Dihydroceramide accumulation and reactive oxygen species are distinct and nonessential events in 4-HPR-mediated leukemia cell death

Biochemistry and Cell Biology

Volumn 90, Issue 2, 2012, Pages 209-223

  Apraiz, Aintzane ^a   Idkowiak Baldys, Jolanta ^b   Nieto Rementería, Naiara ^a   Boyano, María Dolores ^a   Hannun, Yusuf A ^b   Asumendi, Aintzane ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

4 HPR; Cell death; Dihydroceramide; Leukemia; ROS

Indexed keywords

4-HPR; ANTIOXIDANT ACTIVITIES; APOPTOTIC EFFECTS; ASCORBIC ACIDS; CANCER CELL LINES; CELLULAR VIABILITY; CERAMIDES; CLINICAL TRIAL; DIHYDROCERAMIDE; DRUG COMBINATIONS; IN-VITRO; JURKAT CELL; LC-MS ANALYSIS; LEUKEMIA; LEUKEMIA CELLS; LIPOXYGENASES; MYRIOCIN; REACTIVE OXYGEN SPECIES; ROS; SPHINGOLIPIDS; VITAMIN-E;

AMIDES; CELL CULTURE; DISEASES; KETONES; ORGANIC ACIDS; OXYGEN;

CELL DEATH;

4 (HYDROXYPHENYL)RETINAMIDE; CERAMIDE; DIHYDROCERAMIDE; REACTIVE OXYGEN METABOLITE; RETINOID; SPHINGOLIPID; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACTIVITY; HUMAN; HUMAN CELL; LEUKEMIA CELL; LIPID PEROXIDATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; OXIDATIVE STRESS;

ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; APOPTOSIS; ASCORBIC ACID; CELL LINE, TUMOR; CELL SURVIVAL; CERAMIDES; FENRETINIDE; FLAVANONES; HUMANS; LEUKEMIA; LIPID PEROXIDATION; LIPOXYGENASE INHIBITORS; MITOCHONDRIA; NORDIHYDROGUAIARETIC ACID; OXIDATIVE STRESS; OXIDOREDUCTASES; REACTIVE OXYGEN SPECIES; SPHINGOLIPIDS; VITAMIN E;

EID: 84862740360     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/o2012-001     Document Type: Article

References (58)

