Combined treatment with TRAIL and PPARγ ligands overcomes chemoresistance of ovarian cancer cell lines

Journal of Cancer Research and Clinical Oncology

Volumn 137, Issue 5, 2011, Pages 875-886

  Bräutigam, Karen ^a   Biernath Wüpping, Julia ^b   Bauerschlag, Dirk O ^a   Von Kaisenberg, Constantin S ^c   Jonat, Walter ^b   Maass, Nicolai ^a   Arnold, Norbert ^b   Meinhold Heerlein, Ivo ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Apoptosis; Drug resistance; Ovarian cancer; PPAR ligands; Proliferation; TRAIL

Indexed keywords

15 DEOXY DELTA 12,14 PROSTAGLANDIN J2; 2 CHLORO 5 NITROBENZANILIDE; CASPASE 8; CIGLITAZONE; CISPLATIN; DEATH RECEPTOR 4; DEATH RECEPTOR 5; DOCETAXEL; ETOPOSIDE; FLICE INHIBITORY PROTEIN; GEMCITABINE; PACLITAXEL; PEMETREXED; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RECOMBINANT TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TROGLITAZONE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR 3; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR 4; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL PROLIFERATION; CYTOSTASIS; DOSE RESPONSE; DRUG MECHANISM; DRUG POTENTIATION; HUMAN; IMMUNOBLOTTING; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 85027937404     PISSN: 01715216     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00432-010-0952-2     Document Type: Article

References (60)

