Publication Cover
Endothelium
Journal of Endothelial Cell Research
Volume 15, 2008 - Issue 1-2
38
Views
6
CrossRef citations to date
0
Altmetric
Mini-Review

Napoleone Ferrara and the Saga of Vascular Endothelial Growth Factor

Pages 1-8 | Received 11 Oct 2007, Accepted 19 Dec 2007, Published online: 13 Jul 2009

REFERENCES

  • Aiello L. P., Avery R., Arrigg R., Keyt B., Jampel H., Shah S., Pasquale L., Thieme H., Iwamoto M., Park J. E., Nguyen H., Aiello L. M., Ferrara N., King G. L. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. New England Journal of Medicine 1994; 331: 1480–1487
  • Bogaert E., Van Damme P., Van Den Bosch L., Robberecht W. Vascular endothelial growth factor in amyotrophic lateral sclerosis and other neurodegenerative diseases. Muscle Nerve 2006; 34: 391–405
  • Borgstrom P., Bourdon M. A., Hillan K. J., Sriramarao P., Ferrara N. Neutralizing anti-vascular endothelial growth factor antibody completely inhibits angiogenesis and growth of human prostate carcinoma microtumors. in vivo. Prostate 1998; 35: 1–10
  • Borgstrom P., Gold D. P., Hillan K. J., Ferrara N. Importance of VEGF for breast cancer angiogenesis in vivo: implications from intravital microscopy of combination treatments with an anti-VEGF neutralizing antibody and doxorubicin. Anticancer Research 1999; 19: 4203–4214
  • Borgstrom P., Hillan K. J., Sriramarao P., Ferrara N. Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: novel concept of angiostatic therapy from intravital videomicroscopy. Cancer Research 1996; 56: 4032–4039
  • Carmeliet P., Ferreira V., Breier G., Pollefeyet S., Kiechens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., 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
  • Cleaver O., Melton D. A. Endothelial signaling during development. Nature Medicine 2003; 9: 661–668
  • Collins P. D., Connolly D. T., Williams T. J. Characterization of the increase in vascular permeability induced by vascular permeability factor in vivo. British Journal of Pharmacology 1993; 109: 195–199
  • Connolly D. T., Heuvelman D. M., Nelson R., Olander J. V., Eppley B. L., Delfino J. J., Siegel N. R., Leimgruber R. M., Feder J. Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. Journal of Clinical Investigation 1989; 84: 1470–1478
  • de Vries C., Escobedo J. A., Ueno H., Houck K., Ferrara N., Williams L. T. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 1992; 255: 989–991
  • Dvorak H. F., Nagy J. A., Berse B., Brown L. F., Yeo K. T., Yeo T. K., Dvorak A. M., van de Water L., Sioussat T. M., Senger D. R. Vascular permeability factor, fibrin, and the pathogenesis of tumor stroma formation. Annals New York Academy of Sciences 1992; 667: 101–111
  • Dvorak H. F., Orenstein N. S., Carvalho A. C., Churchill W. H., Dvorak A. M., Galli S. J., Feder A. M., Rypysc J., Giovinco F. Induction of a fibrin-gel investment: an early event in line 10 hepatocarcinoma growth mediated by tumor-secreted products. Journal of Immunology 1979; 122: 166–74
  • Esser S., Wolburg K., Wolburg H., Breier G., Kurzchaliam T., Risau W. Vascular endothelial growth factor induces endothelial fenestrations in vitro. Journal of Cell Biology 1998; 140: 947–959
  • Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K. S., Powell Braxton L., Hillan K. J., Moore M. W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996; 380: 439–442
  • Ferrara N., Chen H., Davis Smyth T., Gerber H. P., Nguyen T. N., Peers D., Chisholm V., Hillan K. J., Schwall R. H. Vascular endothelial growth factor is essential for corpus luteum angiogenesis. Nature Medicine 1998; 4: 336–340
  • Ferrara N., Fujii D. K., Goldsmith P. C., Widdicombe J. H., Weiner R. I. Transport epithelial characteristics of cultured bovine pituitary follicular cells. American Journal of Physiology 1987; 252: E304–E312
  • Ferrara N., Frantz G., Le Couter J., Dillard-Telm L., Pham T., Draksharapu A., Giordano T., Peale F. Differential expression of the angiogenic factor genes VEGF and EG-VEGF in normal and polycistic human ovaries. American Journal of Pathology 2003; 162: 1881–1893
