Regulation of endothelial function and angiogenesis by vascular endothelial growth factor-A (VEGF-A);Regulation der endothelfunktion und der angiogenese durch den vaskularen endothelialen wachstumsfaktor-A (VEGF-A)

Zeitschrift fur Kardiologie

Volumn 89, Issue 3, 2000, Pages 206-218

  Kroll, J ^a   Waltenberger, J ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

Angiogenesis; Arteriogenesis; Endothelial function; Growth factor therapy; Signal transduction; Therapeutic angiogenesis therapeutic arteriogenesis; VEGF A

Indexed keywords

NITRIC OXIDE; RECOMBINANT VASCULOTROPIN; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CARDIOVASCULAR DISEASE; ENDOTHELIUM CELL; HUMAN; ISCHEMIC HEART DISEASE; SIGNAL TRANSDUCTION; TREATMENT INDICATION; VASCULAR ENDOTHELIUM;

EID: 0034042236     PISSN: 03005860     EISSN: None     Source Type: Journal    
DOI: 10.1007/s003920050472     Document Type: Article

References (101)

1. 1. Waltenberger J (1997) Modulation of ~ h factor action: Implications for the treatment of cardiovascular diseases. Circulation 96:4083-4094
2. 2. Furchgott RF, Zawadski JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373-376
3. 3. Fulton D, Gratton JP, McCabe TJ, Fonlana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399:597-601
4. 4. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605
5. 5. Busse R, Flemming I (1996) Endothelial dysfunction in atherosclerosis. J Vasc Res 33:181-194
6. 6. Schaper W, Ito WD (1996) Molecular mechanisms of coronary collateral vessel growth. Circ Res 79:911-919
7. 7. Risau W, Flamme I (1995) Vasculogenesis. Ann Rev Cell Dev Biol 11:73-91
8. 8. Carmeliet P, Collen D (1997) Molecular analysis of blood vessel formation and disease. Amer J Physiol 42:H2091-H2104
9. 9. Risau W (1997) Mechanisms of angiogenesis. Nature 386:671-674
10. 10. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen DH, Chen DF, Symes JF, Fishman MC, Huang PL, Isner JM (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101:2567-2578
11. 11. Ku DD, Zaleski JK, Liu S, Brock TA (1993) Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am J Physiol 265:H586-H592
12. 12. Kroll J, Waltenberger J (1998) VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem Biophys Res Commun 252:743-746
13. 13. Parenti A, Morbidelli L, Cui XL, Douglas JG, Hood JD, Granger HJ, Ledda F, Ziche M (1998) Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase(1/2) activation in postcapillary endothelium. J Biol Chem 273:4220-4226
14. 14. Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ, Bicknell R (1997) Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99:2625-2634
15. 15. Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med 1:27-31
16. 16. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182-1186
17. 17. Folkman J (1998) Therapeutic angiogenesis in ischemic limbs. Circulation 97: 1108-1110
18. 18. Schaper W, Buschmann I (1999) Collateral circulation and diabetes. Circulation 99:2224-2226
19. 19. Ferrara N, Davis-Smyth T (1997) The biology of vascular endothelial growth factor. Endocrine Rev 18:4-25
20. 20. Korpelainen ET, Alitalo K (1998) Signaling angiogenesis and lymphangiogenesis. Curr Opin Cell Biol 10:159-164
21. 21. Meyer M, Clauss M, LeppleWienhues A, Waltenberger J, Augustin HG, Ziche M, Lanz C, Buttner M, Rziha HJ, Dehio C (1999) A novel vascular endothelial growth factor encoded by Orf virus, VEGF-E, mediates angiogenesis via signalling through VEGFR-2 (KDR) but not VEGFR-1 (Flt-1) receptor tyrosine kinases. EMBO J 18:363-374
22. 22. Wise LM, Veikkola T, Mercer AA, Savory LJ, Fleming SB, Caesar C, Vitali A, Makinen T, Alitalo K, Stacker SA (1999) Vascular endothelial growth factor (VEGF)-like protein from orf virus NZ2 binds to VEGFR2 and neuropilin-1. Proc Natl Acad Sci USA 96:3071-3076
