Determining the Turnover of Glycosphingolipid Species by Stable-Isotope Tracer Lipidomics

Journal of Molecular Biology

Volumn 428, Issue 24, 2016, Pages 4856-4866

  Skotland, Tore ^a,b   Ekroos, Kim ^c   Kavaliauskiene, Simona ^a,b,d   Bergan, Jonas ^a,b   Kauhanen, Dimple ^c   Lintonen, Tuulia ^c   Sandvig, Kirsten ^a,b,d  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c Zora Biosciences Oy   (Finland)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

FLUX lipidomics; lipid turnover; mass isotopes; mass spectrometry; sphingolipids

Indexed keywords

CERAMIDE; GLOBOTRIAOSYLCERAMIDE; GLUCOSE C 13; GLUCOSYLCERAMIDE; GLYCOSPHINGOLIPID; HEXOSE; LACTOSYLCERAMIDE; SERINE C 13; TRACER; UNCLASSIFIED DRUG; CARBON; GLUCOSE; ISOTOPE; SERINE;

ARTICLE; CELL METABOLISM; HEP 2 CELL LINE; HUMAN; HUMAN CELL; LIPID METABOLISM; LIPIDOMICS; LIPOGENESIS; PRIORITY JOURNAL; TURNOVER TIME; CELL LINE; EPITHELIUM CELL; ISOTOPE LABELING; METABOLISM; PROCEDURES;

CARBON ISOTOPES; CELL LINE; EPITHELIAL CELLS; GLUCOSE; GLYCOSPHINGOLIPIDS; HUMANS; ISOTOPE LABELING; ISOTOPES; SERINE;

EID: 84996843171     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.06.013     Document Type: Article

References (37)

