Sphingomyelin synthase 1 activity is regulated by the BCR-ABL oncogene

Journal of Lipid Research

Volumn 54, Issue 3, 2013, Pages 794-805

  Burns, Tara Ann ^a   Subathra, Marimuthu ^a   Signorelli, Paola ^b   Choi, Young ^a   Yang, Xiaofeng ^a   Wang, Yong ^a   Villani, Maristella ^a,c   Bhalla, Kapil ^d   Zhou, Daohong ^e   Luberto, Chiara ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b SAN PAOLO HOSPITAL   (Italy)

^c Polispecialistica Bios   (Italy)

^d UNIVERSITY OF KANSAS CANCER CENTER   (United States)

^e UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Ceramide; Diacylglycerol; Imatinib mesylate

Indexed keywords

BCR ABL PROTEIN; CERAMIDE; DIACYLGLYCEROL; IMATINIB; ISOENZYME; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; SPHINGOMYELIN SYNTHASE 1; SYNTHETASE; TRICYCLO[4.3.0.1]DECAN 9 YL XANTHOGENATE; UNCLASSIFIED DRUG;

ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CELL STRAIN HL 60; CELL STRAIN K 562; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME REGULATION; GENE ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LEUKEMOGENESIS; LIPOGENESIS; ONCOGENE; ONCOGENE BCR-ABL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SMS1 GENE;

BENZAMIDES; BRIDGED COMPOUNDS; CELL LINE; CERAMIDES; DIGLYCERIDES; GENES, ABL; HL-60 CELLS; HUMANS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; PIPERAZINES; PYRIMIDINES; THIONES; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

EID: 84874035435     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M033985     Document Type: Article

References (59)

