Exploring the link between ceramide and ionizing radiation

Glycoconjugate Journal

Volumn 31, Issue 6, 2014, Pages 449-459

  Aureli, Massimo ^a   Murdica, Valentina ^a   Loberto, Nicoletta ^a   Samarani, Maura ^a   Prinetti, Alessandro ^a   Bassi, Rosaria ^a   Sonnino, Sandro ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Apoptosis; Ceramide; Glycohydrolases; Glycosphingolipids; Sphingomyelin; Sphingomyelinase

Indexed keywords

CERAMIDE; DNA; GLYCOSIDASE; GLYCOSPHINGOLIPID; SPHINGOLIPID; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE;

APOPTOSIS; ARTICLE; CANCER CELL; CATABOLISM; CELL CYCLE ARREST; CELL DEATH; CELL DIFFERENTIATION; CELL SURFACE; DNA DAMAGE; HUMAN; INTRACELLULAR MEMBRANE; IONIZING RADIATION; IRRADIATION; MITOCHONDRION; MOLECULAR MECHANICS; PRIORITY JOURNAL; RADIATION RESPONSE; RADIOTHERAPY; SENSOR; SPHINGOLIPID METABOLISM; CHEMISTRY; METABOLISM;

CERAMIDES; GLYCOSIDE HYDROLASES; RADIATION, IONIZING; SPHINGOMYELINS;

EID: 84926670928     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-014-9541-y     Document Type: Article

References (75)

