Gene-therapy delivery strategies in cardiology

Future Cardiology

Volumn 4, Issue 2, 2008, Pages 135-150

  Müller, Oliver J ^a   Ksienzyk, Jan ^a   Katus, Hugo A ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Adeno associated virus; Adenovirus; Animal models; Clinical trials; Endothelium; Gene transfer; Heart; Nonviral vector

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENOVIRUS VECTOR; ALKALINE PHOSPHATASE; BETA GALACTOSIDASE; DELTA SARCOGLYCAN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 4; GLUCAN 1,4 ALPHA GLUCOSIDASE; GLYCERYL TRINITRATE; GREEN FLUORESCENT PROTEIN; GROWTH HORMONE; HISTAMINE; LUCIFERASE; PARVOVIRUS VECTOR; PHOSPHODIESTERASE V INHIBITOR; PHOSPHOLAMBAN; PLACEBO; PLASMID DNA; SARCOGLYCAN; SEROTONIN; SODIUM CHLORIDE; TISSUE INHIBITOR OF METALLOPROTEINASE 3; VASCULOTROPIN;

ANGIOGENESIS; CARDIOPULMONARY BYPASS; CARDIOVASCULAR DISEASE; CLINICAL TRIAL; CONGESTIVE CARDIOMYOPATHY; CORONARY ARTERY DISEASE; DNA TRANSFER; GENE DELIVERY SYSTEM; GENE THERAPY; GENE VECTOR; GENETIC TRANSCRIPTION; GENETIC TRANSDUCTION; HEART ARREST; HEART FAILURE; HEART MUSCLE ISCHEMIA; HUMAN; HYPOTHERMIA; IMMUNOGENICITY; INTERMETHOD COMPARISON; NONHUMAN; PERICARDIAL EFFUSION; PRIORITY JOURNAL; REVIEW; STENOSIS;

EID: 40649121773     PISSN: 14796678     EISSN: 17448298     Source Type: Journal    
DOI: 10.2217/14796678.4.2.135     Document Type: Review

References (141)

1. Markkanen JE, Rissanen TT, Kivela A, Yla-Herttuala S: Growth factor-induced therapeutic angiogenesis and arteriogenesis in the heart - gene therapy. Cardiovasc. Res. 65, 656-664 (2005).
2. Yla-Herttuala S, Alitalo K: Gene transfer as a tool to induce therapeutic vascular growth. Nat. Med. 9, 694-701 (2003).
3. Rissanen TT, Yla-Herttuala S: Current status of cardiovascular gene therapy. Mol. Ther. 15, 1233-1247 (2007).
4. Hedman M, Hartikainen J, Syvanne M et al.: Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangloplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia: Phase II results of the Kuopio Angiogenesis Trial (KAT). Circulation 107, 2677-2683 (2003).
5. Müller OJ, Leuchs B, Pleger ST et al.: Improved cardiac gene transfer by transcriptional and transductional targeting of adeno-associated viral vectors. Cardiovasc. Res. 70, 70-78 (2006).
6. Müller OJ, Katus HA, Bekeredjian R: Targeting the heart with gene therapy-optimized gene delivery methods. Cardiovasc. Res. 73, 453-462 (2007).
7. Kastrup J, Jorgensen E, Ruck A et al.: Direct intramyocardial plasmid vascular endothelial growth factor-A165 gene therapy in patients with stable severe angina pectoris. A randomized double-blind placebo-controlled study: the Euroinject One trial. J. Am. Coll. Cardiol. 45, 982-988 (2005).
8. Kornowski R, Leon MB, Fuchs S et al.: Electromagnetic guidance for catheter-based transendocardial injection: a platform for intramyocardial angiogenesis therapy. Results in normal and ischemic porcine models. J. A. Coll. Cardiol. 35, 1031-1039 (2000).
9. Rutanen J, Rissanen TT, Markkanen JE et al.: Adenoviral catheter-mediated intramyocardial gene transfer using the mature form of vascular endothelial growth factor-D induces transmural angiogenesis in porcine heart. Circulation 109, 1029-1035 (2004).
