Deficiency of sphingosine-1-phosphate lyase impairs lysosomal metabolism of the amyloid precursor protein

Journal of Biological Chemistry

Volumn 289, Issue 24, 2014, Pages 16761-16772

  Karaca, Ilker ^a   Tamboli, Irfan Y ^a,e   Glebov, Konstantin ^a   Richter, Josefine ^b   Fell, Lisa H ^c   Grimm, Marcus O ^c   Haupenthal, Viola J ^c   Hartmann, Tobias ^c   Gräler, Markus H ^d   Van Echten Deckert, Gerhild ^a   Walter, Jochen ^a  

^a UNIVERSITY OF BONN   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

^d JENA UNIVERSITY HOSPITAL   (Germany)

^e GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIODEGRADATION; CELL MEMBRANES; CYTOLOGY; GLYCOPROTEINS; METABOLISM; PHYSIOLOGY; SPHINGOSINES;

AMYLOID PRECURSOR PROTEINS; BIOCHEMICAL METHODS; C-TERMINAL FRAGMENTS; ENDOPLASMIC RETICULUM; INTRACELLULAR ACCUMULATION; PROGRESSIVE ACCUMULATION; PROTEOLYTIC PROCESSING; SPHINGOSINE-1-PHOSPHATE LYASE;

ENZYME ACTIVITY;

AMYLOID PRECURSOR PROTEIN; CALCIUM ION; CATHEPSIN D; GAMMA SECRETASE; LYASE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE LYASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CELL VIABILITY; CONTROLLED STUDY; DENSITOMETRY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME INHIBITION; FIBROBLAST; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID; AMYLOID PRECURSOR PROTEIN (APP); LYSOSOME; SPHINGOLIPID; SPHINGOSINE-1-PHOSPHATE (S1P);

ALDEHYDE-LYASES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CALCIUM; CATHEPSIN D; HEK293 CELLS; HUMANS; LYSOPHOSPHOLIPIDS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOMES; MICE; PROTEOLYSIS; SPHINGOSINE;

EID: 84902438348     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.535500     Document Type: Article

References (59)

