Antinociceptive effects of FTY720 during trauma-induced neuropathic pain are mediated by spinal S1P receptors

Biological Chemistry

Volumn 396, Issue 6-7, 2015, Pages 783-794

  Zhang, Dong Dong ^a   Linke, Bona ^a   Suo, Jing ^a   Zivkovic, Aleksandra ^b   Schreiber, Yannick ^a   Ferreirós, Nerea ^a   Henke, Marina ^a,c   Geisslinger, Gerd ^a   Stark, Holger ^b   Scholich, Klaus ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

Author keywords

FTY720; Neuropathic pain; S1P receptor; Sphingosine 1 phosphate; Spinal cord

Indexed keywords

FINGOLIMOD; SPHINGOSINE 1 PHOSPHATE 1 RECEPTOR; SPHINGOSINE 1 PHOSPHATE 3 RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR; UNCLASSIFIED DRUG; 3-AMINO-4-(3-HEXYLPHENYLAMINO)-4-OXOBUTYLPHOSPHONIC ACID; ANALGESIC AGENT; ANILIDE; FTY 720P; LYSOPHOSPHOLIPID; ORGANOPHOSPHATE; PHOSPHONIC ACID DERIVATIVE; PHOSPHOTRANSFERASE; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; SPHINGOSINE KINASE 2, MOUSE;

ADULT; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG EFFICACY; INTRACELLULAR SIGNALING; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; SPINAL CORD; THERAPEUTIC INDEX; WHITE MATTER; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; COMPLICATION; DRUG EFFECTS; GENETICS; IN SITU HYBRIDIZATION; INJURY; MALE; METABOLISM; NEURALGIA; SIGNAL TRANSDUCTION;

ANALGESICS; ANILIDES; ANIMALS; IN SITU HYBRIDIZATION; LYSOPHOSPHOLIPIDS; MALE; MICE; NEURALGIA; ORGANOPHOSPHATES; ORGANOPHOSPHONATES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE; WOUNDS AND INJURIES;

EID: 84941013057     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0276     Document Type: Article

References (45)

