Therapeutic myocardial angiogenesis with vascular endothelial growth factors

Molecular and Cellular Biochemistry

Volumn 264, Issue 1-2, 2004, Pages 63-74

  Yoon, Young Sup ^a   Johnson, Ingrid A ^a   Park, Jong Seon ^a   Diaz, Larry ^a   Losordo, Douglas W ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gene therapy; Myocardium; Neovascularization; Vascular endothelial growth factor (VEGF)

Indexed keywords

ADENOVIRUS VECTOR; NAKED DNA; PLACEBO; PLASMID DNA; RECOMBINANT PROTEIN; RECOMBINANT VASCULOTROPIN; RECOMBINANT VASCULOTROPIN 165; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN 1; VASCULOTROPIN 121; VASCULOTROPIN 145; VASCULOTROPIN 183; VASCULOTROPIN 189; VASCULOTROPIN 206; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGINA PECTORIS; ANGIOGENESIS; BONE MARROW; CARDIOVASCULAR DISEASE; CLINICAL TRIAL; CORONARY ARTERY BYPASS GRAFT; CORONARY ARTERY DISEASE; DISEASE MODEL; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; EDEMA; EXERCISE; GENE EXPRESSION; GENE TRANSFER; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE ISCHEMIA; HEART MUSCLE REVASCULARIZATION; HUMAN; HYPOTENSION; IN VIVO STUDY; INTRACORONARY INFUSION; LIMB ISCHEMIA; NONHUMAN; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PROTEIN BINDING; REVIEW; RISK ASSESSMENT; STEM CELL; SYMPTOMATOLOGY; THORACOTOMY; TISSUE PERFUSION;

ANIMALS; BLOOD VESSELS; CLINICAL TRIALS; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; MODELS, BIOLOGICAL; MYOCARDIAL ISCHEMIA; NEOVASCULARIZATION, PHYSIOLOGIC; RECOMBINANT PROTEINS; VASCULAR DISEASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA;

EID: 5644294560     PISSN: 03008177     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:MCBI.0000044375.33928.62     Document Type: Review

References (119)

1. Folkman J: Tumor angiogenesis: Therapeutic implications. New Engl J Med 285: 1182-1186, 1971
2. Takeshita S, Zheng LP, Brogi E, Kearney M, Pit LQ, Bunting S, Ferrara N, Symes JF, Isner JM: Therapeutic angiogenesis: A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hindlimb model. J Clin Invest 93: 662-670, 1994
3. 165. Lancet 348: 370-374, 1996
4. Isner JM, Walsh K, Symes J, Pieczek A, Takeshita S, Lowry J, Rosenfield K, Weir L, Brogi E, Jurayj D: Arterial gene transfer for therapeutic angiogenesis in patients with peripheral artery disease. Hum Gene Ther 7: 959-988, 1996
5. Mukherjee D, Bhatt DL, Roe MT, Patel V, Ellis SG: Direct myocardial revascularization and angiogenesis - how many patients might be eligible? Am J Cardiol 84: 598-600, 1999
6. Gilbert SF: Developmental Biology, 4th edn. Smarter Associates, Sunderland, MA, 1997
7. Flamme I, Risau W: Induction of vasculogenesis and hematopoiesis in vitro. Development 116: 435-439, 1992
8. Risau W, Flamme I: Vasculogenesis. Annual review of cell developmental biology 11: 73-91, 1995
9. Risau W: Differentiation of endothelium. EASEB J 9: 926-933, 1995
10. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM: Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967, 1997
11. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM: VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J 18: 3964-3972, 1999
12. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T: Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5: 434-438, 1999
13. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T: Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA 97: 3422-3427, 2000
14. Arras M, Ito WD, Scholz D, Winkler B, Schaper J, Schaper W: Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest 101: 40-50, 1998