1. Selkoe, D. J. (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766
2. Walter, J., Kaether, C., Steiner, H., and Haass, C. (2001) The cell biology of Alzheimer's disease: uncovering the secrets of secretases. Curr. Opin. Neurobiol. 11, 585-590 (Pubitemid 32938290)
3. Thinakaran, G., and Koo, E. H. (2008) Amyloid precursor protein trafficking, processing, and function. J. Biol. Chem. 283, 29615-29619
4. Kandalepas, P. C., and Vassar, R. (2012) Identification and biology of β-secretase. J. Neurochem. 120, 55-61
5. Hussain, I., Powell, D., Howlett, D. R., Tew, D. G., Meek, T. D., Chapman, C., Gloger, I. S., Murphy, K. E., Southan, C. D., Ryan, D. M., Smith, T. S., Simmons, D. L., Walsh, F. S., Dingwall, C., and Christie, G. (1999) Identification of a novel aspartic protease (Asp 2) as β-secretase. Mol. Cell Neurosci. 14, 419-427 (Pubitemid 30026585)
6. Sinha, S., Anderson, J. P., Barbour, R., Basi, G. S., Caccavello, R., Davis, D., Doan, M., Dovey, H. F., Frigon, N., Hong, J., Jacobson-Croak, K., Jewett, N., Keim, P., Knops, J., Lieberburg, I., Power, M., Tan, H., Tatsuno, G., Tung, J., Schenk, D., Seubert, P., Suomensaari, S. M., Wang, S., Walker, D., Zhao, J., McConlogue, L., and John, V. (1999) Purification and cloning of amyloid precursor protein β-secretase from human brain. Nature 402, 537-540
7. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S., Mendiaz, E. A., Denis, P., Teplow, D. B., Ross, S., Amarante, P., Loeloff, R., Luo, Y., Fisher, S., Fuller, J., Edenson, S., Lile, J., Jarosinski, M. A., Biere, A. L., Curran, E., Burgess, T., Louis, J. C., Collins, F., Treanor, J., Rogers, G., and Citron, M. (1999) β-Secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741
8. Yan, R., Bienkowski, M. J., Shuck, M. E., Miao, H., Tory, M. C., Pauley, A. M., Brashier, J. R., Stratman, N. C., Mathews, W. R., Buhl, A. E., Carter, D. B., Tomasselli, A. G., Parodi, L. A., Heinrikson, R. L., and Gurney, M. E. (1999) Membrane-anchored aspartyl protease with Alzheimer's disease β-secretase activity. Nature 402, 533-537
9. Tamboli, I. Y., Hampel, H., Tien, N. T., Tolksdorf, K., Breiden, B., Mathews, P. M., Saftig, P., Sandhoff, K., and Walter, J. (2011) Sphingolipid storage affects autophagic metabolism of the amyloid precursor protein and promotes Aβ generation. J. Neurosci. 31, 1837-1849
10. Haass, C., Koo, E. H., Mellon, A., Hung, A. Y., and Selkoe, D. J. (1992) Targeting of cell-surface β-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357, 500-503
11. van Echten-Deckert, G., and Walter, J. (2012) Sphingolipids: Critical players in Alzheimer's disease. Prog. Lipid Res. 51, 378-393
12. 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
13. Zhang, H., Desai, N. N., Olivera, A., Seki, T., Brooker, G., and Spiegel, S. (1991) Sphingosine-1-phosphate, a novel lipid, involved in cellular proliferation. J. Cell Biol. 114, 155-167 (Pubitemid 21909788)
14. Spiegel, S., and Milstien, S. (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407 (Pubitemid 36565571)
15. van Echten-Deckert, G., and Herget, T. (2006) Sphingolipid metabolism in neural cells. Biochim. Biophys. Acta 1758, 1978-1994 (Pubitemid 44879360)
16. Le Stunff, H., Giussani, P., Maceyka, M., Lépine, S., Milstien, S., and Spiegel, 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)
17. Van Veldhoven, P. P. (2000) Sphingosine-1-phosphate lyase. Methods Enzymol. 311, 244-254
18. 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)
19. Schmahl, J., Raymond, C. S., and Soriano, P. (2007) PDGF signaling specificity is mediated through multiple immediate early genes. Nat. Genet. 39, 52-60 (Pubitemid 46026501)
20. Hannun, Y. A., and Obeid, L. M. (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9, 139-150 (Pubitemid 351158911)
21. Payne, S. G., Milstien, S., and Spiegel, S. (2002) Sphingosine-1- phosphate: dual messenger functions. FEBS Lett. 531, 54-57 (Pubitemid 35232784)
