Roles, regulation and inhibitors of sphingosine kinase 2

FEBS Journal

Volumn 280, Issue 21, 2013, Pages 5317-5336

  Neubauer, Heidi A ^a,b   Pitson, Stuart M ^a,b,c  

^a CENTRE FOR CANCER BIOLOGY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

apoptosis; cancer; inhibitors; phosphorylation; sphingolipids; sphingosine kinase 2; sphingosine 1 phosphate; subcellular localization

Indexed keywords

2 ( 4 HYDROXYANILINO) 4 (4 CHLOROPHENYL)THIAZOLE; 2 [3 (4 OCTYLPHENYL) 1,2,4 OXADIAZOL 5 YL]PYRROLIDINE 1 ARBOXIMIDAMIDE; 2 AMINO 3 (O METHYL) [2 (4' NOCTYLPHENYL)ETHYL]PROPANOL; 2 AMINO 4 (4 OCTYLPHENYL)BUTANE 1,3 DIOL; 3 (2 AMINOETHYL) 5 [3 (4 BUTOXYLPHENYL)PROPYLIDENE]THIAZOLIDINE 2,4 DIONE; 3 (4 CHLOROPHENYL)ADAMANTANE 1 CARBOXYLIC ACID(PYRIDIN 4 YLMETHYL)AMIDE; ABC 294640; ENZYME INHIBITOR; N,N,N TRIMETHYL 4(4 OCTYLPHENYL)CYCLOHEXANAMINIUM IODIDE; SLR 080811; SPHINGOLIPID; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1; SPHINGOSINE KINASE 2; SPHINGOSINE KINASE 2 INHIBITOR; UNCLASSIFIED DRUG;

APOPTOSIS; BREAST ADENOCARCINOMA; CANCER INHIBITION; CARCINOGENESIS; CATALYSIS; CELL FATE; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONFERENCE PAPER; CROHN DISEASE; DIABETIC RETINOPATHY; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME REGULATION; ENZYME SPECIFICITY; GROWTH INHIBITION; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; LEUKEMIA; MALIGNANT TRANSFORMATION; NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOARTHRITIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PROCESSING; REGULATORY MECHANISM; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; ULCERATIVE COLITIS;

APOPTOSIS; CANCER; INHIBITORS; PHOSPHORYLATION; SPHINGOLIPIDS; SPHINGOSINE KINASE 2; SPHINGOSINE-1-PHOSPHATE; SUBCELLULAR LOCALIZATION;

ANIMALS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN KINASE INHIBITORS;

EID: 84886101285     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12314     Document Type: Conference Paper

References (164)

1. Hannun YA, &, Obeid LM, (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9, 139-150.
2. Maceyka M, Milstien S, &, Spiegel S, (2009) Sphingosine-1-phosphate: the Swiss army knife of sphingolipid signaling. J Lipid Res 50, S272-S276.
3. Pitson SM, &, Pebay A, (2009) Regulation of stem cell pluripotency and neural differentiation by lysophospholipids. Neurosignals 17, 242-254.
4. Pitson SM, (2011) Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem Sci 36, 97-107.
5. Pitman MR, &, Pitson SM, (2010) Inhibitors of the sphingosine kinase pathway as potential therapeutics. Curr Cancer Drug Targets 10, 354-367.
6. Pyne NJ, &, Pyne S, (2010) Sphingosine 1-phosphate and cancer. Nat Rev Cancer 10, 489-503.
7. Gault CR, &, Obeid LM, (2011) Still benched on its way to the bedside: sphingosine kinase 1 as an emerging target in cancer chemotherapy. Crit Rev Biochem Mol Biol 46, 342-351.
8. Cuvillier O, Ader I, Bouquerel P, Brizuela L, Malavaud B, Mazerolles C, &, Rischmann P, (2010) Activation of sphingosine kinase-1 in cancer: implications for therapeutic targeting. Curr Mol Pharmacol 3, 53-65.
9. Edmonds Y, Milstien S, &, Spiegel S, (2011) Development of small-molecule inhibitors of sphingosine-1-phosphate signaling. Pharmacol Ther 132, 352-360.
10. Strub GM, Maceyka M, Hait NC, Milstien S, &, Spiegel S, (2010) Extracellular and intracellular actions of sphingosine-1-phosphate. Adv Exp Med Biol 688, 141-155.
11. Yatomi Y, Igarashi Y, Yang L, Hisano N, Qi R, Asazuma N, Satoh K, Ozaki Y, &, Kume S, (1997) Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J Biochem 121, 969-973.
12. Sensken SC, Bode C, Nagarajan M, Peest U, Pabst O, &, Graler MH, (2010) Redistribution of sphingosine 1-phosphate by sphingosine kinase 2 contributes to lymphopenia. J Immunol 184, 4133-4142.
13. Sato K, Malchinkhuu E, Horiuchi Y, Mogi C, Tomura H, Tosaka M, Yoshimoto Y, Kuwabara A, &, Okajima F, (2007) Critical role of ABCA1 transporter in sphingosine 1-phosphate release from astrocytes. J Neurochem 103, 2610-2619.
14. Takabe K, Kim RH, Allegood JC, Mitra P, Ramachandran S, Nagahashi M, Harikumar KB, Hait NC, Milstien S, &, Spiegel S, (2010) Estradiol induces export of sphingosine 1-phosphate from breast cancer cells via ABCC1 and ABCG2. J Biol Chem 285, 10477-10786.