1. Asumendi A. Morales M.C. Alvarez A. Aréchaga J. Pérez-Yarza G. 2002. Implication of mitochondria-derivated ROS and cardiolipin peroxidation in N-(4-hydroxyphenyl) retinamide-induced apoptosis. Br. J. Cancer, 86 (12): 1951-1956. 10.1038/sj.bjc.6600356 12085192
2. Batra S. Reynolds C.P. Maurer B.J. 2004. Fenretinide cytotoxicity for Ewing's sarcoma and primitive neuroectodermal tumor cell lines is decreased by hypoxia and synergistically enhanced by ceramide modulators. Cancer Res. 64 (15): 5415-5424. 10.1158/0008-5472.CAN-04-0377 15289350
3. Bielawski J. Szulc Z.M. Hannun Y.A. Bielawska A. 2006. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods, 39 (2): 82-91. 10.1016/j.ymeth.2006.05.004 16828308
4. Cao J. Xu D. Wang D. Wu R. Zhang L. Zhu H. et al. 2009. ROS-driven Akt dephosphorylation at Ser-473 is involved in 4-HPR-mediated apoptosis in NB4 cells. Free Radic. Biol. Med. 47 (5): 536-547. 10.1016/j.freeradbiomed.2009.05. 024 19482076
5. Carpinteiro A. Dumitru C. Schenck M. Gulbins E. 2008. Ceramide-induced cell death in malignant cells. Cancer Lett. 264 (1): 1-10. 10.1016/j.canlet. 2008.02.020 18353542
6. Chen S. Samuel W. Fariss R.N. Duncan T. Kutty R.K. Wiggert B. 2003. Differentiation of human retinal pigment epithelial cells into neuronal phenotype by N-(4-hydroxyphenyl)retinamide. J. Neurochem. 84 (5): 972-981. 10.1046/j.1471-4159.2003.01608.x 12603822
7. Cook-Moreau J.M. El-Makhour Hojeij Y. Barrière G. Rabinovitch-Chable H.C. Faucher K.S. Sturtz F.G. Rigaud M.A. 2007. Expression of 5-lipoxygenase (5-LOX) in T lymphocytes. Immunology, 122 (2): 157-166. 10.1111/j.1365-2567.2007.02621.x 17484769
8. Cuperus R. Tytgat G.A. Leen R. Brites P. Bras J. Caron H.N. Van Kuilenburg A.B. 2008. Pleiotropic effects of fenretinide in neuroblastoma cell lines and multicellular tumor spheroids. Int. J. Oncol. 32 (5): 1011-1019. 18425327
9. Cuperus R. Leen R. Tytgat G.A. Caron H.N. van Kuilenburg A.B. 2010. Fenretinide induces mitochondrial ROS and inhibits the mitochondrial respiratory chain in neuroblastoma. Cell. Mol. Life Sci. 67 (5): 807-816. 10.1007/s00018-009-0212-2 19941060
10. Darwiche N. Abou-Lteif G. Najdi T. Kozhaya L. Abou Tayyoun A. Bazarbachi A. Dbaibo G.S. 2005. Human T-cell lymphopropic virus type I-transformed T-cells have a partial defect in ceramide synthesis in response to N-(4-hydroxyphenyl)- retinamide. Biochem. J. 392 (1): 231-239. 10.1042/BJ20050578 16086670
11. Darwiche N. Abou-Lteif G. Bazarbachi A. 2007. Reactive oxygen species mediate N-(4-hydroxyphenyl)retinamide-induced cell death in malignant T cells and are inhibited by the HTLV-1 oncoprotein Tax. Leukemia, 21 (2): 261-269. 10.1038/sj.leu.2404472 17122865
12. Delia D. Aiello A. Lombardi L. Pelicci P.G. Grignani F. Grignani F. et al. 1993. N-(4-hydroxyphenyl)retinamide induces apoptosis of malignant hemopoietic cell lines including those unresponsive to retinoic acid. Cancer Res. 53 (24): 6036-6041. 8261419
13. Delia D. Aiello A. Formelli F. Fontanella E. Costa A. Miyashita T. et al. 1995. Regulation of apoptosis induced by the retinoid N-(4-hydroxyphenyl) retinamide and effect of deregulated bcl-2. Blood, 85 (2): 359-367. 7811993
14. Faderl S. Lotan R. Kantarjian H.M. Harris D. Van Q. Estrov Z. 2003. N-(4-Hydroxylphenyl)retinamide (fenretinide, 4-HPR), a retinoid compound with antileukemic and proapoptotic activity in acute lymphoblastic leukemia (ALL). Leuk. Res. 27 (3): 259-266. 10.1016/S0145-2126(02)00162-5 12537979
