A selective ATP-competitive sphingosine kinase inhibitor demonstrates anti-cancer properties

Oncotarget

Volumn 6, Issue 9, 2015, Pages 7065-7083

  Pitman, Melissa R ^a   Powell, Jason A ^a,b   Coolen, Carl ^a   Moretti, Paul A B ^a   Zebol, Julia R ^a   Pham, Duyen H ^a   Finnie, John W ^b,c   Don, Anthony S ^d   Ebert, Lisa M ^a,b   Bonder, Claudine S ^a,b   Gliddon, Briony L ^a   Pitson, Stuart M ^a,b  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c HANSON INSTITUTE   (Australia)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Apoptosis; In silico docking; Molecular modeling; Small molecule inhibitor; Sphingosine kinase

Indexed keywords

ANTINEOPLASTIC AGENT; MP A 08; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; ENZYME INHIBITOR; PHOSPHOTRANSFERASE; PROTEIN BINDING; SPHINGOLIPID; SPHINGOSINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; DRUG PROTEIN BINDING; DRUG SCREENING; DRUG STRUCTURE; DRUG TARGETING; EMBRYO; FEMALE; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MALE; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; TOXICITY TESTING; ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; CANCER TRANSPLANTATION; CELL LINE; CHEMISTRY; CONFORMATION; HEK293 CELL LINE; LUNG NEOPLASMS; MCF-7 CELL LINE; METABOLISM; MUTAGENESIS; MUTATION; NEOVASCULARIZATION (PATHOLOGY); TRANSGENIC MOUSE; TUMOR CELL LINE;

ADENOCARCINOMA; ADENOSINE TRIPHOSPHATE; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BINDING SITES; CELL LINE; CELL LINE, TUMOR; ENZYME INHIBITORS; FEMALE; HEK293 CELLS; HUMANS; LUNG NEOPLASMS; MALE; MCF-7 CELLS; MICE; MICE, TRANSGENIC; MOLECULAR CONFORMATION; MUTAGENESIS; MUTATION; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; SPHINGOLIPIDS;

EID: 84927166176     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3178     Document Type: Article

References (76)