15. Hisano Y, Kobayashi N, Yamaguchi A, &, Nishi T, (2012) Mouse SPNS2 functions as a sphingosine-1-phosphate transporter in vascular endothelial cells. PLoS One 7, e38941.
16. Chun J, Hla T, Lynch KR, Spiegel S, &, Moolenaar WH, (2010) International Union of Basic and Clinical Pharmacology. LXXVIII. Lysophospholipid receptor nomenclature. Pharmacol Rev 62, 579-587.
17. Hanson MA, Roth CB, Jo E, Griffith MT, Scott FL, Reinhart G, Desale H, Clemons B, Cahalan SM, Schuerer SC, et al,. (2012) Crystal structure of a lipid G protein-coupled receptor. Science 335, 851-855.
18. Meyer zu Heringdorf D, &, Jakobs KH, (2007) Lysophospholipid receptors: signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim Biophys Acta 1768, 923-940.
19. Rosen H, Gonzalez-Cabrera PJ, Sanna MG, &, Brown S, (2009) Sphingosine 1-phosphate receptor signaling. Annu Rev Biochem 78, 743-768.
20. Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, Singh SK, Luo C, Marmorstein R, Kordula T, Milstien S, et al,. (2009) Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325, 1254-1257.
21. Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, Kim EY, Maceyka M, Jiang H, Luo C, Kordula T, et al,. (2010) Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465, 1084-1088.
22. Strub GM, Paillard M, Liang J, Gomez L, Allegood JC, Hait NC, Maceyka M, Price MM, Chen Q, Simpson DC, et al,. (2011) Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate complex IV assembly and respiration. FASEB J 25, 600-612.
23. Maceyka M, Alvarez SE, Milstien S, &, Spiegel S, (2008) Filamin A links sphingosine kinase 1 and sphingosine-1-phosphate receptor 1 at lamellipodia to orchestrate cell migration. Mol Cell Biol 28, 5687-5697.
24. Chipuk JE, McStay GP, Bharti A, Kuwana T, Clarke CJ, Siskind LJ, Obeid LM, &, Green DR, (2012) Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis. Cell 148, 988-1000.
25. Spiegel S, &, Milstien S, (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 4, 397-407.
26. Pebay A, Bonder CS, &, Pitson SM, (2007) Stem cell regulation by lysophospholipids. Prostaglandins Other Lipid Mediat 84, 83-97.
27. Gillies L, Lee SC, Long JS, Ktistakis N, Pyne NJ, &, Pyne S, (2009) The sphingosine 1-phosphate receptor 5 and sphingosine kinases 1 and 2 are localised in centrosomes: possible role in regulating cell division. Cell Signal 21, 675-684.
28. Chalfant CE, Szulc Z, Roddy P, Bielawska A, &, Hannun YA, (2004) The structural requirements for ceramide activation of serine-threonine protein phosphatases. J Lipid Res 45, 496-506.
29. Perry DM, Kitatani K, Roddy P, El-Osta M, &, Hannun YA, (2012) Identification and characterization of protein phosphatase 2C activation by ceramide. J Lipid Res 53, 1513-1521.
30. Muller G, Ayoub M, Storz P, Rennecke J, Fabbro D, &, Pfizenmaier K, (1995) PKCζ is a molecular switch in signal transduction of TNF-α, bifunctionally regulated by ceramide and arachidonic acid. EMBO J 14, 1961-1969.
31. Wang G, Silva J, Krishnamurthy K, Tran E, Condie BG, &, Bieberich E, (2005) Direct binding to ceramide activates protein kinase Cζ before the formation of a pro-apoptotic complex with PAR-4 in differentiating stem cells. J Biol Chem 280, 26415-26424.
32. Zhang Y, Yao B, Delikat S, Bayoumy S, Lin XH, Basu S, McGinley M, Chan-Hui PY, Lichenstein H, &, Kolesnick R, (1997) Kinase suppressor of Ras is ceramide-activated protein kinase. Cell 89, 63-72.
33. Heinrich M, Neumeyer J, Jakob M, Hallas C, Tchikov V, Winoto-Morbach S, Wickel M, Schneider-Brachert W, Trauzold A, Hethke A, et al,. (2004) Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and -3 activation. Cell Death Differ 11, 550-563.
34. Woodcock JM, Ma Y, Coolen C, Pham D, Jones C, Lopez AF, &, Pitson SM, (2010) Sphingosine and FTY720 directly bind pro-survival 14-3-3 proteins to regulate their function. Cell Signal 22, 1291-1299.
35. Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind JS, &, Spiegel S, (1996) Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 381, 800-803.
36. Taha TA, Hannun YA, &, Obeid LM, (2006) Sphingosine kinase: biochemical and cellular regulation and role in disease. J Biochem Mol Biol 39, 113-131.
37. Pitson SM, Powell JA, &, Bonder CS, (2011) Regulation of sphingosine kinase in hematological malignancies and other cancers. Anticancer Agents Med Chem 11, 799-809.
38. Liu H, Sugiura M, Nava VE, Edsall LC, Kono K, Poulton S, Milstien S, Kohama T, &, Spiegel S, (2000) Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J Biol Chem 275, 19513-19520.
39. Leclercq TM, &, Pitson SM, (2006) Cellular signalling by sphingosine kinase and sphingosine 1-phosphate. IUBMB Life 58, 467-472.
40. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, Latham V, &, Sullivan M, (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40, D261-D270.
