Sphingosine kinase expression increases intracellular sphingosine-1- phosphate and promotes cell growth and survival

Journal of Cell Biology

Volumn 147, Issue 3, 1999, Pages 545-557

  Olivera, Ana ^a   Kohama, Takafumi ^a   Edsall, Lisa ^a   Nava, Victor ^a   Cuvillier, Olivier ^a   Poulton, Samantha ^a   Spiegel, Sarah ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Cell growth; Sphingosine kinase; Sphingosine 1 phosphate

Indexed keywords

CELL SURFACE RECEPTOR; CERAMIDE; FAS LIGAND; GUANINE NUCLEOTIDE BINDING PROTEIN; N,N DIMETHYLSPHINGOSINE; PERTUSSIS TOXIN; PHOSPHOTRANSFERASE; SPHINGOSINE 1 PHOSPHATE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOGENICITY; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; RECEPTOR BINDING; SECOND MESSENGER;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; CASPASE 3; CASPASES; CELL DIVISION; CELL LINE; CELL SURVIVAL; CYTOSOL; DNA; ENZYME ACTIVATION; HUMANS; LYSOPHOSPHOLIPIDS; MICE; PEPTIDE HYDROLASES; PERTUSSIS TOXIN; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PLATELET-DERIVED GROWTH FACTOR; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LYSOPHOSPHOLIPID; RECOMBINANT FUSION PROTEINS; SECOND MESSENGER SYSTEMS; SPHINGOSINE; TRANSFECTION; VIRULENCE FACTORS, BORDETELLA;

EID: 0033230364     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.3.545     Document Type: Article

References (80)

1. An, S., T. Bleu, W. Huang, O.G. Hallmark, S.R. Coughling, and E.J. Goetzl. 1997. Identification of cDNAs encoding two G protein-coupled receptors for lysosphingolipids. FEBS Lett. 417:279-282.
2. Bhattacharya, M., K.G. Peri, G. Almazan, A. Ribeiro-da-Silva, H. Shichi, Y. Durocher, M. Abramovitz, X. Hou, D.R. Varma, and S. Chemtob. 1998. Nuclear localization of prostaglandin E2 receptors. Proc. Natl. Acad. Sci. USA. 95:15792-15797.
3. Bornfeldt, K.E., L.M. Graves, E.W. Raines, Y. Igarashi, G. Wayman, S. Yamamura, Y. Yatomi, J.S. Sidhu, E.G. Krebs, S. Hakomori, and R. Ross. 1995. Sphingosine-1-phosphate inhibits PDGF-induced chemotaxis of human arterial smooth muscle cells: spatial and temporal modulation of PDGF chemotactic signal transduclion. J. Cell Biol. 130:193-206.
4. Brancolini, C., D. Lazarevic, J. Rodriguez, and C. Schneider. 1997. Dismantling cell-cell contacts during apoptosis is coupled to a caspase-dependent proteolytic cleavage of beta-catenin. J. Cell Biol. 139:759-771.
5. Buehrer, B.M., E.S. Bardes, and R.M. Bell. 1996. Protein kinase C-dependent regulation of human erythroleukemia (HEL) cell sphingosine kinase activity. Biochim. Biophys. Acta. 1303:233-242.
6. Buehrer, B.M., and R.M. Bell. 1992. Inhibition of sphingosine kinase in vitro and in platelets. Implications for signal transduction pathways. J. Biol. Chem. 267:3154-3159.
7. Choi, O.H., J.-H. Kim, and J.-P. Kinet. 1996. Calcium mobilization via sphingosine kinase in signalling by the Fc∈RI antigen receptor. Nature. 380:634-636.
8. Coroneos, E., M. Martinez, S. McKenna, and M. Kester. 1995. Differential regulation of sphingomyelinase and ceramidase activities by growth factors and cytokines. J. Biol. Chem. 270:23305-23309.
9. Cuvillier, O., G. Pirianov, B. Kleuser, P.G. Vanek, O.A. Coso, S. Gutkind, and S. Spiegel. 1996. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 381:800-803.
