Tyrosine phosphorylation of DEP-1/CD148 as a mechanism controlling Src kinase activation, endothelial cell permeability, invasion, and capillary formation

Blood

Volumn 120, Issue 13, 2012, Pages 2745-2756

  Spring, Kathleen ^a   Chabot, Catherine ^a   Langlois, Simon ^a   Lapointe, Line ^a   Trinh, Nguyen Thu Ngan ^a   Caron, Christine ^a   Hebda, Jagoda K ^b   Gavard, Julie ^b   Elchebly, Mounib ^c,d   Royal, Isabelle ^a,d  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b INSTITUT COCHIN   (France)

^c UNIVERSITY OF MONTREAL   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN DEP 1; PROTEIN SH2; PROTEIN TYROSINE KINASE; RECEPTOR; TYROSINE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; CAPILLARY; CELL INVASION; CELL MEMBRANE PERMEABILITY; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 84866880821     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-398040     Document Type: Article

References (50)

1. Hermiston ML, Zikherman J, Zhu JW. CD45, CD148, and Lyp/Pep: critical phosphatases regulating Src family kinase signaling networks in immune cells. Immunol Rev. 2009;228(1):288-311.
2. Ostman A, Yang Q, Tonks N. Expression of DEP-1, a receptor-like protein-tyrosine-phosphatase, is enhanced with increasing cell density. Proc Natl Acad Sci U S A. 1994;91(21):9680-9684. (Pubitemid 24311871)
3. Borges LG, Seifert RA, Grant FJ, et al. Cloning and characterization of rat density-enhanced phosphatase-1, a protein tyrosine phosphatase expressed by vascular cells. Circ Res. 1996; 79(3):570-580. (Pubitemid 26276917)
4. Keane M, Lowrey G, Ettenberg S, Dayton M, Lipkowitz S. The protein tyrosine phosphatase DEP-1 is induced during differentiation and inhibits growth of breast cancer cells. Cancer Res. 1996;56(18):4236-4243. (Pubitemid 26305022)
5. Zhang L, Martelli M, Battaglia C, et al. Thyroid cell transformation inhibits the expression of a novel rat protein tyrosine phosphatase. Exp Cell Res. 1997;235(1):62-70. (Pubitemid 27381682)
6. Trapasso F, Yendamuri S, Dumon KR, et al. Restoration of receptor-type protein tyrosine phosphatase eta function inhibits human pancreatic carcinoma cell growth in vitro and in vivo. Carcinogenesis. 2004;25(11):2107-2114. (Pubitemid 39534847)
7. Trapasso F, Iuliano R, Boccia A, et al. Rat protein tyrosine phosphatase eta suppresses the neoplastic phenotype of retrovirally transformed thyroid cells through the stabilization of p27Kip1. Mol Cell Biol. 2000;20(24):9236- 9246. (Pubitemid 32246110)
8. Balavenkatraman KK, Jandt E, Friedrich K, et al. DEP-1 protein tyrosine phosphatase inhibits proliferation and migration of colon carcinoma cells and is upregulated by protective nutrients. Oncogene. 2006;25(47):6319-6324. (Pubitemid 44564747)
9. Ruivenkamp CAL, van Wezel T, Zanon C, et al. Ptprj is a candidate for the mouse colon-cancer susceptibility locus Scc1 and is frequently deleted in human cancers. Nat Genet. 2002;31(3):295-300.
10. Kovalenko M, Denner K, Sandström J, et al. Site-selective dephosphorylation of the platelet-derived growth factor beta-receptor by the receptor-like protein-tyrosine phosphatase DEP-1. J Biol Chem. 2000;275(21):16219-16226. (Pubitemid 30366934)
11. Palka HL, Park M, Tonks NK. Hepatocyte growth factor receptor tyrosine kinase Met is a substrate of the receptor protein-tyrosine phosphatase DEP-1. J Biol Chem. 2003;278(8):5728-5735. (Pubitemid 36800817)
12. Le Pera I, Iuliano R, Florio T, et al. The rat tyrosine phosphatase eta increases cell adhesion by activating c-Src through dephosphorylation of its inhibitory phosphotyrosine residue. Oncogene. 2005;24(19):3187-3195. (Pubitemid 40695087)
13. Lampugnani MG, Zanetti A, Corada M, et al. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J Cell Biol. 2003;161(4):793-804. (Pubitemid 36648762)
14. Holsinger LJ, Ward K, Duffield B, Zachwieja J, Jallal B. The transmembrane receptor protein tyrosine phosphatase DEP1 interacts with p120ctn. Oncogene. 2002;21(46):7067-7076. (Pubitemid 35252981)
15. Chabot C, Spring K, Gratton JP, Elchebly M, Royal I. New role for the protein tyrosine phosphatase DEP-1 in Akt activation and endothelial cell survival. Mol Cell Biol. 2009;29(1):241-253.
16. Sacco F, Tinti M, Palma A, et al. Tumor suppressor density-enhanced phosphatase-1 (DEP-1) inhibits the RAS pathway by direct dephosphorylation of ERK1/2 kinases. J Biol Chem. 2009; 284(33):22048-22058.
17. Tsuboi N, Utsunomiya T, Roberts RL, et al. The tyrosine phosphatase CD148 interacts with the p85 regulatory subunit of phosphoinositide 3-kinase. Biochem J. 2008;413(1):193-200. (Pubitemid 351946875)
18. Zhu JW, Brdicka T, Katsumoto TR, Lin J, Weiss A. Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity. 2008;28(2): 183-196.
19. Sallee JL, Burridge K. Density-enhanced phosphatase 1 regulates phosphorylation of tight junction proteins and enhances barrier function of epithelial cells. J Biol Chem. 2009;284(22):14997-15006.
20. Koch S, Tugues S, Li X, Gualandi L, Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Biochem J. 2011; 437(2):169-183.