1. [1] van Meer, G., Voelker, D.R., Feigenson, G.W., Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9 (2008), 112–124.
2. [2] Shevchenko, A., Simons, K., Lipidomics: coming to grips with lipid diversity. Nat. Rev. Mol. Cell Biol. 11 (2010), 593–598.
3. [3] Jung, H.R., Sylvanne, T., Koistinen, K.M., Tarasov, K., Kauhanen, D., Ekroos, K., High throughput quantitative molecular lipidomics. Biochim. Biophys. Acta. 1811 (2011), 925–934.
4. [4] Hoetzl, S., Sprong, H., van Meer, G., The way we view cellular (glyco)sphingolipids. J. Neurochem. 103:Suppl. 1 (2007), 3–13.
5. [5] Ekroos, K., Janis, M., Tarasov, K., Hurme, R., Laaksonen, R., Lipidomics: a tool for studies of atherosclerosis. Curr. Atheroscler. Rep. 12 (2010), 273–281.
6. [6] D'Auria, L., Van der Smissen, P., Bruyneel, F., Courtoy, P.J., Tyteca, D., Segregation of fluorescent membrane lipids into distinct micrometric domains: evidence for phase compartmentation of natural lipids?. PLoS. One., 6, 2011, e17021.
7. [7] Sezgin, E., Levental, I., Grzybek, M., Schwarzmann, G., Mueller, V., Honigmann, A., et al. Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim. Biophys. Acta. 1818 (2012), 1777–1784.
8. [8] Smith, E.R., Merrill, A.H. Jr., Differential roles of de novo sphingolipid biosynthesis and turnover in the “burst” of free sphingosine and sphinganine, and their 1-phosphates and N-acyl-derivatives, that occurs upon changing the medium of cells in culture. J. Biol. Chem. 270 (1995), 18,749–18,758.
9. [9] Raa, H., Grimmer, S., Schwudke, D., Bergan, J., Walchli, S., Skotland, T., et al. Glycosphingolipid requirements for endosome-to-Golgi transport of Shiga toxin. Traffic. 10 (2009), 868–882.
10. [10] Hannun, Y.A., Obeid, L.M., Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9 (2008), 139–150.
11. [11] Wymann, M.P., Schneiter, R., Lipid signalling in disease. Nat. Rev. Mol. Cell Biol. 9 (2008), 162–176.
12. [12] Futerman, A.H., Schuldiner, M., Lipids: the plasma membrane code. Nat. Chem. Biol. 6 (2010), 487–488.
13. [13] Ejsing, C.S., Sampaio, J.L., Surendranath, V., Duchoslav, E., Ekroos, K., Klemm, R.W., et al. Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 2136–2141.
14. [14] Bergan, J., Skotland, T., Sylvanne, T., Simolin, H., Ekroos, K., Sandvig, K., The ether lipid precursor hexadecylglycerol causes major changes in the lipidome of HEp-2 cells. PLoS. One., 8, 2013, e75904.
15. [15] Postle, A.D., Lipidomics. Curr. Opin. Clin. Nutr. Metab Care 15 (2012), 127–133.
16. [16] Ecker, J., Liebisch, G., Application of stable isotopes to investigate the metabolism of fatty acids, glycerophospholipid and sphingolipid species. Prog. Lipid Res. 54 (2014), 14–31.
17. [17] Wennekes, T., van den Berg, R.J., Boot, R.G., van der Marel, G.A., Overkleeft, H.S., Aerts, J.M., Glycosphingolipids—nature, function, and pharmacological modulation. Angew. Chem. Int. Ed. Eng. 48 (2009), 8848–8869.
18. [18] Blom, T., Somerharju, P., Ikonen, E., Synthesis and biosynthetic trafficking of membrane lipids. Cold Spring Harb. Perspect. Biol., 3, 2011, a0047.
19. [19] Ben-David, O., Futerman, A.H., The role of the ceramide acyl chain length in neurodegeneration: involvement of ceramide synthases. Neruomol. Med. 12 (2010), 341–350.
20. [20] Tidhar, R., Futerman, A.H., The complexity of sphingolipid biosynthesis in the endoplasmic reticulum. Biochim. Biophys. Acta. 1833 (2013), 2511–2518.
21. [21] Kavaliauskiene, S., Nymark, C.M., Bergan, J., Simm, R., Sylvanne, T., Simolin, H., et al. Cell density-induced changes in lipid composition and intracellular trafficking. Cell. Mol. Life Sci. 71 (2014), 1097–1116.
22. [22] D'Angelo, G., Uemura, T., Chuang, C.C., Polishchuk, E., Santoro, M., Ohvo-Rekila, H., et al. Vesicular and non-vesicular transport feed distinct glycosylation pathways in the Golgi. Nature. 501 (2013), 116–120.
23. [23] Bergan, J., Skotland, T., Lingelem, A.B., Simm, R., Spilsberg, B., Lindback, T., et al. The ether lipid precursor hexadecylglycerol protects against Shiga toxins. Cell. Mol. Life Sci. 71 (2014), 4285–4300.
24. [24] Chen, C.S., Bach, G., Pagano, R.E., Abnormal transport along the lysosomal pathway in mucolipidosis, type IV disease. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 6373–6378.
25. [25] Gillard, B.K., Clement, R.G., Marcus, D.M., Variations among cell lines in the synthesis of sphingolipids in de novo and recycling pathways. Glycobiology. 8 (1998), 885–890.
26. [26] Tettamanti, G., Ganglioside/glycosphingolipid turnover: new concepts. Glycoconj. J. 20 (2004), 301–317.
27. [27] Schulze, H., Sandhoff, K., Lysosomal lipid storage diseases. Cold Spring Harb. Perspect. Biol., 3, 2011, a00480.
28. [28] Kitatani, K., Idkowiak-Baldys, J., Hannun, Y.A., The sphingolipid salvage pathway in ceramide metabolism and signaling. Cell. Signal. 20 (2008), 1010–1018.
29. [29] Thomsen, P., Roepstorff, K., Stahlhut, M., van, D.B., Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell 13 (2002), 238–250.
30. [30] Hayer, A., Stoeber, M., Ritz, D., Engel, S., Meyer, H.H., Helenius, A., Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J. Cell Biol. 191 (2010), 615–629.
31. [31] Goldstein, J.L., Brown, M.S., Anderson, R.G., Russell, D.W., Schneider, W.J., Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1 (1985), 1–39.
32. [32] Stoscheck, C.M., Carpenter, G., Down regulation of epidermal growth factor receptors: direct demonstration of receptor degradation in human fibroblasts. J. Cell Biol. 98 (1984), 1048–1053.
33. [33] Zech, T., Ejsing, C.S., Gaus, K., de, W.B., Shevchenko, A., Simons, K., Harder, T., Accumulation of raft lipids in T-cell plasma membrane domains engaged in TCR signalling. EMBO J. 28 (2009), 466–476.
34. [34] Klemm, R.W., Ejsing, C.S., Surma, M.A., Kaiser, H.J., Gerl, M.J., Sampaio, J.L., et al. Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. J. Cell Biol. 185 (2009), 601–612.
35. [35] Ekroos, K., Chernushevich, I.V., Simons, K., Shevchenko, A., Quantitative profiling of phospholipids by multiple precursor ion scanning on a hybrid quadrupole time-of-flight mass spectrometer. Anal. Chem. 74 (2002), 941–949.
36. [36] Merrill, A.H. Jr., Sullards, M.C., Allegood, J.C., Kelly, S., Wang, E., Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry. Methods. 36 (2005), 207–224.
37. [37] Ansari, S., Baumer, K., Boue, S., Dijon, S., Dulize, R., Ekroos, K., et al. Comprehensive systems biology analysis of a 7-month cigarette smoke inhalation study in C57BL/6 mice. Sci. Data, 3, 2016, 150,077.