A specific screen for oligosaccharyltransferase mutations identifies the 9 kDa OST5 protein required for optimal activity in vivo and in vitro

EMBO Journal

Volumn 16, Issue 6, 1997, Pages 1164-1172

  Reiss, Gilles ^a   Te Heesen, Stephan ^a   Gilmore, Reid ^b   Zufferey, Romain ^a,c   Aebi, Markus ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Endoplasmic reticulum; Glycosylation; Membrane protein; Oligosaccharyltransferase; Saccharomyces cerevisiae

Indexed keywords

ASPARAGINE; MEMBRANE PROTEIN; MUTANT PROTEIN; OLIGOSACCHARIDE; TRANSFERASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SUBUNIT; GENE LOCUS; GENE MUTATION; GENETIC COMPLEMENTATION; INTRON; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; PROTEIN INTERACTION;

AMINO ACID SEQUENCE; BASE SEQUENCE; CARBOHYDRATE SEQUENCE; CHROMOSOME MAPPING; DNA PRIMERS; DNA, FUNGAL; GENE EXPRESSION; GENES, FUNGAL; GLYCOSYLATION; HEXOSYLTRANSFERASES; INTRONS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; OLIGOSACCHARIDES; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY; SUPPRESSION, GENETIC; TRANSFERASES;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 0030962027     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.6.1164     Document Type: Article

References (62)

