FTY720 inhibits tumor growth and enhances the tumor-suppressive effect of topotecan in neuroblastoma by interfering with the sphingolipid signaling pathway

Pediatric Blood and Cancer

Volumn 60, Issue 9, 2013, Pages 1418-1423

  Li, Mei Hong ^a   Hla, Timothy ^b   Ferrer, Fernando ^a,c  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Division of Pediatric Infectious Diseases   (United States)

Author keywords

Apoptosis; FTY720; Neuroblastoma; Sphingosine; Sphingosine kinase 2

Indexed keywords

CASPASE; CYTOCHROME C; FINGOLIMOD; MESSENGER RNA; PROTEIN BAD; PROTEIN BAX; PROTEIN KINASE B; SERINE; SPHINGOLIPID; SPHINGOSINE; SPHINGOSINE KINASE 2; TOPOTECAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL ASSAY; CELL DEATH; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MALE; MOUSE; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TUMOR GROWTH; TUMOR XENOGRAFT; WESTERN BLOTTING;

APOPTOSIS; FTY720; NEUROBLASTOMA; SPHINGOSINE; SPHINGOSINE KINASE 2;

ANIMALS; CELL DEATH; CHILD; CHILD, PRESCHOOL; DRUG SYNERGISM; HUMANS; IMMUNOSUPPRESSIVE AGENTS; INFANT; MALE; MICE; MICE, NUDE; NEUROBLASTOMA; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROPYLENE GLYCOLS; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; SPHINGOSINE; TOPOISOMERASE I INHIBITORS; TOPOTECAN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84880328774     PISSN: 15455009     EISSN: 15455017     Source Type: Journal    
DOI: 10.1002/pbc.24564     Document Type: Article

References (41)

