Techniques in Vascular & Interventional Radiology
Volume 7, Issue 1 , Pages 40-48 , March 2004

Therapeutic angiogenesis: the next frontier for interventional radiology

  • Robert P Liddell, MD

      Affiliations

    • Russell H. Morgan Department of Radiology and Radiological Science, Division of Vascular and Interventional Radiology, The Johns Hopkins Medical Institutions, Baltimore, MD, USA
    • ,
  • Clifford R Weiss, MD

      Affiliations

    • Russell H. Morgan Department of Radiology and Radiological Science, Division of Vascular and Interventional Radiology, The Johns Hopkins Medical Institutions, Baltimore, MD, USA
    • ,
  • Lawrence V Hofmann, MD

      Affiliations

    • Russell H. Morgan Department of Radiology and Radiological Science, Division of Vascular and Interventional Radiology, The Johns Hopkins Medical Institutions, Baltimore, MD, USA
    • Corresponding Author InformationAddress reprint requests to Lawrence V. Hofmann, MD, Department of Radiology, Division of Vascular and Interventional Radiology, The Johns Hopkins Medical Institutions, Blalock 545, 600 N. Wolfe Street, Baltimore, MD 21287 USA

References 

  1. Criqui MH, Fronek A, Barrett O, et al.  The prevelance of peripheral vascular arterial disease in a defined population. Circulation. 1985;71:510–515
  2. Tunis SR, Bass EB, Steinberg EP. The use of angioplasty, bypass surgery, and amputation in the management of peripheral vascular disease. N Engl J Med. 1991;325:556–562
  3. Hertig A. Angiogenesis in the early human chorion and in the primary placenta of the Macaque monkey. Contrib Embryo. 1935;25:37–62
  4. Folkman J. Tumor angiogenesis (Therapeutic implications). N Engl J Med. 1971;285:1182–1186
  5. Bussolino F, Mantovani FA, Persisco G. Molecular mechanisms of blood vessel formation. Trens Biochem Sci. 1997;22:251–256
  6. Risau W. Mechanisms of angiogenesis. Nature. 1997;386:671–674
  7. Asahara T, Murohara T, Sullivan A, et al.  Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:965–967
  8. Asahara T, Masuda H, Takahashi T, et al.  Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221–228
  9. Takashita T, Kalka C, Masuda H, et al.  Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nature Med. 1999;5:434–438
  10. Kalka C, Masuda H, Tahashi T, et al.  Bone marrow origin of endothelial progenitor cells responsible for therapeutic neovascularization. Proc Natl Acad Sci USA. 2000;97:3422–3427
  11. Filkman J, Shing Y. Angiogenesis. J Biol Chem. 1992;116:435–439
  12. Risau W. Mechanisms of angiogenesis. Nature. 1997;386:671–674
  13. Swift ME, Kleinman HK, DiPietro LA. Impaired wound repair and delayed angiogenesis in aged mice. Lab Invest. 1999;79:1479–1487
  14. Folkman J. What is the evidence that tumors are angiogenesis-dependent?. J Natl Cancer Inst. 1991;82:4–6
  15. Giatromanolaki A, Sivridis E, Athanassou N, et al.  The angiogenic pathway “vascular endothelial growth factor/flk 1(KDR)-receptor” in rheumatoid arthritis and osteorthritis. J Pathol. 2001;194:101–108
  16. Veves A, King GL. Can VEGF reverse diabetic retinopathy in human subjects?. J Clin Invest. 2001;107:1215–1218
  17. Semenza GL. Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med. 2003;54:17–28
  18. Iba O, Matsubara H, Nozawa Y, et al.  Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation. 2002;106:2019–2025
  19. Etoh T, Inoue H, Tanaka S, et al.  Angiopoietin-2 is related to tumor angiogenesis in gastric carcinoma (Possible in vivo regulation via induction of proteases). Cancer Res. 2001;61:2145–2153