10. Cuvillier, O., D.S. Rosenthal, M.E. Smulson, and S. Spiegel. 1998. Sphingosine-1-phosphate inhibits activation of caspases that cleave poly(ADP-ribose) polymerase and lamins during Fas-and ceramide-mediated apoptosis in Jurkat T lymphocytes. J. Biol. Chem. 273:2910-2916.
11. Dickson, R.C., E.E. Nagiec, M. Skrzypek, P. Tillman, G.B. Wells, and R.L. Lester. 1997. Sphingolipids are potential heat stress signals in Saccharomyces. J. Biol. Chem. 272:30196-30200.
12. Edsall, L.C., G.G. Pirianov, and S. Spiegel. 1997. Involvement of sphingosine 1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J. Neurosci. 17:6952-6960.
13. Edsall, L.C., and S. Spiegel. 1999. Enzymatic measurement of sphingosine-1-phosphate. Anal. Biochem. 272:80-86.
14. Evan, G., and T. Littlewood. 1998. A matter of life and cell death. Science. 281: 1317-1322.
15. Ghosh, T.K., J. Bian, and D.L. Gill. 1994. Sphingosine 1-phosphate generated in the endoplasmic reticulum membrane activates release of stored calcium. J. Biol. Chem. 269:22628-22635.
16. Goetzl, E.J., and S. An. 1998. Diversity of cellular receptors and functions for the lysophospholipid growth factors lysophosphatidic acid and sphingosine 1-phosphate. FASEB J. 12:1589-1598.
17. Goetzl, E.J., Y. Kong, and B. Mei. 1999. Lysophosphatidic acid and sphingosine 1-phosphate protection of T cells from apoptosis in association with suppression of Bax. J. Immunol. 162:2049-2056.
18. Gonda, K., H. Okamoto, N. Takuwa, Y. Yatomi, H. Okazaki, T. Sakurai, S. Kimura, R. Sillard, K. Harii, and Y. Takuwa. 1999. The novel sphingosine 1-phosphate receptor AGR16 is coupled via pertussis toxin-sensitive and -insensitive G-proteins to multiple signalling pathways. Biochem. J. 337:67-75.
19. Goodemote, K.A., M.E. Mattie, A. Berger, and S. Spiegel. 1995. Involvement of a pertussis toxin sensitive G protein in the mitogenic signaling pathways of sphingosine 1-phosphate. J. Biol. Chem. 270:10272-10277.
20. Gottlieb, D., W. Heideman, and J.D. Saba. 1999. The DPL1 gene is involved in mediating the response to nutrient deprivation in Saccharomyces cerevisiae. Mol. Cell Biol. Res. Commun. 1:66-71.
21. Hannun, Y. 1996. Functions of ceramide in coordinating cellular responses to stress. Science. 274:1855-1859.
22. Harrington, E.A., A. Fanadi, and G.I. Evan. 1994. Oncogenes and cell death. Curr. Biol. 4:120-129.
23. Jacobsen, M.D., M. Weil, and M.C. Raff. 1996. Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J. Cell Biol. 133: 1041-1051.
24. Jenkins, G.M., A. Richards, T. Wahl, C. Mao, L. Obeid, and Y. Hannun. 1997. Involvement of yeast sphingolipids in the heat stress response of Saccharomyces cerevisiae. J. Biol. Chem. 272:32566-32572.
25. Kleuser, B., O. Cuvillier, and S. Spiegel. 1998. 1α,25-dihydroxyvitamin D3 inhibits programmed cell death in HL-60 cells by activation of sphingosine kinase. Cancer Res. 58:1817-1824.
26. Kohama, T., A. Olivera, L. Edsall, M.M. Nagiec, R. Dickson, and S. Spiegel. 1998. Molecular cloning and functional characterization of murine sphingosine kinase. J. Biol. Chem. 273:23722-23728.
27. Kolesnick, R.N., and M. Kronke. 1998. Regulation of ceramide production and apoptosis. Annu. Rev. Physiol. 60:643-665.
28. Kon, J., K. Sato, T. Watanabe, H. Tomura, A. Kuwabara, T. Kimura, K. Tamama, T. Ishizuka, N. Murata, T. Kanda, et al. 1999. Comparison of intrinsic activities of the putative sphingosine 1-phosphate receptor subtypes to regulate several signaling pathways in their cDNA-transfected Chinese hamster ovary cells. J. Biol. Chem. 274:23940-23947.
