Antitumor effect of the novel sphingosine kinase 2 inhibitor ABC294640 is enhanced by inhibition of autophagy and by sorafenib in human cholangiocarcinoma cells

Oncotarget

Volumn 7, Issue 15, 2016, Pages 20080-20092

  Ding, Xiwei ^a,b   Chaiteerakij, Roongruedee ^b,c   Moser, Catherine D ^b   Shaleh, Hassan ^b   Boakye, Jeffrey ^b   Chen, Gang ^b   Ndzengue, Albert ^b   Li, Ying ^b   Zhou, Yanling ^b   Huang, Shengbing ^b   Sinicrope, Frank A ^b   Zou, Xiaoping ^a   Thomas, Melanie B ^d   Smith, Charles D ^e   Roberts, Lewis R ^b  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^b MAYO CLINIC CANCER CENTER   (United States)

^c KING CHULALONGKORN MEMORIAL HOSPITAL   (Thailand)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e APOGEE BIOTECHNOLOGY CORPORATION   (United States)

Author keywords

ABC294640; Autophagy; Cholangiocarcinoma; Sorafenib; Sphingosine kinase 2

Indexed keywords

3 (4 CHLOROPHENYL) N (4 PYRIDINYLMETHYL)ADAMANTANE 1 CARBOXAMIDE; BAFILOMYCIN A1; CHLOROQUINE; SORAFENIB; SPHINGOSINE KINASE 2; STAT3 PROTEIN; 3-(4-CHLOROPHENYL)-ADAMANTANE-1-CARBOXYLIC ACID (PYRIDIN-4-YLMETHYL)AMIDE; ADAMANTANE; CARBANILAMIDE DERIVATIVE; NICOTINAMIDE; PHOSPHOTRANSFERASE; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE; SPHINGOSINE KINASE 2, HUMAN;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BILE DUCT CARCINOMA; CANCER CELL; CELL SURVIVAL; CLONOGENESIS; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; UPREGULATION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BILE DUCT TUMOR; CELL PROLIFERATION; COMBINATION DRUG THERAPY; DRUG EFFECTS; DRUG POTENTIATION; METABOLISM; PATHOLOGY; TUMOR CELL CULTURE;

ADAMANTANE; APOPTOSIS; AUTOPHAGY; BILE DUCT NEOPLASMS; CELL PROLIFERATION; CHOLANGIOCARCINOMA; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; HUMANS; NIACINAMIDE; PHENYLUREA COMPOUNDS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN KINASE INHIBITORS; PYRIDINES; TUMOR CELLS, CULTURED;

EID: 84964720733     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7914     Document Type: Article

References (42)

