Calyculin A causes sensitization to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by ROSmediated down-regulation of cellular FLICE-inhibiting protein (c-FLIP) and by enhancing death receptor 4 mRNA stabilization

Apoptosis

Volumn 17, Issue 11, 2012, Pages 1223-1234

  Woo, Seon Min ^a   Min, Kyoung Jin ^a   Kwon, Taeg Kyu ^a  

^a Keimyung University   (South Korea)

Author keywords

c FLIP(L); Calyculin A; Death receptor; Protein phosphatase; Reactive oxygen species; TRAIL

Indexed keywords

CALYCULIN A; CASPASE 3; COMPLEMENTARY DNA; DEATH RECEPTOR 4; FLICE INHIBITORY PROTEIN; MESSENGER RNA; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 1; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CONTROLLED STUDY; DNA TRANSFECTION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; LUNG ADENOCARCINOMA; MOUSE; NONHUMAN; OSTEOSARCOMA CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIZATION; WESTERN BLOTTING;

APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL LINE, TUMOR; DOWN-REGULATION; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; MODELS, BIOLOGICAL; OXAZOLES; PROTEIN PHOSPHATASE 1; REACTIVE OXYGEN SPECIES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA STABILITY; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; UP-REGULATION;

EID: 84868139074     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-012-0753-y     Document Type: Article

References (69)

1. Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, Sutherland GR, Smith TD, Rauch C, Smith CA et al (1995) Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3(6):673-682 (Pubitemid 26091143)
2. Pan G, Ni J, Wei YF, Yu G, Gentz R, Dixit VM (1997) An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 277(5327):815-818 (Pubitemid 27366732)
3. Pan G, O'Rourke K, Chinnaiyan AM, Gentz R, Ebner R, Ni J, Dixit VM (1997) The receptor for the cytotoxic ligand TRAIL. Science 276(5309):111-113 (Pubitemid 27161256)
4. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, Goddard AD, Godowski P, Ashkenazi A (1997) Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277(5327):818-821 (Pubitemid 27366733)
5. Walczak H, Degli-Esposti MA, Johnson RS, Smolak PJ, Waugh JY, Boiani N, Timour MS, Gerhart MJ, Schooley KA, Smith CA, Goodwin RG, Rauch CT (1997) TRAIL-R2: a novel apoptosismediating receptor for TRAIL. EMBO J 16(17):5386-5397. doi: 10.1093/emboj/16.17.5386 (Pubitemid 27380146)
6. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104(2):155-162. doi:10.1172/jci6926
7. Leverkus M, Neumann M, Mengling T, Rauch CT, Brocker EB, Krammer PH, Walczak H (2000) Regulation of tumor necrosis factor-related apoptosis-inducing ligand sensitivity in primary and transformed human keratinocytes. Cancer Res 60(3):553-559 (Pubitemid 30094550)
8. Jin Z, McDonald ER 3rd, Dicker DT, El-Deiry WS (2004) 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 279(34):35829-35839. doi:10.1074/jbc.M405538200 (Pubitemid 39100590)
9. Kelly MM, Hoel BD, Voelkel-Johnson C (2002) Doxorubicin pretreatment sensitizes prostate cancer cell lines to TRAIL induced apoptosis which correlates with the loss of c-FLIP expression. Cancer Biol Ther 1(5):520-527
10. Ng CP, Zisman A, Bonavida B (2002) Synergy is achieved by complementationwithApo2L/TRAILand actinomycinDinApo2L/ TRAIL-mediated apoptosis of prostate cancer cells: role of XIAP in resistance. Prostate 53(4):286-299. doi:10.1002/pros.10155 (Pubitemid 35398499)
11. Walczak H, Bouchon A, Stahl H, Krammer PH (2000) Tumor necrosis factor-related apoptosis-inducing ligand retains its apoptosis-inducing capacity on Bcl-2- or Bcl-xL-overexpressing chemotherapy-resistant tumor cells. Cancer Res 60(11):3051-3057 (Pubitemid 30395834)
12. Zhang Y, Zhang B (2008) TRAIL resistance of breast cancer cells is associated with constitutive endocytosis of death receptors 4 and 5. Mol Cancer Res 6(12):1861-1871. doi:10.1158/1541-7786.mcr-08-0313
13. McConnell JL, Wadzinski BE (2009) Targeting protein serine/threonine phosphatases for drug development. Mol Pharmacol 75(6):1249-1261. doi:10.1124/mol.108.053140
14. Shi Y (2009) Serine/threonine phosphatases: mechanism through structure. Cell 139(3):468-484. doi:10.1016/j.cell.2009.10.006
15. Prickett TD, Brautigan DL (2006) The alpha4 regulatory subunit exerts opposing allosteric effects on protein phosphatases PP6 and PP2A. J Biol Chem 281(41):30503-30511. doi:10.1074/jbc.M601054200 (Pubitemid 44582107)
16. Swingle M, Ni L, Honkanen RE (2007) Small-molecule inhibitors of ser/thr protein phosphatases: specificity, use and common forms of abuse. Methods Mol Biol 365:23-38. doi:10.1385/1-59745-267-X:23
17. Tanaka H, Yoshida K, Okamura H, Morimoto H, Nagata T, Haneji T (2007) Calyculin A induces apoptosis and stimulates phosphorylation of p65NF-kappaB in human osteoblastic osteosarcoma MG63 cells. Int J Oncol 31(2):389-396
18. Morimoto Y, Ohba T, Kobayashi S, Haneji T (1997) The protein phosphatase inhibitors okadaic acid and calyculin A induce apoptosis in human osteoblastic cells. Exp Cell Res 230(2): 181-186. doi:10.1006/excr.1996.3404 (Pubitemid 27190638)
19. Fujita M, Seta C, Fukuda J, Kobayashi S, Haneji T (1999) Induction of apoptosis in human oral squamous carcinoma cell lines by protein phosphatase inhibitors. Oral Oncol 35(4):401-408 (Pubitemid 29276976)