1. Zelefsky,M.J., Fuks, Z.V.I., Hunt,M., Lee, H.J., Lombardi, D., Ling, C.C., Reuter, V.E., Venkatraman, E.S., Leibel, S.A.: High dose radiation delivered by intensity modulated conformal radiotherapy improves the outcome of localized prostate cancer. J Urol 166, 876-881 (2001)
2. Haimovitz-Friedman, A., Kan, C.C., Ehleiter, D., Persaud, R.S., McLoughlin, M., Fuks, Z., Kolesnick, R.N.: Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J Exp Med 180, 525-535 (1994)
3. Kolesnick, R., Fuks, Z.: Radiation and ceramide-induced apoptosis. Oncogene 22, 5897-5906 (2003)
4. Zhang, Y., Yao, B., Delikat, S., Bayoumy, S., Lin, X.H., Basu, S., McGinley, M., Chan-Hui, P.Y., Lichenstein, H., Kolesnick, R.: Kinase suppressor of Ras is ceramide-activated protein kinase. Cell 89, 63-72 (1997)
5. Chalfant, C.E., Rathman, K., Pinkerman, R.L., Wood, R.E., Obeid, L.M., Ogretmen, B., 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, 12587-12595 (2002)
6. Kashiwagi, K., Shirai, Y., Kuriyama, M., Sakai, N., Saito, N.: Importance of C1B domain for lipid messenger-induced targeting of protein kinase C. J Biol Chem 277, 18037-18045 (2002)
7. Huwiler, A., Brunner, J., Hummel, R., Vervoordeldonk, M., Stabel, S., van den Bosch, H., Pfeilschifter, J.: Ceramide-binding and activation defines protein kinase c-Raf as a ceramide-activated protein kinase. Proc Natl Acad Sci U S A 93, 6959-6963 (1996)
8. Gulbins, E., Bissonnette, R., Mahboubi, A., Martin, S., Nishioka,W., Brunner, T., Baier, G., Baier-Bitterlich, G., Byrd, C., Lang, F., et al.: FAS-induced apoptosis is mediated via a ceramide-initiated RAS signaling pathway. Immunity 2, 341-351 (1995)
9. Gulbins, E., Grassme, H.: Ceramide and cell death receptor clustering. Biochim Biophys Acta 1585, 139-145 (2002)
10. Huwiler, A., Johansen, B., Skarstad, A., Pfeilschifter, J.: Ceramide binds to the CaLB domain of cytosolic phospholipase A2 and facilitates its membrane docking and arachidonic acid release. FASEB J 15, 7-9 (2001)
11. Deiss, L.P., Galinka, H., Berissi, H., Cohen, O., Kimchi, A.: Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J 15, 3861-3870 (1996)
12. Gulbins, E., Szabo, I., Baltzer, K., Lang, F.: Ceramide-induced inhibition of T lymphocyte voltage-gated potassium channel is mediated by tyrosine kinases. Proc Natl Acad Sci U S A 94, 7661-7666 (1997)
13. Lepple-Wienhues, A., Belka, C., Laun, T., Jekle, A., Walter, B., Wieland, U., Welz, M., Heil, L., Kun, J., Busch, G., Weller, M., Bamberg, M., Gulbins, E., Lang, F.: Stimulation of CD95 (Fas) blocks T lymphocyte calcium channels through sphingomyelinase and sphingolipids. Proc Natl Acad Sci U S A 96, 13795-13800 (1999)
14. Westwick, J.K., Bielawska, A.E., Dbaibo, G., Hannun, Y.A., Brenner, D.A.: Ceramide activates the stress-activated protein kinases. J Biol Chem 270, 22689-22692 (1995)
15. Basu, S., Bayoumy, S., Zhang, Y., Lozano, J., Kolesnick, R.: BAD enables ceramide to signal apoptosis via Ras and Raf-1. J Biol Chem 273, 30419-30426 (1998)
16. Cremesti, A.E., Goni, F.M., Kolesnick, R.: Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome? FEBS Lett 531, 47-53 (2002)
17. Cremesti, A., Paris, F., Grassme, H., Holler, N., Tschopp, J., Fuks, Z., Gulbins, E., Kolesnick, R.: Ceramide enables Fas to cap and kill. J Biol Chem 276, 23954-23961 (2001)
18. Kolesnick, R.N., Goni, F.M., Alonso, A.: Compartmentalization of ceramide signaling: physical foundations and biological effects. J Cell Physiol 184, 285-300 (2000)
19. Hueber, A.O., Bernard,A.M.,Herincs, Z., Couzinet, A., He, H.T.: An essential role for membrane rafts in the initiation of Fas/CD95- triggered cell death in mouse thymocytes. EMBO Rep 3, 190-196 (2002)
20. Zundel, W., Giaccia, A.: Inhibition of the anti-apoptotic PI(3)K/Akt/ Bad pathway by stress. Genes Dev 12, 1941-1946 (1998)
21. Rehemtulla, A., Hamilton, C.A., Chinnaiyan, A.M., Dixit, V.M.: Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/APO-1). J Biol Chem 272, 25783-25786 (1997)