23. 23. Ogawa S, Oku A, Sawano A, Yamaguchi S, Yazaki Y, Shibuya M (1998) A novel type of vascular endothelial growth factor, VEGF-E (NZ-7 VEGF), preferentially utilize KDR/Flk-1 receptor and carries a potent activity without heparin-binding domain. J Biol Chem 273:31273-31282
24. 24. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:435-439
25. 25. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439
26. 26. Carmeliet P, NG Y-S, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Muttot V, Perriard J-C, Dewerchin M, Flameng W, Nagy A, Lupu F, Moons L, Collen D, D'Amore PA, Shima DT (1999) Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nature Med 5:495-502
27. 27. Pepper MS, Ferrara N, Orci L, Montesano R (1991) Vascular endothelial growth factor (VEGF) induces plasminogen activators and plasminogen activator inhibitor type 1 in microvascular endothelial cells. Biochem Biophys Res Commun 181:902-908
28. 28. Unemori EN, Ferrara N, Bauer EA, Amento EP (1992) Vascular endothelial growth factor induces interstitial collagenase expression in human endothelial cells. J Cell Physiol 153:557-562
29. 29. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219:983-985
30. 30. Melder RJ, Koenig GC, Witwer BP, Safabakhsh N, Munn LL, Jain RK (1996) During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nature Med 2:992-997
31. 31. Clauss M, Weich H, Breier G, Knies U, Röckl W, Waltenberger J, Risau W (1996) The vascular endothelial growth factor receptor Flt-1 mediates biological activities - Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 271:17629-17634
32. 32. Hood JD, Meininger CJ, Ziche M, Granger HJ (1998) VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells - Rapid Communication. Amer J Physiol 43: H1054-H1058
33. 33. Lei JX, Jiang AX, Pei DQ (1998) Identification and characterization of a new splicing variant of vascular endothelial growth factor: VEGF183. BBA Gene Struct Express 1443:400-406
34. 34. Breier G, Clauss M, Risau W (1995) Coordinate expression of vascular endothelial growth factor receptor-1 (flt-1) and its ligand suggests a parcrine regulation of murine vascular develpoment. Dev Dyn 204:228-239
35. 35. Kranz A, Rau C, Kochs M, Waltenberger J (2000) Elevation of vascular endothelial growth factor-A serum levels following acute myocardial infarction. Evidence for its origin and functional significance. J Mol Cell Cardiol 32:65-72
36. 36. Shweiki D, Itin A, Soffer D, Keshet E (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843-845
37. 37. Banai S, Shweiki D, Pinson A, Chandra M, Lazarovici G, Keshet E (1994) Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: implications for coronary angiogenesis. Cardiovasc Res 28:1176-1179
38. 38. Ikeda E, Achen MG, Breier G, Risau W (1995) Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 270:19761-19766
39. 39. Levy AP, Levy NS, Goldberg MA (1996) Hypoxia-inducible protein binding to vascular endothelial growth factor mRNA and its modulation by the von Hippel Lindau protein. J Biol Chem 271:25492-25497
40. 40. Cao Y, Linden P, Shima D, Browne F, Folkman J (1996) In vivo angiogenic activity and hypoxia induction of heterodimeres of Placenta Growth Factor/Vascular Endothelial Growth Factor. J Clin Invest 98:2507-2511
41. 41. Olofsson B, Pajusola K, Kaipainen A, Voneuler G, Joukov V, Saksela O, Orpana A, Petersson RF, Alitalo K, Eriksson U (1996) Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc Natl Acad Sci USA 93:2576-2581
42. 42. Achen MG, Jeltsch M, Kukk E, Makinen T, Vitali A, Wilks AF, Alitalo K, Stacker SA (1998) Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 95:548-553
43. 43. Terman BI, Carrion ME, Kovacs E, Rasmussen BA, Eddy RL, Shows TB (1991) Identification of a new endothelial cell growth factor receptor tyrosine kinase. Oncogene 6:1677-1683
