Glucosylceramide modulates endolysosomal pH in Gaucher disease

Molecular Genetics and Metabolism

Volumn 109, Issue 2, 2013, Pages 194-200

  Sillence, Dan J ^a  

^a DE MONTFORT UNIVERSITY   (United Kingdom)

Author keywords

BODIPY LacCer; CBE; Endocytic trafficking; GalSph; GlcCer; GlcSph; Glycosphingolipid; Golgi; GSL; Lysosomal pH; Lysosomal storage disease; NB DGJ; PDMP; PPMP

Indexed keywords

BAFILOMYCIN A1; CERAMIDE GLUCOSYLTRANSFERASE; CHOLESTEROL; GLUCOSYLCERAMIDE; GLUCOSYLSPHINGOSINE; PSYCHOSINE; SPHINGOSINE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOCYTOSIS; FABRY DISEASE; GAUCHER DISEASE; GLOBOID CELL LEUKODYSTROPHY; GM1 GANGLIOSIDOSIS; GOLGI COMPLEX; HUMAN; HUMAN CELL; LIPID ANALYSIS; LIPOGENESIS; LYMPHOBLAST; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; TAY SACHS DISEASE;

ACID-BASE EQUILIBRIUM; ANIMALS; CELL LINE; CHOLESTEROL; DRUG EVALUATION, PRECLINICAL; ENDOSOMES; GAUCHER DISEASE; GLUCOSYLCERAMIDES; HUMANS; LYMPHOID PROGENITOR CELLS; LYSOSOMES; MICE; TRIGLYCERIDES;

EID: 84878481561     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2013.03.015     Document Type: Article

References (52)

