TRAIL sensitize MDR cells to MDR-related drugs by down-regulation of P-glycoprotein through inhibition of DNA-PKcs/Akt/GSK-3β pathway and activation of caspases

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Seo, Suk Bin ^a   Hur, Jung Gu ^a   Kim, Mi Ju ^a   Lee, Jae Won ^a   Kim, Hak Bong ^a   Bae, Jae Ho ^a   Kim, Dong Wan ^b   Kang, Chi Dug ^a   Kim, Sun Hee ^a  

^a Pusan National University School of Medicine   (South Korea)

^b Changwon National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; DEATH RECEPTOR 5; DNA DEPENDENT PROTEIN KINASE; DOXORUBICIN; FLICE INHIBITORY PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOPROTEIN P; MYC PROTEIN; PROTEIN KINASE B; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VINCRISTINE; ANTINEOPLASTIC AGENT; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; TNFSF10 PROTEIN, HUMAN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; LYMPHATIC LEUKEMIA; MITOCHONDRION; MOLECULAR DYNAMICS; MULTIDRUG RESISTANCE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; DRUG RESISTANCE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CASPASES; CELL LINE, TUMOR; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; P-GLYCOPROTEIN; PROTO-ONCOGENE PROTEINS C-AKT; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 77954945993     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-199     Document Type: Article

References (48)

1. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002, 2:48-58. 10.1038/nrc706, 11902585.
2. Tsuruo T, Naito M, Tomida A, Fujita N, Mashima T, Sakamoto H, Haga N. Molecular targeting therapy of cancer: drug resistance, apoptosis and survival signal. Cancer Sci 2003, 94:15-21. 10.1111/j.1349-7006.2003.tb01345.x, 12708468.
3. Tan B, Piwnica-Worms D, Ratner L. Multidrug resistance transporters and modulation. Curr Opin Oncol 2000, 12:450-458. 10.1097/00001622-200009000-00011, 10975553.
4. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 2006, 5:219-234. 10.1038/nrd1984, 16518375.
5. Trock BJ, Leonessa F, Clarke R. Multidrug resistance in breast cancer: a meta-analysis of MDR1/gp170 expression and its possible functional significance. J Natl Cancer Inst 1997, 89:917-931. 10.1093/jnci/89.13.917, 9214671.
6. Norgaard JM, Bukh A, Langkjer ST, Clausen N, Palshof T, Hokland P. MDR1 gene expression and drug resistance of AML cells. Br J Haematol 1998, 100:534-540. 10.1046/j.1365-2141.1998.00593.x, 9504636.
7. Steinbach D, Legrand O. ABC transporters and drug resistance in leukemia: was P-gp nothing but the first head of the Hydra?. Leukemia 2007, 21:1172-1176. 10.1038/sj.leu.2404692, 17429427.
8. Ivy SP, Olshefski RS, Taylor BJ, Patel KM, Reaman GH. Correlation of P-glycoprotein expression and function in childhood acute leukemia: a children's cancer group study. Blood 1996, 88:309-318.
9. Li X, Li JP, Yuan HY, Gao X, Qu XJ, Xu WF, Tang W. Recent advances in P-glycoprotein-mediated multidrug resistance reversal mechanisms. Methods Find Exp Clin Pharmacol 2007, 29:607-617. 10.1358/mf.2007.29.9.1139054, 18193112.
10. Kim SH, Um JH, Dong-Won B, Kwon BH, Kim DW, Chung BS, Kang CD. Potentiation of chemosensitivity in multidrug-resistant human leukemia CEM cells by inhibition of DNA-dependent protein kinase using wortmannin. Leuk Res 2000, 24:917-925. 10.1016/S0145-2126(00)00061-8, 11086175.
11. Bolderson E, Richard DJ, Zhou BB, Khanna KK. Recent advances in cancer therapy targeting proteins involved in DNA double-strand break repair. Clin Cancer Res 2009, 15:6314-6320. 10.1158/1078-0432.CCR-09-0096, 19808869.
