Re-evaluating therapeutic neovascularization

Journal of Molecular and Cellular Cardiology

Volumn 36, Issue 1, 2004, Pages 25-32

  De Muinck, E D ^a   Simons, M ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Arteriogenesis; Clinical trials; Hypoxia; Inflammation; Review

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; ERYTHROPOIETIN; HYPOXIA INDUCIBLE FACTOR 1; VASCULOTROPIN;

ANGIOGENESIS; CLINICAL TRIAL; COLLATERAL CIRCULATION; DRUG CHOICE; DRUG EFFICACY; DRUG SCREENING; GENE INDUCTION; HEART MUSCLE ISCHEMIA; HEMODYNAMICS; HUMAN; HYPOXIA; INFLAMMATION; MACROPHAGE; METABOLISM; PATIENT SELECTION; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; STIMULUS; STIMULUS RESPONSE; T LYMPHOCYTE;

ANIMALIA;

EID: 0347635349     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2003.10.002     Document Type: Review

References (88)

1. Risau W., Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol. 11:1995;73-91.
2. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 6:2000;389-395.
3. Hatzopoulos A.K., Rosenberg R.D. Embryonic development of the vascular system. Ware J.A., Simons M. Angiogenesis and cardiovascular disease. 1999;3-29 Oxford University Press, New York, Oxford.
4. Sabin F.R. Origin and development of the primitive vessels of the chick and of the pig. Contrib Embryol Carnegie Inst Publ Wash. 6:1917;61-124.
5. Moore M.A. Putting the neo into neoangiogenesis. J Clin Invest. 109:2002;313-315.
6. Helisch A., Schaper W. Arteriogenesis: the development and growth of collateral arteries. Microcirculation. 10:2003;83-97.
7. Folkman J. Tumor angiogenesis: therapeutic implications. New Engl J Med. 285:1971;1182-1186.
8. Heart disease and stroke statistics - 2003 update. 2002;American Heart Association, Dallas, Texas.
9. Baumgartner I., Pieczek A., Manor O., Blair R., Kearney M., Walsh K., et al. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation. 97:1998;1114-1123.
10. Ruel M., Laham R.J., Parker J.A., Post M.J., Ware J.A., Simons M., et al. Long-term effects of surgical angiogenic therapy with fibroblast growth factor 2 protein. J Thorac Cardiovasc Surg. 124:2002;28-34.
11. Losordo D.W., Vale P.R., Hendel R.C., Milliken C.E., Fortuin F.D., Cummings N., et al. 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. 105:2002;2012-2018.
12. Grines C.L., Watkins M.W., Helmer G., Penny W., Brinker J., Marmur J.D., et al. Angiogenic gene therapy (AGENT) trial in patients with stable angina pectoris. Circulation. 105:2002;1291-1297.
13. Henry T.D., Annex B.H., McKendall G.R., Azrin M.A., Lopez J.J., Giordano F.J., et al. The VIVA trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation. 107:2003;1359-1365.
14. Simons M., Annex B.H., Laham R.J., Kleiman N., Henry T., Dauerman H., et al. Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial. Circulation. 105:2002;788-793.
15. Scholz D., Cai W.J., Schaper W. Arteriogenesis, a new concept of vascular adaptation in occlusive disease. Angiogenesis. 4:2001;247-257.
16. Semenza G. Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol. 64:2002;993-998.
17. Zhu H., Bunn H.F. Signal transduction. How do cells sense oxygen? Science. 292:2001;449-451.
18. Cockman M.E., Masson N., Mole D.R., Jaakkola P., Chang G.W., Clifford S.C., et al. Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem. 275:2000;25733-25741.
19. Pugh C.W., Ratcliffe P.J. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med. 9:2003;677-684.
20. Brusselmans K., Compernolle V., Tjwa M., Wiesener M.S., Maxwell P.H., Collen D., et al. Heterozygous deficiency of hypoxia-inducible factor-2alpha protects mice against pulmonary hypertension and right ventricular dysfunction during prolonged hypoxia. J Clin Invest. 111:2003;1519-1527.
21. Makino Y., Cao R., Svensson K., Bertilsson G., Asman M., Tanaka H., et al. Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature. 414:2001;550-554.
22. Sullivan G.W., Sarembock I.J., Linden J. The role of inflammation in vascular diseases. J Leukoc Biol. 67:2000;591-602.