22. 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
23. Hagen-Euteneuer, N., Lütjohann, D., Park, H., Merrill, A. H., Jr., and van Echten-Deckert, G. (2012) Sphingosine 1-phosphate (S1P) lyase deficiency increases sphingolipid formation via recycling at the expense of de novo biosynthesis in neurons. J. Biol. Chem. 287, 9128-9136
24. 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
25. 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
26. 2+ storage in sphingosine-1-phosphate lyase-deficient fibroblasts. Cell Signal. 22, 476-483
27. 2+ homoeostasis in sphingosine-1-phosphate lyase-deficient fibroblasts. Biochem. J. 447, 457-464
28. Wahle, T., Thal, D. R., Sastre, M., Rentmeister, A., Bogdanovic, N., Famulok, M., Heneka, M. T., and Walter, J. (2006) GGA1 is expressed in the human brain and affects the generation of amyloid β-peptide. J. Neurosci. 26, 12838-12846 (Pubitemid 44904579)
29. Grimm, M. O., Haupenthal, V. J., Rothhaar, T. L., Zimmer, V. C., Grösgen, S., Hundsdörfer, B., Lehmann, J., Grimm, H. S., and Hartmann, T. (2013) Effect of different phospholipids on α-secretase activity in the non-amyloidogenic pathway of Alzheimer's disease. Int. J. Mol. Sci. 14, 5879-5898
30. Rothhaar, T. L., Grösgen, S., Haupenthal, V. J., Burg, V. K., Hundsdörfer, B., Mett, J., Riemenschneider, M., Grimm, H. S., Hartmann, T., and Grimm, M. O. (2012) Plasmalogens inhibit APP processing by directly affecting γ-secretase activity in Alzheimer's disease. ScientificWorldJournal 2012, 141240
31. Sastre, M., Steiner, H., Fuchs, K., Capell, A., Multhaup, G., Condron, M. M., Teplow, D. B., and Haass, C. (2001) Presenilin-dependent γ-secretase processing of β-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Rep. 2, 835-841 (Pubitemid 32982753)
32. Bode, C., and Gräler, M. H. (2012) Quantification of sphingosine-1-phosphate and related sphingolipids by liquid chromatography coupled to tandem mass spectrometry. Methods Mol. Biol. 874, 33-44
33. Liu, K., Doms, R. W., and Lee, V. M. (2002) Glu11 site cleavage and N-terminally truncated Aβ production upon BACE overexpression. Biochemistry 41, 3128-3136 (Pubitemid 34184644)
34. Haass, C., Schlossmacher, M. G., Hung, A. Y., Vigo-Pelfrey, C., Mellon, A., Ostaszewski, B. L., Lieberburg, I., Koo, E. H., Schenk, D., and Teplow, D. B. (1992) Amyloid β-peptide is produced by cultured cells during normal metabolism. Nature 359, 322-325
35. Fluhrer, R., Capell, A., Westmeyer, G., Willem, M., Hartung, B., Condron, M. M., Teplow, D. B., Haass, C., and Walter, J. (2002) A non-amyloidogenic function of BACE-2 in the secretory pathway. J. Neurochem. 81, 1011-1020 (Pubitemid 34809283)
36. Tamboli, I. Y., Tien, N. T., and Walter, J. (2011) Sphingolipid storage impairs autophagic clearance of Alzheimer-associated proteins. Autophagy 7, 645-646
37. Agholme, L., Hallbeck, M., Benedikz, E., Marcusson, J., and Kågedal, K. (2012) Amyloid-β secretion, generation, and lysosomal sequestration in response to proteasome inhibition: involvement of autophagy. J. Alzheimers Dis. 31, 343-358
38. Yanagawa, M., Tsukuba, T., Nishioku, T., Okamoto, Y., Okamoto, K., Takii, R., Terada, Y., Nakayama, K. I., Kadowaki, T., and Yamamoto, K. (2007) Cathepsin E deficiency induces a novel form of lysosomal storage disorder showing the accumulation of lysosomal membrane sialoglycoproteins and the elevation of lysosomal pH in macrophages. J. Biol. Chem. 282, 1851-1862 (Pubitemid 47076688)
39. Lloyd-Evans, E., Morgan, A. J., He, X., Smith, D. A., Elliot-Smith, E., Sillence, D. J., Churchill, G. C., Schuchman, E. H., Galione, A., and Platt, F. M. (2008) Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247-1255
40. Shen, D., Wang, X., Li, X., Zhang, X., Yao, Z., Dibble, S., Dong, X. P., Yu, T., Lieberman, A. P., Showalter, H. D., and Xu, H. (2012) Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat. Commun. 3, 731