1. Pitson SM. Regulation of sphingosine kinase and sphingolipid signaling. Trends Biochem Sci. 2011; 36:97-107.
2. Kunkel GT, Maceyka M, Milstien S, Spiegel S. Targeting the sphingosine-1-phosphate axis in cancer, inflammation and beyond. Nat Rev Drug Discov. 2013; 12:688-702.
3. Maceyka M, Harikumar KB, Milstien S, Spiegel S. Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol. 2012; 22:50-60.
4. Harikumar KB, Yester JW, Surace MJ, Oyeniran C, Price MM, Huang WC, Hait NC, Allegood JC, Yamada A, Kong X, Lazear HM, Bhardwaj R, Takabe K, Diamond MS, Luo C, Milstien S, et al. K63-linked polyubiquitination of transcription factor IRF1 is essential for IL-1-induced production of chemokines CXCL10 and CCL5. Nat Immunol. 2014; 15:231-238.
5. Maceyka M, Spiegel S. Sphingolipid metabolites in inflammatory disease. Nature. 2014; 510:58-67.
6. Hannun YA, Obeid LM. Principles of bioactive lipid signalling:lessons from sphingolipids. Nat Rev Mol Cell Biol. 2008; 9:139-150.
7. Neubauer HA, Pitson SM. Roles, regulation and inhibitors of sphingosine kinase 2. FEBS J. 2013; 280:5317-5336.
8. Chan H, Pitson SM. Post-translational regulation of sphingosine kinases. Biochim Biophys Acta. 2013; 1831:147-156.
9. Wang Q, Li J, Li G, Li Y, Xu C, Li M, Xu G, Fu S. Prognostic significance of sphingosine kinase 2 expression in non-small cell lung cancer. Tumour Biol. 2014; 35:363-368.
10. Orr Gandy KA, Obeid LM. Targeting the sphingosine kinase/sphingosine 1-phosphate pathway in disease: review of sphingosine kinase inhibitors. Biochim Biophys Acta. 2013; 1831:157-166.
11. Pitman MR, Pitson SM. Inhibitors of the sphingosine kinase pathway as potential therapeutics. Curr Cancer Drug Targets. 2010; 10:354-367.
12. Kawamori T, Kaneshiro T, Okumura M, Maalouf S, Uflacker A, Bielawski J, Hannun YA, Obeid LM. Role for sphingosine kinase 1 in colon carcinogenesis. FASEB J. 2009; 23:405-414.
13. Weigert A, Schiffmann S, Sekar D, Ley S, Menrad H, Werno C, Grosch S, Geisslinger G, Brune B. Sphingosine kinase 2 deficient tumor xenografts show impaired growth and fail to polarize macrophages towards an anti-inflammatory phenotype. Int J Cancer. 2009; 125:2114-2121.
14. Shirai K, Kaneshiro T, Wada M, Furuya H, Bielawski J, Hannun YA, Obeid LM, Ogretmen B, Kawamori T. A role of sphingosine kinase 1 in head and neck carcinogenesis. Cancer Prev Res. 2011; 4:454-462.
15. Bao M, Chen Z, Xu Y, Zhao Y, Zha R, Huang S, Liu L, Chen T, Li J, Tu H, He X. Sphingosine kinase 1 promotes tumour cell migration and invasion via the S1P/EDG1 axis in hepatocellular carcinoma. Liver Int. 2012; 32:331-338.
16. Heffernan-Stroud LA, Helke KL, Jenkins RW, De Costa AM, Hannun YA, Obeid LM. Defining a role for sphingosine kinase 1 in p53-dependent tumors. Oncogene. 2012; 31:1166-1175.
17. Albinet V, Bats ML, Huwiler A, Rochaix P, Chevreau C, Segui B, Levade T, Andrieu-Abadie N. Dual role of sphingosine kinase-1 in promoting the differentiation of dermal fibroblasts and the dissemination of melanoma cells. Oncogene. 2014; 33:3364-3373.
18. Ponnusamy S, Selvam SP, Mehrotra S, Kawamori T, Snider AJ, Obeid LM, Shao Y, Sabbadini R, Ogretmen B. 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. 2012; 4:761-775.
19. Kohno M, Momoi M, Oo ML, Paik JH, Lee YM, Venkataraman K, Ai Y, Ristimaki AP, Fyrst H, Sano H, Rosenberg D, Saba JD, Proia RL, Hla T. Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol Cell Biol. 2006; 26:7211-7223.