12. Zhong X, Safa AR. Phosphorylation of RNA helicase A by DNA-dependent protein kinase is indispensable for expression of the MDR1 gene product P-glycoprotein in multidrug-resistant human leukemia cells. Biochemistry 2007, 46:5766-5775. 10.1021/bi700063b, 17441731.
13. West KA, Castillo SS, Dennis PA. Activation of the PI3K/Akt pathway and chemotherapeutic resistance. Drug Resist Updat 2002, 5:234-248. 10.1016/S1368-7646(02)00120-6, 12531180.
14. Chiarini F, Del Sole M, Mongiorgi S, Gaboardi GC, Cappellini A, Mantovani I, Follo MY, McCubrey JA, Martelli AM. The novel Akt inhibitor, perifosine, induces caspase-dependent apoptosis and downregulates P-glycoprotein expression in multidrug-resistant human T-acute leukemia cells by a JNK-dependent mechanism. Leukemia 2008, 22:1106-1116. 10.1038/leu.2008.79, 18385752.
15. Choi BH, Kim CG, Lim Y, Shin SY, Lee YH. Curcumin down-regulates the multidrug-resistance mdr1b gene by inhibiting the PI3K/Akt/NF kappa B pathway. Cancer Lett 2008, 259:111-118. 10.1016/j.canlet.2007.10.003, 18006147.
16. Zhang Y, Qu X, Hu X, Yang X, Hou K, Teng Y, Zhang J, Sada K, Liu Y. Reversal of P-glycoprotein-mediated multi-drug resistance by the E3 ubiquitin ligase Cbl-b in human gastric adenocarcinoma cells. J Pathol 2009, 218:248-255. 10.1002/path.2533, 19274672.
17. Bozulic L, Surucu B, Hynx D, Hemmings BA. PKBalpha/Akt1 acts downstream of DNA-PK in the DNA double-strand break response and promotes survival. Mol Cell 2008, 30:203-213. 10.1016/j.molcel.2008.02.024, 18439899.
18. Feng J, Park J, Cron P, Hess D, Hemmings BA. Identification of a PKB/Akt hydrophobic motif Ser-473 kinase as DNA-dependent protein kinase. J Biol Chem 2004, 279:41189-41196. 10.1074/jbc.M406731200, 15262962.
19. Beurel E, Jope RS. The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways. Prog Neurobiol 2006, 79:173-189. 10.1016/j.pneurobio.2006.07.006, 1618798, 16935409.
20. Srivastava RK. TRAIL/Apo-2L: mechanisms and clinical applications in cancer. Neoplasia 2001, 3:535-546. 10.1038/sj.neo.7900203, 1506567, 11774036.
21. Falschlehner C, Emmerich CH, Gerlach B, Walczak H. TRAIL signalling: decisions between life and death. Int J Biochem Cell Biol 2007, 39:1462-1475. 10.1016/j.biocel.2007.02.007, 17403612.
22. Day TW, Huang S, Safa AR. c-FLIP knockdown induces ligand-independent DR5-, FADD-, caspase-8-, and caspase-9-dependent apoptosis in breast cancer cells. Biochem Pharmacol 2008, 76:1694-1704. 10.1016/j.bcp.2008.09.007, 2610355, 18840411.
23. Nam SY, Amoscato AA, Lee YJ. Low glucose-enhanced TRAIL cytotoxicity is mediated through the ceramide-Akt-FLIP pathway. Oncogene 2002, 21:337-346. 10.1038/sj.onc.1205068, 11821946.
24. Cenni V, Maraldi NM, Ruggeri A, Secchiero P, Del Coco R, De Pol A, Cocco L, Marmiroli S. Sensitization of multidrug resistant human ostesarcoma cells to Apo2 Ligand/TRAIL-induced apoptosis by inhibition of the Akt/PKB kinase. Int J Oncol 2004, 25:1599-1608.