20. Song Q, Lavin MF (1993) Calyculin A, a potent inhibitor of phosphatases-1 and -2A, prevents apoptosis. Biochem Biophys Res Commun 190(1):47-55 (Pubitemid 23227286)
21. Luo Y, Kessel D (1996) The phosphatase inhibitor calyculin antagonizes the rapid initiation of apoptosis by photodynamic therapy. Biochem Biophys Res Commun 221(1):72-76. doi: 10.1006/bbrc.1996.0547 (Pubitemid 26136425)
22. Kiss A, Lontay B, Becsi B, Markasz L, Olah E, Gergely P, Erdodi F (2008) Myosin phosphatase interacts with and dephosphorylates the retinoblastoma protein in THP-1 leukemic cells: its inhibition is involved in the attenuation of daunorubicin-induced cell death by calyculin-A. Cell Signal 20(11):2059-2070. doi: 10.1016/j.cellsig.2008.07.018
23. LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 20,70-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5(2): 227-231
24. Lee TJ, Um HJ, Min do S, Park JW, Choi KS, Kwon TK (2009) Withaferin A sensitizes TRAIL-induced apoptosis through reactive oxygen species-mediated up-regulation of death receptor 5 and down-regulation of c-FLIP. Free Radic Biol Med 46(12):1639-1649. doi:10.1016/j.freeradbiomed.2009.03.022
25. Jang JH, Lee TJ, Yang ES, Min do S, Kim YH, Kim SH, Choi YH, Park JW, Choi KS, Kwon TK (2010) Compound C sensitizes Caki renal cancer cells to TRAIL-induced apoptosis through reactive oxygen species-mediated down-regulation of c-FLIPL and Mcl-1. Exp Cell Res 316(13):2194-2203. doi:10.1016/j.yexcr.2010. 04.028
26. Um HJ, Oh JH, Kim YN, Choi YH, Kim SH, Park JW, Kwon TK (2010) The coffee diterpene kahweol sensitizes TRAIL-induced apoptosis in renal carcinoma Caki cells through down-regulation of Bcl-2 and c-FLIP. Chem Biol Interact 186(1):36-42. doi: 10.1016/j.cbi.2010.04.013
27. Sayers TJ, Brooks AD, Koh CY, Ma W, Seki N, Raziuddin A, Blazar BR, Zhang X, Elliott PJ, Murphy WJ (2003) The proteasome inhibitor PS-341 sensitizes neoplastic cells to TRAILmediated apoptosis by reducing levels of c-FLIP. Blood 102(1):303-310. doi:10.1182/blood-2002-09-2975 (Pubitemid 36759669)
28. Zhang S, Shen HM, Ong CN (2005) Down-regulation of c-FLIP contributes to the sensitization effect of 3,3′-diindolylmethane on TRAIL-induced apoptosis in cancer cells. Mol Cancer Ther 4(12):1972-1981. doi:10.1158/1535- 7163.mct-05-0249 (Pubitemid 43056980)
29. Kim H, Kim EH, Eom YW, Kim WH, Kwon TK, Lee SJ, Choi KS (2006) Sulforaphane sensitizes tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-resistant hepatoma cells to TRAIL-induced apoptosis through reactive oxygen speciesmediated up-regulation of DR5. Cancer Res 66(3):1740-1750. doi:10.1158/0008-5472.can-05-1568 (Pubitemid 43259959)
30. Chaudhari AA, Seol JW, Kim SJ, Lee YJ, Kang HS, Kim IS, Kim NS, Park SY (2007) Reactive oxygen species regulate Bax translocation and mitochondrial transmembrane potential, a possible mechanism for enhanced TRAIL-induced apoptosis by CCCP. Oncol Rep 18(1):71-76
31. Kim YH, Jung EM, Lee TJ, Kim SH, Choi YH, Park JW, Choi KS, Kwon TK (2008) Rosiglitazone promotes tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by reactive oxygen species-mediated up-regulation of death receptor 5 and down-regulation of c-FLIP. Free Radic Biol Med 44(6):1055-1068. doi:10.1016/j.freeradbiomed.2007.12.001
32. Yamaguchi M, Sasaki J, Kuwana M, Sakai M, Okamura N, Ishibashi S (1993) Cytosolic protein phosphatase may turn off activated NADPH oxidase in guinea pig neutrophils. Arch Biochem Biophys 306(1):209-214 (Pubitemid 23291305)
33. Forman HJ, Zhou H, Gozal E, Torres M (1998) Modulation of the alveolar macrophage superoxide production by protein phosphorylation. Environ Health Perspect 106(Suppl 5):1185-1190 (Pubitemid 28554526)
34. Dang PM, Raad H, Derkawi RA, Boussetta T, Paclet MH, Belambri SA, Makni-Maalej K, Kroviarski Y, Morel F, Gougerot-Pocidalo MA, El-Benna J (2011) The NADPH oxidase cytosolic component p67phox is constitutively phosphorylated in human neutrophils: regulation by a protein tyrosine kinase, MEK1/2 and phosphatases 1/2A. Biochem Pharmacol 82(9):1145-1152. doi: 10.1016/j.bcp.2011. 07.070
