Cell wall 1,6-β-glucan synthesis in Saccharomyces cerevisiae depends on ER glucosidases I and II, and the molecular chaperone BiP/Kar2p

EMBO Journal

Volumn 17, Issue 2, 1998, Pages 396-405

  Simons, Jan Fredrik ^a,b   Ebersold, Melanie ^a   Helenius, Ari ^a,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CURAGEN CORPORATION   (United States)

^c ETH ZURICH   (Switzerland)

Author keywords

1,6 glucan; BiP Kar2p; Cell wall synthesis; Endoplasmic reticulum; Glucosidase

Indexed keywords

CASTANOSPERMINE; CHAPERONE; GLUCAN; GLUCOSE; GLUCOSIDASE; OLIGOSACCHARIDE;

ARTICLE; CARBOHYDRATE SYNTHESIS; CELL AGGREGATION; CELL WALL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ALPHA-GLUCOSIDASES; BETA-GLUCANS; CELL WALL; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GLUCANS; HSP70 HEAT-SHOCK PROTEINS; INDOLIZINES; MEMBRANE GLYCOPROTEINS; MUTAGENESIS; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0032518912     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.2.396     Document Type: Article

References (53)

1. Ausubel, F.M. (1994) Current Protocols in Molecular Biology. John Wiley & Sons, Inc., New York.
2. Boone, C., Sommer, S.S., Hensel, A. and Bussey, H. (1990) Yeast KRE genes provide evidence for a pathway of cell wall β-glucan assembly. J. Cell Biol., 110, 1833-1843.
3. Brodsky, J.L. and Schekman, R. (1993) A Sec63p-BiP complex from yeast is required for protein translocation in a reconstituted proteoliposome. J. Cell Biol., 123, 1355-1363.
4. Brown, J.L. and Bussey, H. (1993) The yeast KRE9 gene encodes an O glycoprotein involved in cell surface β-glucan assembly. Mol. Cell. Biol., 13, 6346-6356.
5. Brown, J.L., Roemer, T., Lussier, M., Sdicu, A.-M. and Bussey, H. (1994) The K1 killer toxin: molecular and genetic applications to secretion and cell surface assembly. In Johnston, J.R. (ed.), Molecular Genetics of Yeast. A Practical Approach. IRL Press, Oxford University Press, Oxford, pp. 217-232.
6. Cid, V.J., Duran, A., Del Rey, F., Snyder, M.P., Nombela, C. and Sanchez, M. (1995) Molecular basis of cell integrity and morphogenesis in S. cerevisiae. Microbiol. Rev., 59, 345-386.
7. Degen, E. and Williams, D.B. (1991) Participation of a novel 88-kD protein in the biogenesis of murine class I histocompatibility molecules. J. Cell Biol., 112, 1099-1115.
8. de Nobel, H. and Lipke, P.N. (1994) Is there a role for GPIs in yeast cell-wall assembly? Trends Cell Biol., 4, 42-45.
9. De Virgilio, C., Bürckert, N., Neuhaus, J.-M., Boller, T. and Wiemken, A. (1993) CNE1, a Saccharomyces cerevisiae homologue of the genes encoding mammalian calnexin and calreticulin. Yeast, 9, 185-188.
10. Elbein, A.D. (1991) Glycosidase inhibitors as antiviral and/or antitumor agents. Semin. Cell Biol., 2, 309-317.
11. Esmon, B., Esmon, P.C. and Schekman, R. (1984) Early steps in processing of yeast glycoproteins. J. Biol. Chem., 259, 10322-10327.
12. Fernandez, F.S., Trombetta, S.E., Hellman, U. and Parodi, A.J. (1994) Purification to homogeneity of UDP-glucose:glycoprotein glucosyltransferase from Schizosaccharomyces pombe and apparent absence of the enzyme from Saccharomyces cerevisiae. J. Biol. Chem., 269, 30701-30706.
13. Fernandez, F., Jannatipour, M., Hellman, U., Rokeach, L.A. and Parodi, A. (1996) A new stress protein: synthesis of Schizosaccharomyces pombe UDP-glc:glycoprotein glucosyltransferase mRNA is induced by stress conditions but the enzyme is not essential for viability. EMBO J., 15, 705-713.
