S1P1-selective in vivo-active agonists from high-throughput screening: Off-the-shelf chemical probes of receptor interactions, signaling, and fate

Chemistry and Biology

Volumn 12, Issue 6, 2005, Pages 703-715

  Jo, Euijung ^a   Sanna, M Germana ^a   Gonzalez Cabrera, Pedro J ^a   Thangada, Shobha ^b   Tigyi, Gabor ^c   Osborne, Daniel A ^d   Hla, Timothy ^b   Parrill, Abby L ^d   Rosen, Hugh ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d University of Memphis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKT1 PROTEIN, HUMAN; DRUG DERIVATIVE; LIGAND; LYSOPHOSPHOLIPID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; ONCOPROTEIN; OXADIAZOLE DERIVATIVE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; RAC PROTEIN; SEW2871; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1-PHOSPHATE; THIOPHENE DERIVATIVE;

ANIMAL; ARTICLE; BINDING SITE; CELL LINE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; DRUG POTENTIATION; DRUG SCREENING; ENZYME ACTIVATION; GENETICS; HAMSTER; HUMAN; METABOLISM; MOLECULAR PROBE; MUTATION; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION;

ANIMALS; BINDING SITES; CELL LINE; CELL MEMBRANE; CRICETINAE; DRUG EVALUATION, PRECLINICAL; ENZYME ACTIVATION; HUMANS; LIGANDS; LYSOPHOSPHOLIPIDS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MODELS, MOLECULAR; MOLECULAR PROBES; MUTATION; OXADIAZOLES; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RAC GTP-BINDING PROTEINS; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE; THIOPHENES;

EID: 24944535833     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2005.04.019     Document Type: Article

References (61)

