C22:0- and C24:0-dihydroceramides Confer Mixed Cytotoxicity in T-Cell Acute Lymphoblastic Leukemia Cell Lines

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Holliday Jr , Michael W ^a   Cox, Stephen B ^b   Kang, Min H ^a   Maurer, Barry J ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b Research and Testing Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE DERIVATIVE; DIHYDROCERAMIDE DERIVATIVE; DIHYDROCERAMIDE DESATURASE 1; OXYGENASE; SERINE PALMITOYLTRANSFERASE; SPHINGOLIPID; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOTOXICITY; DNA FRAGMENTATION; ENZYME METABOLISM; ENZYME SYNTHESIS; FATTY ACID ANALYSIS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; LIQUID CHROMATOGRAPHY; MEMBRANE DEPOLARIZATION; PROTEIN CLEAVAGE; REAL TIME POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY;

ANTINEOPLASTIC AGENTS; AUTOPHAGY; CELL LINE, TUMOR; CERAMIDES; CULTURE MEDIA; DNA FRAGMENTATION; FATTY ACIDS; HUMANS; MITOCHONDRIA; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; REACTIVE OXYGEN SPECIES; SPHINGOLIPIDS; SPHINGOSINE;

EID: 84883642398     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074768     Document Type: Article

References (47)

