Evidence for the existence of a novel pregnancy-associated soluble variant of the vascular endothelial growth factor receptor, Flt-1

Molecular Human Reproduction

Volumn 4, Issue 4, 1998, Pages 377-386

  Banks, R E ^a   Forbes, M A ^a   Searles, J ^a   Pappin, D ^b   Canas, B ^b   Rahman, D ^b   Kaufmann, S ^a   Walters, C E ^c   Jackson, A ^a   Eves, P ^a   Linton, G ^a   Keen, J ^c   Walker, J J ^a   Selby, P J ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Angiogenesis; Flt 1; Pregnancy; Soluble receptor; VEGF

Indexed keywords

VASCULOTROPIN;

ALTERNATIVE RNA SPLICING; ANGIOGENESIS; ARTICLE; BIOSENSOR; EMBRYO DEVELOPMENT; EXON; EXTRACELLULAR MATRIX; GLYCOSYLATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; OVULATION; PREGNANCY; PRIORITY JOURNAL; RECEPTOR AFFINITY; RETINOPATHY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMINO ACID SEQUENCE; ENDOTHELIAL GROWTH FACTORS; FEMALE; FETAL BLOOD; HUMANS; LYMPHOKINES; MALE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PLACENTA; PREGNANCY; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SOLUBILITY; UMBILICAL VEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 7144255515     PISSN: 13609947     EISSN: None     Source Type: Journal    
DOI: 10.1093/molehr/4.4.377     Document Type: Article

References (74)