1. Spiegel, S., and Milstien, M. (2003). Sphingosine 1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407.
2. Kluck, M.J., and Hla, T. (2002). Signaling of sphingosine-1-phosphate via the S1P/EDG-family of G-protein-coupled receptors. Biochim. Biophys. Acta 1582, 72-80.
3. Siehler, S., and Manning, D.R. (2002). Pathways of transduction engaged by sphingosine 1-phosphate through G protein-coupled receptors. Biochim. Biophys. Acta 1582, 94-99.
4. Spiegel, S., English, D., and Milstien, S. (2002). Sphingosine 1-phosphate signaling: providing cells with a sense of direction. Trends Cell Biol. 12, 236-242.
5. Spiegel, S., and Milstien, S. (2002). Sphingosine 1-phosphate, a key cell signaling molecule. J. Biol. Chem. 277, 25851-25854. Published online May 13, 2002. 10.1074/jbc.R200007200
6. Payne, S.G., Milstien, S., and Spiegel, S. (2002). Sphingosine-1- phosphate: dual messenger functions. FEBS Lett. 531, 54-57.
7. Pyne, S., and Pyne, N.J. (2002). Sphingosine 1-phosphate signalling and termination at lipid phosphate receptors. Biochim. Biophys. Acta 1582, 121-131.
8. Spiegel, S., and Milstien, S. (2000). Functions of a new family of sphingosine-1-phosphate receptors. Biochim. Biophys. Acta 1484, 107-116.
9. Spiegel, S., and Milstien, S. (2003). Exogenous and intracellularly generated sphingosine 1-phosphate can regulate cellular processes by divergent pathways. Biochem. Soc. Trans. 31, 1216-1219.
10. Sugiyama, A., Yatomi, Y., Ozaki, Y., and Hashimoto, K. (2000). Sphingosine 1-phosphate induces sinus tachycardia and coronary vasoconstriction in the canine heart. Cardiovasc. Res. 46, 119-125.
11. Ohmori, T., Yatomi, Y., Osada, M., Kazama, F., Takafuta, T., Ikeda, H., and Ozaki, Y. (2003). Sphingosine 1-phosphate induces contraction of coronary artery smooth muscle cells via S1P(2). Cardiovasc. Res. 58, 170-177.
12. Karliner, J.S. (2002). Lysophospholipids and the cardiovascular system. Biochim. Biophys. Acta 1582, 216-221.
13. English, D., Brindley, D.N., Spiegel, S., and Garcia, J.G.N. (2002). Lipid mediators of angiogenesis and the signalling pathways they initiate. Biochim. Biophys. Acta 1582, 228-239.
14. Garcia, J.G.N., Liu, F., Verin, A.D., Birukova, A., Dechert, M.A., Gerthoffer, W.T., Bamburg, 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.
15. Rosen, H., Alfonso, C., Surh, C.D., and McHeyzer-Williams, M.G. (2003). Rapid induction of medullary thymocyte phenotypic maturation and egress inhibition by nanomolar sphingosine 1-phosphate receptor agonist. Proc. Natl. Acad. Sci. USA 100, 10907-10912. Published online September 3, 2003. 10.1073/pnas.1832725100
16. Xie, J., Nomura, N., Quackenbush, E., Forrest, M., and Rosen, H. (2003). Sphingosine-1-phosphate receptor agonists impair the efficiency of the local immune response by altering trafficking of naïve and antigen-activated CD4+ T cells. J. Immmunol. 170, 3662-3670.
17. Mandala, S., Hajdu, R., Bergstrom, J., Quackenbush, E., Xie, J., Milligan, J., Thornton, R., Shei, G.-J., Card, D., Keohane, C., et al. (2002). Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296, 346-349.
18. Brinkmann, V., Davis, M.D., Heise, C.E., Albert, R., Cottens, S., Hof, R., Bruns, C., Prieschl, E., Baumruker, T., Hiestand, P., et al. (2002). The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J. Biol. Chem. 277, 21453-21457.
19. Rosen, H., Sanna, M., and Alfonso, C. (2003). Egress: a receptor-regulated step in lymphocyte trafficking. Immunol. Rev. 195, 160-177.
20. Igarashi, J., and Michel, T. (2000). Agonist-modulated targeting of the EDG-1 receptor to plasmalemmal caveolae. eNOS activation by sphingosine 1-phosphate and the role of caveolin-1 in sphingolipid signal transduction. J. Biol. Chem. 275, 32363-32370.
21. Igarashi, J., and Michel, T. (2001). Sphingosine 1-phosphate and isoform-specific activation of phosphoinositide 3-kinase β. J. Biol. Chem. 276, 36281-36288.
22. Dantas, A.P.V., Igarashi, J., and Michel, T. (2003). Sphingosine 1-phosphate and control of vascular tone. Am. J. Physiol. Heart Circ. Physiol. 284, H2045-H2052.
23. Murata, N., Sato, K., Tomura, H., Kon, J., Yanagita, M., Kuwabara, A., Ul, M., and Okajima, F. (2000). Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem. J. 352, 809-815.
