Microenvironmental VEGF concentration, not total dose, determines a threshold between normal and aberrant angiogenesis

Journal of Clinical Investigation

Volumn 113, Issue 4, 2004, Pages 516-527

  Ozawa, Clare R ^a   Banfi, Andrea ^a   Glazer, Nicole L ^b   Thurston, Gavin ^c   Springer, Matthew L ^a,d   Kraft, Peggy E ^a   McDonald, Donald M ^b   Blau, Helen M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c REGENERON PHARMACEUTICALS INC   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HEMANGIOMA; IMPLANTATION; MALE; MAXIMUM ALLOWABLE CONCENTRATION; MORPHOLOGY; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; RETROVIRUS; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL TRANSPLANTATION; CYTOLOGY; EAR; GENETICS; HISTOLOGY; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PHENOTYPE; PHYSIOLOGY;

ANIMALS; BLOOD VESSELS; CELL TRANSPLANTATION; CELLS, CULTURED; EAR; MALE; MICE; MICE, INBRED C57BL; MYOBLASTS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85047694677     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI18420     Document Type: Article

References (48)

1. Ferrara, N. 2000. VEGF: an update on biological and therapeutic aspects. Curr. Opin. Biotechnol. 11:617-624.
2. Jones, N., Iljin, K., Dumont, D.J., and Alitalo, K. 2001. Tie receptors: new modulators of angiogenic and lymphangiogenic responses. Nat. Rev. Mol. Cell. Biol. 2:257-267.
3. Yancopoulos, G.D., Davis, S., Gale, N.W., Rudge, J.S., Wiegand, S.J., and Holash, J. 2000. Vascular-specific growth factors and blood vessel formation. Nature. 407:242-248.
4. Carmeliet, P., and Jain, R.K. 2000. Angiogenesis in cancer and other diseases. Nature. 407:249-257.
5. Isner, J.M., et al. 1996. Clinical evidence of angiogenesis after arterial gene transfer of phVEGF165 in patient with ischaemic limb. Lancet. 348:370-374.
6. Mack, C.A., et al. 1998. Biologic bypass with the use of adenovirus-mediated gene transfer of the complementary deoxyribonucleic acid for vascular endothelial growth factor 121 improves myocardial perfusion and function in the ischemic porcine heart. J. Thorac. Cardiovasc. Surg. 115:168-176.
7. Magovern, C.J., et al. 1997. Regional angiogenesis induced in nonischemic tissue by an adenoviral vector expressing vascular endothelial growth factor. Hum. Gene Ther. 8:215-227.
8. Muhlhauser, J., et al. 1995. VEGF165 expressed by a replication-deficient recombinant adenovirus vector induces angiogenesis in vivo. Circ. Res. 77:1077-1086.
9. Takeshita, S., et al. 1996. Gene transfer of naked DNA encoding for three isoforms of vascular endothelial growth factor stimulates collateral development in vivo. Lab. Invest. 75:487-501.
10. Tsurumi, Y., et al. 1996. Direct intramuscular gene transfer of naked DNA encoding vascular endothelial growth factor augments collateral development and tissue perfusion. Circulation. 94:3281-3290.
11. Drake, C.J., and Little, C.D. 1995. Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc. Natl. Acad. Sci. U. S. A. 92:7657-7661.
12. Ash, J.D., and Overbeek, P.A. 2000. Lens-specific VEGF-A expression induces angioblast migration and proliferation and stimulates angiogenic remodeling. Dev. Biol. 223:383-398.
13. Dor, Y., et al. 2002. Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J. 21:1939-1947.
14. Thurston, G., et al. 1999. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 286:2511-2514.
15. Springer, M.L., Chen, A.S., Kraft, P.E., Bednarski, M., and Blau, H.M. 1998. VEGF gene delivery to muscle: potential role for vasculogenesis in adults. Mol. Cell. 2:549-558.
16. Lee, R.J., et al. 2000. VEGF gene delivery to myocardium: deleterious effects of unregulated expression. Circulation. 102:898-901.
17. Schwarz, E.R., et al. 2000. 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.
18. Pettersson, A., et al. 2000. Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab. Invest. 80:99-115.
19. Sundberg, C., et al. 2001. Glomeruloid microvascular proliferation follows adenoviral vascular permeability factor/vascular endothelial growth factor-164 gene delivery. Am. J. Pathol. 158:1145-1160.