15. Floriano-Sánchez E. Villanueva C. Medina-Campos O.N. Rocha D. Sánchez-González D.J. Cárdenas-Rodríguez N. Pedraza-Chaverrí J. 2006. Nordihydroguaiaretic acid is a potent in vitro scavenger of peroxynitrite, singlet oxygen, hydroxyl radical, superoxide anion and hypochlorous acid and prevents in vivo ozone-induced tyrosine nitration in lungs. Free Radic. Res. 40 (5): 523-533. 10.1080/10715760500419365 16551579
16. Garaventa A. Luksch R. Lo Piccolo M.S. Cavadini E. Montaldo P.G. Pizzitola M.R. et al. 2003. Phase I trial and pharmacokinetics of fenretinide in children with neuroblastoma. Clin. Cancer Res. 9 (6): 2032-2039. 12796365
17. Hail N. Jr Kim H.J. Lotan R. 2006. Mechanisms of fenretinide-induced apoptosis. Apoptosis, 11 (10): 1677-1694. 10.1007/s10495-006-9289-3 16850162
18. Hannun Y.A. Obeid L.M. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9 (2): 139-150. 10.1038/nrm2329 18216770
19. Idkowiak-Baldys J. Apraiz A. Li L. Rahmaniyan M. Clarke C.J. Kraveka J.M. et al. 2010. Dihydroceramide desaturase activity is modulated by oxidative stress. Biochem. J. 427 (2): 265-274. 10.1042/BJ20091589 20105137
20. Jiang L. Pan X. Chen Y. Wang K. Du Y. Zhang J. 2011. Preferential involvement of both ROS and ceramide in fenretinide-induced apoptosis of HL60 rather than NB4 and U937 cells. Biochem. Biophys. Res. Commun. 405 (2): 314-318. 10.1016/j.bbrc.2011.01.036 21237137
21. Kadara H. Lacroix L. Lotan D. Lotan R. 2007. Induction of endoplasmic reticulum stress by the pro-apoptotic retinoid N-(4-hydroxyphenyl)retinamide via a reactive oxygen species-dependent mechanism in human head and neck cancer cells. Cancer Biol. Ther. 6 (5): 705-711. 10.4161/cbt.6.5.3963 17404501
22. Kadara H. Tahara E. Kim H.J. Lotan D. Myers J. Lotan R. 2008. Involvement of Rac in fenretinide-induced apoptosis. Cancer Res. 68 (11): 4416-4423. 18519704
23. Kang M.H. Wan Z. Kang Y.H. Sposto R. Reynolds C.P. 2008. Mechanism of synergy of N-(4-hydroxyphenyl)retinamide and ABT-737 in acute lymphoblastic leukemia cell lines: Mcl-1 inactivation. J. Natl. Cancer Inst. 100 (8): 580-595. 10.1093/jnci/djn076 18398104
24. Kim H.J. Chakravarti N. Oridate N. Choe C. Claret F.X. Lotan R. 2006. N-(4-hydroxyphenyl)retinamide-induced apoptosis triggered by reactive oxygen species is mediated by activation of MAPKs in head and neck squamous carcinoma cells. Oncogene, 25 (19): 2785-2794. 10.1038/sj.onc.1209303 16407847
25. Kitareewan S. Spinella M.J. Allopenna J. Reczek P.R. Dmitrovsky E. 1999. 4HPR triggers apoptosis but not differentiation in retinoid sensitive and resistant human embryonal carcinoma cells through an RARgamma independent pathway. Oncogene, 18 (42): 5747-5755. 10.1038/sj.onc.1202981 10523855
26. Kitatani K. Idkowiak-Baldys J. Hannun Y.A. 2008. The sphingolipid salvage pathway in ceramide metabolism and signalling. Cell. Signal. 20 (6): 1010-1018. 10.1016/j.cellsig.2007.12.006 18191382
27. Kraveka J.M. Li L. Szulc Z.M. Bielawski J. Ogretmen B. Hannun Y.A. et al. 2007. Involvement of dihydroceramide desaturase in cell cycle progression in human neuroblastoma cells. J. Biol. Chem. 282 (23): 16718-16728. 10.1074/jbc.M700647200 17283068
28. Kühn H. Borchert A. 2002. Regulation of enzymatic lipid peroxidation: the interplay of peroxidizing and peroxide reducing enzymes. Free Radic. Biol. Med. 33 (2): 154-172. [Review.] 10.1016/S0891-5849(02)00855-9 12106812
29. Lovat P.E. Oliverio S. Ranalli M. Corazzari M. Rodolfo C. Bernassola F. et al. 2002. GADD153 and 12-lipoxygenase mediate fenretinide-induced apoptosis of neuroblastoma. Cancer Res. 62 (18): 5158-5167. 12234979
