Sphingosine kinase 2 deficiency increases proliferation and migration of renal mouse mesangial cells and fibroblasts

Biological Chemistry

Volumn 396, Issue 6-7, 2015, Pages 813-825

  Schwalm, Stephanie ^a,b   Timcheva, Tankica Maneva ^b   Filipenko, Iuliia ^b   Ebadi, Mahsa ^a   Hofmann, Lotte P ^a,b   Zangemeister Wittke, Uwe ^b   Pfeilschifter, Josef ^a   Huwiler, Andrea ^b  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Fibroblasts; Migration; Proliferation; Renal mesangial cells; Sphingosine 1 phosphate; Sphingosine kinase

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 AMINO 2 (3 OCTYLPHENYLCARBAMOYL)ETHYL PHOSPHATE; 3 (4 CHLOROPHENYL) N (4 PYRIDINYLMETHYL)ADAMANTANE 1 CARBOXAMIDE; 4 (2,6 DICHLORO 4 PYRIDINYL) 1 (1,3 DIMETHYL 4 ISOPROPYL 1H PYRAZOLO[3,4 B]PYRIDIN 6 YL)SEMICARBAZIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SPHINGOSINE 1 PHOSPHATE 3 RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE KINASE 2; UNCLASSIFIED DRUG; WORTMANNIN; PHOSPHOTRANSFERASE; SPHINGOSINE KINASE 2, HUMAN;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL LYSATE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; FIBROBLAST; MESANGIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; DEFICIENCY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; FIBROBLASTS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR);

EID: 84957366334     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0289     Document Type: Article

References (50)

