3(6):831-841
106. MURRAY KD, ETHERIDGE CJ, SHAH SI et al.: Enhanced cationic liposome-mediated transfection using the DNA-binding peptide mu (mu) from the adenovirus core. Gene Ther. (2001) 8(6):453-460.
107. TAGAWA T, MANVELL M, BROWN N et al.: Characterisation of LMD virus-like nanoparticles self-assembled from cationic liposomes, adenovirus core peptide mu and plasmid DNA. Gene Ther. (2002) 9(9):564-576.
108. SUBRAMANIAN A, RANGANATHAN P, DIAMOND SL: Nuclear targeting peptide scaffolds for lipofection of nondividing mammalian cells. Nat. Biotechnol. (1999) 17(9):873-877.
109. CARLISLE RC, BETTINGER T, OGRIS M et al.: Adenovirus hexon protein enhances nuclear delivery and increases transgene expression of polyethylenimine/plasmid DNA vectors. Mol. Ther. (2001) 4(5):473-483.
110. BRANDEN LJ, MOHAMED AJ, SMITH CI: A peptide nucleic acid-nuclear localization signal fusion that mediates nuclear transport of DNA. Nat. Biotechnol. (1999) 17(8):784-787.
111. BRISSON M, HE Y, LI S, YANG JP, HUANG L: A novel T7 RNA polymerase autogene for efficient cytoplasmic expression of target genes. Gene Ther. (1999) 6(2):263-270.
112. READ ML, SINGH S, AHMED Z et al.: A versatile reducible polycation-based system for efficient delivery of a broad range of nucleic acids. Nucleic Acids Res. (2005) 33(9):e86.
113. IVICS Z, HACKETT PB, PLASTERK RH, IZSVAK Z: Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell (1997) 91(4):501-510.
114. GROTH AC, OLIVARES EC, THYAGARAJAN B, CALOS MP: A phage integrase directs efficient site-specific integration in human cells. Proc. Natl. Acad. Sci. USA (2000) 97(11):5995-6000.
115. BAUMGARTNER I, PIECZEK A, MANOR O et al.: Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation (1998) 97(12):1114-1123.
116. TAN PH: 9th American Society of Gene Therapy Annual Meeting. Expert Opin. Biol. Ther. (2006) 6(8):839-842.
117. http://www.wiley.co.uk/genetherapy/clinical/ The Journal of Gene Medicine Clinical Trial website.