S1PR1 Tyr143 phosphorylation downregulates endothelial cell surface S1PR1 expression and responsiveness

Journal of Cell Science

Volumn 128, Issue 5, 2015, Pages 878-887

  Chavez, Alejandra ^a   Schmidt, Tracy Thennes ^a   Yazbeck, Pascal ^a   Rajput, Charu ^a   Desai, Bhushan ^a   Sukriti, Sukriti ^a   Giantsos Adams, Kristina ^a   Knezevic, Nebojsa ^a   Malik, Asrar B ^a   Mehta, Dolly ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Adherens junctions; Endothelial barrier function; Endothelium; Serine phosphorylation; Sphingosine 1 phosphate receptor 1; Tyrosine phosphorylation

Indexed keywords

SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 1; UNCLASSIFIED DRUG; LYSOPHOSPHOLIPID; S1PR1 PROTEIN, HUMAN; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; TYROSINE;

ANIMAL CELL; ANTIGEN ANTIBODY COMPLEX; ARTICLE; BIOTINYLATION; CELL SURFACE; CHO CELL LINE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNALIZATION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; AMINO ACID SUBSTITUTION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DOWN REGULATION; GENETICS; METABOLISM; MISSENSE MUTATION; PHOSPHORYLATION; PHYSIOLOGY;

AMINO ACID SUBSTITUTION; CELLS, CULTURED; DOWN-REGULATION; ENDOTHELIAL CELLS; HUMANS; LYSOPHOSPHOLIPIDS; MUTATION, MISSENSE; PHOSPHORYLATION; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE; TYROSINE;

EID: 84924873766     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.154476     Document Type: Article

References (52)

