Sphingosine kinase 1 overexpression is regulated by signaling through PI3K, AKT2, and mTOR in imatinib-resistant chronic myeloid leukemia cells

Experimental Hematology

Volumn 39, Issue 6, 2011, Pages

  Marfe, Gabriella ^a   Di Stefano, Carla ^a   Gambacurta, Alessandra ^a   Ottone, Tiziana ^a,b   Martini, Valentina ^a   Abruzzese, Elisabetta ^a   Mologni, Luca ^c   Sinibaldi Salimei, Paola ^a   de Fabritis, Paolo ^d   Gambacorti Passerini, Carlo ^c   Amadori, Sergio ^a   Birge, Raymond B ^e  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d S EUGENIO HOSPITAL   (Italy)

^e RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BCR ABL PROTEIN; IMATINIB; MAMMALIAN TARGET OF RAPAMYCIN; N,N DIMETHYLSPHINGOSINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AKT1; PROTEIN AKT3; PROTEIN CRK; PROTEIN KINASE; PROTEIN KINASE B BETA; RNA; SMALL INTERFERING RNA; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1; TYROSINE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CHRONIC MYELOID LEUKEMIA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UPREGULATION;

SPHINGOIDEA;

EID: 79956274055     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2011.02.013     Document Type: Article

References (54)