30. Lovat P.E. Di Sano F. Corazzari M. Fazi B. Donnorso R.P. Pearson A.D. et al. 2004. Gangliosides link the acidic sphingomyelinase-mediated induction of ceramide to 12-lipoxygenase-dependent apoptosis of neuroblastoma in response to fenretinide. J. Natl. Cancer Inst. 96 (17): 1288-1299. 10.1093/jnci/djh254 15339967
31. Maurer B.J. Metelitsa L.S. Seeger R.C. Cabot M.C. Reynolds C.P. 1999. Increase of ceramide and induction of mixed apoptosis/necrosis by N-(4-hydroxyphenyl)retinamide in neuroblastoma cell lines. J. Natl. Cancer Inst. 91 (13): 1138-1146. 10.1093/jnci/91.13.1138 10393722
32. Morales M.C. Pérez-Yarza G. Nieto-Rementería N. Boyano M.D. Jangi M. Atencia R. Asumendi A. 2005. Intracellular glutathione levels determine cell sensitivity to apoptosis induced by the antineoplasic agent N-(4-hydroxyphenyl)retinamide. Anticancer Res. 25 (3B): 1945-1951. 16158929
33. Morales M.C. Pérez-Yarza G. Rementería N.N. Boyano M.D. Apraiz A. Gómez-Muñoz A. et al. 2007. 4-HPR-mediated leukemia cell cytotoxicity is triggered by ceramide-induced mitochondrial oxidative stress and is regulated downstream by Bcl-2. Free Radic. Res. 41 (5): 591-601. 10.1080/10715760701218558 17454142
34. O'Donnell P.H. Guo W.X. Reynolds C.P. Maurer B.J. 2002. N-(4-hydroxyphenyl)retinamide increases ceramide and is cytotoxic to acute lymphoblastic leukemia cell lines, but not to non-malignant lymphocytes. Leukemia, 16 (5): 902-910. 10.1038/sj.leu.2402485 11986953
35. Obeid L.M. Linardic C.M. Karolak L.A. Hannun Y.A. 1993. Programmed cell death induced by ceramide. Science, 259 (5102): 1769-1771. 10.1126/science. 8456305 8456305
36. Ponzoni M. Bocca P. Chiesa V. Decensi A. Pistoia V. Raffaghello L. et al. 1995. Differential effects of N-(4-hydroxyphenyl)retinamide and retinoic acid on neuroblastoma cells: apoptosis versus differentiation. Cancer Res. 55 (4): 853-861. 7850799
37. Rahmaniyan M. Curley R.W. Jr Obeid L.M. Hannun Y.A. Kraveka J.M. 2011. Identification of dihydroceramide desaturase as a direct in vitro target for fenretinide. J. Biol. Chem. 286 (28): 24754-24764. 10.1074/jbc.M111.250779 21543327
38. Rehman F. Shanmugasundaram P. Schrey M.P. 2004. Fenretinide stimulates redox-sensitive ceramide production in breast cancer cells: potential role in drug-induced cytotoxicity. Br. J. Cancer, 91 (10): 1821-1828. 10.1038/sj.bjc.6602212 15505623
39. Reynolds C.P. Lemons R.S. 2001. Retinoid therapy of childhood cancer. Hematol. Oncol. Clin. North Am. 15 (5): 867-910. 10.1016/S0889-8588(05)70256-2 11765378
40. Rotmensz N. De Palo G. Formelli F. Costa A. Marubini E. Campa T. et al. 1991. Long-term tolerability of fenretinide (4-HPR) in breast cancer patients. Eur. J. Cancer, 27 (9): 1127-1131. 10.1016/0277-5379(91)90309-2 1835622
41. Ruvolo V.R. Karanjeet K.B. Schuster T.F. Brown R. Deng Y. Hinchcliffe E. Ruvolo P.P. 2010. Role for PKC δ in fenretinide-mediated apoptosis in lymphoid leukemia cells. J. Signal Transduct. 2010: 584657. 20844597
42. Sabichi A.L. Lerner S.P. Atkinson E.N. Grossman H.B. Caraway N.P. Dinney C.P. et al. 2008. Phase III prevention trial of fenretinide in patients with resected non-muscle-invasive bladder cancer. Clin. Cancer Res. 14 (1): 224-229. 10.1158/1078-0432.CCR-07-0733 18172274
43. Salari H. Braquet P. Borgeat P. 1984. Comparative effects of indomethacin, acetylenic acids, 15-HETE, nordihydroguaiaretic acid and BW755C on the metabolism of arachidonic acid in human leukocytes and platelets. Prostaglandins Leukot. Med. 13 (1): 53-60. 10.1016/0262-1746(84)90102-1 6424136