10. Vale PR, Losordo DW, Milliken CE et al.: Randomized, single-blind, placebo-controlled pilot study of catheter-based myocardial gene transfer for therapeutic angiogenesis using left ventricular electromechanical mapping in patients with chronic myocardial ischemia. Circulation 103, 2138-2143 (2001).
11. Lyons M, Onion D, Green NK et al.: Adenovirus type 5 interactions with human blood cells may compromise systemic delivery. Mol. Ther. 14, 118-128 (2006).
12. Baker AH, McVey JH, Waddington SN, Di Paolo NC, Shayakhmetov DM: The influence of blood on in vivo adenovirus bio-distribution and transduction. Mol. Ther. 15, 1410-1416 (2007).
13. Losordo DW, Vale PR, Symes JF et al.: Gene therapy for myocardial angiogenesis: initial clinical results with direct myocardial injection of phVEGF165 as sole therapy for myocardial ischemia. Circulation 98, 2800-2804 (1998).
14. Stewart DJ, Hilton JD, Arnold JM et al.: Angiogenic gene therapy in patients with nonrevascularizable ischemic heart disease: a Phase 2 randomized, controlled trial of AdVEGF(121) (AdVEGF121) versus maximum medical treatment. Gene Ther. 13, 1503-1511 (2006).
15. Wright MJ, Wightman LM, Lilley C et al.: In vivo myocardial gene transfer: optimization, evaluation and direct comparison of gene transfer vectors. Basic Res. Cardiol. 96, 227-236 (2001).
16. French BA, Mazur W, Geske RS, Bolli R: Direct in vivo gene transfer into porcine myocardium using replication-deficient adenoviral vectors. Circulation 90, 2414-2424 (1994).
17. Ding W, Zhang L, Yan Z, Engelhardt JF: Intracellular trafficking of adeno-associated viral vectors. Gene Ther. 12, 873-880 (2005).
18. Greber UF, Willetts M, Webster P, Helenius A: Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75, 477-486 (1993).
19. Roelvink PW, Mi Lee G, Einfeld DA, Kovesdi I, Wickham TJ: Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 286, 1568-1571 (1999).
20. Summerford C, Samulski RJ: Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72, 1438-45 (1998).
21. Chirmule N, Moscioni AD, Qian Y, Qlan R, Chen Y, Wilson JM: Fas-Fas ligand interactions play a major role in effector functions of cytotoxic T lymphocytes after adenovirus vector-mediated gene transfer. Hum. Gene Ther. 10, 259-269 (1999).
22. Jooss K, Yang Y, Fisher KJ, Wilson JM: Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. J. Virol. 72, 4212-4223 (1998).
23. Yang Y, Nunes FA, Berencsi K, Furth EE, Gonczoi E, Wilson JM: Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc. Natl Acad. Sci. USA 91, 4407-4411 (1994).
24. Kochanek S, Clemens PR, Mitani K, Chen HH, Chan S, Caskey CT: A new adenoviral vector: replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and beta-galactosidase. Proc. Natl Acad. Sci. USA 93, 5731-5736 (1996).
25. Chu D, Sullivan CC, Weitzman MD et al.: Direct comparison of efficiency and stability of gene transfer into the mammalian heart using adeno-associated virus versus adenovirus vectors. J Thorac. Cardiovasc Surg. 126, 671-679 (2003).
26. Vassalli G, Bueler H, Dudler J, von Segesser LK, Kappenberger L: Adeno-associated virus (AAV) vectors achieve prolonged transgene expression in mouse myocardium and arteries in vivo: a comparative study with adenovirus vectors. Int. J. Cardiol. 90, 229-238 (2003).
27. Jiang H, Pierce GF, Ozelo, MC et al.: Evidence of multiyear factor IX expression by AAV mediated gene transfer to skeletal muscle in an individual with severe hemophilia B. Mol. Ther. 14, 452-455 (2006).
28. Nakai H, Montini E, Fuess S, Storm TA, Grompe M, Kay MA: AAV serotype 2 vectors preferentially integrate into active genes in mice. Nat. Genet. 34, 297-302 (2003).