20. Woodcock J. Sphingosine and ceramide signalling in apoptosis. IUBMB Life. 2006; 58:462-466.
21. 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.
22. Cingolani F, Casasampere M, Sanllehi P, Casas J, Bujons J, Fabrias G. Inhibition of dihydroceramide desaturase activity by the sphingosine kinase inhibitor SKI, II. J Lipid Res. 2014; 55:1711-1720.
23. Mercado N, Kizawa Y, Ueda K, Xiong Y, Kimura G, Moses A, Curtis JM, Ito K, Barnes PJ. Activation of transcription factor Nrf2 signalling by the sphingosine kinase inhibitor SKI-II is mediated by the formation of Keap1 dimers. PLoS One. 2014; 9:e88168.
24. Antoon JW, White MD, Meacham WD, Slaughter EM, Muir SE, Elliott S, Rhodes LV, Ashe HB, Wiese TE, Smith CD, Burow ME, Beckman BS. Antiestrogenic effects of the novel sphingosine kinase-2 inhibitor ABC294640. Endocrinology. 2010; 151:5124-5135.
25. Kharel Y, Mathews TP, Gellett AM, Tomsig JL, Kennedy PC, Moyer ML, Macdonald TL, Lynch KR. Sphingosine kinase type 1 inhibition reveals rapid turnover of circulating sphingosine 1-phosphate. Biochem J. 2011; 440:345-353.
26. Rex K, Jeffries S, Brown ML, Carlson T, Coxon A, Fajardo F, Frank B, Gustin D, Kamb A, Kassner PD, Li S, Li Y, Morgenstern K, Plant M, Quon K, Ruefli-Brasse A, et al. Sphingosine kinase activity is not required for tumor cell viability. PLoS One. 2013; 8:e68328.
27. Schnute ME, McReynolds MD, Kasten T, Yates M, Jerome G, Rains JW, Hall T, Chrencik J, Kraus M, Cronin CN, Saabye M, Highkin MK, Broadus R, Ogawa S, Cukyne K, Zawadzke LE, et al. Modulation of cellular S1P levels with a novel, potent and specific inhibitor of sphingosine kinase-1. Biochem J. 2012; 444:79-88.
28. Pitson SM, Moretti PA, Zebol JR, Zareie R, Derian CK, Darrow AL, Qi J, D'Andrea RJ, Bagley CJ, Vadas MA, Wattenberg BW. The nucleotide-binding site of human sphingosine kinase 1. J Biol Chem. 2002; 277:49545-49553.
29. Miller AV, Alvarez SE, Spiegel S, Lebman DA. Sphingosine kinases and sphingosine-1-phosphate are critical for transforming growth factor beta-induced extracellular signal-regulated kinase 1 and 2 activation and promotion of migration and invasion of esophageal cancer cells. Mol Cell Biol. 2008; 28:4142-4151.
30. Bakali HM, Herman MD, Johnson KA, Kelly AA, Wieslander A, Hallberg BM, Nordlund P. 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.
31. Pitman MR, Jarman KE, Leclercq TM, Pham DH, Pitson S. Sphingosine kinases: biochemistry, regulation and roles. Lysophospholipid receptors: signaling and biochemistry. Chun J. 2013; New Jersey, USA: John Wiley & Sons:153-183.
32. Wang Z, Min X, Xiao SH, Johnstone S, Romanow W, Meininger D, Xu H, Liu J, Dai J, An S, Thibault S, Walker N. Molecular basis of sphingosine kinase 1 substrate recognition and catalysis. Structure. 2013; 21:798-809.
33. Lim KG, Tonelli F, Berdyshev E, Gorshkova I, Leclercq T, Pitson SM, Bittman R, Pyne S, Pyne NJ. Inhibition kinetics and regulation of sphingosine kinase 1 expression in prostate cancer cells: functional differences between sphingosine kinase 1a and 1b. Int J Biochem Cell Biol. 2012; 44:1457-1464.
34. Loveridge C, Tonelli F, Leclercq T, Lim KG, Long JS, Berdyshev E, Tate RJ, Natarajan V, Pitson SM, Pyne NJ, Pyne S. 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. 2010; 285:38841-38852.
35. Tonelli F, Alossaimi M, Natarajan V, Gorshkova I, Berdyshev E, Bittman R, Watson DG, Pyne S, Pyne NJ. The roles of sphingosine kinase 1 and 2 in regulating the metabolome and survival of prostate cancer cells. Biomolecules. 2013; 3:316-333.