1. von Hahn T, Ciesek S, Wegener G, Plentz RR, Weismuller TJ, Wedemeyer H, Manns MP, Greten TF, Malek NP. Epidemiological trends in incidence and mortality of hepatobiliary cancers in Germany. Scand J Gastroenterol. 2011; 46:1092-1098.
2. Yang JD, Kim B, Sanderson SO, Sauver JS, Yawn BP, Larson JJ, Therneau TM, Roberts LR, Gores GJ, Kim WR. Biliary tract cancers in Olmsted County, Minnesota, 1976-2008. Am J Gastroenterol. 2012; 107:1256-1262.
3. Pinter M, Hucke F, Zielonke N, Waldhor T, Trauner M, Peck-Radosavljevic M, Sieghart W. Incidence and mortality trends for biliary tract cancers in Austria. Liver Int. 2014; 34:1102-1108.
4. Rizvi S, Gores GJ. Pathogenesis, diagnosis, and management of cholangiocarcinoma. Gastroenterology. 2013; 145:1215-1229.
5. Chen MH, Yen CC, Cheng CT, Wu RC, Huang SC, Yu CS, Chung YH, Liu CY, Chang PM, Chao Y, Chen MH, Chen YF, Chiang KC, et al. Identification of SPHK1 as a therapeutic target and marker of poor prognosis in cholangiocarcinoma. Oncotarget. 2015; 15:23594-23608. doi: 10.18632/oncotarget.4335.
6. Le Scolan E, Pchejetski D, Banno Y, Denis N, Mayeux P, Vainchenker W, Levade T, Moreau-Gachelin F. Overexpression of sphingosine kinase 1 is an oncogenic event in erythroleukemic progression. Blood. 2005; 106:1808-1816.
7. Li W, Yu CP, Xia JT, Zhang L, Weng GX, Zheng HQ, Kong QL, Hu LJ, Zeng MS, Zeng YX, Li M, Li J, Song LB. Sphingosine kinase 1 is associated with gastric cancer progression and poor survival of patients. Clin Cancer Res. 2009; 15:1393-1399.
8. Datta A, Loo SY, Huang B, Wong L, Tan SS, Tan TZ, Lee SC, Thiery JP, Lim YC, Yong WP, Lam Y, Kumar AP, Yap CT. SPHK1 regulates proliferation and survival responses in triple-negative breast cancer. Oncotarget. 2014; 5:5920-5933. doi: 10.18632/oncotarget.1874.
9. Wallington-Beddoe CT, Powell JA, Tong D, Pitson SM, Bradstock KF, Bendall LJ. Sphingosine kinase 2 promotes acute lymphoblastic leukemia by enhancing MYC expression. Cancer Res. 2014; 74:2803-2815.
10. Pyne NJ, Tonelli F, Lim KG, Long JS, Edwards J, Pyne S. Sphingosine 1-phosphate signalling in cancer. Biochem Soc Trans. 2012; 40:94-100.
11. Liu R, Zhao R, Zhou X, Liang X, Campbell DJ, Zhang X, Zhang L, Shi R, Wang G, Pandak WM, Sirica AE, Hylemon PB, Zhou H. Conjugated bile acids promote cholangiocarcinoma cell invasive growth through activation of sphingosine 1-phosphate receptor 2. Hepatology. 2014; 60:908-918.
12. 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; 11:678-689.
13. Beljanski V, Knaak C, Zhuang Y, Smith CD. Combined anticancer effects of sphingosine kinase inhibitors and sorafenib. Invest New Drugs. 2011; 29:1132-1142.
14. Beljanski V, Lewis CS, Smith CD. Antitumor activity of sphingosine kinase 2 inhibitor ABC294640 and sorafenib in hepatocellular carcinoma xenografts. Cancer Biol Ther. 2011; 11:524-534.
15. 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.
16. Kummetha Venkata J, An N, Stuart R, Costa LJ, Cai H, Coker W, Song JH, Gibbs K, Matson T, Garrett-Mayer E, Wan Z, Ogretmen B, Smith C, et al. Inhibition of sphingosine kinase 2 down-regulates the expression of c-Myc and Mcl-1 and induces apoptosis in multiple myeloma. Blood. 2014; 124:1915-1925.
17. Qin Z, Dai L, Trillo-Tinoco J, Senkal C, Wang W, Reske T, Bonstaff K, Del Valle L, Rodriguez P, Flemington E, Voelkel-Johnson C, Smith CD, Ogretmen B, et al. Targeting sphingosine kinase induces apoptosis and tumor regression for KSHV-associated primary effusion lymphoma. Mol Cancer Ther. 2014; 13:154-164.
18. 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; 33:3573-3579.
19. Gestaut MM, Antoon JW, Burow ME, Beckman BS. Inhibition of sphingosine kinase-2 ablates androgen resistant prostate cancer proliferation and survival. Pharmacol Rep. 2014; 66:174-178.
20. Yang J, Yang C, Zhang S, Mei Z, Shi M, Sun S, Shi L, Wang Z, Wang Y, Li Z, Xie C. ABC294640, a sphingosine kinase 2 inhibitor, enhances the antitumor effects of TRAIL in non-small cell lung cancer. Cancer Biol Ther. 2015; 16:1194-1204.
21. Beljanski V, Knaak C, Smith CD. A novel sphingosine kinase inhibitor induces autophagy in tumor cells. J Pharmacol Exp Ther. 2010; 333:454-464.
