ABC294640, a sphingosine kinase 2 inhibitor, enhances the antitumor effects of TRAIL in non-small cell lung cancer

Cancer Biology and Therapy

Volumn 16, Issue 8, 2015, Pages 1194-1204

  Yang, Jie ^a   Yang, Chunxu ^a   Zhang, Shimin ^a   Mei, Zijie ^a   Shi, Mingjun ^a   Sun, Shaoxing ^a   Shi, Liu ^a   Wang, Zhihao ^a   Wang, Yacheng ^a   Li, Zhenzhen ^a   Xie, Conghua ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Death receptor; NSCLC; Resistance; Sphingosine kinase 2; TRAIL

Indexed keywords

3 (4 CHLOROPHENYL) N (4 PYRIDINYLMETHYL)ADAMANTANE 1 CARBOXAMIDE; CASPASE 3; CASPASE 8; DEATH RECEPTOR 4; DEATH RECEPTOR 5; MESSENGER RNA; PROTEIN BCL 2; SMALL INTERFERING RNA; SPHINGOSINE KINASE 2; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; 3-(4-CHLOROPHENYL)-ADAMANTANE-1-CARBOXYLIC ACID (PYRIDIN-4-YLMETHYL)AMIDE; ADAMANTANE; ANTINEOPLASTIC AGENT; PHOSPHOTRANSFERASE; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE; SPHINGOSINE KINASE; SPHINGOSINE KINASE 2, HUMAN; TNFRSF10A PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL MEMBRANE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NON SMALL CELL LUNG CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; CARCINOMA, NON-SMALL-CELL LUNG; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; LUNG NEOPLASMS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PROCEDURES; PROTEIN TRANSPORT; TUMOR CELL LINE;

ADAMANTANE; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MOLECULAR TARGETED THERAPY; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; PYRIDINES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84983440132     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.1080/15384047.2015.1056944     Document Type: Article