41. Chen R-Q, Yang Q-K, Lu B-W, Yi W, Cantin G, Chen Y-I, Fearns C, Yates JR, &, Lee J-D, (2009) CDC25B mediates rapamycin-induced oncogenic responses in cancer cells. Cancer Res 69, 2663-2668.
42. Daub H, Olsen JV, Bairlein M, Gnad F, Oppermann FS, Korner R, Greff Z, Keri G, Stemmann O, &, Mann M, (2008) Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol Cell 31, 438-448.
43. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, &, Gygi SP, (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105, 10762-10767.
44. Christensen GL, Kelstrup CD, Lyngso C, Sarwar U, Bogebo R, Sheikh SP, Gammeltoft S, Olsen JV, &, Hansen JL, (2010) Quantitative phosphoproteomics dissection of seven-transmembrane receptor signaling using full and biased agonists. Mol Cell Proteomics 9, 1540-1553.
45. Ding G, Sonoda H, Yu H, Kajimoto T, Goparaju SK, Jahangeer S, Okada T, &, Nakamura S, (2007) Protein kinase D-mediated phosphorylation and nuclear export of sphingosine kinase 2. J Biol Chem 282, 27493-27502.
46. Hait NC, Bellamy A, Milstien S, Kordula T, &, Spiegel S, (2007) Sphingosine kinase type 2 activation by ERK-mediated phosphorylation. J Biol Chem 282, 12058-12065.
47. Gao P, Peterson YK, Smith RA, &, Smith CD, (2012) Characterization of isoenzyme-selective inhibitors of human sphingosine kinases. PLoS One 7, e44543.
48. French KJ, Zhuang Y, Maines LW, Gao P, Wang W, Beljanski V, Upson JJ, Green CL, Keller SN, &, Smith CD, (2010) Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J Pharmacol Exp Ther 333, 129-139.
49. Maceyka M, Sankala H, Hait NC, Le Stunff H, Liu H, Toman R, Collier C, Zhang M, Satin LS, Merrill AH, et al,. (2005) SphK1 and SphK2, sphingosine kinase isoenzymes with opposing functions in sphingolipid metabolism. J Biol Chem 280, 37118-37129.
50. Pitson SM, Moretti PAB, Zebol JR, Xia P, Gamble JR, Vadas MA, D'Andrea RJ, &, Wattenberg BW, (2000) Expression of a catalytically inactive sphingosine kinase mutant blocks agonist-induced sphingosine kinase activation: a dominant-negative sphingosine kinase. J Biol Chem 275, 33945-33950.
51. Pitson SM, Moretti PA, Zebol JR, Zareie R, Derian CK, Darrow AL, Qi J, D'Andrea RJ, Bagley CJ, Vadas MA, et al,. (2002) The nucleotide-binding site of human sphingosine kinase 1. J Biol Chem 277, 49545-49553.
52. Pitson SM, D'Andrea RJ, Vandeleur L, Moretti PA, Xia P, Gamble JR, Vadas MA, &, Wattenberg BW, (2000) Human sphingosine kinase: purification, molecular cloning and characterization of the native and recombinant enzymes. Biochem J 350, 429-441.
53. Pitman MR, Pham DH, &, Pitson SM, (2012) Isoform-selective assays for sphingosine kinase activity. Methods Mol Biol 874, 21-31.
54. Kono K, Sugiura M, &, Kohama T, (2002) Inhibition of recombinant sphingosine kinases by novel inhibitors of microbial origin, F-12509A and B-5354c. J Antibiot 55, 99-103.
55. Chan HS, &, Pitson SM, (2013) Post-translational regulation of sphingosine kinases. Biochim Biophys Acta 1831, 147-156.
56. Melendez AJ, Carlos-Dias E, Gosink M, Allen JM, &, Takacs L, (2000) Human sphingosine kinase: molecular cloning, functional characterization and tissue distribution. Gene 251, 19-26.
57. Olivera A, Kohama T, Edsall L, Nava V, Cuvillier O, Poulton S, &, Spiegel S, (1999) Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J Cell Biol 147, 545-557.
58. Xia P, Gamble JR, Wang L, Pitson SM, Moretti PA, Wattenberg BW, D'Andrea RJ, &, Vadas MA, (2000) An oncogenic role of sphingosine kinase. Curr Biol 10, 1527-1530.
59. French KJ, Schrecengost RS, Lee BD, Zhuang Y, Smith SN, Eberly JL, Yun JK, &, Smith CD, (2003) Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res 63, 5962-5969.
60. Bayerl MG, Bruggeman RD, Conroy EJ, Hengst JA, King TS, Jimenez M, Claxton DF, &, Yun JK, (2008) Sphingosine kinase 1 protein and mRNA are overexpressed in non-Hodgkin lymphomas and are attractive targets for novel pharmacological interventions. Leuk Lymphoma 49, 948-954.
61. Malavaud B, Pchejetski D, Mazerolles C, de Paiva GR, Calvet C, Doumerc N, Pitson S, Rischmann P, &, Cuvillier O, (2010) Sphingosine kinase-1 activity and expression in human prostate cancer resection specimens. Eur J Cancer 46, 3417-3424.
62. Li J, Guan HY, Gong LY, Song LB, Zhang N, Wu J, Yuan J, Zheng YJ, Huang ZS, &, Li M, (2008) Clinical significance of sphingosine kinase-1 expression in human astrocytomas progression and overall patient survival. Clin Cancer Res 14, 6996-7003.