1. Alemany, R., van Koppen, C. J., Danneberg, K., Ter Braak, M., and Meyer Zu Heringdorf, D. (2007). Regulation and functional roles of sphingosine kinases. Naunyn-Schmiedeberg's Arch. Pharmacol. 374, 413-428.
2. An, S., Zheng, Y., and Bleu, T. (2000). Sphingosine 1-phosphateinduced cell proliferation, survival, and related signaling events mediated by G protein-coupled receptors Edg3 and Edg5. J. Biol. Chem. 275, 288-296.
3. Antoon, J. W., White, M. D., Meacham, W. D., Slaughter, E. M., Muir, S. E., Elliott, S., Rhodes, L. V., Ashe, H. B., Wiese, T. E., Smith, C. D., et al. (2010). Antiestrogenic effects of the novel sphingosine kinase-2 inhibitor ABC294640. Endocrinology 151, 5124-5135.
4. Antoon, J. W., White, M. D., Slaughter, E. M., Driver, J. L., Khalili, H. S., Elliott, S., Smith, C. D., Burow, M. E., and Beckman, B. S. (2011). Targeting NF-kB mediated breast cancer chemoresistance through selective inhibition of sphingosine kinase-2. Cancer Biol. Ther. 11, 678-689.
5. Arikawa, K., Takuwa, N., Yamaguchi, H., Sugimoto, N., Kitayama, J., Nagawa, H., Takehara, K., and Takuwa, Y. (2003). Liganddependent inhibition of B16 melanoma cell migration and invasion via endogenous S1P2 G protein-coupled receptor. Requirement of inhibition of cellular RAC activity. J. Biol. Chem. 278, 32841-32851.
6. Baker, D. A., Eudaly, J., Smith, C. D., Obeid, L. M., and Gilkeson, G. S. (2013). Impact of sphingosine kinase 2 deficiency on the development of TNF-a-induced inflammatory arthritis. Rheumatol. Int. 33, 2677-2681.
7. Bessa, C., Pereira, C., Leao, M., Maciel, C., Gomes, S., Goncalves, J., Corte-Real, M., Costa, V., and Saraiva, L. (2013). Using yeast to uncover the regulation of protein kinase Cdelta by ceramide. FEMS Yeast Res. 13, 700-705.
8. Calise, S., Blescia, S., Cencetti, F., Bernacchioni, C., Donati, C., and Bruni, P. (2012). Sphingosine 1-phosphate stimulates proliferation and migration of satellite cells: role of S1P receptors. Biochim. Biophys. Acta. 1823, 439-450.
9. Conner, D. A. (2001). Mouse embryo fibroblast (MEF) feeder cell preparation. Curr. Protoc. Mol. Biol. Chapter 23, Unit 23 22.
10. Döll, F., Pfeilschifter, J., and Huwiler, A. (2005). The epidermal growth factor stimulates sphingosine kinase-1 expression and activity in the human mammary carcinoma cell line MCF7. Biochim. Biophys. Acta. 1738, 72-81.
11. Döll, F., Pfeilschifter, J., and Huwiler, A. (2007). Prolactin upregulates sphingosine kinase-1 expression and activity in the human breast cancer cell line MCF7 and triggers enhanced proliferation and migration. Endocr. Relat. Cancer 14, 325-335.
12. Favata, M. F., Horiuchi, K. Y., Manos, E. J., Daulerio, A. J., Stradley, D. A., Feeser, W. S., Van Dyk, D. E., Pitts, W. J., Earl, R. A., Hobbs, F., et al. (1998). Identification of a novel inhibitor of mitogenactivated protein kinase kinase. J. Biol. Chem. 273, 18623-18632.
13. French, K. J., Schrecengost, R. S., Lee, B. D., Zhuang, Y., Smith, S. N., Eberly, J. L., Yun, J. K., and Smith, C. D. (2003). Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res. 63, 5962-5969.
14. French, K. J., Upson, J. J., Keller, S. N., Zhuang, Y., Yun, J. K., and Smith, C. D. (2006). Antitumor activity of sphingosine kinase inhibitors. J. Pharmacol. Exp. Ther. 318, 596-603.
15. French, K. J., Zhuang, Y., Maines, L. W., Gao, P., Wang, W., Beljanski, V., Upson, J. J., Green, C. L., Keller, S. N., and Smith, C. D. (2010). Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J. Pharmacol. Exp. Ther. 333, 129-139.
16. Goparaju, S. K., Jolly, P. S., Watterson, K. R., Bektas, M., Alvarez, S., Sarkar, S., Mel, L., Ishii, I., Chun, J., Milstien, S., et al. (2005). The S1P2 receptor negatively regulates platelet-derived growth factor-induced motility and proliferation. Mol. Cell. Biol. 25, 4237-4249.
17. Hait, N. C., Bellamy, A., Milstien, S., Kordula, T., and Spiegel, S. (2007). Sphingosine kinase type 2 activation by ERK-mediated phosphorylation. J. Biol. Chem. 282, 12058-12065.
18. Hall, A. (1990). The cellular functions of small GTP-binding proteins. Science 249, 635-640.
19. Hofmann, L. P., Ren, S., Schwalm, S., Pfeilschifter, J., and Huwiler, A. (2008). Sphingosine kinase 1 and 2 regulate the capacity of mesangial cells to resist apoptotic stimuli in an opposing manner. Biol. Chem. 389, 1399-1407.
20. Huwiler, A., Brunner, J., Hummel, R., Vervoordeldonk, M., Stabel, S., van den Bosch, H., and Pfeilschifter, J. (1996). Ceramidebinding and activation defines protein kinase c-Raf as a ceramide-activated protein kinase. Proc. Natl. Acad. Sci. USA 93, 6959-6963.
21. Huwiler, A., Doll, F., Ren, S., Klawitter, S., Greening, A., Romer, I., Bubnova, S., Reinsberg, L., and Pfeilschifter, J. (2006). Histamine increases sphingosine kinase-1 expression and activity in the human arterial endothelial cell line EA. hy 926 by a PKC-alpha-dependent mechanism. Biochim. Biophys. Acta. 1761, 367-376.
22. Huwiler, A., Fabbro, D., and Pfeilschifter, J. (1998). Selective ceramide binding to protein kinase C-a and -d isoenzymes in renal mesangial cells. Biochemistry 37, 14556-14562.
23. Huwiler, A., Kolter, T., Pfeilschifter, J., and Sandhoff, K. (2000). Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim. Biophys. Acta. 1485, 63-99.
24. Huwiler, A. and Pfeilschifter, J. (2006). Altering the sphingosine-1-phosphate/ceramide balance: a promising approach for tumor therapy. Curr. Pharm. Des. 12, 4625-4635.