36. Tonelli F, Lim KG, Loveridge C, Long J, Pitson SM, Tigyi G, Bittman R, Pyne S, Pyne NJ. FTY720 and (S)-FTY720 vinylphosphonate inhibit sphingosine kinase 1 and promote its proteasomal degradation in human pulmonary artery smooth muscle, breast cancer and androgen-independent prostate cancer cells. Cell Signal. 2010; 22:1536-1542.
37. Pebay A, Bonder CS, Pitson SM. Stem cell regulation by lysophospholipids. Prostaglandins Other Lipid Mediat. 2007; 84:83-97.
38. Taha TA, Kitatani K, El-Alwani M, Bielawski J, Hannun YA, Obeid LM. Loss of sphingosine kinase-1 activates the intrinsic pathway of programmed cell death: modulation of sphingolipid levels and the induction of apoptosis. FASEB J. 2006; 20:482-484.
39. Gao P, Smith CD. Ablation of sphingosine kinase-2 inhibits tumor cell proliferation and migration. Mol Cancer Res. 2011; 9:1509-1519.
40. Hahn WC, Counter CM, Lundberg AS, Beijersbergen RL, Brooks MW, Weinberg RA. Creation of human tumour cells with defined genetic elements. Nature. 1999; 400:464-468.
41. Nagahashi M, Ramachandran S, Kim EY, Allegood JC, Rashid OM, Yamada A, Zhao R, Milstien S, Zhou H, Spiegel S, Takabe K. Sphingosine-1-phosphate produced by sphingosine kinase 1 promotes breast cancer progression by stimulating angiogenesis and lymphangiogenesis. Cancer Res. 2012; 72:726-735.
42. Pitman MR, Woodcock JM, Lopez AF, Pitson SM. Molecular targets of FTY720 (fingolimod). Curr Mol Med. 2012; 12:1207-1219.
43. Zhang J, Yang PL, Gray NS. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer. 2009; 9:28-39.
44. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000; 351:95-105.
45. Byun HS, Pyne S, Macritchie N, Pyne NJ, Bittman R. Novel sphingosine-containing analogues selectively inhibit sphingosine kinase (SK) isozymes, induce SK1 proteasomal degradation and reduce DNA synthesis in human pulmonary arterial smooth muscle cells. Medchemcomm. 2013; 4:1394-1399.
46. Gao P, Peterson YK, Smith RA, Smith CD. Characterization of isoenzyme-selective inhibitors of human sphingosine kinases. PLoS One. 2012; 7:e44543.
47. Xu B, Hao Z, Jha KN, Zhang Z, Urekar C, Digilio L, Pulido S, Strauss JF, 3rd , Flickinger CJ, Herr JC. Targeted deletion of Tssk1 and 2 causes male infertility due to haploinsufficiency. Dev Biol. 2008; 319:211-222.
48. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL. Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol. 2005; 25:11113-11121.
49. Mizugishi K, Li C, Olivera A, Bielawski J, Bielawska A, Deng CX, Proia RL. Maternal disturbance in activated sphingolipid metabolism causes pregnancy loss in mice. J Clin Invest. 2007; 117:2993-3006.
50. Paugh SW, Paugh BS, Rahmani M, Kapitonov D, Almenara JA, Kordula T, Milstien S, Adams JK, Zipkin RE, Grant S, Spiegel S. A selective sphingosine kinase 1 inhibitor integrates multiple molecular therapeutic targets in human leukemia. Blood. 2008; 112:1382-1391.
51. French KJ, Upson JJ, Keller SN, Zhuang Y, Yun JK, Smith CD. Antitumor activity of sphingosine kinase inhibitors. J Pharmacol Exp Ther. 2006; 318:596-603.
52. French KJ, Zhuang Y, Maines LW, Gao P, Wang W, Beljanski V, Upson JJ, Green CL, Keller SN, Smith CD. Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J Pharmacol Exp Ther. 2010; 333:129-139.
53. Pyne NJ, Pyne S. Sphingosine 1-phosphate and cancer. Nat Rev Cancer. 2010; 10:489-503.
54. Vadas M, Xia P, McCaughan G, Gamble J. The role of sphingosine kinase 1 in cancer: oncogene or non-oncogene addiction? Biochim Biophys Acta. 2008; 1781:442-447.