29. McCarty DM, Young SM Jr, Samulski RJ: Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu. Rev. Genet. 38, 819-845 (2004).
30. Schnepp BC, Jensen RL, Chen CL, Johnson PR, Clark KR: Characterization of adeno-associated virus genomes isolated from human tissues. J. Virol. 79, 14793-14803 (2005).
31. Donsante A, Miller DG, Li Y et al.: AAV vector integration sites in mouse hepatocellular carcinoma. Science 317, 477 (2007).
32. Kay MA: AAV vectors and tumorigenicity. Nat. Biotechnol. 25, 1111-1113 (2007).
33. Melo LG, Agrawal R, Zhang L et al.: Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene. Circulation 105, 602-607 (2002).
34. Hoshijima M, Ikeda Y, Iwanaga Y et al.: Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nat. Med. 8, 864-871 (2002).
35. Kawada T, Nakazawa M, Nakauchi S et al.: Rescue of hereditary form of dilated cardiomyopathy by rAAV-mediated somatic gene therapy: amelioration of morphological findings, sarcolenimal permeability, cardiac performances, and the prognosis of TO-2 hamsters. Proc. Natl Acad. Sci. USA 99, 901-906 (2002).
36. Su H, Joho S, Huang Y et al.: Adeno-associated viral vector delivers cardiac-specific and hypoxia-inducible VEGF expression in ischemic mouse hearts. Proc. Natl Acad. Sci. USA 101, 16280-16285 (2004).
37. Gregorevic P, Blankinship MJ, Allen JM et al.: Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat. Med. 10, 828-834 (2004).
38. Inagaki K, Fuess S, Storm TA et al.: Robust systemic with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol. Ther. 14, 45-53 (2006).
39. Nakai H, Fuess S, Storm TA, Muramatsu S, Nara Y, Kay MA: Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice. J. Virol. 79, 214-224 (2005).
40. Pacak CA, Mah CS, Thattaliyath BD et al.: Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ. Res. 99, E3-E9 (2006).
41. Zhu T, Zhou L, Mori S et al.: Sustained whole-body functional rescue in congestive heart failure and muscular dystrophy. hamsters by systemic gene transfer. Circulation 112, 2650-2659 (2005).
42. Du L, Kido M, Lee DV et al.: Differential myocardial gene delivery by recombinant serotype-specific adeno-associated viral vectors. Mol. Ther. 10, 604-608 (2004).
43. Palomeque J, Chemaly ER, Colosi P et al.: Efficiency of eight different AAV serotypes in transducing rat myocardium in vivo. Gene Ther. 14, 1055 (2007).
44. Raake P, Hinkel R, Müller S et al.: Cardio-specific long-term gene expression in a porcine model after selective pressure-regulated retroinfusion of adeno-associated viral (AAV) vectors. Gene Ther. 15(1), 12-17 (2008).
45. Sasano T, Kikuchi K, McDonald AD, Lai S, Donahue JK: Targeted high-efficiency, homogeneous myocardial gene transfer. J. Mol. Cell. Cardiol. 42, 954-961 (2007).
46. Brooks AR, Harkins RN, Wang P, Qian HS, Liu P, Rubanyi GM: Transcriptional silencing is associated with extensive methylation of the CMV promoter following adenoviral gene delivery to muscle. J. Gene Med. 6, 395-404 (2004).
47. Qin L, Ding Y, Pahud DR, Chang E, Imperiale MJ, Bromberg JS: Promoter attenuation in gene therapy: interferon-γ and tumor necrosis factor-α inhibit transgene expression. Hum Gene Ther. 8, 2019-2029 (1997).
48. Wang Z, Zhu T, Qiao C et al.: Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat. Biotechnol. 23, 321-328 (2005).
49. Kawamoto S, Shi Q, Nitta Y, Miyazaki J, Allen MD: Widespread and early myocardial gene expression by adeno-associated virus vector type 6 with a β-actin hybrid promoter. Mol. Ther. 11, 980-985 (2005).