63. Van Brocklyn JR, Jackson CA, Pearl DK, Kotur MS, Snyder PJ, &, Prior TW, (2005) Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme: roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J Neuropathol Exp Neurol 64, 695-705.
64. Kawamori T, Osta W, Johnson KR, Pettus BJ, Bielawski J, Tanaka T, Wargovich MJ, Reddy BS, Hannun YA, Obeid LM, et al,. (2006) Sphingosine kinase 1 is up-regulated in colon carcinogenesis. FASEB J 20, 386-388.
65. Johnson KR, Johnson KY, Crellin HG, Ogretmen B, Boylan AM, Harley RA, &, Obeid LM, (2005) Immunohistochemical distribution of sphingosine kinase 1 in normal and tumor lung tissue. J Histochem Cytochem 53, 1159-1166.
66. Li W, Yu CP, Xia JT, Zhang L, Weng GX, Zheng HQ, Kong QL, Hu LJ, Zeng MS, Zeng YX, et al,. (2009) Sphingosine kinase 1 is associated with gastric cancer progression and poor survival of patients. Clin Cancer Res 15, 1393-1399.
67. Ruckhaberle E, Rody A, Engels K, Gaetje R, von Minckwitz G, Schiffmann S, Grosch 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.
68. Liu G, Zheng H, Zhang Z, Wu Z, Xiong H, Li J, &, Song L, (2010) Overexpression of sphingosine kinase 1 is associated with salivary gland carcinoma progression and might be a novel predictive marker for adjuvant therapy. BMC Cancer 10, 495.
69. Pan J, Tao YF, Zhou Z, Cao BR, Wu SY, Zhang YL, Hu SY, Zhao WL, Wang J, Lou GL, et al,. (2011) An novel role of sphingosine kinase-1 (SPHK1) in the invasion and metastasis of esophageal carcinoma. J Transl Med 9, 157.
70. Facchinetti MM, Gandini NA, Fermento ME, Sterin-Speziale NB, Ji Y, Patel V, Gutkind JS, Rivadulla MG, &, Curino AC, (2010) The expression of sphingosine kinase-1 in head and neck carcinoma. Cells Tissues Organs 192, 314-324.
71. Sinha UK, Schorn VJ, Hochstim C, Chinn SB, Zhu S, &, Masood R, (2011) Increased radiation sensitivity of head and neck squamous cell carcinoma with sphingosine kinase 1 inhibition. Head Neck 33, 178-188.
72. Long JS, Edwards J, Watson C, Tovey S, Mair KM, Schiff R, Natarajan V, Pyne NJ, &, Pyne S, (2010) 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 30, 3827-3841.
73. Kohno M, Momoi M, Oo ML, Paik JH, Lee YM, Venkataraman K, Ai Y, Ristimaki AP, Fyrst H, Sano H, et al,. (2006) Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol Cell Biol 26, 7211-7223.
74. Endo K, Igarashi Y, Nisar M, Zhou QH, &, Hakomori S, (1991) Cell membrane signaling as target in cancer therapy: inhibitory effect of N, N-dimethyl and N, N, N-trimethyl sphingosine derivatives on in vitro and in vivo growth of human tumor cells in nude mice. Cancer Res 51, 1613-1618.
75. Park YS, Hakomori S, Kawa S, Ruan F, &, Igarashi Y, (1994) Liposomal N, N, N-trimethylsphingosine (TMS) as an inhibitor of B16 melanoma cell growth and metastasis with reduced toxicity and enhanced drug efficacy compared to free TMS: cell membrane signaling as a target in cancer therapy III. Cancer Res 54, 2213-2217.
76. French KJ, Upson JJ, Keller SN, Zhuang Y, Yun JK, &, Smith CD, (2006) Antitumor activity of sphingosine kinase inhibitors. J Pharmacol Exp Ther 318, 596-603.
77. Pchejetski D, Doumerc N, Golzio M, Naymark M, Teissie J, Kohama T, Waxman J, Malavaud B, &, Cuvillier O, (2008) Chemosensitizing effects of sphingosine kinase-1 inhibition in prostate cancer cell and animal models. Mol Cancer Ther 7, 1836-1845.
78. Kawamori T, Kaneshiro T, Okumura M, Maalouf S, Uflacker A, Bielawski J, Hannun YA, &, Obeid LM, (2009) Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J 23, 405-414.
79. Ponnusamy S, Selvam SP, Mehrotra S, Kawamori T, Snider AJ, Obeid LM, Shao Y, Sabbadini R, &, Ogretmen B, (2012) Communication between host organism and cancer cells is transduced by systemic sphingosine kinase 1/sphingosine 1-phosphate signalling to regulate tumour metastasis. EMBO Mol Med 4, 761-775.
80. Shirai K, Kaneshiro T, Wada M, Furuya H, Bielawski J, Hannun YA, Obeid LM, Ogretmen B, &, Kawamori T, (2011) A role of sphingosine kinase 1 in head and neck carcinogenesis. Cancer Prev Res 4, 454-462.
81. Pitson SM, Xia P, Leclercq TM, Moretti PAB, Zebol JR, Lynn HE, Wattenberg BW, &, Vadas MA, (2005) Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J Exp Med 201, 49-54.
82. Jarman KE, Moretti PAB, Zebol JR, &, Pitson SM, (2010) Translocation of sphingosine kinase 1 to the plasma membrane is mediated by calcium- and integrin-binding protein 1. J Biol Chem 285, 483-492.
