Distinct role of PLCβ3 in VEGF-mediated directional migration and vascular sprouting

Journal of Cell Science

Volumn 122, Issue 7, 2009, Pages 1025-1034

  Bhattacharya, Resham ^a   Kwon, Junhye ^a   Li, Xiujuan ^b   Wang, Enfeng ^a   Patra, Sujata ^a   Bida, John Paul ^a   Bajzer, Zeijko ^a   Claesson Welsh, Lena ^b   Mukhopadhyay, Debabrata ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Endothelial signaling; Migration; PLC 3; Proliferation

Indexed keywords

ACTIN; GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOLIPASE C BETA3; PHOSPHOLIPASE C GAMMA1; PROTEIN CDC42; PROTEIN TYROSINE KINASE; SERINE; VASCULOTROPIN RECEPTOR 2; INOSITOL PHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C BETA; PHOSPHOSERINE; PLCB3 PROTEIN, HUMAN; VASCULOTROPIN A;

ARTICLE; CELL CYCLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UMBILICAL VEIN; ANGIOGENESIS; ANIMAL; ANIMAL EMBRYO; CELL MOTION; CYTOLOGY; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; GENE SILENCING; METABOLISM; MOUSE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TRANSPORT;

ACTINS; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INOSITOL PHOSPHATES; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHOLIPASE C BETA; PHOSPHORYLATION; PHOSPHOSERINE; PROTEIN BINDING; PROTEIN TRANSPORT; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 66849115292     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.041913     Document Type: Article

References (51)