50. Cordier L, Gao GR Hack AA et al.: Muscle-specific promoters may be necessary for adeno-associated virus-mediated gene transfer in the treatment of muscular dystrophies. Hum. Gene Ther. 12, 205-215 (2001).
51. Scdiedner G, Hertel S, Johnston M, Biermann V. D ries V, Kochanek S: Variables affecting in vivo performance of high-capacity adenovirus vectors. J. Virol. 76, 1600-1609 (2002).
52. Salva MZ, Himeda CL, Tai PW et al.: Design of tissue-specific regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol. Ther. 15, 320-329 (2007).
53. Franz WM, Rothmann T, Frey N, Katus HA: Analysis of tissue-specific gene delivery by recombinant adenoviruses containing cardiac-specific promoters. Cardiovasc. Res. 35, 560-566 (1997).
54. Aikawa R, Huggins GS, Snyder RO: Cardiomyocyte-specific gene expression following recombinant adeno-assoclated viral vector transduction. J. Biol. Chem. 277, 18979-18985 (2002).
55. Boecker W, Bernecker OY, Wu JC et al.: Cardiac-specific gene expression facilitated by an enhanced myosin light chain promoter. Mol. Imaging 3, 69-75 (2004).
56. Champion HC, Georgakopoulos D, Haldar S, Wang L, Wang Y, Kass DA: Robust adenoviral and adeno-associated viral gene transfer to the in vivo murine heart: application to study of phospholamban physiology. Circulation 108, 2790-2797 (2003).
57. Griscelli F, Gilardi-Hebenstreit P, Hanania N et al.: Heart-specific targeting of β-galactosidase by the ventricle-specific cardiac myosin light chain 2 promoter using adenovirus vectors. Hum. Gene Ther. 9, 1919-1928 (1998).
58. Phillips MI, Tang Y, Schmidt-Ott K, Qian K, Kagiyama S: Vigilant vector heart-specific promoter in an adeno-associated virus vector for cardioprotection. Hypertension 39, 651-655 (2002).
59. Pleger ST, Most B, Boucher M et al.: Stable myocardial-specific AAV6-S100A1 gene therapy results in chronic functional heart failure rescue. Circulation 115, 2506-2515 (2007).
60. Pachori AS, Melo LG, Hart ML et al.: Hypoxia-regulated therapeutic gene as a preemptive treatment strategy against ischemia/reperfusion tissue injury. Proc. Natl Acad. Sci. USA 101, 12282-12287 (2004).
61. Pajusola K, Gruchala M, Joch H, Luscher TF, Yla-Herttuala S, Bueler H: Cell-type-specific characteristics modulate the transduction efficiency of adeno-associated virus type 2 and restrain infection of endothelial cells. J. Virol. 76, 11530-11540 (2002).
62. Hayashi K, Hayashi M, Jalkanen M, Firestone JH, Trelstad RL, Bernfield M: Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissues. A light and electron microscopic study. J. Histochim. Cytochem. 35, 1079-1088 (1987).
63. Kern A, Schmidt K, Leder C et al: Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J. Virol. 77, 11072-11081 (2003).
64. Smith TA, Idamakanti N, Rollence ML et al.: Adenovirus serotype 5 fiber shaft influences In vivo gene transfer in mice. Hum. Gene Ther. 14, 777-787 (2003).
65. Nicol CG, Graham D, Miller WH et al.: Effect of adenovirus serotype 5 fiber and penton modifications on in vivo tropism in rats. Mol. Ther. 10, 344-354 (2004).
66. Kritz AB, Nicol CG, Dishart KL et al.: Adenovirus 5 fibers mutated at the putative HSPG-binding site show restricted retargeting with targeting peptides in the HI loop. Mol. Ther. 15, 741-749 (2007).
67. Waddington SN, Parker AL, Havenga M et al.: Targeting of adenovirus serotype 5 (Ad5) and 5/47 pseudotyped vectors in vivo: fundamental Involvement of coagulation factors and redundancy of CAR binding by Ad5. J. Virol. 81, 9568-9571 (2007).
