Basal Flt1 tyrosine kinase activity is a positive regulator of endothelial survival and vascularization during zebrafish embryogenesis

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 2, 2015, Pages 373-384

  Li, Shang ^a   Zhou, Xue Lin ^b   Dang, Yuan Ye ^a   Kwan, Yiu Wa ^b   Chan, Shun Wan ^c   Leung, George Pak Heng ^d   Lee, Simon Ming Yuen ^a   Hoi, Maggie Pui Man ^a  

^a University of Macau   (Macao)

^b and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

^c HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Calycosin; Endothelial cell; Flt1; Molecular docking; VEGF receptor inhibitor; Zebrafish

Indexed keywords

FLT1 TYROSINE KINASE; KDR TYROSINE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; 7,3'-DIHYDROXY-4'-METHOXYISOFLAVONE; ANDROSTANE DERIVATIVE; FLT1 PROTEIN, ZEBRAFISH; ISOFLAVONE DERIVATIVE; PROTEIN KINASE B; PROTEIN KINASE INHIBITOR; WORTMANNIN; ZEBRAFISH PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; IN VITRO STUDY; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; VASCULARIZATION; ZEBRA FISH; ANGIOGENESIS; ANIMAL; ANIMAL EMBRYO; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

DANIO RERIO;

ANDROSTADIENES; ANIMALS; CELL SURVIVAL; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; ISOFLAVONES; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84912534207     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.10.023     Document Type: Article

References (38)