15. Isner JM: Tissue responsLs to ischemia: local and remote responses for preserving perfusion of ischemic muscle. J Clin Invest 106: 615-619, 2000
16. Goldberg MA, Schneider TJ: Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J Biol Chem 269: 4355-4359, 1994
17. Forsythe JA, Jiang BH, Lyer NV, Agani F, Leung SW, Koos RD, Semenza GL: Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613, 1996
18. Levy AP, Levy NS, Goldberg MA: Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J Biol Chem 371: 2746-2753, 1996
19. Ferrara N: VEGF and the quest for tumour angiogenesis factors. Nat Rev Cancer 2: 795-803, 2002
20. Carmeliet P: Mechanisms of angiogenesis and arteriogenesis. Nat Med 6: 389-395, 2000
21. Ferrara N, Davis-Smyth: The biology of vascular endothelial growth factor. Endocr Rev 18: 4-25, 1997
22. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z: Vascular endothelial growth factor (VEGF) and its receptors. EASEB J 13: 9-22, 1999
23. Ferrara N, Henzel WJ: Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 161: 851-855, 1989
24. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N: Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267: 26031-26037, 1992
25. Takeshita S, Tsurumi Y, Couffinhal T, Asahara T, Bauters C, Symes JF, Ferrara N, Isner JM: Gene transfer of naked DNA encoding for three isoforms of vascular endothelial growth factor stimulates collateral development in vivo. Lab Invest 75: 487-502, 1996
26. Takeshita S, Weir L, Chen D, Zheng LP, Riessen R, Bauters C, Symes JF, Ferrara N, Isner JM: Therapeutic angiogenesis following arterial gene transfer of vascular endothelial growth factor in a rabbit model of hindlimb ischemia. BiochemBiophys Res Commum 227: 628-635, 1996
27. Broxmeyer HE, Cooper S, Li ZH, Song H-Y, Kwon BS, Warren RE, Donner DB: Myeloid progenitor cell regulatory effects of vascular endothelial cell growth factor. Int J Hematol 62: 203-215, 1995
28. Gerber HP, Malik AK, Solar GP, Sherman D, Liang XH, Meng G, Hong K, Marsters JC, Ferrara N: VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 417: 954-958, 2002
29. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu X-F, Breitman ML, Schuh AC: Failure of blood-island formation and vasculogenesis in Flk-1 deficient mice Nature 376: 62-66, 1995
30. Carmeliet P, Collen D: Molecular analysis of blood vessel formation and disease. Am J Physiol 273: H2091-H2104, 1997
31. Fong GH, Rossant J, Gertsenstein M, Breitman ML: Role of flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376: 66-70, 1995
32. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ, Carmeliet P: Revascularization of ischemic tissues by PIGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-flt1. Nat Med 8: 831-840, 2002
33. Kaipainen A, Korhonen J, Mustonen T, van Hinsbergh VWM, Fang T-H, Dumont D, Breitman M, Alitalo K: Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Nat Acad Sci USA 92: 3566-3570, 1995
34. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K: A Novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15: 290-298, 1996
35. Yoon YS, Murayama T, Gravereaux E, Tkebuchava T, Silver M, Curry C, Wecker A, Kirchmair R, Hu CS, Kearney M, Ashare A, Jackson DG, Kubo H, Isner JM, Losordo DW: VEGF-C gene therapy augments postnatal lymphangiogenesis and ameliorates secondary lymphedema. J Clin Invest 111: 717-725, 2003
36. Witzenbichler B, Asahara T, Murohara T, Silver M, Spyridopoulos I, Magner M, Principe N, Kearney M, Hu J-S, Isner JM: Vascular endothelial growth factor-C (VEGF-C/VEGF-2) promotes angiogenesis in the setting of tissue ischemia. Am J Pathol 153: 381-394, 1998
