Altering the sphingolipid acyl chain composition prevents LPS/GLN-mediated hepatic failure in mice by disrupting TNFR1 internalization

Cell Death and Disease

Volumn 4, Issue 11, 2013, Pages

  Ali, M ^a   Fritsch, J ^b   Zigdon, H ^a   Pewzner Jung, Y ^a   Schutze S ^b   Futerman, A H ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Apoptosis; Ceramide; Clathrin; Fulminant hepatic failure; Sphingolipids

Indexed keywords

CASPASE; CERAMIDE; FAS ANTIGEN; GALACTOSAMINE; LIPOPOLYSACCHARIDE; SPHINGOLIPID; TUMOR NECROSIS FACTOR RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; ENZYME ACTIVITY; FULMINANT HEPATIC FAILURE; INTERNALIZATION; LIPID COMPOSITION; LIVER CELL; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; GALACTOSAMINE; HEPATOCYTES; LIPOPOLYSACCHARIDES; LIVER; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SPHINGOLIPIDS; SPHINGOSINE N-ACYLTRANSFERASE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84889598683     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.451     Document Type: Article

References (51)

1. Cabal-Hierro L, Lazo PS. Signal transduction by tumor necrosis factor receptors. Cell Signal 2012; 24: 1297-1305
2. Shuh M, Bohorquez H, Loss GE, Cohen AJ. Tumor necrosis factor-A: Mife and death of hepatocytes during liver ischemia/reperfusion injury. Ochsner J 2013; 13: 119-130
3. Legler DF, Micheau O, Doucey M-A, Tschopp J, Bron C. Recruitment of TNF receptor 1 to lipid rafts is essential for TNFa-mediated NF-kB activation. Immunity 2003; 18: 655-664
4. Schneider-Brachert W, Tchikov V, Neumeyer J, Jakob M, Winoto-Morbach S, Held-Feindt J, et al. Compartmentalization of TNF receptor 1 signaling: Internalized TNF receptosomes as death signaling vesicles. Immunity 2004; 21: 415-428
5. Schütze S, Tchikov V, Schneider-Brachert W. Regulation of TNFR1 and CD95 signalling by receptor compartmentalization. Nat Rev Mol Cell Biol 2008; 9: 655-662
6. Schütze S, Schneider-Brachert W. Results and Problems in Cell Differentiation, Vol 49. Springer: Berlin Heidelberg, 2009. pp 63-85
7. Edelmann BAR, Bertsch U, Tchikov V, Winoto-Morbach S, Perrotta C, Jakob M, et al. Caspase-8 and caspase-7 sequentially mediate proteolytic activation of acid sphingomyelinase in TNF-R1 receptosomes. EMBO J 2010; 30: 379-394
8. Heinrich M, Neumeyer J, Jakob M, Hallas C, Tchikov V, Winoto-Morbach S, et al. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and-3 activation. Cell Death Differ 2004; 11: 550-563
9. Gulbins E, Grassmé H. Ceramide and cell death receptor clustering. Biochim Biophys Acta 2002; 1585: 139-145
10. Verheij M, Bose R, Lin XH, Yao B, JarvisWD, Grant S, et al. Requirement for ceramideinitiated SAPK/JNK signalling in stress-induced apoptosis. Nature 1996; 380: 75-79
11. Milhas D, Clarke CJ, Hannun YA. Sphingomyelin metabolism at the plasma membrane: Implications for bioactive sphingolipids. FEBS Lett 2010; 584: 1887-1894
12. Patti GJ, Yanes O, Shriver LP, Courade JP, Tautenhahn R, Manchester M, et al. Metabolomics implicates altered sphingolipids in chronic pain of neuropathic origin. Nat Chem Biol 2012; 8: 232-234
13. García-Ruiz C, Colell A, Marí M, Morales A, Calvo M, Enrich C, et al. Defective TNF-Alphamediated hepatocellular apoptosis and liver damage in acidic sphingomyelinase knockout mice. J Clin Invest 2003; 111: 197-208
