Transport of human lysosomal neuraminidase to mature lysosomes requires protective protein/cathepsin A

EMBO Journal

Volumn 17, Issue 6, 1998, Pages 1588-1597

  Van Der Spoel, Aarnoud ^a   Bonten, Erik ^a   D'Azzo, Alessandra ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Activation; Lysosomes; Neuraminidase; Protective protein; Transport

Indexed keywords

CARBOXYPEPTIDASE C; CELL ENZYME; GLYCOPROTEIN; LYSOSOME ENZYME; SIALIDASE;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; CONTROLLED STUDY; DNA TRANSFECTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME LOCALIZATION; ENZYME SYNTHESIS; FRACTIONATION; GALACTOSIALIDOSIS; GENE MUTATION; HALF LIFE TIME; INTRACELLULAR TRANSPORT; LYSOSOME; LYSOSOME STORAGE DISEASE; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT; SIALIDOSIS;

ANIMALS; BIOLOGICAL TRANSPORT; CARBOXYPEPTIDASE C; CARBOXYPEPTIDASES; CELL FRACTIONATION; COS CELLS; DNA, COMPLEMENTARY; ENZYME ACTIVATION; HUMANS; LYSOSOMES; MOLECULAR WEIGHT; NEURAMINIDASE; PHOSPHORYLATION; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSFECTION;

ANIMALIA;

EID: 0032536852     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.6.1588     Document Type: Article

References (55)

