Involvement of Flt-1 (VEGF receptor-1) in cancer and preeclampsia

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 87, Issue 4, 2011, Pages 167-178

  Shibuya, Masabumi ^a,b  

^a JOBU UNIVERSITY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Hypertension; Natural VEGF inhibitor; sFlt 1; Tyrosine kinase

Indexed keywords

VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL; ARTICLE; CHEMISTRY; DISEASE COURSE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; NEOPLASM; PHYLOGENY; PREECLAMPSIA; PREGNANCY;

AMINO ACID SEQUENCE; ANIMALS; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASMS; NEOVASCULARIZATION, PHYSIOLOGIC; PHYLOGENY; PRE-ECLAMPSIA; PREGNANCY; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 82255171009     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.87.167     Document Type: Article

References (59)

1. Risau, W. (1997) Mechanism of angiogenesis. Nature 386, 671-674.
2. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364.
3. Ferrara, N. (2004) Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 25, 581-611.
4. Shibuya, M. and Claesson-Welsh, L. (2006) Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp. Cell Res. 312, 549-560.
5. Takahashi, H. and Shibuya, M. (2005) The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clin. Sci. 109, 227-241.
6. Shibuya, M., Yamaguchi, S., Yamane, A., Ikeda, T., Tojo, A., Matsushime, H. and Sato, M. (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.
7. de Vries, C., Escobedo, J.A., Ueno, H., Houck, K., Ferrara, N. and Williams, L.T. (1992) The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255, 989-991.
8. Terman, B.I., Dougher-Vermazen, M., Carrion, M.E., Dimitrov, D., Armellino, D.C., Gospodarowicz, D. and Bohlen, P. (1992) Identification of the KDR tyrosine kinase as a receptor for Vascular Endothelial Growth Factor. Biochem. Biophys. Res. Commun. 187, 1579-1586.
9. Matthews, W., Jordan, C.T., Gavin, M., Jenkins, N.A., Copeland, N.G. and Lemischka, I.R. (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.
10. Alitalo, K. and Carmeliet, P. (2002) Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 1, 219-227.
11. 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.
12. Hornig, C., Barleon, B., Ahmad, S., Vuorela, P., Ahmed, A. and Weich, H.A. (2000) Release and complex formation of soluble VEGFR-1 from endothelial cells and biological fluids. Lab. Invest. 80, 443-454.
13. Helske, S., Vuorela, P., Carpen, O., Hornig, C., Weich, H. and Halmesmaki, E. (2001) Expression of vascular endothelial growth factor receptors 1, 2 and 3 in placentas from normal and complicated pregnancies. Mol. Hum. Reprod. 7, 205-210.
14. Maynard, S.E., Min, J.Y., Merchan, J., Lim, K.H., Li, J., Mondal, S., Libermann, T.A., Morgan, J.P., Sellke, F.W., Stillman, I.E., Epstein, F.H., Sukhatme, V.P. and Karumanchi, S.A. (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 111, 649-658.
15. Koga, K., Osuga, Y., Yoshino, O., Hirota, Y., Ruimeng, X., Hirata, T., Takeda, S., Yano, T., Tsutsumi, O. and Taketani, Y. (2003) Elevated serum soluble vascular endothelial growth factor receptor 1 (sVEGFR-1) levels in women with preeclampsia. J. Clin. Endocrinol. Metab. 88, 2348-2351.
16. Levine, R.J., Maynard, S.E., Qian, C., Lim, K.H., England, L.J., Yu, K.F., Schisterman, E.F., Thadhani, R., Sachs, B.P., Epstein, F.H., Sibai, B.M., Sukhatme, V.P. and Karumanchi, S.A. (2004) Circulating angiogenic factors and the risk of preeclampsia. N. Engl. J. Med. 350, 672-683.
17. Hurwitz, H., Fehrenbacher, L., Novotny, W., Cartwright, T., Hainsworth, J., Heim, W., Berlin, J., Baron, A., Griffing, S., Holmgren, E., Ferrara, N., Fyfe, G., Rogers, B., Ross, R. and Kabbinavar, F. (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 350, 2335-2342.
18. Cohen, M.H., Gootenberg, J., Keegan, P. and Pazdur, R. (2007) FDA drug approval summary: bevacizumab (Avastin) plus Carboplatin and Paclitaxel as first-line treatment of advanced/ metastatic recurrent nonsquamous non-small cell lung cancer. Oncologist 12, 713-718.
19. Barleon, B., Sozzani, S., Zhou, D., Weich, H.A., Martovani, A. and Marme, D. (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.
20. Clauss, M., Weich, H., Breier, G., Knies, U., Röckl, W., Waltenberger, J. and Risau, W. (1996) The vascular endothelial growth factor receptor Flt-1 mediates biological activities. J. Biol. Chem. 271, 17629-17634.