1. Rowley J.D. Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973, 243:290-293.
2. Kantarjian H., Dixon D., Keating M.J., et al. Characteristics of accelerated disease in chronic myelogenous leukemia. Cancer 1988, 61:1441-1446.
3. Goldman J.M., Melo J.V. Chronic myeloid leukemia advances in biology and new approaches to treatment. N Engl J Med 2003, 349:1451-1464.
4. Kantarjian H., Sawyers C., Hochhaus A., et al. International STI571 CML Study Group. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med 2002, 346:645-652.
5. Sawyers C.L., Hochhaus A., Feldman E., et al. Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase II study. Blood 2002, 99:3530-3539.
6. Schindler T., Bornmann W., Pellicena P., et al. Structural mechanism for STI-571 inhibition of abelson tyrosine kinase. Science 2000, 289:1938-1942.
7. Gambacorti-Passerini C.B., Gunby R.H., Piazza R., et al. Molecular mechanisms of resistance to imatinib in Philadelphia-chromosome-positive leukaemias. Lancet Oncol 2003, 4:75-85.
8. Krystal G.W. Mechanisms of resistance to imatinib (STI571) and prospects for combination with conventional chemotherapeutic agents. Drug Resis Updates 2001, 4:16-21.
9. Hegedus T., Orfi L., Seprodi A., et al. Interaction of tyrosine kinase inhibitors with the human multidrug transporter proteins, MDR1 and MRP1. Biochim Biophys Acta 2002, 1587:318-325.
10. Deininger M. Resistance to imatinib: mechanisms and management. J Natl Compr Canc Netw 2005, 3:757-768.
11. Walz C., Sattler M. Novel targeted therapies to overcome imatinib mesylate resistance in chronic myeloid leukemia (CML). Crit Rev Oncol Hematol 2006, 57:145-164.
12. Baran Y., Salas A., Senkal C.E., et al. Alterations of ceramide/sphingosine 1-phosphate rheostat involved in the regulation of resistance to imatinib-induced apoptosis in K562 human chronic myeloid leukemia cells. J Biol Chem 2007, 282:10922-10934.
13. Kharas M.G., Janes M.R., Scarfone V.M., et al. Ablation of PI3K blocks BCR-ABL leukemogenesis in mice, and a dual PI3K/mTOR inhibitor prevents expansion of human BCR-ABL+ leukemia cells. J Clin Invest 2008, 118:3038-3050.
14. Um S.H., Frigerio F., Thomas G., et al. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 2004, 431:200-205.
15. Majumber P.K., Febbo P.G., Sellers W.R., et al. mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways. Nat Med 2004, 10:594-601.
16. Ruggero D., Montanaro L., Ma L., et al. The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med 2004, 10:484-486.
17. Edsall L.C., Van Brocklyn J.R., Cuvillier O., et al. 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.
18. Olivera A., Barlow K.D., Spiegel S. Assaying sphingosine kinase activity. Methods Enzymol 2000, 311:215-223.
19. Xia P., Gamble J.R., Wang L., et al. An oncogenic role of sphingosine kinase. Curr Biol 2000, 10:1527-1530.
20. Jendiroba D.B., Klostergaard J., Keyhani A., et al. Effective cytotoxicity against human leukemias and chemotherapy-resistant leukemia cell lines by N-N-dimethylsphingosine. Leuk Res 2002, 26:301-310.
21. Maceyka M., Payne S.G., Milstien S., Spiegel S. Sphingosine kinase, sphingosine-1-phosphate, and apoptosis. Biochim Biophys Acta 2002, 1585:193-201.
22. Le Scolan E., Pchejetski D., Banno Y., et al. Overexpression of sphingosine kinase 1 is an oncogenic event in erythroleukemic progression. Blood 2005, 106:1808-1816.
23. Van Brocklyn J.R., Jackson C.A., Pearl D.K., et al. Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme: roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J Neuropathol Exp Neurol 2005, 64:695-705.
24. Blakesly V.A., Beitner-Johnson D., Van Brocklyn J.R., et al. Sphingosine 1-phosphate stimulates tyrosine phosphorylation of Crk. J Biol Chem 1997, 272:16211-16215.
25. Birge R.B., Kalodimos C., Inagaki F., Tanaka S. Crk and CrkL adaptor proteins: networks for physiological and pathological signalling. Cell Commun Signal 2009, 7:13.
26. Mahon F.X., Deininger M.W., Schultheis B., et al. Selection and characterization of Bcr-Abl positive cell lines with differential sensitivity to the tyrosine kinase inhibitor STI571: diverse mechanisms of resistance. Blood 2000, 96:1070-1079.
27. Soverini S., Martinelli G., Amabile M., et al. Italian Cooperative Study Group on Chronic Myeloid Leukemia; European LeukemiaNet-6th Framework Program of the European Community. Denaturing-HPLC-based assay for detection of ABL mutations in chronic myeloid leukemia patients resistant to Imatinib. Clin Chem 2004, 50:1205-12013.
28. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, p. 2.
29. Mensink E., van de Locht A., Schattenberg A., et al. Quantitation of minimal residual disease in Philadelphia chromosome positive chronic myeloid leukaemia patients using real-time quantitative RT-PCR. Br J Haematol 1998, 102:768-774.
30. Venkataraman K., Thangada S., Michaud J., et al. Extracellular export of sphingosine kinase-1a contributes to the vascular S1P gradient. Biochem J 2006, 397:461-471.
31. le Coutre P., Tassi E., Varella-Garcia M., et al. Induction of resistance to the Abelson inhibitor STI571 in human leukemic cells through gene amplification. Blood 2000, 95:1758-1766.
32. Kono K., Tanaka M., Ogita T., Hosoya T., Kohama T. F-12509A, a new sphingosine kinase inhibitor, produced by a discomycete. J Antibiotics (Tokyo) 2000, 53:459-466.
33. Kohno M., Momoi M., Oo M., et al. Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol Cell Biol 2006, 26:7211-7223.
34. Bonhoure E., Pchejetski D., Aouali N., et al. Overcoming MDR-associated chemoresistance in HL-60 acute myeloid leukemia cells by targeting sphingosine kinase-1. Leukemia 2006, 20:95-102.
35. Bonhoure E., Lauret A., Barnes D.J., et al. Sphingosine kinase-1 is a downstream regulator of imatinib-induced apoptosis in chronic myeloid leukemia cells. Leukemia 2008, 22:971-979.
36. Ricci C., Onida F., Servida F., et al. In vitro anti-leukaemia activity of sphingosine kinase inhibitor. Br J Haematol 2009, 144:350-357.
37. Pene-Dumitrescu T., Smithgall T.E. Expression of a Src family kinase in chronic myelogenous leukemia cells induces resistance to imatinib in a kinase-dependent manner. J Biol Chem 2010, 285:21446-21457.
38. Monick M.M., Cameron K., Powers L.S., et al. Sphingosine kinase mediates activation of extracellular signal-related kinase and Akt by respiratory syncytial virus. Am J Respir Cell Mol Biol 2004, 30:844-852.
39. Johnson K.R., Becker K.P., Facchinetti M.M., Hannun Y.A., Lina M., Obeid L.M. 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.
40. Vadas M., Xia P., McCaughan G., Gamble J. The role of sphingosine kinase 1 in cancer: oncogene or non-oncogene addiction?. Biochim Biophys Acta 2008, 1781:442-447.
41. Cuvillier O. Downregulating sphingosine kinase-1 for cancer therapy. Expert Opin Ther Targets 2008, 12:1009-1020.
42. Shida D., Takabe K., Kapitonov D., et al. Targeting SphK1 as a new strategy against cancer. Curr Drug Targets 2008, 9:662-673.
43. Sobue S., Iwasaki T., Sugisaki C., et al. Quantitative RT-PCR analysis of sphingolipid metabolic enzymes in acute leukemia and myelodysplastic syndromes. Leukemia 2006, 20:2042-2046.
44. Pchejetski D., Golzio M., Bonhoure E., et al. Sphingosine kinase-1 as a chemotherapy sensor in prostate adenocarcinoma cell and mouse models. Cancer Res 2005, 65:11667-11675.
45. Endo A., Nagashima K., Kurose H., et al. Sphingosine 1-phosphate induces membrane ruffling and increases motility of human umbilical vein endothelial cells via vascular endothelial growth factor receptor and CrkI. J Biol Chem 2002, 277:23747-23754.
46. Panwalkar A., Verstovsek S., Giles F.J. Mammalian target of rapamycin inhibition as therapy for hematologic malignancies. Cancer 2004, 100:657-666.
47. Kharas M.G., Fruman D.A. ABL oncogenes and phosphoinositide 3-kinase: mechanism of activation and downstream effectors. Cancer Res 2005, 65:2047-2053.
48. Ly C., Arechiga A.F., Walsh C.M., Ong S.T. Bcr-Abl kinase modulates the translation regulators ribosomal protein S6 and 4E-BP1 in chronic myelogenous leukemia cells via the mammalian target of rapamycin. Cancer Res 2003, 63:5716-5722.
49. Parmar S., Smith J., Sassano A., et al. Differential regulation of the p70 S6 kinase pathway by interferon alpha (IFN alpha) and imatinib mesylate (STI571) in chronic myelogenous leukemia cells. Blood 2005, 106:2436-2443.
50. Manning B.D., Tee A.R., Logsdon M.N., et al. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell 2002, 10:151-162.
51. Zhang Y., Gao X., Saucedo L.J., et al. Rheb is a direct target of the tuberous sclerosis tumour suppressor proteins. Nat Cell Biol 2003, 5:578-581.
52. Schmelzle T., Hall M.N. TOR, a central controller of cell growth. Cell 2000, 103:253-262.
53. Hahn-Windgassen A., Nogueira A., Chen C.C., et al. Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem 2005, 280:32081-32089.
54. Francy J.M., Nag A., Conroy E.J., et al. Sphingosine kinase 1 expression is regulated by signaling through PI3K, AKT2, and mTOR in human coronary artery smooth muscle cells. Biochim Biophys Acta 2007, 269:253-265.