44. 44. Shibuya M, Yamaguchi S, Yamane A, Ikeda T, Tojo A, Matsushime H, Sato M (1990) Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 5:519-524
45. 45. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH (1994) Different signal transduction properties of KDR and Fltl, two receptors for vascular endothelial growth factor. J Biol Chem 269:26988-26995
46. 46. Kranz A, Mayr U, Frank H, Waltenberger J (1999) The coronary endothelium: A target for VEGF. Human coronary artery endothelilal cells express functional receptor for VEGF in vitro and in vivo. Lab Invest 79:985-991
47. 47. Waltenberger J, Mayr U, Pentz S, Hombach V (1996) Functional upregulation of the vascular endothelial growth factor receptor KDR by hypoxia. Circulation 94:1647-1654
48. 48. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu X-F, Breitman ML, Schuh AC (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:62-66
49. 49. Fong G-H, Rossant J, Gertsenstein M, Breitman ML (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70
50. 50. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M (1998) Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA 95:9349-9354
51. 51. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92:735-745
52. 52. Kendall RL, Wang G, Thomas KA (1996) Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem Biophys Res Commun 226:324-328
53. 53. Aprelikova O, Pajusola K, Partanen J, Armstrong E, Alitalo R, Bailey SK, McMahon J, Wasmuth J, Huebner K, Alitalo K (1992) FLT4, a novel class III receptor tyrosine kinase in chromosome 5q33-qter. Cancer Res 52:746-748
54. 54. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K (1996) 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
55. 55. Dumont DJ, Jussila L, Taipale J, Lymboussaki A, Mustonen T, Pajusola K, Breitman M, Alitalo K (1998) Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282:946-949
56. 56. Hunter T (1996) Tyrosine phosphorylation: Past, present and future. Biochem Soc Trans 24:307-327
57. 57. Claesson-Welsh L (1996) Mechanism of action of platelet-derived growth factor. Tnt J Biochem Cell Biol 28:373-385
58. 58. Landgren E, Schiller P, Cao YH, Claesson-Welsh L (1998) Placenta growth factor stimulates MAP kinase and mitogenicity but not phospholipase C-gamma and migration of endothelial cells expressing Flt 1. Oncogene 16:359-367
59. 59. Kroll J, Waltenberger J (1997) The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J Biol Chem 272:32521-32527
60. 60. Cunningham SA, Tran TM, Arrate MP, Bjerckc R, Brock TA (1999) KDR activation is crucial for VEGF(165)-mediated Ca2+ mobilization in human umbilical vein endothelial cells. Amer J Physiol Cell Physiol 45:C176-C181
61. 61. Yu Y, Sato JD (1999) MAP kinases, phosphatidylinositol 3-kinase, and p70 S6 kinase mediate the mitogenic response of human endothelial cells to vascular endothelial growth factor. J Cell Physiol 178:235-246
62. 62. Wellner M, Maasch C, Kupprion C, Lindschau C, Luft FC, Haller H (1999) The proliferative effect of vascular endothelial growth factor requires protein kinase C-alpha and protein kinase C-zeta. Arterioscler Thromb Vasc Biol 19:178-185
63. 63. Seetharam L, Gotoh N, Maru Y, Neufeld G, Yamaguchi S, Shibuya M (1995) A unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF. Oncogene 10:135-147
64. 64. Abedi H, Zachary I (1997) Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J Biol Chem 272:15442-15451
65. 65. Rousseau S, Houle F, Landry J, Huot J (1997) p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 15:2169-2177
66. 66. Mukhopadhyay D, Nagy JA, Manseau EJ, Dvorak HF (1998) Vascular Permeability Factor/Vascular Endothelial Growth Factor-mediated Signaling In Mouse Mesentery Vascular Endothelium. Cancer Res 58:1278-1284
67. 67. Tonks NK, Neel BG (1996) From Form to Function: Signaling by Protein Tyrosine Phosphatases. Cell 87:365-368