14. Flynn, G.C., Pohl, J., Flocco, M.T. and Rothman, J.E. (1991) Peptide-binding specificity of the molecular chaperone BiP. Nature, 353, 726-730.
15. Gaut, J.R. and Hendershot, L.M. (1993) Mutations within the nucleotide binding site of immunoglobulin-binding protein inhibit ATPase activity and interfere with release of immunoglobulin heavy chain. J. Biol. Chem., 268, 7248-7255.
16. Gething, M.-J. and Sambrook, J. (1992) Protein folding in the cell. Nature, 355, 33-45.
17. Haas, I.G. and Wabl, M. (1983) Immunoglobulin heavy chain binding protein. Nature, 306, 387-389.
18. Hammond, C. and Helenius, A. (1993) A chaperone with a sweet tooth. Curr. Biol., 3, 884-885.
19. Hammond, C. and Helenius, A. (1994) Folding of VSV G protein: sequential interaction with BiP and calnexin. Science, 266, 456-458.
20. Hammond, C., Braakman, I. and Helenius, A. (1994) Role of N-linked oligosaccharides, glucose trimming and calnexin during glycoprotein folding in the endoplasmic reticulum. Proc. Natl Acad. Sci. USA, 91, 913-917.
21. Hebert, D.N., Foellmer, B. and Helenius, A. (1995) Glucose trimming and reglucosylation determines glycoprotein association with calnexin. Cell, 81, 425-433.
22. Helenius, A., Tatu, U., Marquardt, T. and Braakman, I. (1992) Protein folding in the endoplasmic reticulum. In Rupp, R.G. and Oka, M.S. (eds), Cell Biology and Biotechnology. Springer Verlag, Berlin, Heidelberg, pp. 125-136.
23. Helenius, A., Trombetta, E.S., Hebert, D.N. and Simons, J.F. (1997) Calnexin, calreticulin and the folding of glycoproteins. Trends Cell Biol., 7, 193-200.
24. Horrisberg, M. and Clerk, M.-F. (1987) Cell wall architecture of a Saccharomyces cerevisiae mutant with a truncated carbohydrate outer chain in the mannoprotein. Eur. J. Cell Biol., 45, 62-71.
25. Horrisberg, M. and Vonlanthen, M. (1977) Localization of mannan and chitin on thin sections of budding yeasts with gold markers. Arch. Microbiol., 115, 1-7.
26. Jiang, B., Sheraton, J., Ram, A.F.J., Dijkgraaf, G.J.P., Klis, F.M. and Bussey, H. (1996) CWH41 encodes a novel endoplasmic reticulum membrane N-glycoprotein involved in β1,6-glucan assembly. J. Bacteriol., 178, 1162-1171.
27. Kalz-Füller, B., Bieberich, E. and Bause, E. (1995) Cloning and expression of glucosidase I from human hippocampus. Eur. J. Biochem., 231, 344-351.
28. Kassenbrock, C.K. and Kelly, R.B. (1989) Interaction of heavy chain binding protein (BiP/GRP78) with adenine nucleotides. EMBO J., 8, 1461-1467.
29. Knittler, M.R. and Haas, I.G. (1992) Interaction of BiP with newly synthesized immunoglobulin light chain molecules: cycles of sequential binding and release. EMBO J., 11, 1573-1581.
30. Kornfeld, R. and Kornfeld, S. (1985) Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem., 54, 631-664.
31. Lu, C.-F., Montijn, R.C., Brown, J.L., Klis, F., Kurjan, J., Bussey, H. and Lipke, P.N. (1995) Glycosyl phosphatidylinositol-dependent cross-linking of α-agglutinin and β1,6-glucan in the Saccharomyces cerevisiae cell wall. J. Cell Biol., 128, 333-340.
32. McKelvy, J. and Lee, Y.C. (1969) Microheterogeneity of the carbohydrate group of Aspergillus oryzae α-amylase. Arch. Biochem. Biophys., 132, 99-110.
33. Meaden, P., Hill, K., Wagner, J., Slipetz, D., Sommer, S.S. and Bussey, H. (1990) The yeast KRE5 gene encodes a probable endoplasmic reticulum protein required for (1-6)-β-D-glucan synthesis and normal cell growth. Mol. Cell. Biol., 10, 3013-3019.
34. Michalak, M., Milner, R.E., Burns, K. and Opas, M. (1992) Calreticulin. Biochem. J., 285, 681-692.