68. Müllier OJ, Kaul F, Weitzman MD et al.: Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat. Biotechnol. 21, 1040-1046 (2003).
69. Perabo L, Buning H, Kofler DM et al.: In vitro selection of viral vectors with modified tropism: the adeno-associated virus display. Mol. Ther. 8, 151-157 (2003).
70. Reilly JP, Grise MA, Fortuin FD et al.: Long-term (2-year) clinical events following transthoracic intramyocardial gene transfer of VEGF-2 in no-option patients. J. Interv. Cardiol. 18, 27-31 (2005).
71. Svensson EC, Marshall DJ, Woodard K et al.: Efficient and stable transduction of cardiomyocytes after intramyocardial Injection or intracoronary perfusion with recombinant adeno-associated virus vectors. Circulation 99, 201-205 (1999).
72. St Michael's, NOGA Angiogenesis Revascularization Therapy: Evaluation by radionuclide Imaging - the Northern trial, Phase II & III clinical trial. St Michael's Hospital, Toronto, Canada. Principal Investigator: Stewart DJ (2007).
73. Corautus, GENASIS, Severe Angina Phase IIb clinical trial. Corautus Genetics Inc., GA, USA (2007).
74. Lamping KG, Rios CD, Chun JA, Ooboshi H, Davidson BL, Heistad DD: Intrapericardial administration of adenovirus for gene transfer. Am. J. Physiol. 272, H310-H317 (1997).
75. March KL, Woody M, Mehdi K, Zipes DP, Brantly M, Trapnell BC: Efficient In vivo catheter-based pericardial gene transfer mediated by adenoviral vectors. Clin. Cardiol. 22, 123429 (1999).
76. Lal NC, Roth DM, Gan MH et al.: Intracoronary delivery of adenovirus encoding adenylyl cyclase VI increases left ventricular function and cAMP-generating capacity. Circulation 102, 2396-2401 (2000).
77. Grines CL, Watkins MW, Mahmarian JJ et al.: Angiogene GENe Therapy (AGENT-2) study group: A randomized, double-blind, placebo-controlled trial of Ad5FGF-4 gene therapy and its effect on myocardial perfusion in patients with stable angina. J. Am. Coll. Cardiol. 42, 1339-1347 (2003).
78. Henry TD, Grines CL, Watkinssfay MW et al.: Effects of Ad5FGF-4 in patients with angina: an analysis of pooled data from the AGENT-3 and AGENT-4 trials. J. Am. Call. Cardiol. 50, 1038-1046 (2007).
79. Moreadith R: Cardium therapeutics: Angiogenesis in Women with Angina Pectoris Who Are Not Candidates for Revascularization (AWARE) Phase III clinical trial. (2007).
80. Phase I clinical trial of MYDICAR AAV1/SERCA2a) in patients with cardiomyopathy and symptoms of heart failure. Celladon Corporation and Targeted Genetics Corporation, CA, USA (2007).
81. Donahue JK, Kikkawa K, Johns DC, Marban E, Lawrence JH: Ultrarapid, highly efficient viral gene transfer to the heart. Proc. Natl. Acad. Sci. USA 94, 466u4-4668 (1997).
82. Donahue JK, Kikkawa K, Thomas AD, Marban E, Lawrence JH: Acceleration of widespread adenoviral gene transfer to intact rabbit hearts by coronary perfusion with low calcium and serotonin. Gene Ther. 5, 630-634 (1998).
83. Logeart D, Hatern SN, Heimburger M, Le Roux A, Michel JB, Mercadier JJ: How to optimize in vivo gene transfer to cardiac myocytes: mechanical or pharmacological procedures? Hum. Geen Ther. 12, 1601-1610 (2001).
84. Raake P, von Degenfeld G, Hinkel R et al.: Myocardial gene transfer by selective pressure-regulated retroinfusion of coronary veins: comparison with surgical and percutaneous intramyocardial gene delivery. J. Am. Coll. Cardiol. 44, 1124-1129 (2004).
85. Nagata K, Marban E, Lawrence JH, Donahue JK: Phosphodiesterase inhibitor-mediated potentiation of adenovirus delivery to myocardium. J. Mol. Cell. Cardiol. 33, 575-580 (2001).
