A novel mode of action of the putative sphingosine kinase inhibitor 2-(p-hydroxyanilino)-4-(p-chlorophenyl) thiazole (SKI II): Induction of lysosomal sphingosine kinase 1 degradation

Cellular Physiology and Biochemistry

Volumn 26, Issue 1, 2010, Pages 97-104

  Ren, Shuyu ^a   Xin, Cuiyan ^a   Pfeilschifter, Josef ^b   Huwiler, Andrea ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Cathepsin B; Chloroquine; Lysosome; Protein degradation; SKI II; Sphingosine kinase 1

Indexed keywords

2 (4 HYDROXYANILINO) 4 (4 CHLOROPHENYL)THIAZOLE; CATHEPSIN B; CHLOROQUINE; CYCLOHEXIMIDE; ENZYME INHIBITOR; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL STRAIN HEK293; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; LYSOSOME; MESANGIUM CELL; NUCLEOTIDE SEQUENCE; PODOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

EID: 77952907876     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000315110     Document Type: Article

References (37)

1. Huwiler A, Kolter T, Pfeilschifter J, Sandhoff K: Physiology and pathophysi-ology of sphingolipid metabolism and signaling. Biochim Biophys Acta 2000;1485:63-99.
2. Spiegel S, Milstien S: Sphingosine 1-phos-phate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003;4:397-407.
3. Huwiler A, Zangemeister-Wittke U: Targeting the conversion of ceramide to sphingosine 1-phosphate as a novel strategy for cancer therapy. Crit Rev Oncol Hematol 2007;63:150-159.
4. Huwiler A, Pfeilschifter J: Altering the sphingosine-1-phosphate/ceramide balance: a promising approach for tumor therapy. Curr Pharm Des 2006;12:4625-4635.
5. Alemany R, van Koppen CJ, Danneberg K, Ter Braak M, Meyer zu Heringdorf D: Regulation and functional roles of sphin-gosine kinases. Naunyn Schmiedebergs Arch Pharmacol 2007;374:413-428.
6. Shida D, Takabe K, Kapitonov D, Milstien S, Spiegel S: Targeting SphK1 as a new strategy against cancer. Curr Drug Targets 2008;9:662-673.
7. Ader I, Malavaud B, Cuvillier O: When the sphingosine kinase 1/sphingosine 1-phosphate pathway meets hypoxia signaling: new targets for cancer therapy. Cancer Res 2009;69:3723-3726.
8. Xia P, Gamble JR, Wang L, Pitson SM, Moretti PA, Wattenberg BW, D'Andrea RJ, Vadas MA: An oncogenic role of sphingosine kinase. Current Biology 2008;10:1527-1530.
9. French KJ, Schrecengost RS, Lee BD, Zhuang Y, Smith SN, Eberly JL, Yun JK, Smith CD: Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res 2003;63:5962-5969.
10. Johnson KR, Johnson KY, Crellin HG, Ogretmen B, Boylan AM, Harley RA, Obeid LM: Immunohistochemical distribution of sphingosine kinase 1 in normal and tumor lung tissue. J Histochem Cytochem 2005;53:1159-1166.
11. Liu H, Toman RE, Goparaju SK, Maceyka M, Nava VE, Sankala H, Payne S G, Bektas M, Ishii I, Chun J, Milstien S, Spiegel S: Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J Biol Chem 2003;278:40330-40336.
12. Sutherland CM, Moretti PA, Hewitt NM, Bagley CJ, Vadas MA, Pitson SM: The calmodulin-binding site of sphingosine kinase and its role in agonist-dependent translocation of sphingosine kinase 1 to the plasma membrane. J Biol Chem 2006;281:11693-11701.
13. Kleuser B, Maceyka M, Milstien S, Spiegel S: Stimulation of nuclear sphingosine ki-nase activity by platelet-derived growth factor. FEBS Lett 2001;503:85-90.
14. Inagaki Y, Li PY, Wada A, Mitsutake S, Igarashi Y: Identification of functional nuclear export sequences in human sphin-gosine kinase 1. Biochem Biophys Res Commun 2003;311:168-173.
15. Igarashi N, Okada T, Hayashi S, Fujita T, Jahangeer S, Nakamura S: Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J Biol Chem 2003;278:46832-46839.
16. Ding G, Sonoda H, Yu H, Kajimoto T, Goparaju SK, Jahangeer S, Okada T, Nakamura S: Protein kinase D-mediated phosphorylation and nuclear export of sphingosine kinase 2. J Biol Chem 2007;282:27493-27502.
17. Buehrer BM, Bell RM: Inhibition of sphingosine kinase in vitro and in platelets: implications for signal transduction pathways. J Biol Chem 1992;267:3154-3159.