29. Lanterman, M.M., and J.D. Saba. 1998. Characterization of sphingosine kinase (SK) activity in Saccharomyces cerevisiae and isolation of SK-deficient mutants. Biochem. J. 332:525-531.
30. Lee, M.-J., J.R. Van Brocklyn, S. Thangada, C.H. Liu, A.R. Hand, R. Menzeleev, S. Spiegel, and T. Hla. 1998. Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science. 279:1552-1555.
31. Liu, C.H., S. Thangada, M.-J. Lee, J.R. Van Brocklyn, S. Spiegel, and T. Hla. 1999. Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG-1. Mol. Biol. Cell. 10:1179-1190.
32. Machwate, M., S.B. Rodan, G.A. Rodan, and S.I. Harada. 1998. Sphingosine kinase mediates cyclic AMP suppression of apoptosis in rat periosteal cells. Mol. Pharmacol. 54:70-77.
33. Mandala, S., R. Thornton, Z. Tu, M. Kurtz, J. Nickels, J. Broach, R. Menzeleev, and S. Spiegel. 1998. Sphingoid base 1-phosphate phosphatase, a key regulator of sphingolipid metabolism and stress response. Proc. Natl. Acad. Sci. USA. 95:150-155.
34. Mao, C., J.D. Saba, and L.M. Obeid. 1999. The dihydrosphingosine-1-phosphate phosphatases of Saccharomyces cerevisiae are important regulators of cell proliferation and heat stress responses. Biochem. J. 342:667-675.
35. Mazurek, N., T. Megidish, S.-I. Hakomori, and Y. Igarashi. 1994. Regulatory effect of phorbol esters on sphingosine kinase in BALB/C 3T3 fibroblasts (variant A31): demonstration of cell type-specific response. Biochem. Biophys. Res. Commun. 198:1-9.
36. Melendez, A., R.A. Floto, D.J. Gillooly, M.M. Harnett, and J.M. Allen. 1998. FcγRI coupling to phospholipase D initiates sphingosine kinase-medialed calcium mobilization and vesicular trafficking. J. Biol. Chem. 273:9393-9402.
37. 2+ signalling by G-protein-coupled receptors. EMBO (Eur. Mol. Biol. Organ.) J. 17:2830-2837.
38. Nagiec, M.M., M. Skrzypek, E.E. Nagiec, R.L. Lester, and R.C. Dickson. 1998. The LCB4 (YOR17Ic) and LCB5 (YLR260w) genes of Saccharomyces encode long chain base kinases. J. Biol. Chem. 273:19437-19442.
39. Nicholson, D.W., A. All, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labelle, Y.A. Lazebnik, et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:37-43.
40. I arrest of Sacharromyces cerevisiae. Genes Dev. 10:382-394.
41. 2+ mobilization, ras-mitogen-activated protein kinase activation, and adenylate cyclase inhibition. J. Biol. Chem. 273:27104-27110.
42. Olivera, A., T. Kohama, Z. Tu, S. Milstien, and S. Spiegel. 1998. Purification and characterization of rat kidney sphingosine kinase. J. Biol. Chem. 273: 12576-12583.
43. Olivera, A., A. Romanowski, C.S. Rani, and S. Spiegel. 1997. Differential effects of sphingomyelinase and cell-permeable ceramide analogs on proliferation of Swiss 3T3 fibroblasts. Biochim. Biophys. Acta. 1348:311-323.
44. Olivera, A., J. Rosenthal, and S. Spiegel. 1994. Sphingosine kinase from Swiss 3T3 fibroblasts: a convenient assay for the measurement of intracellular levels of free sphingoid bases. Anal. Biochem. 223:306-312.
45. Olivera, A., and S. Spiegel. 1993. Sphingosine-1-phosphate as a second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature. 365: 557-560.
46. Olivera, A., and S. Spiegel. 1998. Sphingosine kinase. Assay and product analysis. In Methods in Molecular Biology. Vol. 105. I.M. Bird, editor. Humana Press Inc., Totawa, NJ. 233-242.