83. Pitson SM, Moretti PAB, Zebol JR, Lynn HE, Xia P, Vadas MA, &, Wattenberg BW, (2003) Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J 22, 5491-5500.
84. Gault CR, Eblen ST, Neumann CA, Hannun YA, &, Obeid LM, (2012) Oncogenic K-Ras regulates bioactive sphingolipids in a sphingosine kinase 1-dependent manner. J Biol Chem 287, 31794-31803.
85. q- mediated plasma membrane translocation of sphingosine kinase-1 and cross-activation of S1P receptors. Biochim Biophys Acta 1791, 357-370.
86. Okada T, Ding G, Sonoda H, Kajimoto T, Haga Y, Khosrowbeygi A, Gao SY, Miwa N, Jahangeer S, &, 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.
87. Igarashi N, Okada T, Hayashi S, Fujita T, Jahangeer S, &, Nakamura S, (2003) Sphingosine kinase 2 is a nuclear protein and inhibits DNA synthesis. J Biol Chem 278, 46832-46839.
88. Liu H, Toman RE, Goparaju SK, Maceyka M, Nava VE, Sankala H, Payne SG, 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.
89. Hofmann LP, Ren S, Schwalm S, Pfeilschifter J, &, 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.
90. Sankala HM, Hait NC, Paugh SW, Shida D, Lepine S, Elmore LW, Dent P, Milstien S, &, Spiegel S, (2007) Involvement of sphingosine kinase 2 in p53-independent induction of p21 by the chemotherapeutic drug doxorubicin. Cancer Res 67, 10466-10474.
91. Schnitzer SE, Weigert A, Zhou J, &, Brune B, (2009) Hypoxia enhances sphingosine kinase 2 activity and provokes sphingosine-1-phosphate-mediated chemoresistance in A549 lung cancer cells. Mol Cancer Res 7, 393-401.
92. Nemoto S, Nakamura M, Osawa Y, Kono S, Itoh Y, Okano Y, Murate T, Hara A, Ueda H, Nozawa Y, et al,. (2009) Sphingosine kinase isoforms regulate oxaliplatin sensitivity of human colon cancer cells through ceramide accumulation and Akt activation. J Biol Chem 284, 10422-10432.
93. Sun DF, Gao ZH, Liu HP, Yuan Y, &, Qu XJ, (2012) Sphingosine 1-phosphate antagonizes the effect of all-trans retinoic acid (ATRA) in a human colon cancer cell line by modulation of RARβ expression. Cancer Lett 319, 182-189.
94. Zemann B, Urtz N, Reuschel R, Mechtcheriakova D, Bornancin F, Badegruber R, Baumruker T, &, Billich A, (2007) Normal neutrophil functions in sphingosine kinase type 1 and 2 knockout mice. Immunol Lett 109, 56-63.
95. Allende ML, Sasaki T, Kawai H, Olivera A, Mi YD, van Echten-Deckert G, Hajdu R, Rosenbach M, Keohane CA, Mandala S, et al,. (2004) Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 279, 52487-52492.
96. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, &, Proia RL, (2005) Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol 25, 11113-11121.
97. Gao P, &, Smith CD, (2011) Ablation of sphingosine kinase-2 inhibits tumor cell proliferation and migration. Mol Cancer Res 9, 1509-1519.
98. Weigert A, Schiffmann S, Sekar D, Ley S, Menrad H, Werno C, Grosch S, Geisslinger G, &, Brune B, (2009) Sphingosine kinase 2 deficient tumor xenografts show impaired growth and fail to polarize macrophages towards an anti-inflammatory phenotype. Int J Cancer 125, 2114-2121.
99. Antoon JW, White MD, Slaughter EM, Driver JL, Khalili HS, Elliott S, Smith CD, Burow ME, &, Beckman BS, (2011) Targeting NFκB mediated breast cancer chemoresistance through selective inhibition of sphingosine kinase-2. Cancer Biol Ther 11, 678-689.
100. Antoon JW, White MD, Driver JL, Burow ME, &, Beckman BS, (2012) Sphingosine kinase isoforms as a therapeutic target in endocrine therapy resistant luminal and basal-A breast cancer. Exp Biol Med 237, 832-844.
101. Beljanski V, Knaak C, Zhuang Y, &, Smith CD, (2011) Combined anticancer effects of sphingosine kinase inhibitors and sorafenib. Invest New Drugs 29, 1132-1142.
102. Beljanski V, Lewis CS, &, Smith CD, (2011) Antitumor activity of sphingosine kinase 2 inhibitor ABC294640 and sorafenib in hepatocellular carcinoma xenografts. Cancer Biol Ther 11, 524-534.
103. Chumanevich AA, Poudyal D, Cui X, Davis T, Wood PA, Smith CD, &, Hofseth LJ, (2010) Suppression of colitis-driven colon cancer in mice by a novel small molecule inhibitor of sphingosine kinase. Carcinogenesis 31, 1787-1793.
104. Miller AV, Alvarez SE, Spiegel S, &, Lebman DA, (2008) Sphingosine kinases and sphingosine-1-phosphate are critical for transforming growth factor β-induced extracellular signal-regulated kinase 1 and 2 activation and promotion of migration and invasion of esophageal cancer cells. Mol Cell Biol 28, 4142-4151.
105. Hait NC, Sarkar S, Le Stunff H, Mikami A, Maceyka M, Milstien S, &, Spiegel S, (2005) Role of sphingosine kinase 2 in cell migration toward epidermal growth factor. J Biol Chem 280, 29462-29469.