References (54)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61:69-90; PMID:21296855; http://dx.doi.org/10.3322/caac.20107
2. Bulzebruck H, Bopp R, Drings P, Bauer E, Krysa S, Probst G, van Kaick G, Muller KM, Vogt-Moykopf I. New aspects in the staging of lung cancer. Prospective validation of the International Union Against Cancer TNM classification. Cancer 1992; 70:1102-10; PMID:1515985; http://dx.doi.org/10.1002/1097-0142(19920901)70:5%3c1102::AID-CNCR2820700514%3e3.0.CO;2-5
3. Detterbeck FC. Diagnosis and treatment of lung canceran evidence-based guide for the practicing clinician. Philadelphia, W.B. Saunders; c2001. Chapter 4, Early Stage Non-Small Cell Lung Cancer (NSCLC); p.181-190.
4. Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, Sutherland GR, Smith TD, Rauch C, Smith CA, Et A. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995; 3:673-82; PMID:8777713; http://dx.doi.org/10.1016/1074-7613(95)90057-8
5. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A. Induction of apoptosis by Apo2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 1996; 271:12687-90; PMID:8663110; http://dx.doi.org/10.1074/jbc.271.22.12687
6. Krammer PH. The CD95(APO-1/Fas)/CD95L system. Toxicol Lett 1998; 102-103:131-7; PMID:10022244
7. Ashkenazi A. Directing cancer cells to self-destruct with pro-apoptotic receptor agonists. Nat Rev Drug Discov 2008; 7:1001-12; PMID:18989337; http://dx.doi.org/10.1038/nrd2637
8. Johnstone RW, Frew AJ, Smyth MJ. The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 2008; 8:782-98; PMID:18813321; http://dx.doi.org/10.1038/nrc2465
9. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998; 94:481-90; PMID:9727491; http://dx.doi.org/10.1016/S0092-8674(00)81589-5
10. Merino D, Lalaoui N, Morizot A, Solary E, Micheau O. TRAIL in cancer therapy: present and future challenges. Expert Opin Ther Targets 2007; 11:1299-314; PMID:17907960 http://dx.doi.org/10.1517/14728222.11.10.1299
11. MacFarlane M. TRAIL-induced signalling and apoptosis. Toxicol Lett 2003; 139:89-97; PMID:12628743; http://dx.doi.org/10.1016/S0378-4274(02)00422-8
12. Wang S, El-Deiry WS. TRAIL and apoptosis induction by TNF-family death receptors. Oncogene 2003; 22:8628-33; PMID:14634624; http://dx.doi.org/10.1038/sj.onc.1207232
13. Bhojani MS, Rossu BD, Rehemtulla A. TRAIL and anti-tumor responses. Cancer Biol Ther 2003; 2:S71-8; PMID:14508083; http://dx.doi.org/10.4161/cbt.205
14. Hao C, Song JH, Hsi B, Lewis J, Song DK, Petruk KC, Tyrrell DL, Kneteman NM. TRAIL inhibits tumor growth but is nontoxic to human hepatocytes in chimeric mice. Cancer Res 2004; 64:8502-6; PMID:15574753; http://dx.doi.org/10.1158/0008-5472.CAN-04-2599
15. Takeda K, Stagg J, Yagita H, Okumura K, Smyth MJ. Targeting death-inducing receptors in cancer therapy. Oncogene 2007; 26:3745-57; PMID:17530027; http://dx.doi.org/10.1038/sj.onc.1210374
16. Kim YS, Schwabe RF, Qian T, Lemasters JJ, Brenner DA. TRAIL-mediated apoptosis requires NF-kappaB inhibition and the mitochondrial permeability transition in human hepatoma cells. Hepatology 2002; 36:1498-508; PMID:12447876
17. Wagner KW, Punnoose EA, Januario T, Lawrence DA, Pitti RM, Lancaster K, Lee D, von Goetz M, Yee SF, Totpal K, Huw L, Katta V, Cavet G, Hymowitz SG, Amler L, Ashkenazi A. Death-receptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat Med 2007; 13:1070-7; PMID:17767167; http://dx.doi.org/10.1038/nm1627
18. Jin Z, McDonald ER, Dicker DT, El-Deiry WS. Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 2004; 279:35829-39; PMID:15155747; http://dx.doi.org/10.1074/jbc.M405538200
19. Wu F, Hu Y, Long J, Zhou YJ, Zhong YH, Liao ZK, Liu SQ, Zhou FX, Zhou YF, Xie CH. Cytotoxicity and radiosensitization effect of TRA-8 on radioresistant human larynx squamous carcinoma cells. Oncol Rep 2009; 21:461-5; PMID:19148523; http://dx.doi.org/10.3892/or_00000347
20. Hu Y, Ouyang W, Wu F, Cao CH, Wang K, Liao ZK, Zhong YH, Zhou FX, Liu SQ, Xia L, Zhou YF, Xie CH. Enhanced radiosensitivity of SW480 cells via TRAIL up-regulation mediated by Egr-1 promoter. Oncol Rep 2009; 22:765-71; PMID:19724854