86. Beeri R, Guerrero JL, Supple G, Sullivan S, Levine RA, Hajjar RJ: New efficient catheter-based system for myocardial gene delivery Circulation 106, 1756-1759 (2002).
87. Bekeredjian R, Chen S, Frenkel PA, Grayburn PA, Shohet RV: Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 108, 1022-1026 (2003).
88. Shohet RV, Chen S, Zhou YT et al.: Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation 101, 2554-2556 (2000).
89. Hajjar RJ, Schmidt U, Matsui T et al.: Modulation of ventricular function through gene transfer in vivo. Proc. Natl Acad. Sci. USA 95, 5251-5256 (1998).
90. Ding Z, Fach C, Sasse A, Godecke A, Schrader J: A minimally invasive approach for efficient gene delivery to rodent hearts. Gene Ther. 11, 260-265 (2004).
91. Ikeda Y, Gu Y, Iwanaga Y et al.: Restoration of deficient membrane proteins in the cardiomyopathic hamster by in vivo cardiac gene transfer. Circulation 105, 502-508 (2002).
92. Iwanaga Y. Hoshyima M, Gu Y et al.: Chronic phospholamban inhibition prevents progressive cardiac dysfunction and pathological remodeling after infarction in rats. J. Clin. Invest. 113, 727-736 (2004).
93. Iwatate M, Gu Y, Dieterle T et al.: In vivo high-efficiency transcoronary gene delivery and Cre-LaxP gene switching in the adult mouse heart. Gene Ther. 10, 1814-1820 (2003).
94. Davidson MJ, Jones JM, Emani SM et al.: Cardiac gene delivery with cardiopulmonary bypass. Circulation 104, 131-133 (2001).
95. Boekstegers P, von Degenfeld G, Giehrl W et al.: Myocardial gene transfer by selective pressure-regulated retroinfusion of coronary veins. Gene Ther. 7, 232-240 (2000).
96. Hayase M, Del Monte F, Kawase Y et al.: Catheter-based antegrade intracoronary viral gene delivery with coronary venous blockade. Am. J. Physiol. Heart Circ. Physiol. 288, H2995-H3000 (2005).
97. Kaye DM, Preovolos A, Marshall T et al.: Percutaneous cardiac recirculation-mediated gene transfer of an inhibitory phospholamban peptide reverses advanced heart failure in large animals. J. Am. Coll. Cardiol. 50, 253-260 (2007).
98. Children's, Phase 1 clinical trial of rAAV2.5-CMV-Mini-Dystrophin Gene Vector in Duchenne Muscular Dystrophy. Nationwide Children's Hospital and Asklepios Biopharmaceutical Inc., NC, USA. Principal Investigator: Mendell JR. (2007).
99. Sun B, Zhang H, Franco LM et al.: Correction of glycogen storage disease type II by an adeno-associated virus vector containing a muscle-specific promoter. Mol. Ther. 11, 889-898 (2005).
100. Vandendriessche T Thorrez L, Acosta-Sanchez A et al.: Efficacy and safety of adeno-associated viral vectors based on serotype 8 and 9 vs. lentiviral vectors for hemophilia B gene therapy. J. Thromb. Haemost. 5, 16-24 (2007).
101. Steg PG, Feldman LJ, Scoazec JY et al.: Arterial gene transfer to rabbit endothelial and smooth muscle cells using percutaneous delivery of an adenoviral vector. Circulation 90, 1648-1656 (1994).
102. Wen S, Graf S, Massey PG, Dichek DA: Improved vascular gene transfer with a helper-dependent adenoviral vector. Circulation 110, 1484-1491 (2004).
103. Gruchala M, Bhardwaj S, Pajusola K et al.: Gene transfer into rabbit arteries with adeno-associated virus and adenovirus vectors. J. Gene Med. 6, 545-554 (2004).
104. Totsugawa T, Kobayashi N, Okitsu T et al.: Lentiviral transfer of the LacZ gene into human endothelial cells and human bone marrow mesenchymal stem cells. Cell Transplant. 11, 481-488 (2002).