1. Maris JM, Hogarty MD, Bagatell R, et al. Neuroblastoma. Lancet 2007; 369:2106-2120.
2. Park JR, Eggert A, Caron H. Neuroblastoma: Biology, prognosis, and treatment. Pediatr Clin North Am 2008; 55:97-120; x.
3. Perwein T, Lackner H, Sovinz P, et al. Survival and late effects in children with stage 4 neuroblastoma. Pediatr Blood Cancer 2011; 57:629-635.
4. Chun J, Brinkmann V. A mechanistically novel, first oral therapy for multiple sclerosis: The development of fingolimod (FTY720, Gilenya). Discov Med 2011; 12:213-228.
5. Azuma H, Takahara S, Ichimaru N, et al. Marked prevention of tumor growth and metastasis by a novel immunosuppressive agent, FTY720, in mouse breast cancer models. Cancer Res 2002; 62:1410-1419.
6. Estrada-Bernal A, Palanichamy K, Ray Chaudhury A, et al. Induction of brain tumor stem cell apoptosis by FTY720: A potential therapeutic agent for glioblastoma. Neuro Oncol 2012; 14:405-415.
7. Hung JH, Lu YS, Wang YC, et al. FTY720 induces apoptosis in hepatocellular carcinoma cells through activation of protein kinase C delta signaling. Cancer Res 2008; 68:1204-1212.
8. Neviani P, Santhanam R, Oaks JJ, et al. FTY720, a new alternative for treating blast crisis chronic myelogenous leukemia and Philadelphia chromosome-positive acute lymphocytic leukemia. J Clin Invest 2007; 117:2408-2421.
9. Pchejetski D, Bohler T, Brizuela L, et al. FTY720 (fingolimod) sensitizes prostate cancer cells to radiotherapy by inhibition of sphingosine kinase-1. Cancer Res 2010; 70:8651-8661.
10. Yasui H, Hideshima T, Raje N, et al. FTY720 induces apoptosis in multiple myeloma cells and overcomes drug resistance. Cancer Res 2005; 65:7478-7484.
11. Zhang N, Qi Y, Wadham C, et al. FTY720 induces necrotic cell death and autophagy in ovarian cancer cells: A protective role of autophagy. Autophagy 2010; 6:1157-1167.
12. Tonelli F, Lim KG, Loveridge C, et al. 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.
13. Arun B, Frenkel EP. Topoisomerase I inhibition with topotecan: Pharmacologic and clinical issues. Expert Opin Pharmacother 2001; 2:491-505.
14. Kingsbury WD, Boehm JC, Jakas DR, et al. Synthesis of water-soluble (aminoalkyl)camptothecin analogues: Inhibition of topoisomerase I and antitumor activity. J Med Chem 1991; 34:98-107.
15. Park JR, Scott JR, Stewart CF, et al. Pilot induction regimen incorporating pharmacokinetically guided topotecan for treatment of newly diagnosed high-risk neuroblastoma: A Children's Oncology Group study. J Clin Oncol 2011; 29:4351-4357.
16. Venkataraman K, Thangada S, Michaud J, et al. Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem J 2006; 397:461-471.
17. Li MH, Hla T, Ferrer F. Sphingolipid modulation of angiogenic factor expression in neuroblastoma. Cancer Prev Res (Phila) 2011; 4:1325-1332.
18. Li MH, Sanchez T, Pappalardo A, et al. Induction of antiproliferative connective tissue growth factor expression in Wilms' tumor cells by sphingosine-1-phosphate receptor 2. Mol Cancer Res 2008; 6:1649-1656.
19. Li MH, Sanchez T, Milne GL, et al. S1P/S1P2 signaling induces cyclooxygenase-2 expression in Wilms tumor. J Urol 2009; 181:1347-1352.
20. Li MH, Sanchez T, Yamase H, et al. S1P/S1P1 signaling stimulates cell migration and invasion in Wilms tumor. Cancer Lett 2009; 276:171-179.
21. Bielawski J, Pierce JS, Snider J, et al. Comprehensive quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods Mol Biol 2009; 579:443-467.
22. Brinkmann V, Davis MD, Heise CE, et al. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J Biol Chem 2002; 277:21453-21457.
23. Staker BL, Hjerrild K, Feese MD, et al. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc Natl Acad Sci U S A 2002; 99:15387-15392.
24. Baran Y, Salas A, Senkal CE, et al. Alterations of ceramide/sphingosine 1-phosphate rheostat involved in the regulation of resistance to imatinib-induced apoptosis in K562 human chronic myeloid leukemia cells. J Biol Chem 2007; 282:10922-10934.
25. Suzuki E, Handa K, Toledo MS, et al. Sphingosine-dependent apoptosis: A unified concept based on multiple mechanisms operating in concert. Proc Natl Acad Sci U S A 2004; 101:14788-14793.
26. Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91:231-241.
27. del Peso L, Gonzalez-Garcia M, Page C, et al. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 1997; 278:687-689.
28. Pyne NJ, Pyne S. Sphingosine 1-phosphate and cancer. Nat Rev Cancer 2010; 10:489-503.
29. French KJ, Zhuang Y, Maines LW, et al. Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J Pharmacol Exp Ther 2010; 333:129-139.
30. Gao P, Smith CD. Ablation of sphingosine kinase-2 inhibits tumor cell proliferation and migration. Mol Cancer Res 2011; 9:1509-1519.
31. Weigert A, Schiffmann S, Sekar D, et al. 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.
32. Lee TK, Man K, Ho JW, et al. FTY720: A promising agent for treatment of metastatic hepatocellular carcinoma. Clin Cancer Res 2005; 11:8458-8466.
33. Liu Q, Alinari L, Chen CS, et al. FTY720 shows promising in vitro and in vivo preclinical activity by downmodulating Cyclin D1 and phospho-Akt in mantle cell lymphoma. Clin Cancer Res 2010; 16:3182-3192.
34. Chua CW, Lee DT, Ling MT, et al. FTY720, a fungus metabolite, inhibits in vivo growth of androgen-independent prostate cancer. Int J Cancer 2005; 117:1039-1048.
35. Zheng T, Meng X, Wang J, et al. PTEN- and p53-mediated apoptosis and cell cycle arrest by FTY720 in gastric cancer cells and nude mice. J Cell Biochem 2010; 111:218-228.
36. Ubai T, Azuma H, Kotake Y, et al. FTY720 induced Bcl-associated and Fas-independent apoptosis in human renal cancer cells in vitro and significantly reduced in vivo tumor growth in mouse xenograft. Anticancer Res 2007; 27:75-88.
37. Ingwersen J, Aktas O, Kuery P, et al. Fingolimod in multiple sclerosis: Mechanisms of action and clinical efficacy. Clin Immunol 2012; 142:15-24.
38. Miron VE, Schubart A, Antel JP. Central nervous system-directed effects of FTY720 (fingolimod). J Neurol Sci 2008; 274:13-17.
39. Don AS, Martinez-Lamenca C, Webb WR, et al. Essential requirement for sphingosine kinase 2 in a sphingolipid apoptosis pathway activated by FTY720 analogues. J Biol Chem 2007; 282:15833-15842.
40. Woodcock JM, Ma Y, Coolen C, et al. Sphingosine and FTY720 directly bind pro-survival 14-3-3 proteins to regulate their function. Cell Signal 2010; 22:1291-1299.
41. Habrukowich C, Han DK. Le A et al. Sphingosine interaction with acidic leucine-rich nuclear phosphoprotein-32A (ANP32A) regulates PP2A activity and cyclooxygenase (COX)-2 expression in human endothelial cells. J Biol Chem 2010; 285:26825-26831.