N-(4-hydroxyphenyl) retinamide (4HPR) enhances TRAIL-mediated apoptosis through enhancement of a mitochondrial-dependent amplification loop in ovarian cancer cell lines

Cell Death and Differentiation

Volumn 11, Issue 5, 2004, Pages 527-541

  Cueloo, M ^a,b   Coats, A O ^a   Darko, I ^a   Ettenberg, S A ^a   Gardner, G J ^a   Nau, M M ^a   Liu, J R ^c   Birrer, M J ^a   Lipkowitz, Stan ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Death receptor; Fenretinide (4HPR); Ovarian cancer; TRAIL

Indexed keywords

CASPASE 8; CASPASE 9; CYTOCHROME C; DEATH RECEPTOR 5; FENRETINIDE; PROTEIN BCL XL; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; CANCER CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; OVARY CANCER; PRIORITY JOURNAL; REVIEW; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASES; CYTOCHROMES C; DNA FRAGMENTATION; FEMALE; FENRETINIDE; HUMANS; MEMBRANE GLYCOPROTEINS; MITOCHONDRIA; OVARY; RETINOID X RECEPTORS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 2442697830     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401387     Document Type: Review

References (71)

1. Ashkenazi A and Dixit VM (1998) Death receptors: signaling and modulation. Science 281: 1305-1308
2. Marsters SA, Pitti RA, Sheridan JP and Ashkenazi A (1999) Control of apoptosis signaling by Apo2 ligand. Recent Prog. Horm. Res. 54: 225-234
3. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, Ramakrishnan L, Gray CL, Baker K, Wood WI, Goddard AD, Godowski P and Ashkenazi A (1997) Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277: 818-821
4. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC and Lynch DH (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5: 157-163
5. Roth W, Isenmann S, Naumann U, Kugler S, Bahr M, Dichgans J, Ashkenazi A and Weller M (1999) Locoregional Apo2L/TRAIL eradicates intracranial human malignant glioma xenografts in athymic mice in the absence of neurotoxicity. Biochem. Biophys. Res. Commun. 265: 479-483
6. Keane MM, Ettenberg SA, Nau MM, Russell EK and Lipkowitz S (1999) Chemotherapy augments TRAIL-induced apoptosis in breast cell lines. Cancer Res. 59: 734-741
7. Cuello M, Ettenberg SA, Nau MM and Lipkowitz S (2001) Synergistic induction of apoptosis by the combination of trail and chemotherapy in chemoresistant ovarian cancer cells. Gynecol. Oncol. 81: 380-390
8. Snell V, Clodi K, Zhao S, Goodwin R, Thomas EK, Morris SW, Kadin ME, Cabanillas F, Andreeff M and Younes A (1997) Activity of TNF-related apoptosis-inducing ligand (TRAIL) in haematological malignancies. Br. J. Haematol. 99: 618-624
9. Lacour S, Hammann A, Wotawa A, Corcos L, Solary E and Dimanche-Boitrel MT (2001) Anticancer agents sensitize tumor cells to tumor necrosis factor-related apoptosis-inducing ligand-mediated caspase-8 activation and apoptosis. Cancer Res. 61: 1645-1651
10. Shin S, Sung BJ, Cho YS, Kim HJ, Ha NC, Hwang JI, Chung CW, Jung YK and Oh BH (2001) An anti-apoptotic protein human survivin is a direct inhibitor of caspase-3 and -7. Biochemistry 40: 1117-1123
11. Burns TF and El-Deiry WS (2001) Identification of inhibitors of TRAIL-induced death (ITIDs) in the TRAIL-sensitive colon carcinoma cell line SW480 using a genetic approach. J. Biol. Chem. 276: 37879-37886
12. Kim K, Fisher MJ, Xu SQ and el-Deiry WS (2000) Molecular determinants of response to TRAIL in killing of normal and cancer cells. Clin. Cancer Res. 6: 335-346
13. Deveraux QL and Reed JC (1999) IAP family proteins - suppressors of apoptosis. Genes Dev. 13: 239-252
14. Ravi R, Bedi GC, Engstrom LW, Zeng Q, Mookerjee B, Gelinas C, Fuchs EJ and Bedi A (2001) Regulation of death receptor expression and TRAIL/Apo2L-induced apoptosis by NF-kappaB. Nat. Cell Biol. 3: 409-416
