Interleukin-1β maintains an apoptosis-resistant phenotype in the blast cells of acute myeloid leukaemia via multiple pathways

Leukemia

Volumn 18, Issue 10, 2004, Pages 1662-1670

  Turzanski, J ^a   Grundy, M ^a   Russell, N H ^a   Pallis, M ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

AML; Apoptosis; Blast cell survival; Interleukin 1 ; NF kappa B; Phosphatidylinositol 3 OH kinase

Indexed keywords

5 (2,2 DICYANOVINYL) 2 NITROPHENOL; ACYLSPHINGOSINE DEACYLASE; ANTINEOPLASTIC AGENT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; N,N DIMETHYLSPHINGOSINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN BCL 2; PROTEIN TYROSINE KINASE INHIBITOR; RECOMBINANT INTERLEUKIN 1BETA; SPHINGOSINE KINASE; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; WORTMANNIN; AMIDASE; ENZYME INHIBITOR; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; PROTEIN KINASE; RECOMBINANT PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BLAST CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR BLOCKING; RECEPTOR DOWN REGULATION; STATISTICAL SIGNIFICANCE; SUSPENSION CELL CULTURE; CANCER STEM CELL; CELL CULTURE; CELL DIVISION; DRUG EFFECT; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMIDOHYDROLASES; APOPTOSIS; CELL DIVISION; ENZYME INHIBITORS; HUMANS; INTERLEUKIN-1; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; LEUKEMIA, MYELOCYTIC, ACUTE; NF-KAPPA B; PHENOTYPE; PHOSPHORYLATION; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TUMOR STEM CELLS;

EID: 6344253247     PISSN: 08876924     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.leu.2403457     Document Type: Article

References (52)

