Vascular endothelial growth factor-C (VEGF-C/VEGF-2) promotes angiogenesis in the setting of tissue ischemia

American Journal of Pathology

Volumn 153, Issue 2, 1998, Pages 381-394

  Witzenbichler, Bernhard ^a   Asahara, Takayuki ^a   Murohara, Toyoaki ^a   Silver, Marcy ^a   Spyridopoulos, Ioakim ^a   Magner, Meredith ^a   Principe, Nicole ^a   Kearney, Marianne ^a   Hu, Jing Shan ^b   Isner, Jeffrey M ^a,c  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GLAXOSMITHKLINE   (United States)

^c ST ELIZABETH'S MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BLOOD VESSEL PERMEABILITY; CHEMOTAXIS; CONTROLLED STUDY; ENDOTHELIUM CELL; HEART MUSCLE ISCHEMIA; HUMAN; HUMAN CELL; ISCHEMIA; LIMB ISCHEMIA; MITOGENESIS; NEOVASCULARIZATION (PATHOLOGY); PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 0031830312     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)65582-4     Document Type: Article

References (76)

1. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N: Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989, 246:1306-1309
2. Connolly DT, Hewelman DM, Nelson R, Olander JV, Eppley BL, Delfino JJ, Siegel RN, Leimgruber RS, Feder J: Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest 1989, 84:1470-1478
3. Plouet J, Schilling J, Gospodarowicz D: Isolation and characterization of a newly identified endothelial cell mitogen produced by AtT-20 cells. EMBO J 1989, 8:3801-3806
4. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF: Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983, 219:983-985
5. Breier G, Albrecht U, Sterrer S, Risau W: Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation Development 1992, 114:521-532
6. Drake CJ, Little CD: Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc Natl Acad Sci USA 1995, 92:7657-7661
7. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Kendraprasad H, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A: Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439
8. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Milan KJ, Moore MW: Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380:439-442
9. 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 1995, 1:1024-1028
10. Peters KG, deVries C, Williams LT: Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci USA 1993, 90:8915-8919
11. Tsurumi Y, Murohara T, Krasinski K, Dongfen C, Witzenbichler B, Kearney M, Couffinhal T, Isner JM: Reciprocal relationship between VEGF and NO in the regulation of endothelial integrity. Nat Med 1997, 3:879-886
12. Takeshita S, Zheng LP, Brogi E, Kearney M, Pu LQ, Bunting S, Ferrara N, Symes JF, Isner JM: Therapeutic angiogenesis: a single intra-arterial bolus of vascular endothelial growth factor augments revascularization in a rabbit ischemic hindlimb model. J Clin Invest 1994, 93:662-670
13. Pearlman JD, Hibberd MG, Chuang ML, Harada K, Lopez JJ, Gladston SR, Friedman M, Sellke FW, Simons M: Magnetic resonance mapping demonstrates benefits of VEGF-induced myocardial angiogenesis. Nat Med 1995, 1:1085-1089
14. Banai S, Jaklitsch MT, Shou M, Lazarous DF, Scheinowitz M, Biro S, Epstein SE, Linger EF: Angiogenic-induced enhancement of collateral blood flow to ischemic myocardium by vascular endothelial growth factor in dogs. Circulation 1994, 89:2183-2189
15. 165. Lancet 1996, 348:370-374
16. Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995, 1:27-30
17. Plate KH, Breier G, Millauer B, Ullrich A, Risau W: Up-regulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res 1993, 53:5822-5827
18. Plate KH, Breier G, Weich HA, Risau W: Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992, 359:845-848
19. Kim KJ, Li B, Winer J, Armanini M, Billett N, Phillips HS, Ferrara N: Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 1993, 362:841-844
20. 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 1996, 15:290-298
21. Olofsson B, Pajusola K, Kaipainen A, vonEuler G, Joukov V, Saksela O, Orpana A, Pettersson RF, Alitalo K, Eriksson U: Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc Natl Acad Sci USA 1996, 93:2576-2581
22. Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG: Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 1991, 88:9267-9271
23. Maglione D, Guerriero V, Viglietto G, Ferrara MG, Aprelikova O, Alitalo K, Del Vecchio S, Lei KJ, Chou JY, Persico MG: Two alternative mRNAs coding for the angiogenic factor, placenta growth factor (PIGF), are transcribed from a single gene of chromosome 14. Oncogene 1993, 8:925-931
24. Hauser S, Weich HA: A heparin-binding form of placenta growth factor (PIGF-2) is expressed in human umbilical vein endothelial cells, and in placenta. Growth Factors 1993, 9:259-268
