The non-lysosomal β-glucosidase GBA2 is a non-integral membrane-associated protein at the endoplasmic reticulum (ER) and Golgi

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3381-3393

  Körschen, Heinz G ^a   Yildiz, Yildiz ^b   Raju, Diana Nancy ^a,b   Schonauer, Sophie ^a   Bönigk, Wolfgang ^a   Jansen, Vera ^a   Kremmer, Elisabeth ^c   Kaupp, U Benjamin ^a   Wachten, Dagmar ^a  

^a CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR MEMBRANES; CERAMIDES; CYTOSOLIC PROTEINS; ENDOPLASMIC RETICULUM; GAUCHER DISEASE; GAUCHER PATIENTS; GLUCOSIDASE; GLYCOSPHINGOLIPIDS; IN-VIVO; INTEGRAL MEMBRANE PROTEINS; INTRACELLULAR MESSENGERS; KNOCK OUTS; LIVER REGENERATION; MEMBRANE-ASSOCIATED PROTEINS; NON INTEGRALS; PHYSIOLOGICAL FUNCTIONS; UNDERLYING MECHANISM;

AMIDES; CELL CULTURE; CELL MEMBRANES; FIBROBLASTS; GLUCOSE; HISTOLOGY; PHOSPHOLIPIDS; TISSUE;

PROTEINS;

BETA GLUCOSIDASE; CALNEXIN; GLUCOSYLCERAMIDE; GLYCOSPHINGOLIPID; MEMBRANE PROTEIN; PHOSPHOLIPID;

ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL GROWTH; CELL MEMBRANE; ENDOPLASMIC RETICULUM; FIBROBLAST; GAUCHER DISEASE; GENE MUTATION; GOLGI COMPLEX; HUMAN; IN VIVO STUDY; LIVER REGENERATION; LYSOSOME; LYSOSOME STORAGE DISEASE; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

ANIMALS; ANTIBODY SPECIFICITY; BETA-GLUCOSIDASE; DOWN-REGULATION; ENDOPLASMIC RETICULUM; ENZYME ASSAYS; FIBROBLASTS; FLUORESCENCE; GOLGI APPARATUS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; LYSOSOMES; MEMBRANE PROTEINS; MICE; NEURONS; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84873283543     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.414714     Document Type: Article

References (41)