41. Kalvodova, L., Kahya, N., Schwille, P., Ehehalt, R., Verkade, P., Drechsel, D., and Simons, K. (2005) Lipids as modulators of proteolytic activity of BACE: involvement of cholesterol, glycosphingolipids, and anionic phospholipids in vitro. J. Biol. Chem. 280, 36815-36823 (Pubitemid 41587762)
42. Osenkowski, P., Ye, W., Wang, R., Wolfe, M. S., and Selkoe, D. J. (2008) Direct and potent regulation of γ-secretase by its lipid microenvironment. J. Biol. Chem. 283, 22529-22540
43. Holmes, O., Paturi, S., Ye, W., Wolfe, M. S., and Selkoe, D. J. (2012) Effects of membrane lipids on the activity and processivity of purified γ-secretase. Biochemistry 51, 3565-3575
44. Walter, J., and van Echten-Deckert, G. (2013) Cross-talk of membrane lipids and Alzheimer-related proteins. Mol. Neurodegener. 8, 34
45. Di Paolo, G., and Kim, T. W. (2011) Linking lipids to Alzheimer's disease: cholesterol and beyond. Nat. Rev. Neurosci. 12, 284-296
46. Winkler, E., Kamp, F., Scheuring, J., Ebke, A., Fukumori, A., and Steiner, H. (2012) Generation of Alzheimer disease-associated amyloid β42/43 peptide by γ-secretase can be inhibited directly by modulation of membrane thickness. J. Biol. Chem. 287, 21326-21334
47. Benes, P., Vetvicka, V., and Fusek, M. (2008) Cathepsin D: many functions of one aspartic protease. Crit. Rev. Oncol. Hematol. 68, 12-28
48. Bankowska, A., Gacko, M., Chyczewska, E., and Worowska, A. (1997) Biological and diagnostic role of cathepsin D. Rocz Akad Med. Bialymst. 42, 79-85
49. Sandhoff, K., and Kolter, T. (1998) Processing of sphingolipid activator proteins and the topology of lysosomal digestion. Acta Biochim. Pol. 45, 373-384 (Pubitemid 128480897)
50. Luzio, J. P., Bright, N. A., and Pryor, P. R. (2007) The role of calcium and other ions in sorting and delivery in the late endocytic pathway. Biochem. Soc. Trans. 35, 1088-1091 (Pubitemid 350206436)
51. Luzio, J. P., Poupon, V., Lindsay, M. R., Mullock, B. M., Piper, R. C., and Pryor, P. R. (2003) Membrane dynamics and the biogenesis of lysosomes. Mol. Membr. Biol. 20, 141-154 (Pubitemid 36841704)
52. 2+ homeostasis: role in pathogenesis of lysosomal storage diseases. Cell Calcium 50, 200-205
53. Buxbaum, J. D., Ruefli, A. A., Parker, C. A., Cypess, A. M., and Greengard, P. (1994) Calcium regulates processing of the Alzheimer amyloid protein precursor in a protein kinase C-independent manner. Proc. Natl. Acad. Sci. U.S.A. 91, 4489-4493 (Pubitemid 24143459)
54. Bastow, E. R., Last, K., Golub, S., Stow, J. L., Stanley, A. C., and Fosang, A. J. (2012) Evidence for lysosomal exocytosis and release of aggrecan-degrading hydrolases from hypertrophic chondrocytes, in vitro and in vivo. Biol. Open 1, 318-328
55. 2+ channels of membrane traffic. Channels 6, 344-351
56. Malnar, M., Kosicek, M., Lisica, A., Posavec, M., Krolo, A., Njavro, J., Omerbasic, D., Tahirovic, S., and Hecimovic, S. (2012) Cholesterol-depletion corrects APP and BACE1 misstrafficking in NPC1-deficient cells. Biochim. Biophys. Acta 1822, 1270-1283
57. Boland, B., Smith, D. A., Mooney, D., Jung, S. S., Walsh, D. M., and Platt, F. M. (2010) Macroautophagy is not directly involved in the metabolism of amyloid precursor protein. J. Biol. Chem. 285, 37415-37426
58. Keilani, S., Lun, Y., Stevens, A. C., Williams, H. N., Sjoberg, E. R., Khanna, R., Valenzano, K. J., Checler, F., Buxbaum, J. D., Yanagisawa, K., Lockhart, D. J., Wustman, B. A., and Gandy, S. (2012) Lysosomal dysfunction in a mouse model of Sandhoff disease leads to accumulation of ganglioside-bound amyloid-β peptide. J. Neurosci. 32, 5223-5236
59. Jin, L. W., Shie, F. S., Maezawa, I., Vincent, I., and Bird, T. (2004) Intracellular accumulation of amyloidogenic fragments of amyloid-β precursor protein in neurons with Niemann-Pick type C defects is associated with endosomal abnormalities. Am. J. Pathol. 164, 975-985 (Pubitemid 38235479)