1. Amigorena, S., Drake, J., Webster, P. and Mellman, I. (1994) Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature, 369, 113-120.
2. Bonten, E.J., Galjart, N.J., Willemsen, R., Usmany, M., Vlak, J.M. and d'Azzo, A. (1995) Lysosomal protective protein/cathepsin A: role of the 'linker' domain in catalytic activation. J. Biol. Chem., 270, 26441-26445.
3. Bonten, E., vanderSpoel, A., Fornerod, M., Grosveld, G. and d'Azzo, A. (1996) Characterization of human lysosomal neuraminidase defines the molecular basis of the metabolic storage disorder sialidosis. Genes Dev., 10, 3156-3169.
4. Burmeister, W., Ruigrok, R. and Cusack, S. (1992) The 2.2 Å resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J., 11, 49-56.
5. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol., 7, 2745-2752.
6. Corfield, T. (1992) Bacterial sialidases - roles in pathogenicity and nutrition. Glycobiology, 2, 509-521.
7. D'Agrosa, R. and Callahan, J. (1988) In vitro activation of neuraminidase in the β-galactosidase-neuraminidase-protective protein complex by cathepsin C. Biochem. Biophys. Res. Commun., 157, 770-775.
8. d'Azzo, A., Hoogeveen, A., Reuser, A.J., Robinson, D. and Galjaard, H. (1982) Molecular defect in combined beta-galactosidase and neuraminidase deficiency in man. Proc. Natl Acad. Sci. USA, 79, 4535-4539.
9. d'Azzo, A., Proia, R.L., Kolodny, E.H., Kaback, M.M. and Neufeld, E.F. (1984) Faulty association of alpha-and beta-subunits in some forms of beta-hexosaminidase A deficiency. J. Biol. Chem., 259, 11070-11074.
10. d'Azzo, A., Andria, G., Strisciuglio, P. and Galjaard, H. (1995) Galactosialidosis. In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic and Molecular Bases of Inherited Disease. McGraw Hill Inc., New York, pp. 2825-2838.
11. Fornerod, M. et al. (1995) Relocation of the carboxyterminal part of CAN from the nuclear envelope to the nucleus as a result of leukemia-specific chromosome rearrangements. Oncogene, 10, 1739-1749.
12. Galjart, N.J., Gillemans, N., Harris, A., van der Horst, G.T.J., Verheijen, F.W., Galjaard, H. and d'Azzo, A. (1988) Expression of cDNA encoding the human 'protective protein' associated with lysosomal beta-galactosidase and neuraminidase: homology to yeast proteases. Cell, 54, 755-764.
13. Galjart, N.J., Morreau, H., Willemsen, R., Gillemans, N., Bonten, E.J. and d'Azzo, A. (1991) Human lysosomal protective protein has cathepsin A-like activity distinct from its protective function. J. Biol. Chem., 266, 14754-14762.
14. Gieselmann, V., Pohlmann, R., Hasilik, A. and vonFigura, K. (1983) Biosynthesis and transport of cathepsin D in cultured human fibroblasts. J. Cell Biol., 97, 1-5.
15. Glombitza, G., Becker, E., Kaiser, H. and Sandhoff, K. (1997) Biosynthesis, processing, and intracellular transport of Gm2 activator protein in human epidermal keratinocytes. J. Biol. Chem., 272, 5199-5207.
16. Gluzman, Y. (1981) SV40-transformed simian cells support the replication of early SV40 mutants. Cell, 23, 175-182.
17. Hasilik, A. (1992) The early and late processing of lysosomal enzymes: proteolysis and compartmentation. Experientia, 48, 130-151.
18. Hille-Rehfeld, A. (1995) Mannose 6-phosphate receptors in sorting and transport of lysosomal enzymes. Biochim. Biophys. Acta, 1241, 177-194.
19. Hiraiwa, M., Yamauchi, T., Tsuji, S., Nishizawa, M., Miyatake, T., Oyanagi, K., Ikuta, F. and Uda, Y. (1993) Activation of human lysosomal sialidase. J. Biochem., 114, 901-905.
20. Hogue, B. and Nayak, D. (1992) Synthesis and processing of the influenza virus neuraminidase A type II transmembrane and glycoprotein. Virology, 188, 510-517.
21. Hunziker, W. and Geuze, H. (1996) Intracellular trafficking of lysosomal membrane proteins. BioEssays, 18, 379-389.
22. Isidoro, C., Grassel, S., Baccino, F. and Hasilik, A. (1991) Determination of the phosphorylation, uncovering of mannose 6-phosphate groups and targeting of lysosomal enzymes. Eur. J. Clin. Chem. Clin. Biochem., 29, 165-171.
23. Kleijer, W.J., Geilen, G.C., Janse, H.C., van Diggelen, O.P., Zhou, X.-Y., Galjart, N.J., Galjaard, H. and d'Azzo, A. (1996) Cathepsin A deficiency in galactosialidosis: studies of patients and carriers in 16 families. Pediatr. Res., 39, 1067-1071.
24. Milner, C., Smith, S., Carrillo, M., Taylor, G., Hollinshead, M. and Campbell, R. (1997) Identification of a sialidase encoded in the human major histocompatibility complex. J. Biol. Chem., 272, 4549-4558.
25. Morreau, H., Galjart, N.J., Gillemans, N., Willemsen, R., van der Horst, G.T.J. and d'Azzo, A. (1989) Alternative splicing of beta-galactosidase mRNA generates the classic lysosomal enzyme and a beta-galactosidase-related protein. J. Biol. Chem., 264, 20655-20663.
26. Morreau, H., Galjart, N.J., Willemsen, R., Gillemans, N., Zhou, X.Y. and d'Azzo, A. (1992) Human lysosomal protective protein. Glycosylation, intracellular transport, and association with β-galactosidase in the endoplasmic reticulum. J. Biol Chem., 267, 17949-17956.
27. Pisoni, R., Flickinger, K., Thoene, J. and Christensen, H. (1987) Characterization of carrier-mediated transport systems for small neutral amino acids in human fibroblast lysosomes. J. Biol. Chem., 5, 6010-6017.
28. Proia, R.L., d'Azzo, A. and Neufeld, E.F. (1984) Association of alpha-and beta-subunits during the biosynthesis of beta-hexosaminidase in cultured human fibroblasts. J. Biol. Chem., 259, 3350-3354.
29. Pshezhetsky, A.V. and Potier, M. (1994) Direct affinity purification and supramolecular organization of human lysosomal cathepsin A. Arch. Biochem. Biophys., 313, 64-70.