106. Xia P, Gamble JR, Rye KA, Wang L, Hii CS, Cockerill P, Khew-Goodall Y, Bert AG, Barter PJ, &, Vadas MA, (1998) Tumor necrosis factor-α induces adhesion molecule expression through the sphingosine kinase pathway. Proc Natl Acad Sci USA 95, 14196-141201.
107. Billich A, Bornancin F, Mechtcheriakova D, Natt F, Huesken D, &, Baumruker T, (2005) Basal and induced sphingosine kinase 1 activity in A549 carcinoma cells: function in cell survival and IL-1β and TNF-α induced production of inflammatory mediators. Cell Signal 17, 1203-1217.
108. Snider AJ, Orr Gandy KA, &, Obeid LM, (2010) Sphingosine kinase: role in regulation of bioactive sphingolipid mediators in inflammation. Biochimie 92, 707-715.
109. Lai WQ, Irwan AW, Goh HH, Melendez AJ, McInnes IB, &, Leung BP, (2009) Distinct roles of sphingosine kinase 1 and 2 in murine collagen-induced arthritis. J Immunol 183, 2097-2103.
110. Samy ET, Meyer CA, Caplazi P, Langrish CL, Lora JM, Bluethmann H, &, Peng SL, (2007) Cutting edge: modulation of intestinal autoimmunity and IL-2 signaling by sphingosine kinase 2 independent of sphingosine 1-phosphate. J Immunol 179, 5644-5648.
111. Maines LW, Fitzpatrick LR, French KJ, Zhuang Y, Xia Z, Keller SN, Upson JJ, &, Smith CD, (2008) Suppression of ulcerative colitis in mice by orally available inhibitors of sphingosine kinase. Dig Dis Sci 53, 997-1012.
112. Maines LW, Fitzpatrick LR, Green CL, Zhuang Y, &, Smith CD, (2010) Efficacy of a novel sphingosine kinase inhibitor in experimental Crohn's disease. Inflammopharmacology 18, 73-85.
113. Fitzpatrick LR, Green C, Frauenhoffer EE, French KJ, Zhuang Y, Maines LW, Upson JJ, Paul E, Donahue H, Mosher TJ, et al,. (2011) Attenuation of arthritis in rodents by a novel orally-available inhibitor of sphingosine kinase. Inflammopharmacology 19, 75-87.
114. Olivera A, Urtz N, Mizugishi K, Yamashita Y, Gilfillan AM, Furumoto Y, Gu H, Proia RL, Baumruker T, &, Rivera J, (2006) IgE-dependent activation of sphingosine kinases 1 and 2 and secretion of sphingosine 1-phosphate requires Fyn kinase and contributes to mast cell responses. J Biol Chem 281, 2515-2525.
115. Olivera A, Mizugishi K, Tikhonova A, Ciaccia L, Odom S, Proia RL, &, Rivera J, (2007) The sphingosine kinase-sphingosine-1-phosphate axis is a determinant of mast cell function and anaphylaxis. Immunity 26, 287-297.
116. Oskeritzian CA, Alvarez SE, Hait NC, Price MM, Milstien S, &, Spiegel S, (2008) Distinct roles of sphingosine kinases 1 and 2 in human mast-cell functions. Blood 111, 4193-4200.
117. Blom T, Slotte JP, Pitson SM, &, Tornquist K, (2005) Enhancement of intracellular sphingosine-1-phosphate production by inositol 1,4,5-trisphosphate-evoked calcium mobilisation in HEK-293 cells: endogenous sphingosine-1-phosphate as a modulator of the calcium response. Cell Signal 17, 827-836.
118. Mathes C, Fleig A, &, Penner R, (1998) Calcium release-activated calcium current (ICRAC) is a direct target for sphingosine. J Biol Chem 273, 25020-25030.
119. Kharel Y, Raje M, Gao M, Gellett AM, Tomsig JL, Lynch KR, &, Santos WL, (2012) Sphingosine kinase type 2 inhibition elevates circulating sphingosine 1-phosphate. Biochem J 447, 149-157.
120. Zemann B, Kinzel B, Muller M, Reuschel R, Mechtcheriakova D, Urtz N, Bornancin F, Baumruker T, &, Billich A, (2006) Sphingosine kinase type 2 is essential for lymphopenia induced by the immunomodulatory drug FTY720. Blood 107, 1454-1458.
121. Liang J, Nagahashi M, Kim EY, Harikumar KB, Yamada A, Huang WC, Hait NC, Allegood JC, Price MM, 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.
122. 3-mediated cardiac fibrosis in sphingosine kinase 1 transgenic mice involves reactive oxygen species. Cardiovasc Res 85, 484-493.
123. Yoshimoto T, Furuhata M, Kamiya S, Hisada M, Miyaji H, Magami Y, Yamamoto K, Fujiwara H, &, Mizuguchi J, (2003) Positive modulation of IL-12 signaling by sphingosine kinase 2 associating with the IL-12 receptor beta 1 cytoplasmic region. J Immunol 171, 1352-1359.
124. Takasugi N, Sasaki T, Suzuki K, Osawa S, Isshiki H, Hori Y, Shimada N, Higo T, Yokoshima S, Fukuyama T, et al,. (2011) BACE1 activity is modulated by cell-associated sphingosine-1-phosphate. J Neurosci 31, 6850-6857.