1. Argraves, K. M., Wilkerson, B. A. and Argraves, W. S. (2010). Sphingosine-1- phosphate signaling in vasculogenesis and angiogenesis. World J. Biol. Chem 1, 291-297.
2. Belvitch, P. and Dudek, S. M. (2012). Role of FAK in S1P-regulated endothelial permeability. Microvasc. Res. 83, 22-30.
3. Bergelin, N., Löf, C., Balthasar, S., Kalhori, V. and Törnquist, K. (2010). S1P1 and VEGFR-2 form a signaling complex with extracellularly regulated kinase 1/2 and protein kinase C-alpha regulating ML-1 thyroid carcinoma cell migration. Endocrinology 151, 2994-3005.
4. Chen, R. H. and Derynck, R. (1994). Homomeric interactions between type II transforming growth factor-beta receptors. J. Biol. Chem. 269, 22868- 22874.
5. Ferguson, S. S., Downey, W. E., 3rd, Colapietro, A. M., Barak, L. S., Ménard, L. and Caron, M. G. (1996). Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 271, 363-366.
6. Garcia, J. G., Liu, F., Verin, A. D., Birukova, A., Dechert, M. A., Gerthoffer, W. T., Bamberg, J. R. and English, D. (2001). Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J. Clin. Invest. 108, 689-701.
7. Garris, C. S., Wu, L., Acharya, S., Arac, A., Blaho, V. A., Huang, Y., Moon, B. S., Axtell, R. C., Ho, P. P., Steinberg, G. K. et al. (2013). Defective sphingosine 1- phosphate receptor 1 (S1P1) phosphorylation exacerbates TH17-mediated autoimmune neuroinflammation. Nat. Immunol. 14, 1166-1172.
8. Graeler, M., Shankar, G. and Goetzl, E. J. (2002). Cutting edge: suppression of T cell chemotaxis by sphingosine 1-phosphate. J. Immunol. 169, 4084-4087.
9. Gräler, M. H. and Goetzl, E. J. (2004). The immunosuppressant FTY720 downregulates sphingosine 1-phosphate G-protein-coupled receptors. FASEB J. 18, 551-553.
10. Hanke, J. H., Gardner, J. P., Dow, R. L., Changelian, P. S., Brissette, W. H., Weringer, E. J., Pollok, B. A. and Connelly, P. A. (1996). Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J. Biol. Chem. 271, 695-701.
11. Hanson, M. A., Roth, C. B., Jo, E., Griffith, M. T., Scott, F. L., Reinhart, G., Desale, H., Clemons, B., Cahalan, S. M., Schuerer, S. C. et al. (2012). Crystal structure of a lipid G protein-coupled receptor. Science 335, 851-855.
12. Hla, T. (2004). Physiological and pathological actions of sphingosine 1-phosphate. Semin. Cell Dev. Biol. 15, 513-520.
13. Holinstat, M., Knezevic, N., Broman, M., Samarel, A. M., Malik, A. B. and Mehta, D. (2006). Suppression of RhoA activity by focal adhesion kinaseinduced activation of p190RhoGAP: role in regulation of endothelial permeability. J. Biol. Chem. 281, 2296-2305.
14. Huang, Y. L., Lin, H. S., Chen, S. U. and Lee, H. (2009). Tyrosine sulphation of sphingosine 1-phosphate 1 (S1P1) is required for S1P-mediated cell migration in primary cultures of human umbilical vein endothelial cells. J. Biochem. 146, 815-820.
15. Klessner, J. L., Desai, B. V., Amargo, E. V., Getsios, S. and Green, K. J. (2009). EGFR and ADAMs cooperate to regulate shedding and endocytic trafficking of the desmosomal cadherin desmoglein 2. Mol. Biol. Cell 20, 328-337.
16. Knezevic, N., Tauseef, M., Thennes, T. and Mehta, D. (2009). The G protein betagamma subunit mediates reannealing of adherens junctions to reverse endothelial permeability increase by thrombin. J. Exp. Med. 206, 2761-2777.
17. Kohno, T., Wada, A. and Igarashi, Y. (2002). N-glycans of sphingosine 1- phosphate receptor Edg-1 regulate ligand-induced receptor internalization. FASEB J. 16, 983-992.
18. Lee, M. J., Van Brocklyn, J. R., Thangada, S., Liu, C. H., Hand, A. R., Menzeleev, R., Spiegel, S. and Hla, T. (1998). Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279, 1552-1555.
19. Lee, O. H., Lee, D. J., Kim, Y. M., Kim, Y. S., Kwon, H. J., Kim, K. W. and Kwon, Y. G. (2000). Sphingosine 1-phosphate stimulates tyrosine phosphorylation of focal adhesion kinase and chemotactic motility of endothelial cells via the G(i) protein-linked phospholipase C pathway. Biochem. Biophys. Res. Commun. 268, 47-53.
20. Lee, J. F., Gordon, S., Estrada, R., Wang, L., Siow, D. L., Wattenberg, B. W., Lominadze, D. and Lee, M. J. (2009). Balance of S1P1 and S1P2 signaling regulates peripheral microvascular permeability in rat cremaster muscle vasculature. Am. J. Physiol. 296, H33-H42.
21. Liu, C. H., Thangada, S., Lee, M. J., Van Brocklyn, J. R., Spiegel, S. and Hla, T. (1999). Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG-1. Mol. Biol. Cell 10, 1179-1190.
22. Luttrell, L. M. and Lefkowitz, R. J. (2002). The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. J. Cell Sci. 115, 455-465.
23. Matloubian, M., Lo, C. G., Cinamon, G., Lesneski, M. J., Xu, Y., Brinkmann, V., Allende, M. L., Proia, R. L. and Cyster, J. G. (2004). Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427, 355-360.
24. McVerry, B. J. and Garcia, J. G. (2004). Endothelial cell barrier regulation by sphingosine 1-phosphate. J. Cell. Biochem. 92, 1075-1085.
25. McVerry, B. J., Peng, X., Hassoun, P. M., Sammani, S., Simon, B. A. and Garcia, J. G. (2004). Sphingosine 1-phosphate reduces vascular leak in murine and canine models of acute lung injury. Am. J. Respir. Crit. Care Med. 170, 987- 993.
26. Mehta, D., Rahman, A. and Malik, A. B. (2001). Protein kinase C-alpha signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function. J. Biol. Chem. 276, 22614- 22620.
27. Mehta, D., Konstantoulaki, M., Ahmmed, G. U. and Malik, A. B. (2005). Sphingosine 1-phosphate-induced mobilization of intracellular Ca2+ mediates rac activation and adherens junction assembly in endothelial cells. J. Biol. Chem. 280, 17320-17328.