35. Frese S, Frese-Schaper M, Andres AC, Miescher D, Zumkehr B, Schmid RA (2006) Cardiac glycosides initiate Apo2L/TRAILinduced apoptosis in non-small cell lung cancer cells by up-regulation of death receptors 4 and 5. Cancer Res 66(11): 5867-5874. doi:10.1158/0008-5472.can-05-3544 (Pubitemid 43927141)
36. Lee JT, Lee TJ, Kim CH, Kim NS, Kwon TK (2009) Overexpression of Reticulon 3 (RTN3) enhances TRAIL-mediated apoptosis via up-regulation of death receptor 5 (DR5) and downregulation of c-FLIP. Cancer Lett 279(2):185-192. doi:10.1016/j.canlet.2009.01.035
37. Sun H, Wang Y (2012) Novel Ser/Thr protein phosphatases in cell death regulation. Physiology (Bethesda) 27(1):43-52. doi: 10.1152/physiol.00034.2011
38. Janssens V, Rebollo A (2012) The role and therapeutic potential of Ser/Thr phosphatase PP2A in apoptotic signalling networks in human cancer cells. Curr Mol Med 12(3):268-287
39. Tocharus J, Chongthammakun S, Govitrapong P (2008) Melatonin inhibits amphetamine-induced nitric oxide synthase mRNA overexpression in microglial cell lines. Neurosci Lett 439(2): 134-137. doi:10.1016/j.neulet.2008.05.036
40. Inomata M, Saijo N, Kawashima K, Kaneko A, Fujiwara Y, Kunikane H, Tanaka Y (1995) Induction of apoptosis in cultured retinoblastoma cells by the protein phosphatase inhibitor, okadaic acid. J Cancer Res Clin Oncol 121(12):729-738
41. Goto K, Fukuda J, Haneji T (2002) Okadaic acid stimulates apoptosis through expression of Fas receptor and Fas ligand in human oral squamous carcinoma cells. Oral Oncol 38(1):16-22 (Pubitemid 34076568)
42. Sheikh MS, Garcia M, Zhan Q, Liu Y, Fornace AJ Jr (1996) Cell cycle-independent regulation of p21Waf1/Cip1 and retinoblastoma protein during okadaic acid-induced apoptosis is coupled with induction of Bax protein in human breast carcinoma cells. Cell Growth Differ 7(12):1599-1607 (Pubitemid 26415155)
43. Rami BG, Chin LS, Lazio BE, Singh SK (2003) Okadaicacid-induced apoptosis in malignant glioma cells. Neurosurg Focus 14(2):e4
44. Haldar S, Jena N, Croce CM (1995) Inactivation of Bcl-2 by phosphorylation. Proc Natl Acad Sci USA 92(10):4507-4511
45. Benito A, Lerga A, Silva M, Leon J, Fernandez-Luna JL (1997) Apoptosis of human myeloid leukemia cells induced by an inhibitor of protein phosphatases (okadaic acid) is prevented by Bcl-2 and Bcl-X(L). Leukemia 11(7):940-944 (Pubitemid 27345938)
46. Cabado AG, Leira F, Vieytes MR, Vieites JM, Botana LM (2004) Cytoskeletal disruption is the key factor that triggers apoptosis in okadaic acid-treated neuroblastoma cells. Arch Toxicol 78(2): 74-85. doi:10.1007/s00204-003-0505-4 (Pubitemid 38316662)
47. Ravindran J, Gupta N, Agrawal M, Bala Bhaskar AS, Lakshmana Rao PV (2011) Modulation of ROS/MAPK signaling pathways by okadaic acid leads to cell death via, mitochondrial mediated caspase-dependent mechanism. Apoptosis 16(2):145-161. doi: 10.1007/s10495-010-0554-0
48. Chatfield K, Eastman A (2004) Inhibitors of protein phosphatases 1 and 2A differentially prevent intrinsic and extrinsic apoptosis pathways. Biochem Biophys Res Commun 323(4):1313-1320. doi:10.1016/j.bbrc.2004.09.003 (Pubitemid 39296568)
49. Song Q, Baxter GD, Kovacs EM, Findik D, Lavin MF (1992) Inhibition of apoptosis in human tumour cells by okadaic acid. J Cell Physiol 153(3):550-556. doi:10.1002/jcp.1041530316
50. Ohoka Y, Nakai Y, Mukai M, Iwata M (1993) Okadaic acid inhibits glucocorticoid-induced apoptosis in T cell hybridomas at its late stage. Biochem Biophys Res Commun 197(2):916-921. doi:10.1006/bbrc.1993.2566 (Pubitemid 24034657)
51. Leira F, Vieites JM, Vieytes MR, Botana LM (2001) Apoptotic events induced by the phosphatase inhibitor okadaic acid in normal human lung fibroblasts. Toxicol In Vitro 15(3):199-208 (Pubitemid 32476830)