1. Abedini MR, Qiu Q, Yan X, Tsang BK (2004) Possible role of flice-like inhibitory protein (flip) in chemoresistant ovarian cancer cells in vitro. Oncogene 23(42):6997-7004 (Pubitemid 39319162)
2. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281(5381):1305-1308 (Pubitemid 28406815)
3. 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
4. Asselin E, Mills GB, Tsang BK (2001) Xiap regulates akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res 61(5):1862-1868 (Pubitemid 32692000)
5. Austin CD, Lawrence DA, Peden AA, Varfolomeev EE, Totpal K, De Maziere AM, Klumperman J, Arnott D, Pham V, Scheller RH, Ashkenazi A (2006) Death-receptor activation halts clathrin-dependent endocytosis. Proc Natl Acad Sci USA 103(27):10283-10288 (Pubitemid 44051158)
6. Avis I, Martinez A, Tauler J, Zudaire E, Mayburd A, Abu-Ghazaleh R, Ondrey F, Mulshine JL (2005) Inhibitors of the arachidonic acid pathway and peroxisome proliferator-activated receptor ligands have superadditive effects on lung cancer growth inhibition. Cancer Res 65(10):4181-4190 (Pubitemid 40775656)
7. Belyanskaya LL, Ziogas A, Hopkins-Donaldson S, Kurtz S, Simon HU, Stahel R, Zangemeister-Wittke U (2008) Trail-induced survival and proliferation of sclc cells is mediated by erk and dependent on trail-r2/dr5 expression in the absence of caspase-8. Lung Cancer 60(3):355-365
8. Bodmer JL, Holler N, Reynard S, Vinciguerra P, Schneider P, Juo P, Blenis J, Tschopp J (2000) Trail receptor-2 signals apoptosis through fadd and caspase-8. Nat Cell Biol 2(4):241-243
9. Bonofiglio D, Cione E, Qi H, Pingitore A, Perri M, Catalano S, Vizza D, Panno ML, Genchi G, Fuqua SA, Ando S (2009) Combined low doses of ppargamma and rxr ligands trigger an intrinsic apoptotic pathway in human breast cancer cells. Am J Pathol 175(3):1270-1280
10. Brautigam K, Bauerschlag DO, Weigel MT, Biernath-Wupping J, Bauknecht T, Arnold N, Maass N, Meinhold-Heerlein I (2009) Combination of enzastaurin and pemetrexed inhibits cell growth and induces apoptosis of chemoresistant ovarian cancer cells regulating extracellular signal-regulated kinase 1/2 phosphorylation. Transl Oncol 2(3):164-173
11. Campbell MJ, Carlberg C, Koeffer HP (2008) A role for the ppargamma in cancer therapy. PPAR Res 2008:314974
12. Cannistra SA (2004) Cancer of the ovary. N Engl J Med 351(24):2519-2529. doi:351/24/2519[pii]10.1056/NEJMra041842
13. Chang DW, Xing Z, Pan Y, Algeciras-Schimnich A, Barnhart BC, Yaish-Ohad S, Peter ME, Yang X (2002) C-flip(l) is a dual function regulator for caspase-8 activation and cd95-mediated apoptosis. EMBO J 21(14):3704-3714 (Pubitemid 34787044)
14. Fenner MH, Elstner E (2005) Peroxisome proliferator-activated receptor- gamma ligands for the treatment of breast cancer. Expert Opin Investig Drugs 14(6):557-568 (Pubitemid 40895186)
15. Fulda S, Debatin KM (2006) Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 25(34):4798-4811 (Pubitemid 44187627)
16. Gibson SB, Oyer R, Spalding AC, Anderson SM, Johnson GL (2000) Increased expression of death receptors 4 and 5 synergizes the apoptosis response to combined treatment with etoposide and trail. Mol Cell Biol 20(1):205-212 (Pubitemid 30002562)
17. Griffith TS, Chin WA, Jackson GC, Lynch DH, Kubin MZ (1998) Intracellular regulation of trail-induced apoptosis in human melanoma cells. J Immunol 161(6):2833-2840 (Pubitemid 28425704)
18. Grotzer MA, Eggert A, Zuzak TJ, Janss AJ, Marwaha S, Wiewrodt BR, Ikegaki N, Brodeur GM, Phillips PC (2000) Resistance to trail-induced apoptosis in primitive neuroectodermal brain tumor cells correlates with a loss of caspase-8 expression. Oncogene 19(40): 4604-4610
19. Han H, Shin SW, Seo CY, Kwon HC, Han JY, Kim IH, Kwak JY, Park JI (2007) 15-deoxy-delta 12, 14-prostaglandin j2 (15d-pgj 2) sensitizes human leukemic hl-60 cells to tumor necrosis factor-related apoptosis-inducing ligand (trail)-induced apoptosis through akt downregulation. Apoptosis 12(11):2101-2114 (Pubitemid 47498232)
20. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57-70 (Pubitemid 30046295)
