Downregulation of neutral ceramidase by gemcitabine: Implications for cell cycle regulation

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 8, 2009, Pages 730-739

  Wu, Bill X ^a   Zeidan, Youssef H ^a   Hannun, Yusuf A ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cell cycle arrest; Ceramide; Gemcitabine; Neutral ceramidase; Sphingolipid

Indexed keywords

ACYLSPHINGOSINE DEACYLASE; GEMCITABINE; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME METABOLISM; FLOW CYTOMETRY; GENETIC TRANSFECTION; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; WESTERN BLOTTING;

ANIMALS; CELL CYCLE; CELL LINE; CERAMIDES; DEOXYCYTIDINE; DOWN-REGULATION; ENDOTHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; MICE; NEUTRAL CERAMIDASE; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN; RNA, SMALL INTERFERING; SPHINGOMYELIN PHOSPHODIESTERASE;

MURINAE;

EID: 67650239637     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.03.012     Document Type: Article

References (52)

1. Hannun Y.A., and Obeid L.M. The ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind. J. Biol. Chem. 277 (2002) 25847-25850
2. Ogretmen B., and Hannun Y.A. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat. Rev. Cancer 4 (2004) 604-616
3. Taha T.A., Hannun Y.A., and Obeid L.M. Sphingosine kinase: biochemical and cellular regulation and role in disease. J. Biochem. Mol. Biol. 39 (2006) 113-131
4. El Alwani M., Wu B.X., Obeid L.M., and Hannun Y.A. Bioactive sphingolipids in the modulation of the inflammatory response. Pharmacol. Ther. 112 (2006) 171-183
5. Pettus B.J., Chalfant C.E., and Hannun Y.A. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 1585 (2002) 114-125
6. Modrak D.E., Gold D.V., and Goldenberg D.M. Sphingolipid targets in cancer therapy. Mol. Cancer Ther. 5 (2006) 200-208
7. Rani C.S., Abe A., Chang Y., Rosenzweig N., Saltiel A.R., Radin N.S., and Shayman J.A. Cell cycle arrest induced by an inhibitor of glucosylceramide synthase. Correlation with cyclin-dependent kinases. J. Biol. Chem. 270 (1995) 2859-2867
8. Jayadev S., Liu B., Bielawska A.E., Lee J.Y., Nazaire F., Pushkareva M., Obeid L.M., and Hannun Y.A. Role for ceramide in cell cycle arrest. J. Biol. Chem. 270 (1995) 2047-2052
9. Kim J.H., Han J.S., and Yoon Y.D. Biochemical and morphological identification of ceramide-induced cell cycle arrest and apoptosis in cultured granulosa cells. Tissue Cell 31 (1999) 531-539
10. Ogretmen B., Schady D., Usta J., Wood R., Kraveka J.M., Luberto C., Birbes H., Hannun Y.A., and Obeid L.M. Role of ceramide in mediating the inhibition of telomerase activity in A549 human lung adenocarcinoma cells. J. Biol. Chem. 276 (2001) 24901-24910
11. Ogretmen B., Pettus B.J., Rossi M.J., Wood R., Usta J., Szulc Z., Bielawska A., Obeid L.M., and Hannun Y.A. Biochemical mechanisms of the generation of endogenous long chain ceramide in response to exogenous short chain ceramide in the A549 human lung adenocarcinoma cell line. Role for endogenous ceramide in mediating the action of exogenous ceramide. J. Biol. Chem. 277 (2002) 12960-12969
12. Marchesini N., Luberto C., and Hannun Y.A. Biochemical properties of mammalian neutral sphingomyelinase 2 and its role in sphingolipid metabolism. J. Biol. Chem. 278 (2003) 13775-13783
13. Marchesini N., Osta W., Bielawski J., Luberto C., Obeid L.M., and Hannun Y.A. Role for mammalian neutral sphingomyelinase 2 in confluence-induced growth arrest of MCF7 cells. J. Biol. Chem. 279 (2004) 25101-25111
14. Tafesse F.G., Huitema K., Hermansson M., van der Poel S., van den Dikkenberg J., Uphoff A., Somerharju P., and Holthuis J.C. Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells. J. Biol. Chem. 282 (2007) 17537-17547
15. Tani M., Okino N., Mori K., Tanigawa T., Izu H., and Ito M. Molecular cloning of the full-length cDNA encoding mouse neutral ceramidase. A novel but highly conserved gene family of neutral/alkaline ceramidases. J. Biol. Chem. 275 (2000) 11229-11234