37. Waltenberger J, Mayr U, Pentz S, Hombach V: Functional upregulation of the vascular endothelial growth factor receptor KDR by hypoxia. Circulation 94: 1647-1654, 1996
38. Li J, Brown LF, Hibberd MG, Grossman JD, Morgan JP, Simons M: VEGF, flk-1, and flt-1 expression in a rat myocardial infarction model of angiogenesis. Am J Physiol 270: H1803-H1811, 1996
39. Namiki A, Brogi E, Kearney M, Wu T, Couffinhal T, Varticovski L, Isner JM: Hypoxia induces vascular endothelial growth factor in cultured human endothelial cells. J Biol Chem 270: 31189-31195, 1995
40. Kalka C, Masuda H, Takahashi T, Gordon R, Tepper O, Gravereaux E, Pieczek A, Iwaguro H, Hayashi SI, Isner JM, Asahara T: Vascular endothelial growth factor(165) gene transfer augments circulating endothelial progenitor cells in human subjects. Circ Res 86: 1198-1202, 2000
41. 165 in patients with inoperable coronary disease. Ann Thorac Surg 70: 829-834, 2000
42. Rivard A, Fabre J-E, Silver M, Chen D, Murohara T, Kearney M, Magner M, Isner JM: Age-dependent impairment of angiogenesis. Circulation 99: 111-120, 1999
43. Rivard A, Silver M, Chen D, Kearney M, Magner M, Annex B, Peters K, Isner JM: Rescue of diabetes-related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol 154: 355-363, 1999
44. Yoon YS US, Masuo O, Cejna M, Park JS, Gwon HC, Kirchmair R, Bahlman F, Curry C, Hanley A, Isner JM, Losordo DW: VEGF plays a central role in the development of diabetic cardiomyopathy and gene transfer of vascular endothelial growth factor(VEGF) improves heart failure in long-standing streptozotocin-induced diabetic rats. J Clin Invest (submitted)
45. -/- Mice. Circulation 99: 3188-3198, 1999
46. Schultz A, Lavie L, Hochberg I, Beyar R, Stone T, Skorecki K, Lavie P, Roguin A, Levy AP: Interindividual heterogeneity in the hypoxic regulation of VEGF: Significance for the development of the coronary artery collateral circulation. Circulation 100: 547-552, 1999
47. Rivard A, Silver M, Chen D, Kearney M, Magner M, Annex B, Peters K, Isner JM: Rescue of diabetes related impairment of angiogenesis by intramuscular gene therapy with adeno-VEGF. Am J Pathol 154: 355-364, 1999
48. Isner JM, Asahara T: Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization (Perspective). J Clin Invest 103: 1231-1236, 1999
49. Asahara T, Kalka C, Isner JM: Stem cell therapy and gene transfer for regeneration. Gene Ther 7: 451-457, 2000
50. Hariawala MD, Horowitz JR, Esakof D, Sheriff DD, Walter DH, Keyt B, Isner JM, Symes JF: VEGF improves myocardial blood flow but produces EDRF-mediated hypotension in porcine hearts. J Surg Res 63: 77-82, 1996
51. Baumgartner I, Rauh G, Pieczek A, Wuensch D, Magner M, Kearney M, Schainfeld R, Isner JM; Lower-extremity edema associated with gene transfer of naked DNA vascular endothelial growth factor. Ann Int Med 132: 880-884, 2000
52. Lazarous DF, Shou M, Stiber JA, Dadhania DM, Thirumurti V, Hodge E, Unger EF: Pharmacodynamics of basic fibroblast growth factor: Route of administration determines myocardial and systemic distribution. Cardiovasc Res 36: 78-85, 1997
53. Giordano FJ, Ping P, McKirnan MD, Nozaki S, DeMaria AN, Dillmann WH, Mathieu-Costello O, Hammond HK: Intracoronary gene transfer of fibroblast growth factor-5 increases blood flow and contractile function in an ischemic region of the heart. Nat Med 2: 534-539, 1996
54. Wolff JA, Ludtke JJ, Acsadi G, Williams P, Jani A: Long-term persistence of plasmid DNA and foreign gene expression in mouse muscle. Hum Mol Genet 1: 363-369, 1992