21. Dvorak, H.F. (2002) Vascular permeability factor/ vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 20, 4368-4380.
22. Carmellet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kleckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C., Declercq, C., Pawlling, J., Moons, L., Collen, D., Risau, W. and Nagy, A. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439.
23. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K.S., Powell-Braxton, L., Hillan, K.J. and Moore, M.W. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442.
24. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.-F., Breitman, M.L., Wu, X.-F., Breitman, M.L. and Schuh, A.C. (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-66.
25. Fong, G.H., Rossant, J., Gertsentein, M. and Breitman, M.L. (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376, 66-70.
26. Dumont, D.J., Jussila, L., Taipale, J., Lymboussaki, A., Mustonen, T., Pajusola, K., Breitman, M. and Alitalo, K. (1998) Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282, 946-949.
27. Saito, M., Hamasaki, M. and Shibuya, M. (2003) Induction of tube formation by angiopoietin-1 in endothelial cell/fibroblast co-culture is dependent on endogenous VEGF. Cancer Sci. 94, 782-790.
28. Sawano, A., Takahashi, T., Yamaguchi, S., Aonuma, T. and Shibuya, M. (1996) Flt-1 but not KDR/ Flk-1 tyrosine kinase is a receptor for Placenta Growth Factor (PlGF), which is related to Vascular Endothelial Growth Factor (VEGF). Cell Growth Differ. 7, 213-221.
29. Heldin, C.H. and Westermark, B. (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79, 1283-1316.
30. Takahashi, T., Ueno, H. and Shibuya, M. (1999) VEGF activates protein kinase C-dependent, but Ras-independent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene 18, 2221-2230.
31. Takahashi, T., Yamaguchi, S., Chida, K. and Shibuya, M. (2001) A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-Adependent activation of PLC-. and DNA synthesis in vascular endothelial cells. EMBO J. 20, 2768-2778.
32. Sakurai, Y., Ohgimoto, K., Kataoka, Y., Yoshida, N. and Shibuya, M. (2005) Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc. Natl. Acad. Sci. USA 102, 1076-1081.
33. Xiong, Y., Huo, Y., Chen, C., Zeng, H., Lu, X., Wei, C., Ruan, C., Zhang, X., Hu, Z., Shibuya, M. and Luo, J. (2009) Vascular endothelial growth factor (VEGF) receptor-2 tyrosine 1175 signaling controls VEGF-induced von Willebrand factor release from endothelial cells via phospholipase C-.-1 and protein kinase A-dependent pathways. J. Biol. Chem. 284, 23217-23224.
34. Matsumoto, T., Bohman, S., Dixelius, J., Berge, T., Dimberg, A., Magnusson, P., Wang, L., Wikner, C., Qi, J.H., Wernstedt, C., Wu, J., Bruheim, S., Mugishima, H., Mukhopadhyay, D., Spurkland, A. and Claesson-Welsh, L. (2005) VEGF receptor-2 Y951 signaling and a role for the adapter molecule TSAd in tumor angiogenesis. EMBO J. 24, 2342-2353.
35. He, Y., Smith, S.K., Day, K.A., Clark, D.E., Licence, D.R. and Charnock-Jones, D.S. (1999) Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol. Endocrinol. 13, 537-545.
36. Kondo, K., Hiratsuka, S., Subbalakshmi, E., Matsushime, H. and Shibuya, M. (1998) Genomic organization of the flt-1 gene encoding for Vascular Endothelial Growth Factor (VEGF) Receptor-1 suggests an intimate evolutionary relationship between the 7-Ig and the 5-Ig tyrosine kinase receptors. Gene 208, 297-305.
37. Yamaguchi, S., Iwata, K. and Shibuya, M. (2002) Soluble Flt-1 (soluble VEGFR-1), a potent natural anti-angiogenic molecule in mammals, is phylogenetically conserved in avians. Biochem. Biophys. Res. Commun. 291, 554-559.
38. Hiratsuka, S., Minowa, O., Kuno, J., Noda, T. and Shibuya, M. (1998) Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. USA 95, 9349-9354.
39. Kerber, M., Reiss, Y., Wickersheim, A., Jugold, M., Kiessling, F., Heil, M., Tchaikovski, V., Waltenberger, J., Shibuya, M., Plate, K.H. and Machein, M.R. (2008) Flt-1 signaling in macrophages promotes glioma growth in vivo. Cancer Res. 68, 7342-7351.
40. Muramatsu, M., Yamamoto, S., Osawa, T. and Shibuya, M. (2010) VEGFR-1 signaling promotes mobilization of macrophage-lineage cells from bone marrow and stimulates solid tumor growth. Cancer Res. 70, 8211-8221.
41. Hiratsuka, S., Nakamura, K., Iwai, S., Murakami, M., Itoh, T., Kijima, H., Shipley, J.M., Senior, R.M. and Shibuya, M. (2002) MMP9 induction by Vascular Endothelial Growth Factor Receptor-1 is involved in lung specific metastasis. Cancer Cell 2, 289-300.