21. Hao C, Beguinot F, Condorelli G, Trencia A, Van Meir EG, Yong VW, Parney IF, Roa WH, Petruk KC (2001) Induction and intracellular regulation of tumor necrosis factor-related apoptosis-inducing ligand (trail) mediated apotosis in human malignant glioma cells. Cancer Res 61(3):1162-1170 (Pubitemid 32174439)
22. Holen I, Croucher PI, Hamdy FC, Eaton CL (2002) Osteoprotegerin (opg) is a survival factor for human prostate cancer cells. Cancer Res 62(6):1619-1623 (Pubitemid 34408480)
23. Horak P, Pils D, Kaider A, Pinter A, Elandt K, Sax C, Zielinski CC, Horvat R, Zeillinger R, Reinthaller A, Krainer M (2005) Perturbation of the tumor necrosis factor-related apoptosis-inducing ligand cascade in ovarian cancer: overexpression of flipl and deregulation of the functional receptors dr4 and dr5. Clin Cancer Res 11(24 Pt 1):8585-8591 (Pubitemid 43005904)
24. Irmler M, Thome M, Hahne M, Schneider P, Hofmann K, Steiner V, Bodmer JL, Schroter M, Burns K, Mattmann C, Rimoldi D, French LE, Tschopp J (1997) Inhibition of death receptor signals by cellular flip. Nature 388(6638):190-195 (Pubitemid 27297457)
25. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59(4):225-249
26. Kim K, Fisher MJ, Xu SQ, el-Deiry WS (2000) Molecular determinants of response to trail in killing of normal and cancer cells. Clin Cancer Res 6(2):335-346 (Pubitemid 30111448)
27. Kim Y, Suh N, Sporn M, Reed JC (2002) An inducible pathway for degradation of flip protein sensitizes tumor cells to trail-induced apoptosis. J Biol Chem 277(25):22320-22329 (Pubitemid 34967199)
28. Kroemer G, Reed JC (2000) Mitochondrial control of cell death. Nat Med 6(5):513-519 (Pubitemid 30305900)
29. Krueger A, Schmitz I, Baumann S, Krammer PH, Kirchhoff S (2001) Cellular flice-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the cd95 death-inducing signaling complex. J Biol Chem 276(23):20633-20640
30. Lane D, Cartier A, L'Esperance S, Cote M, Rancourt C, Piche A (2004) Differential induction of apoptosis by tumor necrosis factor- related apoptosis-inducing ligand in human ovarian carcinoma cells. Gynecol Oncol 93(3):594-604 (Pubitemid 38766041)
31. Lemke J, Noack A, Adam D, Tchikov V, Bertsch U, Roder C, Schutze S, Wajant H, Kalthoff H, Trauzold A (2010) Trail signaling is mediated by dr4 in pancreatic tumor cells despite the expression of functional dr5. J Mol Med. doi:10.1007/s00109-010-0619-0
32. Li J, Feng Q, Kim JM, Schneiderman D, Liston P, Li M, Vanderhyden B, Faught W, Fung MF, Senterman M, Korneluk RG, Tsang BK (2001) Human ovarian cancer and cisplatin resistance: possible role of inhibitor of apoptosis proteins. Endocrinology 142(1):370-380 (Pubitemid 32183698)
33. Micheau O, Thome M, Schneider P, Holler N, Tschopp J, Nicholson DW, Briand C, Grutter MG (2002) The long form of flip is an activator of caspase-8 at the fas death-inducing signaling complex. J Biol Chem 277(47):45162-45171 (Pubitemid 36159119)
34. Nakata S, Yoshida T, Shiraishi T, Horinaka M, Kouhara J, Wakada M, Sakai T (2006) 15-deoxy-delta12, 14-prostaglandin j(2) induces death receptor 5 expression through mrna stabilization independently of ppargamma and potentiates trail-induced apoptosis. Mol Cancer Ther 5(7):1827-1835 (Pubitemid 44323251)
35. Okano H, Shiraki K, Inoue H, Yamanaka Y, Kawakita T, Saitou Y, Yamaguchi Y, Enokimura N, Yamamoto N, Sugimoto K, Murata K, Nakano T (2003) 15-deoxy-delta-12-14-pgj2 regulates apoptosis induction and nuclear factor-kappab activation via a peroxisome proliferator-activated receptor-gamma-independent mechanism in hepatocellular carcinoma. Lab Invest 83(10):1529-1539 (Pubitemid 37267836)
36. Partridge EE, Barnes MN (1999) Epithelial ovarian cancer: prevention, diagnosis, and treatment. CA Cancer J Clin 49(5):297-320
37. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A (1996) Induction of apoptosis by apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 271(22):12687-12690 (Pubitemid 26175834)
38. Plissonnier ML, Fauconnet S, Bittard H, Lascombe I (2010) Insights on distinct pathways of thiazolidinediones (ppargamma ligand)- promoted apoptosis in trail-sensitive or -resistant malignant urothelial cells. Int J Cancer. doi:10.1002/ijc.25189
39. Rumi MA, Ishihara S, Kazumori H, Kadowaki Y, Kinoshita Y (2004) Can ppar gamma ligands be used in cancer therapy? Curr Med Chem Anticancer Agents 4(6):465-477