1. Bernert, J. T., and M. D. Ullman. 1981. Biosynthesis of sphingomyelin from erythro-ceramides and phosphatidylcholine by a microsomal cholinephosphoesterase. Biochim. Biophys. Acta. 666 : 99-109.
2. Hatch, G. M., and D. E. Vance. 1992. Stimulation of sphingomyelin biosynthesis by brefeldin A and sphingomyelin breakdown by okadaic acid treatment of rat hepatocytes. J. Biol. Chem. 267 : 12443-12451.
3. Marggraf, W. D., F. A. Anderer, and J. Kanfer. 1981. The formation of sphingomyelin from phosphatidylcholine in plasma membrane preparations from mouse fi broblasts. Biochim. Biophys. Acta. 664 : 61-73.
4. Marggraf, W. D., R. Zertani, F. A. Anderer, and J. N. Kanfer. 1982. The role of endogenous phosphatidylcholine and ceramide in the biosynthesis of sphingomyelin in mouse fi broblasts. Biochim. Biophys. Acta. 710 : 314-323.
5. Merrill, A. H., Jr., and D. D. Jones. 1990. An update of the enzymology and regulation of sphingomyelin metabolism. Biochim.Biophys. Acta Lipids Lipid Metab. 1044 : 1-12.
6. Ullman, M. D., and N. S. Radin. 1974. The enzymatic formation of sphingomyelin from ceramide and lecithin in mouse liver. J. Biol. Chem. 249 : 1506-1512.
7. Voelker, D. R. K., and E. P. Kennedy. 1982. Cellular and enzymic synthesis of sphingomyelin. Biochemistry. 21 : 2753-2759.
8. Luberto, C., and Y. A. Hannun. 1998. Sphingomyelin synthase, a potential regulator of intracellular levels of ceramide and diacylglycerol during SV40 transformation. Does sphingomyelin synthase account for the putative phosphatidylcholine-phospholipase C? J. Biol. Chem. 273 : 14550-14559.
9. Miro-Obradors, M.-J., J. Osada, H. Aylagas, I. Sanchez-Vegazo, and E. Palacios-Alaiz. 1993. Microsomal sphingomyelin accumulation in thioacetamide-injured regenerating rat liver: involvement of sphingomyelin synthase activity. Carcinogenesis. 14 : 941-946.
10. Riboni, L., P. Viani, R. Bassi, P. Giussani, and G. Tettamanti. 2001. Basic fi broblast growth factor-induced proliferation of primary astrocytes. evidence for the involvement of sphingomyelin biosynthesis. J. Biol. Chem. 276 : 12797-12804.
11. van den Hill, A., G. P. van Heusden, and K. W. Wirtz. 1985. The synthesis of sphingomyelin in the Morris hepatomas 7777 and 5123D is restricted to the plasma membrane. Biochim. Biophys. Acta. 833 : 354-357.
12. Bourteele, S., A. Hausser, H. Doppler, J. Horn-Muller, C. Ropke, G. Schwarzmann, K. Pfi zenmaier, and G. Muller. 1998. Tumor necrosis factor induces ceramide oscillations and negatively controls sphingolipid synthases by caspases in apoptotic Kym-1 cells. J. Biol. Chem. 273 : 31245-31251.
13. Watanabe, M., T. Kitano, T. Kondo, T. Yabu, Y. Taguchi, M. Tashima, H. Umehara, N. Domae, T. Uchiyama, and T. Okazaki. 2004. Increase of nuclear ceramide through caspase-3-dependent regulation of the "sphingomyelin cycle" in Fas-induced apoptosis. Cancer Res. 64 : 1000-1007.
14. Huitema, K., J. Van Den Dikkenberg, J. F. Brouwers, and J. C. Holthuis. 2004. Identifi cation of a family of animal sphingomyelin synthases. EMBO J. 23 : 33-44.
15. Yamaoka, S., M. Miyaji, T. Kitano, H. Umehara, and T. Okazaki. 2004. Expression cloning of a human cDNA restoring sphingomyelin synthesis and cell growth in sphingomyelin synthase-defective lymphoid cells. J. Biol. Chem. 279 : 18688-18693.
16. Villani, M., M. Subathra, Y. B. Im, Y. Choi, P. Signorelli, M. Del Poeta, and C. Luberto. 2008. Sphingomyelin synthases regulate production of diacylglycerol at the Golgi. Biochem. J. 414 : 31-41.
17. Yeang, C., S. Varshney, R. Wang, Y. Zhang, D. Ye, and X. C. Jiang. 2008. The domain responsible for sphingomyelin synthase (SMS) activity. Biochim. Biophys. Acta. 1781 : 610-617.
18. Tani, M., and O. Kuge. 2009. Sphingomyelin synthase 2 is palmitoylated at the COOH-terminal tail, which is involved in its localization in plasma membranes. Biochem. Biophys. Res. Commun. 381 : 328-332.
19. Separovic, D., K. Hanada, M. Y. Maitah, B. Nagy, I. Hang, M. A. Tainsky, J. M. Kraniak, and J. Bielawski. 2007. Sphingomyelin synthase 1 suppresses ceramide production and apoptosis post-photodamage. Biochem. Biophys. Res. Commun. 358 : 196-202.