1. Albert, R., Hinterding, K., Brinkmann, V., Guerini, D., Muller-Hartwieg, C., Knecht, H., Simeon, C., Streiff, M., Wagner, T., Welzenbach, K., et al. (2005). Novel immunomodulator FTY720 is phosphorylated in rats and humans to form a single stereoisomer. Identification, chemical proof, and biological characterization of the biologically active species and its enantiomer. J. Med. Chem. 48, 5373-5377.
2. Anliker, B. and Chun, J, (2004). Lysophospholipid G protein-coupled receptors. J. Biol. Chem. 279, 20555-20558.
3. Billich, A., Bornancin, F., Devay, P., Mechtcheriakova, D., Urtz, N., and Baumruker, T. (2003). Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J. Biol. Chem. 278, 47408-47415.
4. Brinkmann, V. (2007). Sphingosine 1-phosphate receptors in health and disease: mechanistic insights from gene deletion studies and reverse pharmacology. Pharmacol. Ther. 115, 84-105.
5. 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.
6. Camprubi-Robles, M., Mair, N., Andratsch, M., Benetti, C., Beroukas, D., Rukwied, R., Langeslag, M., Proia, R. L., Schmelz, M., Ferrer Montiel, A. V., et al. (2013). Sphingosine-1-phosphateinduced nociceptor excitation and ongoing pain behavior in mice and humans is largely mediated by S1P3 receptor. J. Neurosci. 33, 2582-2592.
7. Chen, X., Wiemer, A. J., Hohl, R. J., and Wiemer, D. F. (2002). Stereoselective synthesis of the 5'-hydroxy-5'-phosphonate derivatives of cytidine and cytosine arabinoside. J. Org. Chem. 67, 9331-9339.
8. Colombaioni, L. and Garcia-Gil, M. (2004). Sphingolipid metabolites in neural signalling and function. Brain Res. Brain Res. Rev. 46, 328-355.
9. Coste, O., Brenneis, C., Linke, B., Pierre, S., Maeurer, C., Becker, W., Schmidt, H., Gao, W., Geisslinger, G., and Scholich, K. (2008a). Sphingosine 1-phosphate modulates spinal nociceptive processing. J. Biol. Chem. 283, 32442-32451.
10. Coste, O., Pierre, S., Marian, C., Brenneis, C., Angioni, C., Schmidt, H., Popp, L., Geisslinger, G., and Scholich, K. (2008b). Antinociceptive activity of the S1P-receptor agonist FTY720. J. Cell. Mol. Med. Med 12, 995-1004.
11. Crossland, L. K. and Servis, K. L. (1970). Facile synthesis of methanesulfonate esters. J. Org. Chem. 35, 3195-3195.
12. Darios, F., Wasser, C., Shakirzyanova, A., Giniatullin, A., Goodman, K., Munoz-Bravo, J. L., Raingo, J., Jorgacevski, J., Kreft, M., Zorec, R., et al. (2009). Sphingosine facilitates SNARE complex assembly and activates synaptic vesicle exocytosis. Neuron 62, 683-694.
13. Decosterd, I. and Woolf, C. J. (2000). Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87, 149-158.
14. Durand, P., Peralba, P., Sierra, F., and Renaut, P. (2000). A new efficient synthesis of the Immuusuppresive Agent FTY-720. Synthesis 4, 505-506.
15. Finley, A., Chen, Z., Esposito, E., Cuzzocrea, S., Sabbadini, R., and Salvemini, D. (2013). Sphingosine 1-phosphate mediates hyperalgesia via a neutrophil-dependent mechanism. PLoS One 8, e55255.
16. Fujita, T., Hirose, R., Yoneta, M., Sasaki, S., Inoue, K., Kiuchi, M., Hirase, S., Chiba, K., Sakamoto, H., and Arita, M. (1996). Potent immunosuppressants, 2-alkyl-2-aminopropane-1, 3-diols. J. Med. Chem. 39, 4451-4459.
17. Grammatikos, G., Muhle, C., Ferreiros, N., Schroeter, S., Bogdanou, D., Schwalm, S., Hintereder, G., Kornhuber, J., Zeuzem, S., Sarrazin, C., et al. (2014). Serum acid sphingomyelinase is upregulated in chronic hepatitis C infection and non alcoholic fatty liver disease. Biochim. Biophys. Acta 1841, 1012-1020.
18. Groves, A., Kihara, Y., and Chun, J. (2013). Fingolimod: direct CNS effects of sphingosine 1-phosphate (S1P) receptor modulation and implications in multiple sclerosis therapy. J. Neurol. Sci. 328, 9-18.
19. Hla, T. and Dannenberg, A. J. (2012). Sphingolipid signaling in metabolic disorders. Cell Metab. 16, 420-434.
20. Jaillard, C., Harrison, S., Stankoff, B., Aigrot, M. S., Calver, A. R., Duddy, G., Walsh, F. S., Pangalos, M. N., Arimura, N., Kaibuchi, K., et al. (2005). Edg8/S1P5: an oligodendroglial receptor with dual function on process retraction and cell survival. J. Neurosci. 25, 1459-1469.
21. Janes, K., Little, J. W., Li, C., Bryant, L., Chen, C., Chen, Z., Kamocki, K., Doyle, T., Snider, A., Esposito, E., et al. (2014). The development and maintenance of paclitaxel-induced neuropathic pain require activation of the sphingosine 1-phosphate receptor subtype 1. J. Biol. Chem. 289, 21082-21097.
22. Karliner, J. S. (2009). Sphingosine kinase regulation and cardioprotection. Cardiovasc Res. 82, 184-192.
23. Lim, K. G., Tonelli, F., Li, Z., Lu, X., Bittman, R., Pyne, S., and Pyne, N. J. (2011). FTY720 analogues as sphingosine kinase 1 inhibitors: enzyme inhibition kinetics, allosterism, proteasomal degradation, and actin rearrangement in MCF-7 breast cancer cells. J. Biol. Chem. 286, 18633-18640.
