Neuronal sphingolipidoses: Membrane lipids and sphingolipid activator proteins regulate lysosomal sphingolipid catabolism

Biochimie

Volumn 130, Issue , 2016, Pages 146-151

  Sandhoff, Konrad ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Cholesterol transfer of NPC2; Lipid modifiers; Regulation of acid sphingomyelinase; Regulation of ganglioside catabolism; Tay Sachs disease

Indexed keywords

CHOLESTEROL; GANGLIOSIDE GM2; HYDROLASE; SPHINGOLIPID ACTIVATOR PROTEIN; MEMBRANE LIPID; SPHINGOLIPID;

CELL ORGANELLE; ENDOSOME; EUKARYOTE; LIPID COMPOSITION; LIPID DEGRADATION; LIPID MEMBRANE; LIPIDOSIS; LIPOLYSIS; LYSOSOME; NERVE CELL; PROTEIN ANALYSIS; REGULATORY MECHANISM; SHORT SURVEY; BIOLOGICAL MODEL; HUMAN; METABOLISM;

CHOLESTEROL; ENDOSOMES; HUMANS; LYSOSOMES; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; SPHINGOLIPID ACTIVATOR PROTEINS; SPHINGOLIPIDOSES; SPHINGOLIPIDS;

EID: 84971367795     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2016.05.004     Document Type: Short Survey

References (37)