25. Park SJ, Wu CH, Choi MR, Najafi F, Emami A, Safa AR. P-glycoprotein enhances TRAIL-triggered apoptosis in multidrug resistant cancer cells by interacting with the death receptor DR5. Biochem Pharmacol 2006, 72:293-307. 10.1016/j.bcp.2006.04.024, 16753135.
26. Krishna R, Mayer LD. Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur J Pharm Sci 2000, 11:265-283. 10.1016/S0928-0987(00)00114-7, 11033070.
27. Safa AR, Day TW, Wu CH. Cellular FLICE-like inhibitory protein (C-FLIP): a novel target for cancer therapy. Curr Cancer Drug Targets 2008, 8:37-46. 10.2174/156800908783497087, 18288942.
28. An J, Yang DY, Xu QZ, Zhang SM, Huo YY, Shang ZF, Wang Y, Wu DC, Zhou PK. DNA-dependent protein kinase catalytic subunit modulates the stability of c-Myc oncoprotein. Mol Cancer 2008, 7:32. 10.1186/1476-4598-7-32, 2383926, 18426604.
29. Nakamura Y, Sato H, Motokura T. Development of multidrug resistance due to multiple factors including P-glycoprotein overexpression under K-selection after MYC and HRAS oncogene activation. Int J Cancer 2006, 118:2448-2454. 10.1002/ijc.21691, 16353156.
30. He Y, Zhang J, Yuan Y. The role of c-myc in regulating mdr1 gene expression in tumor cell line KB. Chin Med J (Engl) 2000, 113:848-851.
31. Klefstrom J, Verschuren EW, Evan G. c-Myc augments the apoptotic activity of cytosolic death receptor signaling proteins by engaging the mitochondrial apoptotic pathway. J Biol Chem 2002, 277:43224-43232. 10.1074/jbc.M206967200, 12202489.
32. Zhang J, Hawkins SF, Glenn MA, Lin K, Johnson GG, Carter A, Cawley JC, Pettitt AR. Akt is activated in chronic lymhocytic leukemia cells and delivers a pro-survival signal: the therapeutic potential of Akt inhibition. Haematologica 2010, 95:110-118. 10.3324/haematol.2009.010272, 2805750, 19713228.
33. Mantovani I, Cappellini A, Tazzari PL, Papa V, Cocco L, Martelli AM. Caspase-dependent cleavage of 170-kDa P-glycoprotein during apoptosis of human T-lymphoblastoid CEM cells. J Cell Physiol 2006, 207:836-844. 10.1002/jcp.20628, 16526059.
34. Affar EB, Germain M, Winstall E, Vodenicharov M, Shah RG, Salvesen GS, Poirier GG. Caspase-3-mediated processing of poly(ADP-ribose) glycohydrolase during apoptosis. J Biol Chem 2001, 276:2935-2942. 10.1074/jbc.M007269200, 11053413.
35. Graham KL, Gustin KE, Rivera C, Kuyumcu-Martinez NM, Choe SS, Lloyd RE, Sarnow P, Utz PJ. Proteolytic cleavage of the catalytic subunit of DNA-dependent protein kinase during poliovirus infection. J Virol 2004, 78:6313-6321. 10.1128/JVI.78.12.6313-6321.2004, 416498, 15163725.
36. Park SJ, Kim MJ, Kim HB, Sohn HY, Bae JH, Kang CD, Kim SH. Cotreatment with apicidin overcomes TRAIL resistance via inhibition of Bcr-Abl signaling pathway in K562 leukemia cells. Exp Cell Res 2009, 315:1809-1818. 10.1016/j.yexcr.2009.02.024, 19268463.
37. Lee NS, Cheong HJ, Kim SJ, Kim SE, Kim CK, Lee KT, Park SK, Baick SH, Hong DS, Park HS, Won JH. Ex vivo purging of leukemia cells using tumor-necrosis-factor-related apoptosis-inducing ligand in hematopoietic stem cell transplantation. Leukemia 2003, 17:1375-1383. 10.1038/sj.leu.2402960, 12835727.