1. Ahmed, A., Dunk, C., Kniss, D. et al. (1997) Role of VEGF receptor-1 (Flt-1) in mediating calcium-dependent nitric oxide release and limiting DNA synthesis in human trophoblast cells. Lab. Invest., 76, 779-791.
2. Baker, P.N., Krasnow, J., Roberts, J.M. et al. (1995) Elevated serum levels of vascular endothelial growth factor in patients with preeclampsia. Obstet. Gynecol., 86, 815-821.
3. Banks, R.E., Forbes, M.A., Kinsey, S.E. et al. (1998) Release of the angiogenic cytokine vascular endothelial growth factor (VEGF) from platelets: significance for VEGF measurements and cancer biology. Br. J. Cancer, 77, 956-964.
4. Barleon, B., Hauser, S., Schollmann, C. et al. (1994) Differential expression of the two VEGF receptors flt and KDR in placenta and vascular endothelial cells. J. Cell. Biochem., 54, 56-46.
5. Barleon, B., Sozzani, S., Zhou, D. et al. (1996) Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood, 87, 3336-3343.
6. Barleon, B., Totzke, F., Herzog, C. et al. (1997) Mapping of the sites for ligand binding and receptor dimerization at the extracellular domain of the vascular endothelial growth factor receptor Flt-1. J. Biol. Chem., 272, 10382-10388.
7. Boocock, C.A., Charnock-Jones, D.S., Sharkey, A.M. et al. (1995) Expression of vascular endothelial growth factor and its receptors flt and KDR in ovarian carcinoma. J. Natl. Cancer Inst., 87, 506-516.
8. Breier, G., Albrecht, U., Sterrer, S. et al. (1992) Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development, 114, 521-532.
9. Carmeliet, P., Ferreira, V., Breier, G. et al. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature, 380, 435-439.
10. Charnock-Jones, D.S., Sharkey, A.M., Boocock, C.A. et al. (1994) Vascular endothelial growth factor receptor localization and activation in human trophoblast and choriocarcinoma cells. Biol. Reprod., 51, 524-530.
11. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
12. Clark, D.E., Smith, S.K., Sharkey, A.M. et al. (1996) Localization of VEGF and expression of its receptors flt and KDR in human placenta throughout pregnancy. Hum. Reprod., 11, 1090-1098
13. Connolly, D.T., Heuvelman, D.M., Nelson, R. et al. (1989) Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J. Clin. Invest., 84, 1470-1478.
14. Cooper, J.C., Sharkey, A.M., Charnock-Jones, D.S. et al. (1996) VEGF mRNA levels in placentae from pregnancies complicated by pre-eclampsia. Br. J. Obstet. Gynaecol., 103, 1191-1196.
15. Coull, J.M. and Pappin, D.J.C. (1990) A rapid fluorescent staining procedure for proteins electroblotted onto PVDF membranes. J. Protein Chem., 9, 259-260.
16. Davis-Smyth, T., Chen, H., Park, J. et al. (1996) The second immunoglobulin-like domain of the VEGF tyrosine kinase receptor Flt-1 determines ligand binding and may initiate a signal transduction cascade. EMBO J., 15, 4919-4927.
17. de Vries, C., Escobedo, J.A., Ueno, H. et al. (1992) The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor Science, 255, 989-991.
18. Englard, S. and Seifter, S. (1990). Precipitation techniques. Meth. Enzymol., 182, 285-306.
19. Ferrara, N. (1996) Vascular endothehal growth factor. Eur. J. Cancer, 32A, 2413-2422.
20. Ferrara, N. and Davis-Smyth, T. (1997) The biology of vascular endothelial growth factor. Endocr. Rev., 18, 4-25.
21. Ferrari, G. and Scagliotti, G.V. (1996) Serum and urinary vascular endothelial growth factor levels in non-small cell lung cancer patients. Eur. J. Cancer, 32A, 2368-2369.
22. Ferrara, N., Carver-Moore, K., Chen, H. et al. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature, 380, 439-442.
23. 121 to one of the three vascular endothelial growth factor receptors of vascular endothelial cells. J. Biol. Chem., 271, 5519-5523.
24. Greb, R R., Heikinheimo, O., Williams, R.F. et al. (1997) Vascular endothelial growth factor in primate endometrium is regulated by oestrogen-receptor and progesterone-receptor ligands in vivo. Hum. Reprod., 12, 1280-1292.
25. Grimmond, S., Lagercrantz, J., Drinkwater, C. et al. (1996) Cloning and characterization of a novel human gene related to vascular endothelial growth factor Genome Res., 6, 124-131.
26. Hanatani, M., Tanaka, Y., Kondo, S. et al. (1995) Sensitive chemiluminescence enzyme immunoassay for vascular endothelial growth factor vascular permeability factor in human serum. Biosci., Biotechnol. Biochem., 59, 1958-1959.
27. Hauser, S. and Weich, H.A. (1993) A heparin-binding form of placenta growth factor (P1GF-2) is expressed in human umbilical vein endothelial cells and in placenta. Growth Factors, 9, 259-268.
28. Houck, K.A., Ferrara, N., Winer, J. et al. (1991) The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol., 5, 1806-1814.
29. Houck, K.A., Leung, D.W., Rowland, A.M. et al. (1992) Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem., 267, 26031-26037.
30. Hunt, D.F., Yates, J.R., Shabanowitz, J. et al. (1986) Protein sequencing by tandem mass spectrometry. Proc. Natl. Acad. Sci. USA. 84, 6233-6237.
31. Jackson, M.R., Carney, E.W., Lye, S.J. et al. (1994) Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation. Placenta, 15, 341-353.
32. Jakeman, L.B., Armanini, M., Phillips, H.S. et al. (1993) Developmental expression of binding sites and messenger ribonucleic acid for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis. Endocrinology, 133, 848-859.
33. Joukov, V., Pajusola, K., Kaipainen, A. et al (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.
34. Katoh, O., Tauchi, H., Kawaishi, K. et al. (1995) Expression of the vascular endothelial growth factor (VEGF) receptor gene, KDR, in hematopoietic cells and inhibitory effect of VEGF on apoptotic cell death caused by ionizing radiation. Cancer Res., 55, 5687-5692.
35. Kendall, R.L., Wang, G. and Thomas, K.A. (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.
36. Kendall, R.L. and Thomas, K.A. (1993) Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc. Natl Acad. Sci. USA, 90, 10705-10709.
37. Keyt, B.A., Nguyen, H.V., Berleau, L.T. et al. (1996) Identification of vascular endothelial growth factor determinants for binding KDR and FLT-1 receptors - Generation of receptor-selective VEGF variants by site-directed mutagenesis. J. Biol. Chem., 271, 5638-5646.
