Lipid phosphate phosphatase 3 stabilization of β-catenin induces endothelial cell migration and formation of branching point structures

Molecular and Cellular Biology

Volumn 30, Issue 7, 2010, Pages 1593-1606

  Humtsoe, Joseph O ^a   Liu, Mingyao ^b   Malik, Asrar B ^c   Wary, Kishore K ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CATENIN; FIBRONECTIN; LIPID PHOSPHATE PHOSPHATASE 3; LYMPHOID ENHANCER FACTOR 1; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P120; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; CELL ADHESION; CELL DENSITY; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; BETA CATENIN; CATENINS; CELL ADHESION; CELL LINE; CELL MOVEMENT; ENDOTHELIAL CELLS; FIBRONECTINS; HUMANS; ISOENZYMES; LYMPHOID ENHANCER-BINDING FACTOR 1; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHATIDATE PHOSPHATASE; PTEN PHOSPHOHYDROLASE; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 77949363045     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00038-09     Document Type: Article

References (44)

1. Adams, J. C., and F. M. Watt. 1993. Regulation of development and differentiation by the extracellular matrix. Development 117:1183-1198.
2. Bazzoni, G., and E. Dejana. 2004. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84:869-901.
3. Bohnsack, B. L., and K. K. Hirschi. 2004. Red light, green light: signals that control endothelial cell proliferation during embryonic vascular development. Cell Cycle 3:1506-1511.
4. Brindley, D. N., and C. Pilquil. 2009. Lipid phosphate phosphatases and signaling. J. Lipid Res. 50(Suppl.):S225-S230.
5. Burnett, C., and K. Howard. 2003. Fly and mammalian lipid phosphate phosphatase isoforms differ in activity both in vitro and in vivo. EMBO Rep. 4:793-799.
6. Carmeliet, P. 2003. Angiogenesis in health and disease. Nat. Med. 9:653-660.
7. Daniel, J. M., and A. B. Reynolds. 1999. The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol. Cell. Biol. 19:3614-3623.
8. Davis, G. E., and D. R. Senger. 2005. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ. Res. 97:1093-1107.
9. Davis, M. A., R. C. Ireton, and A. B. Reynolds. 2003. A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163:525-534.
10. De Langhe, S. P., F. G. Sala, P. M. Del Moral, T. J. Fairbanks, K. M. Yamada, D. Warburton, R. C. Burns, and S. Bellusci. 2005. Dickkopf-1 (DKK1) reveals that fibronectin is a major target of Wnt signaling in branching morphogenesis of the mouse embryonic lung. Dev. Biol. 277:316-331.
11. Escalante-Alcalde, D., L. Hernandez, H. Le Stunff, R. Maeda, H. S. Lee, Jr-Gang-Cheng, V. A. Sciorra, I. Daar, S. Spiegel, A. J. Morris, and C. L. Stewart. 2003. The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development 130:4623-4637.
12. Folkman, J., and P. A. D'Amore. 1996. Blood vessel formation: what is its molecular basis? Cell 87:1153-1155.
13. Goodwin, A. M., and P. A. D'Amore. 2002. Wnt signaling in the vasculature. Angiogenesis 5:1-9.
14. Gory-Faure, S., M. H. Prandini, H. Pointu, V. Roullot, I. Pignot-Paintrand, M. Vernet, and P. Huber. 1999. Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126:2093- 2102.
15. Grosheva, I., M. Shtutman, M. Elbaum, and A. D. Bershadsky. 2001. p120catenin affects cell motility via modulation of activity of Rho-family GTPases: a link between cell-cell contact formation and regulation of cell locomotion. J. Cell Sci. 114:695-707.
16. Hoppler, S., and C. L. Kavanagh. 2007. Wnt signalling: variety at the core. J. Cell Sci. 120:385-393.
17. Horowitz, A., and M. Simons. 2008. Branching morphogenesis. Circ. Res. 103:784-795.
18. Humtsoe, J. O., R. A. Bowling, Jr., S. Feng, and K. K. Wary. 2005. Murine lipid phosphate phosphohydrolase-3 acts as a cell-associated integrin ligand. Biochem. Biophys. Res. Commun. 335:906-919.
19. Humtsoe, J. O., S. Feng, G. D. Thakker, J. Yang, J. Hong, and K. K. Wary. 2003. Regulation of cell-cell interactions by phosphatidic acid phosphatase 2b/VCIP. EMBO J. 22:1539-1554.