47. Ozawa, K., K. Kuwabara, M. Tamatani, K. Takatsuji, Y. Tsukamoto, S. Kaneda, H. Yanagi, D.M. Stern, Y. Eguchi, Y. Tsujimoto, et al. 1999. 150-kDa oxygen-regulated protein (ORP150) suppresses hypoxia-induced apoptotic cell death. J. Biol. Chem. 274:6397-6404.
48. Perez, G.I., C.M. Knudson, L. Leykin, S.J. Korsmeyer, and J.L. Tilly. 1997. Apoptosis-associated signaling pathways are required for chemotherapy-mediated female germ cell destruction. Nat. Med. 3:1228-1232.
49. Postma, F.R., K. Jalink, T. Hengeveld, and W.H. Moolenaar. 1996. Sphingosine-1-phosphate rapidly induces rho-dependent neurite retraction: action through a specific cell surface receptor. EMBO (Eur. Mol. Biol. Organ.) J. 15:2388-2392.
50. Pyne, S., J. Chapman, L. Steele, and N.J. Pyne. 1996. Sphingomyelin-derived lipids differentially regulate the extracellular signal-regulated kinase 2 (ERK-2) and c-Jun N-terminal kinase (JNK) signal cascades in airway smooth muscle cells. Eur. J. Biochem. 237:819-826.
51. Qiao, L., A.P. Kozikowski, A. Olivera, and S. Spiegel. 1998. Synthesis and evaluation of a photolyzable derivative of sphingosine 1-phosphate-caged SPP. Bioorg. Med. Chem. 8:711-714.
52. Rani, C.S., A. Berger, J. Wu, T.W. Sturgill, D. Beitner-Johnson, D. LeRoith, L. Varticovski, and S. Spiegel. 1997. Divergence in signal transduction pathways of PDGF and EGF receptors: involvement of sphingosine-1-phosphate in PDGF but not EGF signaling. J. Biol. Chem. 272:10777-10783.
53. Rius, R.A., L.C. Edsall, and S. Spiegel. 1997. Activation of sphingosine kinase in pheochromocytoma PC12 neuronal cells in response to trophic factors. FEBS Lett. 417:173-176.
54. Saba, J.D., F. Nara, A. Bielawska, S. Garrett, and Y.A. Hanun. 1997. The BST1 gene of Saccharomyces cerevisiae is the sphingosine-1-phosphate lyase. J. Biol. Chem. 272:26087-26090.
55. Sato, K., H. Tomura, Y. Igarashi, M. Ui, and F. Okajima. 1997. Exogenous sphingosine 1-phosphate induces neurite retraction possibly through a cell surface receptor in PC12 colls. Biochem. Biophys. Res. Commun. 240:329-334.
56. Sato, K., H. Tomura, Y. Igarashi, M. Ui, and F. Okajima. 1999. Possible involvement of cell surface receptors in sphingosine 1-phosphate-induced activation of extracellular signal-regulated kinase in C6 glioma cells. Mol. Pharmacol. 55:126-133.
57. Skrzypek, M.S., M.M. Nagiec, R.L. Lester, and R.C. Dickson. 1999. Analysis of phosphorylated sphingolipid long-chain bases reveals potential roles in heat stress and growth control in Saccharomyces. J. Bacteriol. 181:1134-1140.
58. Spiegel, S. 1999. Sphingosine 1-phosphate: a prototype of a new class of second messengers. J. Leukoc. Biol. 65:341-344.
59. Spiegel, S., O. Cuvillier, L. Edsall, T. Kohama, R. Menzeleev, A. Olivera, D. Thomas, Z. Tu, J. Van Brocklyn, and F. Wang. 1998. Roles of sphingosine-1-phosphate in cell growth, differentiation, and death. Biochemistry (Mosc.). 63:69-73.
60. Spiegel, S., D. Foster, and R.N. Kolesnick. 1996. Signal transduction through lipid second messengers. Curr. Opin. Cell Biol. 8:159-167.
61. Spiegel, S., and A.H. Merrill, Jr. 1996. Sphingolipid metabolism and cell growth regulation. FASEB J. 10:1388-1397.
62. Stoffel, W., B. Hellenbroich, and G. Heimann. 1973. Properties and specificities of sphingosine kinase from blood platelets. Hoppe-Seyler's Z. Physiol. Chem. 354:1311-1316.
