Sphingosine Kinases: Emerging Structure-Function Insights

Trends in Biochemical Sciences

Volumn 41, Issue 5, 2016, Pages 395-409

  Adams, David R ^a   Pyne, Susan ^b   Pyne, Nigel J ^b  

^a HERIOT WATT UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

DAGK_cat; Diacylglycerol kinase (DGK); Membrane curvature; SK2); Sphingosine kinase (SK1; TRAF2

Indexed keywords

PHOSPHOLIPID; PROTEIN; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; ISOENZYME; LYSOPHOSPHOLIPID; PHOSPHOTRANSFERASE; PROTEIN BINDING; SPHINGOSINE 1-PHOSPHATE; SPHINGOSINE KINASE 2, HUMAN;

CATALYSIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME REGULATION; HUMAN; IMMUNE SYSTEM; MOLECULAR INTERACTION; PHOSPHORYLATION; PLASTICITY; PRIORITY JOURNAL; PROKARYOTE; REVIEW; STRUCTURE ACTIVITY RELATION; ALPHA HELIX; ALTERNATIVE RNA SPLICING; ANALOGS AND DERIVATIVES; BETA SHEET; CHEMISTRY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; METABOLISM; MOLECULAR DOCKING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

ALTERNATIVE SPLICING; AMINO ACID MOTIFS; CATALYTIC DOMAIN; HUMANS; ISOENZYMES; LYSOPHOSPHOLIPIDS; MOLECULAR DOCKING SIMULATION; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SPHINGOSINE; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84961825588     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2016.02.007     Document Type: Review

References (73)