15. Keane MM, Rubinstein Y, Cuello M, Ettenberg SA, Banerjee P, Nau MM and Lipkowitz S (2000) Inhibition of NF-kappaB activity enhances TRAIL mediated apoptosis in breast cancer cell lines. Breast Cancer Res. Treat. 64: 211-219
16. Nagane M, Pan G, Weddle JJ, Dixit VM, Cavenee WK and Huang HJ (2000) Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res. 60: 847-853
17. Yamanaka T, Shiraki K, Sugimoto K, Ito T, Fujikawa K, Ito M, Takase K, Moriyama M, Nakano T and Suzuki A (2000) Chemotherapeutic agents augment TRAIL-induced apoptosis in human hepatocellular carcinoma cell lines. Hepatology 32: 482-490
18. Ulukaya E and Wood EJ (1999) Fenretinide and its relation to cancer. Cancer Treat. Rev. 25: 229-235
19. Zhang D, Holmes WF, Wu S, Soprano DR and Soprano KJ (2000) Retinoids and ovarian cancer. J. Cell Physiol. 185: 1-20
20. Sabichi AL, Hendricks DT, Bober MA and Birrer MJ (1998) Retinoic acid receptor beta expression and growth inhibition of gynecologic cancer cells by the synthetic retinoid N-(4-hydroxyphenyl) retinamide. J. Natl. Cancer Inst. 90: 597-605
21. Wu JM, DiPietrantonio AM and Hsieh TC (2001) Mechanism of fenretinide (4HPR)-induced cell death. Apoptosis 6: 377-388
22. Lovat PE, Ranalli M, Annichiarrico-Petruzzelli M, Bernassola F, Piacentini M, Malcolm AJ, Pearson AD, Melino G and Redfern CP (2000) Effector mechanisms of fenretinide-induced apoptosis in neuroblastoma. Exp. Cell Res. 260: 50-60
23. Sun SY, Li W, Yue P, Lippman SM, Hong WK and Lotan R (1999) Mediation of N-(4-hydoxyphenyl)retinamide-induced apoptosis in human cancer cells by different mechanisms. Cancer Res. 59: 2493-2498
24. Chen YR, Zhou G and Tan TH (1999) c-Jun N-terminal kinase mediates apoptotic signaling induced by N-(4- hydroxyphenyl)retinamide. Mol. Pharmacol. 56: 1271-1279
25. Lovat PE, Ranalli M, Bernassola F, Tilby M, Malcolm AJ, Pearson AD, Piacentini M, Melino G and Redfern CP (2000) Synergistic induction of apoptosis of neuroblastoma by fenretinide or CD437 in combination with chemotherapeutic drugs. Int. J. Cancer 88: 977-985
26. Supino R, Crosti M, Clerici M, Warlters A, Cleris L, Zunino F and Formelli F (1996) Induction of apoptosis by fenretinide (4HPR) in human ovarian carcinoma cells and its association with retinoic acid receptor expression. Int. J. Cancer 65: 491-497
27. Lovat PE, Ranalli M, Bernassola F, Tilby M, Malcolm AJ, Pearson AD, Piacentini M, Melino G and Redfern CP (2000) Distinct properties of fenretinide and CD437 lead to synergistic responses with chemotherapeutic reagents. Med. Pediatr. Oncol. 35: 663-668
28. Senchenkov A, Litvak DA and Cabot MC (2001) Targeting ceramide metabolism - a strategy for overcoming drug resistance. J. Natl. Cancer Inst. 93: 347-357
29. Suliman A, Lam A, Datta R and Srivastava RK (2001) Intracellular mechanisms of TRAIL: apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 20: 2122-2133
30. Webb JL (1963) Effects of more than one inhibitor. In: Enzymes and Metabolic Inhibitors Vol. 1. (New York: Academic Press) pp 487-512
31. Chou TC and Hayball MP (1996) CalcuSyn Manual: Windows Software for Dose Effect Analysis. (Cambridge U.K.: Biosoft)
32. 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 and Schwall RH (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Invest. 104: 155-162
33. Uslu R, Jewett A and Bonavida B (1996) Sensitization of human ovarian tumor cells by subtoxic CDDP to anti-fas antibody-mediated cytotoxicity and apoptosis. Gynecol. Oncol. 62: 282-291
34. Wakahara Y, Nawa A, Okamoto T, Hayakawa A, Kikkawa F, Suganama N, Wakahara F and Tomoda Y (1997) Combination effect of anti-Fas antibody and chemotherapeutic drugs in ovarian cancer cells in vitro. Oncology 54: 48-54
35. Napoli JL (1996) Biochemical pathways of retinoid transport, metabolism, and signal transduction. Clin. Immunol. Immunopathol. 80: S52-S62