16. Mao C., Xu R., Bielawska A., and Obeid L.M. Cloning of an alkaline ceramidase from Saccharomyces cerevisiae. An enzyme with reverse (CoA-independent) ceramide synthase activity. J. Biol. Chem. 275 (2000) 6876-6884
17. Mao C., Xu R., Bielawska A., Szulc Z.M., and Obeid L.M. Cloning and characterization of a Saccharomyces cerevisiae alkaline ceramidase with specificity for dihydroceramide. J. Biol. Chem. 275 (2000) 31369-31378
18. Mao C., Xu R., Szulc Z.M., Bielawska A., Galadari S.H., and Obeid L.M. Cloning and characterization of a novel human alkaline ceramidase. A mammalian enzyme that hydrolyzes phytoceramide. J. Biol. Chem. 276 (2001) 26577-26588
19. Mao C., Xu R., Szulc Z.M., Bielawski J., Becker K.P., Bielawska A., Galadari S.H., Hu W., and Obeid L.M. Cloning and characterization of a mouse endoplasmic reticulum alkaline ceramidase: an enzyme that preferentially regulates metabolism of very long chain ceramides. J. Biol. Chem. 278 (2003) 31184-31191
20. Sugita M., Dulaney J.T., and Moser H.W. Ceramidase deficiency in Farber's disease (lipogranulomatosis). Science 178 (1972) 1100-1102
21. Coroneos E., Martinez M., McKenna S., and Kester M. Differential regulation of sphingomyelinase and ceramidase activities by growth factors and cytokines. Implications for cellular proliferation and differentiation. J. Biol. Chem. 270 (1995) 23305-23309
22. Nikolova-Karakashian M., Morgan E.T., Alexander C., Liotta D.C., and Merrill A.H. Bimodal regulation of ceramidase by interleukin-1beta. Implications for the regulation of cytochrome p450 2C11. J. Biol. Chem. 272 (1997) 18718-18724
23. Franzen R., Pautz A., Brautigam L., Geisslinger G., Pfeilschifter J., and Huwiler A. Interleukin-1beta induces chronic activation and de novo synthesis of neutral ceramidase in renal mesangial cells. J. Biol. Chem. 276 (2001) 35382-35389
24. Franzen R., Fabbro D., Aschrafi A., Pfeilschifter J., and Huwiler A. Nitric oxide induces degradation of the neutral ceramidase in rat renal mesangial cells and is counterregulated by protein kinase C. J. Biol. Chem. 277 (2002) 46184-46190
25. Geoffroy K., Wiernsperger N., Lagarde M., and El Bawab S. Bimodal effect of advanced glycation end products on mesangial cell proliferation is mediated by neutral ceramidase regulation and endogenous sphingolipids. J. Biol. Chem. 279 (2004) 34343-34352
26. Rohrbough J., Rushton E., Palanker L., Woodruff E., Matthies H.J., Acharya U., Acharya J.K., and Broadie K. Ceramidase regulates synaptic vesicle exocytosis and trafficking. J. Neurosci. 24 (2004) 7789-7803
27. Acharya U., Patel S., Koundakjian E., Nagashima K., Han X., and Acharya J.K. Modulating sphingolipid biosynthetic pathway rescues photoreceptor degeneration. Science 299 (2003) 1740-1743
28. P.Y. Muller, H. Janovjak, A.R. Miserez, Z. Dobbie, Processing of gene expression data generated by quantitative real-time RT-PCR, Biotechniques 32 (2002) 1372-1374, 1376, 1378-1379.
29. Zeidan Y.H., Pettus B.J., Elojeimy S., Taha T., Obeid L.M., Kawamori T., Norris J.S., and Hannun Y.A. Acid ceramidase but not acid sphingomyelinase is required for tumor necrosis factor-{alpha}-induced PGE2 production. J. Biol. Chem. 281 (2006) 24695-24703
30. Wu B.X., Snook C.F., Tani M., Bullesbach E.E., and Hannun Y.A. Large-scale purification and characterization of recombinant Pseudomonas ceramidase: regulation by calcium. J. Lipid Res. 48 (2007) 600-608
31. Tani M., Okino N., Mitsutake S., and Ito M. Specific and sensitive assay for alkaline and neutral ceramidases involving C12-NBD-ceramide. J. Biochem. (Tokyo) 125 (1999) 746-749
32. Bielawski J., Szulc Z.M., Hannun Y.A., and Bielawska A. Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39 (2006) 82-91
33. Wang J., Zhao Y., Kauss M.A., Spindel S., and Lian H. Akt regulates vitamin D3-induced leukemia cell functional differentiation via Raf/MEK/ERK MAPK signaling. Eur. J. Cell Biol. 88 (2009) 103-115
34. Tani M., Iida H., and Ito M. O-glycosylation of mucin-like domain retains the neutral ceramidase on the plasma membranes as a type II integral membrane protein. J. Biol. Chem. 278 (2003) 10523-10530