21. Voelkel-Johnson C, Hannun YA, El-Zawahry A. Resistance to TRAIL is associated with defects in ceramide signaling that can be overcome by exogenous C6-ceramide without requiring downregulation of cellular FLICE inhibitory protein. Mol Cancer Ther 2005; 4:1320-7; PMID:16170023; http://dx.doi.org/10.1158/1535-7163.MCT-05-0086
22. Ipatova OM, Torkhovskaya TI, Zakharova TS, Khalilov EM. Sphingolipids and cell signaling: involvement in apoptosis and atherogenesis. Biochemistry (Mosc) 2006; 71:713-22; PMID:16903825; http://dx.doi.org/10.1134/S0006297906070030
23. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 2008; 9:139-50; PMID:18216770; http://dx.doi.org/10.1038/nrm2329
24. Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind S, Spiegel S. Suppression of ceramidemediated programmed cell death by sphingosine-1-phosphate. Nature 1996; 381:800-3; PMID:8657285; http://dx.doi.org/10.1038/381800a0
25. Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003; 4:397-407; PMID:12728273; http://dx.doi.org/10.1038/nrm1103
26. Spiegel S, Milstien S. Sphingosine 1-phosphate, a key cell signaling molecule. J Biol Chem 2002; 277:258-514; PMID:12011102; http://dx.doi.org/10.1074/jbc.R200007200
27. Kohama T, Olivera A, Edsall L, Nagiec MM, Dickson R, Spiegel S. Molecular cloning and functional characterization of murine sphingosine kinase. J Biol Chem 1998; 273:23722-8; PMID:9726979; http://dx.doi.org/10.1074/jbc.273.37.23722
28. Liu H, Sugiura M, Nava VE, Edsall LC, Kono K, Poulton S, Milstien S, Kohama T, Spiegel S. Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J Biol Chem 2000; 275:19513-20; PMID:10751414; http://dx.doi.org/10.1074/jbc.M002759200
29. Gault CR, Obeid LM. Still benched on its way to the bedside: sphingosine kinase 1 as an emerging target in cancer chemotherapy. Crit Rev Biochem Mol Biol 2011; 46:342-51; PMID:21787121; http://dx.doi.org/10.3109/10409238.2011.597737
30. Song L, Xiong H, Li J, Liao W, Wang L, Wu J, Li M. Sphingosine kinase-1 enhances resistance to apoptosis through activation of PI3K/Akt/NF-kappaB pathway in human non-small cell lung cancer. Clin Cancer Res 2011; 17:1839-49; PMID:21325072; http://dx.doi.org/10.1158/1078-0432.CCR-10-0720
31. 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; 35:363-8; PMID:23918304; http://dx.doi.org/10.1007/s13277-013-1051-1
32. Antoon JW, White MD, Slaughter EM, Driver JL, Khalili HS, Elliott S, Smith CD, Burow ME, Beckman BS. Targeting NFkB mediated breast cancer chemoresistance through selective inhibition of sphingosine kinase-2. Cancer Biol Ther 2011; 11:678-89; PMID:21307639; http://dx.doi.org/10.4161/cbt.11.7.14903
33. 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; 333:129-39; PMID:20061445; http://dx.doi.org/10.1124/jpet.109.163444
34. Johnson KR, Johnson KY, Crellin HG, Ogretmen B, Boylan AM, Harley RA, Obeid LM. Immunohistochemical distribution of sphingosine kinase 1 in normal and tumor lung tissue. J Histochem Cytochem 2005; 53:1159-66; PMID:15923363; http://dx.doi.org/10.1369/jhc.4A6606.2005
35. Li J, Guan HY, Gong LY, Song LB, Zhang N, Wu J, Yuan J, Zheng YJ, Huang ZS, Li M. Clinical significance of sphingosine kinase-1 expression in human astrocytomas progression and overall patient survival. Clin Cancer Res 2008; 14:6996-7003; PMID:18980995; http://dx.doi.org/10.1158/1078-0432.CCR-08-0754
36. Taha TA, Hannun YA, Obeid LM. Sphingosine kinase: biochemical and cellular regulation and role in disease. J Biochem Mol Biol 2006; 39:113-31; PMID:16584625; http://dx.doi.org/10.5483/BMBRep.2006.39.2.113
37. Ozoren N, Fisher MJ, Kim K, Liu CX, Genin A, Shifman Y, Dicker DT, Spinner NB, Lisitsyn NA, El-Deiry WS. Homozygous deletion of the death receptor DR4 gene in a nasopharyngeal cancer cell line is associated with TRAIL resistance. Int J Oncol 2000; 16:917-25; PMID:10762627