24. Sanna, M.G., Liao, J., Jo, E., Alfonso, C., Ahn, M.-Y., Peterson, M.S., Webb, B., Lefebvre, S., Chun, J., Gray, N., et al. (2004). Sphingosine 1-phosphate (S1P) receptor subtypes S1P1 and S1P3, respectively. Regulate Lymphocyte Recirculation and Heart Rate. J. Biol. Chem. 279, 13839-13848.
25. Matloubian, M., Lo, C., Cinamon, G., Lesneski, M., Xu, Y., Brinkmann, V., Allende, M., Proia, R., and Cyster, J. (2004). Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427, 355-360.
26. Allende, M.L., Dreier, J.L., Mandala, S., and Proia, R.L. (2004). Expression of the sphingosine-1-phosphate receptor, S1P1, on T-cells controls thymic emigration. J. Biol. Chem. 279, 15396-15401.
27. Hale, J.J., Lynch, C.L., Neway, W., Mills, S.G., Hajdu, R., Keohane, C.A., Rosenbach, M.J., Milligan, J.A., Shei, G.J., Parent, S.A., et al. (2004). A rational utilization of high-throughput screening affords selective, orally bioavailable 1-benzyl-3-carboxyazetidine sphingosine-1-phosphate-1 receptor agonists. J. Med. Chem. 47, 6662-6665.
28. Liu, C.H., Thangada, S., Lee, M.J., Van Brooklyn, J.R., Spiegel, S., and Hla, T. (1999). Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG1. Mol. Biol. Cell 10, 1179-1190.
29. 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.
30. Graler, M.H., and Goetzl, E.J. (2004). The immunosuppressant FTY720 down-regulates sphingosine 1-phosphate G-protein-coupled receptors. FASEB J. 18, 551-553. Published online January 8, 2004. 10.1096/fj.03-0910fje
31. Parrill, A.L., Wang, D., Bautista, D.L., Van Brocklyn, J.R., Lorincz, Z., Fischer, D.J., Baker, D.L., Liliom, K., Spiegel, S., and Tigyi, G. (2000). Identification of Edg1 receptor residues that recognize sphingosine 1-phosphate. J. Biol. Chem. 275, 39379-39384.
32. Rosen, H., and Liao, J. (2003). Sphingosine 1-phosphate pathway therapeutics: a lipid-receptor paradigm. Curr. Opin. Chem. Biol. 7, 461-468.
33. Kolesnick, R. (2002). The therapeutic potential of modulating the ceramide/sphingomyelin pathway. J. Clin. Invest. 110, 3-8.
34. An, S., Zheng, Y., and Bleu, T. (2000). Sphingosine 1-phosphate-induced cell proliferation, survival, and related signaling events mediated by G-protein-coupled receptors Edg3 and Edg5. J. Biol. Chem. 275, 288-296.
35. Pebay, A., Toutant, M., Premont, J., Calvo, C., Venance, L., Cordier, J., Glowinski, J., and Tence, M. (2001). Sphingosine-1-phosphate induces proliferation of astrocytes: regulation by intracellular signalling cascades. Eur. J. Neurosci. 13, 2067-2076.
36. Wang, L., Cummings, R., Usatyuk, P., Morris, A., Irani, K., and Natarajan, V. (2002). Involvement of phospholipases D1 and D2 in sphingosine 1-phosphate-induced ERK (extracellular-signal-regulated kinase) activation and interleukin-8 secretion in human bronchial epithelial cells. Biochem. J. 367, 751-760.
37. Harada, J., Foley, M., Moskowitz, M.A., and Waeber, C. (2004). Sphingosine-1-phosphate induces proliferation and morphological changes of neural progenitor cells. J. Neurochem. 88, 1026-1039.
38. Kim, D.S., Hwang, E.S., Lee, J.E., Kim, S.Y., Kwon, S.B., and Park, K.C. (2003). Sphingosine-1-phosphate decreases melanin synthesis via sustained ERK activation and subsequent MITF degradation. J. Cell Sci. 116, 1699-1706.
39. Tanimoto, T., Lungu, A.O., and Berk, B.C. (2004). Sphingosine 1-phosphate transactivates the platelet-derived growth factor beta receptor and epidermal growth factor receptor in vascular smooth muscle cells. Circ. Res. 94, 1050-1058. Published on-line March 25, 2004. 10.1161/01.RES.0000126404.41421.BE
40. Davaille, J., Li, L., Mallat, A., and Lotersztajn, S. (2002). Sphingosine 1-phosphate triggers both apoptotic and survival signals for human hepatic myofibroblasts. J. Biol. Chem. 277, 37323-37330. Published online July 22, 2002. 10.1074/jbc.M202798200
41. Lee, M., Thangada, S., Paik, J., Sapkota, G., Ancellin, N., Chae, S., Wu, M., Morales-Ruiz, M., Sessa, W., Alessi, D., et al. (2001). Akt-mediated phosphorylation of the G protein-coupled receptor EDG-1 is required for endothelial cell chemotaxis. Mol. Cell 8, 693-704.
42. Igarashi, J., Erwin, P.A., Dantas, A.P.V., Chen, H., and Michel, T. (2003). VEGF induces S1P1 receptors in endothelial cells: implications for cross-talk between sphingolipid and growth factor receptors. Proc. Natl. Acad. Sci. USA 100, 10664-10669.