1. H. Habeck, J. Odenthal, B. Walderich, H. Maischein, and S. Schulte-Merker Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis Curr. Biol. 12 2002 1405 1412
2. G.H. Fong, J. Rossant, M. Gertsenstein, and M.L. Breitman Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium Nature 376 1995 66 70
3. S. Koch, S. Tugues, X. Li, L. Gualandi, and L. Claesson-Welsh Signal transduction by vascular endothelial growth factor receptors Biochem. J. 437 2011 169 183
4. F. Shalaby, J. Rossant, T.P. Yamaguchi, M. Gertsenstein, X.F. Wu, M.L. Breitman, and A.C. Schuh Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice Nature 376 1995 62 66
5. P. Carmeliet, N. Mackman, L. Moons, T. Luther, P. Gressens, I. Van Vlaenderen, H. Demunck, M. Kasper, G. Breier, P. Evrard, M. Muller, W. Risau, T. Edgington, and D. Collen Role of tissue factor in embryonic blood vessel development Nature 383 1996 73 75
6. A. Shinkai, M. Ito, H. Anazawa, S. Yamaguchi, K. Shitara, and M. Shibuya Mapping of the sites involved in ligand association and dissociation at the extracellular domain of the kinase insert domain-containing receptor for vascular endothelial growth factor J. Biol. Chem. 273 1998 31283 31288
7. M. Shibuya Structure and dual function of vascular endothelial growth factor receptor-1 (Flt-1) Int. J. Biochem. Cell Biol. 33 2001 409 420
8. S. Hiratsuka, O. Minowa, J. Kuno, T. Noda, and M. Shibuya Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice Proc. Natl. Acad. Sci. U. S. A. 95 1998 9349 9354
9. N.C. Kappas, G. Zeng, J.C. Chappell, J.B. Kearney, S. Hazarika, K.G. Kallianos, C. Patterson, B.H. Annex, and V.L. Bautch The VEGF receptor Flt-1 spatially modulates Flk-1 signaling and blood vessel branching J. Cell Biol. 181 2008 847 858
10. N. Bahary, K. Goishi, C. Stuckenholz, G. Weber, J. Leblanc, C.A. Schafer, S.S. Berman, M. Klagsbrun, and L.I. Zon Duplicate VegfA genes and orthologues of the KDR receptor tyrosine kinase family mediate vascular development in the zebrafish Blood 110 2007 3627 3636
11. J. Chan, P.E. Bayliss, J.M. Wood, and T.M. Roberts Dissection of angiogenic signaling in zebrafish using a chemical genetic approach Cancer Cell 1 2002 257 267
12. J. Cai, S. Ahmad, W.G. Jiang, J. Huang, C.D. Kontos, M. Boulton, and A. Ahmed Activation of vascular endothelial growth factor receptor-1 sustains angiogenesis and Bcl-2 expression via the phosphatidylinositol 3-kinase pathway in endothelial cells Diabetes 52 2003 2959 2968
13. F. Wang, M. Yamauchi, M. Muramatsu, T. Osawa, R. Tsuchida, and M. Shibuya RACK1 regulates VEGF/Flt1-mediated cell migration via activation of a PI3K/Akt pathway J. Biol. Chem. 286 2011 9097 9106
14. W.D. Zhao, W. Liu, W.G. Fang, K.S. Kim, and Y.H. Chen Vascular endothelial growth factor receptor 1 contributes to Escherichia coli K1 invasion of human brain microvascular endothelial cells through the phosphatidylinositol 3-kinase/Akt signaling pathway Infect. Immun. 78 2010 4809 4816
15. N. Ito, C. Wernstedt, U. Engstrom, and L. Claesson-Welsh Identification of vascular endothelial growth factor receptor-1 tyrosine phosphorylation sites and binding of SH2 domain-containing molecules J. Biol. Chem. 273 1998 23410 23418
16. Y. Yu, J.D. Hulmes, M.T. Herley, R.G. Whitney, J.W. Crabb, and J.D. Sato Direct identification of a major autophosphorylation site on vascular endothelial growth factor receptor Flt-1 that mediates phosphatidylinositol 3′-kinase binding Biochem. J. 358 2001 465 472
17. S.A. Cunningham, M.N. Waxham, P.M. Arrate, and T.A. Brock Interaction of the Flt-1 tyrosine kinase receptor with the p85 subunit of phosphatidylinositol 3-kinase. Mapping of a novel site involved in binding J. Biol. Chem. 270 1995 20254 20257
18. S. Li, S. Lou, B.U. Lei, T.F. Chan, Y.W. Kwan, S.W. Chan, G.P. Leung, S.K. Tsui, and S.M. Lee Transcriptional profiling of angiogenesis activities of calycosin in zebrafish Mol. Biosyst. 7 2011 3112 3121
19. J.Y. Tang, S. Li, Z.H. Li, Z.J. Zhang, G. Hu, L.C. Cheang, D. Alex, M.P. Hoi, Y.W. Kwan, S.W. Chan, G.P. Leung, and S.M. Lee Calycosin promotes angiogenesis involving estrogen receptor and mitogen-activated protein kinase (MAPK) signaling pathway in zebrafish and HUVEC PLoS One 5 2010 e11822
20. M. Westerfield The zebrafish book A Guide for the Laboratory Use of Zebrafish (Danio rerio) 3rd Edition 1995 University of Oregon Press Eugene, OR 385
21. O. Trott, and A.J. Olson AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2010 455 461
22. X. Zhou, Y. Wang, T. Hu, P.M. Or, J. Wong, Y.W. Kwan, D.C. Wan, P.M. Hoi, P.B. Lai, and J.H. Yeung Enzyme kinetic and molecular docking studies for the inhibitions of miltirone on major human cytochrome P450 isozymes Phytomedicine 20 2013 367 374