38. Eggert A, Grotzer MA, Zuzak TJ, Wiewrodt BR, Ho R, Ikegaki N, Brodeur GM. Resistance to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)induced apoptosis in neuroblastoma cells correlates with a loss of caspase-8 expression. Cancer Res 2001; 61:1314-9; PMID:11245427
39. Abdulghani J, El-Deiry WS. TRAIL receptor signaling and therapeutics., 2010:1091-108
40. Pan G, Ni J, Wei YF, Yu G, Gentz R, Dixit VM. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 1997; 277:815-8; PMID:9242610; http://dx.doi.org/10.1126/science.277.5327.815
41. Dimberg LY, Anderson CK, Camidge R, Behbakht K, Thorburn A, Ford HL. On the TRAIL to successful cancer therapy? Predicting and counteracting resistance against TRAIL-based therapeutics. Oncogene 2013; 32:1341-50; PMID:22580613; http://dx.doi.org/10.1038/onc.2012.164
42. Sorli SC, Colie S, Albinet V, Dubrac A, Touriol C, Guilbaud N, Bedia C, Fabrias G, Casas J, Segui B, Levade T, Andrieu-Abadie N. The nonlysosomal b-glucosidase GBA2 promotes endoplasmic reticulum stress and impairs tumorigenicity of human melanoma cells. Faseb J 2013; 27:489-98; PMID:23073830; http://dx.doi.org/10.1096/fj.12-215152
43. Liu YY, Han TY, Giuliano AE, Cabot MC. Ceramide glycosylation potentiates cellular multidrug resistance. Faseb J 2001; 15:719-30; PMID:11259390; http://dx.doi.org/10.1096/fj.00-0223com
44. Pchejetski D, Golzio M, Bonhoure E, Calvet C, Doumerc N, Garcia V, Mazerolles C, Rischmann P, Teissie J, Malavaud B, Cuvillier O. Sphingosine kinase-1 as a chemotherapy sensor in prostate adenocarcinoma cell and mouse models. Cancer Res 2005; 65:11667-75; PMID:16357178; http://dx.doi.org/10.1158/0008-5472.CAN-05-2702
45. Ozoren N, El-Deiry WS., Defining characteristics of Types I and II apoptotic cells in response to TRAIL. Neoplasia 2002. Four (6): p. 551-7; PMID:12407450; http://dx.doi.org/10.1038/sj.neo.7900270
46. White MD, Chan L, Antoon JW, Beckman BS. Targeting ovarian cancer and chemoresistance through selective inhibition of sphingosine kinase-2 with ABC294640. Anticancer Res 2013; 33:3573-9; PMID:24023282
47. Gao P, Peterson YK, Smith RA, Smith CD. Characterization of isoenzyme-selective inhibitors of human sphingosine kinases. PLoS One 2012; 7:e44543; PMID:22970244; http://dx.doi.org/10.1371/journal.pone.0044543
48. Henson ES, Gibson EM, Villanueva J, Bristow NA, Haney N, Gibson SB. Increased expression of Mcl-1 is responsible for the blockage of TRAIL-induced apoptosis mediated by EGF/ErbB1 signaling pathway. J Cell Biochem 2003; 89:1177-92; PMID:12898516; http://dx.doi.org/10.1002/jcb.10597
49. Kreuz S, Siegmund D, Scheurich P, Wajant H. NFkappaB inducers upregulate cFLIP, a cycloheximidesensitive inhibitor of death receptor signaling. Mol Cell Biol 2001; 21:3964-73; PMID:11359904; http://dx.doi.org/10.1128/MCB.21.12.3964-3973.2001
50. Azijli K, Yuvaraj S, Peppelenbosch MP, Wurdinger T, Dekker H, Joore J, van Dijk E, Quax WJ, Peters GJ, de Jong S, Kruyt FA. Kinome profiling of non-canonical TRAIL signaling reveals RIP1-Src-STAT3-dependent invasion in resistant non-small cell lung cancer cells. J Cell Sci 2012; 125:4651-61; PMID:22797920; http://dx.doi.org/10.1242/jcs.109587
51. Stegehuis JH, de Wilt LH, de Vries EG, Groen HJ, de Jong S, Kruyt FA. TRAIL receptor targeting therapies for non-small cell lung cancer: current status and perspectives. Drug Resist Updat 2010; 13:2-15; PMID:20036602; http://dx.doi.org/10.1016/j.drup.2009.11.001
52. Hellwig CT, Rehm M. TRAIL signaling and synergy mechanisms used in TRAIL-based combination therapies. Mol Cancer Ther 2012; 11:3-13; PMID:22234808; http://dx.doi.org/10.1158/1535-7163.MCT-11-0434
53. Jin Z, McDonald ER, Dicker DT, El-Deiry WS. Deficient tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor transport to the cell surface in human colon cancer cells selected for resistance to TRAIL-induced apoptosis. J Biol Chem 2004; 279:35829-39; PMID:15155747; http://dx.doi.org/10.1074/jbc.M405538200
54. Beljanski V, Knaak C, Smith CD. A novel sphingosine kinase inhibitor induces autophagy in tumor cells. J Pharmacol Exp Ther 2010; 333:454-64; PMID:20179157; http://dx.doi.org/10.1124/jpet.109.163337