23. Couffinhal T., Silver M., Kearney M., Sullivan A., Witzenbichler B., Magner M., et al. Impaired collateral vessel development associated with reduced expression of vascular endothelial growth factor in ApoE-/- mice. Circulation. 99:1999;3188-3198.
24. Arras M., Ito W.D., Scholz D., Winkler B., Schaper J., Schaper W. Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest. 101:1998;40-50.
25. Sunderkotter C., Steinbrink K., Goebeler M., Bhardwaj R., Sorg C. Macrophages and angiogenesis. J Leukoc Biol. 55:1994;410-422.
26. More J.W.I., Sholley M.M. Comparison of the neovascular effects of stimulated macrophages and neutrophils in autologous rabbit corneas. Am J Pathol. 120:1985;87-98.
27. Rivard A., Fabre J.E., Silver M., Chen D., Murohara T., Kearney M., et al. Age-dependent impairment of angiogenesis. Circulation. 99:1999;111-120.
28. Sasaki K-I, Murohara T., Ikeda H., Sugaya T., Seiyaku T., Shintani S., et al. Direct evidence for the important role of the angiotensin II type IA receptor in postnatal angiogenesis. Circulation. 102:(Suppl II):2000;196-197.
29. Morrissey J.J. Angiotensin II: an immune costimulator? Am J Kidney Dis. 36:2000;434-440.
30. Carmeliet P., Moons L., Luttun A., Vincenti V., Compernolle V., de Mol M., et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med. 7:2001;575-583.
31. Pipp F., Heil M., Issbrücker K., Ziegelhoeffer T., Martin S., van den Heuvel J., et al. VEGFR-1-selective VEGF homologue PlGF is arteriogenic: evidence for a monocyte-mediated mechanism. Circ Res. 92:2003;378-385.
32. Heil M., Clauss M., Suzuki K., Buschmann I.R., Willuweit A., Fischer S., et al. Vascular endothelial growth factor (VEGF) stimulates monocyte migration through endothelial monolayers via increased integrin expression. Eur J Cell Biol. 79:2000;850-857.
33. Galis Z.S., Sukhova G.K., Kranzhofer R., Clark S., Libby P. Macrophage foam cells from experimental atheroma constitutively produce matrix-degrading proteinases. Proc Natl Acad Sci USA. 92:1995;402-406.
34. Polverini P.J., Cotran P.S., Gimbrone M.A. Jr, Unanue E.R. Activated macrophages induce vascular proliferation. Nature. 269:1977;804-806.
35. Schmeisser A., Graffy C., Daniel W.G., Strasser R.H. Phenotypic overlap between monocytes and vascular endothelial cells. Adv Exp Med Biol. 522:2003;59-74.
36. Heil M., Ziegelhoeffer T., Pipp F., Kostin S., Martin S., Clauss M., et al. Blood monocyte concentration is critical for enhancement of collateral artery growth. Am J Physiol Heart Circ Physiol. 283:2002;H2411-H2419.
37. Cramer T., Yamanishi Y., Clausen B.E., Forster I., Pawlinski R., Mackman N., et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 112:2003;645-657.
38. Eliceiri B.P. Integrin and growth factor receptor crosstalk. Circ Res. 89:2001;1104-1110.
39. Mostafavi-Pour Z., Askari J.A., Parkinson S.J., Parker P.J., Ng T.T.C., Humphries M.J. Integrin-specific signaling pathways controlling focal adhesion formation and cell migration. J Cell Biol. 161:2003;155-167.
40. Izzard C.S., Radinsky R., Culp L.A. Substratum contacts and cytoskeletal reorganization of BALB/c 3T3 cells on a cell-binding fragment and heparin-binding fragments of plasma fibronectin. Exp Cell Res. 165:1986;320-336.
41. Thodeti C.K., Albrechtsen R., Grauslund M., Asmar M., Larsson C., Takada Y., et al. ADAM12/syndecan-4 signaling promotes beta 1 integrin-dependent cell spreading through protein kinase Calpha and RhoA. J Biol Chem. 278:2003;9576-9584.
42. Li L., Couse T.L., Deleon H., Xu C.P., Wilcox J.N., Chaikof E.L. Regulation of syndecan-4 expression with mechanical stress during the development of angioplasty-induced intimal thickening. J Vasc Surg. 36:2002;361-370.
43. Kojima T., Takagi A., Maeda M., Segawa T., Shimizu A., Yamamoto K., et al. Plasma levels of syndecan-4 (ryudocan) are elevated in patients with acute myocardial infarction. Thromb Haemost. 85:2001;793-799.
44. Deindl E., Hoefer I.E., Fernandez B., Barancik M., Heil M., Strniskova M., et al. Involvement of the fibroblast growth factor system in adaptive and chemokine-induced arteriogenesis. Circ Res. 92:2003;561-568.