21. Carmeliet P, Lampugnani M-G, Moons L, et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell. 1999;98(2):147-157. (Pubitemid 29344903)
22. Takahashi T, Takahashi K, Mernaugh R, et al. Endothelial localization of receptor tyrosine phosphatase, ECRTP/DEP-1, in developing and mature renal vasculature. J Am Soc Nephrol. 1999; 10(10):2135-2145. (Pubitemid 29453491)
23. Takahashi T, Takahashi K, St John PL, et al. A mutant receptor tyrosine phosphatase, CD148, causes defects in vascular development. Mol Cell Biol. 2003;23(5):1817-1831. (Pubitemid 36246061)
24. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell. 1999;4(6): 915-924. (Pubitemid 30054898)
25. Dejana E, Orsenigo F, Lampugnani MG. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci. 2008; 121(13):2115-2122.
26. van Hinsbergh VWM, Koolwijk P. Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc Res. 2008;78(2): 203-212. (Pubitemid 351556093)
27. Eilken HM, Adams RH. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol. 2010;22(5):617-625.
28. Bjorge JD, Jakymiw A, Fujita DJ. Selected glimpses into the activation and function of Src kinase. Oncogene. 2000;19(49):5620-5635.
29. Senis YA, Tomlinson MG, Ellison S, et al. The tyrosine phosphatase CD148 is an essential positive regulator of platelet activation and thrombosis. Blood. 2009;113(20):4942-4954.
30. Zheng XM, Resnick RJ, Shalloway D. A phosphotyrosine displacement mechanism for activation of Src by PTP alpha. EMBO J. 2000;19:964-978. (Pubitemid 30119822)
31. Berman-Golan D, Elson A. Neu-mediated phosphorylation of protein tyrosine phosphatase epsilon is critical for activation of Src in mammary tumor cells. Oncogene. 2007;26(49):7028-7037. (Pubitemid 350014610)
32. Vacaru AM, den Hertog J. Serine dephosphorylation of receptor protein tyrosine phosphatase α in mitosis induces Src binding and activation. Mol Cell Biol. 2010;30(12):2850-2861.
33. Kilarski WW, Jura N, Gerwins P. Inactivation of Src family kinases inhibits angiogenesis in vivo: implications for a mechanism involving organization of the actin cytoskeleton. Exp Cell Res. 2003; 291(1):70-82. (Pubitemid 37338684)
34. Granot-Attas S, Elson A. Protein tyrosine phosphatase epsilon activates Yes and Fyn in Neuinduced mammary tumor cells. Exp Cell Res. 2004;294(1):236-243. (Pubitemid 38229794)
35. Flint AJ, Tiganis T, Barford D, Tonks NK. Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci U S A. 1997;94(5): 1680-1685.
36. den Hertog J, Ostman A, Bohmer FD. Protein tyrosine phosphatases: regulatory mechanisms. FEBS J. 2008;275(5):831-847. (Pubitemid 351230200)
37. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci. 1998;111:1853-1865. (Pubitemid 28370530)
38. Potter MD, Barbero S, Cheresh DA. Tyrosine phosphorylation of VE-cadherin prevents binding of p120 and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem. 2005;280: 31906-31912. (Pubitemid 41291941)
39. Gavard J, Gutkind JS. VEGF controls endothelialcell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol. 2006;8(11):1223-1234. (Pubitemid 44660587)
40. Monaghan-Benson E, Burridge K. The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem. 2009;284(38): 25602-25611.
41. Kirkbride KC, Sung BH, Sinha S, Weaver AM. Cortactin: a multifunctional regulator of cellular invasiveness. Cell Adh Migr. 2011;5(2):187-198.
42. Kaluza D, Kroll J, Gesierich S, et al. Class IIb HDAC6 regulates endothelial cell migration and angiogenesis by deacetylation of cortactin. EMBO J. 2011;30(20):4142-4156.
43. Lee J-F, Ozaki H, Zhan X, Wang E, Hla T, Lee M-J. Sphingosine-1-phosphate signaling regulates lamellipodia localization of cortactin complexes in endothelial cells. Histochem Cell Biol. 2006;126(3):297-304.
44. Huang C, Liu J, Haudenschild CC, Zhan X. The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J Biol Chem. 1998;273(40):25770-25776. (Pubitemid 28475803)
45. Ayala I, Baldassarre M, Giacchetti G, et al. Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation. J Cell Sci. 2008;121(3):369-378. (Pubitemid 351356708)
46. Ha CH, Bennett AM, Jin Z-G. A novel role of vascular endothelial cadherin in modulating c-Src activation and downstream signaling of vascular endothelial growth factor. J Biol Chem. 2008; 283(11):7261-7270.
47. Lampugnani MG, Dejana E. Adherens junctions in endothelial cells regulate vessel maintenance and angiogenesis. Thromb Res. 2007;120(Suppl 2):S1-S6. (Pubitemid 350101767)
48. Lin M-T, Yen M-L, Lin C-Y, Kuo M-L. Inhibition of vascular endothelial growth factor-induced angiogenesis by resveratrol through interruption of Srcdependent vascular endothelial cadherin tyrosine phosphorylation. Mol Pharmacol. 2003;64(5): 1029-1036. (Pubitemid 37310735)
49. Ammer AG, Weed SA. Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskel. 2008;65(9):687-707.
50. McNeill L, Salmond RJ, Cooper JC, et al. The differential regulation of Lck kinase phosphorylation sites by CD45 is critical for T cell receptor signaling responses. Immunity. 2007;27(3):425-437. (Pubitemid 47418669)