125. Jo SK, Bajwa A, Ye H, Vergis AL, Awad AS, Kharel Y, Lynch KR, &, Okusa MD, (2009) Divergent roles of sphingosine kinases in kidney ischemia-reperfusion injury. Kidney Int 75, 167-175.
126. Yung LM, Wei Y, Qin T, Wang YM, Smith CD, &, Waeber C, (2012) Sphingosine kinase 2 mediates cerebral preconditioning and protects the mouse brain against ischemic injury. Stroke 43, 199-204.
127. Wacker BK, Park TS, &, Gidday JM, (2009) Hypoxic preconditioning- induced cerebral ischemic tolerance role of microvascular sphingosine kinase 2. Stroke 40, 3342-3348.
128. Vessey DA, Li L, Jin Z-Q, Kelley M, Honbo N, Zhang J, &, Karliner JS, (2011) A sphingosine kinase form 2 knockout sensitizes mouse myocardium to ischemia/reoxygenation injury and diminishes responsiveness to ischemic preconditioning. Oxid Med Cell Longev 2011, 961059.
129. Gomez L, Paillard M, Price M, Chen Q, Teixeira G, Spiegel S, &, Lesnefsky EJ, (2011) A novel role for mitochondrial sphingosine-1-phosphate produced by sphingosine kinase-2 in PTP-mediated cell survival during cardioprotection. Basic Res Cardiol 106, 1341-1353.
130. Blondeau N, Lai YS, Tyndall S, Popolo M, Topalkara K, Pru JK, Zhang L, Kim H, Liao JK, Ding K, et al,. (2007) Distribution of sphingosine kinase activity and mRNA in rodent brain. J Neurochem 103, 509-517.
131. Shi YJ, Rehman H, Ramshesh VK, Schwartz J, Liu QL, Krishnasamy Y, Zhang X, Lemasters JJ, Smith CD, &, Zhong Z, (2012) Sphingosine kinase-2 inhibition improves mitochondrial function and survival after hepatic ischemia-reperfusion. J Hepatol 56, 137-145.
132. Fitzpatrick LR, Green C, Maines LW, &, Smith CD, (2011) Experimental osteoarthritis in rats is attenuated by ABC294640, a selective inhibitor of sphingosine kinase-2. Pharmacology 87, 135-143.
133. Maines LW, French KJ, Wolpert EB, Antonetti DA, &, Smith CD, (2006) Pharmacologic manipulation of sphingosine kinase in retinal endothelial cells: implications for angiogenic ocular diseases. Invest Ophthalmol Vis Sci 47, 5022-5031.
134. Mastrandrea LD, Sessanna SM, &, Laychock SG, (2005) Sphingosine kinase activity and sphingosine-1 phosphate production in rat pancreatic islets and INS-1 cells: response to cytokines. Diabetes 54, 1429-1436.
135. Leclercq TM, Moretti PAB, Vadas MA, &, Pitson SM, (2008) Eukaryotic elongation factor 1A interacts with sphingosine kinase and directly enhances its catalytic activity. J Biol Chem 283, 9606-9614.
136. Siow D, &, Wattenberg B, (2011) The compartmentalization and translocation of the sphingosine kinases: mechanisms and functions in cell signaling and sphingolipid metabolism. Crit Rev Biochem Mol Biol 46, 365-375.
137. Wattenberg BW, (2010) Role of sphingosine kinase localization in sphingolipid signaling. World J Biol Chem 1, 362-368.
138. Don AS, &, Rosen H, (2009) A lipid binding domain in sphingosine kinase 2. Biochem Biophys Res Commun 380, 87-92.
139. Siow DL, Anderson CD, Berdyshev EV, Skobeleva A, Pitson SM, &, Wattenberg BW, (2010) Intracellular localization of sphingosine kinase 1 alters access to substrate pools but does not affect the degradative fate of sphingosine-1-phosphate. J Lipid Res 51, z2546-2559.
140. Barth BM, Shanmugavelandy SS, Kaiser JM, McGovern C, Altinoglu EI, Haakenson JK, Hengst JA, Gilius EL, Knupp SA, Fox TE, et al,. (2013) PhotoImmunoNanoTherapy reveals an anticancer role for sphingosine kinase 2 and dihydrosphingosine-1-phosphate. ACS Nano 7, 2132-2144.
141. Weigert A, Cremer S, Schmidt MV, von Knethen A, Angioni C, Geisslinger G, &, Brune B, (2010) Cleavage of sphingosine kinase 2 by caspase-1 provokes its release from apoptotic cells. Blood 115, 3531-3540.
142. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, Villen J, Haas W, Sowa ME, &, Gygi SP, (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189.
143. Alemany R, van Koppen CJ, Danneberg K, Ter Braak M, &, Meyer Zu Heringdorf D, (2007) Regulation and functional roles of sphingosine kinases. Naunyn-Schmiedeberg's Arch Pharmacol 374, 413-428.
144. Billich A, Bornancin F, Devay P, Mechtcheriakova D, Urtz N, &, Baumruker T, (2003) Phosphorylation of the immunomodulatory drug FTY720 by sphingosine kinases. J Biol Chem 278, 47408-47415.
145. Yokota S, Taniguchi Y, Kihara A, Mitsutake S, &, Igarashi Y, (2004) Asp177 in C4 domain of mouse sphingosine kinase 1a is important for the sphingosine recognition. FEBS Lett 578, 106-110.
146. Roberts JL, Moretti PA, Darrow AL, Derian CK, Vadas MA, &, Pitson SM, (2004) An assay for sphingosine kinase activity using biotinylated sphingosine and streptavidin-coated membranes. Anal Biochem 331, 122-129.