25. Park JE, Keller G-A, Ferrara N: The vascular endothelial growth factor (VEGF) isoforms differential deposition into the subepithelial ECM and bioactivity of ECM-bound VEGF. Mol Biol Cell 1993, 4:1317-1326
26. Park JE, Chen HH, Winer J, Houck KA, Ferrara N: Placenta growth factor: potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J Biol Chem 1994, 269:25646-25654
27. DiSalvo J, Bayne ML, Conn G, Kwok PW, Trivedi PG, Soderman DD, Palisi TM, Sullivan KA, Thomas KA: Purification and characterization of a naturally occurring vascular endothelial growth factor: placenta growth factor heterodimer. J Biol Chem 1995, 270:7717-7723
28. Cao Y, Linden P, Shima D, Browne F, Folkman J: In vivo angiogenic activity and hypoxia induction of heterodimer of placenta growth factor/vascular endothelial growth factor. J Clin Invest 1996, 98:2507-2511
29. Cao Y, Chen H, Zhou L, Chiang MK, Anand-Apte B, Weatherbee JA, Wang Y, Fang F, Flanagan JG, Tsang MLS: Heterodimers of placenta growth factor/vascular endothelial growth factor: endothelial activity, tumor cell expression and high affinity binding to Flk-1/KDR. J Biol Chem 1996, 271:3154-3162
30. Shweiki D, Itin A, Soffer D, Keshet E: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992, 359:843-845
31. Brogi E, Wu T, Namiki A, Isner JM: Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, while hypoxia upregulates VEGF expression only. Circulation 1994, 90:649-652
32. Lee J, Gray A, Yuan J, Luoh S, Avraham H, Wood WI: Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA 1996, 93:1988-1992
33. Pajusola K, Aprelikova O, Pelicci G, Weich H, Claesson Welsh L, Alitalo K: Signaling properties of FLT4, a proteolytically processed receptor tyrosine kinase related to two VEGF receptors. Oncogene 1994, 9:3545-3555
34. Ferrara N, Davis-Smyth: The biology of vascular endothelial growth factor. Endocr Rev 1997, 18:4-25
35. Couffinhal T, Kearney M, Witzenbichler B, Chen D, Murohara T, Losordo DW, Symes JF, Isner JM: Vascular endothelial growth factor/ vascular permeability factor (VEGF/VPF) in normal and atherosclerotic human arteries. Am J Pathol 1997, 150:1673-1685
36. Jeltsch M, Kaipainen A, Joukov V, Meng X, Lakso M, Rauvala H, Swartz M, Fukumura D, Jain RK, Alitalo K: Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 1997, 276:1423-1425
37. Leibovich SJ, Polverini PJ, Fong TW, Harlow LA, Koch AE: Production of angiogenic activity by human monocytes requires an L-arginine/ nitric oxide-synthase-dependent effector mechanism. Proc Natl Acad Sci USA 1994, 91:4190-4194
38. Asahara T, Bauters C, Wu T, Zheng LP, Chen D, Symes J, Isner JM: Nitric oxide precursor augments angiogenesis and attenuates endothelial dysfunction in collateral circulation in rabbit ischemic hindlimb in vivo (Abstract). FASEB J 1996, 10:A545
39. Morbidelli L, Chang C-H, Douglas JG, Granger HJ, Ledda F, Ziche M: Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol 1995, 270:H411-H415
40. Ziehe M, Morbidelli L, Masini E, Amerini S, Granger HJ, Maggi CA, Geppetti P, Ledda F: Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 1994, 94:2036-2044
41. Hu J-S, Hastings GA, Cherry S, Gentz R, Ruben S, Coleman TA: A novel regulatory function of proteolytically cleaved VEGF-2 for vascular endothelial and smooth muscle cells. FASEB J 1997, 11:498-504
42. Bonnerot C, Rocancourt D, Briand P, Grimber G: A β-galactosidase hybrid protein targeted to nuclei as a marker for developmental studies. Proc Natl Acad Sci USA 1987, 84:6795-6799
43. Jaffe EA, Nachman RL, Becker CG, Minick CR: Culture of human endothelial cells derived from umbilical veins. J Clin Invest 1973, 52:2745-2756
44. Schlingemann RO, Domgjan GM, Emeis JJ, Blok J, Warnaar SO, Ruiter DJ: Monoclonal antibody PAL-E specific for endothelium. Lab Invest 1985, 52:71-76
45. Buttke TM, McCubrey JA, Owen TC: Use of an aqueous soluble tetrazolium/formazan assay to measure viability and proliferation of lymphokine-dependent cell lines. J Immunol Methods 1993, 157:233-240
46. Falk W, Goodwin RH, Leonard EJ: A 48 well microchemotaxis assembly for rapid and accurate measurement of leukocyte migration. J Immunol Methods 1980, 33:239-247
47. Shibuki K, Okada D: endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 1991, 358: 676-678
48. Weyrich AS, Ma X-I, Buerke M, Murohara T, Armstead VE, Lefer AM, Nicolas JM, Thomas AP, Lefer DJ, Vinten-Johansen J: Physiological concentrations of nitric oxide do not elicit an acute negative inotropic effect in unstimulated cardiac muscle. Circ Res 1994, 75:692-700
