VEGF and VEGF-C: Specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane

Developmental Biology

Volumn 188, Issue 1, 1997, Pages 96-109

  Oh, Su Ja ^a,d   Jeltsch, Markku M ^b   Birkenhäger, Ralf ^c   McCarthy, John E G ^c   Weich, Herbert A ^c   Christ, Bodo ^a   Alitalo, Kari ^b   Wilting, Jörg ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF HELSINKI   (Finland)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d The Catholic University of Korea College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN C;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CHICK EMBRYO; CHORIOALLANTOIS; EMBRYO; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; LYMPHOCYTE DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA; AVES;

EID: 0031213636     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1997.8639     Document Type: Article

References (47)

1. Barsky S. H., Baker A., Siegal G. P., Togo S., Liotta L. A. Use of anti-basement membrane antibodies to distinguish blood vessel capillaries from lymphatic capillaries. Am. J. Surg. Pathol. 7:1983;667-677.
2. Berens von Rautenfeld D., Drenckhahn D. Bau der Lymphgefässe. Benninghoff, Alfred: Anatomie: makroskopische Anatomie, Embryologie und Histologie des Menschen. 1994;Urban & Schwarzenberg, Munich. p. 756-761.
3. Birkenhäger R., Schneppe B., Röckl W., Wilting J., Weich H. A., McCarthy J. E. G. Synthesis and physiological activity of heterodimers comprising different splice-forms of vascular endothelial growth factor and placenta growth factor. Biochem. J. 316:1996;703-707.
4. Budge A. Untersuchungen über die Entwicklung des Lymphsystems beim Hühnerembr yo. Arch. Anat. Entwickl. Gesch. 1887;59-89.
5. Cao Y., Chen H., Zhou L., Chiang M. K., Anand-Apte B., Weatherbee J. A., Wang Y., Fang F., Flanagan J. G., Lik-Shing Tsang M. Heterodimers of placenta growth factor/vascular endothelial growth factor. J. Biol. Chem. 270:1996;3154-3162.
6. 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. Abnormal blood vessel development and lethality in embryos lacking a single VEGF gene. Nature. 380:1996;435-439.
7. Casley-Smith J. R. The fine structure and functioning of tissue channels and lymphatics. Lymphology. 12:1980;177-183.
8. Clark E. R., Clark E. L. On the origin and early development of the lymphatic system of the chick. Contr. Embryol. 9:1920;447-482.
9. Connolly D. T., Heuvelman D., Nelson R., Olander J. V., Eppler B. L., Delfino J. J., Siegel N. R., Leimgruber R. M., Feder J. Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J. Clin. Invest. 84:1989;1470-1478.
10. DiSalvo J., Bayne M. L., Conn G., Kwok P. W., Trivedi P. G., Sonderman D. D., Palisi T. M., Sullivan K. A., Thomas K. A. Purification and characterization of a naturally occuring vascular endothelial growth factor:placenta growth factor heterodimer. J. Biol. Chem. 270:1995;7717-7723.
11. Eichmann A., Marcelle C., Bréant C., Le Douarin N. M. Two molecules related to the VEGF receptor are expressed in early endothelial cells during avian embryonic development. Mech. Dev. 42:1993;33-48.
12. Eichmann A., Marcelle C., Bréant C., Le Douarin N. M. Molecular cloning of Quek1 and 2, two vascular endothelial growth factor(VEGF) receptor-like molecules. Gene. 174:1996;3-8.
13. Ezaki T., Matsuno K., Fujii H., Hayashi N., Miyakawa K., Ohmori J., Kotani M. A new approach for identification of rat lymphatic capillaries using a monoclonal antibody. Arch. Histol. Cytol. Suppl. 53:1990;77-86.
14. 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. 380:1996;439-442.
15. Folkman J. Tumor angiogenesis factor. Cancer Res. 34:1974;2109-2113.
16. Fong G. H., Rossant J., Gertsenstein M., Breitman M. L. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature. 376:1995;66-70.
17. Gardner J. M., Fambrough D. M. Fibronectin expression during myogenesis. J. Cell Biol. 96:1983;474-485.
18. Gratzner H. G. Monoclonal antibody to 5-bromo 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science. 218:1982;474-475.
19. Gumkowski F., Kaminska G., Kaminski M., Morrissey L. W., Auerbach R. Heterogeneity of mouse vascular endothelium: In vitro studies of lymphatic, large blood vessel and microvascular endothelial cells. Blood Vessels. 24:1987;11-23.
20. Hamilton H. L. Lillie's development of the chick: An introduction to embryology. 1965;Holt, Rinehart & Winston, New York.