38. Kondo, S., Asano, M., Matsuo, K. et al. (1994) Vascular endothelial growth factor/vascular permeability factor is detectable in the sera of tumor-bearing mice and cancer patients. Biochim. Biophys. Acta, 1221, 211-214.
39. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
40. Lyall, F., Greer, I.A., Boswell, F. et al. (1997) Suppression of serum vascular endothelial growth factor immunoreactivity in normal pregnancy and in preeclampsia. Br. J. Obstet. Gynaecol, 104, 223-228.
41. Maglione, D., Guerriero, V, Viglietto, G. et al. (1991) Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc. Natl. Acad. Sci. USA, 88, 9267-9271
42. Maglione, D., Guerriero, V., Viglietto, G. et al. (1993) Two alternative mRNAs coding for the angiogenic factor, placenta growth factor (PIGF), are transcribed from a single gene of chromosome 14. Oncogene, 8, 925-931.
43. Matthews, W., Jordan, C.T., Gavin, M. et al. (1991) A receptor tyrosine kinase cDNA isolated from a population of enriched primitive hematopoietic cells and exhibiting close genetic linkage to c-kit. Proc. Natl. Acad. Sci. USA, 88, 9026-9030.
44. Millauer, B., Wizigmann-Voos, S., Schnurch, H. et al. (1993) High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell, 72, 835-846.
45. Mock, K.K., Sutton, C.W. and Cottrell, J.S. (1992) Sample immobilisation protocols for matrix-assisted laser desorption mass spectrometry. Rapid Commun. Mass Spectrom., 6, 233-238.
46. Olofsson, B., Pajusola, K., Kaipainen, A. et al. (1996) Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc. Natl. Acad. Sci USA, 93, 2576-2581.
47. Paavonen, K., Horelli-Kuitunen, N., Chilov, D. et al. (1996) Novel human vascular endothelial growth factor genes VEGF-B and VEGF-C localize to chromosomes 11q13 and 4q34, respectively. Circulation, 93, 1079-1082.
48. Pappin, D.J.C., Hojrup, P. and Bleasby, A.J. (1993) Rapid identification of proteins by peptide-mass fingerprinting. Curr. Biol., 3, 327-332.
49. Pappin, D.J.C., Rahman, D., Hansen, H.F. et al. (1996) Chemistry, mass spectrometry and peptide-mass databases: evolution of methods for the rapid identification and mapping of cellular proteins. In Burlingame, A.L. and Carr, S.A. (eds), Mass Spectrometry in the Biological Sciences. Humana Press, Totowa, NJ, USA, pp. 135-150.
50. Park, J.E., Chen, H.H., Winer, J. et al (1994) 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., 269, 25646-25654.
51. Peters, K.G., de Vries, C. and Williams, L.T. (1993) 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. 90, 8915-8919.
52. Quinn, T P., Peters, K.G., de Vries, C. et al. (1993) Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc. Natl. Acad. Sci. USA, 90, 7533-7537.
53. Roberts, W.G. and Palade, G.E. (1997) Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res., 57, 765-772.
54. Sawano, A., Takahashi, T., Yamaguchi, S. et al. (1996) Flt-1 but not KDR/Flk-1 tyrosine kinase is a receptor for placenta growth factor, which is related to vascular endothelial growth factor. Cell Growth Diff., 7, 213-221.
55. Senger, D.R., Galli, S.J., Dvorak, A.M. et al. (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science, 219, 983-985.
56. Sharkey, A M., Charnock-Jones, D.S., Boocock, C.A. et al. (1993) Expression of mRNA for vascular endothelial growth factor in human placenta. J. Reprod. Fertil., 99, 609-615.
57. Sharkey, A.M., Cooper, J.C., Balmforth, J.R. et al. (1996) Maternal plasma levels of vascular endothelial growth factor in normotensive pregnancies and in pregnancies complicated by pre-eclampsia. Eur. J. Clin. Invest., 26, 1182-1185.
58. Sherman, N.E., Yates, N.A., Shabanowitz, J. et al. (1995) Proceedings of the 43rd ASMS Conference on Mass Spectrometry and Allied Topics, Atlanta, Georgia, USA, pp. 626.
59. Shibuya, M., Yamaguchi, S., Yamane, A. et al. (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.
60. Shifren, J.L., Doldi, N., Ferrara, N. et al. (1994) In the human fetus, vascular endothelial growth factor is expressed in epithelial cells and myocytes, but not vascular endothelium: Implications for mode of action. J. Clin. Endocrinol. Metab., 79, 316-322.
61. Shiraishi, S., Nakagawa, K., Kinukawa, N. et al. (1996) Immunohistochemical localization of vascular endothelial growth factor in the human placenta. Placenta, 17, 111-121.
62. Smith, S.K. (1996) Vascular endothelial growth factor and the endometrium. Hum. Reprod., 11 (Suppl. 2), 56-61.
63. 2-macroglobulin and the binding is inhibited by heparin. J. Biol. Chem., 268, 7685-7691.
64. 165 via its exon 7-encoded domain. J. Biol. Chem., 271, 5761-5767.
65. Sutton, C.W., Pemberton, K.S., Cottrell, J.S. et al. (1995) Identification of myocardial proteins from two-dimensional gels by peptide-mass fingerprinting. Electrophoresis, 16, 308-316.
66. Takano, S., Yoshii, Y., Kondo, S. et al. (1996) Concentration of vascular endothelial growth factor in the serum and tumor tissue of brain tumor patients. Cancer Res., 56, 2185-2190.
67. Terman, B.I., Carrion, M.E., Kovacs, E. et al. (1991) Identification of a new endothelial cell growth factor receptor tyrosine kinase. Oncogene, 6, 1677-1683.
68. Thomas, K.A. (1996) Vascular endothelial growth factor, a potent and selective angiogenic agent. J. Biol. Chem., 271, 603-606.
69. Tischer, E., Mitchell, R., Hartman, T. et al. (1991) The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem., 266, 11947-11954.
70. Vaisman, N., Gospodarowicz, D. and Neufeld, G. (1990) Characterization of the receptors for vascular endothelial growth factor. J. Biol. Chem., 265, 19461-19466.
71. Vuckovic, M., Ponting, J., Terman, B.I. et al. (1996) Expression of the vascular endothelial growth factor receptor, KDR, in human placenta. J. Anat., 188, 361-366.
72. Watanabe, O., Arimura, K., Kitajima, I et al. (1996) Greatly raised vascular endothelial growth factor (VEGF) in POEMS syndrome. Lancet, 347, 702.
73. Wilm, M. and Mann, M. (1996) Analytical properties of the nanoelectrospray ion source. Anal. Chem., 68, 1-8.
74. Yamada, Y., Nezu, J.O., Shimane, M. et al. (1997) Molecular cloning of a novel vascular endothelial growth factor, VEGF-D. Genomics, 42, 483-488.