  20. Hirschi KK, Rohovsky SA, D’Amore PA. PDGF, TGF-b, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol. 1998;141:805–814
  21. Takeshita S, Zheng LP, Asahara T, et al.  Therapeutic angiogenesis (A single intra-arterial bolus of vascular endothelial growth factor augments collateral vessel formation in a rabbit hindlimb ischemia). Circulation. 1993;88:1–370 (abstr)
  22. Baumgartner I, Pieczek A, Manor O, et al.  Constitutive expression of phVEGF165 following intramuscular gene transfer promotes collateral vessel development in patients with CLI. Circulation. 1998;97:1114–1123
  23. Schumacher B, Pecher P, vonSpecht BU, et al.  Induction of neoangiogenesis in ischemic myocardium by human growth factors (First clinical results of a new treatment of coronary heart disease). Circulation. 1998;97:645–650
  24. Losorda DW, Vale PR, Symes J, et al.  Gene therapy for myocardial angiogenesis (Initial clinical results with direct myocardial injection of phVEGF165 as sole therapy for myocardial ischemia). Circulation. 1998;98:2800–2804
  25. Buschman I, Schaper W. The pathophysiology of the collateral circulation. J Pathol. 2000;190:338–342
  26. Schaper W. Control of coronary arteriogenesis. Eur Heart J. 1995;16(Suppl):66–68
  27. Deindl E, Buschmann I, Hoefer IE, et al.  Role of ischemia and hypoxia-induced genes in arteriogenesis after femoral artery occlusion in the rabbit. Circ Res. 2001;89:779–786
  28. Gloe T, Sohn HY, Meininger GA, et al.  Shear stress-induced release of basic fibroblast growth factor from endothelial cells is mediated by matrix interaction via integrin alpha (v) beta 3. J Biol Chem. 2002;277:2345
  29. Ballermann BJ, Daardik A, Eng E, et al.  Shear stress and the endothelium. Kidney Int. 1998;69(Suppl):S100–S108
  30. Walpola PL, Gotlieb AI, Cybulsky MI, et al.  Expression of ICAM-1 and VCAM-1 and monocyte adherence in arteries exposed to altered shear stress. Arterioscler Thromb Vasc Biol. 1995;15:2–10
  31. Wolf C, Cai WJ, Vosschulte R, et al.  Vascular remodeling and altered protein expression during growth of coronary collateral arteries. J Mol Cell Cardiol. 1998;30:2291–2305
  32. 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. 1998;98:2800–2804
  33. Takeshita S, Zheng LP, Brogi E, et al.  A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest. 1994;93:662–670
  34. Rissen TT, Vajanto I, Yla-Herttuala S. Gene therapy for therapeutic angiogenesis in critically ischemic lower limb-on the way to the clinic. Eur J Clin Invest. 2001;31:651–666
  35. Morishita R. Recent progress in gene therapy from cardiovascular disease. Circ J. 2002;66:1077–1086
  36. Zabner J. Cationic lipids used in gene transfer. Adv Drug Deliv Rev. 1997;27:17–28
  37. Yang L, Nunes FA, Berensci K, et al.  Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci. 1994;91:4407–4411
  38. Kalka C, Masuda H, Takashi T, et al.  Transplantation of ex vivo expanded progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA. 2000;97:3422–3427
  39. Iwaguro H, Yamaguchi J, Kalka C, et al.  Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation. 2002;105:732–738
  40. Assmus B, Schachinger V, Teupe C, et al.  Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation. 2002;106:3009–3017
  41. Rehman J, Jingling L, Orschell CM, et al.  Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogeneic growth factors. Circulation. 2003;107:1164–1169
  42. Kamihata H, Matsubara H, Nishue T, et al.  Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation. 2001;104:1046–1052
  43. Shintani S, Murohara T, Ikeda H, et al.  Augmentation of postnatal neovascularization with autologuous bone marrow transplantation. Circulation. 2001;103: 897–895