55. Lee OH, Kim YM, Lee YM, Moon EJ, Lee DJ, Kim JH, Kim KW, Kwon YG. Sphingosine 1-phosphate induces angiogenesis: its angiogenic action and signaling mechanism in human umbilical vein endothelial cells. Biochem Biophys Res Commun. 1999; 264:743-750.
56. Chae SS, Paik JH, Furneaux H, Hla T. Requirement for sphingosine 1-phosphate receptor-1 in tumor angiogenesis demonstrated by in vivo RNA interference. J Clin Invest. 2004; 114:1082-1089.
57. Anelli V, Gault CR, Snider AJ, Obeid LM. Role of sphingosine kinase-1 in paracrine/transcellular angiogenesis and lymphangiogenesis in vitro. FASEB J. 2010; 24:2727-2738.
58. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22:4673-4680.
59. Sanchez R, Sali A. Evaluation of comparative protein structure modeling by MODELLER-3. Proteins. 1997; 1:50-58.
60. Collaborative Computational Project 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr. 1994; 760-763.
61. DeLano WL. The PyMOL molecular graphics system. (Palo Alto, CA, USA: DeLano Scientific) 2002.
62. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF chimera-a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25:1605-1612.
63. Shoichet BK, Bodian DL, Kuntz ID. Molecular docking using shape descriptors. J Comput Chem. 1992; 13:380-397.
64. Ewing TJA, Kuntz ID. Critical Evaluation of Search Algorithms for Automated Molecular Docking and Database Screening. J Comput Chem. 1996; 18:1175-1189.
65. Irwin JJ, Sterling T, Mysinger MM, Bolstad ES, Coleman RG. ZINC: a free tool to discover chemistry for biology. J Chem Inf Model. 2012; 52:1757-1768.
66. Pitson SM, D'Andrea RJ, Vandeleur L, Moretti PA, Xia P, Gamble JR, Vadas MA, Wattenberg BW. Human sphingosine kinase: purification, molecular cloning and characterization of the native and recombinant enzymes. Biochem J. 2000; 350:429-441.
67. Roberts JL, Moretti PA, Darrow AL, Derian CK, Vadas MA, Pitson SM. An assay for sphingosine kinase activity using biotinylated sphingosine and streptavidin-coated membranes. Anal Biochem. 2004; 331:122-129.
68. Pitman MR, Pham DH, Pitson SM. Isoform-selective assays for sphingosine kinase activity. Methods Mol Biol. 2012; 874:21-31.
69. Walsh JP, Bell RM. sn-1,2-diacylglycerol kinase of Escherichia coli. Structural and kinetic analysis of the lipid cofactor dependence. J Biol Chem. 1986; 261:15062-15069.
70. Wijesinghe DS, Lamour NF, Gomez-Munoz A, Chalfant CE. Ceramide kinase and ceramide-1-phosphate. Methods Enzymol. 2007; 434:265-292.
71. Munoz-Olaya JM, Matabosch X, Bedia C, Egido-Gabas M, Casas J, Llebaria A, Delgado A, Fabrias G. Synthesis and biological activity of a novel inhibitor of dihydroceramide desaturase. ChemMedChem. 2008; 3:946-953.
72. Pitson SM, Xia P, Leclercq TM, Moretti PA, Zebol JR, Lynn HE, Wattenberg BW, Vadas MA. Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J Exp Med. 2005; 201:49-54.
73. Bielawski J, Szulc ZM, Hannun YA, Bielawska A. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods. 2006; 39:82-91.
74. Woodcock JM, Ma Y, Coolen C, Pham D, Jones C, Lopez AF, Pitson SM. Sphingosine and FTY720 directly bind pro-survival 14-3-3 proteins to regulate their function. Cell Signal. 2010; 22:1291-1299.
75. Xia P, Gamble JR, Wang L, Pitson SM, Moretti PA, Wattenberg BW, D'Andrea RJ, Vadas MA. An oncogenic role of sphingosine kinase. Curr Biol. 2000; 10:1527-1530.
76. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012; 9:671-675.