45. Murakami M., Horowitz A., Tang S., Ware J.A., Simons M. Protein kinase C (PKC) delta regulates PKCalpha activity in a Syndecan-4-dependent manner. J Biol Chem. 277:2002;20367-20371.
46. Horowitz A., Tkachenko E., Simons M. Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J Cell Biol. 157:2002;715-725.
47. Li J., Partovian C., Hampton T.G., Metais C., Tkachenko E., Sellke F.W., et al. Modulation of microvascular signaling by heparan sulfate matrix: studies in syndecan-4 transgenic mice. Microvasc Res. 64:2002;38-46.
48. Volk R., Schwartz J.J., Li J., Rosenberg R.D., Simons M. The role of syndecan cytoplasmic domain in basic fibroblast growth factor-dependent signal transduction. J Biol Chem. 274:1999;24417-24424.
49. Zhang Y., Li J., Partovian C., Sellke F.W., Simons M. Syndecan-4 modulates basic fibroblast growth factor 2 signaling in vivo. Am J Physiol Heart Circ Physiol. 284:2003;H2078-H2082.
50. Cao G., O'Brien C.D., Zhou Z., Sanders S.M., Greenbaum J.N., Makrigiannakis A., et al. Involvement of human PECAM-1 in angiogenesis and in vitro endothelial cell migration. Am J Physiol Cell Physiol. 282:2002;C1181-C1190.
51. Solowiej A., Biswas P., Graesser D., Madri J.A. Lack of platelet endothelial cell adhesion molecule-1 attenuates foreign body inflammation because of decreased angiogenesis. Am J Pathol. 162:2003;953-962.
52. Piali L., Hammel P., Uherek C., Bachmann F., Gisler R.H., Dunon D., et al. CD31/PECAM-1 is a ligand for alpha v beta 3 integrin involved in adhesion of leukocytes to endothelium. J Cell Biol. 130:1995;451-460.
53. Jackson D.E. The unfolding tale of PECAM-1. FEBS Lett. 540:2003;7-14.
54. Dor Y., Djonov V., Abramovitch R., Itin A., Fishman G.I., Carmeliet P., et al. Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J. 21:2002;1939-1947.
55. Laham R.J., Sellke F.W., Edelman E.R., Pearlman J.D., Ware J.A., Brown D.L., et al. Local perivascular delivery of basic fibroblast growth factor in patients undergoing coronary bypass surgery: results of a phase I randomized, double-blind, placebo-controlled trial. Circulation. 100:1999;1865-1871.
56. Khurana R., Simons M. Insights from angiogenesis trials using fibroblast growth factor for advanced arteriosclerotic disease. Trend Cardiovasc Med. 13:2003;116-122.
57. Simons M., Post M.J. Angiogenesis. Topol E.J. Textbook of interventional cardiology. 2003;757-779 Saunders, Philadelphia.
58. Maseri A., Aranjo L., Finocchiaro M.L. Collateral circulation: heart, brain, kidney, limbs. Schaper W., Shaper J. Collateral development and function in man. 1993;381-402 Kluwer Academic Publishers, Boston, MA.
59. Scholz D., Ziegelhoeffer T., Helisch A., Wagner S., Friedrich C., Podzuweit T., et al. Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice. J Mol Cell Cardiol. 34:2002;775-787.
60. Schultz A., Lavie L., Hochberg I., Beyar R., Stone T., Skorecki K., et al. Interindividual heterogeneity in the hypoxic regulation of VEGF: significance for the development of the coronary artery collateral circulation. Circulation. 100:1999;547-552.
61. Frenkel-Denkberg G., Gershon D., Levy A.P. The function of hypoxia-inducible factor 1 (HIF-1) is impaired in senescent mice. FEBS Lett. 462:1999;341-344.
62. Rohan R.M., Fernandez A., Udagawa T., Yuan J., D'Amato R.J. Genetic heterogeneity of angiogenesis in mice. FASEB J. 14:2000;871-876.
63. Simons M., Bonow R.O., Chronos N.A., Cohen D.J., Giordano F.J., Hammond H.K., et al. Clinical trials in coronary angiogenesis: issues, problems, consensus: an expert panel summary. Circulation. 102:2000;E73-E86.
64. Alon T., Hemo I., Itin A., Pe'er J., Stone J., Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med. 1:1995;1024-1028.
65. Darland D.C., D'Amore P.A. Blood vessel maturation: vascular development comes of age. J Clin Invest. 103:1999;157-158.
66. Thurston G., Suri C., Smith K., McClain J., Sato T.N., Yancopoulos G.D., et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 286:1999;2511-2514.
67. Lee S.H., Wolf P.L., Escudero R., Deutsch R., Jamieson S.W., Thistletwaite P. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. New Engl J Med. 342:2000;626-633.
