Sphingosine 1-phosphate (S1P) lyase deficiency increases sphingolipid formation via recycling at the expense of de Novo biosynthesis in neurons

Journal of Biological Chemistry

Volumn 287, Issue 12, 2012, Pages 9128-9136

  Hagen Euteneuer, Nadine ^a   Lütjohann, Dieter ^b   Park, Hyejung ^c   Merrill, Alfred H ^c   Van Echten Deckert, Gerhild ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CHOLESTEROL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; RECYCLING;

BIOACTIVE LIPIDS; METABOLIC INTERMEDIATES; NEURODEGENERATION; PHYSIOLOGICAL PROCESS; SPHINGOID BASIS; SPHINGOLIPID METABOLISM; SPHINGOLIPIDS; SPHINGOSINE 1 PHOSPHATES; SPHINGOSINE-1-PHOSPHATE LYASE; WILD-TYPE LEVELS;

BIOSYNTHESIS;

SERINE PALMITOYLTRANSFERASE; SPHINGOLIPID; SPHINGOSINE 1 PHOSPHATE;

ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CATABOLISM; CATALYSIS; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DENSITOMETRY; ENZYME ACTIVITY; ENZYME DEFICIENCY; GAS LIQUID CHROMATOGRAPHY; HOMEOSTASIS; LIMIT OF DETECTION; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; SPHINGOSINE 1 PHOSPHATE LYASE DEFICIENCY;

MUS; SPHINGOIDEA;

EID: 84863348086     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.302380     Document Type: Article

References (42)