20. Separovic, D., L. Semaan, A. L. Tarca, M. Y. Awad Maitah, K. Hanada, J. Bielawski, M. Villani, and C. Luberto. 2008. Suppression of sphingomyelin synthase 1 by small interference RNA is associated with enhanced ceramide production and apoptosis after photodamage. Exp. Cell Res. 314 : 1860-1868.
21. Ding, T., Z. Li, T. Hailemariam, S. Mukherjee, F. R. Maxfi eld, M. P. Wu, and X. C. Jiang. 2008. SMS overexpression and knockdown: impact on cellular sphingomyelin and diacylglycerol metabolism, and cell apoptosis. J. Lipid Res. 49 : 376-385.
22. Tafesse, F. G., K. Huitema, M. Hermansson, S. van der Poel, J. van den Dikkenberg, A. Uphoff, P. Somerharju, and J. C. Holthuis. 2007. Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells. J. Biol. Chem. 282 : 17537-17547.
23. Li, Z., T. K. Hailemariam, H. Zhou, Y. Li, D. C. Duckworth, D. A. Peake, Y. Zhang, M. S. Kuo, G. Cao, and X. C. Jiang. 2007. Inhibition of sphingomyelin synthase (SMS) affects intracellular sphingomyelin accumulation and plasma membrane lipid organization. Biochim. Biophys. Acta. 1771 : 1186-1194.
24. Lafont, E., D. Milhas, S. Carpentier, V. Garcia, Z. X. Jin, H. Umehara, T. Okazaki, K. Schulze-Osthoff, T. Levade, H. Benoist, et al. 2009. Caspase-mediated inhibition of sphingomyelin synthesis is involved in FasL-triggered cell death. Cell Death Differ. 17 : 642-654.
25. Itoh, M., T. Kitano, M. Watanabe, T. Kondo, T. Yabu, Y. Taguchi, K. Iwai, M. Tashima, T. Uchiyama, and T. Okazaki. 2003. Possible roleof 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.
26. Wong, S., and O. N. Witte. 2004. The BCR-ABL story: bench to bedside and back. Annu. Rev. Immunol. 22 : 247-306.
27. Quintas-Cardama, A., and J. Cortes. 2009. Molecular biology of bcrabl1-positive chronic myeloid leukemia. Blood. 113 : 1619-1630.
28. Marley, S. B., and M. Y. Gordon. 2005. Chronic myeloid leukaemia: stem cell derived but progenitor cell driven. Clin. Sci. (Lond.). 109 : 13-25.
29. Karbasian Esfahani, M., E. L. Morris, J. P. Dutcher, and P. H. Wiernik. 2006. Blastic phase of chronic myelogenous leukemia. Curr. Treat. Options Oncol. 7 : 189-199.
30. Ren, R. 2005. Mechanisms of BCR-ABL in the pathogenesis of chronic myelogenous leukaemia. Nat. Rev. Cancer. 5 : 172-183.
31. Deininger, M. W., J. M. Goldman, and J. V. Melo. 2000. The molecular biology of chronic myeloid leukemia. Blood. 96 : 3343-3356.
32. Sessions, J. 2007. Chronic myeloid leukemia in 2007. Am. J. Health Syst. Pharm. 64 : S4-S9.
33. Kantarjian, H. M., J. Cortes, S. O'Brien, F. J. Giles, M. Albitar, M. B. Rios, J. Shan, S. Faderl, G. Garcia-Manero, D. A. Thomas, et al. 2002. Imatinib mesylate (STI571) therapy for Philadelphia chromosome-positive chronic myelogenous leukemia in blast phase. Blood. 99 : 3547-3553.
34. Lydon, N. B., and B. J. Druker. 2004. Lessons learned from the development of imatinib. Leuk. Res. 28 ( Suppl 1 ): S29-S38.
35. Marin, D., S. Marktel, M. Bua, L. Armstrong, J. M. Goldman, J. F. Apperley, and E. Olavarria. 2002. The use of imatinib (STI571) in chronic myelod leukemia: some practical considerations. Haematologica. 87 : 979-988.
36. Apperley, J. F. 2007. Part I: mechanisms of resistance to imatinib in chronic myeloid leukaemia. Lancet Oncol. 8 : 1018-1029.
37. Kantarjian, H. M., M. Talpaz, D. Kontoyiannis, J. Gutterman, M. J. Keating, E. H. Estey, S. O'Brien, M. B. Rios, M. Beran, and A. Deisseroth. 1992. Treatment of chronic myelogenous leukemia in accelerated and blastic phases with daunorubicin, high-dose cytarabine, and granulocyte-macrophage colony-stimulating factor. J. Clin. Oncol. 10 : 398-405.
38. Kantarjian, H. M., R. S. Walters, M. J. Keating, M. Talpaz, B. Andersson, M. Beran, K. B. McCredie, and E. J. Freireich. 1988. Treatment of the blastic phase of chronic myelogenous leukemia with mitoxantrone and high-dose cytosine arabinoside. Cancer. 62 : 672-676.
39. Axdorph, U., L. Stenke, G. Grimfors, J. Carneskog, J. Hansen, O. Linder, P. Ljungman, E. Lofvenberg, C. Malm, B. Simonsson, et al. 2002. Intensive chemotherapy in patients with chronic myelogenous leukaemia (CML) in accelerated or blastic phase: a report from the Swedish CML Group. Br. J. Haematol. 118 : 1048-1054.