1. Yamashita T., Wada R., Sasaki T., Deng C., Bierfreund U., Sandhoff K., Proia R.L. A vital role for glycosphingolipid synthesis during development and differentiation. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9142-9147.
2. 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. 1998, 95:6373-6378.
3. Chen C.S., Patterson M.C., Wheatley C.L., O'Brien J.F., Pagano R.E. Broad screening test for sphingolipid-storage diseases. Lancet 1999, 354:901-905.
4. Puri V., Watanabe R., Dominguez M., Sun X., Wheatley C.L., Marks D.L., Pagano R.E. Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat. Cell Biol. 1999, 1:386-388.
5. Puri V., Watanabe R., Singh R.D., Dominguez M., Brown J.C., Wheatley C.L., Marks D.L., Pagano R.E. Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways. J. Cell Biol. 2001, 154:535-548.
6. Sillence D.J., Puri V., Marks D.L., Butters T.D., Dwek R.A., Pagano R.E., Platt F.M. Glucosylceramide modulates membrane traffic along the endocytic pathway. J. Lipid Res. 2002, 43:1837-1845.
7. A. Fraldi, F. Annunziata, A. Lombardi, H.J. Kaiser, D.L. Medina, C. Spampanato, A.O. Fedele, R. Polishchuk, N.C. Sorrentino, K. Simons, A. Ballabio, Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders, EMBO J. 29 3607-3620.
8. Clague M.J., Urbe S., Aniento F., Gruenberg J. Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 1994, 269:21-24.
9. Vanweert A.W.M., Dunn K.W., Geuze H.J., Maxfield F.R., Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol. 1995, 130:821-834.
10. Gu F., Gruenberg J. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J. Biol. Chem. 2000, 275:8154-8160.
11. +-ATPase, blocks lysosomal cholesterol trafficking in macrophages. J. Biol. Chem. 1993, 268:27345-27348.
12. Suomi W.D., Agranoff B.W. Lipids of the spleen in Gaucher's disease. J. Lipid Res. 1965, 6:211-219.
13. S. van der Poel, J. Wolthoorn, D. van den Heuvel, M. Egmond, S. Groux-Degroote, S. Neumann, H. Gerritsen, G. van Meer, H. Sprong, Hyperacidification of trans-Golgi network and endo/lysosomes in melanocytes by glucosylceramide-dependent V-ATPase activity, Traffic 12 1634-1647.
14. Bach G., Chen C.S., Pagano R.E. Elevated lysosomal pH in Mucolipidosis type IV cells. Clin. Chim. Acta 1999, 280:173-179.
15. Lin H.J., Herman P., Kang J.S., Lakowicz J.R. Fluorescence lifetime characterization of novel low-pH probes. Anal. Biochem. 2001, 294:118-125.
16. Diwu Z., Chen C.S., Zhang C., Klaubert D.H., Haugland R.P. A novel acidotropic pH indicator and its potential application in labeling acidic organelles of live cells. Chem. Biol. 1999, 6:411-418.
17. Hein L.K., Meikle P.J., Hopwood J.J., Fuller M. Secondary sphingolipid accumulation in a macrophage model of Gaucher disease. Mol. Genet. Metab. 2007, 92:336-345.
18. Puri V., Jefferson J.R., Singh R.D., Wheatley C.L., Marks D.L., Pagano R.E. Sphingolipid storage induces accumulation of intracellular cholesterol by stimulating SREBP-1 cleavage. J. Biol. Chem. 2003, 278:20961-20970.
19. Sprong H., Degroote S., Claessens T., van Drunen J., Oorschot V., Westerink B.H., Hirabayashi Y., Klumperman J., van Der Sluijs P., van Meer G. Glycosphingolipids are required for sorting melanosomal proteins in the Golgi complex. J. Cell Biol. 2001, 155:369-380.
20. Farrer R.G., Dawson G. Acylation of exogenous glycosylsphingosines by intact neuroblastoma (NCB-20) cells. J. Biol. Chem. 1990, 265:22217-22222.
21. van Genderen I., van Meer G. Differential targeting of glucosylceramide and galactosylceramide analogues after synthesis but not during transcytosis in Madin-Darby canine kidney cells. J. Cell Biol. 1995, 131:645-654.
22. Vanijzendoorn S.C.D., Zegers M.M.P., Kok J.W., Hoekstra D. Segregation of glucosylceramide and sphingomyelin occurs in the apical to basolateral transcytotic route in HepG2 cells. J. Cell Biol. 1997, 137:347-357.
23. +-ATPase by tonoplast glycolipids prepared from cultured rice (Oryza sativa L. var. Boro) cells. Plant Cell Physiol. 2001, 42:516-523.
24. +-ATPase from cultured rice (Oryza sativa L. var. Boro) cells by acyl steryl glucoside and steryl glucoside. Plant Cell Physiol. 2002, 43:816-822.
25. Wang R., Hosaka M., Han L., Yokota-Hashimoto H., Suda M., Mitsushima D., Torii S., Takeuchi T. Molecular probes for sensing the cholesterol composition of subcellular organelle membranes. Biochim. Biophys. Acta 2006, 1761:1169-1181.
26. Ichikawa S., Nakajo N., Sakiyama H., Hirabayashi Y. A mouse B16 melanoma mutant deficient in glycolipids. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:2703-2707.
27. D.I. Mundy, W.P. Li, K. Luby-Phelps, R.G. Anderson, Caveolin targeting to late endosome/lysosomal membranes is induced by perturbations of lysosomal pH and cholesterol content, Mol. Biol. Cell 23 864-880.
28. Schapiro F.B., Lingwood C., Furuya W., Grinstein S. pH-independent retrograde targeting of glycolipids to the Golgi complex. Am. J. Physiol. 1998, 274:C319-C332.
29. Bowman E.J., Siebers A., Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:7972-7976.
30. 14C]Methylamine accumulation in cultured human skin fibroblasts-a biochemical test for lysosomal storage and lysosomal diseases. Clin. Chim. Acta 1994, 227:121-133.