1. van Echten-Deckert, G., and Herget, T. (2006) Sphingolipid metabolism in neural cells. Biochim. Biophys. Acta 1758, 1978-1994 (Pubitemid 44879360)
2. Hannun, Y. A., and Obeid, L. M. (2008) Principles of bioactive lipid signaling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150 (Pubitemid 351158911)
3. Stiban, J., Tidhar, R., and Futerman, A. H. (2010) Ceramide synthases: roles in cell physiology and signaling. Adv. Exp. Med. Biol. 688, 60-71
4. Kohama, T., Olivera, A., Edsall, L., Nagiec, M. M., Dickson, R., and Spiegel, S. (1998) Molecular cloning and functional characterization of murine sphingosine kinase. J. Biol. Chem. 273, 23722-23728 (Pubitemid 28435703)
5. Liu, H., Sugiura, M., Nava, V. E., Edsall, L. C., Kono, K., Poulton, S., Milstien, S., Kohama, T., and Spiegel, S. (2000) Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J. Biol. Chem. 275, 19513-19520 (Pubitemid 30441543)
6. Van Veldhoven, P. P. (2000) Sphingosine-1-phosphate lyase. Methods Enzymol. 311, 244-254
7. Fyrst, H., and Saba, J. D. (2008) Sphingosine-1-phosphate lyase in development and disease: sphingolipid metabolism takes flight. Biochim. Biophys. Acta 1781, 448-458
8. Bektas, M., Allende, M. L., Lee, B. G., Chen, W., Amar, M. J., Remaley, A. T., Saba, J. D., and Proia, R. L. (2010) Sphingosine-1-phosphate lyase deficiency disrupts lipid homeostasis in liver. J. Biol. Chem. 285, 10880-10889
9. Van Veldhoven, P. P. (2005) Sphingosine 1-phosphate lyase deficient mice. Chem. Phys. Lipids 136, 164-165
10. Hagen, N., Van Veldhoven, P. P., Proia, R. L., Park, H., Merrill, A. H., Jr., and van Echten-Deckert, G. (2009) Subcellular origin of sphingosine 1-phosphate is essential for its toxic effect in lyase-deficient neurons. J. Biol. Chem. 284, 11346-11353
11. Weber, C., Krueger, A., Münk, A., Bode, C., Van Veldhoven, P. P., and Gräler, M. H. (2009) Discontinued postnatal thymocyte development in sphingosine-1-phosphate lyase-deficient mice. J. Immunol. 183, 4292-4301
12. Hagen, N., Hans, M., Hartmann, D., Swandulla, D., and van Echten-Deckert, G. (2011) Sphingosine 1-phosphate links glycosphingolipid metabolism to neurodegeneration via a calpain-mediated mechanism. Cell Death Differ. 18, 1356-1365
13. van Echten-Deckert, G., Zschoche, A., Bär, T., Schmidt, R. R., Raths, A., Heinemann, T., and Sandhoff, K. (1997) cis-4-Methylsphingosine decreases sphingolipid biosynthesis by specifically interfering with serine palmitoyltransferase activity in primary cultured neurons. J. Biol. Chem. 272, 15825-15833 (Pubitemid 27265560)
14. Herget, T., Esdar, C., Oehrlein, S. A., Heinrich, M., Schütze, S., Maelicke, A., and van Echten-Deckert, G. (2000) Production of ceramides causes apoptosis during early neural differentiation in vitro. J. Biol. Chem. 275, 30344-30354
15. Päivä, H., Thelen, K. M., Van Coster, R., Smet, J., De Paepe, B., Mattila, K. M., Laakso, J., Lehtimäki, T., von Bergmann, K., Lütjohann, D., and Laaksonen, R. (2005) High-dose statins and skeletal muscle metabolism in humans: a randomized, controlled trial. Clin. Pharmacol. Ther. 78, 60-68 (Pubitemid 40956932)
16. Lütjohann, D., Breuer, O., Ahlborg, G., Nennesmo, I., Sidén, A., Diczfalusy, U., and Björkhem, I. (1996) Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24(S)-hydroxycholesterol from the brain into the circulation. Proc. Natl. Acad. Sci. U.S.A. 93, 9799-9804
17. Shaner, R. L., Allegood, J. C., Park, H., Wang, E., Kelly, S., Haynes, C. A., Sullards, M. C., and Merrill, A. H., Jr. (2009) Quantitative analysis of sphingolipids for lipidomics using triple quadrupole and quadrupole linear ion trap mass spectrometers. J. Lipid Res. 50, 1692-1707
18. Gillard, B. K., Clement, R. G., and Marcus, D. M. (1998) Variations among cell lines in the synthesis of sphingolipids in de novo and recycling pathways. Glycobiology 8, 885-890 (Pubitemid 28398985)
19. Breslow, D. K., Collins, S. R., Bodenmiller, B., Aebersold, R., Simons, K., Shevchenko, A., Ejsing, C. S., and Weissman, J. S. (2010) Orm family proteins mediate sphingolipid homeostasis. Nature 463, 1048-1053
20. Han, S., Lone, M. A., Schneiter, R., and Chang, A. (2010) Orm1 and Orm2 are conserved endoplasmic reticulum membrane proteins regulating lipid homeostasis and protein quality control. Proc. Natl. Acad. Sci. U.S.A. 107, 5851-5856
21. Puri, V., Jefferson, J. R., Singh, R. D., Wheatley, C. L., Marks, D. L., and Pagano, R. E. (2003) Sphingolipid storage induces accumulation of intracellular cholesterol by stimulating SREBP-1 cleavage. J. Biol. Chem. 278, 20961-20970 (Pubitemid 36806405)