21. Hauser S., Weich H. A. A heparin-binding form of placenta growth factor (PlGF-2) is expressed in human umbilical vein endothelial cells and in placenta. Growth Factors. 9:1993;259-268.
22. Jeltsch M., Kaipainen A., Joukov V., Meng X., Lakso M., Rauvala H., Swartz M., Fukumura D., Jain R. K., Alitalo K. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science. 276:1997;1423-1425.
23. 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. 15:1996;290-298.
24. Joukov V., Kumar V., Jeltsch M., Claesson-Welsh L., Cao Y., Saksela O., Kalkkinen N., Alitalo K. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 13:1997;3898-3911.
25. Kaipainen A., Korhonen J., Mustonen T., van Hinsbergh V. W., Fang G. 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. 92:1995;3566-3570.
26. 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. 122:1996;3829-3837.
27. Kurz H., Ambrosy S., Wilting J., Marmé D., Christ B. The proliferation pattern of capillary endothelial cells in chorioallantoic membrane development indicates local growth control, which is counteracted by vascular endothelial growth factor application. Dev. Dyn. 203:1995;174-186.
28. Leung D. W., Cachianes G., Kuang W. J., Goeddel D. V., Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 246:1989;1306-1309.
29. Maglione D., Guerriero V., Viglietto G., Delli-Bovi P., Persico M. G. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc. Natl. Acad. Sci. USA. 88:1991;9267-9271.
30. Millauer B., Wizigmann-Voos S., Schnürch H., Martinez R., Moller N. P. H., Risau W., Ullrich A. High affinity VEGF binding and developmental expression suggest flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell. 72:1993;835-846.
31. Olofsson B., Pajusola K., Kaipainen A., von Euler G., Joukov V., Saksela O., Orpana A., Pettersson R. F., Alitalo K., Eriksson U. Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc. Natl. Acad. Sci. USA. 93:1996;2576-2581.
32. Park J. E., Chen H. H., Winer J., Houck K. A., Ferrara N. Placenta growth factor. J. Biol. Chem. 269:1994;25646-25654.
33. Romanoff A. L. The avian embryo: Structural and functional development. 1960;Macmillan, New York.
34. Sabin F. R. The lymphatic system in human embryos, with a consideration of the morphology of the system as a whole. Am. J. Anat. 9:1909;43-91.
35. 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. 219:1983;983-985.
36. Serra J. A. Histochemical tests for protein and aminoacids: The characterization of basic proteins. Stain Technol. 21:1946;5-18.
37. Shalaby F., Rossant J., Yamaguchi T. P., Gertsenstein M., Wu X. F., Breitman M. L., Schuh A. C. Failure of blood-island formation and vasculogenesis in flk-1 deficient mice. Nature. 376:1995;62-66.
38. Terman B. I., Dougher-Vermazen M., Carrion M. E., Dimitrov D., Armellino D. C., Gospodarowicz D., Böhlen P. Identification of the KDR tyrosine kinease as a receptor for vascular endothelial cell growth factor. Biochem. Biophys. Res. Commun. 187:1992;1579-1586.
39. Wilting J., Christ B., Bokeloh M. A modified chorioallantoic membrane (CAM) assay for qualitative and quantitative study of growth factors. Anat. Embryol. 183:1991;259-271.
40. 165. Anat. Embryol. 186:1992;251-257.
41. Wilting J., Christ B., Bokeloh M., Weich H. A. In vivo effects of vascular endothelial growth factor on the chicken chorioallantoic membrane. Cell Tissue Res. 274:1993;163-172.
42. Wilting J., Kurz H., Brand-Saberi B., Steding G., Yang Y. X., Hasselhorn H. M., Epperlein H. H., Christ B. Kinetics and differentiation of somite cells forming the vertebral column: Studies on human and chick embryos. Anat. Embryol. 190:1994;573-581.
43. 121. Dev. Biol. 176:1996;76-85.
44. Wilting J., Eichmann A., Christ B. The avian VEGF receptor homologues Quek1 and Quek2 during quail embryonic development: Expression in blood-vascular and lymphatic endothelial and non-endothelial cells. Cell Tissue Res. 288:1997a;207-223.
45. Wilting J., Kurz H., Oh S-J., Christ B. Angiogenesis and lymphangiogenesis: Analogous mechansims and homologous growth factors. Little C., Mironov V., Sage H. Vascular Morphogenesis: In Vivo, in Vitro and in Sapiente. 1997b;Birkhäuser, Boston.
46. Witte M. H., Witte C. L. Lymphangiogenesis and lymphologic syndromes. Lymphology. 19:1986;21-28.
47. Witte M. H., Witte C. L. Lymphatics and blood vessels, lymphangiogenesis and hemangiogenesis: From cell biology to clinical medicine. Lymphology. 20:1987;257-266.