35. Mitsutake S., Tani M., Okino N., Mori K., Ichinose S., Omori A., Iida H., Nakamura T., and Ito M. Purification, characterization, molecular cloning, and subcellular distribution of neutral ceramidase of rat kidney. J. Biol. Chem. 276 (2001) 26249-26259
36. Bose R., Verheij M., Haimovitz-Friedman A., Scotto K., Fuks Z., and Kolesnick R. Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals. Cell 82 (1995) 405-414
37. Zeidan Y.H., Jenkins R.W., and Hannun Y.A. Remodeling of cellular cytoskeleton by the acid sphingomyelinase/ceramide pathway. J. Cell Biol. 181 (2008) 335-350
38. Chalfant C.E., Rathman K., Pinkerman R.L., Wood R.E., Obeid L.M., Ogretmen B., and Hannun Y.A. De novo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1. J. Biol. Chem. 277 (2002) 12587-12595
39. Wolff R.A., Dobrowsky R.T., Bielawska A., Obeid L.M., and Hannun Y.A. Role of ceramide-activated protein phosphatase in ceramide-mediated signal transduction. J. Biol. Chem. 269 (1994) 19605-19609
40. El Bawab S., Usta J., Roddy P., Szulc Z.M., Bielawska A., and Hannun Y.A. Substrate specificity of rat brain ceramidase. J. Lipid Res. 43 (2002) 141-148
41. Taha T.A., El-Alwani M., Hannun Y.A., and Obeid L.M. Sphingosine kinase-1 is cleaved by cathepsin B in vitro: identification of the initial cleavage sites for the protease. FEBS Lett. 580 (2006) 6047-6054
42. Momoi T., Ben-Yoseph Y., and Nadler H.L. Substrate-specificities of acid and alkaline ceramidases in fibroblasts from patients with Farber disease and controls. Biochem. J. 205 (1982) 419-425
43. Zeidan Y.H., and Hannun Y.A. Activation of acid sphingomyelinase by protein kinase Cdelta-mediated phosphorylation. J. Biol. Chem. 282 (2007) 11549-11561
44. Alphonse G., Bionda C., Aloy M.T., Ardail D., Rousson R., and Rodriguez-Lafrasse C. Overcoming resistance to gamma-rays in squamous carcinoma cells by poly-drug elevation of ceramide levels. Oncogene 23 (2004) 2703-2715
45. Selzner M., Bielawska A., Morse M.A., Rudiger H.A., Sindram D., Hannun Y.A., and Clavien P.A. Induction of apoptotic cell death and prevention of tumor growth by ceramide analogues in metastatic human colon cancer. Cancer Res. 61 (2001) 1233-1240
46. Raisova M., Goltz G., Bektas M., Bielawska A., Riebeling C., Hossini A.M., Eberle J., Hannun Y.A., Orfanos C.E., and Geilen C.C. Bcl-2 overexpression prevents apoptosis induced by ceramidase inhibitors in malignant melanoma and HaCaT keratinocytes. FEBS Lett. 516 (2002) 47-52
47. Samsel L., Zaidel G., Drumgoole H.M., Jelovac D., Drachenberg C., Rhee J.G., Brodie A.M., Bielawska A., and Smyth M.J. The ceramide analog, B13, induces apoptosis in prostate cancer cell lines and inhibits tumor growth in prostate cancer xenografts. Prostate 58 (2004) 382-393
48. Swanton C., Marani M., Pardo O., Warne P.H., Kelly G., Sahai E., Elustondo F., Chang J., Temple J., Ahmed A.A., Brenton J.D., Downward J., and Nicke B. Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell 11 (2007) 498-512
49. Romiti E., Meacci E., Tani M., Nuti F., Farnararo M., Ito M., and Bruni P. Neutral/alkaline and acid ceramidase activities are actively released by murine endothelial cells. Biochem. Biophys. Res. Commun. 275 (2000) 746-751
50. Garlanda C., Parravicini C., Sironi M., De Rossi M., Wainstok de Calmanovici R., Carozzi F., Bussolino F., Colotta F., Mantovani A., and Vecchi A. Progressive growth in immunodeficient mice and host cell recruitment by mouse endothelial cells transformed by polyoma middle-sized T antigen: implications for the pathogenesis of opportunistic vascular tumors. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 7291-7295
51. Wang R., and Bautch V.L. The polyomavirus early region gene in transgenic mice causes vascular and bone tumors. J. Virol. 65 (1991) 5174-5183
52. Lin E.Y., Jones J.G., Li P., Zhu L., Whitney K.D., Muller W.J., and Pollard J.W. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 163 (2003) 2113-2126