36. Umemiya H, Fukasawa H, Ebisawa M, Eyrolles L, Kawachi E, Eisenmann G, Gronemeyer H, Hashimoto Y, Shudo K and Kagechika H (1997) Regulation of retinoidal actions by diazepinylbenzoic acids. Retinoid synergists which activate the RXR-RAR heterodimers. J. Med. Chem. 40: 4222-4234
37. Ebisawa M, Umemiya H, Ohta K, Fukasawa H, Kawachi E, Christoffel G, Gronemeyer H, Tsuji M, Hashimoto Y, Shudo K and Kagechika H (1999) Retinoid X receptor-antagonistic diazepinylbenzoic acids. Chem. Pharm. Bull (Tokyo) 47: 1778-1786
38. Chinnaiyan A, Prasad U, Shankar S, Hamstra DA, Shanaiah M, Chenevert TL, Ross BD and Rehemtulla A (2000) Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc. Natl. Acad. Sci. USA 97: 1754-1759
39. Cuello M, Ettenberg SA, Clark AS, Keane MM, Posner RH, Nau MM, Dennis PA and Lipkowitz S (2001) Down-regulation of the erbB-2 receptor by trastuzumab (herceptin) enhances tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis in breast and ovarian cancer cell lines that overexpress erbB-2. Cancer Res. 61: 4892-4900
40. Panka DJ, Mano T, Suhara T, Walsh K and Mier JW (2001) Phosphatidylinositol 3-kinase/Akt activity regulates c-FLIP expression in tumor cells. J. Biol. Chem. 276: 6893-6896
41. Wen J, Ramadevi N, Nguyen D, Perkins C, Worthington E and Bhalla K (2000) Antileukemic drugs increase death receptor 5 levels and enhance Apo-2L-induced apoptosis of human acute leukemia cells. Blood 96: 3900-3906
42. Altucci L, Rossin A, Raffelsberger W, Reitmair A, Chomienne C and Gronemeyer H (2001) Retinoic acid-induced apoptosis in leukemia cells is mediated by paracrine action of tumor-selective death ligand TRAIL. Nat. Med. 7: 680-686
43. Nicholson DW and Thornberry NA (1997) Caspases: killer proteases. Trends Biochem. Sci. 22: 299-306
44. Bodmer JL, Holler N, Reynard S, Vinciguerra P, Schneider P, Juo P, Blenis J and Tschopp J (2000) TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat. Cell. Biol. 2: 241-243
45. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR and Martin SJ (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell. Biol. 144: 281-292
46. Suzuki S, Higuchi M, Proske RJ, Oridate N, Hong WK and Lotan R (1999) Implication of mitochondria-derived reactive oxygen species, cytochrome C and caspase-3 in N-(4-hydroxyphenyl)retinamide-induced apoptosis in cervical carcinoma cells. Oncogene 18: 6380-6387
47. Hail Jr N and Lotan R (2000) Mitochondrial permeability transition is a central coordinating event in N-(4-hydroxyphenyl)retinamide-induced apoptosis. Cancer Epidemiol. Biomarkers Prev. 9: 1293-1301
48. Maurer BJ, Metelitsa LS, Seeger RC, Cabot MC and Reynolds CP (1999) Increase of ceramide and induction of mixed apoptosis/necrosis by N-(4-hydroxyphenyl)-retinamide in neuroblastoma cell lines. J. Natl. Cancer Inst. 91: 1138-1146
49. Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind S and Spiegel S (1996) Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 381: 800-803
50. Liu JR, Fletcher B, Page C, Hu C, Nunez G and Baker V (1998) Bcl-xL is expressed in ovarian carcinoma and modulates chemotherapy-induced apoptosis. Gynecol. Oncol. 70: 398-403
51. Bossy-Wetzel E, Newmeyer DD and Green DR (1998) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17: 37-49
52. Johnson BW, Cepero E and Boise LH (2000) Bcl-xL inhibits cytochrome c release but not mitochondrial depolarization during the activation of multiple death pathways by tumor necrosis factor-alpha. J. Biol. Chem. 275: 31546-31553
53. Rokhlin OW, Guseva N, Tagiyev A, Knudson CM and Cohen MB (2001) Bcl-2 oncoprotein protects the human prostatic carcinoma cell line PC3 from TRAIL-mediated apoptosis. Oncogene 20: 2836-2843
54. Ogasawara J, Watanabe FR, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, Itoh N, Suda T and Nagata S (1993) Lethal effect of the anti-Fas antibody in mice. Nature 364: 806-809