55. Tsurumi Y, Takeshita S, Chen D, Kearney M, Rossow ST, Passeri J, Horowitz JR, Symes JF: Direct intramuscular gene transfer of naked DNA encoding vascular endothelial growth factor augments collateral development and tissue perfusion. Circulation 94: 3281-3290, 1996
56. Takeshita S, Isshiki T, Sato T: Increased expression of direct gene transfer into skeletal muscles observed after acute ischemic injury in rats. Lab Invest 74: 1061-1065, 1996
57. 125I-labeled basic fibroblast growth factor (bFGF) favor intramyocardial delivery. J Am Coll Cardiol 35: 10A, 2000
58. Schaper W, Munoz-Chapuli R, Wolf C, Ito W: Collateral circulation of the heart. In: J.A. Ware, M. Simons (eds). Angiogenesis and Cardiovascular Disease, 159th edn. Oxford University Press, New York, , 1999, pp 159-198
59. Lopez JJ, Laham RJ, Stamler A, Pearlman JD, Bunting S, Kaplan A, Carrozza JP, Sellke FW, Simons M: VEGF administration in chronic myocardial ischemia in pigs. Cardiovasc Res 40: 272-281, 1998
60. Harada K, Friedman M, Lopez JJ, Wang SY, Li J, Prasad PV, Pearlman JD, Edelman ER, Sellke FW, Simons M: Vascular endothelial growth factor in chronic myocardial ischemia. Am J Physiol 270: H1791-H1802, 1996
61. Hughes CG, Biswas SS, Yin B, Baklanov DV, DeGrado TR, Coleman RE, Donovan CL, Lowe JE, Landolfo KP, Annex BH: Intramyocardial but not intravenous vascular endothelial growth factor improves regional perfusion in hibernating porcine myocardium. Circulation 100: 1-476, 1999
62. Banai S, Jaklitsch MT, Shou M, Lazarous DF, Scheinowitz M, Biro S, Epstein SE, Unger EF: Angiogenic-induced enhancement of collateral blood flow to ischemic myocardium by vascular endothelial growth factor in dogs. Circulation 89: 2183-2189, 1994
63. Tio RA, Tkebuchava T, Scheuermann TH, Lebherz C, Magner M, Kearney M, Esakof D, Isner JM, Symes JF: Intramyocardial gene therapy with naked DNA encoding vascular endothelial growth factor improves collateral flow to ischemic myocardium. Hum Gene Tber 10: 2953-2960, 1999
64. Vale PR, Milliken CE, Tkebuchava T, Chen D, Igawura H, Magner M, Kearney M, Isner JM: Catheter-based gene transfer of VEGF utilizing electromechanical LV mapping accomplishes therapeutic angiogenesis: Pre-clinical studies in swine. Circulation 100: I-512, 1999
65. Vale PR, Losordo DW, Milliken CE, Esakof DD, Isner JM: Percutaneous myocardial gene transfer of phVEGF-2. Circulation 100: 2462-2463, 1999
66. Mack CA, Patel SR, Schwarz EA, Zanzonico P, Hahn RT, Ilercil A, Devereux RB, Goldsmith SJ, Christian TF, Sanborn TA, Kovesdi I, Itackett N, Isom OW, Crystal RG, Rosengart TK: Biologic bypass with the use of adenovirus-mediated gene transfer of the conplementary deoxyribonucleic acid for vascular endothelial growth factor 121 improves myocardial perfusion and function in the ischemic porcine heart. J Tborac Cardiovasc Surg 115: 168-176, 1998
67. Lee LY, Patel SR, Hackett NR, Mack CA, Polce DR, El-Sawy T, Hachamovitch R, Zanzonico P, Crystal RG, Rosengard TK: Focal angiogen therapy using intramyocardial delivery of an adenovirus vector coding for vascular endotehlial growth factor 121. Ann Thorac Surg 69: 14-24, 2000
68. Lazarous DF, Shou M, Stiber JA, Hodge E, Thirumurti V, Goncalves L, Unger EF: Adenoviral-mediated gene transfer induces sustained pericardial VEGF expression in dogs: Effect on myocardial angiogenesis. Cardiovasc Res 44: 294-302, 1999
69. Vale PR, Losordo DW, Milliken CE, McDonald MC, Gravelin LM, Curry CM, Esakof DD, Maysky M, Symes JF, Isner JM: 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
70. 121 offers equivalent gene delivery and protein expression compared to a surgical-based transepicardial injection approach. J Am Coll Cardiol 35: 73A, 2000