22. Aureli, M., Bassi, R., Prinetti, A., Chiricozzi, E., Pappalardi, B., Chigorno, V., Di Muzio, N., Loberto, N., Sonnino, S.: Ionizing radiations increase the activity of the cell surface glycohydrolases and the plasma membrane ceramide content. Glycoconj J 29, 585 (2012)
23. Spiegel, S., Foster, D., Kolesnick, R.: Signal transduction through lipid second messengers. Curr Opin Cell Biol 8, 159-167 (1996)
24. Hannun, Y.A., Luberto, C., Argraves, K.M.: Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry 40, 4893-4903 (2001)
25. Merrill Jr., A.H., Schmelz, E.M., Dillehay, D.L., Spiegel, S., Shayman, J.A., Schroeder, J.J., Riley, R.T., Voss, K.A., Wang, E.: Sphingolipids-the enigmatic lipid class: biochemistry, physiology, and pathophysiology. Toxicol Appl Pharmacol 142, 208-225 (1997)
26. Mandon, E.C., Ehses, I., Rother, J., van Echten, G., Sandhoff, K.: Subcellular localization and membrane topology of serine palmitoyltransferase, 3-dehydrosphinganine reductase, and sphinganine N-acyltransferase in mouse liver. J Biol Chem 267, 11144-11148 (1992)
27. White-Gilbertson, S., Mullen, T., Senkal, C., Lu, P., Ogretmen, B., Obeid, L., Voelkel-Johnson, C.: Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells. Oncogene 28, 1132-1141 (2009)
28. Liao, W.C., Haimovitz-Friedman, A., Persaud, R.S., McLoughlin, M., Ehleiter, D., Zhang, N., Gatei, M., Lavin, M., Kolesnick, R., Fuks, Z.: Ataxia telangiectasia-mutated gene product inhibits DNA damage-induced apoptosis via ceramide synthase. J Biol Chem 274, 17908-17917 (1999)
29. Mesicek, J., Lee, H., Feldman, T., Jiang, X., Skobeleva, A., Berdyshev, E.V., Haimovitz-Friedman, A., Fuks, Z., Kolesnick, R.: Ceramide synthases 2, 5, and 6 confer distinct roles in radiationinduced apoptosis in HeLa cells. Cell Signal 22, 1300-1307 (2010)
30. Vit, J.P., Rosselli, F.: Role of the ceramide-signaling pathways in ionizing radiation-induced apoptosis. Oncogene 22, 8645-8652 (2003)
31. Deng, X., Yin, X., Allan, R., Lu, D.D., Maurer, C.W., Haimovitz- Friedman, A., Fuks, Z., Shaham, S., Kolesnick, R.: Ceramide biogenesis is required for radiation-induced apoptosis in the germ line of C. elegans. Science 322, 110-115 (2008)
32. Santana, P., Pena, L.A., Haimovitz-Friedman, A., Martin, S., Green, D., McLoughlin, M., Cordon-Cardo, C., Schuchman, E.H., Fuks, Z., Kolesnick, R.: Acid sphingomyelinase-deficient human lymphoblasts and mice are defective in radiation-induced apoptosis. Cell 86, 189-199 (1996)
33. Alphonse, G., Aloy, M.T., Broquet, P., Gerard, J.P., Louisot, P., Rousson, R., Rodriguez-Lafrasse, C.: Ceramide induces activation of the mitochondrial/caspases pathway in Jurkat and SCC61 cells sensitive to gamma-radiation but activation of this sequence is defective in radioresistant SQ20B cells. Int J Radiat Biol 78, 821-835 (2002)
34. Mahdy, A.E., Cheng, J.C., Li, J., Elojeimy, S., Meacham, W.D., Turner, L.S., Bai, A., Gault, C.R., McPherson, A.S., Garcia, N., Beckham, T.H., Saad, A., Bielawska, A., Bielawski, J., Hannun, Y.A., Keane, T.E., Taha, M.I., Hammouda, H.M., Norris, J.S., Liu, X.: Acid ceramidase upregulation in prostate cancer cells confers resistance to radiation: AC inhibition, a potential radiosensitizer.Mol Ther 17, 430-438 (2009)
35. Beckham, T.H., Lu, P., Cheng, J.C., Zhao, D., Turner, L.S., Zhang, X.,Hoffman, S., Armeson, K.E., Liu,A.,Marrison, T.,Hannun,Y.A., Liu, X.: Acid ceramidase-mediated production of sphingosine 1- phosphate promotes prostate cancer invasion through upregulation of cathepsin B. Int J Cancer 131, 2034-2043 (2012)
36. Cheng, J.C., Bai, A., Beckham, T.H., Marrison, S.T., Yount, C.L., Young, K., Lu, P., Bartlett, A.M., Wu, B.X., Keane, B.J., Armeson, K.E.,Marshall, D.T.,Keane, T.E., Smith, M.T., Jones, E.E., Drake Jr., R.R., Bielawska, A., Norris, J.S., Liu, X.: Radiation-induced acid ceramidase confers prostate cancer resistance and tumor relapse. J Clin Invest 123, 4344-4358 (2013)