63. Su, Y., D. Rosenthal, M. Smulson, and S. Spiegel. 1994. Sphingosine 1-phosphate, a novel signaling molecule, stimulates DNA binding activity of AP-1 in quiescent Swiss 3T3 fibroblasts. J. Biol. Chem. 269:16512-16517.
64. Thornberry, N.A., and Y. Lazebnik. 1998. Caspases: enemies within. Science. 281:1312-1316.
65. Topham, M.K., M. Bunting, G.A. Zimmerman, T.M. McIntyre, P.J. Blackshear, and S.M. Prescott. 1998. Protein kinase C regulates the nuclear localization of diacylglycerol kinase-ζ. Nature. 394:697-700.
66. i-coupled orphan receptor edg-1 and intracellular to regulate proliferation and survival. J. Cell Biol. 142:229-240.
67. Van Brocklyn, J.R., Z. Tu, L. Edsall, R.R. Schmidt, and S. Spiegel. 1999. Sphingosine 1-phosphate-induced cell rounding and neurite retraction are mediated by the G protein-coupled receptor H218. J. Biol. Chem. 274:4626-4632.
68. i protein-coupled plasma membrane receptor by sphingosine-1-phosphate. J. Biol. Chem. 271:2082-2087.
69. Van Veldhoven, P.P., and G.P. Mannaerts. 1991. Subcellular localization and membrane topology of sphingosine-1-phosphate lyase in rat liver. J. Biol. Chem. 266:12502-12507.
70. Van Veldhoven, P.P., and G.P. Mannaerts. 1994. Sphinganine 1-phosphate metabolism in cultured skin fibroblasts: evidence for the existence of a sphingosine phosphatase. Biochem. J. 299:597-601.
71. Wang, F., K. Nohara, O. Olivera, E.W. Thompson, and S. Spiegel. 1999a. Involvement of focal adhesion kinase in inhibition of motility of human breast cancer cells by sphingosine 1-phosphate. Exp. Cell Res. 247:17-28.
72. 0-coupled cell surface receptor: potential involvement in angiogencsis. J. Biol. Chem. In press.
73. Xia, P., J.R. Gamble, KA. Rye, L. Wang, C.S.T. Hii, P. Cockerill, Y. Khew-Goodall, A.G. Bert, P.J. Barter, and M.A. Vadas. 1998. Tumor necrosis factor-α induces adhesion molecule expression through the sphingosine kinase pathway. Proc. Natl. Acad. Sci. USA. 95:14196-14201.
74. Yamamura, S., Y. Yatomi, F. Ruan, E.A. Sweeney, S. Hakomori, and Y. Igarashi. 1997. Sphingosine 1-phosphate regulates melanoma cell motility through a receptor-coupled extracellular action and in a pertussis toxin-insensitive manner. Biochemistry. 36:10751-10759.
75. Yatomi, Y., Y. Igarashi, L. Yang, N. Hisano, R. Qi, N. Asazuma, K. Satoh, Y. Ozaki, and S. Kume. 1997a. Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J. Biochem. 121:969-973.
76. Yatomi, Y., F. Ruan, S. Hakomori, and Y. Igarashi. 1995. Sphingosine-1-phosphate: a platelet-activating sphingolipid released from agonist-stimulated human platelets. Blood. 86:193-202.
77. Yatomi, Y., S. Yamamura, F. Ruan, and Y. Igarashi. 1997b. Sphingosine 1-phospliate induces platelet activation through an extracellular action and shares a platelet surface receptor with lysophosphatidic acid. J. Biol. Chem. 272: 5291-5297.
78. Zhang, H., N.N. Desai, A. Olivera, T. Seki, G. Brooker, and S. Spiegel. 1991. Sphingosine-1-phosphate, a novel lipid, involved in cellular proliferation. J. Cell Biol. 114:155-167.
79. Zhou, J., and J.D. Saba. 1998. Identification of the first mammalian sphingosine phosphate lyase gene and its functional expression in yeast. Biochem. Biophys. Res. Commun. 242:502-507.
80. Zondag, G.C.M., F.R. Postma, I.V. Etten, I. Verlaan, and W.H. Moolenaar. 1998. Sphingosine 1-phosphate signalling through the G-protein-coupled receptor Edg-1. Biochem. J. 330:605-609.