42. Kaplan, R.N., Riba, R.D., Zacharoulis, S., Bramley, A.H., Vincent, L., Costa, C., MacDonald, D.D., Jin, D.K., Shido, K., Kerns, S.A., Zhu, Z., Hicklin, D., Wu, Y., Port, J.L., Altorki, N., Port, E.R., Ruggero, D., Shmelkov, S.V., Jensen, K.K., Rafii, S. and Lyden, D. (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438, 820-827.
43. Murakami, M., Iwai, S., Hiratsuka, S., Yamauchi, M., Nakamura, K., Iwakura, Y. and Shibuya, M. (2006) Signaling of vascular endothelial growth factor receptor-1 tyrosine kinase promotes rheumatoid arthritis through activation of monocyte/ macrophages. Blood 108, 1849-1856.
44. Kami, J., Muranaka, K., Yanagi, Y., Obata, R., Tamaki, Y. and Shibuya, M. (2008) Inhibition of choroidal neovascularization by blocking vascular endothelial growth factor receptor tyrosine kinase. Jpn. J. Ophthalmol. 52, 91-98.
45. Niida, S., Kondo, T., Hiratsuka, S., Hayashi, S.-I., Amizuka, N., Noda, T., Ikeda, K. and Shibuya, M. (2005) Vascular endothelial growth factor receptor-1 signaling is essential for osteoclast development and bone-marrow formation in CSF-1-deficient mice. Proc. Natl. Acad. Sci. USA 102, 14016-14021.
46. Young, B.C., Levine, R.J. and Karumanchi, S.A. (2010) Pathogenesis of preeclampsia. Annu. Rev. Pathol. 5, 173-192.
47. Foidart, J.M., Schaaps, J.P., Chantraine, F., Munaut, C. and Lorquet, S. (2009) Dysregulation of anti-angiogenic agents (sFlt-1, PLGF, and sEndoglin) in preeclampsia-a step forward but not the definitive answer. J. Reprod. Immunol. 82, 106-111.
48. Gilbert, J.S., Babcock, S.A. and Granger, J.P. (2007) Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 50, 1142-1147.
49. Barleon, B., Hauser, S., Schollmann, C., Weindel, K., Marme, D., Yayon, A. and Weich, H.A. (1994) Differential expression of the two VEGF receptors flt and KDR in placenta and vascular endothelial cells. J. Cell. Biochem. 54, 56-66.
50. Clark, D.E., Smith, S.K., He, Y., Day, K.A., Licence, D.R., Corps, A.N., Lammoglia, R. and Charnock-Jones, D.S. (1998) A Vascular Endothelial Growth Factor antagonist is produced by the human placenta and released into the maternal circulation. Biol. Reprod. 59, 1540-1548.
51. Tanaka, K., Yamaguchi, S., Sawano, A. and Shibuya, M. (1997) Characterization of the extracellular domain in the Vascular Endothelial Growth Factor Receptor-1 (Flt-1 tyrosine kinase). Jpn. J. Cancer Res. 88, 867-876.
52. Nomura, M., Yamagishi, S., Harada, S., Hayashi, Y., Yamashima, T., Yamashita, J. and Yamamoto, H. (1995) Possible participation of autocrine and paracrine vascular endothelial growth factors in hypoxia-induced proliferation of endothelial cells and pericytes. J. Biol. Chem. 270, 28316-28324.
53. Schwartz, J.D., Rowinsky, E.K., Youssoufian, H., Pytowski, B. and Wu, Y. (2010) Vascular endothelial growth factor receptor-1 in human cancer: concise review and rationale for development of IMC-18F1 (Human antibody targeting vascular endothelial growth factor receptor-1). Cancer 116, 1027-1032.
54. Tsuchida, R., Das, B., Yeger, H., Koren, G., Shibuya, M., Thorner, P.S., Baruchel, S. and Malkin, D. (2008) Cisplatin treatment increases survival and expansion of a highly tumorigenic side-population fraction by upregulating VEGF/Flt1 autocrine signaling. Oncogene 27, 3923-3934.
55. Wakiya, K., Begue, A., Stehelin, D. and Shibuya, M. (1996) A cyclic AMP response element and an ETS motif are involved in the transcriptional regulation of flt-1 tyrosine kinase (VEGF receptor 1) gene. J. Biol. Chem. 271, 30823-30828.
56. Barleon, B., Siemeister, G., Martiny-Baron, G., Weindel, K., Herzog, C. and Marmé, D. (1997) Vascular endothelial growth factor up-regulates its receptor fms-like tyrosine kinase 1 (FLT-1) and a soluble variant of FLT-1 in human vascular endothelial cells. Cancer Res. 57, 5421-5425.
57. Nagamatsu, T., Fujii, T., Kusumi, M., Zou, L., Yamashita, T., Osuga, Y., Momoeda, M., Kozuma, S. and Taketani, Y. (2004) Cytotrophoblasts upregulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 145, 4838-4845.
58. Mezquita, J., Mezquita, B., Pau, M. and Mezquita, C. (2003) Down-regulation of flt-1 gene expression by the proteasome inhibitor MG262. J. Cell. Biochem. 89, 1138-1147.
59. Kumasawa, K., Ikawa, M., Kidoya, H., Hasuwa, H., Saito-Fujita, T., Morioka, Y., Takakura, N., Kimura, T. and Okabe, M. (2011) Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc. Natl. Acad. Sci. USA 108, 1451-1455.