Ceramide promotes apoptosis in chronic myelogenous leukemia-derived K562 cells by a mechanism involving caspase-8 and JNK

Cell Cycle

Volumn 7, Issue 21, 2008, Pages 3362-3370

  Nica, Alina Felicia ^a   Chun, Chui Tsao ^a   Watt, Julie C ^b   Jiffar, Tilahun ^a   Kurinna, Svitlana ^a   Jurasz, Paul ^a   Konopleva, Marina ^b   Andreeff, Michael ^b   Radomski, Marek W ^a,c   Ruvolo, Peter P ^a,d,e  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c TRINITY COLLEGE DUBLIN   (Ireland)

^d University of Minnesota Hormel Institute   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Apoptosis; Casapse 8; Ceramide; Chronic myelogenous leukemia; JNK; Stress signal pathway

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BCR ABL PROTEIN; BENZYLOXYCARBONYL ASPARTYLGLUTAMYLVALYLASPARTIC ACID FLUOROMETHYLKETONE; BENZYLOXYCARBONYL ISOLEUCYLGLUTAMYLTHREONYLASPARTIC ACID FLUOROMETHYLKETONE; BENZYLOXYCARBONYL LEUCYLGLUTAMYLHISTIDYLASPARTIC ACID FLUOROMETHYLKETONE; CASPASE 3; CASPASE 3 INHIBITOR; CASPASE 8; CASPASE 8 INHIBITOR; CASPASE 9; CASPASE 9 INHIBITOR; CERAMIDE; CERAMIDE C6; IMATINIB; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN BCL XL; PROTEIN C JUN; PROTEIN MCL 1; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ACUTE LEUKEMIA; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL DEATH; CELL KILLING; CELL PROLIFERATION; CELL STRAIN K 562; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; DRUG POTENTIATION; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; PROTEIN FUNCTION; REGULATORY MECHANISM;

EID: 55849099564     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.7.21.6894     Document Type: Article

References (52)