55. Behrens BC, Hamilton TC, Masuda H, Grotzinger KR, Whang-Peng J, Louie KG, Knutsen T, McKoy WM, Young RC and Ozols RF (1987) Characterization of a cis-diamminedichloroplatinum(II)-resistant human ovarian cancer cell line and its use in evaluation of platinum analogues. Cancer Res. 47: 414-418
56. Parker RJ, Dabholkar MD, Lee KB, Bostick-Bruton F and Reed E (1993) Taxol effect on cisplatin sensitivity and cisplatin cellular accumulation in human ovarian cancer cells. J. Natl. Cancer. Inst. Monogr. 83-88
57. Sun SY, Yue P, Hong WK and Lotan R (2000) Augmentation of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by the synthetic retinod 6-[3-(1-adamantyl)- 4-hydroxyphenyl]-2-naphthalene carboxylic acid (CD437) through up-regulation of TRAIL receptors in human lung cancer cells. Cancer Res. 60: 7149-7155
58. Sun SY, Yue P and Lotan R (2000) Implication of multiple mechanisms in apoptosis induced by the synthetic retinoid CD437 in human prostate carcinoma cells. Oncogene 19: 4513-4522
59. Wolf JK, Mills GB, Bazzet L, Bast RC, Roth JA and Gershenson DM (1999) Adenovirus-mediated p53 growth inhibition of ovarian cancer cells is independent of endogenous p53 status. Gynecol. Oncol. 75: 261-266
60. Yazlovitskaya EM, DeHaan RD and Persons DL (2001) Prolonged wild-type p53 protein accumulation and cisplatin resistance. Biochem. Biophys. Res. Commun. 283: 732-737
61. Engels IH, Stepczynska A, Stroh C, Lauber K, Berg C, Schwenzer R, Wajant H, Janicke RU, Porter AG, Belka C, Gregor M, Schulze-Osthoff K and Wessellborg S (2000) Caspase-8/FLICE functions as an executioner caspase in anticancer drug- induced apoptosis. Oncogene 19: 4563-4573
62. Wieder T, Essmann F, Prokop A, Schmelz K, Schulze-Osthoff K, Beyaert R, Dorken B and Daniel PT (2001) Activation of caspase-8 in drug-induced apoptosis of B-lymphoid cells is independent of CD95/Fas receptor-ligand interaction and occurs downstream of caspase-3. Blood 97: 1378-1387
63. Fulda S, Meyer E and Debatin KM (2002) Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene 21: 2283-2294
64. Pirnia F, Schneider E, Betticher DC and Borner MM (2002) Mitomycin C induces apoptosis and caspase-8 and -9 processing through a caspase-3 and Fas-independent pathway. Cell Death Differ. 9: 905-914
65. Zimmermann KC, Bonzon C and Green DR (2001) The machinery of programmed cell death. Pharmacol. Ther. 92: 57-70
66. Sun XM, MacFarlane M, Zhuang J, Wolf BB, Green DR and Cohen GM (1999) Distinct caspase cascades are initiated in receptor-mediated and chemical-induced apoptosis. J. Biol. Chem. 274: 5053-5060
67. Pergolizzi R, Appierto V, Crosti M, Cavadini E, Cleris L, Guffanti A and Formelli F (1999) Role of retinoic acid receptor overexpression in sensitivity to fenretinide and tumorigenicity of human ovarian carcinoma cells. Int. J. Cancer 81: 829-834
68. Pastorino U, Warrell RJ and Formelli F (1995) Clinical pharmacology of the retinoids. In Retinoids in Oncology Degos L, Parkinson DR (eds.) (Berlin, Germany: Springer-Verlag) pp 55-66
69. Maines-Bandiera SL, Kruk PA and Auersperg N (1992) Simian virus 40-transformed human ovarian surface epithelial cells escape normal growth controls but retain morphogenetic responses to extracellular matrix. Am. J. Obstet. Gynecol. 167: 729-735
70. Lawrence D, Shahrokh Z, Marsters S, Achilles K, Shih D, Mounho B, Hillan K, Totpal K, DeForge L, Schow P, Hooley J, Sherwood S, Pai R, Leung S, Khan L, Gliniak B, Bussiere J, Smith CA, Strom SS, Kelley S, Fox JA, Thomas D and Ashkenazi A (2001) Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat. Med. 7: 383-385
71. Sun SY, Yue P, Wu GS, El-Deiry WS, Shroot B, Hong WK and Lotan R (1999) Implication of p53 in growth arrest and apoptosis induced by the synthetic retinoid CD437 in human lung cancer cells. Cancer Res. 59: 2829-2833