68. Vincent K.A., Shyu K.G., Luo Y., Magner M., Tio R.A., Jiang C., et al. Angiogenesis is induced in a rabbit model of hindlimb ischemia by naked DNA encoding an HIF-1alpha/VP16 hybrid transcription factor. Circulation. 102:2000;2255-2261.
69. Li J., Post M., Volk R., Gao Y., Li M., Metais C., et al. PR 39, a peptide regulator of angiogenesis. Nat Med. 6:2000;49-55.
70. Post M.J., Bao J., Sato K., Murakami M., Pearlman J.D., Simons M. Adenoviral PR-39 improves perfusion and function in a pig model of chronic myocardial ischemia. Circulation. 106:2002;II-275.
71. Tomita N., Morishita R., Taniyama Y., Koike H., Aoki M., Shimizu H., et al. Angiogenic property of hepatocyte growth factor is dependent on upregulation of essential transcription factor for angiogenesis, ets-1. Circulation. 107:2003;1411-1417.
72. Kola I., Brookes S., Green A.R., Garber R., Tymms M., Papas T.S., et al. The Ets1 transcription factor is widely expressed during murine embryo development and is associated with mesodermal cells involved in morphogenetic processes such as organ formation. Proc Natl Acad Sci USA. 90:1993;7588-7592.
73. Wojta J., Kaun C., Breuss J.M., Koshelnick Y., Beckmann R., Hattey E., et al. Hepatocyte growth factor increases expression of vascular endothelial growth factor and plasminogen activator inhibitor-1 in human keratinocytes and the vascular endothelial growth factor receptor flk-1 in human endothelial cells. Lab Invest. 79:1999;427-438.
74. Aoki M., Morishita R., Taniyama Y., Kida I., Moriguchi A., Matsumoto K., et al. Angiogenesis induced by hepatocyte growth factor in non-infarcted myocardium and infarcted myocardium: up-regulation of essential transcription factor for angiogenesis, ets. Gene Ther. 7:2000;417-427.
75. Taniyama Y., Morishita R., Hiraoka K., Aoki M., Nakagami H., Yamasaki K., et al. Therapeutic angiogenesis induced by human hepatocyte growth factor gene in rat diabetic hind limb ischemia model: molecular mechanisms of delayed angiogenesis in diabetes. Circulation. 104:2001;2344-2350.
76. Luttun A., Tjwa M., Moons L., Wu Y., Angelillo-Scherrer A., Liao F., et al. Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med. 8:2002;831-840.
77. Luttun A., Tjwa M., Carmeliet P. Placental growth factor (PlGF) and its receptor Flt-1 (VEGFR-1): novel therapeutic targets for angiogenic disorders. Ann NY Acad Sci. 979:2002;80-93.
78. Hattori K., Heissig B., Wu Y., Dias S., Tejada R., Ferris B., et al. Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone-marrow microenvironment. Nat Med. 8:2002;841-849.
79. Autiero M., Waltenberger J., Communi D., Kranz A., Moons L., Lambrechts D., et al. Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med. 9:2003;936-943.
80. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 380:1996;435-439.
81. Springer M.L., Chen A.S., Kraft P.E., Bednarski M., Blau H.M. VEGF gene delivery to muscle: potential role for vasculogenesis in adults. Mol Cell. 2:1998;549-558.
82. Helmlinger G., Endo M., Ferrara N., Hlatky L., Jain R.K. Formation of endothelial cell networks. Nature. 405:2000;139-141.
83. Hood J.D., Bednarski M., Frausto R., Guccione S., Reisfeld R.A., Xiang R., et al. Tumor regression by targeted gene delivery to the neovasculature. Science. 296:2002;2404-2407.
84. Prchal J.T. Delivery on demand - a new era of gene therapy? New Engl J Med. 348:2003;1282-1283.
85. Binley K., Askham Z., Iqball S., Spearman H., Martin L., de Alwiss M., et al. Long-term reversal of chronic anemia using a hypoxia-regulated erythropoietin gene therapy. Blood. 100:2002;2406-2413.
86. Li K.C., Bednarski M.D. Vascular-targeted molecular imaging using functionalized polymerized vesicles. J Magn Reson Imag. 16:2002;388-393.
87. Meoli D.F., Sadeghi M.M., Bourke B.N., Hu J., Brown L.M., Krassilnikova S., et al. Targeted imaging of myocardial angiogenesis in chronic model of infarction. Circulation. 106:2002;II-331.
88. Simons M. Therapeutic coronary angiogenesis: a fronte praecipitium a tergo lupi? Am J Physiol Heart Circ Physiol. 280:2001;H1923-H1927.