1. Lahiri, S., and Futerman, A. H. (2007) The metabolism and function of sphingolipids and glycosphingolipids. Cell. Mol. Life Sci. 64, 2270-2284
2. Hirabayashi, Y. (2012) A world of sphingolipids and glycolipids in the brain. Novel functions of simple lipids modified with glucose. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 88, 129-143
3. Futerman, A. H., and Pagano, R. E. (1991) Determination of the intracellular sites and topology ofglucosylceramide synthesisin rat liver. Biochem. J. 280, 295-302
4. Jeckel, D., Karrenbauer, A., Burger, K. N., Van Meer, G., and Wieland, F. (1992) Glucosylceramide is synthesized at the cytosolic surface of various Golgi subfractions. J. Cell Biol. 117, 259-267
5. Paul, P., Kamisaka, Y., Marks, D. L., and Pagano, R. E. (1996) Purification and characterization of UDP-glucose: ceramide glucosyltransferase from rat liver Golgi membranes. J. Biol. Chem. 271, 2287-2293
6. Lannert, H., Bünning, C., Jeckel, D., and Wieland, F. T. (1994) Lactosylceramide is synthesized in the lumen of the Golgi apparatus. FEBS Lett. 342, 91-96
7. Schnaar, R. L., Suzuki, A., and Stanley, P. (2009) Glycosphingolipids. in Essentials of Glycobiology, 2nd Ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
8. Chalat, M., Menon, I., Turan, Z., and Menon, A. K. (2012) Reconstitution of glucosylceramide flip-flop across endoplasmic reticulum. Implications for mechanism of glycosphingolipid biosynthesis. J. Biol. Chem. 287, 15523-15532
9. Halter, D., Neumann, S., Van Dijk, S. M., Wolthoorn, J., De Mazière, A. M., Vieira, O. V., Mattjus, P., Klumperman, J., Van Meer, G., and Sprong, H. (2007) Pre-and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J. Cell Biol. 179, 101-115
10. D'Angelo, G., Polishchuk, E., Di Tullio, G., Santoro, M., Di Campli, A., Godi, A., West, G., Bielawski, J., Chuang, C. C., Van der Spoel, A. C., Platt, F. M., Hannun, Y. A., Polishchuk, R., Mattjus, P., and De Matteis, M. A. (2007) Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide. Nature 449, 62-67
11. De Graaf, M., Van Veen, I. C., Van der Meulen-Muileman, I. H., Gerritsen, W. R., Pinedo, H. M., and Haisma, H. J. (2001) Cloning and characterization of human liver cytosolic β-glycosidase. Biochem. J. 356, 907-910
12. Hayashi, Y., Okino, N., Kakuta, Y., Shikanai, T., Tani, M., Narimatsu, H., and Ito, M. (2007) Klotho-related protein is a novel cytosolic neutral β-glycosylceramidase. J. Biol. Chem. 282, 30889-30900
13. Van Weely, S., Brandsma, M., Strijland, A., Tager, J. M., and Aerts, J. M. (1993) Demonstration of the existence of a second, non-lysosomal glucocerebrosidase that is not deficient in Gaucher disease. Biochim. Biophys. Acta 1181, 55-62
14. Yahata, K., Mori, K., Arai, H., Koide, S., Ogawa, Y., Mukoyama, M., Sugawara, A., Ozaki, S., Tanaka, I., Nabeshima, Y., and Nakao, K. (2000) Molecular cloning and expression of a novel klotho-related protein. J. Mol. Med. 78, 389-394
15. Yildiz, Y., Matern, H., Thompson, B., Allegood, J. C., Warren, R. L., Ramirez, D. M., Hammer, R. E., Hamra, F. K., Matern, S., and Russell, D. W. (2006) Mutation of β-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J. Clin. Invest. 116, 2985-2994
16. Matern, H., Heinemann, H., Legler, G., and Matern, S. (1997) Purification and characterization of a microsomal bile acid β-glucosidase from human liver. J. Biol. Chem. 272, 11261-11267
17. Brady, R. O., Kanfer, J. N., and Shapiro, D. (1965) Metabolism of glucocerebrosides. II. Evidence of an Enzymatic Deficiency in Gaucher's Disease. Biochem. Biophys. Res. Commun. 18, 221-225
18. Hruska, K. S., La Marca, M. E., Scott, C. R., and Sidransky, E. (2008) Gaucher disease. Mutation and polymorphism spectrum in the glucocerebrosidase gene (GBA). Hum. Mutat. 29, 567-583
19. Boot, R. G., Verhoek, M., Donker-Koopman, W., Strijland, A., Van Marle, J., Overkleeft, H. S., Wennekes, T., and Aerts, J. M. (2007) Identification of the non-lysosomal glucosylceramidase as β-glucosidase 2. J. Biol. Chem. 282, 1305-1312
20. Matern, H., Boermans, H., Lottspeich, F., and Matern, S. (2001) Molecular cloning and expression of human bile acid β-glucosidase. J. Biol. Chem. 276, 37929-37933
