Inhibition of Ceramide Metabolism Sensitizes Human Leukemia Cells to Inhibition of BCL2-Like Proteins

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Casson, Lavona ^a   Howell, Lauren ^b   Mathews, Lesley A ^c   Ferrer, Marc ^c   Southall, Noel ^c   Guha, Rajarshi ^c   Keller, Jonathan M ^c   Thomas, Craig ^c   Siskind, Leah J ^b,d   Beverly, Levi J ^a,e  

^a University of Louisville School of Medicine   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 DEOXYNOJIRIMYCIN; 2 DECANOYLAMINO 3 MORPHOLINO 1 PHENYL 1 PROPANOL; CERAMIDE; CERAMIDE GLUCOSYLTRANSFERASE; NAVITOCLAX; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN BCL 2; SPHINGOSINE; SPHINGOSINE KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CHEMOSENSITIZATION; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SCREENING; HUMAN; HUMAN CELL; INHIBITION KINETICS; LEUKEMIA CELL; LIPID METABOLISM;

ANILINE COMPOUNDS; CELL LINE, TUMOR; CELL SURVIVAL; CERAMIDES; ENZYME INHIBITORS; GLUCOSYLTRANSFERASES; HUMANS; MORPHOLINES; SULFONAMIDES;

EID: 84872468446     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054525     Document Type: Article

References (50)

1. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
2. Adams JM, Cory S, (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322-1326.
3. Tsujimoto Y, (1998) Role of Bcl-2 family proteins in apoptosis: apoptosomes or mitochondria? Genes Cells 3: 697-707.
4. Perera MN, Lin SH, Peterson YK, Bielawska A, Szulc ZM, et al. (2012) Bax and Bcl-xL exert their regulation on different sites of the ceramide channel. Biochem J 445: 81-91.
5. Hannun YA, Obeid LM, (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150.
6. Cory S, Huang DC, Adams JM, (2003) The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22: 8590-8607.
7. Horvitz HR, (1999) Genetic control of programmed cell death in the nematode Caenorhabditis elegans. Cancer Res 59: 1701s-1706s.
8. Letai A, Sorcinelli MD, Beard C, Korsmeyer SJ, (2004) Antiapoptotic BCL-2 is required for maintenance of a model leukemia. Cancer Cell 6: 241-249.
9. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681.
10. Reed JC, (2006) Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities. Cell Death Differ 13: 1378-1386.
11. Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, et al. (2008) ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer research 68: 3421-3428.
12. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, et al. (2006) The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10: 389-399.
13. Nguyen M, Marcellus RC, Roulston A, Watson M, Serfass L, et al. (2007) Small molecule obatoclax (GX15-070) antagonizes MCL-1 and overcomes MCL-1-mediated resistance to apoptosis. Proc Natl Acad Sci USA 104: 19512-19517.
14. Del Gaizo Moore V, Schlis KD, Sallan SE, Armstrong SA, Letai A, (2008) BCL-2 dependence and ABT-737 sensitivity in acute lymphoblastic leukemia. Blood 111: 2300-2309.
15. Konopleva M, Contractor R, Tsao T, Samudio I, Ruvolo PP, et al. (2006) Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 10: 375-388.
16. Wilson WH, O'Connor OA, Czuczman MS, LaCasce AS, Gerecitano JF, et al. (2010) Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: a phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. The lancet oncology 11: 1149-1159.
17. Siskind LJ, Mullen TD, Romero Rosales K, Clarke CJ, Hernandez-Corbacho MJ, et al. (2010) The BCL-2 protein BAK is required for long-chain ceramide generation during apoptosis. J Biol Chem 285: 11818-11826.
18. Siskind LJ, Kolesnick RN, Colombini M, (2006) Ceramide forms channels in mitochondrial outer membranes at physiologically relevant concentrations. Mitochondrion 6: 118-125.
19. Allouche M, Bettaieb A, Vindis C, Rousse A, Grignon C, et al. (1997) Influence of Bcl-2 overexpression on the ceramide pathway in daunorubicin-induced apoptosis of leukemic cells. Oncogene 14: 1837-1845.
20. El-Assaad W, El-Sabban M, Awaraji C, Abboushi N, Dbaibo GS, (1998) Distinct sites of action of Bcl-2 and Bcl-xL in the ceramide pathway of apoptosis. Biochem J 336 (Pt 3): 735-741.
21. Ganesan V, Colombini M, (2010) Regulation of ceramide channels by Bcl-2 family proteins. FEBS Lett 584: 2128-2134.
22. Geley S, Hartmann BL, Kofler R, (1997) Ceramides induce a form of apoptosis in human acute lymphoblastic leukemia cells that is inhibited by Bcl-2, but not by CrmA. FEBS Lett 400: 15-18.
23. Kawatani M, Uchi M, Simizu S, Osada H, Imoto M, (2003) Transmembrane domain of Bcl-2 is required for inhibition of ceramide synthesis, but not cytochrome c release in the pathway of inostamycin-induced apoptosis. Exp Cell Res 286: 57-66.
24. Sawada M, Nakashima S, Banno Y, Yamakawa H, Takenaka K, et al. (2000) Influence of Bax or Bcl-2 overexpression on the ceramide-dependent apoptotic pathway in glioma cells. Oncogene 19: 3508-3520.
25. Zhang J, Alter N, Reed JC, Borner C, Obeid LM, et al. (1996) Bcl-2 interrupts the ceramide-mediated pathway of cell death. Proc Natl Acad Sci U S A 93: 5325-5328.
26. Baran Y, Bielawski J, Gunduz U, Ogretmen B, (2011) Targeting glucosylceramide synthase sensitizes imatinib-resistant chronic myeloid leukemia cells via endogenous ceramide accumulation. Journal of cancer research and clinical oncology 137: 1535-1544.
27. Itoh M, Kitano T, Watanabe M, Kondo T, Yabu T, et al. (2003) Possible role of ceramide as an indicator of chemoresistance: decrease of the ceramide content via activation of glucosylceramide synthase and sphingomyelin synthase in chemoresistant leukemia. Clin Cancer Res 9: 415-423.
28. Liu YY, Han TY, Yu JY, Bitterman A, Le A, et al. (2004) Oligonucleotides blocking glucosylceramide synthase expression selectively reverse drug resistance in cancer cells. J Lipid Res 45: 933-940.
29. Messner MC, Cabot MC Glucosylceramide in humans. Adv Exp Med Biol 688: 156-164.
30. Taha TA, El-Alwani M, Hannun YA, Obeid LM, (2006) Sphingosine kinase-1 is cleaved by cathepsin B in vitro: identification of the initial cleavage sites for the protease. FEBS Lett 580: 6047-6054.
31. Taha TA, Hannun YA, Obeid LM, (2006) Sphingosine kinase: biochemical and cellular regulation and role in disease. J Biochem Mol Biol 39: 113-131.
32. 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.
33. Rani CS, Abe A, Chang Y, Rosenzweig N, Saltiel AR, et al. (1995) Cell cycle arrest induced by an inhibitor of glucosylceramide synthase. Correlation with cyclin-dependent kinases. The Journal of biological chemistry 270: 2859-2867.
34. Aerts JM, Ottenhoff R, Powlson AS, Grefhorst A, van Eijk M, et al. (2007) Pharmacological inhibition of glucosylceramide synthase enhances insulin sensitivity. Diabetes 56: 1341-1349.
35. Colombini M, (2010) Ceramide channels and their role in mitochondria-mediated apoptosis. Biochim Biophys Acta 1797: 1239-1244.
36. Siskind LJ, Feinstein L, Yu T, Davis JS, Jones D, et al. (2008) Anti-apoptotic Bcl-2 family proteins disassemble ceramide channels. J Biol Chem.
37. Kim HJ, Mun JY, Chun YJ, Choi KH, Kim MY, (2001) Bax-dependent apoptosis induced by ceramide in HL-60 cells. FEBS Lett 505: 264-268.
38. von Haefen C, Wieder T, Gillissen B, Starck L, Graupner V, et al. (2002) Ceramide induces mitochondrial activation and apoptosis via a Bax-dependent pathway in human carcinoma cells. Oncogene 21: 4009-4019.
39. Chipuk JE, McStay GP, Bharti A, Kuwana T, Clarke CJ, et al. (2012) Sphingolipid metabolism cooperates with BAK and BAX to promote the mitochondrial pathway of apoptosis. Cell 148: 988-1000.
40. Ganesan V, Perera MN, Colombini D, Datskovskiy D, Chadha K, et al. (2010) Ceramide and activated Bax act synergistically to permeabilize the mitochondrial outer membrane. Apoptosis 15: 553-562.
41. Camgoz A, Gencer EB, Ural AU, Avcu F, Baran Y, (2011) Roles of ceramide synthase and ceramide clearence genes in nilotinib-induced cell death in chronic myeloid leukemia cells. Leukemia & lymphoma 52: 1574-1584.
42. Kartal M, Saydam G, Sahin F, Baran Y, (2011) Resveratrol triggers apoptosis through regulating ceramide metabolizing genes in human K562 chronic myeloid leukemia cells. Nutrition and cancer 63: 637-644.
43. Alphonse G, Bionda C, Aloy MT, Ardail D, Rousson R, et al. (2004) Overcoming resistance to gamma-rays in squamous carcinoma cells by poly-drug elevation of ceramide levels. Oncogene 23: 2703-2715.
44. Sinha UK, Schorn VJ, Hochstim C, Chinn SB, Zhu S, et al. (2011) Increased radiation sensitivity of head and neck squamous cell carcinoma with sphingosine kinase 1 inhibition. Head & neck 33: 178-188.
45. Grazide S, Terrisse AD, Lerouge S, Laurent G, Jaffrezou JP, (2004) Cytoprotective effect of glucosylceramide synthase inhibition against daunorubicin-induced apoptosis in human leukemic cell lines. The Journal of biological chemistry 279: 18256-18261.
46. Sobue S, Nemoto S, Murakami M, Ito H, Kimura A, et al. (2008) Implications of sphingosine kinase 1 expression level for the cellular sphingolipid rheostat: relevance as a marker for daunorubicin sensitivity of leukemia cells. International journal of hematology 87: 266-275.
47. Lim KG, Gray AI, Pyne S, Pyne NJ, (2012) Resveratrol dimers are novel sphingosine kinase 1 inhibitors and affect sphingosine kinase 1 expression and cancer cell growth and survival. British journal of pharmacology 166: 1605-1616.
48. Issuree PD, Pushparaj PN, Pervaiz S, Melendez AJ, (2009) Resveratrol attenuates C5a-induced inflammatory responses in vitro and in vivo by inhibiting phospholipase D and sphingosine kinase activities. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 23: 2412-2424.
49. Giraldo P, Alfonso P, Atutxa K, Fernandez-Galan MA, Barez A, et al. (2009) Real-world clinical experience with long-term miglustat maintenance therapy in type 1 Gaucher disease: the ZAGAL project. Haematologica 94: 1771-1775.
50. Schnute ME, McReynolds MD, Kasten T, Yates M, Jerome G, et al. (2012) Modulation of cellular S1P levels with a novel, potent and specific inhibitor of sphingosine kinase-1. The Biochemical journal 444: 79-88.