23. J. Krueger, D. Liu, K. Scholz, A. Zimmer, Y. Shi, C. Klein, A. Siekmann, S. Schulte-Merker, M. Cudmore, A. Ahmed, and F. le Noble Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafish embryo Development 138 2011 2111 2120
24. J.M. Wood, G. Bold, E. Buchdunger, R. Cozens, S. Ferrari, J. Frei, F. Hofmann, J. Mestan, H. Mett, T. O'Reilly, E. Persohn, J. Rosel, C. Schnell, D. Stover, A. Theuer, H. Towbin, F. Wenger, K. Woods-Cook, A. Menrad, G. Siemeister, M. Schirner, K.H. Thierauch, M.R. Schneider, J. Drevs, G. Martiny-Baron, F. Totzke, and D. Marme PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration Cancer Res. 60 2000 2178 2189
25. L. Sun, N. Tran, F. Tang, H. App, P. Hirth, G. McMahon, and C. Tang Synthesis and biological evaluations of 3-substituted indolin-2-ones: a novel class of tyrosine kinase inhibitors that exhibit selectivity toward particular receptor tyrosine kinases J. Med. Chem. 41 1998 2588 2603
26. L. Sun, N. Tran, C.X. Liang, F. Tang, A. Rice, R. Schreck, K. Waltz, L.K. Shawver, G. McMahon, and C. Tang Design, synthesis, and evaluations of substituted 3-[(3-or 4-carboxyethylpyrrol-2-yl)methylidenyl]indolin-2-ones as inhibitors of VEGF, FGF, and PDGF receptor tyrosine kinases J. Med. Chem. 42 1999 5120 5130
27. G. Aparicio-Gallego, M. Blanco, A. Figueroa, R. Garcia-Campelo, M. Valladares-Ayerbes, E. Grande-Pulido, and L. Anton-Aparicio New insights into molecular mechanisms of Sunitinib-associated side effects Mol. Cancer Ther. 10 2011 2215 2223
28. L. Sun, C. Liang, S. Shirazian, Y. Zhou, T. Miller, J. Cui, J.Y. Fukuda, J.Y. Chu, A. Nematalla, X.Y. Wang, H. Chen, A. Sistla, T.C. Luu, F. Tang, J. Wei, and C. Tang Discovery of 5-[5-fluoro-2-oxo-1,2-dihydroindol-(3Z)-ylidenemethyl]-2,4-dimethyl-1H-pyrrole-3-carboxylic acid (2-diethylaminoethyl)amide, a novel tyrosine kinase inhibitor targeting vascular endothelial and platelet-derived growth factor receptor tyrosine kinase J. Med. Chem. 46 2003 1116 1119
29. L. Sun, N. Tran, C.X. Liang, S. Hubbard, F. Tang, K. Lipson, R. Schreck, Y. Zhou, G. McMahon, and C. Tang Identification of substituted 3-[(4,5,6,7-tetrahydro-1H-indol-2-yl)methylene]-1,3-dihydroindol-2-ones as growth factor receptor inhibitors for VEGF-R2 (Flk-1/KDR), FGF-R1, and PDGF-R beta tyrosine kinases J. Med. Chem. 43 2000 2655 2663
30. A.P. Kornev, N.M. Haste, S.S. Taylor, and L.F. Eyck Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism Proc. Natl. Acad. Sci. U. S. A. 103 2006 17783 17788
31. R. Roskoski Jr. VEGF receptor protein-tyrosine kinases: structure and regulation Biochem. Biophys. Res. Commun. 375 2008 287 291
32. S. Hiratsuka, K. Nakao, K. Nakamura, M. Katsuki, Y. Maru, and M. Shibuya Membrane fixation of vascular endothelial growth factor receptor 1 ligand-binding domain is important for vasculogenesis and angiogenesis in mice Mol. Cell. Biol. 25 2005 346 354
33. N.K. Singh, D.E. Hansen, V. Kundumani-Sridharan, and G.N. Rao Both Kdr and Flt1 play a vital role in hypoxia-induced Src-PLD1-PKC gamma-cPLA(2) activation and retinal neovascularization Blood 121 2013 1911 1923
34. L. Zanetta, S.G. Marcus, J. Vasile, M. Dobryansky, H. Cohen, K. Eng, P. Shamamian, and P. Mignatti Expression of von Willebrand factor, an endothelial cell marker, is up-regulated by angiogenesis factors: a potential method for objective assessment of tumor angiogenesis Int. J. Cancer J. Int. Cancer 85 2000 281 288
35. E. Tischer, R. Mitchell, T. Hartman, M. Silva, D. Gospodarowicz, J.C. Fiddes, and J.A. Abraham The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing J. Biol. Chem. 266 1991 11947 11954
36. M. Inoue, H. Itoh, M. Ueda, T. Naruko, A. Kojima, R. Komatsu, K. Doi, Y. Ogawa, N. Tamura, K. Takaya, T. Igaki, J. Yamashita, T.H. Chun, K. Masatsugu, A.E. Becker, and K. Nakao Vascular endothelial growth factor (VEGF) expression in human coronary atherosclerotic lesions: possible pathophysiological significance of VEGF in progression of atherosclerosis Circulation 98 1998 2108 2116
37. I.K. Lam, D. Alex, Y.H. Wang, P. Liu, A.L. Liu, G.H. Du, and S.M. Lee In vitro and in vivo structure and activity relationship analysis of polymethoxylated flavonoids: identifying sinensetin as a novel antiangiogenesis agent Mol. Nutr. Food Res. 56 2012 945 956
38. K.H. Lam, D. Alex, I.K. Lam, S.K. Tsui, Z.F. Yang, and S.M. Lee Nobiletin, a polymethoxylated flavonoid from citrus, shows anti-angiogenic activity in a zebrafish in vivo model and HUVEC in vitro model J. Cell. Biochem. 112 2011 3313 3321