40. Saelens X, Festjens N, Vande Walle L, van Gurp M, van Loo G, Vandenabeele P (2004) Toxic proteins released from mitochondria in cell death. Oncogene 23(16):2861-2874 (Pubitemid 38638848)
41. Safa AR, Day TW, Wu CH (2008) Cellular flice-like inhibitory protein (c-flip): a novel target for cancer therapy. Curr Cancer Drug Targets 8(1):37-46 (Pubitemid 351237908)
42. Sallman DA, Chen X, Zhong B, Gilvary DL, Zhou J, Wei S, Djeu JY (2007) Clusterin mediates trail resistance in prostate tumor cells. Mol Cancer Ther 6(11):2938-2947 (Pubitemid 350206772)
43. Sanlioglu AD, Dirice E, Aydin C, Erin N, Koksoy S, Sanlioglu S (2005) Surface trail decoy receptor-4 expression is correlated with trail resistance in mcf7 breast cancer cells. BMC Cancer 5:54
44. Sasaki H, Sheng Y, Kotsuji F, Tsang BK (2000) Down-regulation of x-linked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells. Cancer Res 60(20):5659-5666
45. Schimmer AD, Dalili S, Batey RA, Riedl SJ (2006) Targeting xiap for the treatment of malignancy. Cell Death Differ 13(2):179-188 (Pubitemid 43102202)
46. Schultze K, Bock B, Eckert A, Oevermann L, Ramacher D, Wiestler O, Roth W (2006) Troglitazone sensitizes tumor cells to trail-induced apoptosis via down-regulation of flip and survivin. Apoptosis 11(9):1503-1512 (Pubitemid 44253668)
47. Shipman CM, Croucher PI (2003) Osteoprotegerin is a soluble decoy receptor for tumor necrosis factor-related apoptosis-inducing ligand/apo2 ligand and can function as a paracrine survival factor for human myeloma cells. Cancer Res 63(5):912-916 (Pubitemid 36278418)
48. Sporn MB, Suh N, Mangelsdorf DJ (2001) Prospects for prevention and treatment of cancer with selective ppargamma modulators (sparms). Trends Mol Med 7(9):395-400 (Pubitemid 32823988)
49. Sussman RT, Ricci MS, Hart LS, Sun SY, El-Deiry WS (2007) Chemotherapy-resistant side-population of colon cancer cells has a higher sensitivity to trail than the non-sp, a higher expression of c-myc and trail-receptor dr4. Cancer Biol Ther 6(9):1490-1495 (Pubitemid 351590363)
50. Tomek S, Horak P, Pribill I, Haller G, Rossler M, Zielinski CC, Pils D, Krainer M (2004) Resistance to trail-induced apoptosis in ovarian cancer cell lines is overcome by co-treatment with cytotoxic drugs. Gynecol Oncol 94(1):107-114 (Pubitemid 38950505)
51. Van Valen F, Fulda S, Schafer KL, Truckenbrod B, Hotfilder M, Poremba C, Debatin KM, Winkelmann W (2003) Selective and nonselective toxicity of trail/apo2l combined with chemotherapy in human bone tumour cells vs. Normal human cells. Int J Cancer 107(6):929-940 (Pubitemid 37429834)
52. Vaux DL, Silke J (2003) Mammalian mitochondrial iap binding proteins. Biochem Biophys Res Commun 304(3):499-504 (Pubitemid 36506522)
53. Vignati S, Codegoni A, Polato F, Broggini M (2002) Trail activity in human ovarian cancer cells: potentiation of the action of cytotoxic drugs. Eur J Cancer 38(1):177-183 (Pubitemid 34031834)
54. Wajant H, Pfizenmaier K, Scheurich P (2002) Tnf-related apoptosis inducing ligand (trail) and its receptors in tumor surveillance and cancer therapy. Apoptosis 7(5):449-459
55. Wang P, Zhang J, Bellail A, Jiang W, Hugh J, Kneteman NM, Hao C (2007) Inhibition of rip and c-flip enhances trail-induced apoptosis in pancreatic cancer cells. Cell Signal 19(11):2237-2246 (Pubitemid 47361680)
56. 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
57. Yang X, Xing H, Gao Q, Chen G, Lu Y, Wang S, Ma D (2005) Regulation of htra2/omi by x-linked inhibitor of apoptosis protein in chemoresistance in human ovarian cancer cells. Gynecol Oncol 97(2):413-421 (Pubitemid 40614884)
58. Yoshida T, Zhang Y, Rosado LA, Zhang B (2009) Repeated treatment with subtoxic doses of trail induces resistance to apoptosis through its death receptors in mda-mb-231 breast cancer cells. Mol Cancer Res 7(11):1835-1844
59. Zhang Y, Yoshida T, Zhang B (2009) Trail induces endocytosis of its death receptors in mda-mb-231 breast cancer cells. Cancer Biol Ther 8(10):917-922
60. Zou W, Liu X, Yue P, Khuri FR, Sun SY (2007) Ppargamma ligands enhance trail-induced apoptosis through dr5 upregulation and c-flip downregulation in human lung cancer cells. Cancer Biol Ther 6(1):99-106 (Pubitemid 46294186)