  • Ferrara N., Henzel W. J. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochemical Biophysical Research Communications 1989; 161: 851–858
  • Gerber H. P., Condorelli F., Park J., Ferrara N. Differential transcriptional regulation of the two VEGF receptor genes. Flt-1, but not Flk-1/KDR is up-regulated by hypoxia. Journal of Biological Chemistry 1997; 272: 23659–23667
  • Gerber H. P., Kowalski J., Sherman D., Eberhard D. A., Ferrara N. Complete inhibition of rhabdomyosarcoma xenograft growth and neovascularization requires blockade of both tumor and host vascular endothelial growth factor. Cancer Research 2000; 60: 6253–6258
  • Gerber H. P., Vu T. H., Ryan A. M., Kowalski J., Werb Z., Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nature Medicine 1999; 5: 623–628
  • Gerhardt H., Ruhrberg C., Abramsson A., Fujisawa H., Shima D., Betsholtz C. Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Developmental Dynamics 2004; 231: 503–09
  • Gordon M. S., Margolin K., Talpaz M., Sledge G. W., Jr., Holmgren E., Benjamin R., Stalter S., Shak S., Adelman D. Phase I safety and pharmacokinetic study of recombinant human anti-vascular endothelial growth factor in patients with advanced cancer. Journal of Clinical Oncology 2001; 19: 843–850
  • Greenberg D. A., Jin K. From angiogenesis to neuropathology. Nature 2005; 438: 954–959
  • Houck K. A., Ferrara N., Winer J., Cachianes G., Li B., Leung D. W. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Molecular Endocrinology 1991; 5: 1806–1814
  • Houck K. A., Leung D. W., Rowland A. M., Winer J., Ferrara N. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. Journal of Biological Chemistry 1992; 267: 26031–26037
  • Hurwitz H., Fehrenbacher L., Novotny W., Cartwright T., Hainsworth H., Helm W., Berlin J., Griffings S., Holmgren R., Ferrara N., Rogers B., Ross R., Baron A., Kabbinavar F. Bevacizumab plus irinotecan, fluorouracil, and leucovarin for metastatic colorectal cancer. New England Journal of Medicine 2004; 350: 2335–2342
  • Horwitz H., Saini S. Bevacizumab in the treatment of metastatic colorectal cancer: safety profile and management of adverse events. Seminars in Oncology 2006; 33: S26–S34
  • Kabbinavar F., Hurwitz H. I., Fehrenbacher L., Meropol N. J., Npvotny W. F., Lieberman G., Griffing S., Bergsland E. Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. Journal of Clinical Oncology 2003; 21: 60–65
  • Karkkainen M. J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T. V., Jeltsch M., Jackson D. G., Talikka M., Rauvala H., Betsholtz C., Alitalo K. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nature Immunology 2004; 5: 74–80
  • Kim K. J., Li B., Winer J., Armanini M., Gillett N., Phillips H. S., Ferrara N. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumor growth in vivo. Nature 1993; 362: 841–844
  • Kukk E., Lymboussaki A., Taira S., Kaipainen A., Jeltsch V., 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, 1996
  • Jussila L., Alitalo K. Vascular growth factors and lymph angiogenesis. Physiological Reviews 2002; 8: 673–700
  • Lambrechts D., Carmeliet P. VEGF at the neurovascular interface: therapeutic implications for motor neuron disease. Biochimica Biophysica Acta 2006; 1762: 1109–1121
  • Lammert E., Gu G., Mc Laughlin M., Brown D., Brekken R., Murtaugh L. C., Gerber H. P., Ferrara N., Melton D. A. Role of VEGF-A in vascularization of pancreatic islets. Current Biology 2003; 13: 1070–1074
  • Le Couter J., Kowalski J., Foster J., Hass P., Zhang Z., Dillard-Telm L., Frants G., Rangell L., Deguzman L., Keller G. A., Peale F., Gurney A., Hillan K. J., Ferrara N. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 2001; 412: 877–884
  • Le Couter J., Lin R., Ferrara N. Endocrine gland-derived VEGF and the emerging hypothesis of organ-specific regulation of angiogenesis. Nature Medicine 2002; 8: 913–917
  • Le Couter J., Moritz D. R., Li B., Phillips G. L., Liang X. H., Gerber H. P., Hillan K. J., Ferrara N. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science 2003; 299: 890–893