1. Blaho V.A., Hla T. Regulation of mammalian physiology, development, and disease by the sphingosine 1-phosphate and lysophosphatidic acid receptors. Chem. Rev. 2011, 111:6299-6320.
2. Spiegel S., Milstien S. The outs and the ins of sphingosine-1-phosphate in immunity. Nat. Rev. Immunol. 2011, 11:403-415.
3. Maceyka M., Spiegel S. Sphingolipid metabolites in inflammatory disease. Nature 2014, 510:58-67.
4. Pyne S., Pyne N.J. Translational aspects of sphingosine 1-phosphate biology. Trends Mol. Med. 2011, 17:463-472.
5. Kunkel G.T., et al. Targeting the sphingosine-1-phosphate axis in cancer, inflammation and beyond. Nat. Rev. Drug Discov. 2013, 12:688-702.
6. Kihara Y., et al. Lysophospholipid receptor nomenclature review: IUPHAR Review 8. Br. J. Pharmacol. 2014, 171:3575-3594.
7. Hait N.C., et al. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 2009, 325:1254-1257.
8. Panneer Selvam S., et al. Binding of the sphingolipid S1P to hTERT stabilizes telomerase at the nuclear periphery by allosterically mimicking protein phosphorylation. Sci. Signal. 2015, 8:ra58.
9. Chan H., Pitson S.M. Post-translational regulation of sphingosine kinases. Biochim. Biophys. Acta 2013, 1831:147-156.
10. Neubauer H.A., Pitson S.M. Roles, regulation and inhibitors of sphingosine kinase 2. FEBS J. 2013, 280:5317-5336.
11. Hannun Y.A., Obeid L.M. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 2008, 9:139-150.
12. Pyne S., et al. 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. Eur. J. Biochem. 1996, 237:819-826.
13. Cuvillier O., et al. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 1996, 381:800-803.
14. Pyne S., et al. Role of sphingosine kinases and lipid phosphate phosphatases in regulating spatial sphingosine 1-phosphate signalling in health and disease. Cell. Signal. 2009, 21:14-21.
15. Newton J., et al. Revisiting the sphingolipid rheostat: evolving concepts in cancer therapy. Exp. Cell Res. 2015, 333:195-200.
16. Hannun Y.A., Obeid L.M. Many ceramides. J. Biol. Chem. 2011, 286:27855-27862.
17. Saddoughi S.A., Ogretmen B. Diverse functions of ceramide in cancer cell death and proliferation. Adv. Cancer Res. 2013, 117:37-58.
18. Santos W.L., Lynch K.R. Drugging sphingosine kinases. ACS Chem. Biol. 2015, 10:225-233.
19. Pyne N.J., Pyne S. Sphingosine 1-phosphate and cancer. Nat. Rev. Cancer 2010, 10:489-503.
20. Long J.S., et al. Sphingosine kinase 1 induces tolerance to human epidermal growth factor receptor 2 and prevents formation of a migratory phenotype in response to sphingosine 1-phosphate in estrogen receptor-positive breast cancer cells. Mol. Cell. Biol. 2010, 30:3827-3841.
21. Gao P., Smith C.D. Ablation of sphingosine kinase-2 inhibits tumor cell proliferation and migration. Mol. Cancer Res. 2011, 9:1509-1519.
22. Wallington-Beddoe C.T., et al. Sphingosine kinase 2 promotes acute lymphoblastic leukemia by enhancing MYC expression. Cancer Res. 2014, 74:2803-2815.
23. Wang Z., et al. Molecular basis of sphingosine kinase 1 substrate recognition and catalysis. Structure 2013, 21:798-809.
24. Gustin D.J., et al. Structure guided design of a series of sphingosine kinase (SphK) inhibitors. Bioorg. Med. Chem. Lett. 2013, 23:4608-4616.
25. Wang J., et al. Crystal structure of sphingosine kinase 1 with PF-543. ACS Med. Chem. Lett. 2014, 5:1329-1333.
26. Pitson S.M., et al. Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 2003, 22:5491-5500.
27. Hait N.C., et al. Sphingosine kinase type 2 activation by ERK-mediated phosphorylation. J. Biol. Chem. 2007, 282:12058-12065.
28. Topham M.K., Epand R.M. Mammalian diacylglycerol kinases: molecular interactions and biological functions of selected isoforms. Biochim. Biophys. Acta 2009, 1790:416-424.
29. Waggoner D.W., et al. MuLK, a eukaryotic multi-substrate lipid kinase. J. Biol. Chem. 2004, 279:38228-38235.
30. Spiegel S., Milstien S. Functions of the multifaceted family of sphingosine kinases and some close relatives. J. Biol. Chem. 2007, 282:2125-2129.
31. Zhang Y.M., Rock C.O. Membrane lipid homeostasis in bacteria. Nat. Rev. Microbiol. 2008, 6:222-233.
32. Bakali H.M., et al. Crystal structure of YegS, a homologue to the mammalian diacylglycerol kinases, reveals a novel regulatory metal binding site. J. Biol. Chem. 2007, 282:19644-19652.
33. Nichols C.E., et al. Characterization of Salmonella typhimurium YegS, a putative lipid kinase homologous to eukaryotic sphingosine and diacylglycerol kinases. Proteins 2007, 68:13-25.
34. Miller D.J., et al. Analysis of the Staphylococcus aureus DgkB structure reveals a common catalytic mechanism for the soluble diacylglycerol kinases. Structure 2008, 16:1036-1046.
35. Emptage R.P., et al. Structural basis of lipid binding for the membrane-embedded tetraacyldisaccharide-1-phosphate 4'-kinase LpxK. J. Biol. Chem. 2014, 289:24059-24068.
36. Liu Z., et al. Synthesis of (S)-FTY720 vinylphosphonate analogues and evaluation of their potential as sphingosine kinase 1 inhibitors and activators. Bioorg. Med. Chem. 2013, 21:2503-2510.
37. Lim K.G., et al. 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. 2011, 286:18633-18640.
38. Kihara A., et al. Mouse sphingosine kinase isoforms SPHK1a and SPHK1b differ in enzymatic traits including stability, localization, modification, and oligomerization. J. Biol. Chem. 2006, 281:4532-4539.