  44. Salven P, Oprana A, Joensuu H. Leukocytes and platelets of patients with cancer contain high levels of vascular endothelial growth factor. Clin Cancer Res. 1999;5:487–491
  45. Gaudry M, Bregerie O, Andrieu V, et al: Intracellular pool of vascular endothelial growth factor in human neutrophils. Blood 90:4153–4161, 197
  46. Kronemann N, Bouloumie A, Bassus S, et al.  Aggregating human platelets stimulate expression of vascular endoth elial growth factor in cultured vascular smooth muscle cells through synergistic effect of transforming growth factor-β1 and platelet-derived growth factor AB. Circulation. 1999;100:855–860
  47. Iba O, Matsubara H, Nozawa Y, et al.  Angiogenesis by implantation of peripheral blood mononuclear cells and platelets into ischemic limbs. Circulation. 2002;106:2019–2025
  48. Mäkinen K, Laitinen M, Manninen H, et al.  Catheter mediated gene transfer to human lower limb arteries after PTA. Circulation. 1999;100:I–770 (abstr)
  49. Laham RJ, Garcia L, Baim DS, et al.  Therapeutic angiogenesis using basic fibroblast growth factor and vascular endothelial growth factor using various delivery strategies. Curr Interv Cardiol Rep. 1999;1:228–233
  50. Hiltunen MO, Turunen MP, Turunen AM, et al.  Biodistribution of adenoviral vector to nontarget tissues after local in vivo gene transfer to arterial wall using intravascular and periadventitial gene delivery methods. FASEB J. 2000;14:2230–2236
  51. Edelman ER, Nugent MA, Karnovsky MJ. Perivascular and intravenous administration of basic fibroblast factor (Vascular and solid organ deposition). Proc Natl Acad Sci. 1993;90:1513–1517
  52. Bauters C, Asahara T, Zheng LP, et al.  Physiological assessment of augmented vascularity induced by VEGF in ischemic rabbit hindlimb. Am J Physiol. 1994;267:H1263–1271
  53. Isner JM, Baumgartner I, Rauh G, et al.  Clinical evidence angiogenesis after arterial gene transfer of phVEGF165 in patient with ischemic disease. Hum Gene Ther. 1996;348:37–374
  54. Hiltunen MO, Turunen MP, Turunen AM, et al.  Biodistribution of adenoviral vector to nontarget tissues after local in vivo gene transfer to arterial wall using intravascular and periadventitial gene delivery methods. FASEB J. 2000;14:2230–2236
  55. Schratzberger P, Krainin JG, Schratzberger G, et al: Transcutaneous ultrasound augments naked DNA transfection of skeletal muscle. Mol Ther 6:576–583, 202
  56. Shen BQ, Lee DY, Gerber HP, et al.  Homologous up-regulation of KDR/Flk-1 receptor expression by vascular endothelial growth factor in vitro. J Biol Chem. 1998;273:29979–29985
  57. Hopkins SP, Bulgrin JP, Sims RL, et al.  Controlled delivery of vascular endothelial growth factor promotes neovascularization and maintains limb function in a rabbit model of ischemia. J Vasc Surg. 1998;27:886–894 discussion 895
  58. Kasahara H, Tanaka E, Fukuyama N, et al.  Biodegradable gelatin hydrogel potentiates the angiogenic effect of fibroblast growth factor 4 plasmid in rabbit hindlimb ischemia. J Am Coll Cardiol. 2003;41:1056–1062
  59. King TW, Patrick CW. Development and in vitro characterization of vascular endothelial growth factor (VEGF)-loaded poly(DL-lactic-co-glycolic acid)/poly(ethylene glycol) microspheres using a solid encapsulation/single emulsion/solvent technique. J Biomed Mater Res. 2000;51:383–390
  60. Cao RR, Brakenhielm E, Pawliuk R, et al.  Angiogenic synergism, vascular stability and improvement of hind-limb ischemia by combination of PDGF-BB and FGF-2. Nat Med. 2003;9:604–613