  • Leung D. W., Cachianes G., Kuang W. J., Goeddel D. V., Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989; 246: 1306–1309
  • Margolin K., Gordon M. S., Holmgren E., Gaudreault J., Novotny W., Fyfe G., Adelman D., Stalter S., Breed J. Phase Ib trial of intravenous recombinant humanized monoclonal antibody to vascular endothelial growth factor in combination with chemotherapy in patients with advanced cancer: pharmacologic and long-term safety data. Journal of Clinical Oncology 2001; 19: 851–856
  • Mesiano S., Ferrara N., Jaffe R. B. Role of vascular endothelial growth factor in ovarian cancer: inhibition of ascite formation by immunoneutralization. American Journal of Pathology 1998; 153: 1249–1256
  • Meyer M., Clauss M., Lepple-Wienhues A., Waltenberger J., Augustin H. G., Ziche M., Lanz C., Buttner M., Rziha H. J., Dehio C. A novel vascular endothelial growth factor encoded by Orf virsu, VEGF-E, mediated angiogenesis via signalling through VEGFR-2 (KDR) but not VEGFR-1 (Flt-1) receptor tyrosine kinases. EMBO Journal 1999; 18: 363–374
  • Nagy J. A., Masse E. M., Herzberg K. T., Meyers M. S., Yeo K. T., Sioussat T. M., Dvorak H. F. Pathogenesis of ascites tumor growth. Vascular permeability factor, vascular hyperpermeability and ascites fluid accumulation. Cancer Research 1995; 55: 360–368
  • Nico B., Mangieri D., Benagiamo V., Crivellato E., Ribatti D. Nerve growth factor as an angiogenic factor. Microvascular Research 2007; 75: 135–141
  • Park J. E., Chen H. H., Winer J., Houck K. A., Ferrara N. Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. Journal of Biological Chemistry 1994; 269: 25646–25654
  • Phillips H. S., Hains J., Leung D. W., Ferrara N. Vascular endothelial growth factor is expressed in rat corpus luteum. Endocrinology 1990; 127: 965–967
  • Presta L. G., Chen H., O'Connor S. J., Chisholm V., Meng Y. G., Krummen L., Winkler M., Ferrara N. Humanization of anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Research 1997; 57: 4593–4599
  • Raab S., Plate K. H. Different networks, common growth factors: shared growth factors and receptors of the vascular and the nervous system. Acta Neuropathologica 2007; 113: 607–626
  • Ravindranath N., Little-Ihrig L., Phillips H. S., Ferrara N., Zeleznik A. J. Vascular endothelial growth factor messanger ribonucleic acid expression in the primate ovary. Endocrinology 1992; 131: 254–260
  • Senger D. R., Connolly D. T., Van de Water L., Feder J., Dvorak H. F. Purification and NH2-terminal amino acid sequence of guinea pig tumor-secreted vascular permeability factor. Cancer Research 1990; 50: 1774–1778
  • Senger D. R., Galli S. J., Dvorak A. M., Perruzzi C. A., Harvey V. S., Dvorak H. F. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983; 219: 983–985
  • Soker S., Takashima S., Miao H. Q., Neufeld G., Klagsbrun H. M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor to vascular endothelial growth factor. Cell 1998; 92: 735–745
  • Warren R. S., Yuan H., Matli M. R., Gillett N. A., Ferrara N. Regulation by vascular endothelial growth factor of human colon cancer tumorigenesis in a mouse model of experimental liver metastasis. Journal of Clinical Investigation 1995; 95: 1789–1797
  • Whitaker G. B., Limberg B. J., Rosembaum J. S. Vascular endothelial growth factor receptor-2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of VEGF(165) and VEGF(121). Journal of Biological Chemistry 2001; 276: 25520–25531
  • Yang J. C., Haworth L., Sherry R. M., Hwu P., Schwartzentruber D. J., Tapalian S. L., Steinberg S. M., Chen H. X., Rosenberg S. A. A randomized trial of bevacizumab, an anti-VEGF antibody, for metastatic renal cancer. New England Journal of Medicine 2003; 349: 427–434
  • Yuan F., Chen Y., Dellian M., Safabakhsh N., Ferrara N., Jain R. K. Time-dependent vascular regression and permeability changes in established xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proceedings of the National Academy of Sciences of the United States of America 1996; 93: 14765–14770

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.