1. Berridge, M. J. (1993). Inositol trisphosphate and calcium signalling. Nature 361, 315-25.
2. 2+ and von Willebrand factor release in human endothelial cells. Am. J. Pathol. 138, 213-221.
3. Cascone, I., Audero, E., Giraudo, E., Napione, L., Maniero, F., Philips, M. R., Collard, J. G., Serini, G. and Bussolino, F. (2003). Tie-2-dependent activation of RhoA and Rac1 participates in endothelial cell motility triggered by angiopoietin-1. Blood 102, 2482-2490.
4. Cockcroft, S. and Thomas, G. M. (1992). Inositol-lipid-specific phospholipase C isoenzymes and their differential regulation by receptors. Biochem. J. 288, 1-14.
5. Dvorak, H. F., Dvorak, A. M., Manseau, E. J., Wiberg, L. and Churchill, W. H. (1979). Fibrin gel investment associated with line 1 and line 10 solid tumor growth, angiogenesis, and fibroplasia in guinea pigs: role of cellular immunity, myofibroblasts, microvascular damage, and infarction in line 1 tumor regression. J. Natl. Cancer Inst. 62, 1459-1472.
6. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177.
7. Grohmanova, K., Schlaepfer, D., Hess, D., Gutierrez, P., Beck, M. and Kroschewski, R. (2004). Phosphorylation of IQGAP1 modulates its binding to Cdc42, revealing a new type of rho-GTPase regulator. J. Biol. Chem. 279, 48495-48504.
8. Guidi, A. J., Abu-Jawdeh, G., Berse, B., Jackman, R. W., Tognazzi, K., Dvorak, H. F. and Brown, L. F. (1995). Vascular permeability factor (vascular endothelial growth factor) expression and angiogenesis in cervical neoplasia. J. Natl. Cancer Inst. 87, 1237-1245.
9. Hamlyn, J. M., Blaustein, M. P., Bova, S., DuCharme, D. W., Harris, D. W., Mandel, F., Mathews, W. R. and Ludens, J. H. (1991). Identification and characterization of a ouabain-like compound from human plasma. Proc. Natl. Acad. Sci. USA 88, 6259-6263.
10. Jakobsson, L., Kreuger, J., Holmborn, K., Lundin, L., Eriksson, I., Kjellén, L. and Claesson-Welsh, L. (2006). Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell 10, 625-634.
11. Jakobsson, L., Kreuger, J. and Claesson-Welsh, L. (2007). Building blood vessels-stem cell models in vascular biology. J. Cell Biol. 177, 751-755.
12. Jia, H., Bagherzadeh, A., Bicknell, R., Duchen, M. R., Liu, D. and Zachary, I. (2004). Vascular endothelial growth factor (VEGF)-D and VEGF-A differentially regulate KDR-mediated signaling and biological function in vascular endothelial cells. J. Biol. Chem. 279, 36148-36157.
13. Jones, N. P., Peak, J., Brader, S., Eccles, S. A. and Katan, M. (2005). PLCgamma1 is essential for early events in integrin signalling required for cell motility. J. Cell Sci. 118, 2695-2706.
14. Joseph, E. K., Bogen, O., Alessandri-Haber, N. and Levine, J. D. (2007). PLC-beta 3 signals upstream of PKC epsilon in acute and chronic inflammatory hyperalgesia. Pain 132, 67-73.
15. Kalashnik, L., Bridgeman, C. J., King, A. R., Francis, S. E., Mikhalovsky, S., Wallis, C., Denyer, S. P., Crossman, D. and Faragher, R. G. (2000). A cell kinetic analysis of human umbilical vein endothelial cells. Mech. Ageing Dev. 120, 23-32.
16. Kanda, S., Miyata, Y. and Kanetake, H. (2004). Role of focal adhesion formation in migration and morphogenesis of endothelial cells. Cell. Signal. 16, 1273-1281.
17. Kanda, S., Miyata, Y., Kanetake, H. and Smithgall, T. E. (2006). Fibroblast growth factor-2 induces the activation of Src through Fes, which regulates focal adhesion disassembly. Exp. Cell Res. 312, 3015-3022.
18. Koch, A. E., Harlow, L. A., Haines, G. K., Amento, E. P., Unemori, E. N., Wong, W. L., Pope, R. M. and Ferrara, N. (1994). Vascular endothelial growth factor. A cytokine modulating endothelial function in rheumatoid arthritis. J. Immunol. 152, 4149-4156.
19. Lamalice, L., Houle, F., Jourdan, G. and Huot, J. (2004). Phosphorylation of tyrosine 1214 on VEGFR2 is required for VEGF-induced activation of Cdc42 upstream of SAPK2/p38. Oncogene 23, 434-445.
20. Lamalice, L., Le Boeuf, F. and Huot, J. (2007). Endothelial cell migration during angiogenesis. Circ. Res. 100, 782-794.
21. Leung, T., Chen, H., Stauffer, A. M., Giger, K. E., Sinha, S., Horstick, E. J., Humbert, J. E., Hansen, C. A. and Robishaw, J. D. (2006). Zebrafish G protein gamma2 is required for VEGF signaling during angiogenesis. Blood 108, 160-166.
22. Marin, V., Kaplanski, G., Gres, S., Farnarier, C. and Bongrand, P. (2001). Endothelial cell culture: protocol to obtain and cultivate human umbilical endothelial cells. J. Immunol. Methods 254, 183-190.
23. Matsumoto, T., Bohman, S., Dixelius, J., Berge, T., Dimberg, A., Magnusson, P., Wang, L., Wikner, C., Qi, J. H., Wernstedt, C. et al. (2005). VEGF receptor-2 Y951 signaling and a role for the adapter molecule TSAd in tumor angiogenesis. EMBO J. 24, 2342-2353.
24. Meyer, R. D., Latz, C. and Rahimi, N. (2003). Recruitment and activation of phospholipase Cgamma1 by vascular endothelial growth factor receptor-2 are required for tubulogenesis and differentiation of endothelial cells. J. Biol. Chem. 278, 16347-16355.
25. Moriya, S., Kazlauskas, A., Akimoto, K., Hirai, S., Mizuno, K., Takenawa, T., Fukui, Y., Watanabe, Y., Ozaki, S. and Ohno, S. (1996). Platelet-derived growth factor activates protein kinase C epsilon through redundant and independent signaling pathways involving phospholipase C gamma or phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 93, 151-155.