22. Lamoureux F, Thomas C, Crafter C, Kumano M, Zhang F, Davies BR, Gleave ME, Zoubeidi A. Blocked autophagy using lysosomotropic agents sensitizes resistant prostate tumor cells to the novel Akt inhibitor AZD5363. Clin Cancer Res. 2013; 19:833-844.
23. Yang ZJ, Chee CE, Huang S, Sinicrope FA. The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther. 2011; 10:1533-1541.
24. Altman JK, Szilard A, Goussetis DJ, Sassano A, Colamonici M, Gounaris E, Frankfurt O, Giles FJ, Eklund EA, Beauchamp EM, Platanias LC. Autophagy is a survival mechanism of acute myelogenous leukemia precursors during dual mTORC2/mTORC1 targeting. Clin Cancer Res. 2014; 20:2400-2409.
25. Blechacz BR, Smoot RL, Bronk SF, Werneburg NW, Sirica AE, Gores GJ. Sorafenib inhibits signal transducer and activator of transcription-3 signaling in cholangiocarcinoma cells by activating the phosphatase shatterproof 2. Hepatology. 2009; 50:1861-1870.
26. Sugiyama H, Onuki K, Ishige K, Baba N, Ueda T, Matsuda S, Takeuchi K, Onodera M, Nakanuma Y, Yamato M, Yamamoto M, Hyodo I, Shoda J. Potent in vitro and in vivo antitumor activity of sorafenib against human intrahepatic cholangiocarcinoma cells. J Gastroenterol. 2011; 46:779-789.
27. Isomoto H, Kobayashi S, Werneburg NW, Bronk SF, Guicciardi ME, Frank DA, Gores GJ. Interleukin 6 upregulates myeloid cell leukemia-1 expression through a STAT3 pathway in cholangiocarcinoma cells. Hepatology. 2005; 42:1329-1338.
28. Isomoto H, Mott JL, Kobayashi S, Werneburg NW, Bronk SF, Haan S, Gores GJ. Sustained IL-6/STAT-3 signaling in cholangiocarcinoma cells due to SOCS-3 epigenetic silencing. Gastroenterology. 2007; 132:384-396.
29. Zheng T, Hong X, Wang J, Pei T, Liang Y, Yin D, Song R, Song X, Lu Z, Qi S, Liu J, Sun B, Xie C, et al. Gankyrin promotes tumor growth and metastasis through activation of IL-6/STAT3 signaling in human cholangiocarcinoma. Hepatology. 2014; 59:935-946.
30. 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.
31. 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.
32. Rosa R, Marciano R, Malapelle U, Formisano L, Nappi L, D'Amato C, D'Amato V, Damiano V, Marfe G, Del Vecchio S, Zannetti A, Greco A, De Stefano A, et al. Sphingosine kinase 1 overexpression contributes to cetuximab resistance in human colorectal cancer models. Clin Cancer Res. 2013; 19:138-147.
33. Liu H, Toman RE, Goparaju SK, Maceyka M, Nava VE, Sankala H, Payne SG, Bektas M, Ishii I, Chun J, Milstien S, Spiegel S. Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J Biol Chem. 2003; 278:40330-40336.
34. Chumanevich AA, Poudyal D, Cui X, Davis T, Wood PA, Smith CD, Hofseth LJ. Suppression of colitis-driven colon cancer in mice by a novel small molecule inhibitor of sphingosine kinase. Carcinogenesis. 2010; 31:1787-1793.
35. 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.
36. Liang J, Nagahashi M, Kim EY, Harikumar KB, Yamada A, Huang WC, Hait NC, Allegood JC, Price MM, Avni D, Takabe K, Kordula T, Milstien S, et al. Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation, and development of colitisassociated cancer. Cancer Cell. 2013; 23:107-120.
37. Hou YJ, Dong LW, Tan YX, Yang GZ, Pan YF, Li Z, Tang L, Wang M, Wang Q, Wang HY. Inhibition of active autophagy induces apoptosis and increases chemosensitivity in cholangiocarcinoma. Lab Invest. 2011; 91:1146-1157.
38. Huang JL, Hezel AF. Autophagy in intra-hepatic cholangiocarcinoma. Autophagy. 2012; 8:1148-1149.
39. O'Dell MR, Huang JL, Whitney-Miller CL, Deshpande V, Rothberg P, Grose V, Rossi RM, Zhu AX, Land H, Bardeesy N, Hezel AF. Kras(G12D) and p53 mutation cause primary intrahepatic cholangiocarcinoma. Cancer Res. 2012; 72:1557-1567.
40. Grubman SA, Perrone RD, Lee DW, Murray SL, Rogers LC, Wolkoff LI, Mulberg AE, Cherington V, Jefferson DM. Regulation of intracellular pH by immortalized human intrahepatic biliary epithelial cell lines. Am J Physiol. 1994; 266:G1060-1070.
41. Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 2010; 70:440-446.
42. Lai JP, Yu C, Moser CD, Aderca I, Han T, Garvey TD, Murphy LM, Garrity-Park MM, Shridhar V, Adjei AA, Roberts LR. SULF1 inhibits tumor growth and potentiates the effects of histone deacetylase inhibitors in hepatocellular carcinoma. Gastroenterology. 2006; 130:2130-2144.