31. E. Lloyd-Evans, A.J. Morgan, X. He, D.A. Smith, E. Elliot-Smith, D.J. Sillence, G.C. Churchill, E.H. Schuchman, A. Galione, F.M. Platt, Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium, Nat. Med. 14 (6) 1247-1255.
32. Ivleva T.S., Ogloblina T.A., Litinskaya L.L., Wiederschain G. Estimation and comparison of lysosomal and cytoplasmic pH of human fibroblasts from healthy donors and patients with lysosomal storage diseases. Biomed. Sci. 1991, 2:398-402.
33. B. Tancini, A. Magini, L. Latterini, L. Urbanelli, V. Ciccarone, F. Elisei, C. Emiliani, Occurrence of an anomalous endocytic compartment in fibroblasts from Sandhoff disease patients, Mol. Cell Biochem. 335 273-282.
34. Pryor P.R., Reimann F., Gribble F.M., Luzio J.P. Mucolipin-1 is a lysosomal membrane protein required for intracellular lactosylceramide traffic. Traffic 2006, 7:1388-1398.
35. M.T. Miedel, Y. Rbaibi, C.J. Guerriero, G. Colletti, K.M. Weixel, O.A. Weisz, K. Kiselyov, Membrane traffic and turnover in TRP-ML1-deficient cells: a revised model for mucolipidosis type IV pathogenesis, J. Exp. Med. 205 (6) 1477-1490.
36. Butor C., Griffiths G., Aronson N.N., Varki A. Co-localization of hydrolytic enzymes with widely disparate pH optima: implications for the regulation of lysosomal pH. J. Cell Sci. 1995, 108(Pt 6):2213-2219.
37. te Vruchte D., Lloyd-Evans E., Veldman R.J., Neville D.C.A., Dwek R.A., Platt F.M., van Blitterswijk W.J., Sillence D.J. Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport. J. Biol. Chem. 2004, 279:26167-26175.
38. C. Lafourcade, K. Sobo, S. Kieffer-Jaquinod, J. Garin, F.G. van der Goot, Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization, PLoS ONE 3 (6) e2758.
39. M. Fuller, T. Rozaklis, M. Lovejoy, K. Zarrinkalam, J.J. Hopwood, P.J. Meikle, Glucosylceramide accumulation is not confined to the lysosome in fibroblasts from patients with Gaucher disease, Mol. Genet. Metab. 93 (6) 437-443.
40. Halter D., Neumann S., van Dijk S.M., Wolthoorn J., de Maziere A.M., Vieira O.V., Mattjus P., Klumperman J., van Meer G., Sprong H. Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J. Cell Biol. 2007, 179:101-115.
41. Boot R.G., Verhoek M., Donker-Koopman W., Strijland A., van Marle J., Overkleeft H.S., Wennekes T., Aerts J.M. Identification of the non-lysosomal glucosylceramidase as beta-glucosidase 2. J. Biol. Chem. 2006.
42. Koerschen H.G., Yildiz Y., Raju D.N., Schonauer S., Boenigk W., Jansen V., Kremmer E., Kaupp U.B., Wachten D. The non-lysosomal beta-glucosidase GBA2 is a non-integral membrane-associated protein at the ER and Golgi. J. Biol. Chem. 2012.
43. Yildiz Y., Matern H., Thompson B., Allegood J.C., Warren R.L., Ramirez D.M., Hammer R.E., Hamra F.K., Matern S., Russell D.W. Mutation of beta-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J. Clin. Invest. 2006, 116:2985-2994.
44. A.C. van der Spoel, R. Mott, F.M. Platt, Differential sensitivity of mouse strains to an N-alkylated imino sugar: glycosphingolipid metabolism and acrosome formation, Pharmacogenomics 9 (6) 717-731.
45. Walden C.M., Sandhoff R., Chuang C.C., Yildiz Y., Butters T.D., Dwek R.A., Platt F.M., van der Spoel A.C. Accumulation of glucosylceramide in murine testis, caused by inhibition of beta-glucosidase 2: implications for spermatogenesis. J. Biol. Chem. 2007, 282:32655-32664.
46. Rittershaus P.C., Kechichian T.B., Allegood J.C., Merrill A.H., Hennig M., Luberto C., Del Poeta M. Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J. Clin. Invest. 2006, 116:1651-1659.
47. Chung J.H., Lester R.L., Dickson R.C. Sphingolipid requirement for generation of a functional v1 component of the vacuolar ATPase. J. Biol. Chem. 2003, 278:28872-28881.
48. B. Lelouvier, R. Puertollano, Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway, J. Biol. Chem. 286 9826-9832.
49. N. Dekker, L. van Dussen, C.E. Hollak, H. Overkleeft, S. Scheij, K. Ghauharali, M.J. van Breemen, M.J. Ferraz, J.E. Groener, M. Maas, F.A. Wijburg, D. Speijer, A. Tylki-Szymanska, P.K. Mistry, R.G. Boot, J.M. Aerts, Elevated plasma glucosylsphingosine in Gaucher disease: relation to phenotype, storage cell markers, and therapeutic response, Blood 118 e118-127.
50. E. Lukina, N. Watman, E.A. Arreguin, M. Banikazemi, M. Dragosky, M. Iastrebner, H. Rosenbaum, M. Phillips, G.M. Pastores, D.I. Rosenthal, M. Kaper, T. Singh, A.C. Puga, P.L. Bonate, M.J. Peterschmitt, A phase 2 study of eliglustat tartrate (Genz-112638), an oral substrate reduction therapy for Gaucher disease type 1, Blood 116 893-899.
51. M.B. Hammer, G. Eleuch-Fayache, L.V. Schottlaender, H. Nehdi, J.R. Gibbs, S.K. Arepalli, S.B. Chong, D.G. Hernandez, A. Sailer, G. Liu, P.K. Mistry, H. Cai, G. Shrader, C. Sassi, Y. Bouhlal, H. Houlden, F. Hentati, R. Amouri, A.B. Singleton, Mutations in GBA2 cause autosomal-recessive cerebellar ataxia with spasticity, Am. J. Hum. Genet. 92 245-251.
52. E. Martin, R. Schule, K. Smets, A. Rastetter, A. Boukhris, J.L. Loureiro, M.A. Gonzalez, E. Mundwiller, T. Deconinck, M. Wessner, L. Jornea, A.C. Oteyza, A. Durr, J.J. Martin, L. Schols, C. Mhiri, F. Lamari, S. Zuchner, P. De Jonghe, E. Kabashi, A. Brice, G. Stevanin, Loss of function of glucocerebrosidase GBA2 is responsible for motor neuron defects in hereditary spastic paraplegia, Am. J. Hum. Genet. 92 238-244.