14. Osawa Y, Uchinami H, Bielawski J, Schwabe RF, Hannun YA, Brenner DA. Roles for C16-ceramide and sphingosine 1-phosphate in regulating hepatocyte apoptosis in response to tumor necrosis factor-Alpha. J Biol Chem 2005; 280: 27879-27887
15. Pewzner-Jung Y, Park H, Laviad EL, Silva LC, Lahiri S, Stiban J, et al. A critical role for ceramide synthase 2 in liver homeostasis: I. alterations in lipid metabolic pathways. J Biol Chem 2010; 285: 10902-10910
16. Pewzner-Jung Y, Brenner O, Braun S, Laviad EL, Ben-Dor S, Feldmesser E, et al. A critical role for ceramide synthase 2 in liver homeostasis: II. insights into molecular changes leading to hepatopathy. J Biol Chem 2010; 285: 10911-10923
17. Laviad EL, Albee L, Pankova-Kholmyansky I, Epstein S, Park H, Merrill AH Jr, et al. Characterization of ceramide synthase 2: Tissue distribution, substrate specificity, and inhibition by sphingosine 1-phosphate. J Biol Chem 2008; 283: 5677-5684
18. Pewzner-Jung Y, Ben-Dor S, Futerman AH. When do Lasses (longevity assurance genes) become CerS (ceramide synthases)?: Insights into the regulation of ceramide synthesis. J Biol Chem 2006; 281: 25001-25005
19. Zigdon H, Kogot-Levin A, Park JW, Goldschmidt R, Kelly S, Merrill AH Jr, et al. Ablation of ceramide synthase 2 causes chronic oxidative stress due to disruption of the mitochondrial respiratory chain. J Biol Chem 2013; 288: 4947-4956
20. Park J-W, Park WJ, Kuperman Y, Boura-Halfon S, Pewzner-Jung Y, Futerman AH. Ablation of very long acyl chain sphingolipids causes hepatic insulin resistance in mice due to altered detergent-resistant membranes. Hepatology 2013; 57: 525-532
21. Silva LC, Ben David O, Pewzner-Jung Y, Laviad EL, Stiban J, Bandyopadhyay S, et al. Ablation of ceramide synthase 2 strongly affects biophysical properties of membranes. J Lipid Res 2012; 53: 430-436
22. Lehmann V, Freudenberg MA, Galanos C. Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and D-galactosamine- Treated mice. J Exp Med 1987; 165: 657-663
23. Leist M, Gantner F, Bohlinger I, Germann PG, Tiegs G, Wendel A. Murine hepatocyte apoptosis induced in vitro and in vivo by TNF-Alpha requires transcriptional arrest. J Immunol 1994; 153: 1778-1788
24. Liao W, Xiao Q, Tchikov V, Fujita K, Yang W, Wincovitch S, et al. CARP-2 is an endosomeassociated ubiquitin ligase for RIP and regulates TNF-induced NF-kappaB activation. Curr Biol 2008; 18: 641-649
25. Schneider-Brachert W, Tchikov V, Merkel O, Jakob M, Hallas C, Kruse ML, et al. Inhibition of TNF receptor 1 internalization by adenovirus 14.7K as a novel immune escape mechanism. J Clin Invest 2006; 116: 2901-2913
26. Mosselmans R, Hepburn A, Dumont JE, Fiers W, Galand P. Endocytic pathway of recombinant murine tumor necrosis factor in L-929 cells. J Immunol 1988; 141: 3096-3100
27. Cheng Z-J, Singh RD, Sharma DK, Holicky EL, Hanada K, Marks DL, et al. Distinct mechanisms of clathrin-independent endocytosis have unique sphingolipid requirements. Mol Biol Cell 2006; 17: 3197-3210
28. Grassmé H, Riethmüller J, Gulbins E. Biological aspects of ceramide-enriched membrane domains. Prog Lipid Res 2007; 46: 161-170
29. Gulbins E, Kolesnick R. Raft ceramide in molecular medicine. Oncogene 2003; 22: 7070-7077
30. Varela ARP, Gonçalves da Silva AM, Fedorov A, Futerman AH, Prieto M, Silva LC. Effect of glucosylceramide on the biophysical properties of fluid membranes. Biochim Biophys Acta 2013; 1828: 1122-1130