35. Normington, K., Kohno, K., Kozutsumi, Y., Gething, M.-J. and Sambrook, J. (1989) S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell, 57, 1223-1236.
36. Ou, W.-J., Cameron, P.H., Thomas, D.Y. and Bergeron, J.J.M. (1993) Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature, 364, 771-776.
37. Parker, C.G., Fessler, L.I., Nelson, R.E. and Fessler, J.H. (1995) Drosophila UDP-glucose:glycoprotein glucosyltransferase: sequence and characterization of an enzyme that distinguishes between denatured and native proteins. EMBO J., 14, 1294-1303.
38. Parlati, F., Dominguez, M., Bergeron, J.J.M. and Thomas, D.Y. (1995) Saccharomyces cerevisiae CNE1 encodes an endoplasmic reticulum (ER) membrane protein with sequence similarity to calnexin and calreticulin and functions as a constituent of the ER quality control apparatus. J. Biol. Chem., 270, 244-253.
39. 2 occurs in rat liver and Phaseus vulgaris cells. J. Biol. Chem., 259, 6351-6357.
40. Peterson, J.R., Ora, A., Nguyen Van, P. and Helenius, A. (1995) Transient, lectin-like association of calreticulin with folding intermediates of cellular and viral glycoproteins. Mol. Biol. Cell, 6, 1173-1184.
41. Roemer, T., Paravicini, G., Payton, M.A. and Bussey, H. (1994) Characterization of the yeast (1-6)-β-glucan biosynthetic components, Kre6p and Skn1p, and genetic interactions between the PKC1 pathway and extracellular matrix assembly. J. Cell Biol., 127, 567-579.
42. Rose, M.D., Misra, L.M. and Vogel, J.P. (1989) KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell, 57, 1211-1221.
43. Sanders, S.L., Whitfield, K.M., Vogel, J.P., Rose, M.D. and Schekman, R.W. (1992) Sec61 and BiP directly facilitate polypeptide translocation into the ER. Cell, 69, 353-365.
44. Shamu, E.C., Cox, J.S. and Walter, P. (1994) The unfolded-protein-response pathway in yeast. Trends Cell Biol., 4, 56-60.
45. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in S. cerevisiae. Genetics, 122, 19-27.
46. Simons, J.F., Ferro-Novick, S., Rose, M.D. and Helenius, A. (1995) BiP/ Kar2p functions as a molecular chaperone during folding of carboxypeptidase Y in yeast. J. Cell Biol., 130, 41-49.
47. Sousa, M.C., Ferrero-Garcia, M.A. and Parodi, A.J. (1992) Recognition of the oligosaccharide and protein moieties of glucoproteins by the UDP-Glc:glycoprotein glucosyltransferase. Biochemistry, 31, 97-105.
48. Spiro, R.G., Zhu, Q., Bhoyroo, V. and Söling, H.-D. (1996) Definition of the lectin-like properties of the molecular chaperone, calreticulin, and demonstration of its copurification with endomannosidase from rat liver Golgi. J. Biol. Chem., 271, 11588-11594.
49. Trombetta, E.S., Simons, J.F. and Helenius, A. (1996) Endoplasmic reticulum glucosidase II is composed of a catalytic subunit, conserved from yeast to mammals, and a tightly bound noncatalytic HDEL-containing subunit. J. Biol. Chem., 271, 27509-27516.
50. Trombetta, S., Bosch, M. and Parodi, A.J. (1989) Glucosylation of glycoproteins by mammalian, plant, fungal and trypanosomatid protozoa microsomal membranes. Biochemistry, 28, 8108-8116.
51. Vogel, J.P., Misra, L.M. and Rose, M.D. (1990) Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J. Cell Biol., 110, 1885-1895.
52. 2 oligosaccharides as an initial step in recognizing unfolded glycoproteins. J. Biol. Chem., 270, 4697-4704.
53. Zhang, J.-X., Braakman, I., Matlack, K. and Helenius, A. (1997) Quality control in the secretory pathway: the role of calreticulin, calnexin and BiP in the retention of glycoproteins with C-terminal truncations. Mol. Biol. Cell, 8, 1943-1954.