105. Totsugawa T, Kobayashi N, Maruyama M et al.: Successful lentivirus-based delivery of a LacZ gene into human endothelial cells. Transplant. Proc. 35, 499-500 (2003).
106. Totsugawa T, Kobayashi N, Maruyama M et al.: Lentiviral vector: a useful tool for transduction of human liver endothelial cells. ASAIO J. 49, 635-640 (2003).
107. De Palma M, Venneri MA, Naldini L: In vivo targeting of tumor endothelial cells by systemic delivery of lentiviral vectors. Hum. Gene Ther. 14, 1193-1206 (2003).
108. Denby L, Nicklin SA, Baker AH: Adeno-associated virus (AAV)-7 and -8 poorly transduce vascular endothelial cells and are sensitive to proteasomal degradation. Gene Ther. 12, 1534-1538 (2005).
109. Chen S, Kapturczak M, Loiler SA et al.: Efficient transduction of vascular endothelial cells with recombinant adeno-associated virus serotype 1 and 5 vectors. Hum. Gene Ther. 16, 235-247 (2005).
110. Nicklin SA, Buening H, Dishart KL et al.: Efficient and selective AAV2-mediated gene transfer directed to human vascular endothelial cells. Mol. Ther. 4, 174-181 (2001).
111. White SJ, Nicklin SA, Buning H et al.: Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 109, 513-519 (2004).
112. Work LM, Buning H, Hunt E et al.: Vascular bed-targeted in vivo gene delivery using tropism-modified adeno-associated viruses. Mol. Ther. 13, 683-693 (2006).
113. Miller WH, Broman MJ, Graham D et al.: Targeting endothelial cells with adenovirus expressing nitric oxide synthase prevents elevation of blood pressure in stroke-prone spontaneously hypertensive rats. Mol. Ther. 12, 321-327 (2005).
114. Reynolds PN, Zinn KR, Gavrilyuk VD et al.: A targetable, injectable adenoviral vector for selective gene delivery to pulmonary endothelium in vivo. Mol. Ther. 2, 562-578 (2000).
115. Reynolds PN, Nicklin SA, Kaliberova L et al.: Combined transductional and transcriptional targeting improves the specificity of transgene expression in vivo. Nat. Biotechnol. 19, 838-842 (2001).
116. Waterkamp DA, Müller OJ, Ying Y, Trepel M, Kleinschmidt JA: Isolation of targeted AAV2 vectors from novel virus display libraries. J. Gene Med. 8, 1307-1319 (2006).
117. Iljin K, Dube A, Kontusaari S et al.: Role of ets factors in the activity and endothelial cell specificity of the mouse Tie gene promoter. FASEB J. 13, 377-386 (1999).
118. Hewett PW, Daft EL, Murray JC: Cloning and partial characterization of the human tie-2 receptor tyrosine kinase gene promoter. Biochem. Biophys. Res. Commun. 252, 546-551 (1998).
119. Korhonen J, Lahtinen I, Halmekyto M et al.: Endothelial-specific gene expression directed by the tie gene promoter in vivo. Blood 86, 1828-1835 (1995).
120. Cho J, Lim W, Jang S, Lee Y: Development of an efficient endothelial cell specific vector using promoter and 5′ untranslated sequences from the human preproendothelin-1 gene. Exp. Mol. Med. 35, 269-274 (2003).
121. Gory S, Vernet M, Laurent M, Dejana E, Dalmon J, Huber P: The vascular endothelial-cadherin promoter directs endothelial-specific expression in transgenic mice. Blood 93, 184-192 (1999).
122. Hegen A, Koidl S, Weindel K, Marme D, Augustin HG, Fiedler U: Expression of angiopoietin-2 in endothelial cells is controlled by positive and negative regulatory promoter elements. Arterioscler. Thromb. Vasc. Biol.. 24, 1803-1809 (2004).
123. Schlaeger TM, Bartunkova S, Lawitts JA et al.: Uniform vascular-endothelial-cell-specific gene expression in both embryonic and adult transgenic mice. Proc. Natl Acad. Sci. USA 94, 3058-3063 (1997).