28. Nakamura, Y., Patrushev, N., Inomata, H., Mehta, D., Urao, N., Kim, H. W., Razvi, M., Kini, V., Mahadev, K., Goldstein, B. J. et al. (2008). Role of protein tyrosine phosphatase 1B in vascular endothelial growth factor signaling and cellcell adhesions in endothelial cells. Circ. Res. 102, 1182-1191.
29. Nottebaum, A. F., Cagna, G., Winderlich, M., Gamp, A. C., Linnepe, R., Polaschegg, C., Filippova, K., Lyck, R., Engelhardt, B., Kamenyeva, O. et al. (2008). VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF. J. Exp. Med. 205, 2929-2945.
30. O'Sullivan, C. and Dev, K. K. (2013). The structure and function of the S1P1 receptor. Trends Pharmacol. Sci. 34, 401-412.
31. Okamoto, H., Takuwa, N., Yokomizo, T., Sugimoto, N., Sakurada, S., Shigematsu, H. and Takuwa, Y. (2000). Inhibitory regulation of Rac activation, membrane ruffling, and cell migration by the G protein-coupled sphingosine-1- phosphate receptor EDG5 but not EDG1 or EDG3. Mol. Cell. Biol. 20, 9247-9261.
32. Oo, M. L., Thangada, S., Wu, M. T., Liu, C. H., Macdonald, T. L., Lynch, K. R., Lin, C. Y. and Hla, T. (2007). Immunosuppressive and anti-angiogenic sphingosine 1-phosphate receptor-1 agonists induce ubiquitinylation and proteasomal degradation of the receptor. J. Biol. Chem. 282, 9082-9089.
33. Oo, M. L., Chang, S. H., Thangada, S., Wu, M. T., Rezaul, K., Blaho, V., Hwang, S. I., Han, D. K. and Hla, T. (2011). Engagement of S1P1-degradative mechanisms leads to vascular leak in mice. J. Clin. Invest. 121, 2290-2300.
34. Paik, J. H., Chae, Ss, Lee, M. J.Thangada, S. and Hla, T. (2001). Sphingosine 1- phosphate-induced endothelial cell migration requires the expression of EDG-1 and EDG-3 receptors and Rho-dependent activation of alpha vbeta3- and beta1-containing integrins. J. Biol. Chem. 276, 11830-11837.
35. Peng, X., Hassoun, P. M., Sammani, S., McVerry, B. J., Burne, M. J., Rabb, H., Pearse, D., Tuder, R. M. and Garcia, J. G. (2004). Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am. J. Respir. Crit. Care Med. 169, 1245-1251.
36. Reiter, E. and Lefkowitz, R. J. (2006). GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol. Metab. 17, 159-165.
37. Ruwisch, L., Schäfer-Korting, M. and Kleuser, B. (2001). An improved highperformance liquid chromatographic method for the determination of sphingosine-1-phosphate in complex biological materials. Naunyn Schmiedebergs Arch. Pharmacol. 363, 358-363.
38. Shikata, Y., Birukov, K. G., Birukova, A. A., Verin, A. and Garcia, J. G. (2003a). Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphateand thrombin-induced focal adhesion remodeling: role of Src and GIT. FASEB J. 17, 2240-2249.
39. Shikata, Y., Birukov, K. G. and Garcia, J. G. (2003b). S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J. Appl. Physiol. 94, 1193-1203.
40. Singh, I., Knezevic, N., Ahmmed, G. U., Kini, V., Malik, A. B. and Mehta, D. (2007). Galphaq-TRPC6-mediated Ca2+ entry induces RhoA activation and resultant endothelial cell shape change in response to thrombin. J. Biol. Chem. 282, 7833-7843.
41. Spiegel, S. and Milstien, S. (2003). Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407.
42. Tauseef, M., Kini, V., Knezevic, N., Brannan, M., Ramchandaran, R., Fyrst, H., Saba, J., Vogel, S. M., Malik, A. B. and Mehta, D. (2008). Activation of sphingosine kinase-1 reverses the increase in lung vascular permeability through sphingosine-1-phosphate receptor signaling in endothelial cells. Circ. Res. 103, 1164-1172.
43. Thangada, S., Khanna, K. M., Blaho, V. A., Oo, M. L., Im, D. S., Guo, C., Lefrancois, L. and Hla, T. (2010). Cell-surface residence of sphingosine 1- phosphate receptor 1 on lymphocytes determines lymphocyte egress kinetics. J. Exp. Med. 207, 1475-1483.
44. Thennes, T. and Mehta, D. (2012). Heterotrimeric G proteins, focal adhesion kinase, and endothelial barrier function. Microvasc. Res. 83, 31-44.
45. Timmerman, I., Hoogenboezem, M., Bennett, A. M., Geerts, D., Hordijk, P. L. and van Buul, J. D. (2012). The tyrosine phosphatase SHP2 regulates recovery of endothelial adherens junctions through control of b-catenin phosphorylation. Mol. Biol. Cell 23, 4212-4225.
46. Ukropec, J. A., Hollinger, M. K., Salva, S. M. and Woolkalis, M. J. (2000). SHP2 association with VE-cadherin complexes in human endothelial cells is regulated by thrombin. J. Biol. Chem. 275, 5983-5986.
47. Wang, L. and Dudek, S. M. (2009). Regulation of vascular permeability by sphingosine 1-phosphate. Microvasc. Res. 77, 39-45.
48. Waters, C. M., Connell, M. C., Pyne, S. and Pyne, N. J. (2005). c-Src is involved in regulating signal transmission from PDGFbeta receptor-GPCR(s) complexes in mammalian cells. Cell. Signal. 17, 263-277.
49. Watterson, K. R., Johnston, E., Chalmers, C., Pronin, A., Cook, S. J., Benovic, J. L. and Palmer, T. M. (2002). Dual regulation of EDG1/S1P(1) receptor phosphorylation and internalization by protein kinase C and G-protein-coupled receptor kinase 2. J. Biol. Chem. 277, 5767-5777.
50. Willinger, T., Ferguson, S. M., Pereira, J. P., De Camilli, P. and Flavell, R. A. (2014). Dynamin 2-dependent endocytosis is required for sustained S1PR1 signaling. J. Exp. Med. 211, 685-700.
51. Zhao, J., Singleton, P. A., Brown, M. E., Dudek, S. M. and Garcia, J. G. (2009). Phosphotyrosine protein dynamics in cell membrane rafts of sphingosine-1- phosphate-stimulated human endothelium: role in barrier enhancement. Cell. Signal. 21, 1945-1960.
52. Zhu, X., Kim, J. L., Newcomb, J. R., Rose, P. E., Stover, D. R., Toledo, L. M., Zhao, H. and Morgenstern, K. A. (1999). Structural analysis of the lymphocytespecific kinase Lck in complex with non-selective and Src family selective kinase inhibitors. Structure 7, 651-661.