30. Pshezhetsky, A. and Potier, M. (1996) Association on N-acetylgalactosamine-6-sulfate sulfatase with the multienzyme lysosomal complex of β-galactosidase, cathepsin A, and neuraminidase. J. Biol. Chem., 271, 28359-28365.
31. Pshezhetsky, A. et al. (1997) Cloning, expression and chromosomal mapping of human lysosomal sialidase and characterization of mutations in sialidosis. Nature Genet., 15, 316-320.
32. Reuter, G. and Gabius, H.-J. (1996) Review: sialic acids: structure-analysis-metabolism-occurrence-recognition. Biol. Chem. Hoppe Seyler, 377, 325-342.
33. Rijnboutt, S., Aerts, H.M., Geuze, H.J., Tager, J.M. and Strous, G.J. (1991a) Mannose 6-phosphate-independent membrane association of cathepsin D, glucocerebrosidase, and sphingolipid-activating protein in HepG2 cells. J. Biol. Chem., 266, 4862-4868.
34. Rijnboutt, S., Kal, A., Geuze, H., Aerts, H. and Strous, G. (1991b) Mannose 6-phosphate-independent targeting of cathepsin D to lysosomes in HepG2 cells. J. Biol. Chem., 266, 23586-23592.
35. Roggentin, P., Schauer, R., Hoyer, L. and Vimr, E. (1993) MicroReview: the sialidase superfamily and its spread by horizontal gene transfer. Mol. Microbiol., 9, 915-921.
36. Sabatini, D. and Adesnik, M. (1995) The biogenesis of membranes and organelles. In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds) The Metabolic and Molecular Bases of Inherited Disease. McGraw Hill Inc., New York, pp. 459-553.
37. Saito, M. and Yu, R.K. (1995) Biochemistry and function of sialidases. In Rosenberg, A. (ed.), Biology of the Sialic Acids. Plenum Press, New York, pp. 261-313.
38. Saito, T., Taylor, G. and Webster, R. (1995) Steps in maturation of influenza A virus neuraminidase. J. Virol., 69, 5011-5017.
39. Schauer, R., Kelm, S., Reuter, G., Roggentin, P. and Shaw, L. (1995) Biochemistry and role of sialic acids. In Rosenberg, A. (ed.), Biology of the Sialic Acids. Plenum Press, New York, pp. 7-67.
40. Shimmoto, M., Fukuhara, Y., Itoh, K., Oshima, A., Sakuraba, H. and Suzuki, Y. (1993) Protective protein gene mutations in galactosialidosis. J. Clin. Invest., 91, 2393-2398.
41. M1-gangliosidosis and Morquio B disease. In Scriver, C., Beaudet, A., Sly, W. and Valle, D. (eds), The Metabolic and Molecular Bases of Inherited Disease. McGraw Hill, Inc., New York, pp. 2785-2824.
42. Thomas, G.H. and Beaudet, A.L. (1995) Disorders of glycoprotein degradation and structure: α-mannosidosis, β-mannosidosis, fucosidosis, sialidosis, aspartylglucosaminuria and carbohydrate-deficient glycoprotein syndrome. In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic and Molecular Bases of Inherited Disease. McGraw Hill, Inc., New York, pp. 2529-2561.
43. Tikkanen R., Enoman, N., Riikonen, A., Ikonen, E. and Peltonen, L. (1995) Intracellular sorting of aspartyglucosaminidase: the role of N-linked oligosaccharides and evidence of Man-6-P-independent lysosomal targeting. DNA Cell Biol., 14, 305-312.
44. Tulp, A., Verwoerd, D. and Pieters, J. (1993) Application of an improved density gradient electrophoresis apparatus to the separation of proteins, cells and subcellular organelles. Electrophoresis, 14, 1295-1301.
45. van Diggelen, O.P, Hoogeveen, A.T., Smith, P.J., Reuser, A.J. and Galjaard, H. (1982) Enhanced proteolytic degradation of normal beta-galactosidase in the lysosomal storage disease with combined beta-galactosidase and neuraminidase deficiency. Biochim. Biophys. Acta, 703, 69-76.
46. van Dongen, J.M., Willemsen, R., Ginns, E.I., Sips, H.J., Tager, J.M., Barranger, J.A. and Reuser, A.J. (1985) The subcellular localization of soluble and membrane-bound lysosomal enzymes in I-cell fibroblasts: a comparative immunocytochemical study. Eur. J. Cell Biol., 39, 179-189.
47. Verheijen, F.W., Palmeri, S., Hoogeveen, A.T. and Galjaard, H. (1985) Human placental neuraminidase. Activation, stabilization and association with beta-galactosidase and its protective protein. Eur. J. Biochem., 149, 315-321.
48. Vielhaber, G., Hurwitz, R. and Sandhoff, K. (1996) Biosynthesis, processing, and targeting of sphingolipid activator protein (SAP) precursor in cultured human fibroblasts. J. Biol. Chem., 271, 32438-32446.
49. Vincent, R. and Nadeau, D. (1984) Adjustment of the osmolality of Percoll for the isopycnic separation of cells and cell organelles. Anal. Biochem., 141, 322-328.
50. von Figura, K. and Hasilik, A. (1986) Lysosomal enzymes and their receptors. Annu. Rev. Biochem., 55, 167-193.
51. Wolf, P. and Ploegh, H. (1995) How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway. Annu. Rev. Cell Dev. Biol., 11, 267-306.
52. Yamamoto, Y. and Nishimura, K. (1987) Copurification and separation of beta-galactosidase and sialidase from porcine testis. Int. J. Biochem., 19, 435-442.
53. Zhou, X.Y., Galjart, N.J., Willemsen, R., Gillemans, N., Galjaard, H. and d'Azzo, A. (1991) A mutation in a mild form of galactosialidosis impairs dimerization of the protective protein and renders it unstable. EMBO J., 10, 4041-4048.
54. Zhou, X.Y. et al. (1995) Mouse model for the lysosomal disorder galactosialidosis and correction of the phenotype with over-expressing erythroid precursor cells. Genes Dev., 9, 2623-2634.
55. Zhou, X.-Y., van der Spoel, A., Rottier, R., Hale, G., Willemsen, R., Berry, G.T., Strisciuglio, P., Andria, G. and d'Azzo, A. (1996) Molecular and biochemical analysis of protective protein/cathepsin A mutations: correlation with clinical severity in galactosialidosis. Hum. Mol. Genet., 12, 1977-1987.