71. Kornowski R, Leon MB, Fuchs S, Vodovotz Y, Flynn MA, Gordon DA, Pierre A, Kovesdi I, Keiser JA, Epstein SE: Electromagnetic guidance for catheter-based transendocardial injection: A platform for intramyocardial angiogenesis therapy. J Am Coll Cardiol 35: 1031-1039, 2000
72. Deutsch E, Tarazona N, Sanborn TA, Martin JL, Lee LY, Hackett N, El-Sawy T, Blanco I, Fromkin KR, Rosengart TK, Crystal RG: Percutaneous endocardial gene therapy: Patterns of in-vivo gene expression related to regional myocardial delivery. J Am Coll Cardiol 35: 6A, 2000
73. Schainfeld RM, Isner JM: Critical limb ischemia: Nothing to give at the office? Ann Int Med 130: 442-444, 1999
74. Isner JM: Arterial gene transfer for naked DNA for therapeutic angiogenesis: Early clinical results. Adv Drug Delivery 30: 185-197, 1998
75. Isner JM, Baumgartner I, Rauh G, Schainfeld R, Blair R, Manor O, Razvi S, Symes JF: Treatment of thromboangiitis obliterans (Buerger's disease) by intramuscular gene transfer of vascular endothelial growth factor: preliminary clinical results. J Vasc Surg 28: 964-73; discussion 73-5, 1998
76. Baumgartner I, Pieczek A, Manor O, Blair R, Kearney M, Walsh K, Isner JM: Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 97: 1114-1123, 1998
77. Hendel RC, Henry TD, Rocha-Singh K, Isner JM, Kereiakes DJ, Giordano FJ, Simons M, Bonow RO: Effect of intracoronary recombinant human vascular endothelial growth factor on myocardial perfusion: Evidence for a dose-dependent effect. Circulation 101: 118-121, 2000
78. Henry TD, Abraham JA: Review of prelcinical and clinical results with vascular endothelial growth factors for therapeutic angiogenesis. Curr Intervent Cardiol Rep 2: 228-241, 2000
79. Henry TD, Rocha-Sing K, Isner JM, Kereiakes DJ, Giordano FJ, Simons M, Losordo DW, Hendel RC, Bonow RO, Eppler SM, Zioncheck TF, Holmgren EB, McCluskey ER: Intracoronary administration of recombinant human vascular endothelial growth factor (rhVEGF) to patients with coronary artery disease. Am Heart J 142(5): 872-880, 2001
80. Henry TD, Annex BH, McKendall GR, Azrin MA, Lopex JJ, Giordano FJ: The VIVA trial: Vascular endothelial growth factor in ischemia or vascular angiogenesis. Circulation 107: 1359-1365, 2003
81. Losordo DW, Vale PR, Symes JF, Dunnington CH, Esakof DD, Maysky M, Ashare AB, Lathi K, Isner JM: 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
82. Vale PR, Losordo DW, Milliken CE, Maysky M, Esakof DD, Symes JF, Isner JM: Left ventricular electromechanical mapping to assess efficacy of phVEGF(165) gene transfer for therapeutic angiogenesis in chronic myocardial ischemia. Circulation 102: 965-974, 2000
83. Symes JF, Losordo DW, Vale PR, Lathi K, Esakof DD, Maysky M, Isner JM: Gene therapy with vascular endothelial growth factor for inoperable coronary artery disease: Preliminary clinical results. Ann Thorac Surg 68: 830-837, 1999
84. Shen Y-T, Vatner SF: Mechanism of impaired myocardial function during progressive coronary stenosis in conscious pigs: Hibernation versus stunning? Circ Res 76: 479-488, 1995
85. Wijns W, Vatner SF, Camici PG: Hibernating myocardium. New Engl J Med 3: 173-181, 1998
86. Vale PR, Milliken CE, Fortuin FD, Schatz RA, Esakof DD, Mysky M, Symes JF, Losordo DW: Effective gene transfer of phVEGF-2 for therapeutic angiogenesis in chronic myocardial ischemia as assessed by NOGA™ left ventricular electromechanical mapping (abstract). Circulation 102: II-689, 2000
87. Hendel RC, Vale PR, Losordo DW, Schatz RA, Fortuin FD, Schaer GL, Henry TD, Lopez JJ: The effects of VEGF-2 gene therapy on rest and stress myocardial perfusion: Results of serial SPECT imaging. Circulation 102: II-769, 2000