1. [1] Schulze, H., Sandhoff, K., Sphingolipids and lysosomal pathologies. Biochim. Biophys. Acta 1841 (2014), 799–810.
2. [2] Kolter, T., Sandhoff, K., Lysosomal degradation of membrane lipids. FEBS Lett. 584 (2010), 1700–1712.
3. [3] Sandhoff, K., My journey into the world of sphingolipids and sphingolipidoses. Proc. Jpn. Acad. Ser. B 88 (2012), 554–582.
4. [4] van Meer, G., Voelker, D.R., Feigenson, G.W., Membrane lipids: where they are and how they behave., 9, 2008, 112–124.
5. [5] Mouritsen, O.G., Zuckermann, M.J., What's so special about cholesterol?. Lipids 39 (2004), 1101–1113.
6. [6] Oninla, V.O., Breiden, B., Babalola, J.O., Sandhoff, K., Acid sphingomyelinase activity is regulated by membrane lipids and facilitates cholesterol transfer by NPC2. J. Lipid Res. 55 (2014), 2606–2619.
7. [7] Wollert, T., Hurley, J.H., Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464 (2010), 864–869.
8. [8] Fürst, W., Sandhoff, K., Activator proteins and topology of lysosomal sphingolipid catabolism. Biochim. Biophys. Acta 1126 (1992), 1–16.
9. [9] Kolter, T., Winau, F., Schaible, U.E., Leippe, M., Sandhoff, K., Lipid-binding proteins in membrane digestion, antigen presentation, and antimicrobial defense. J. Biol. Chem. 280 (2005), 41125–41128.
10. [10] Burkhardt, J.K., Hüttler, S., Klein, A., Möbius, W., Habermann, A., Griffiths, G., Sandhoff, K., Accumulation of sphingolipids in SAP-precursor (prosaposin)-deficient fibroblasts occurs as intralysosomal membrane structures and can be completely reversed by treatment with human SAP-precursor. Eur. J. Cell Biol. 73 (1997), 10–18.
11. [11] Vanier, M.T., Complex lipid trafficking in Niemann-Pick disease type C. J. Inherit. Metab. Dis. 38 (2015), 187–199.
12. [12] Vanier, M.T., Millat, G., Niemann-Pick disease type C. Clin. Genet. 64 (2003), 269–281.
13. [13] Sandhoff, K., Metabolic and cellular bases of sphingolipidoses. Biochem. Soc. Trans. 41 (2013), 1562–1568.
14. [14] Kwon, H.J., Abi-Mosleh, L., Wang, M.L., Deisenhofer, J., Goldstein, J.L., Brown, M.S., Infante, R.E., Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137 (2009), 1213–1224.
15. [15] Vanier, M., Biochemical studies in Niemann-Pick disease: I. Major sphingolipids of liver and spleen. Biochim. Biophys. Acta 750 (1983), 178–184.
16. [16] Linke, T., Wilkening, G., Lansmann, S., Moczall, H., Bartelsen, O., Weisgerber, J., Sandhoff, K., Stimulation of acid sphingomyelinase activity by lysosomal lipids and sphingolipid activator proteins. Biol. Chem. 382 (2001), 283–290.
17. [17] Hurwitz, R., Ferlinz, K., Sandhoff, K., The tricyclic antidepressant desipramine causes proteolytic degradation of lysosomal sphingomyelinase in human fibroblasts. Biol. Chem. Hoppe Seyler 375 (1994), 447–450.
18. [18] Kölzer, M., Werth, N., Sandhoff, K., Interactions of acid sphingomyelinase and lipid bilayers in the presence of the tricyclic antidepressant desipramine. FEBS Lett. 559 (2004), 96–98.
19. [19] Anheuser, S., Breiden, B., Schwarzmann, G., Sandhoff, K., Membrane lipids regulate ganglioside GM2 catabolism and GM2 activator protein activity. J. Lipid Res. 56 (2015), 1747–1761.
20. [20] Gondre-Lewis, M.C., McGlynn, R., Walkley, S.U., Cholesterol accumulation in NPC1-deficient neurons is ganglioside dependent. Curr. Biol. 13 (2003), 1324–1329.
21. [21] Cheruku, S.R., Xu, Z., Dutia, R., Lobel, P., Storch, J., Mechanism of cholesterol transfer from the Niemann-Pick type C2 protein to model membranes supports a role in lysosomal cholesterol transport. J. Biol. Chem. 281 (2006), 31594–31604.
22. [22] Naureckiene, S., Sleat, D.E., Lackland, H., Fensom, A., Vanier, M.T., Wattiaux, R., Jadot, M., Lobel, P., Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290 (2000), 2298–2301.
23. [23] Locatelli-Hoops, S., Remmel, N., Klingenstein, R., Breiden, B., Rossocha, M., Schoeniger, M., Koenigs, C., Saenger, W., Sandhoff, K., Saposin A mobilizes lipids from low cholesterol and high bis(monoacylglycerol)phosphate-containing membranes: patient variant saposin A lacks lipid extraction capacity. J. Biol. Chem. 281 (2006), 32451–32460.
24. [24] Remmel, N., Locatelli-Hoops, S., Breiden, B., Schwarzmann, G., Sandhoff, K., Saposin B mobilizes lipids from cholesterol-poor and bis(monoacylglycero)phosphate-rich membranes at acidic pH. Unglycosylated patient variant saposin B lacks lipid-extraction capacity. FEBS J. 274 (2007), 3405–3420.
25. [25] Bowman, E.A., Walterfang, M., Abel, L., Desmond, P., Fahey, M., Velakoulis, D., Longitudinal changes in cerebellar and subcortical volumes in adult-onset Niemann-Pick disease type C patients treated with miglustat. J. Neurol. 262 (2015), 2106–2114.