24. Mair, N., Benetti, C., Andratsch, M., Leitner, M. G., Constantin, C. E., Camprubi-Robles, M., Quarta, S., Biasio, W., Kuner, R., Gibbins, I. L., et al. (2011). Genetic evidence for involvement of neuronally expressed S1P receptor in nociceptor sensitization and inflammatory pain. PLoS One 6, e17268.
25. Mulgaonkar, S., Tedesco, H., Oppenheimer, F., Walker, R., Kunzendorf, U., Russ, G., Knoflach, A., Patel, Y., and Ferguson, R. (2006). FTY720/cyclosporine regimens in de novo renal transplantation: a 1-year dose-finding study. Am. J. Transplant 6, 1848-1857.
26. Payne, S. G., Oskeritzian, C. A., Griffiths, R., Subramanian, P., Barbour, S. E., Chalfant, C. E., Milstien, S., and Spiegel, S. (2006). The immunosuppressant drug FTY720 inhibits cytosolic phospholipase A2 independently of sphingosine-1-phosphate receptors. Blood 109, 1077-1085.
27. Pchejetski, D., Bohler, T., Brizuela, L., Sauer, L., Doumerc, N., Golzio, M., Salunkhe, V., Teissie, J., Malavaud, B., Waxman, J., et al. (2010). FTY720 (fingolimod) sensitizes prostate cancer cells to radiotherapy by inhibition of sphingosine kinase-1. Cancer Res. 70, 8651-8661.
28. Pierre, S. C., Hausler, J., Birod, K., Geisslinger, G., and Scholich, K. (2004). PAM mediates sustained inhibition of cAMP signaling by sphingosine-1-phosphate. EMBO J. 23, 3031-3040.
29. Pyne, S., Lee, S. C., Long, J., and Pyne, N. J. (2009). Role of sphingosine kinases and lipid phosphate phosphatases in regulating spatial sphingosine 1-phosphate signalling in health and disease. Cell Signal. 21, 14-21.
30. Saba, J. D. and Hla, T. (2004). Point-counterpoint of sphingosine 1-phosphate metabolism. Circ. Res. 94, 724-734.
31. 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.
32. Schmidtko, A., Gao, W., Sausbier, M., Rauhmeier, I., Sausbier, U., Niederberger, E., Scholich, K., Huber, A., Neuhuber, W., Allescher, H. D., et al. (2008). Cysteine-rich protein 2, a novel downstream effector of cGMP/cGMP-dependent protein kinase I-mediated persistent inflammatory pain. J. Neurosci. 28, 1320-1330.
33. Scott, C. W. and Peters, M. F. (2010). Label-free whole-cell assays: expanding the scope of GPCR screening. Drug Discov. Today 15, 704-716.
34. Sisignano, M., Bennett, D. L., Geisslinger, G., and Scholich, K. (2014). TRP-channels as key integrators of lipid pathways in nociceptive neurons. Progr. Lipid Res. 53, 93-107.
35. Spiegel, S. and Milstien, S. (2002). Sphingosine 1-phosphate, a key cell signaling molecule. J. Biol. Chem. 277, 25851-25854.
36. Spiegel, S. and Milstien, S. (2003). Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell. Biol. 4, 397-407.
37. Spiegel, S. and Milstien, S. (2011). The outs and the ins of sphingosine-1-phosphate in immunity. Nat. Rev. Immunol. 11, 403-415.
38. Spiegel, S., Milstien, S., and Grant, S. (2012). Endogenous modulators and pharmacological inhibitors of histone deacetylases in cancer therapy. Oncogene 31, 537-551.
39. Tedesco-Silva, H., Mourad, G., Kahan, B. D., Boira, J. G., Weimar, W., Mulgaonkar, S., Nashan, B., Madsen, S., Charpentier, B., Pellet, P., et al. (2005). FTY720, a novel immunomodulator: efficacy and safety results from the first phase 2A study in de novo renal transplantation. Transplantation 79, 1553-1560.
40. Van Brocklyn, J. R., Lee, M. J., Menzeleev, R., Olivera, A., Edsall, L., Cuvillier, O., Thomas, D. M., Coopman, P. J., Thangada, S., Liu, C. H., et al. (1998). Dual actions of sphingosine-1-phosphate: extracellular through the Gi-coupled receptor Edg-1 and intracellular to regulate proliferation and survival. J. Cell Biol. 142, 229-240.
41. Zemann, B., Kinzel, B., Muller, M., Reuschel, R., Mechtcheriakova, D., Urtz, N., Bornancin, F., Baumruker, T., and Billich, A. (2006). Sphingosine kinase type 2 is essential for lymphopenia induced by the immunomodulatory drug FTY720. Blood 107, 1454-1458.
42. Zhang, Y. H., Fehrenbacher, J. C., Vasko, M. R., and Nicol, G. D. (2006a). Sphingosine-1-phosphate via activation of a G-protein-coupled receptor (s) enhances the excitability of rat sensory neurons. J. Neurophysiol. 96, 1042-1052.
43. Zhang, Y. H., Vasko, M. R., and Nicol, G. D. (2006b). Intracellular sphingosine 1-phosphate mediates the increased excitability produced by nerve growth factor in rat sensory neurons. J. Physiol. 575, 101-113.
44. + monocytes in early lesions of rat traumatic brain injury. J. Cell. Mol. Med. Med 11, 307-314.
45. Zivkovic, A. S. and Stark, H. (2010). Efficient chromatograpy-free synthesis of the oxy-anylogue of fingolimod. Tetrahedron Lett. 51, 3769-3771.