43. Tanimoto, T., Jin, Z., and Berck, B. (2002). Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1 -phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (eNOS). J. Biol. Chem. 277, 42997-43001.
44. Sanchez, T., Estrada-Hernandez, T., Paik, J., Wu, M., Venkataraman, K., Brinkmann, V., Claffey, K., and Hla, T. (2003). Phosphorylation and action of the immunomodulator FTY720 inhibits VEGF-induced vascular permeability. J. Biol. Chem. 278, 47281-47290.
45. Connolly, J.O., Simpson, N., Hewlett, L., and Hall, A. (2002). Rac regulates endothelial morphogenesis and capillary assembly. Mol. Biol. Cell 13, 2474-2485.
46. Takuwa, Y. (2002). Subtype-specific differential regulation of Rho family G proteins and cell migration by the Edg family sphingosine-1-phosphate receptors. Biochim. Biophys. Acta 1582, 112-120.
47. Sugimoto, N., Takuwa, N., Okamoto, H., Sakurada, S., and Takuwa, Y. (2003). Inhibitory and stimulatory regulation of Rac and cell motility by the G12/13-Rho and Gi pathways integrated downstream of a single G protein-coupled sphingosine-1-phosphate receptor isoform. Mol. Cell. Biol. 23, 1534-1545.
48. Ryu, Y., Takuwa, N., Sugimoto, N., Sakurada, S., Usui, S., Okamoto, H., Matsui, O., and Takuwa, Y. (2002). Sphingosine-1-phosphate, a platelet-derived lysophospholipid mediator, negatively regulates cellular Rac activity and cell migration in vascular smooth muscle cells. Circ. Res. 90, 325-332.
49. Gonzalez, E., Nagiel, A., Lin, A.J., Golan, D.E., and Michel, T. (2004). Small interfering RNA-mediated down-regulation of caveolin-1 differentially modulates signaling pathways in endothelial cells. J. Biol. Chem. 279, 40659-40669. Published online July 30, 2004.10.1074/jbc.M407051200
50. Doherty, G., Forrest, M., Hajdu, R., Hale, J., Zhen, L., Mandala, S., Mills, S., Rosen, H., and Scolnick, E. July 2003. Selective S1P1/EDG1 receptor agonists. European patent WO03061567.
51. Yeagle, P.L., and Albert, A.D. (2003). A conformational trigger for activation of a G protein by a G protein-coupled receptor. Biochemistry 42, 1365-1368.
52. Wetzker, R., and Bohmer, F.D. (2003). Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat. Rev. Mol. Cell Biol. 4, 651-657.
53. Lopez-Ilasaca, M., Crespo, P., Pellici, P.G., Gutkind, J.S., and Wetzker, R. (1997). Linkage of G protein-coupled receptors to the MAPK signaling pathway through PI 3-kinase gamma. Science 275, 394-397.
54. Forrest, M., Sun, S.Y., Hajdu, R., Bergstrom, J., Card, D., Doherty, G., Hale, J., Keohane, C., Meyers, C., Milligan, J., et al. (2004). Immune cell regulation and cardiovascular effects of sphingosine 1-phosphate receptor agonists in rodents are mediated via distinct receptor subtypes. J. Pharmacol. Exp. Ther. 309, 758-768. Published online January 27, 2004. 10.1124/jpet.103. 062828
55. Candelore, M.R., Wright, M.J., Tota, L.M., Milligan, J., Shei, G.J., Bergstrom, J.D., and Mandala, S.M. (2002). Phytosphingosine 1-phosphate: a high affinity ligand for the S1P(4)/Edg-6 receptor. Biochem. Biophys. Res. Commun. 297, 600-606.
56. Ballesteros, J.A., and Weinstein, H. (1995). Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors. Methods Neurosci. 25, 366-428.
57. Bautista, D.L., Baker, D.L., Wang, D., Fischer, D.J., Van Brocklyn, J., Spiegel, S., Tigyi, G., and Parrill, A.L. (2000). Dynamic modeling of EDG1 receptor structural changes induced by site-directed mutations. J. Mol. Struct. THEOCHEM 529, 219-224.
58. Konvicka, K., Guarnieri, F., Ballesteros, J.A., and Weinstein, H. (1998). A Proposed structure for transmembrane segment 7 of G protein-coupled receptors incorporating an asn-Pro/Asp-Pro motif. Biophys. J. 75, 601-611.
59. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M.J., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W., and Kollman, P.A. (1995). A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117, 5179-5197.
60. Halgren, T.A. (1996). Merck molecular force field. I. Basis, form, scope, parameterization, and performance of MMFF94. J. Comp. Chem. 17, 490-519.
61. Morris, G.M., Goodsell, D.S., Halliday, R.S., Huey, R., Hart, W.E., Belew, R.K., and Olson, A.J. (1998). Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comp. Chem. 19, 1639-1662.