22. Worgall, T. S. (2008) Regulation of lipid metabolism by sphingolipids. Subcell. Biochem. 49, 371-385
23. Le Stunff, H., Giussani, P., Maceyka, M., Lépine, S., Milstien, S., and Spie- gel, S. (2007) Recycling of sphingosine is regulated by the concerted actions of sphingosine-1-phosphate phosphohydrolase 1 and sphingosine kinase 2. J. Biol. Chem. 282, 34372-34380 (Pubitemid 350159464)
24. Levy, M., and Futerman, A. H. (2010) Mammalian ceramide synthases. IUBMB Life 62, 347-356
25. Chigorno, V., Riva, C., Valsecchi, M., Nicolini, M., Brocca, P., and Sonnino, S. (1997) Metabolic processing of gangliosides by human fibroblasts in culture: formation and recycling of separate pools of sphingosine. Eur. J. Biochem. 250, 661-669 (Pubitemid 28022482)
26. Riboni, L., Prinetti, A., Bassi, R., and Tettamanti, G. (1994) Formation of bioactive sphingoid molecules from exogenous sphingomyelin in primary cultures of neurons and astrocytes. FEBS Lett. 352, 323-326
27. Prinetti, A., Chigorno, V., Tettamanti, G., and Sonnino, S. (2000) Sphingolipid- enriched membrane domains from rat cerebellar granule cells differentiated in culture: a compositional study. J. Biol. Chem. 275, 11658-11665 (Pubitemid 30237726)
28. van Echten, G., Iber, H., Stotz, H., Takatsuki, A., and Sandhoff, K. (1990) Uncoupling of ganglioside biosynthesis by brefeldin A. Eur. J. Cell Biol. 51, 135-139 (Pubitemid 20067343)
29. Riboni, L., Bassi, R., Prinetti, A., and Tettamanti, G. (1996) Salvage of catabolic products in ganglioside metabolism: a study on rat cerebellar granule cells in culture. FEBS Lett. 391, 336-340 (Pubitemid 26259785)
30. van Echten, G., Birk, R., Brenner-Weiss, G., Schmidt, R. R., and Sandhoff, K. (1990) Modulation of sphingolipid biosynthesis in primary cultured neurons by long chain bases. J. Biol. Chem. 265, 9333-9339
31. Mandon, E. C., van Echten, G., Birk, R., Schmidt, R. R., and Sandhoff, K. (1991) Sphingolipid biosynthesis in cultured neurons: down-regulation of serine palmitoyltransferase by sphingoid bases. Eur. J. Biochem. 198, 667-674
32. Hjelmqvist, L., Tuson, M., Marfany, G., Herrero, E., Balcells, S., and Gonzàlez-Duarte, R. (2002) ORMDL proteins are a conserved new family of endoplasmic reticulum membrane proteins. Genome Biol. 3, RESEARCH0027
33. Tettamanti, G., Bassi, R., Viani, P., and Riboni, L. (2003) Salvage pathways in glycosphingolipid metabolism. Biochimie 85, 423-437 (Pubitemid 36626013)
34. Chigorno, V., Giannotta, C., Ottico, E., Sciannamblo, M., Mikulak, J., Prinetti, A., and Sonnino, S. (2005) Sphingolipid uptake by cultured cells: complex aggregates of cell sphingolipids with serum proteins and lipoproteins are rapidly catabolized. J. Biol. Chem. 280, 2668-2675 (Pubitemid 40189371)
35. Kitatani, K., Idkowiak-Baldys, J., and Hannun, Y. A. (2008) The sphingolipid salvage pathway in ceramide metabolism and signaling. Cell. Signal. 20, 1010-1018
36. Puglielli, L., Konopka, G., Pack-Chung, E., Ingano, L. A., Berezovska, O., Hyman, B. T., Chang, T. Y., Tanzi, R. E., and Kovacs, D. M. (2001) Acylcoenzyme A: cholesterol acyltransferase modulates the generation of the amyloid β-peptide. Nat. Cell Biol. 3, 905-912 (Pubitemid 32952255)
37. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B. A., and Yuan, J. (2000) Caspase-12 mediates endoplasmic reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 403, 98-103 (Pubitemid 30038529)
38. Lopes, J. P., Oliveira, C. R., and Agostinho, P. (2010) Neurodegeneration in an Aβ-induced model of Alzheimer disease: the role of Cdk5. Aging Cell 9, 64-77
39. Nakagawa, T., and Yuan, J. (2000) Cross-talk between two cysteine protease families: activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150, 887-894 (Pubitemid 30663424)
40. Takasugi, N., Sasaki, T., Suzuki, K., Osawa, S., Isshiki, H., Hori, Y., Shimada, N., Higo, T., Yokoshima, S., Fukuyama, T., Lee, V. M., Trojanowski, J. Q., Tomita, T., and Iwatsubo, T. (2011) BACE1 activity is modulated by cell-associated sphingosine 1-phosphate. J. Neurosci. 31, 6850-6857
41. Lütjohann, D., Stroick, M., Bertsch, T., Kühl, S., Lindenthal, B., Thelen, K., Andersson, U., Björkhem, I., Bergmann Kv, K., and Fassbender, K. (2004) High doses of simvastatin, pravastatin, and cholesterol reduce brain cholesterol synthesis in guinea pigs. Steroids 69, 431-438 (Pubitemid 38829339)
42. Svennerholm, L. (1963) Chromatographic separation of human gangliosides. J. Neurochem. 10, 613-623