147. Paugh SW, Payne SG, Barbour SE, Milstien S, &, Spiegel S, (2003) The immunosuppressant FTY720 is phosphorylated by sphingosine kinase type 2. FEBS Lett 554, 189-193.
148. Sanchez T, Estrada-Hernandez T, Paik JH, Wu MT, Venkataraman K, Brinkmann
149. Kharel Y, Lee S, Snyder AH, Sheasley-O'Neill SL, Morris MA, Setiady Y, Zhu R, Zigler MA, Burcin TL, Ley K, et al,. (2005) Sphingosine kinase 2 is required for modulation of lymphocyte traffic by FTY720. J Biol Chem 280, 36865-36872.
150. Schnute ME, McReynolds MD, Kasten T, Yates M, Jerome G, Rains JW, Hall T, Chrencik J, Kraus M, Cronin CN, et al,. (2012) Modulation of cellular S1P levels with a novel, potent and specific inhibitor of sphingosine kinase-1. Biochem J 444, 79-88.
151. Kharel Y, Mathews TP, Gellett AM, Tomsig JL, Kennedy PC, Moyer ML, Macdonald TL, &, Lynch KR, (2011) Sphingosine kinase type 1 inhibition reveals rapid turnover of circulating sphingosine 1-phosphate. Biochem J 440, 345-353.
152. Beljanski V, Knaak C, &, Smith CD, (2010) A novel sphingosine kinase inhibitor induces autophagy in tumor cells. J Pharmacol Exp Ther 333, 454-464.
153. Antoon JW, White MD, Meacham WD, Slaughter EM, Muir SE, Elliott S, Rhodes LV, Ashe HB, Wiese TE, Smith CD, et al,. (2010) Antiestrogenic effects of the novel sphingosine kinase-2 inhibitor ABC294640. Endocrinology 151, 5124-5135.
154. Raje MR, Knott K, Kharel Y, Bissel P, Lynch KR, &, Santos WL, (2012) Design, synthesis and biological activity of sphingosine kinase 2 selective inhibitors. Bioorg Med Chem 20, 183-194.
155. Liu K, Guo TL, Hait NC, Allegood J, Parikh HI, Xu W, Kellogg GE, Grant S, Spiegel S, &, Zhang S, (2013) Biological characterization of 3-(2-amino-ethyl)-5-[3-(4-butoxyl-phenyl)-propylidene]-thiazolidine-2,4-dione (K145) as a selective sphingosine kinase-2 inhibitor and anticancer agent. PLoS One 8, e56471.
156. Lim KG, Sun C, Bittman R, Pyne NJ, &, Pyne S, (2011) (R)-FTY720 methyl ether is a specific sphingosine kinase 2 inhibitor: effect on sphingosine kinase 2 expression in HEK 293 cells and actin rearrangement and survival of MCF-7 breast cancer cells. Cell Signal 23, 1590-1595.
157. Watson DG, Tonelli F, Alossaimi M, Williamson L, Chan E, Gorshkova I, Berdyshev E, Bittman R, Pyne NJ, &, Pyne S, (2013) The roles of sphingosine kinases 1 and 2 in regulating the Warburg effect in prostate cancer cells. Cell Signal 25, 1011-1017.
158. Kim JW, Kim YW, Inagaki Y, Hwang YA, Mitsutake S, Ryu YW, Lee WK, Ha HJ, Park CS, &, Igarashi Y, (2005) Synthesis and evaluation of sphingoid analogs as inhibitors of sphingosine kinases. Bioorg Med Chem 13, 3475-3485.
159. Hara-Yokoyama M, Terasawa K, Ichinose S, Watanabe A, Podyma-Inoue KA, Akiyoshi K, Igarashi Y, &, Yanagishita M, (2013) Sphingosine kinase 2 inhibitor SG-12 induces apoptosis via phosphorylation by sphingosine kinase 2. Bioorg Med Chem Lett 23, 2220-2224.
160. Nishiuma T, Nishimura Y, Okada T, Kuramoto E, Kotani Y, Jahangeer S, &, Nakamura S, (2008) Inhalation of sphingosine kinase inhibitor attenuates airway inflammation in asthmatic mouse model. Am J Physiol Lung Cell Mol Physiol 294, L1085-L1093.
161. Ricci C, Onida F, Servida F, Radaelli F, Saporiti G, Todoerti K, Deliliers GL, &, Ghidoni R, (2009) In vitro anti-leukaemia activity of sphingosine kinase inhibitor. Br J Haematol 144, 350-357.
162. Lee C, Xu DZ, Feketeova E, Kannan KB, Yun JK, Deitch EA, Fekete Z, Livingston DH, &, Hauser CJ, (2004) Attenuation of shock-induced acute lung injury by sphingosine kinase inhibition. J Trauma 57, 955-960.
163. Ren S, Xin C, Pfeilschifter J, &, Huwiler A, (2010) 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. Cell Physiol Biochem 26, 97-104.
164. Loveridge C, Tonelli F, Leclercq T, Lim KG, Long JS, Berdyshev E, Tate RJ, Natarajan V, Pitson SM, Pyne NJ, et al,. (2010) The sphingosine kinase 1 inhibitor 2-(p-hydroxyanilino)-4-(p-chlorophenyl)thiazole induces proteasomal degradation of sphingosine kinase 1 in mammalian cells. J Biol Chem 285, 38841-38852.