20. Blau, H.M., and Banfi, A. 2001. The well-tempered vessel. Nat. Med. 7:532-534.
21. Carmeliet, P., et al. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 380:435-439.
22. Ferrara, N., et al. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 380:439-442.
23. Miquerol, L., Langille, B.L., and Nagy, A. 2000. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development. 127:3941-3946.
24. Suri, C., et al. 1998. Increased vascularization in mice overexpressing angiopoietin-1. Science. 282:468-471.
25. Thurston, G., et al. 2000. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat. Med. 6:460-463.
26. Rando, T.A., and Blau, H.M. 1994. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell Biol. 125:1275-1287.
27. Springer, M.L., and Blau, H.M. 1997. High-efficiency retroviral infection of primary myoblasts. Somat. Cell Mol. Genet. 23:203-209.
28. Field, J., et al. 1988. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol. 8:2159-2165.
29. Springer, M.L., Rando, T.A., and Blau, H.M. 1997. Gene delivery to muscle. In Curentprotocols in human genetics. A.L. Boyle, editor. John Wiley & Sons. New York, New York, USA. 13.4.1-13.4.19.
30. Holash, J., et al. 2002. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc. Natl. Acad. Sci. U. S. A. 99:11393-11398.
31. Rosai, J. 1996. Soft tissues. In Ackerman's surgical pathology. Mosby-Year Book Inc. St. Louis, Missouri, USA. 2061-2064.
32. Springer, M.L., et al. 2003. Localized arteriole formation directly adjacent to the site of VEGF-Induced angiogenesis in muscle. Mol. Ther. 7:441-449.
33. Isner, J.M. 2002. Myocardial gene therapy. Nature. 415:234-239.
34. Carmeliet, P. 2000. VEGF gene therapy: stimulating angiogenesis or angioma-genesis? Nat. Med. 6:1102-1103.
35. Morikawa, S., et al. 2002. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 160:985-1000.
36. Hirschi, K.K., Rohovsky, S.A., Beck, L.H., Smith, S.R., and D'Amore, P.A. 1999. Endothelial cells modulate the proliferation of mural cell precursors via platelet-derived growth factor-BB and heterotypic cell contact. Circ. Res. 84:298-305.
37. Anronelli-Orlidge, A., Saunders, K.B., Smith, S.R., and D'Amore, P.A. 1989. An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proc. Natl. Acad. Sci. U. S. A. 86:4544-4548.
38. Hellstrom, M., et al. 2001. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J. Cell Biol. 153: 543-553.
39. Gussoni, E., Blau, H.M., and Kunkel, L.M. 1997. The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat. Med. 3:970-977.
40. Rando, T.A., Pavlath, G.K., and Blau, H.M. 1995. The fate of myoblasts following transplantation into mature muscle. Exp. Cell Res. 220:383-389.
41. Houck, K.A., Leung, D.W., Rowland, A.M., Winer, J., and Ferrara, N. 1992. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem. 267:26031-26037.
42. Park, J.E., Keller, G.A., and Ferrara, N. 1993. The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol. Biol. Cell. 4:1317-1326.
43. Simons, M., et al. 2000. Clinical trials in coronary angiogenesis: issues, problems, consensus: An expert panel summary. Circulation. 102:E73-E86.
44. Epstein, S.E., Fuchs, S., Zhou, Y.F., Baffour, R., and Kornowski, R. 2001. Therapeutic interventions for enhancing collateral development by administration of growth factors: basic principles, early results and potential hazards. Cardiovasc. Res. 49:532-542.
45. Isner, J.M., Vale, P.R., Symes, J.F., and Losordo, D.W. 2001. Assessment of risks associated with cardiovascular gene therapy in human subjects. Circ. Res. 89:389-400.
46. Ozawa, C.R., Springer, M.L., and Blau, H.M. 2000. A novel means of drug delivery: myoblast-mediated gene therapy and regulatable retroviral vectors. Annu. Rev. Pharmacol. Toxicol. 40:295-317.
47. Lutolf, M.P., et al. 2003. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc. Natl. Acad. Sci. U. S. A. 100:5413-5418.
48. Richardson, T.P., Peters, M.C., Ennett, A.B., and Mooney, D.J. 2001. Polymeric system for dual growth factor delivery. Nat. Biotechnol. 19:1029-1034.