124. Rome JJ, Shayani V, Newman KD et al.: Adenoviral vector-mediated gene transfer into sheep arteries using a double-balloon catheter. Hum. Gene Ther. 5, 1249-1258 (1994).
125. Sharif F, Hynes SO, McMahon J et al.: Gene-eluting stents: comparison of adenoviral and adeno- associated viral gene delivery to the blood vessel wall in vivo. Hum. Gene Ther. 17, 741-750 (2006).
126. Walter DH, Cejna M, Diaz-Sandoval L et al.: Local gene transfer of ph VEGF-2 plasmid by gene-eluting stents: an alternative strategy for inhibition of restenosis. Circulation 110, 36-45 (2004).
127. Nikol S, Huehns TY, Krausz E et al.: Needle injection catheter delivery of the gene for an antibacterial agent inhibits neointimal formation. Gene Ther. 6, 737-748 (1999).
128. Baker AH, Yim AP, Wan S: Opportunities for gene therapy in preventing vein graft failure after coronary artery bypass surgery. Diabetes Obes. Metab. 8, 119-124 (2006).
129. Bryan AJ, Angelini GD: The biology of saphenous vein graft occlusion: etiology and strategies for prevention. Curr. Opin. Cardiol. 9, 641-649 (1994).
130. Cox JL, Chiasson DA, Gotlieb, AI: Stranger in a strange land: the pathogenesis of saphenous vein graft stenosis with emphasis on structural and functional differences between veins and arteries. Prog. Cardiovasc. Dis. 34, 45-68 (1991).
131. Davies MG, Hagen PO: Pathobiology of intimal hyperplasia. Br. J. Surg. 81, 1254-1269 (1994).
132. Bhardwaj S, Roy H, Heikura T, Yla-Herttuala S: VEGF-A, VEGF-D and VEGF-D(δNδC) induced intimal hyperplasia in carotid arterles. Eur J. Clin. Invest. 35, 669-676 (2005).
133. Khurana R, Zhuang Z, Bhardwaj S et al.: Anglogenesis-dependent and independent phases of intimal hyperplasia. Circulation 110, 2436-2443 (2004).
134. Lemstrom KB, Krebs R, Nykanen AI et al.: Vascular endothelial growth factor enhances cardiac allograft arteriosclerosis. Circulation 105, 2524-2530 (2002).
135. Yla-Herttuala S, Markkanen JE, Rissanen TT: Gene therapy for ischemic cardiovascular diseases: some lessons learned from the first clinical trials. Trends Cardiovasc. Med. 14, 295-300 (2004).
136. George SJ, Johnson JL, Angelini GD, Newby AC, Baker AH: Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits smooth muscle cell migration and neointimal formation in human saphenous vein. Hum. Gene Ther. 9, 867-877 (1998).
137. George SJ, Lloyd CT, Angelini GD, Newby AC, Baker AH: Inhibition of late vein graft neointima formation in human and porcine models by adenovirus-mediated overexpression of tissue inhibitor of metalloproteinase-3. Circulation 101, 296-304 (2000).
138. Channon KM, Fulton GJ, Gray JL et al.: Efficient adenoviral gene transfer to early venous bypass grafts: comparison with native vessels. Cardiovasc. Res. 35, 505-513 (1997).
139. Akowuah EF, Gray C, Lawrie A et al.: Ultrasound-mediated delivery of TIMP-3 plasmid DNA into saphenous vein leads to increased lumen size in a porcine interposition graft model. Gene Ther. 12, 1154-1157 (2005).
140. Franz WM, Mueller OJ, Hartong R, Frey N, Katus HA: Transgenic animal models: new avenues in cardiovascular physiology. J. Mol. Med. 75, 115-129 (1997).
141. LaPointe MC, Yan XP, Carretero OA, He Q: Left ventricular targeting of reporter gene expression in vivo by human BNP promoter in an adenoviral vector. Am. J. Physiol. Heart Circ. Physiol. 283, H1439-H1445 (2002).