68. 68. Vogel W, Lammers R, Huang J, Ullrich A (1993) Activation of a Phosphotyrosine Phosphatase by Tyrosine Phosphorylation. Science 259:1611-1614
69. 69. Hof P, Pluskey S, DhePaganon S, Eck MJ, Shoelson SE (1998) Crystal structure of the tyrosine phosphatase SHP-2. Cell 92:441-450
70. 70. Leung DW, Cachianes G, Kuang W-J, Goeddel DV, Ferrara N (1989) Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246:1306-1309
71. 71. Connolly DT, Heuvelman DM, Nelson R, Olander JV, Eppley BL, Delfino JJ, Siegel NR, Leimgruber RM, Feder J (1989) Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest 84: 1470-1478
72. 72. Ferrara N (1999) Role of vascular endothelial growth factor in the regulation of angiogenesis. Kidney Int 56:794-814
73. 73. Marumo T, Schini-Kerth V, Busse R (1999) Vascular endothelial growth factor activates nuclear factor-kappaB and induce monocyte chemoattractant protein-1 in bovine retinal endothelial cells. Diabetes 48:1131-1137
74. 74. Arras M, Ito WD, Scholz D, Winkler B, Schaper J, Schaper W (1998) Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest 101:40-50
75. 75. Laitinen M, Zachary I, Breier G, Pakkanen T, Hakkinen T, Luoma J, Abedi H, Risau W, Soma M, Laakso M, Martin JF, Ylä-Herttuala S (1997) VEGF gene transfer reduces intimal thickening via increased production of nitric oxide in carotid arteries. Hum Gene Ther 8:1737-1744
76. 76. O'Brian ER, Garvin MR, Dev R, Stewart DK, Hinohara T, Simpson JB, Schwartz SM (1994) Angiogenesis in human coronary atherosclerotic plaques. Am J Pathol 145:883-894
77. 77. Inoue M, Itoh H, Ueda M, Naruko T, Kojima A, Komatsu R, Doi K, Ogawa Y, Tamura N, Takaya K, Igaki T, Yamashita J, Chun TH, Masatsugu K, Becker AE, Nakao K (1998) Vascular endothelial growth factor (VEGF) expression in human coronary atherosclerotic lesions: Possible pathophysiological significance of VEGF in progression of atherosclerosis. Circulation 98:2108-2116
78. 78. Chen YX, Nakashima Y, Tanaka K, Shiraishi S, Nakagawa K, Sueishi K (1999) Immunohistochemical expression of vascular endothelial growth factor vascular permeability factor in atherosclerotic intimas of human coronary arteries. Arterioscler Thromb Vasc Biol 19:131-139
79. 79. Ramos MA, Kuzuya M, Esaki T, Miura S, Satake S, Asai T, Kanda S, Hayashi T, Iguchi A (1998) Induction of macrophage VEGF in response to oxidized LDL and VEGF accumulation in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol 18:1188-1196
80. 80. Moulton KS, Heller E, Konerding MA, Flynn E, Palinski W, Folkman J (1999) Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation 99:1726-1732
81. 81. Laitinen M, Hartikainen J, Eranen J, Kiviniemi M, Hiltunen MO, Laakso M, Ylä-Herttuala S (1998) Catheter-mediated VEGF gene transfer to human coronary arteries after angioplasty. Safety results from phase I Kuopio angioplasty gene transfer trial. Circulation 98:1-322
82. 82. Höckel M, Burke JF (1989) Angiotropin treatment prevents flap necrosis and enhance dermal regeneration in rabbits. Arch Surg 124:693-698
83. 83. Höckel M, Schlenger K, Doctrow S, Kissel T, Vaupel P (1993) Therapeutic angiogenesis. Arch Surg 128:423-429
84. 84. Takeshita S, Zheng LP, Brogi E, Kearney M, Pu L-Q, Bunting S, Ferrara N, Symes JF, Isner JM (1994) Therapeutic angiogenesis. A single intraarterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hind limb model. J Clin Invest 93:662-670
85. 85. Harada K, Friedman M, Lopez JJ, Wang SY, Li J, Prasad PV, Pearlman JD, Edelman ER, Sellke FW, Simons M (1996) Vascular endothelial growth factor administration in chronic myocardial ischemia. Amer J Physiol 39:H1791-H1802