26. [26] Patterson, M.C., Mengel, E., Vanier, M.T., Schwierin, B., Muller, A., Cornelisse, P., Pineda, M.N.P.C.R. investigators, Amado-Fondo, A., Amraoui, Y., Andria, G., Arellano, M., Audoin, B., Azcona, C., Barr, C., Baruteau, J., Baumgartner, C., Bell, L., Bembi, B., Benneddif, K., Bernard, G., Bobocea, N., Bodzioch, M., Boettcher, T., Bonnan, M., Broue, P., Bruni, A., Caceres, M., Camino, R., Campbell, E., Cances, C., Cannell, P., Cesar, J., Chabrol, B., Chakrapani, A., Colao, R., Collet, A., Corsetti, T., Cousins, A., Covanis, A., Cox, T., Cuisset, J.M., Dardis, A., Das, A., Deegan, P., Dengler, T., Deodato, F., Derralynn, H., Di Donato, I., Di Rocco, M., Dinopoulos, A., DomanskaPakiela, Eckehard, S., Engelen, M., Eyer, D., Fecarotta, S., Federico, A., Filla, A., Fiumara, A., Fonseca, M.J., Gabrielli, O., Garcia, T., Garrote, J., Gissen, P., Giugliani, L., Greenberg, C., Heron, B., Hertzberg, C., Higgins, F., Hill, A., Hiwot, T., Hlavata, A., Horbe-Blindt, A., Howley, E., Hussain, N., Illsinger, S., Imrie, J., Jacklin, E., Jones, S., Jovanovic, A., Kaczmarek, V., Kaphan, E., Kibaek, M., Kleinhans, P., Klunemann, K.H., Koch, S.M., Koegl-Wallner, W., Kolnikova, M., Korenke, G.C., Korinthenberg, R., Kumari, S., Lachmann, R., Lee Ann, L., Likopoulou, L., Lilienthal, E., Link, B., Lippold, M., Lopez-Laso, E., Luecke, T., Lundgren, J., Mackrell, M., Madruga, M., Maletta, R., Malinova, V., Manners, J., Marinei, R., Marquardt, T., Martins, E., Martins, A.M., Martins, N., McAlister, L., McCabe, A., McKie, M., McMahon, S., Meehan, M., Meldgaard Lund, A., Mendozah, C., Mengel, E., Meyer, A., Mielke, S., Milligan, A., Mir, P., Moisa, M., Mombelli, C., Morris, L., Muller vom Hagen, J., Munoz, B., Murphy, E., Nagarajan, L., Neto, P.B., Nevsimalova, S., Nia, S., Nicolai, J., Niemann, D., Niktari, G., O'Callaghan, M.D.M., Paucar-Arce, M., Peers, K., Peintinger, L., Peralta, M., Perez, J., Perez-Poyato, M., Petrariu, A., Pineda, Puschmann, A., Raiman, J., Rask, O., Rataj, J., Raymond-Gaynor, C., Reichelt, G., Ribeiro, E., Riches, V., Roberts, A., Roelants, J., Rohrbach, M., Rokicki, D., Rolfs, A., Russo, C., Rutsch, F., Saleem, R., Santos, M., Schmutz, P., Schwahn, B., Sedel, F., Semotok, J., Sharma, R., Silska, S., Silva, A., Simmons, L., Sivera, R., Skorpen, J., Sole, G., Souza, C., Stadlober-Degwerth, M., Starling, J., Temudo, T., Tomas, M., Tranchant, C., Uziel, G., Valayannopoulous, V., Van den Hout, H., Van der Tol, L., Van Spronsen, F., Vellodi, A., Verdu, A., Vilchez, J.J., Vinaixa, A., Visser, G., Voelker, J., Waldek, S., Walter, A., Walterfang, M., Wein, U., Widner, H., Wilcke, C., Wildish, L., Wraith, E., Wright, N., Xaidara, A., Yamamoto, M., Zallocco, F., Zielke, S., Stable or improved neurological manifestations during miglustat therapy in patients from the international disease registry for Niemann-Pick disease type C: an observational cohort study. Orphanet J. Rare Dis., 10, 2015, 65.
27. [27] Schwarzmann, G., Breiden, B., Sandhoff, K., Membrane-spanning lipids for an uncompromised monitoring of membrane fusion and intermembrane lipid transfer. J. Lipid Res. 56 (2015), 1861–1879.
28. [28] Vaccaro, A.M., Tatti, M., Ciaffoni, F., Salvioli, R., Serafino, A., Barca, A., Saposin-C induces pH-dependent destabilization and fusion of phosphatidylserine-containing vesicles. FEBS Lett. 349 (1994), 181–186.
29. [29] Conzelmann, E., Burg, J., Stephan, G., Sandhoff, K., Complexing of glycolipids and their transfer between membranes by the activator protein for degradation of lysosomal ganglioside GM2. Eur. J. Biochem. 123 (1982), 455–464.
30. [30] Wilkening, G., Linke, T., Sandhoff, K., Lysosomal degradation on vesicular membrane surfaces. Enhanced glucosylceramide degradation by lysosomal anionic lipids and activators. J. Biol. Chem. 273 (1998), 30271–30278.
31. [31] Linke, T., Wilkening, G., Sadeghlar, F., Mozcall, H., Bernardo, K., Schuchman, E., Sandhoff, K., Interfacial regulation of acid ceramidase activity. Stimulation of ceramide degradation by lysosomal lipids and sphingolipid activator proteins. J. Biol. Chem. 276 (2001), 5760–5768.
32. [32] Breiden, B., Sandhoff, K., The role of sphingolipid metabolism in cutaneous permeability barrier formation. Biochim. Biophys. Acta 1841 (2014), 441–452.
33. [33] Henseler, M., Klein, A., Glombitza, G.J., Suzuki, K., Sandhoff, K., Expression of the three alternative forms of the sphingolipid activator protein precursor in baby hamster kidney cells and functional assays in a cell culture system. J. Biol. Chem. 271 (1996), 8416–8423.
34. [34] Bradova, V., Smid, F., Ulrich-Bott, B., Roggendorf, W., Paton, B.C., Harzer, K., Prosaposin deficiency: further characterization of the sphingolipid activator protein-deficient sibs. Multiple glycolipid elevations (including lactosylceramidosis), partial enzyme deficiencies and ultrastructure of the skin in this generalized sphingolipid storage disease. Hum. Genet. 92 (1993), 143–152.
35. [35] Sandhoff, K., Harzer, K., Wässle, W., Jatzkewitz, H., Enzyme alterations and lipid storage in three variants of Tay-Sachs disease. J. Neurochem. 18 (1971), 2469–2489.
36. [36] Geiger, B., Arnon, R., Sandhoff, K., Immunochemical and biochemical investigation of hexosaminidase S. Am. J. Hum. Genet. 29 (1977), 508–522.
37. [37] Wilkening, G., Linke, T., Uhlhorn-Dierks, G., Sandhoff, K., Degradation of membrane-bound ganglioside GM1. Stimulation by bis(monoacylglycero)phosphate and the activator proteins SAP-B and GM2-AP. J. Biol. Chem. 275 (2000), 35814–35819.