1. Delia D, Aiello A, Lombardi L, Pelicci PG, 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: 6036-6041. PubMed: 8261419.
2. O'Donnell PH, Guo WX, Reynolds CP, Maurer BJ, (2002) N-(4-hydroxyphenyl)retinamide increases ceramide and is cytotoxic to acute lymphoblastic leukemia cell lines, but not to non-malignant lymphocytes. Leukemia 16: 902-910. doi:10.1038/sj.leu.2402485. PubMed: 11986953.
3. Faderl S, Lotan R, Kantarjian HM, Harris D, Van Q, et al. (2003) N-(4-Hydroxylphenyl)retinamide (fenretinide, 4-HPR), a retinoid compound with antileukemic and proapoptotic activity in acute lymphoblastic leukemia (ALL). Leuk Res 27: 259-266. doi:10.1016/S0145-2126(02)00162-5. PubMed: 12537979.
4. Kang MH, Wan Z, Kang YH, Sposto R, Reynolds CP, (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: 580-595. doi:10.1093/jnci/djn076. PubMed: 18398104.
5. Oridate N, Suzuki S, Higuchi M, Mitchell MF, Hong WK, et al. (1997) Involvement of reactive oxygen species in N-(4-hydroxyphenyl)retinamide-induced apoptosis in cervical carcinoma cells. J Natl Cancer Inst 89: 1191-1198. doi:10.1093/jnci/89.16.1191. PubMed: 9274913.
6. Delia D, Aiello A, Meroni L, Nicolini M, Reed JC, et al. (1997) Role of antioxidants and intracellular free radicals in retinamide-induced cell death. Carcinogenesis 18: 943-948. doi:10.1093/carcin/18.5.943. PubMed: 9163679.
7. Hail N Jr., 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. PubMed: 11142414.
8. Sun SY, Li W, Yue P, Lippman SM, Hong WK, et al. (1999) Mediation of N-(4-hydoxyphenyl)retinamide-induced apoptosis in human cancer cells by different mechanisms. Cancer Res 59: 2493-2498. PubMed: 10344763.
9. Maurer BJ, Metelitsa LS, Seeger RC, Cabot MC, 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. doi:10.1093/jnci/91.13.1138. PubMed: 10393722.
10. Maurer BJ, Melton L, Billups C, Cabot MC, Reynolds CP, (2000) Synergistic cytotoxicity in solid tumor cell lines between N-(4-hydroxyphenyl)retinamide and modulators of ceramide metabolism. J Natl Cancer Inst 92: 1897-1909. doi:10.1093/jnci/92.23.1897. PubMed: 11106681.
11. Schulz A, Mousallem T, Venkataramani M, Persaud-Sawin DA, Zucker A, et al. (2006) The CLN9 protein, a regulator of dihydroceramide synthase. J Biol Chem 281: 2784-2794. PubMed: 16303764.
12. Kraveka JM, Li L, Szulc ZM, Bielawski J, Ogretmen B, et al. (2007) Involvement of the dihydroceramide desaturase in cell cycle progression in human neuroblastoma cells. J Biol Chem 282: 16718-16728. doi:10.1074/jbc.M700647200. PubMed: 17283068.
13. Kong G, Wang D, Wang H, Wu J, Bielawski J, et al. (2008) Synthetic triterpenoids have cytotoxicity in pediatric acute lymphoblastic leukemia cell lines but cytotoxicity is independent of induced ceramide increase in MOLT-4 cells. Leukemia 22: 1258-1262. doi:10.1038/sj.leu.2405023. PubMed: 18033322.
14. Wang H, Maurer BJ, Liu Y-Y, Wang E, Allegood JC, et al. (2008) N-(4-Hydroxyphenyl)retinamide increases dihydroceramides and synergizes with dimethylsphingosine to enhance cancer cell killing. Mol Cancer Ther 7: 2967-2976. doi:10.1158/1535-7163.MCT-08-0549. PubMed: 18790777.
15. Rahmaniyan M, Curley RW Jr., Obeid LM, Hannun YA, Kraveka JM, (2011) Identification of dihydroceramide desaturase as a direct in vitro target for fenretinide. J Biol Chem 286: 24754-24764. doi:10.1074/jbc.M111.250779. PubMed: 21543327.
16. Lahiri S, Lee H, Mesicek J, Fuks Z, Haimovitz-Friedman A, et al. (2007) Kinetic characterization of mammalian ceramide synthases: determination of K(m) values towards sphinganine. FEBS Lett 581: 5289-5294. doi:10.1016/j.febslet.2007.10.018. PubMed: 17977534.
17. Gault CR, Obeid LM, Hannun YA, (2010) An overview of sphingolipid metabolism: from synthesis to breakdown. Adv Exp Med Biol 688: 1-23. doi:10.1007/978-1-4419-6741-1_1. PubMed: 20919643.
18. Levy M, Futerman AH, (2010) Mammalian ceramide synthases. IUBMB Life 62: 347-356. PubMed: 20222015.
19. Michel C, Echten-Deckert G, Rother J, Sandhoff K, Wang E, et al. (1997) Characterization of ceramide synthesis. A dihydroceramide desaturase introduces the 4,5-trans-double bond of sphingosine at the level of dihydroceramide. J Biol Chem 272: 22432-22437. doi:10.1074/jbc.272.36.22432. PubMed: 9312549.
20. Wang H, Maurer BJ, Reynolds CP, Cabot MC, (2001) N-(4-hydroxyphenyl)retinamide elevates ceramide in neuroblastoma cell lines by coordinate activation of serine palmitoyltransferase and ceramide synthase. Cancer Res 61: 5102-5105. PubMed: 11431347.
21. Ogretmen B, Hannun YA, (2004) Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 4: 604-616. doi:10.1038/nrc1411. PubMed: 15286740.
22. Reynolds CP, Maurer BJ, Kolesnick RN, (2004) Ceramide synthesis and metabolism as a target for cancer therapy. Cancer Lett 206: 169-180. doi:10.1016/j.canlet.2003.08.034. PubMed: 15013522.
23. Bielawska A, Crane HM, Liotta D, Obeid LM, Hannun YA, (1993) Selectivity of ceramide-mediated biology. Lack of activity of erythro-dihydroceramide. J Biol Chem 268: 26226-26232. PubMed: 8253743.
24. Ghafourifar P, Klein SD, Schucht O, Schenk U, Pruschy M, et al. (1999) Ceramide induces cytochrome c release from isolated mitochondria. Importance of mitochondrial redox state. J Biol Chem 274: 6080-6084. doi:10.1074/jbc.274.10.6080. PubMed: 10037689.