39. Wattenberg B.W., et al. The sphingosine and diacylglycerol kinase superfamily of signaling kinases: localization as a key to signaling function. J. Lipid Res. 2006, 47:1128-1139.
40. Wattenberg B.W. Role of sphingosine kinase localization in sphingolipid signaling. World J. Biol. Chem. 2010, 1:362-368.
41. Siow D., Wattenberg B. The compartmentalization and translocation of the sphingosine kinases: mechanisms and functions in cell signaling and sphingolipid metabolism. Crit. Rev. Biochem. Mol. Biol. 2011, 46:365-375.
42. Siow D.L., et al. Sphingosine kinase localization in the control of sphingolipid metabolism. Adv. Enzyme Regul. 2011, 51:229-244.
43. Pitson S.M. Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem. Sci. 2011, 36:97-107.
44. Pitson S.M., et al. Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J. Exp. Med. 2005, 201:49-54.
45. Olivera A., Spiegel S. Sphingosine-1-phosphate as second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 1993, 365:557-560.
46. Rius R.A., et al. Activation of sphingosine kinase in pheochromocytoma PC12 neuronal cells in response to trophic factors. FEBS Lett. 1997, 417:173-176.
47. Xia P., et al. Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:14196-14201.
48. 2+ signalling by epidermal growth factor receptor. FEBS Lett. 1999, 461:217-222.
49. Alemany R., et al. Formyl peptide receptor signaling in HL-60 cells through sphingosine kinase. J. Biol. Chem. 1999, 274:3994-3999.
50. 2+ mobilization in human SH-SY5Y neuroblastoma cells is independent of phosphoinositide signalling, but dependent on sphingosine kinase activation. Biochem. J. 1999, 343:45-52.
51. Meyer zu Heringdorf D., et al. Stimulation of intracellular sphingosine-1-phosphate production by G-protein-coupled sphingosine-1-phosphate receptors. Eur. J. Pharmacol. 2001, 414:145-154.
52. Blaukat A., Dikic I. Activation of sphingosine kinase by the bradykinin B2 receptor and its implication in regulation of the ERK/MAP kinase pathway. Biol. Chem. 2001, 382:135-139.
53. Shu X., et al. Sphingosine kinase mediates vascular endothelial growth factor-induced activation of ras and mitogen-activated protein kinases. Mol. Cell. Biol. 2002, 22:7758-7768.
54. MacKinnon A.C., et al. Sphingosine kinase: a point of convergence in the action of diverse neutrophil priming agents. J. Immunol. 2002, 169:6394-6400.
55. Mastrandrea L.D., et al. Sphingosine kinase activity and sphingosine-1 phosphate production in rat pancreatic islets and INS-1 cells: response to cytokines. Diabetes 2005, 54:1429-1436.
56. 2+/calmodulin-dependent translocation of sphingosine kinase: role in plasma membrane relocation but not activation. Cell Calcium 2003, 33:119-128.
57. Johnson K.R., et al. PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA). J. Biol. Chem. 2002, 277:35257-35262.
58. Rosenfeldt H.M., et al. EDG-1 links the PDGF receptor to Src and focal adhesion kinase activation leading to lamellipodia formation and cell migration. FASEB J. 2001, 15:2649-2659.
59. 2+ signals, enzyme release, cytokine production, and chemotaxis. J. Immunol. 2004, 173:1596-1603.
60. Barr R.K., et al. Deactivation of sphingosine kinase 1 by protein phosphatase 2A. J. Biol. Chem. 2008, 283:34994-35002.
61. Olivera A., et al. Effect of acidic phospholipids on sphingosine kinase. J. Cell. Biochem. 1996, 60:529-537.
62. Stahelin R.V., et al. The mechanism of membrane targeting of human sphingosine kinase 1. J. Biol. Chem. 2005, 280:43030-43038.
63. Delon C., et al. Sphingosine kinase 1 is an intracellular effector of phosphatidic acid. J. Biol. Chem. 2004, 279:44763-44774.
64. Hengst J.A., et al. Sphingosine kinase 1 localized to the plasma membrane lipid raft microdomain overcomes serum deprivation induced growth inhibition. Arch. Biochem. Biophys. 2009, 492:62-73.
65. Sutherland C.M., et al. 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.
66. Jarman K.E., et al. Translocation of sphingosine kinase 1 to the plasma membrane is mediated by calcium- and integrin-binding protein 1. J. Biol. Chem. 2010, 285:483-492.
67. Shen H., et al. Coupling between endocytosis and sphingosine kinase 1 recruitment. Nat. Cell Biol. 2014, 16:652-662.
68. Hengst J.A., et al. Enhancement of sphingosine kinase 1 catalytic activity by deletion of 21 amino acids from the COOH-terminus. Arch. Biochem. Biophys. 2010, 494:23-31.
69. q-mediated plasma membrane translocation of sphingosine kinase-1 and cross-activation of S1P receptors. Biochim. Biophys. Acta 2009, 1791:357-370.
70. Yamniuk A.P., et al. The interaction between calcium- and integrin-binding protein 1 and the αIIb integrin cytoplasmic domain involves a novel C-terminal displacement mechanism. J. Biol. Chem. 2006, 281:26455-26464.
71. 2+-CIB1 and their interactions with the platelet integrin αIIb cytoplasmic domain. J. Biol. Chem. 2011, 286:17181-17192.
72. Freeman T.C., et al. Identification of novel integrin binding partners for calcium and integrin binding protein 1 (CIB1): structural and thermodynamic basis of CIB1 promiscuity. Biochemistry 2013, 52:7082-7090.
73. Xia P., et al. Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J. Biol. Chem. 2002, 277:7996-8003.