37. Sinha, U.K., Schorn, V.J., Hochstim, C., Chinn, S.B., Zhu, S., Masood, R.: Increased radiation sensitivity of head and neck squamous cell carcinoma with sphingosine kinase 1 inhibition. Head Neck 33, 178-188 (2011)
38. Goni, F.M., Alonso, A.: Sphingomyelinases: enzymology and membrane activity. FEBS Lett 531, 38-46 (2002)
39. Schissel,S.L., Jiang, X.,Tweedie-Hardman, J., Jeong, T.,Camejo, E.H., Najib, J., Rapp, J.H., Williams, K.J., Tabas, I.: Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH. Implications for atherosclerotic lesion development. J Biol Chem 273, 2738-2746 (1998)
40. Schissel, S.L., Keesler, G.A., Schuchman, E.H., Williams, K.J., Tabas, I.: The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J Biol Chem 273, 18250-18259 (1998)
41. Milhas, D., Clarke, C.J., Hannun, Y.A.: Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett 584, 1887-1894 (2010)
42. Horres, C.R., Hannun, Y.A.: The roles of neutral sphingomyelinases in neurological pathologies. Neurochem Res 37, 1137-1149 (2012)
43. Nilsson, A., Duan, R.D.: Alkaline sphingomyelinases and ceramidases of the gastrointestinal tract. Chem Phys Lipids 102, 97-105 (1999)
44. Marathe, S., Schissel, S.L., Yellin, M.J., Beatini, N., Mintzer, R., Williams, K.J., Tabas, I.: Human vascular endothelial cells are a rich and regulatable source of secretory sphingomyelinase. Implications for early atherogenesis and ceramide-mediated cell signaling. J Biol Chem 273, 4081-4088 (1998)
45. Pena, L.A., Fuks, Z., Kolesnick, R.N.: Radiation-induced apoptosis of endothelial cells in the murine central nervous system: protection by fibroblast growth factor and sphingomyelinase deficiency. Cancer Res 60, 321-327 (2000)
46. Paris, F., Fuks, Z., Kang, A., Capodieci, P., Juan, G., Ehleiter, D., Haimovitz-Friedman, A., Cordon-Cardo, C., Kolesnick, R.: Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 293, 293-297 (2001)
47. Morita, Y., Perez, G.I., Paris, F., Miranda, S.R., Ehleiter, D., Haimovitz-Friedman, A., Fuks, Z., Xie, Z., Reed, J.C., Schuchman, E.H., Kolesnick, R.N., Tilly, J.L.: Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1- phosphate therapy. Nat Med 6, 1109-1114 (2000)
48. Kolesnick, R.: The therapeutic potential of modulating the ceramide/ sphingomyelin pathway. J Clin Invest 110, 3-8 (2002)
49. Rodriguez-Lafrasse, C., Alphonse, G., Aloy, M.T., Ardail, D., Gerard, J.P., Louisot, P., Rousson, R.: Increasing endogenous ceramide using inhibitors of sphingolipid metabolism maximizes ionizing radiation-induced mitochondrial injury and apoptotic cell killing. Int J Cancer 101, 589-598 (2002)
50. Bruno, A.P., Laurent, G., Averbeck, D., Demur, C., Bonnet, J., Bettaieb, A., Levade, T., Jaffrezou, J.P.: Lack of ceramide generation in TF-1 human myeloid leukemic cells resistant to ionizing radiation. Cell Death Differ 5, 172-182 (1998)
51. Chmura, S.J., Nodzenski, E., Beckett, M.A., Kufe, D.W., Quintans, J., Weichselbaum, R.R.: Loss of ceramide production confers resistance to radiation-induced apoptosis. Cancer Res 57, 1270-1275 (1997)
52. Aureli, M., Masilamani, A.P., Illuzzi, G., Loberto, N., Scandroglio, F., Prinetti, A., Chigorno, V., Sonnino, S.: Activity of plasma membrane beta-galactosidase and beta-glucosidase. FEBS Lett 583, 2469-2473 (2009)
53. Mencarelli, S., Cavalieri, C., Magini, A., Tancini, B., Basso, L., Lemansky, P., Hasilik, A., Li, Y.T., Chigorno, V., Orlacchio, A., Emiliani, C., Sonnino, S.: Identification of plasma membrane associated mature beta-hexosaminidase A, active towards GM2 ganglioside, in human fibroblasts. FEBS Lett 579, 5501-5506 (2005)
54. Aureli, M., Loberto, N., Chigorno, V., Prinetti, A., Sonnino, S.: Remodeling of sphingolipids by plasma membrane associated enzymes. Neurochem Res 36, 1636-1644 (2011)
55. Kolter, T., Sandhoff, K.: Sphingolipid metabolism diseases. Biochim Biophys Acta 1758, 2057-2079 (2006)
56. Reddy, A., Caler, E.V., Andrews, N.W.: Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 106, 157-169 (2001)