88. Losordo DW, Vale PR, Hendel RC, Milliken CE, Fortuin FD, Cummings N, Schatz RA, Asahara T, Isner JM, Kuntz RE: Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia. Circulation 105: 2012-2018, 2002
89. Schofield PM, Sharples LD, Caine N, Burns S, Tait S, Wistow T, Buxton M, Wallwork J: Transmyocardial laser revascularisation in patients with refractory angina: A randomised controlled trial. Lancet 353: 519-524, 1999
90. Allen KB, Dowling RD, Fudge TL, Shoettle GP, Selinger SL, Gangahar DM, Angell WW, Petracek MR, Shaar CJ, O'Neill WW: Comparison of transmyocardial revascularization with medical therapy in patients with refractory angina. New Engl J Med 341: 1029-1036, 1999
91. Frazier OH, March RJ, Horvath KA, Group FtTCDLRS: Transmyocardial revascularization with a carbon dioxide laser in patients with endstage coronary artery disease. New Engl J Med 341: 1021-1028, 1999
92. Burkhoff D, Schmidt S, Schulman SP, Myers J, Resar J, Becker LC, Weiss J, Jones JW: Investigators FtA. Transmyocardial laser revascularisation compared with continued medical therapy for treatment of refractory angina pectoris: A prospective randomised trial. Lancet 354: 885-890, 1999
93. Rosengart TK, Lee LY, Patel SR, Sanborn TA, Parikh M, Bergman GW, Hachamovitch R, Szulc M, Kligfield PD, Okin PM, Hahn RT, Devereaux RB, Post MR, Hackett NR, Foster T, Grasso TM, Lesser ML, Isom W, Crystal RG: Angiogenesis gene therapy, Phase I: Assessment of direct intramyocardial administration of an adenovirus vector expression VEGF121 cDNA to individuals with clinically significant severe coronary artery disease. Circulation 100: 468-474, 1999
94. Rosengart TK, Lee LY, Port JL, Hahn RT, Devereux RB, Finnin E, Isom WO, Crystal RG: Video assisted epicardial delivery of angiogenic gene therapy to the human myocardium utilizing an adenovirus vector encoding for VEGF121. Circulation 100: I-770, 1999
95. Hariawala M, Horowitz JR, Esakof D, Sheriff DD, Walter DH, Chaudhry GM, Desai V, Keyt B, Isner JM, Symes JF: VEGF improves myocardial blood flow but produces EDRF-mediated hypotension in porcine hearts J Surg Res 63: 77-82, 1996
96. Horowitz JR, Rivard A, van der Zee R, Hariawala MD, Sheriff DD, Esakof DD, Chaudhry M, Symes JF, Isner JM: Vascular endothelial growth factor/vascular permeability factor produces nitric oxide-dependent hypotension. Arterioscler Thromb Vasc Biol 17: 2793-2800, 1997
97. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM: Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578, 1998
98. van der Zee R, Murohara T, Luo Z, Zollmann F, Passeri J, Lekutat C, Isner JM: Vascular endothelial growth factor (VEGF)/vascular permeability factor (VPF) augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation 95: 1030-1037, 1997
99. Springer ML, Chen AS, Kraft PE, Bednarski M, Blau HM: VEGF gene delivery to muscle: Potential role of vasculogenesis in adults. Mol Cell 2: 549-558, 1998
100. Lee RJ, Springer ML, Blanco-Bose WE, Shaw R, Ursell PC, Blau HM: VEGF gene delivery to myocardium: Deleterious effects of unregulated expression. Circulation 102: 898-901, 2000
101. Schwartz ER, Speakman MT, Patterson M, Hale SS, Isner JM, Kedes LH, Kloner RA: Evaluation of the effects of intramyocardial injection of DNA expressing vascular endothelial growth factor (VEGF) in a myocardial infarction model in the rat - angiogenesis and angioma formation. J Am Coll Cardiol 35: 1323-1330, 2000
102. Kloner RA, Dow J, Chung G, Kedes LH: Intramyocardial injection of DNA encoding vascular endothelial growth factor in a myocardial infarction model. J Thromb Thrombolysis 10: 285-289, 2000