38. Nakamura H, Kawakami A, Iwamoto N, Ida H, Koji T, Eguchi K. Rapid and significant induction of TRAIL-mediated type II cells in apoptosis of primary salivary epithelial cells in primary Sjogren's syndrome. Apoptosis 2008, 13:1322-1330. 10.1007/s10495-008-0261-2, 18791828.
39. Wang Y, Engels IH, Knee DA, Nasoff M, Deveraux QL, Quon KC. Synthetic lethal targeting of MYC by activation of the DR5 death receptor pathway. Cancer Cell 2004, 5:501-512. 10.1016/S1535-6108(04)00113-8, 15144957.
40. Ricci MS, Jin Z, Dews M, Yu D, Thomas-Tikhonenko A, Dicker DT, El-Deiry WS. Direct repression of FLIP expression by c-myc is a major determinant of TRAIL sensitivity. Mol Cell Biol 2004, 24:8541-8555. 10.1128/MCB.24.19.8541-8555.2004, 516765, 15367674.
41. Han Z, Hong L, Han Y, Wu K, Han S, Shen H, Li C, Yao L, Qiao T, Fan D. Phospho Akt mediates multidrug resistance of gastric cancer cells through regulation of P-gp, Bcl-2 and Bax. J Exp Clin Cancer Res 2007, 26:261-268.
42. Lim JC, Kania KD, Wijesuriya H, Chawla S, Sethi JK, Pulaski L, Romero IA, Couraud PO, Weksler BB, Hladky SB, Barrand MA. Activation of beta-catenin signalling by GSK-3 inhibition increases p-glycoprotein expression in brain endothelial cells. J Neurochem 2008, 106:1855-1865.
43. David E, Sinha R, Chen J, Sun SY, Kaufman JL, Lonial S. Perifosine synergistically enhances TRAIL-induced myeloma cell apoptosis via up-regulation of death receptors. Clin Cancer Res 2008, 14:5090-5098. 10.1158/1078-0432.CCR-08-0016, 18698026.
44. Nam SY, Jung GA, Hur GC, Chung HY, Kim WH, Seol DW, Lee BL. Upregulation of FLIP(S) by Akt, a possible inhibition mechanism of TRAIL-induced apoptosis in human gastric cancers. Cancer Sci 2003, 94:1066-1073. 10.1111/j.1349-7006.2003.tb01402.x, 14662022.
45. Gul O, Basaga H, Kutuk O. Apoptotic blocks and chemotherapy resistance: strategies to identify Bcl-2 protein signatures. Brief Funct Genomic Proteomic 2008, 7:27-34. 10.1093/bfgp/eln002, 18283052.
46. Del Poeta G, Bruno A, Del Principe MI, Venditti A, Maurillo L, Buccisano F, Stasi R, Neri B, Luciano F, Siniscalchi A, et al. Deregulation of the mitochondrial apoptotic machinery and development of molecular targeted drugs in acute myeloid leukemia. Curr Cancer Drug Targets 2008, 8:207-222. 10.2174/156800908784293640, 18473734.
47. Nuessler V, Stotzer O, Gullis E, Pelka-Fleischer R, Pogrebniak A, Gieseler F, Wilmanns W. Bcl-2, bax and bcl-xL expression in human sensitive and resistant leukemia cell lines. Leukemia 1999, 13:1864-1872. 10.1038/sj/leu/2401571, 10557064.
48. Ji M, Li J, Yu H, Ma D, Ye J, Sun X, Ji C. Simultaneous targeting of MCL1 and ABCB1 as a novel strategy to overcome drug resistance in human leukaemia. Br J Haematol 2009, 145:648-656. 10.1111/j.1365-2141.2009.07678.x, 19344413.