86. 86. Takeshita S, Pu LQ, Stein LA, Sniderman AD, Bunting S, Ferrara N, Isner JM, Symes JF (1994) Intramuscular administration of vascular endothelial growth factor induces dose-dependent collateral artery augmentation in a rabbit model of chronic limb ischemia. Circulation 90:228-234
87. 87. Unger EF, Banai S, Shou M, Lazarous DF, Jaklitsch MT, Scheinowitz M, Correa R, Klingbeil C, Epstein SE (1994) Basic fibroblast growth factor enhances myocardial collateral flow in a canine model. Am J Physiol 35:H1588-H1595
88. 88. Harada K, Grossman W, Friedman M, Edelman ER, Prasad PV, Keighley CS, Manning WJ, Sellke FW, Simons M (1994) Basic fibroblasl growth factor improves myocardial function in chronically ischemic porcine hearts. J Clin Invest 94:623-630
89. 89. Lazarous DF, Shou M, Scheinowitz M, Hodge E, Thirumurti V, Kitsiou AN, Stiber JA, Lobo AD, Hunsberger S, Guetta E, Epstein SE, Unger EF (1996) Comparative effects of basic fibroblast growth factor and vascular endothelial growth factor on coronary collateral development and the arterial response to injury. Circulation 94:1074-1082
90. 90. Isner JM, Pieczek A, Schainfeld R, Blair R, Haley L, Asahara T, Rosenfield K, Razvi S, Walsh E, Symes JF (1996) Clinical evidence of angiogenesis after arterial gene transfer of phVEGF(165) in patient with ischemic limb. Lancet 348:370-374
91. 91. Baumgartner I, Pieczek A, Manor O, Blair R, Kearney M, Walsh K, Isner JM (1998) Constitutive expression of phVEGF(165) after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 97:1114-1123
92. 92. Losordo DW, Vale PR, Symes JF, Dunnington CH, Esakof DD, Maysky M, Ashare AB, Lathi K, Isner JM (1998) Gene therapy for myocardial angiogenesis - Initial clinical results with direct myocardial injection of phVEGF(165) as sole therapy for myocardial ischemia. Circulation 98:2800-2804
93. 93. Brower V (1999) Genentech enlightens other angiogenesis programs. Nat Biotechnol 17:326-327
94. 94. Rosengart TK, Lee LY, Patel SR, Sanborn TA, Parikh M, Bergman GW, Hachamovitch R, Szulc M, Kligfield PD, Okin PM, Hahn RT, Devereux RB, Post MR, Hackett NR, Foster T, Grasso TM, Lesser ML, Isom OW, Crystal RG (1999) Angiogenesis gene therapy: phase I assessment of direct intramyocardial administration of an adenovirus vector expressing VEGF121 cDNA to individuals with clinically significant severe coronary artery disease. Circulation 100:468-474
95. 95. Rosengart TK, Patel SR, Lee LY, Sanborn TA, Hachamovitch R, Kligfield PD, Hahn RT, Isom OW, Crystal RG (1998) Safety of direct myocardial VEGF121 cDNA adenovirus-mediated angiogenesis gene therapy in conjunction with coronary bypass surgery. Circulation 98:1-321
96. 96. Waltenberger J (1998) Therapeutic angiogenesis in the heart using peptide growth factors: angiogenesis research entering clinical trials. Angiogenesis 2:115-117
97. 97. Schumacher B, Pecher P, vonSpecht BU, Stegmann T (1998) Induction of neoangiogenesis in ischemic myocardium by human growth factors: First clinical results of a new treatment of coronary heart disease. Circulation 97: 645-650
98. 98. Ito WD, Arras M, Winkler B, Scholz D, Schaper J, Schaper W (1997) Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res 80: 829-837
99. 99. Kroll J, Waltenberger J (1999) A novel function of VEGF receptor-2 (KDR): Rapid release of nitric oxide in response to VEGF-A stimulation in endothelial cells. Biochem Biophys Res Commun 265:636-639
100. 100. Hendel RC, Henry TD, Rocha-Singh K, Isner JM, Kereiakes DJ, Giordano FJ, Simons M, Bonow RO (2000) Effect of intracoronary recombinant human vascular endothelial growth factor on myocardial perfusion evidence for a dose-dependent effect. Circulation 101: 118-121
101. 101. Henry TD, Annex BH, Azrin MA, McKendall G, Willerson JT, Giordano FJ, Klein R, Gibson M, Berman DS, Luce CA, McCluskey ER (1999) Final results of the VIVA trial of rhVEGF for human therapeutic angiogenesis. Circulation 101:1-476