49. Miles AA, Miles EM: Vascular reactions to histamine, histamine liberators or leukotoxins in the skin of the guinea pig. J Physiol 1952, 118:228-257
50. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159
51. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, ed 2. New York, Cold Spring Harbor Laboratory Press, 1989, pp 8.60-8.63
52. Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KG, Ehrlich HA: Primer-directed enzymatic amplification of DNA with thermostable DNA polymerase. Science 1988, 239:487-491
53. Hewett PW, Murray JC: Coexpression of flt-1, flt-4 and KDR in freshly isolated and cultured human endothelial cells. Biochem Biophys Res Commun 1996, 221:697-702
54. Bauters C, Asahara T, Zheng LP, Takeshita S, Bunting S, Ferrara N, Symes JF, Isner JM: Physiologic assessment of augmented vascularity induced by VEGF in ischemic rabbit hindlimb. Am J Physiol 1994, 267:H1263-H1271
55. Pu LQ, Jackson S, Lachapelle KJ, Arekat Z, Graham AM, Lisbona R, Brassard R, Carpenter S, Symes JF: A persistent hindlimb ischemia model in the rabbit. J Invest Surg 1994, 7:49-60
56. Takeshita S, Pu L-Q, Zheng L, Ferrara N, Stein LA, Sniderman AD, Isner JM, Symes JF: Vascular endothelial growth factor induces dose-dependent revascularization in a rabbit model of persistent limb ischemia. Circulation 1994, 90:II-228-II-234
57. Walter DH, Hink U, Asahara T, Van Belle E, Horowitz J, Tsurumi Y, Vandlen R, Heinsohn H, Keyt B, Ferrara N, Symes JF, Isner JM: The in vivo bioactivity of vascular endothelial growth factor/vascular permeability factor is independent of N-linked glycosylation. Lab Invest 1996, 74:546-556
58. Ku DD, Zaleski JK, Liu S, Brock TA: Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am J Physiol 1993, 265:H586-H592
59. Doucette JW, Corl PD, Payne HM, Flynn AE, Goto M, Nassi M, Segal J: Validation of a Doppler wire for intravascular measurements of coronary artery flow velocity. Circulation 1992, 85:1899-1911
60. Ziada AM, Hudlicka O, Tyler KR, Wright AJ: The effect of long-term vasodilation on capillary growth and performance in rabbit heart and skeletal muscle. Cardiovasc Res 1984, 18:724-732
61. 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 1997, 95:1030-1037
62. Paavonen K, Horeli-Kuitunen N, Chilov D, Kukk E, Pennanen S, Kallioniemi O, Pajusola K, Olofsson B, Eriksson U, Joukov V, Palotie A, Alitalo K: Novel human vascular endothelial growth factor genes VEGF-B and VEGF-C localize to chromosomes 11q13 and 4q34, respectively. Circulation 1996, 93:1079-1082
63. 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 Natl Acad Sci USA 1995, 92:3566-3570
64. 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 1996, 75:487-502
65. Sholley MM, Ferguson GP, Seibel HR, Montour JL, Wilson JD: Mechanisms of neovascularization: vascular sprouting can occur without proliferation of endothelial cells. Lab Invest 1984, 51:624-634
66. Ziehe M, Morbidelli L, Choudhuri R, Zhang H-T, Donnini S, Granger HJ, Bicknell R: Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not fibroblast growth factor-induced angiogenesis. J Clin Invest 1997, 99:2625-2634
67. 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 1998, 101:2567-2578
68. Murohara T, Horowitz J, Silver M, Tsurumi Y, Sullivan A, Isner JM: Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation 1998, 97:99-107
69. Dvorak HF, Brown LF, Detmar M, Dvorak AM: Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 1995, 146:1029-1039
70. Takeshita S, Rossow ST, Kearney M, Zheng LP, Bauters C, Bunting S, Ferrara N, Symes JF, Isner JM: Time course of increased cellular proliferation in collateral arteries following administration of vascular endothelial growth factor in a rabbit model of lower limb vascular insufficiency. Am J Pathol 1995, 147:1649-1660
71. 165 following intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 1998, 97:1114-1123
72. 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. Biochem Biophys Res Commun 1996, 227: 628-635
73. Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsch M, Joukov V, Alitalo K: VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 1996, 122:3829-3837
74. Brogi E, Schatteman G, Wu T, Kim EA, Varticovski L, Keyt B, Isner JM: Hypoxia-induced paracrine regulation of VEGF receptor expression. J Clin Invest 1996, 97:469-476
75. Waltenberger J, Mayr U, Pentz S, Hombach V: Functional upregulation of the vascular endothelial growth factor receptor KDR by hypoxia. Circulation 1996, 94:1647-1654
76. 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 1996, 7:959-988