40. Amarante-Mendes, G. P., C. Naekyung Kim, L. Liu, Y. Huang, C. L. Perkins, D. R. Green, and K. Bhalla. 1998. Bcr-Abl exerts its antiapoptotic effect against diverse apoptotic stimuli through blockage of mitochondrial release of cytochrome C and activation of caspase-3. Blood. 91 : 1700-1705.
41. Scherr, M., K. Battmer, T. Winkler, O. Heidenreich, A. Ganser, and M. Eder. 2003. Specifi c inhibition of bcr-abl gene expression by small interfering RNA. Blood. 101 : 1566-1569.
42. Ames, B. N., and D. T. Dubin. 1960. The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J. Biol. Chem. 235 : 769-775.
43. Kishimoto, A., Y. Takai, T. Mori, U. Kikkawa, and Y. Nishizuka. 1980. Activation of calcium and phospholipid-dependent protein kinase by diacylglycerol, its possible relation to phosphatidylinositol turnover. J. Biol. Chem. 255 : 2273-2276.
44. Takai, Y., A. Kishimoto, U. Kikkawa, T. Mori, and Y. Nishizuka. 1979. Unsaturated diacylglycerol as a possible messenger for the activation of calcium-activated, phospholipid-dependent protein kinase system. Biochem. Biophys. Res. Commun. 91 : 1218-1224.
45. Griner, E. M., and M. G. Kazanietz. 2007. Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer. 7 : 281-294.
46. Obeid, L. M., C. M. Linardic, L. A. Karolak, and Y. A. Hannun. 1993. Programmed cell death induced by ceramide. Science. 259 : 1769-1771.
47. Senkal, C. E., S. Ponnusamy, M. J. Rossi, J. Bialewski, D. Sinha, J. C. Jiang, S. M. Jazwinski, Y. A. Hannun, and B. Ogretmen. 2007. Role of human longevity assurance gene 1 and C18-ceramide in chemotherapy-induced cell death in human head and neck squamous cell carcinomas. Mol. Cancer Ther. 6 : 712-722.
48. Marchesini, N., W. Osta, J. Bielawski, C. Luberto, L. M. Obeid, and Y. A. Hannun. 2004. Role for mammalian neutral sphingomyelinase 2 in confl uence-induced growth arrest of MCF7 cells. J. Biol. Chem. 279 : 25101-25111.
49. Kroesen, B. J., S. Jacobs, B. J. Pettus, H. Sietsma, J. W. Kok, Y. A. Hannun, and L. F. de Leij. 2003. BcR-induced apoptosis involves differential regulation of C16 and C24-ceramide formation and sphingolipid-dependent activation of the proteasome. J. Biol. Chem. 278 : 14723-14731.
50. White-Gilbertson, S., T. Mullen, C. Senkal, P. Lu, B. Ogretmen, L. Obeid, and C. Voelkel-Johnson. 2009. Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells. Oncogene. 28 : 1132-1141.
51. Bikman, B. T., and S. A. Summers. 2011. Ceramides as modulators of cellular and whole-body metabolism. J. Clin. Invest. 121 : 4222-4230.
52. Henry, B., C. Moller, M. T. Dimanche-Boitrel, E. Gulbins, and K. A. Becker. 2011. Targeting the ceramide system in cancer. Cancer Lett.
53. Mullen, T. D., and L. M. Obeid. 2011. Ceramide and apoptosis: exploring the enigmatic connections between sphingolipid metabolism and programmed cell death. Anticancer. Agents Med. Chem.
54. Nica, A. F., C. C. Tsao, J. C. Watt, T. Jiffar, S. Kurinna, P. Jurasz, M. Konopleva, M. Andreeff, M. W. Radomski, and P. P. Ruvolo. 2008. Ceramide promotes apoptosis in chronic myelogenous leukemia-derived K562 cells by a mechanism involving caspase-8 and JNK. Cell Cycle. 7 : 3362-3370.
55. Baran, Y., A. Salas, C. E. Senkal, U. Gunduz, J. Bielawski, L. M. Obeid, and B. Ogretmen. 2007. 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. 282 : 10922-10934.
56. Bonhoure, E., A. Lauret, D. J. Barnes, C. Martin, B. Malavaud, T. Kohama, J. V. Melo, and O. Cuvillier. 2008. Sphingosine kinase-1 is a downstream regulator of imatinib-induced apoptosis in chronic myeloid leukemia cells. Leukemia. 22 : 971-979.
57. Perry, R. J., and N. D. Ridgway. 2004. The role of de novo ceramide synthesis in the mechanism of action of the tricyclic xanthate D609. J. Lipid Res. 45 : 164-173.
58. Gotoh, A., K. Miyazawa, K. Ohyashiki, and K. Toyama. 1994. Potential molecules implicated in downstream signaling pathways of p185BCR-ABL in Ph+ ALL involve GTPase-activating protein, phospholipase C-gamma 1, and phosphatidylinositol 3 ?-kinase. Leukemia. 8 : 115-120.
59. Markova, B., C. Albers, F. Breitenbuecher, J. V. Melo, T. H. Brummendorf, F. Heidel, D. Lipka, J. Duyster, C. Huber, and T. Fischer. 2010. Novel pathway in Bcr-Abl signal transduction involves Akt-independent, PLC-gamma1-driven activation of mTOR/p70S6-kinase pathway. Oncogene. 29 : 739-751.