25. Igarashi, N., Okada, T., Hayashi, S., Fujita, T., Jahangeer, S., and Nakamura, S. (2003). Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J. Biol. Chem. 278, 46832-46839.
26. Ishii, I., Friedman, B., Ye, X., Kawamura, S., McGiffert, C., Contos, J. J., Kingsbury, M. A., Zhang, G., Brown, J. H., and Chun, J. (2001). Selective loss of sphingosine 1-phosphate signaling with no obvious phenotypic abnormality in mice lacking its G protein-coupled receptor, LP (B3)/EDG-3. J. Biol. Chem. 276, 33697-33704.
27. Jo, S. K., Bajwa, A., Ye, H., Vergis, A. L., Awad, A. S., Kharel, Y., Lynch, K. R., and Okusa, M. D. (2009). Divergent roles of sphingosine kinases in kidney ischemia-reperfusion injury. Kidney Int. 75, 167-175.
28. Katsuma, S., Hada, Y., Ueda, T., Shiojima, S., Hirasawa, A., Tanoue, A., Takagaki, K., Ohgi, T., Yano, J., and Tsujimoto, G. (2002). Signalling mechanisms in sphingosine 1-phosphate-promoted mesangial cell proliferation. Genes Cells 7, 1217-1230.
29. Keely, P. J., Conklin, M. W., Gehler, S., Ponik, S. M., and Provenzano, P. P. (2007). Investigating integrin regulation and signaling events in three-dimensional systems. Methods Enzymol. 426, 27-45.
30. Klawitter, S., Hofmann, L. P., Pfeilschifter, J., and Huwiler, A. (2007). Extracellular nucleotides induce migration of renal mesangial cells by upregulating sphingosine kinase-1 expression and activity. Br. J. Pharmacol. 150, 271-280.
31. Kunkel, G. T., Maceyka, M., Milstien, S., and Spiegel, S. (2013). Targeting the sphingosine-1-phosphate axis in cancer, inflammation and beyond. Nat. Rev. Drug Discov. 12, 688-702.
32. Liang, J., Nagahashi, M., Kim, E. Y., Harikumar, K. B., Yamada, A., Huang, W. C., Hait, N. C., Allegood, J. C., Price, M. M., Avni, D., et al. (2013). Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation, and development of colitis-associated cancer. Cancer Cell 23, 107-120.
33. Liu, H., Sugiura, M., Nava, V. E., Edsall, L. C., Kono, K., Poulton, S., Milstien, S., Kohama, T., and Spiegel, S. (2000a). Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J. Biol. Chem. 275, 19513-19520.
34. Liu, Y., Wada, R., Yamashita, T., Mi, Y., Deng, C. X., Hobson, J. P., Rosenfeldt, H. M., Nava, V. E., Chae, S. S., Lee, M. J., et al. (2000b). Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Invest. 106, 951-961.
35. Liu, H., Toman, R. E., Goparaju, S. K., Maceyka, M., Nava, V. E., Sankala, H., Payne, S. G., Bektas, M., Ishii, I., Chun, J., et al. (2003). Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J. Biol. Chem. 278, 40330-40336.
36. Muller, G., Ayoub, M., Storz, P., Rennecke, J., Fabbro, D., and Pfizenmaier, K. (1995). PKC zeta is a molecular switch in signal transduction of TNF-a, bifunctionally regulated by ceramide and arachidonic acid. EMBO J. 14, 1961-1969.
37. O'Connor, K. and Chen, M. (2013). Dynamic functions of RhoA in tumor cell migration and invasion. Small GTPases 4, 141-147.
38. Okada, T., Ding, G., Sonoda, H., Kajimoto, T., Haga, Y., Khosrowbeygi, A., Gao, S., Miwa, N., Jahangeer, S., and Nakamura, S. (2005). Involvement of N-terminal-extended form of sphingosine kinase 2 in serum-dependent regulation of cell proliferation and apoptosis. J. Biol. Chem. 280, 36318-36325.
39. 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.
40. Osada, M., Yatomi, Y., Ohmori, T., Ikeda, H., and Ozaki, Y. (2002). Enhancement of sphingosine 1-phosphate-induced migration of vascular endothelial cells and smooth muscle cells by an EDG-5 antagonist. Biochem. Biophys. Res. Commun. 299, 483-487.
41. Paik, J. H., Chae, S., 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 Rhodependent activation of avb3- and b1-containing integrins. J. Biol. Chem. 276, 11830-11837.
42. Pertz, O., Hodgson, L., Klemke, R. L., and Hahn, K. M. (2006). Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440, 1069-1072.
43. Pyne, N. J. and Pyne, S. (2010). Sphingosine 1-phosphate and cancer. Nat. Rev. Cancer 10, 489-503.
44. Rölz, W., Xin, C., Ren, S., Pfeilschifter, J., and Huwiler, A. (2002). Interleukin-1 inhibits angiotensin II-stimulated protein kinase B pathway in renal mesangial cells via the inducible nitric oxide synthase. Eur. J. Pharmacol. 442, 195-203.
45. Ruckhäberle, E., Rody, A., Engels, K., Gaetje, R., von Minckwitz, G., Schiffmann, S., Grösch, S., Geisslinger, G., Holtrich, U., Karn, T., et al. (2008). Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res. Treat. 112, 41-52.
46. Shida, D., Takabe, K., Kapitonov, D., Milstien, S., and Spiegel, S. (2008). Targeting SphK1 as a new strategy against cancer. Curr. Drug Targets 9, 662-673.
47. Vivanco, I. and Sawyers, C. L. (2002). The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2, 489-501.
48. vom Dorp, F., Sanders, H., Boergermann, C., Lummen, G., Rubben, H., Jakobs, K. H., and Schmidt, M. (2011). Inhibition of Rho-kinase abrogates migration of human transitional cell carcinoma cells: results of an in vitro study. Urol. Int. 86, 220-227.
49. Wymann, M. P., Bulgarelli-Leva, G., Zvelebil, M. J., Pirola, L., Vanhaesebroeck, B., Waterfield, M. D., and Panayotou, G. (1996). Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys-802, a residue involved in the phosphate transfer reaction. Mol. Cell Biol. 16, 1722-1733.
50. Zhang, W., Zhao, J., Lee, J. F., Gartung, A., Jawadi, H., Lambiv, W. L., Honn, K. V., and Lee, M. J. (2013). ETS-1-mediated transcriptional up-regulation of CD44 is required for sphingosine-1-phosphate receptor subtype 3-stimulated chemotaxis. J. Biol. Chem. 288, 32126-32137.