1. Smith BD, Bambach BJ, Vala MS, Barber JP, Enger C, Brodsky RA et al. Inhibited apoptosis and drug resistance in acute myeloid leukaemia. Br J Haematol 1998; 102: 1042-1049.
2. Wuchter C, Karawajew L, Ruppert V, Buchner T, Schoch C, Haferlach T et al. Clinical significance of CD95, Bcl-2 and Bax expression and CD95 function in adult de novo acute myeloid leukemia in context of P-glycoprotein function, maturation stage, and cytogenetics. Leukemia 1999; 13: 1943-1953.
3. Pallis M, Turzanski J, Higashi Y, Russell N. P-glycoprotein in acute myeloid leukaemia: therapeutic implications of its association with both a multidrug-resistant and an apoptosis-resistant phenotype. Leuk Lymphoma 2002; 43: 1221-1228.
4. Hoang T, Haman A, Goncalves O, Letendre F, Mathieu M, Wong GG et al. Interleukin 1 enhances growth factor-dependent proliferation of the clonogenic cells in acute myeloblastic leukemia and of normal human primitive hemopoietic precursors. J Exp Med 1988; 168: 463-474.
5. Griffin JD, Rambaldi A, Vellenga E, Young DC, Ostapovicz D, Cannistra SA. Secretion of interleukin-1 by acute myeloblastic leukemia cells in vitro induces endothelial cells to secrete colony stimulating factors. Blood 1987; 70: 1218-1221.
6. Cozzolino F, Rubartelli A, Aldinucci D, Sitia R, Torcia M, Shaw A et al. Interleukin 1 as an autocrine growth factor for acute myeloid leukemia cells. Proc Natl Acad Sci USA 1989; 86: 2369-2373.
7. Ezaki K, Tsuzuki M, Katsuta I, Maruyama F, Kojima H, Okamoto M et al. Interleukin-1 beta (IL-1 beta) and acute leukemia: in vitro proliferative response to IL-1 beta, IL-1 beta content of leukemic cells and treatment outcome. Leuk Res 1995; 19: 35-41.
8. Bradbury D, Rogers S, Kozlowski R, Bowen G, Reilly IA, Russell NH. Interleukin-1 is one factor which regulates autocrine production of GM-CSF by the blast cells of acute myeloblastic leukaemia. Br J Haematol 1990; 76: 488-493.
9. Bradbury D, Rogers S, Reilly IA, Kozlowski R, Russell NH. Role of autocrine and paracrine production of granulocyte-macrophage colony-stimulating factor and interleukin-1 beta in the autonomous growth of acute myeloblastic leukaemia cells - studies using purified CD34-positive cells. Leukemia 1992; 6: 562-566.
10. Estrov Z, Kurzrock R, Estey E, Wetzler M, Ferrajoli A, Harris D et al. Inhibition of acute myelogenous leukemia blast proliferation by interleukin-1 (IL-1) receptor antagonist and soluble IL-1 receptors. Blood 1992; 79: 1938-1945.
11. Auron PE. The interleukin 1 receptor: ligand interactions and signal transduction. Cytokine Growth Factor Rev 1998; 9: 221-237.
12. Franzen R, Pautz A, Brautigam L, Geisslinger G, Pfeilschifter J, Huwiler A. Interleukin-1beta induces chronic activation and de novo synthesis of neutral ceramidase in renal mesangial cells. J Biol Chem 2001; 276: 35382-35389.
13. Stosic-Grujicic S, Basara N, Dinarello CA. Modulatory in vitro effects of interleukin-1 receptor antagonist (IL-1Ra) or antisense oligonucleotide to interleukin-1 beta converting enzyme (ICE) on acute myeloid leukaemia (AML) cell growth. Clin Lab Haematol 1999; 21: 173-185.
14. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999; 13: 2905-2927.
15. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002; 2: 489-501.
16. Madge LA, Pober JS. A phosphatidylinositol 3-kinase/Akt pathway, activated by tumor necrosis factor or interleukin-1, inhibits apoptosis but does not activate NFkappaB in human endothelial cells. J Biol Chem 2000; 275: 15458-15465.
17. McCubrey JA, May WS, Duronio V, Mufson A. Serine/threonine phosphorylation in cytokine signal transduction. Leukemia 2000; 14: 9-21.
18. Tsuruta F, Masuyama N, Gotoh Y. The phosphatidylinositol 3-kinase (PI3K)-Akt pathway suppresses Bax translocation to mitochondria. J Biol Chem 2002; 277: 14040-14047.
19. Birkenkamp KU, Esselink MT, Kruijer W, Vellenga E. An inhibitor of PI3-K differentially affects proliferation and IL-6 protein secretion in normal and leukemic myeloid cells depending on the stage of differentiation. Exp Hematol 2000; 28: 1239-1249.
20. Xu Q Simpson SE, Scialla TJ, Bagg A, Carroll M. Survival of acute myeloid leukemia cells requires PI3 kinase activation. Blood 2003; 102: 972-980.
21. May WS, Tyler PG, Ito T, Armstrong DK, Qatsha KA, Davidson NE. Interleukin-3 and bryostatin-1 mediate hyperphosphorylation of BCL2 alpha in association with suppression of apoptosis. J Biol Chem 1994; 269: 26865-26870.
22. Ruvolo PP. Intracellular signal transduction pathways activated by ceramide and its metabolites. Pharmacol Res 2003; 47: 383-392.
23. 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: 20296-20300.
24. Itoh M, Kitano T, Watanabe M, Kondo T, Yabu T, Taguchi Y et al. 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 2003; 9: 415-423.
25. Okazaki T, Kondo T, Kitano T, Tashima M. Diversity and complexity of ceramide signalling in apoptosis. Cell Signal 1998; 10: 685-692.
26. Le Stunff H, Peterson C, Thornton R, Milstien S, Mandala SM, Spiegel S. Characterization of murine sphingosine-1-phosphate phosphohydrolase. J Biol Chem 2002; 277: 8920-8927.
27. Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003; 4: 397-407.
28. Cuvillier O, Levade T. Sphingosine 1-phosphate antagonizes apoptosis of human leukemia cells by inhibiting release of cytochrome c and Smac/DIABLO from mitochondria. Blood 2001; 98: 2828-2836.
29. Johnson KR, Becker KP, Facchinetti MM, Hannun YA, Obeid LM. PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA). J Biol Chem 2002; 277 35257-35262.
30. Pallis M. Sphingosine kinase inhibitors in the apoptosis of leukaemia cells. Leuk Res 2002; 26: 415-416.
31. Jendiroba DB, Klostergaard J, Keyhani A, Pagliaro L, Freireich EJ. Effective cytotoxicity against human leukemias and chemotherapy-resistant leukemia cell lines by N-N-dimethylsphingosine. Leuk Res 2002; 26: 301-310.
32. Li X, Stark GR. NFkappaB-dependent signaling pathways. Exp Hematol 2002; 30: 285-296.
33. Estrov Z, Manna SK, Harris D, Van Q, Estey EH, Kantarjian HM et al. Phenylarsine oxide blocks interleukin-1beta-induced activation of the nuclear transcription factor NF-kappaB, inhibits proliferation, and induces apoptosis of acute myelogenous leukemia cells. Blood 1999; 94: 2844-2853.
34. Estrov Z, Shishodia S, Faderl S, Harris D, Van Q, Kantarjian HM et al. Resveratrol blocks interleukin-1beta-induced activation of the nuclear transcription factor NF-kappaB, inhibits proliferation, causes S-phase arrest, and induces apoptosis of acute myeloid leukemia cells. Blood 2003; 102: 987-995.
35. Bol G, Kreuzer OJ, Brigelius-Flohe R. Translocation of the interleukin-1 receptor-associated kinase-1 (IRAK-1) into the nucleus. FEBS Lett 2000; 477: 73-78.
36. Cooke EL, Uings IJ, Xia CL, Woo P, Ray KP. Functional analysis of the interleukin-1-receptor-associated kinase (IRAK-1) in interleukin-1 beta-stimulated nuclear factor kappa B (NF-kappa B) pathway activation: IRAK-1 associates with the NF-kappa B essential modulator (NEMO) upon receptor stimulation. Biochem J 2001; 359: 403-410.
37. Guzman ML, Neering SJ, Upchurch D, Grimes B, Howard DS, Rizzieri DA et al. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood 2001; 98: 2301-2307.
38. Dinarello CA, Thompson RC. Blocking IL-1: interleukin 1 receptor antagonist in vivo and in vitro. Immunol Today 1991; 12: 404-410.
39. Dinarello CA. Biologic basis for interleukin-1 in disease. Blood 1996; 87: 2095-2147.
40. Pallis M, Syan J, Russell NH. Flow cytometric chemosensitivity analysis of blasts from patients with acute myeloblastic leukemia and myelodysplastic syndromes: the use of 7AAD with antibodies to CD45 or CD34. Cytometry 1999; 37: 308-313.
41. Pallis M, Russell N. P-glycoprotein plays a drug-efflux-independent role in augmenting cell survival in acute myeloblastic leukemia and is associated with modulation of a sphingomyelinceramide apoptotic pathway. Blood 2000; 95: 2897-2904.
42. Pallis M, Turzanski J, Grundy M, Seedhouse C, Russell N. Resistance to spontaneous apoptosis in acute myeloid leukaemia blasts is associated with p-glycoprotein expression and function, but not with the presence of FLT3 internal tandem duplications. Br J Haematol 2003; 120: 1009-1016.
43. Tazzari PL, Cappellini A, Bortul R, Ricci F, Billi AM, Tabellini G et al. Flow cytometric detection of total and serine 473 phosphorylated Akt. J Cell Biochem 2002; 86: 704-715.
44. Renard P, Ernest I, Houbion A, Art M, Le Calvez H, Raes M, Remacle J. Development of a sensitive multi-well colorimetric assay for active NFkappaB. Nucleic Acids Res 2001; 29: E21.20.
45. Lang RA, Burgess AW. Autocrine growth factors and tumourigenic transformation. Immunol Today 1990; 11: 244-249.
46. Franklin RA, McCubrey JA. Kinases: positive and negative regulators of apoptosis. Leukemia 2000; 14: 2019-2034.
47. Schultz RM, Merriman RL, Andis SL, Bonjouklian R, Grindey GB, Rutherford PG et al. In vitro and in vivo antitumor activity of the phosphatidylinositol-3-kinase inhibitor, wortmannin. Anticancer Res 1995; 15: 1135-1139.
48. Li L, Cousart S, Hu J, McCall CE. Characterization of interleukin-1 receptor-associated kinase in normal and endotoxin-tolerant cells. J Biol Chem 2000; 275: 23340-23345.
49. Khan WA, Dobrowsky R, el Touny S, Hannun YA. Protein kinase C and platelet inhibition by D-erythro-sphingosine: comparison with N,N-dimethylsphingosine and commercial preparation. Biochem Biophys Res Commun 1990; 172: 683-691.
50. Edsall LC, Van Brocklyn JR, Cuvillier O, Kleuser B, Spiegel S. N,N-dimethylsphingosine is a potent competitive inhibitor of sphingosine kinase but not of protein kinase C: modulation of cellular levels of sphingosine 1-phosphate and ceramide. Biochemistry 1998; 37: 12892-12898.
51. Zhao S, Konopleva M, Cabreira-Hansen M, Xie Z, Hu W, Milella M et al. Inhibition of phosphatidylinositol 3-kinase dephosphorylates BAD and promotes apoptosis in myeloid leukemias. Leukemia 2004; 18: 267-275.
52. Ito T, Deng X, Carr B, May WS. Bcl-2 phosphorylation required for anti-apoptosis function. J Biol Chem 1997; 272: 11671-11673.