103. Vale PR, Rauh G, Wuensch DI, Pieczek A, Schainfeld RM: Influence of vascular endothelial growth factor on diabetic retinopathy. Circulation 17: 1-353, 1998
104. Isner JM, Vale PR, Symes JF, Losordo DW: Assessment of risks associated with cardiovascular gene therapy in human subjects. Circ Res 89(5): 389-400, 2001
105. Van Belle E, Tio FO, Couffinhal T, Maillard L, Passeri J, Isner JM: Stent endothelialization: Time course, impact of local catheter delivery, feasibility of recombinant protein administration, and response to cytokine expedition. Circulation 95: 438-448, 1997
106. 165 inhibits thrombus formation and intimal thickening. J Am Coll Cardiol 29: 1371-1379, 1997
107. Asahara T, Bauters C, Pastore CJ, Kearney M, Rossow S, Bunting S, Ferrara N, Symes JF, Isner JM: Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation 91: 2793-2801, 1995
108. Asahara T, Chen D, Tsurumi Y, Kearney M, Rossow S, Passeri J, Symes J, Isner J: Accelerated restitution of endothelial integrity and endothelium-dependent function following phVEGF165 gene transfer. Circulation 94: 3291-3302, 1996
109. Hiltunen MO, Laitinen M, Turunen MP, Jeltsch M, Hartikainen J, Rissanen TT, Laukkanen J, Niemi M, Kossila M, Hakkinen TP, Kivela A, Enholm B, Mansukoski H, Turunen A-M, Alitalo K, Yia-Herttuala S: Intravascular adenovirus-mediated VEGF-C gene transfer reduces neointima formation in balloon-denuded rabbit aorta. Circulation 102: 2262-2268, 2000
110. Vale PR, Wuensch DI, Rauh GF, Rosenfield K, Schainfeld RM, Isner JM: Arterial gene therapy for inhibiting restenosis in patients with claudication undergoing superficial femoral artery angioplasty. Circulation 98: I-66, 1998
111. Laitinen M, Hartikainen J, Hiltunen MO, Eranen JK, M., Narvanen O, Makinen K, Manninen H, Syvanne M, Martin JF, Laakso M, Yla-Herttuala S: Catheter-mediated vascular endothelial growth factor gene transfer to human coronary arteries after angioplasty. Hum Gene Ther 11: 263-270, 2000
112. Lemarchand P, Jones M, Yamada I, Crystal RG: In vivo gene transfer and expression in normal uninjured blood vessels using replication-deficient recombinant adenovirus vectors. Circ Res 72: 1132-1138, 1993
113. Asahara T, Bauters C, Zheng LP, Takeshita S, Bunting S, Ferrara N, Symes JF, Isner JM: Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation 92: II-365-II-371, 1995
114. Asahara T, Chen D, Takahashi T, Fujikawa K, Kearney M, Magner M, Yancopoulos GD, Isner JM: Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circ Res 83: 233-240, 1998
115. Van Belle E, Rivard A, Chen D, Silver M, Bunting S, Ferrara N, Symes JF, Bauters C, Isner JM: Hypercholesterolemia attenuates angiogenesis but does not preclude augmentation by angiogenic cytokines. Circulation 96: 2667-2674, 1997
116. Luscher TF, Noll G: Endothelium dysfunction in the coronary ciruclation. J Cardiovasc Pharmacol 24: 16S-26S, 1994
117. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T: Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103: 634-637, 2001
118. Kawamoto A, Tkebuchava T, Yamaguchi J, Nishimura H, Yoon YS, Milliken C, Uchida S, Masuo O, Iwaguro H, Ma H, Hanley A, Silver M, Kearney M, Losordo DW, Isner JM, Asahara T: Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107: 461-468, 2003
119. Schultz A, Lavie L, Hochberg I, Beyar R, Stone T, Skorechi K, Lavie P, Roguin A, Levy AP: Interindividual heterogeneity in the hypoxic regulation of VEGF: Significance for the development of the coronary artery collateral circulation. Circulation 100: 547-552, 1999