1. Allen, S., Naim, H. and Bulleid, N. (1995) Intracellular folding of tissue-type plasminogen activator. Effects of disulfide bond formation on N-linked glycosylation and secretion. J. biol. Chem., 270, 4797-4804.
2. Badet, J. and Jeanloz, R.W. (1988) Isolation and partial purification of lipid-linked oligosaccharides from calf pancreas. Carbohydr. Res., 178, 49-65.
3. Ballou, L., Gopal, P., Krummel, B., Tammi, M. and Ballou, C.E. (1986) A mutation that prevents glucosylation of the lipid-linked oligosaccharide precursor leads to underglycosylation of secreted invertase. Proc. Natl Acad. Sci. USA, 83, 3081-3085.
4. Baudin, A., Ozier-Kalogeropoulos, O., Denouel, A., Lacroute, F. and Cullin, C. (1993) A simple and efficient method for direct gene deletion in S.cerevisiae. Nucleic Acids Res., 21, 3329-3330.
5. Bause, E. (1984) Model studies on N-glycosylation of proteins. Biochem. Soc. Trans., 12, 514-517.
6. Boeke, J., LaCroute, F. and Fink, G. (1984) A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5FOA resistance. Mol. Gen. Genet., 197, 345-346.
7. Breuer, W. and Bause, E. (1995) Oligosaccharyl transferase is a constitutive component of an oligomeric protein complex from pig liver endoplasmic reticulum. Eur. J. Biochem., 228, 689-696.
8. Chi, J.H., Roos, J. and Dean, N. (1996) The OST4 gene of Saccharomyces cerevisiae encodes an unusually small protein required for normal levels of oligosaccharyltransferase activity. J. Biol. Chem., 271, 3132-3140.
9. Das, R.C. and Heath, E.C. (1980) Dolichyldiphosphoryloligosaccharide-protein oligosaccharyltransferase; solubilization, purification and properties. Proc. Natl Acad. Sci. USA, 77, 3811-3815.
10. Fiedler, K. and Simons, K. (1995) The role of N-glycans in the secretory pathway. Cell, 81, 309-312.
11. Finke, K., Plath, K., Panzner, S., Prehn, S., Rapoport, T., Hartmann, E. and Sommer, T. (1996) A second trimeric complex containing homologs of the sec61p complex functions in protein transport across the ER membrane of S.cerevisiae. EMBO J., 15, 1482-1494.
12. Franzusoff, A., Rothblatt, J. and Schekman, R. (1991) Analysis of polypeptide transit through yeast secretory pathway. Methods Enzymol., 194, 662-674.
13. Gavel, Y. and Van Heinje, G. (1990) Sequence differences between glycosylated and non-glycosylated Asn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Engng, 3, 433-442.
14. Guthrie, C. and Fink, G.R. (1991) Guide to yeast genetics and molecular biology. Methods Enzymol., 194, 1-251.
15. Hasilik, A. and Tanner, W. (1978) Carbohydrate moiety of carboxypeptidase Y and perturbation of its biosynthesis. Eur. J. Biochem., 91, 567-575.
16. Helenius, A. (1994) How N-linked oligosaccharides affect glycoprotem folding in the endoplasmic reticulum. Mol. Biol. Cell, 5, 253-265.
17. Hill, J.E., Myers, A.M., Koerner, T.J. and Tzagaloff, A. (1986) Yeast/E.coli shuttle vectors with multiple unique restriction sites. Yeast, 2, 163-168.
18. Hill, K.J. and Stevens, T.H. (1994) Vma21p is a yeast membrane protein retained in the endoplasmic reticulum by a di-lysine motif and is required for the assembly of the vacuolar H(+)-ATPase complex. Mol. Biol. Cell, 5, 1039-1050.
19. Holst, B., Bruun, A., Killand-Brandt, M. and Winther, J. (1996) Competition between folding and glycosylation in the endoplasmic reticulum. EMBO J., 15, 3538-3546.
20. Huffaker, T.C. and Robbins, P.W. (1983) Yeast mutants deficient in protein glycosylation. Proc. Natl Acad. Sci. USA, 80, 7466-7470.
21. Iwata, S., Ostermeier, C., Ludwig, B. and Michel, H. (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from P.denitrificans. Nature, 376, 660-669.
22. Kalies, K.U. and Hartmann, E. (1996) Membrane topology of the 12- and the 25-kD subunits of the mammalian signal peptidase complex. J. Biol. Chem., 271, 3925-3929.
23. Karaoglu, D., Kelleher, D.J. and Gilmore, R. (1995) Functional characterization of Ost3p. Loss of the 34-kD subunit of the Saccharomyces cerevisiae oligosaccharyltransferase results in biased underglycosylation of acceptor substrates. J. Cell Biol., 130, 567-577.
24. Kassenbrock, C., Cao, W. and Douglas, M. (1993) Genetic and biochemical characterization of ISP6, a small mitochondrial outer membrane protein associated with the protein translocation complex. EMBO J., 12, 3023-3034.
25. Kelleher, D.J. and Gilmore, R. (1994) The Saccharomyces cerevisiae oligosaccharyltransferase is a protein complex composed of Wbp1p, Swp1p and four additional polypeptides. J. Biol. Chem., 269, 12908-12917.
26. Kelleher, D.J., Kreibich, G. and Gilmore, R. (1992) Oligosaccharyltransferase activity is associated with a protein complex composed of ribophorin I and II and a 48 kDa protein. Cell, 69, 55-65.
27. Kendall, R., Yamada, R. and Bradshaw, R. (1990) Cotranslational aminoterminal processing. Methods Enzymol., 185, 398-407.
28. Knauer, R. and Lehle, L. (1994) The N-oligosaccharyltransferase complex from yeast. FEBS Lett., 344, 83-86.
29. Kornfeld, R. and Kornfeld, S. (1985) Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem., 54, 631-664.
30. Kranz, J.E. and Holm, C. (1990) Cloning by function: an alternative approach for identifying yeast homologs of genes from other organisms. Proc. Natl Acad. Sci. USA, 87, 6629-6633.
31. Kumar, V., Heinemann, F.S. and Ozols, J. (1994) Purification and characterization of avian oligosaccharyltransferase. J. Biol. Chem., 269, 13451-13457.