18. Yatomi Y, Ruan F, Megidish T, Toyokuni T, Hakomori S, Igarashi Y: N,N-Dimethylsphingosine inhibition of sphin-gosine kinase and sphingosine 1-phos-phate activity in human platelets. Biochemistry 1996;35:626-633.
19. Olivera A, Kohama T, Tu Z, Milstien S, Spiegel S: Purification and characterization of rat kidney sphingosine kinase. J Biol Chem 1998;273:12576-12583 (Pubitemid 28240634)
20. Igarashi Y, Hakomori S, Toyokuni T, Dean B, Fujita S, Sugimoto M, Ogawa T, el-Ghendy K, Racker E Effect of chemically well-defined sphingosine and its N-methyl derivatives on protein kinase C and src kinase activities. Biochemistry 1989;28:6796-6800.
21. Schwartz GK, Ward D, Saltz L, Casper ES, Spiess T, Mullen E, Woodworth J, Venuti R, Zervos P, Storniolo AM, Kelsen DP: A pilot clinical/pharmacological study of the protein kinase C-specific inhibitor safingol alone and in combination with doxorubicin. Clin Cancer Res 1997;3:537-543.
22. Edsall LC, Van Brocklyn JR, Cuvillier O, Kleuser B, Spiegel S: N,N-Dimethylsphingosine is a potent competitive inhibitor of sphingosine kinase but not of protein kinase C: modulation of cellular levels of sphingosine 1-phos-phate and ceramide. Biochemistry 1998;37:12892-12898.
23. Döll F, Pfeilschifter J, Huwiler A: The epidermal growth factor stimulates sphingosine kinase-1 expression and activity in the human mammary carcinoma cell line MCF7. Biochim Biophys Acta 2005;1738:72-81.
24. Huwiler A, Döll F, Ren S, Klawitter S, Greening A, Römer I, Bubnova S, Reinsberg L, Pfeilschifter J: Histamine increases sphingosine kinase-1 expression and activity in the human arterial endothelial cell line EA.hy 926 by a PKC-α-dependent mechanism. Biochim Biophys Acta 2006;1761:367-376.
25. Ren S, Babelova A, Moreth K, Xin C, Eberhardt W, Doller A, Pavenstädt H, Schaefer L, Pfeilschifter J, Huwiler A: Transforming growth factor-beta2 upregulates sphingosine kinase-1 activity, which in turn attenuates the fibrotic response to TGF-beta2 by impeding CTGF expression. Kidney Int 2009;76:857-867.
26. Edgell CJ, McDonald CC, Graham JB: Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci USA 1983;80:3734-3737.
27. Huwiler A, Pfeilschifter J: Stimulation by extracellular ATP and UTP of the mi-togen-activated protein kinase cascade and proliferation of rat renal mesangial cells. Br J Pharmacol 1994;113:1455-1463. (Pubitemid 24364434)
28. Fenteany G, Standaert RF, Lane WS, Choi S, Corey EJ, Schreiber SL: Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 1995;268:726-731.
29. de Duve C, de Barsy T, Poole B, Trouet A, Tulkens P, Van Hoof F: Lysosomotropic agents. Biochem Pharmacol 1974;23:2495-2531.
30. Linebaugh BE, Sameni M, Day NA, Sloane BF, Keppler D: Exocytosis of active cathepsin B enzyme activity at pH 7.0, inhibition and molecular mass. Eur J Biochem 1999;264:100-109.
31. Taha TA, Kitatani K, Bielawski J, Cho W, Hannun YA, Obeid LM: Tumor necrosis factor induces the loss of sphin-gosine kinase-1 by a cathepsin B-depend-ent mechanism. J Biol Chem 2005;280:17196-17202.
32. Taha TA, El-Alwani M, Hannun YA, Obeid LM: Sphingosine kinase-1 is cleaved by cathepsin B in vitro: identification of the initial cleavage sites for the protease. FEBS Lett 2006;580:6047-6054.
33. Turk B, Stoka V, Rozman-Pungercar J, Cirman T, Droga-Mazovec G, Oresiæ K, Turk V: Apoptotic pathways: involvement of lysosomal proteases. Biol Chem 2002;383:1035-1044.
34. Conus S, Simon H: Cathepsins: key modulator of cell death and inflammotry responses. Biochem Pharmacol 2008;76:1374-1382.
35. Hicke L: Gettin' down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 1999;9:107-112.
36. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, Thomsen GH, Wrana JL: Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 2000;6:1365-1375.
37. Heinrich M, Wickel M, Schneider-Brachert W, Sandberg C, Gahr J, Schwandner R, Weber T, Saftig P, Peters C, Brunner J, Krönke M, Schütze S: Cathepsin D targeted by acid sphingomyelinase-derived ceramide. EMBO J 1999;18:5252-5263.