31. Holopainen JM, Angelova MI, Kinnunen PKJ. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys J 2000; 78: 830-838
32. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008; 319: 1244-1247
33. Rollason R, Korolchuk V, Hamilton C, Schu P, Banting G. Clathrin-mediated endocytosis of a lipid-raft-Associated protein is mediated through a dual tyrosine motif. J Cell Sci 2007; 120: 3850-3858
34. Masuyama N, Kuronita T, Tanaka R, Muto T, Hirota Y, Takigawa A, et al. HM1.24 is internalized from lipid rafts by clathrin-mediated endocytosis through interaction with alpha-Adaptin. J Biol Chem 2009; 284: 15927-15941
35. Smith EL, Schuchman EH. Acid sphingomyelinase overexpression enhances the antineoplastic effects of irradiation in vitro and in vivo. Mol Ther 2008; 16: 1565-1571
36. Smith EL, Schuchman EH. The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. FASEB J 2008; 22: 3419-3431
37. Zeidan YH, Hannun YA. The acid sphingomyelinase/ceramide pathway: Biomedical significance and mechanisms of regulation. Curr Mol Med 2010; 10: 454-466
38. Carpinteiro A, Dumitru C, Schenck M, Gulbins E. Ceramide-induced cell death in malignant cells. Cancer Lett 2008; 264: 1-10
39. Neumeyer J, Hallas C, Merkel O, Winoto-Morbach S, Jakob M, Thon L, et al. TNF-receptor I defective in internalization allows for cell death through activation of neutral sphingomyelinase. Exp Cell Res 2006; 312: 2142-2153
40. Daido S, Kanzawa T, Yamamoto A, Takeuchi H, Kondo Y, Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res 2004; 64: 4286-4293
41. Thon L, Möhlig H, Mathieu S, Lange A, Bulanova E, Winoto-Morbach S, et al. Ceramide mediates caspase-independent programmed cell death. FASEB J 2005; 19: 1945-1956
42. Philipp S, Puchert M, Adam-Klages S, Tchikov V, Winoto-Morbach S, Mathieu S, et al. The polycomb group protein EED couples TNF receptor 1 to neutral sphingomyelinase. Proc Natl Acad Sci USA 2010; 107: 1112-1117
43. Ullio C, Casas J, Brunk UT, Sala G, Fabriàs G, Ghidoni R, et al. Sphingosine mediates TNFa-induced lysosomal membrane permeabilization and ensuing programmed cell death in hepatoma cells. J Lipid Res 2012; 53: 1134-1143
44. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S, et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kB signalling. Nature 2004; 430: 694-699
45. Boone DL, Turer EE, Lee EG, Ahmad RC, Wheeler MT, Tsui C, et al. The ubiquitinmodifying enzyme A20 is required for termination of Toll-like receptor responses. Nat Immunol 2004; 5: 1052-1060
46. Levy M, Futerman AH. Mammalian ceramide synthases. IUBMB life 2010; 62: 347-356
47. Burow ME, Weldon CB, Tang Y, Navar GL, Krajewski S, Reed JC, et al. Differences in susceptibility to tumor necrosis factor alpha-induced apoptosis among MCF-7 breast cancer cell variants. Cancer Res 1998; 58: 4940-4946
48. Donato NJ, Klostergaard J. Distinct stress and cell destruction pathways are engaged by TNF and ceramide during apoptosis of MCF-7 cells. Exp Cell Res 2004; 294: 523-533
49. Hannun YA, Obeid LM. Many ceramides. J Biol Chem 2011; 286: 27855-27862
50. Moshitzky S, Asher C, Garty H. Intracellular trafficking of FXYD1 (phospholemman) and FXYD7 proteins in Xenopus oocytes and mammalian cells. J Biol Chem 2012; 287: 21130-21141
51. Halasiddappa LM, Koefeler H, Futerman AH, Hermetter A. Oxidized phospholipids induce ceramide accumulation in RAW 264.7 macrophages: Role of ceramide synthases. PLoS ONE 2013; 8: E70002