52. Golstein J, Swillens S, Dumont JE (1995) Comparative cytotoxic effects of two protein phosphatase inhibitors, okadaic acid and calyculin A, on thyroid cells. Cell Death Differ 2(4):321-329
53. Hong HN, Yoon SY, Suh J, Lee JH, Kim D (2002) Differential activation of caspase-3 at two maturational stages during okadaic acid-induced rat neuronal death. Neurosci Lett 334(1):63-67 (Pubitemid 35335933)
54. Micheau O, Lens S, Gaide O, Alevizopoulos K, Tschopp J (2001) NF-kappaB signals induce the expression of c-FLIP. Mol Cell Biol 21(16):5299-5305. doi:10.1128/mcb.21.16.5299-5305.2001 (Pubitemid 32702435)
55. Panka DJ, Mano T, Suhara T, Walsh K, Mier JW (2001) Phosphatidylinositol 3-kinase/Akt activity regulates c-FLIP expression in tumor cells. J Biol Chem 276(10):6893-6896. doi: 10.1074/jbc.C000569200
56. Fukazawa T, Fujiwara T, Uno F, Teraishi F, Kadowaki Y, Itoshima T, Takata Y, Kagawa S, Roth JA, Tschopp J, Tanaka N (2001) Accelerated degradation of cellular FLIP protein through the ubiquitin-proteasome pathway in p53-mediated apoptosis of human cancer cells. Oncogene 20(37):5225-5231. doi:10.1038/sj.onc. 1204673 (Pubitemid 32844053)
57. Zhou XD, Yu JP, Chen HX, Yu HG, Luo HS (2005) Expression of cellular FLICE-inhibitory protein and its association with p53 mutation in colon cancer. World J Gastroenterol 11(16): 2482-2485
58. Ricci MS, Jin Z, Dews M, Yu D, Thomas-Tikhonenko A, Dicker DT, El-Deiry WS (2004) Direct repression of FLIP expression by c-myc is a major determinant of TRAIL sensitivity. Mol Cell Biol 24(19):8541-8555. doi:10.1128/mcb.24.19. 8541-8555.2004 (Pubitemid 39245075)
59. Lutterbach B, Hann SR (1994) Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis. Mol Cell Biol 14(8): 5510-5522 (Pubitemid 24235980)
60. Bhatia K, Huppi K, Spangler G, Siwarski D, Iyer R, Magrath I (1993) Point mutations in the c-Myc transactivation domain are common in Burkitt's lymphoma and mouse plasmacytomas. Nat Genet 5(1):56-61. doi:10.1038/ng0993-56 (Pubitemid 23261519)
61. Henriksson M, Bakardjiev A, Klein G, Luscher B (1993) Phosphorylation sites mapping in the N-terminal domain of c-myc modulate its transforming potential. Oncogene 8(12):3199-3209 (Pubitemid 23342616)
62. Noguchi K, Kitanaka C, Yamana H, Kokubu A, Mochizuki T, Kuchino Y (1999) Regulation of c-Myc through phosphorylation at Ser-62 and Ser-71 by c-Jun N-terminal kinase. J Biol Chem 274(46):32580-32587 (Pubitemid 129535283)
63. Gupta S, Seth A, Davis RJ (1993) Transactivation of gene expression by Myc is inhibited by mutation at the phosphorylation sites Thr-58 and Ser-62. Proc Natl Acad Sci USA 90(8): 3216-3220 (Pubitemid 23111336)
64. Li W, Zhang X, Olumi AF (2007) MG-132 sensitizes TRAILresistant prostate cancer cells by activating c-Fos/c-Jun heterodimers and repressing c-FLIP(L). Cancer Res 67(5):2247-2255. doi:10.1158/0008-5472.can-06-3793 (Pubitemid 46424244)
65. Pulverer BJ, Kyriakis JM, Avruch J, Nikolakaki E, Woodgett JR (1991) Phosphorylation of c-jun mediated by MAP kinases. Nature 353(6345):670-674. doi:10.1038/353670a0 (Pubitemid 21912588)
66. Monje P, Marinissen MJ, Gutkind JS (2003) Phosphorylation of the carboxyl-terminal transactivation domain of c-Fos by extracellular signal-regulated kinase mediates the transcriptional activation of AP-1 and cellular transformation induced by platelet-derived growth factor. Mol Cell Biol 23(19):7030-7043 (Pubitemid 37214669)
67. Park SJ, Sohn HY, Yoon J, Park SI (2009) Down-regulation of FoxO-dependent c-FLIP expression mediates TRAIL-induced apoptosis in activated hepatic stellate cells. Cell Signal 21(10):1495-1503. doi:10.1016/j.cellsig. 2009.05.008
68. Srivastava RK, Unterman TG, Shankar S (2010) FOXO transcription factors and VEGF neutralizing antibody enhance antiangiogenic effects of resveratrol. Mol Cell Biochem 337(1-2): 201-212. doi:10.1007/s11010-009-0300-5
69. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96(6):857-868 (Pubitemid 29165088)