21. Gonzalez-Carmona, M. A., Sandhoff, R., Tacke, F., Vogt, A., Weber, S., Canbay, A. E., Rogler, G., Sauerbruch, T., Lammert, F., and Yildiz, Y. (2012) β-Glucosidase 2 knockout mice with increased glucosylceramide show impaired liver regeneration. Liver. Int. 32, 1354-1362
22. Tybulewicz, V. L., Tremblay, M. L., La Marca, M. E., Willemsen, R., Stubblefield, B. K., Winfield, S., Zablocka, B., Sidransky, E., Martin, B. M., and Huang, S. P. (1992) Animal model of Gaucher's disease from targeted disruption of the mouse glucocerebrosidase gene. Nature 357, 407-410
23. Lorenz, H, Hailey, D. W., and Lippincott-Schwartz, J. (2006) Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat. Methods 3, 205-210
24. Korschen, H. G., Beyermann, M., Müller, F., Heck, M., Vantler, M., Koch, K. W., Kellner, R., Wolfrum, U., Bode, C., Hofmann, K. P., and Kaupp, U. B. (1999) Interaction of glutamic-acid-rich proteins with the cGMP signalling pathway in rod photoreceptors. Nature 400, 761-766
25. Cook, N. J., Zeilinger, C, Koch, K. W., and Kaupp, U. B. (1986) Solubilization and functional reconstitution of the cGMP-dependent cation channel from bovine rod outer segments. J. Biol. Chem. 261, 17033-17039
26. Ben-Yoseph, Y., and Nadler, H. L. (1978) Pitfalls in the use of artificial substrates for the diagnosis of Gaucher's disease. J. Clin. Pathol. 31, 1091-1093
27. Robinson, D. (1956) The fluorimetric determination of β-glucosidase. Its occurrence in the tissues of animals, including insects. Biochem. J. 63, 39-44
28. Fujiki, Y., Hubbard, A. L., Fowler, S., and Lazarow, P. B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment. Application to endoplasmic reticulum. J. Cell Biol. 93, 97-102
29. Ho, M. W., and O'Brien, J. S. (1971) Gaucher's disease. Deficiency of "acid"-glucosidase and reconstitution of enzyme activity in vitro. Proc. Natl. Acad. Sci. U. S. A. 68, 2810-2813
30. Turner, B. M., Beratis, N. G., and Hirschhorn, K. (1977) Cell-specific differences in membrane β-glucosidase from normal and Gaucher cells. Biochim. Biophys. Acta 480, 442-449
31. Legler, G. (1977) Glucosidases. Methods Enzymol. 46, 368-381
32. Overkleeft, H. S., Renkema, G. H., Neele, J., Vianello, P., Hung, I. O., Strijland, A., Van der Burg, A. M., Koomen, G. J., Pandit, U. K., and Aerts, J. M. (1998) Generation of specific deoxynojirimycin-type inhibitors of the non-lysosomal glucosylceramidase. J. Biol. Chem. 273, 26522-26527
33. Turner, B. M., and Hirschhorn, K. (1978) Properties of β-glucosidase in cultured skin fibroblasts from controls and patients with Gaucher disease. Am. J. Hum. Genet. 30, 346-358
34. Huitema, K., Van Den Dikkenberg, J., Brouwers, J. F., and Holthuis, J. C. (2004) Identification of a family of animal sphingomyelin synthases. EMBOJ. 23, 33-44
35. Yeang, C, Varshney, S., Wang, R., Zhang, Y., Ye, D., and Jiang, X. C (2008) The domain responsible for sphingomyelin synthase (SMS) activity. Biochim. Biophys. Acta 1781, 610-617
36. Reczek, D., Schwake, M., Schroder, J., Hughes, H., Blanz, J., Jin, X., Brondyk, W., Van Patten, S., Edmunds, T., and Saftig, P. (2007) LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of beta-glucocerebrosidase. Cell 131, 770-783
37. Vaccaro, A. M., Tatti, M., Ciaffoni, F., Salvioli, R., Serafino, A., and Barca, A. (1994) Saposin C induces pH-dependent destabilization and fusion of phosphatidylserine-containing vesicles. FEBS Lett. 349, 181-186
38. Neufeld, E. F. (1991) Lysosomal storage diseases. Annu. Rev. Biochem. 60, 257-280
39. Germain, D. P., Puech, J. P., Caillaud, C, Kahn, A., and Poenaru, L. (1998) Exhaustive screening of the acid β-glucosidase gene, by fluorescence-assisted mismatch analysis using universal primers. Mutation profile and genotype/phenotype correlations in Gaucher disease. Am. J. Hum. Genet. 63, 415-427
40. Lachmann, R. H, Grant, I. R., Halsall, D., and Cox, T. M. (2004) Twin pairs showing discordance of phenotype in adult Gaucher's disease. QJM 97, 199-204
41. Aureli, M., Bassi, R., Loberto, N., Regis, S., Prinetti, A., Chigorno, V., Aerts, J. M., Boot, R. G., Filocamo, M., and Sonnino, S. (2012) Cell surface associated glycohydrolases in normal and Gaucher disease fibroblasts. J. Inherit. Metab. Dis. 35, 1081-1091