32. Kyte, J. and Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol., 157, 105-132.
33. Lawrence, C.L. (1991) Guide to yeast genetics and molecular biology. Methods Enzymol., 194, 273-278.
34. Parker, R. and Guthrie, C. (1985) A point mutation in the conserved hexanucleotide at a yeast 5′ splice junction uncouples recognition, cleavage and ligation. Cell, 41, 107-118.
35. Pathak, R., Hendrickson, T.L. and Imperiali, B. (1995) Sulfhydryl modification of the yeast Wbp1p inhibits oligosaccharyl transferase activity. Biochemistry, 34, 4179-4185.
36. Pless, D. and Lennarz, W. (1977) Enzymatic conversion of proteins to glycoproteins. Proc. Natl Acad. Sci. USA, 74, 134-138.
37. Rose, M., Winston, F. and Hieter, P. (1990) Methods in Yeast Genetics: A Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Rost, B., Casadio, R., Foriselli, P. and Sander, C. (1995) Transmembrane helices predicted at 95% accuracy. Protein Sci., 4, 521-533.
39. Runge, K.W., Huffaker, T.C. and Robbins, P.W. (1984) Two yeast mutations in glucosylation steps of the asparagine glycosylation pathway. J. Biol. Chem., 259, 412-417.
40. Sailer, A. and Weissmann, C. (1991) A sensitive and rapid protein assay impervious to detergents. Technique. 3, 37-38.
41. Sathe, G.M., Obrien, S., McLaughlin, M., Watson, F. and Livi, G.P. (1991) Use of polymerase chain reaction for rapid detection of gene insertions in whole yeast cells. Nucleic Acids Res., 19, 4475.
42. Sharma, C.B., Lehle, L. and Tanner, W. (1981) N-Glycosylation of yeast proteins, characterization of the solubilized oligosaccharyl transferase. Eur. J. Biochem., 116, 101-108.
43. Silberstein, S. and Gilmore, R. (1996) Biochemistry, molecular biology and genetics of the oligosaccharyltransferase. FASEB J., 10, 849-858.
44. Silberstein, S., Kelleher, D. and Gilmore, R. (1992) The 48 kDa subunit of the mammalian oligosaccharyltransferase complex is homologous to the essential yeast protein WPB1. J. Biol. Chem., 267, 23658-23663.
45. Silberstein, S., Collins, P., Kelleher, D., Rapiejko, P. and Gilmore, R. (1995a) The a subunit of the S.cererisiae oligosaccharyltransferase complex is essential for vegetative growth of yeast and is homologous to mammalian ribophorin I. J. Cell Biol. 128, 525-536.
46. Silberstein, S., Collins, P., Kelleher, D. and Gilmore, R. (1995b) The essential OST2 gene encodes the 16 kDa subunit of yeast oligosaccharyltransferase, a highly conserved protein expressed in diverse eukaryotic organisms. J. Cell Biol., 131, 371-383.
47. Spiess, M. (1995) Heads or tails - what determines the orientation of proteins in the membrane. FEBS Lett., 369, 76-79.
48. Spiro, M.J., Spiro, R.G. and Bhoyroo, V.D. (1976) Lipid-saccharide intermediates in glycoprotein biosynthesis. II. Studies on the structure of an oligosaccharide-lipid from thyroid. J. Biol. Chem., 251. 6409-6419.
49. Stagljar, I., te Heesen, S. and Aebi, M. (1994) New phenotype of mutations deficient in glucosylation of the lipid-linked oligosaccharide: cloning of the ALG8 locus. Proc. Natl Acad. Sci. USA, 91, 5977-5981.
50. Struhl, K. and Davis, R.W. (1981) Transcription of the HIS3 gene region in S.cerevisiae. J. Mol. Biol., 152, 535-552.
51. te Heesen, S., Janetzky, B., Lehle, L. and Aebi, M. (1992) The yeast WBP1 is essential for oligosaccharyltransferase activity in vivo and in vitro. EMBO J., 11, 2071-2075.
52. te Heesen, S., Knauer, R., Lehle, L. and Aebi, M. (1993) Yeast Wbp1p and Swp1p form a protein complex essential for oligosaccharyltransferase activity. EMBO J., 12, 279-284.
53. te Heesen, S., Lehle, L., Weissmann, A. and Aebi, M. (1994) Isolation of the ALG5 locus, encoding the UDP-glucose:dolichyl phosphate glucosyltransferase from Saccharomyces cerevisiae. Eur. J. Biochem., 224, 71-79.
54. Trimble, R.B., Byrd, J.C. and Maley, F. (1980) Effect of glucosylation of lipid intermediates on oligosaccharide transfer in solubilized microsomes from Saccharomyces cerevisiae. J. Biol. Chem., 255, 11892-11895.
55. Varki, A. (1993) Biological roles of oligosaccharides: all of the theories are correct. J. Biol. Chem., 255, 97-130.
56. Vijayraghavan, U., Company, M. and Abelson, J. (1989) Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev., 3, 1206-1216.
57. Wieland, F., Gleason, M., Serafini, T. and Rothman, J. (1987) The rate of bulk flow from the endoplasmic reticulum to the cell surface. Cell, 50, 289-300.
58. Wimmer, C., Doye, V., Grandi, P., Nehrbass, U. and Hurt, E. (1992) A new subclass of nucleoporins that functionally interact with nuclear pore protein NSP1. EMBO J., 11, 5051-5061.
59. Winther, J.R., Stevens, T.H. and Kielland Brandt, M.C. (1991) Yeast carboxypeptidase Y requires glycosylation for efficient intracellular transport, but not for vacuolar sorting, in vivo stability, or activity. Eur. J. Biochem., 197, 681-689.
60. Woolford, J. (1989) Nuclear pre-mRNA splicing in yeast. Yeast, 5, 439-457.
61. Yu, Y., Sabatini, D. and Kreibich, G. (1990) Antiribophorin antibodies inhibit the targeting to the ER membrane of ribosomes containing secretory polypeptides. J. Cell Biol., 111, 1335-1342.
62. Zufferey, R., Knauer, R., Burda, P., Stagljar, I., te Heesen, S., Lehle, L. and Aebi, M. (1995) STT3, a highly conserved protein required for yeast oligosaccharyl transferase activity in vivo. EMBO J., 14, 4949-4960.