25. Sugiki H, Hozumi Y, Maeshima H, Katagata Y, Mitsuhashi Y, et al. (2000) C2-ceramide induces apoptosis in a human squamous cell carcinoma cell line. Br J Dermatol 143: 1154-1163. doi:10.1046/j.1365-2133.2000.03882.x. PubMed: 11122015.
26. Ahn EH, Schroeder JJ, (2002) Sphingoid bases and ceramide induce apoptosis in HT-29 and HCT-116 human colon cancer cells. Exp Biol Med (Maywood) 227: 345-353. PubMed: 11976405.
27. Shikata K, Niiro H, Azuma H, Ogino K, Tachibana T, (2003) Apoptotic activities of C2-ceramide and C2-dihydroceramide homologues against HL-60 cells. Bioorg Med Chem 11: 2723-2728. doi:10.1016/S0968-0896(03)00228-1. PubMed: 12788346.
28. Zheng W, Kollmeyer J, Symolon H, Momin A, Munter 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: 1864-1884. doi:10.1016/j.bbamem.2006.08.009. PubMed: 17052686.
29. Separovic D, Bielawski J, Pierce JS, Merchant S, Tarca AL, et al. (2009) Increased tumour dihydroceramide production after Photofrin-PDT alone and improved tumour response after the combination with the ceramide analogue LCL29. Evidence from mouse squamous cell carcinomas. Br J Cancer 100: 626-632. doi:10.1038/sj.bjc.6604896. PubMed: 19223911.
30. Signorelli P, Munoz-Olaya JM, Gagliostro V, Casas J, Ghidoni R, et al. (2009) Dihydroceramide intracellular increase in response to resveratrol treatment mediates autophagy in gastric cancer cells. Cancer Lett 282: 238-243. doi:10.1016/j.canlet.2009.03.020. PubMed: 19394759.
31. Devlin CM, Lahm T, Hubbard WC, Van DM, Wang KC, et al. (2011) Dihydroceramide-based response to hypoxia. J Biol Chem 286: 38069-38078. doi:10.1074/jbc.M111.297994. PubMed: 21914808.
32. Jiang Q, Rao X, Kim CY, Freiser H, Zhang Q, et al. (2012) Gamma-tocotrienol induces apoptosis and autophagy in prostate cancer cells by increasing intracellular dihydrosphingosine and dihydroceramide. Int J Cancer 130: 685-693. doi:10.1002/ijc.26054. PubMed: 21400505.
33. Fabrias G, Muñoz-Olaya J, Cingolani F, Signorelli P, Casas J, et al. (2012) Dihydroceramide desaturase and dihydrosphingolipids: Debutant players in the sphingolipid arena. Prog Lipid Res 51: 82-94. doi:10.1016/j.plipres.2011.12.002. PubMed: 22200621.
34. Triola G, Fabriàs G, Casas J, Llebaria A, (2003) Synthesis of cyclopropene analogues of ceramide and their effect on dihydroceramide desaturase. J Org Chem 68: 9924-9932. doi:10.1021/jo030141u. PubMed: 14682684.
35. Singh I, Kishimoto Y, (1983) Effect of cyclodextrins on the solubilization of lignoceric acid, ceramide, and cerebroside, and on the enzymatic reactions involving these compounds. J Lipid Res 24: 662-665. PubMed: 6875391.
36. Frgala T, Kalous O, Proffitt RT, Reynolds CP, (2007) A fluorescence microplate cytotoxicity assay with a 4-log dynamic range that identifies synergistic drug combinations. Mol Cancer Ther 6: 886-897. doi:10.1158/1535-7163.MCT-04-0331. PubMed: 17363483.
37. Bielawski J, Szulc ZM, Hannun YA, Bielawska A, (2006) Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39: 82-91. doi:10.1016/j.ymeth.2006.05.004. PubMed: 16828308.
38. Van Veldhoven PP, Bell RM, (1988) Effect of harvesting methods, growth conditions and growth phase on diacylglycerol levels in cultured human adherent cells. Biochim Biophys Acta 959: 185-196. doi:10.1016/0005-2760(88)90030-6. PubMed: 3349097.
39. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917. doi:10.1139/o59-099. PubMed: 13671378.
40. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609.
41. Sandhoff R, (2010) Very long chain sphingolipids: tissue expression, function and synthesis. FEBS Lett 584: 1907-1913. doi:10.1016/j.febslet.2009.12.032. PubMed: 20035755.
42. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, et al. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 5: 167-179. doi:10.1016/j.cmet.2007.01.002. PubMed: 17339025.
43. Apraiz A, Idkowiak-Baldys J, Nieto-Rementería N, Boyano MD, Hannun YA, et al. (2012) Dihydroceramide accumulation and reactive oxygen species are distinct and nonessential events in 4-HPR-mediated leukemia cell death. Biochem Cell Biol 90: 209-223. doi:10.1139/o2012-001. PubMed: 22428532.
44. Mao Z, Sun W, Xu R, Novgorodov S, Szulc ZM, et al. (2010) Alkaline ceramidase 2 (ACER2) and its product dihydrosphingosine mediate the cytotoxicity of N-(4-hydroxyphenyl)retinamide in tumor cells. J Biol Chem 285: 29078-29090. doi:10.1074/jbc.M110.105296. PubMed: 20628055.
45. Laviad EL, Albee L, Pankova-Kholmyansky I, Epstein S, Park H, et al. (2008) Characterization of ceramide synthase2: tissue distribution, substrate specificity, and inhibition by sphingosine 1-phosphate. J Biol Chem 283: 5677-5684. PubMed: 18165233.
46. Kummar S, Gutierrez ME, Maurer BJ, Reynolds CP, Kang M, et al. (2011) Phase I trial of fenretinide lym-x-sorb oral powder in adults with solid tumors and lymphomas. Anticancer Res 31: 961-966. PubMed: 21498721.
47. Maurer BJ, Kalous O, Yesair DW, Wu X, Janeba J, et al. (2007) Improved oral delivery of N-(4-hydroxyphenyl)retinamide with a novel LYM-X-SORB organized lipid complex. Clin Cancer Res 13: 3079-3086. doi:10.1158/1078-0432.CCR-06-1889. PubMed: 17505011.