57. Fanzani, A., Colombo, F., Giuliani, R., Preti, A., Marchesini, S.: Cytosolic sialidase Neu2 upregulation during PC12 cells differentiation. FEBS Lett 566, 178-182 (2004)
58. Kopitz, J., von Reitzenstein, C., Muhl, C., Cantz, M.: Role of plasma membrane ganglioside sialidase of human neuroblastoma cells in growth control and differentiation. Biochem Biophys Res Commun 199, 1188-1193 (1994)
59. Monti, E., Preti, A., Venerando, B., Borsani, G.: Recent development in mammalian sialidase molecular biology. Neurochem Res 27, 649-663 (2002)
60. Miyagi, T., Wada, T., Yamaguchi, K.: Roles of plasma membraneassociated sialidase NEU3 in human cancers. Biochim Biophys Acta 1780, 532-537 (2008)
61. Miyagi, T.,Wada, T., Yamaguchi, K., Hata, K., Shiozaki, K.: Plasma membrane-associated sialidase as a crucial regulator of transmembrane signalling. J Biochem 144, 279-285 (2008)
62. Ueno, S., Saito, S., Wada, T., Yamaguchi, K., Satoh, M., Arai, Y., Miyagi, T.: Plasma membrane-associated sialidase is up-regulated in renal cell carcinoma and promotes interleukin-6-induced apoptosis suppression and cell motility. J Biol Chem 281, 7756-7764 (2006)
63. Kakugawa, Y., Wada, T., Yamaguchi, K., Yamanami, H., Ouchi, K., Sato, I., Miyagi, T.: Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon cancer and its involvement in apoptosis suppression. Proc Natl Acad Sci U S A 99, 10718-10723 (2002)
64. Venerando, B., Fiorilli, A., Croci, G., Tringali, C., Goi, G., Mazzanti, L., Curatola, G., Segalini, G., Massaccesi, L., Lombardo, A., Tettamanti, G.: Acidic and neutral sialidase in the erythrocyte membrane of type 2 diabetic patients. Blood 99, 1064-1070 (2002)
65. Tringali, C., Anastasia, L., Papini, N., Bianchi, A., Ronzoni, L., Cappellini, M.D., Monti, E., Tettamanti, G., Venerando, B.: Modification of sialidase levels and sialoglycoconjugate pattern during erythroid and erytroleukemic cell differentiation. Glycoconj J 24, 67-79 (2007)
66. Valaperta, R., Chigorno, V., Basso, L., Prinetti, A., Bresciani, R., Preti, A., Miyagi, T., Sonnino, S.: Plasma membrane production of ceramide from ganglioside GM3 in human fibroblasts. FASEB J 20, 1227-1229 (2006)
67. Chigorno, V., Cardace, G., Pitto, M., Sonnino, S., Ghidoni, R., Tettamanti, G.: A radiometric assay for ganglioside sialidase applied to the determination of the enzyme subcellular location in cultured human fibroblasts. Anal Biochem 153, 283-294 (1986)
68. Huang, Q., Shur, B.D., Begovac, P.C.: Overexpressing cell surface beta 1.4-galactosyltransferase in PC12 cells increases neurite outgrowth on laminin. J Cell Sci 108(Pt 2), 839-847 (1995)
69. Neufeld, E.B., Cooney, A.M., Pitha, J., Dawidowicz, E.A., Dwyer, N.K., Pentchev, P.G., Blanchette-Mackie, E.J.: Intracellular trafficking of cholesterol monitored with a cyclodextrin. J Biol Chem 271, 21604-21613 (1996)
70. van Weely, S., Brandsma, M., Strijland, A., Tager, J.M., Aerts, J.M.: Demonstration of the existence of a second, non-lysosomal glucocerebrosidase that is not deficient in Gaucher disease. Biochim Biophys Acta 1181, 55-62 (1993)
71. Daniels, L.B., Coyle, P.J., Chiao, Y.B., Glew, R.H., Labow, R.S.: Purification and characterization of a cytosolic broad specificity betaglucosidase from human liver. J Biol Chem 256, 13004-13013 (1981)
72. Yap, T.L., Velayati, A., Sidransky, E., Lee, J.C.: Membrane-bound alpha-synuclein interacts with glucocerebrosidase and inhibits enzyme activity. Mol Genet Metab 108, 56-64 (2013)
73. Korschen, H.G., Yildiz, Y., Raju, D.N., Schonauer, S., Bonigk, W., Jansen, V., Kremmer, E., Kaupp, U.B., Wachten, D.: The nonlysosomal beta-glucosidase GBA2 is a non-integral membrane-associated protein at the endoplasmic reticulum (ER) and Golgi. J Biol Chem 288, 3381-3393 (2012)
74. Yu, R.K., Macala, L.J., Taki, T., Weinfield, H.M., Yu, F.S.: Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem 50, 1825-1829 (1988)
75. Miyagi, T., Tsuiki, S.: Evidence for sialidase hydrolyzing gangliosides GM2 and GM1 in rat liver plasma membrane. FEBS Lett 206, 223-228 (1986)