20. Hynes, R. O. 2007. Cell-matrix adhesion in vascular development. J. Thromb. Haemost. 5:32-40.
21. Ichii, T., and M. Takeichi. 2007. p120-catenin regulates microtubule dynamics and cell migration in a cadherin-independent manner. Genes Cells 12:827-839.
22. Jia, Y. J., M. Kai, I. Wada, F. Sakane, and H. Kanoh. 2003. Differential localization of lipid phosphate phosphatases 1 and 3 to cell surface subdomains in polarized MDCK cells. FEBS Lett. 552:240-246.
23. 2-inducible hic53 clone yielded the cDNA encoding phosphatidic acid phosphatase. J. Biol. Chem. 271:18931-18938.
24. Kamei, M., M. Kamei, W. B. Saunders, K. J. Bayless, L. Dye, G. E. Davis, and B. M. Weinstein. 2006. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442:453-456.
25. Korswagen, H. C., and H. C. Clevers. 1999. Activation and repression of wingless/Wnt target genes by the TCF/LEF-1 family of transcription factors. Cold Spring Harb. Symp. Quant. Biol. 64:141-147.
26. Loscertales, M., A. J. Mikels, J. K. Hu, P. K. Donahoe, and D. J. Roberts. 2008. Chick pulmonary Wnt5a directs airway and vascular tubulogenesis. Development 135:1365-1376.
27. Marsden, M., and D. W. DeSimone. 2001. Regulation of cell polarity, radial intercalation and epiboly in Xenopus: novel roles for integrin and fibronectin. Development 128:3635-3647.
28. Noren, N. K., P. Liu, K. Burridge, and B. Kreft. 2000. p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150:567-580.
29. Olsson, A. K., A. Dimberg, J. Kreuger, and L. Claesson-Welsh. 2006. VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7:359-371.
30. Park, J. I., H. Ji, S. Jun, D. Gu, H. Hikasa, L. Li, S. Y. Sokol, and P. D. McCrea. 2006. Frodo links Dishevelled to the p120-catenin/Kaiso pathway: distinct catenin subfamilies promote Wnt signals. Dev. Cell 11:683-695.
31. Parmalee, N. L., and J. Kitajewski. 2008. Wnt signaling in angiogenesis. Curr. Drug Targets 9:558-564.
32. Prokhortchouk, A., B. Hendrich, H. Jørgensen, A. Ruzov, M. Wilm, G. Georgiev, A. Bird, and E. Prokhortchouk. 2001. The p120catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev. 15:1613-1618.
33. Risau, W. 1997. Mechanisms of angiogenesis. Nature 386:671-674.
34. Ruoslahti, E. 1992. Control of cell motility and tumour invasion by extracellular matrix interactions. Br. J. Cancer 66:239-242.
35. Sciorra, V. A., and A. J. Morris. 2002. Roles for lipid phosphate phosphatases in regulation of cellular signaling. Biochim. Biophys. Acta 1582:45-51.
36. Sharma, M., W. W. Chuang, and Z. Sun. 2002. Phosphatidylinositol 3-kinase/Akt stimulates androgen pathway through GSK3beta inhibition and nuclear beta-catenin accumulation. J. Biol. Chem. 277:30935-30941.
37. Uegaki, K., Y. Kanamori, J. Kigawa, W. Kawaguchi, R. Kaneko, J. Naniwa, M. Takahashi, M. Shimada, T. Oishi, H. Itamochi, and N. Terakawa. 2006. PTEN is involved in the signal transduction pathway of contact inhibition in endometrial cells. Cell Tissue Res. 323:523-528.
38. Vestweber, D. 2008. VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28:223-232.
39. Waggoner, D. W., J. Xu, I. Singh, R. Jasinska, Q. X. Zhang, and D. N. Brindley. 1999. Structural organization of mammalian lipid phosphate phosphatases: implications for signal transduction. Biochim. Biophys. Acta 439:299-316.
40. Wallez, Y., and P. Huber. 2008. Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim. Biophys. Acta 1778:794-809.
41. Wary, K. K., G. D. Thakker, J. O. Humtsoe, and J. Yang. 2003. Analysis of VEGF-responsive genes involved in the activation of endothelial cells. Mol. Cancer 2:25.
42. Wary, K. K., and J. O. Humtsoe. 2005. Anti-lipid phosphate phosphohydrolase-3 (LPP3) antibody inhibits bFGF- and VEGF-induced capillary morphogenesis of endothelial cells. Cell Commun. Signal. 3:9.
43. Wildenberg, G. A., M. R. Dohn, R. H. Carnahan, M. A. Davis, N. A. Lobdell, J. Settleman, and A. B. Reynolds. 2006. p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127:1027-1039.
44. Zerlin, M., M. A. Julius, and J. Kitajewski. 2008. Wnt/Frizzled signaling in angiogenesis. Angiogenesis 11:63-69.