  61. Lederman RJ, Mendelsohn FO, Anderson RD, et al.  Therapeutic angiogenesis with recombinant fibroblast growth factor-2 for intermittent claudication (the TRAFFIC study) (A randomised trial). Lancet. 2002;359:2053–2058
  62. Rajagopalan S, Mohler E, Lederman RJ, et al.  Regional Angiogenesis with Vascular Endothelial Growth Factor (VEGF) in peripheral arterial disease (Design of the RAVE trial). Am Heart J. 2003;145:1114–1118
  63. Rajagopalan S, Mohler ER, Lederman RJ, et al.  Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease (A phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication). Circulation. 2003;108:1933–1938
  64. Tateishi-Yuyama E, Matsubara H, Murohara T, et al.  Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells (A pilot study and a randomised controlled trial). Lancet. 2002;360:427–435
  65. Detmer M, Brown LF, Berse B, et al.  Hypoxia upregulates the expression of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) and its receptors in human skin. J Invest Dermatol. 1997;108:263–268
  66. Masumura M, Murayama N, Inoue T, et al.  Selective induction of fibroblast growth factor receptor-1 mRNA after transient focal ischemia in the cerebral cortex of rats. Neuroscience. 1996;213:119–122
  67. Baumgartner I, Rauh G, Pieczek A, et al.  Lower-extremity edema associated with gene transfer of naked DNA vascular endothelial growth factor. Ann Int Med. 2000;32:880–884
  68. Isner JM, Vale PR, Symes JF, et al.  Assessment of risks associated with cardiovascular gene therapy in human subjects. Circ Res. 2001;89:389–400
  69. Hariawala M, Horowitz JR, Esakof D. VEGF improves myocardial blood flow but produces EDRF-mediated hypotension in porcine hearts. J Surg Res. 1996;63–82
  70. Horowitz JR, Rivard A, van der Zee R, et al.  Vascular endothelial growth factor/vascular permeability factor produces nitric oxide-dependent hypotension. Arterioscler Thromb Vasc Biol. 1997;17:2793–2800
  71. Lazarous DF, Unger EF, Epstein SE, et al.  Basic fibroblast growth factor in patients with intermittent claudication (Results of phase I trial). J Am Coll Cardiol. 2000;1239–1244
  72. Simons M, Annex BH, Laham RJ, et al.  Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2 (Double-blind, randomized, controlled clinical trial). Circulation. 2002;105:788–793
  73. Lee RJ, Springer ML, Blanco-Bose WE, et al.  VEGF gene delivery into myocardium (Deleterious effects of unregulated expression). Circulation. 2000;102:898–901
  74. Schwartz ER, Speakman MT, Paterson M, et al.  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. 2000;35:1323–1330
  75. Okamoto N, Tobe T, Hackett SF, et al.  Animal model: Transgenic mice with increased expression of vascular endothelial growth factor in the retina: A new model of intraretinal and subretinal neovascularization. Am J Pathol. 1997;151:281–291
  76. Adamis AP, Miller JW, Bernal M-T, et al.  Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Opthamol. 1994;118:445–450
  77. Vale PR, Rauh G, Wuensch DI, et al.  Influence of vascular endothelial growth factor on diabetic retinopathy. Circulation. 1998;17:1–353 (abstr)
  78. Celletti FL, Waugh JM, Amabile PG, et al.  Vascular endothelial growth factor enhances atherosclerosis plaque progression. Nature Med. 2001;7:425–429
  79. Moulton KS, Heller E, Konerding MA, et al.  Angiogenesis inhibitors endostatin and TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation. 1999;99:1726–1732

PII: S1089-2516(04)00003-4

doi: 10.1053/j.tvir.2004.01.002

Techniques in Vascular & Interventional Radiology
Volume 7, Issue 1 , Pages 40-48 , March 2004

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