26. Mukhopadhyay, D. and Zeng, H. (2002). Involvement of G proteins in vascular permeability factor/vascular endothelial growth factor signaling. Cold Spring Harb. Symp. Quant. Biol. 67, 275-283.
27. Nakamura, F., Kato, M., Kameyama, K., Nukada, T., Haga, T., Kato, H., Takenawa, T. and Kikkawa, U. (1995). Characterization of Gq family G proteins GL1 alpha (G14 alpha), GL2 alpha (G11 alpha), and Gq alpha expressed in the baculovirus-insect cell system. J. Biol. Chem. 270, 6246-6253.
28. Noh, D. Y., Shin, S. H. and Rhee, S. G. (1995). Phosphoinositide-specific phospholipase C and mitogenic signaling. Biochim. Biophys. Acta 1242, 99-113.
29. Pankov, R., Endo, Y., Even-Ram, S., Araki, M., Clark, K., Cukierman, E., Matsumoto, K. and Yamada, K. M. (2005). A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170, 793-802.
30. Rhee, S. G. and Choi, K. D. (1992). Regulation of inositol phospholipid-specific phospholipase C isozymes. J. Biol. Chem. 267, 12393-12396.
31. Rhee, S. G. and Bae, Y. S. (1997). Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem. 272, 15045-15048.
32. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674.
33. Senger, D. R., Galli, S. J., Dvorak, A. M., Perruzzi, C. A., Harvey, V. S. and Dvorak, H. F. (1983). Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219, 983-985.
34. Senger, D. R., Ledbetter, S. R., Claffey, K. P., Papadopoulos-Sergiou, A., Peruzzi, C. A. and Detmar, M. (1996). Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the alphavbeta3 integrin, osteopontin, and thrombin. Am. J. Pathol. 149, 293-305.
35. Soker, S., Takashima, S., Miao, H. Q., Neufeld, G. and Klagsbrun, M. (1998). Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92, 735-745.
36. Soker, S., Miao, H. Q., Nomi, M., Takashima, S. and Klagsbrun, M. (2002). VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J. Cell Biochem. 85, 357-368.
37. Sternweis, P. C. and Smrcka, A. V. (1992). Regulation of phospholipase C by G proteins. Trends Biochem. Sci. 17, 502-506.
38. Strassheim, D. and Williams, C. L. (2000). P2Y2 purinergic and M3 muscarinic acetylcholine receptors activate different phospholipase C-beta isoforms that are uniquely susceptible to protein kinase C-dependent phosphorylation and inactivation. J. Biol. Chem. 275, 39767-39772.
39. Strassheim, D., Law, P. Y. and Loh, H. H. (1998). Contribution of phospholipase C-beta3 phosphorylation to the rapid attenuation of opioid-activated phosphoinositide response. Mol. Pharmacol. 53, 1047-1053.
40. Takahashi, T., Yamaguchi, S., Chida, K. and Shibuya, M. (2001). A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J. 20, 2768-2778.
41. 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 cell growth factor. Biochem. Biophys. Res. Commun. 187, 1579-1586.
42. Vaisman, N., Gospodarowicz, D. and Neufeld, G. (1990). Characterization of the receptors for vascular endothelial growth factor. J. Biol. Chem. 265, 19461-19466.
43. van Nieuw Amerongen, G. P., Koolwijk, P., Versteilen, A. and van Hinsbergh, V. W. (2003). Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler. Thromb. Vasc. Biol. 23, 211-217.
44. Walker, M. B., Miller, C. T., Swartz, M. E., Eberhart, J. K. and Kimmel, C. B. (2007). phospholipase C, beta 3 is required for Endothelin1 regulation of pharyngeal arch patterning in zebrafish. Dev. Biol. 304, 194-207.
45. Wang, S., Gebre-Medhin, S., Betsholtz, C., Stalberg, P., Zhou, Y., Larsson, C., Weber, G., Feinstein, R., Oberg, K., Gobl, A. et al. (1998). Targeted disruption of the mouse phospholipase C beta3 gene results in early embryonic lethality. FEBS Lett. 441, 261-265.
46. Xia, C., Bao, Z., Yue, C., Sanborn, B. M. and Liu, M. (2001). Phosphorylation and regulation of G-protein-activated phospholipase C-beta 3 by cGMP-dependent protein kinases. J. Biol. Chem. 276, 19770-19777.
47. Xie, W., Samoriski, G. M., McLaughlin, J. P., Romoser, V. A., Smrcka, A., Hinkle, P. M., Bidlack, J. M., Gross, R. A., Jiang, H. and Wu, D. (1999). Genetic alteration of phospholipase C beta3 expression modulates behavioral and cellular responses to mu opioids. Proc. Natl. Acad. Sci. USA 96, 10385-10390.
48. Zeng, H., Dvorak, H. F. and Mukhopadhyay, D. (2001a). Vascular permeability factor (VPF)/vascular endothelial growth factor (VEGF) peceptor-1 down-modulates VPF/VEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylinositol 3-kinase-dependent pathways. J. Biol. Chem. 276, 26969-26979.
49. Zeng, H., Sanyal, S. and Mukhopadhyay, D. (2001b). Tyrosine residues 951 and 1059 of vascular endothelial growth factor receptor-2 (KDR) are essential for vascular permeability factor/vascular endothelial growth factor-induced endothelium migration and proliferation, respectively. J. Biol. Chem. 276, 32714-32719.
50. Zeng, H., Zhao, D. and Mukhopadhyay, D. (2002). KDR stimulates endothelial cell migration through heterotrimeric G protein Gq/ 11-mediated activation of a small GTPase RhoA. J. Biol. Chem. 277, 46791-46798.
51. Zeng, H., Zhao, D., Yang, S., Datta, K. and Mukhopadhyay, D. (2003). Heterotrimeric G alpha q/G alpha 11 proteins function upstream of vascular endothelial growth factor (VEGF) receptor-2 (KDR) phosphorylation in vascular permeability factor/VEGF signaling. J. Biol. Chem. 278, 20738-20745.