1. Cortes JE, Talpaz M, Kantarjian H. Chronic myelogenous leukemia: a review. Am J Med 1996; 100:555-70.
2. Tefferi A, Gilliland DG. Oncogenes in myeloproliferative disorders. Cell Cycle 2007; 6:550-66.
3. Calabretta B, Perrotti D. The biology of CML blast crisis. Blood 2004; 103:4010-22.
4. Quintas-Cardama A, Kantarjian H, Cortes J. Flying under the radar: the new wave of BCRABL inhibitors. Nat Rev Drug Discov 2007; 6:834-48.
5. Kurzrock R, Gutterman JU, Talpaz M. The molecular genetics of Philadelphia chromosome-positive leukemias. N Engl J Med 1988; 319:990-8.
6. Shtivelman E, Lifshitz B, Gale RP, Canaani E. Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature 1985; 315:550-4.
7. Ben-Neriah Y, Daley GQ, Mes-Masson AM, Witte ON, Baltimore D. The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science 1986; 233:212-4.
8. Puil L, Liu J, Gish G, Mbamalu G, Bowtell D, Pelicci PG, Arlinghaus R, Pawson T. Bcr-Abl oncoproteins bind directly to activators of the Ras signalling pathway. EMBO J 1994; 13:764-73.
9. Deininger MW, Vieira S, Mendiola R, Schultheis B, Goldman JM, Melo JV. BCR-ABL tyrosine kinase activity regulates the expression of multiple genes implicated in the pathogenesis of chronic myeloid leukemia. Cancer Res 2000; 60:2049-55.
10. Deininger MW, Druker BJ. Specific targeted therapy of chronic myelogenous leukemia with imatinib. Pharmacol Rev 2003; 55:401-23.
11. Steelman LS, Pohnert SC, Shelton JG, Franklin RA, Bertrand FE, McCubrey JA. JAK/STAT, Raf/MEK/ERK, PI3K/Akt and BCR-ABL in cell cycle progression and leukemogenesis. Leukemia 2004; 18:189-218.
12. Thiesing JT, Ohno-Jones S, Kolibaba KS, Druker BJ. Efficacy of STI571, an abl tyrosine kinase inhibitor, in conjunction with other antileukemic agents against bcr-abl-positive cells. Blood 2000; 96:3195-9.
13. Druker BJ, Guilhot F, O'Brien SG, Gathmann I, Kantarjian H, Gattermann N, et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 2006; 355:2408-17.
14. Hochhaus A, Druker B, Sawyers C, Guilhot F, Schiffer CA, Cortes J, et al. Favorable long-term follow-up results over 6 years for response, survival and safety with imatinib mesylate therapy in chronic-phase chronic myeloid leukemia after failure of interferon-alpha treatment. Blood 2008; 111:1039-43.
15. Barnes DJ, Melo JV. Primitive, quiescent and difficult to kill: the role of non-proliferating stem cells in chronic myeloid leukemia. Cell Cycle 2006; 5:2862-6.
16. Ruvolo PP. Ceramide regulates cellular homeostasis via diverse stress signaling pathways. Leukemia 2001; 15:1153-60.
17. Hannun YA, Obeid LM. The Ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J Biol Chem 2002; 277:25847-50.
18. Pettus BJ, Chalfant CE, Hannun YA. Ceramide in apoptosis: an overview and current perspectives. Biochim Biophys Acta 2002; 1585:114-25.
19. Morales A, Lee H, Goñi FM, Kolesnick R, Fernandez-Checa JC. Sphingolipids and cell death. Apoptosis 2007; 12:923-39.
20. Kaufmann SH, Hengartner MO. Programmed cell death: alive and well in the new millennium. Trends Cell Biol 2001; 11:526-34.
21. Taylor RC, Cullen SP, Martin SJ. Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008; 9:231-41.
22. Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates and functions during apoptosis. Annu Rev Biochem 1999; 68:383-424.
23. Yang E, Korsmeyer SJ. Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood 1996; 88:386-401.
24. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007; 26:1324-37.
25. Basu A, You SA, Haldar S. Regulation of Bcl2 phosphorylation by stress response kinase pathway. Int J Oncol 2000; 16:497-500.
26. Deng X, Xiao L, Lang W, Gao F, Ruvolo P, May WS. Novel role for JNK as a stress-activated Bcl2 kinase. J Biol Chem 2001; 276:23681-8.
27. Ruvolo PP, Deng X, May WS. Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia 2001; 15:515-22.
28. Zhou P, Qian L, Kozopas KM, Craig RW. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood 1997; 89:630-43.
29. Le Gouill S, Podar K, Harousseau JL, Anderson KC. Mcl-1 regulation and its role in multiple myeloma. Cell Cycle 2004; 3:1259-62.
30. Inoshita S, Takeda K, Hatai T, Terada Y, Sano M, Hata J, Umezawa A, Ichijo H. Phosphorylation and inactivation of myeloid cell leukemia 1 by JNK in response to oxidative stress. J Biol Chem 2002; 277:43730-4.
31. Domina AM, Vrana JA, Gregory MA, Hann SR and Craig RW. MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 2004; 23:5301-15.
32. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 2006; 21:749-60.
33. Kobayashi S, Lee SH, Meng XW, Mott JL, Bronk SF, Werneburg NW, et al. Serine 64 phosphorylation enhances the antiapoptotic function of Mcl-1. J Biol Chem 2007; 282:18407-17.
34. Ruvolo PP, Deng X, Ito T, Carr BK, May WS. Ceramide induces Bcl2 dephosphorylation via a mechanism involving mitochondrial PP2A. J Biol Chem 1999; 274:20296-300.
35. Xie P, Shen YF, Shi YP, Ge SM, Gu ZH, Wang J, Mu HJ, et al. Overexpression of glucosylceramide synthase in associated with multidrug resistance of leukemia cells. Leuk Res 2008; 32:475-80.
36. Neviani P, Santhanam R, Trotta R, Notari M, Blaser BW, Liu S, et al. The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein. Cancer Cell 2005; 8:355-68.
37. Perrotti D, Neviani P. ReSETting PP2A tumour suppressor activity in blast crisis and imatinib-resistant chronic myelogenous leukaemia. Br J Cancer 2006; 95:775-81.
38. Neviani P, Santhanam R, Oaks JJ, Eiring AM, Notari M, Blaser BW, et al. FTY720, a new alternative for treating blast crisis chronic myelogenous leukemia and Philadelphia chromosome-positive acute lymphocytic leukemia. J Clin Invest 2007; 117:2408-21.
39. Ruvolo PP, Clark W, Mumby M, Gao F, May WS. A functional role for the B56 alpha-subunit of protein phosphatase 2A in ceramide-mediated regulation of Bcl2 phosphorylation status and function. J Biol Chem 2002; 277:22847-52.
40. Ricci C, Scappini B, Divoky V, Gatto S, Onida F, Verstovsek S, Kantarjian HM, Beran M. Mutation in the ATP-binding pocket of the ABL kinase domain in an STI571-resistant BCR/ABL-positive cell line. Cancer Res 2002; 62:5995-8.
41. Amarante-Mendes GP, Naekyung Kim C, Liu L, Huang Y, Perkins CL, et al. Bcr-Abl exerts its antiapoptotic effect against diverse apoptotic stimuli through blockage of mitochondrial release of cytochrome c and activation of caspase-3. Blood 1998; 91:1700-5.
42. Thomas RL Jr, Matsko CM, Lotze MT, Amoscato AA. Mass spectrometric identification of increased C16 ceramide levels during apoptosis. J Biol Chem 1999; 274:30580-8.
43. Ogretmen B, Schady D, Usta J, Wood R, Kraveka JM, Luberto C, Birbes H, et al. Role of ceramide in mediating the inhibition of telomerase activity in A549 human lung adenocarcinoma cells. J Biol Chem 2001; 276:24901-10.
44. Flamigni F, Faenza I, Marmiroli S, Stanic I, Giaccari A, Muscari C, et al. Inhibition of the expression of ornithine decarboxylase and c-Myc by cell-permeant ceramide in difluoromethylornithine-resistant leukaemia cells. Biochem J 1997; 324:783-9.
45. Dbaibo GS, Hannun YA. Signal transduction and the regulation of apoptosis: roles of ceramide. Apoptosis 1998; 3:317-34.
46. Mathias S, Peña LA, Kolesnick RN. Signal transduction of stress via ceramide. Biochem J 1998; 335:465-80.
47. Lin CF, Chen CL, Lin YS. Ceramide in apoptotic signaling and anticancer therapy. Curr Med Chem 2006; 13:1609-16.
48. Obeid LM, Lindardic CM, Karolak LA and Hannun YA. Programmed cell death induced by ceramide. Science 1993; 259:1769-71.
49. Mumby MC, Walter G. Protein serine/threonine phosphatases: Structure, regulation and function in cell growth. Physiological Reviews 1993; 73:673-99.
50. Arroyo JD, Hahn WC. Involvement of PP2A in viral and cellular transformation. Oncogene 2005; 24:7746-755.
51. Basu A, Haldar S. Identification of a novel Bcl-xL phosphorylation site regulating the sensitivity of taxol- or 2-methoxyestradiol-induced apoptosis. FEBS Lett 2003; 538:41-7.
52. Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, et al. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 1996; 380:75-9.