44. Sun S.-Y. Li W. Yue P. Lippman S.M. Hong W.K. Lotan R. 1999. Mediation of N-(4-hydroxyphenyl)retinamide-induced apoptosis in human cancer cells by different mechanisms. Cancer Res. 59 (10): 2493-2498. 10344763
45. Suzuki S. Higuchi M. Proske R.J. Oridate N. Hong W.K. Lotan R. 1999. Implications of mitochondria-derived reactive oxygen species, cytochrome C and caspase-3 in N-(4-hydroxyphenyl)retinamide-induced apoptosis in cervical carcinoma cells. Oncogene, 18 (46): 6380-6387. 10.1038/sj.onc.1203024 10597238
46. Szulc Z.M. Bielawski J. Gracz H. Gustilo M. Mayroo N. Hannun Y.A. et al. 2006. Tailoring structure-function and targeting properties of ceramides by site-specific cationization. Bioorg. Med. Chem. 14 (21): 7083-7104. 10.1016/j.bmc.2006.07.016 16919460
47. Taha T.A. Mullen T.D. Obeid L.M. 2006. A house divided: ceramide, sphingosine, and sphinosine-1-phosphate in programmed cell death. Biochim. Biophys. Acta, 1758 (12): 2007-2036.
48. Tiwari M. Kumar A. Sinha R.A. Shrivastava A. Balapure A.K. Sharma R. et al. 2006. Mechanism of 4-HPR-induced apoptosis in glioma cells: evidences suggesting role of mitochondrial-mediated pathway and endoplasmic reticulum stress. Carcinogenesis, 27 (10): 2047-2058. 10.1093/carcin/bgl051 16675469
49. Tiwari M. Bajpai V.K. Sahasrabuddhe A.A. Kumar A. Sinha R.A. Behari S. Godbole M.M. 2008. Inhibition of N-(4-hydroxyphenyl)retinamide-induced autophagy at a lower dose enhances cell death in malignant glioma cells. Carcinogenesis, 29 (3): 600-609. 10.1093/carcin/bgm264 18174255
50. Traber M.G. Atkinson J. 2007. Vitamin E, antioxidant and nothing more. Free Radic. Biol. Med. 43 (1): 4-15. [Review.] 10.1016/j.freeradbiomed.2007.03. 024 17561088
51. Valsecchi M. Aureli M. Mauri L. Illuzzi G. Chigorno V. Prinetti A. Sonnino S. 2010. Sphingolipidomics of A2780 human ovarian carcinoma cells treated with synthetic retinoids. J. Lipid Res. 51 (7): 1832-1840. 10.1194/jlr.M004010 20194109
52. Van Veldhoven P.P. Bell R.M. 1988. Effect of harvesting methods, growth conditions and growth phase on diacylglycerol levels in cultured human adherent cells. Biochim. Biophys. Acta, 959 (2): 185-196. 3349097
53. Veronesi U. Mariani L. Decensi A. Formelli F. Camerini T. Miceli R. et al. 2006. Fifteen-years results of a randomized phase III trial of fenretinide to prevente second breast cancer. Ann. Oncol. 17 (7): 1065-1071. 10.1093/annonc/mdl047 16675486
54. Wang H. Maurer B.J. Reynolds C.P. Cabot M.C. 2001. N-(4-hydroxylphenyl) retinamide elevates ceramide in neuroblastoma cell lines by coordinate activation of serine palmitoyltransferase and ceramide synthase. Cancer Res. 61 (13): 5102-5105. 11431347
55. Wang H. Maurer B.J. Liu Y.Y. Wang E. Allegood J.C. Kelly S. et al. 2008. N-(4-Hydroxyphenyl)retinamide increases dihydroceramide and synergizes with dimethylsphingosine to enhance cancer cell killing. Mol. Cancer Ther. 7 (9): 2967-2976. 10.1158/1535-7163.MCT-08-0549 18790777
56. Wang K. Fang H. Xiao D. Zhu X. He M. Pan X. et al. 2009. Converting redox signaling to apoptotic activities by stress-responsive regulators HSF1 and NRF2 in fenretinide treated cancer cells. PLoS ONE, 4 (10): e7538. 10.1371/journal.pone.0007538 19844581
57. Wu J.M. DiPietrantonio A.M. Hsieh T.C. 2001. Mechanism of fenretinide (4-HPR)-induced cell death. Apoptosis, 6 (5): 377-388. 10.1023/A:1011342220621 11483862
58. Zheng W. Kollmeyer J. Symolon H. Momin A. Munter E. Wang E. et al. 2006. Ceramides and other bioactive sphingolipid backbones in health and disease: lipidomic analysis, metabolism and roles in membrane structure, dynamics, signaling and autophagy. Biochim. Biophys. Acta, 1758 (12): 1864-1884. 17052686