An N-acetylglucosaminyltransferase of the Golgi apparatus of the yeast Saccharomyces cerevisiae that can modify N-linked glycans

Glycobiology

Volumn 13, Issue 8, 2003, Pages 581-589

  Yoko o, Takehiko ^a,b   Wiggins, Christine A R ^a   Stolz, Jürgen ^a,c   Peak Chew, Sew Y ^a   Munro, Sean ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Glycosylation; GNT1; Golgi; N acetylglucosaminyltransferase; Yeast

Indexed keywords

GLYCAN; HEXOSAMINE; LECTIN; LYSOZYME; N ACETYLGLUCOSAMINE; N ACETYLGLUCOSAMINYLTRANSFERASE; URIDINE DIPHOSPHATE N ACETYLGALACTOSAMINE;

ARTICLE; CARBOHYDRATE ANALYSIS; CELL GROWTH; CELL WALL; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL STRAIN; GENE DELETION; GENETIC CODE; GLYCOSYLATION; GOLGI COMPLEX; IN VITRO STUDY; LECTIN BINDING; MASS SPECTROMETRY; MUTANT; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REPORTER GENE; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; GENE DELETION; GLYCOSYLATION; GOLGI APPARATUS; MASS SPECTROMETRY; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MURAMIDASE; N-ACETYLGLUCOSAMINYLTRANSFERASES; OPEN READING FRAMES; POLYSACCHARIDES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EUKARYOTA; FUNGI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0042697170     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/cwg063     Document Type: Article

References (63)

1. Abeijon, C., Yanagisawa, K,, Mandon, E.C., Hausler, A., Moremen, K., Hirschberg, C.B., and Robbins, P.W. (1993) Guanosine diphosphatase is required for protein and sphingolipid glycosylation in the Golgi lumen of Saccharomyces cerevisiae. J. Cell Biol., 122, 307-323.
2. Aebi, M. and Hennet, T. (2001) Congenital disorders of glycosylation: genetic model systems lead the way. Trends Cell Biol., 11, 136-141.
3. Alvarado, E., Ballou, L., Hernandez, L.M., and Ballou, C.E. (1990) Localization of α1-3-linked mannoses in the N-linked oligosaccharides of Saccharomyces cerevisiae mnn mutants. Biochemistry, 29, 2471-2482.
4. 2+-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell, 3, 633-654.
5. Ballou, L., Hernandez, L.M., Alvarado, E., and Ballou, C.E. (1990) Revision of the oligosaccharide structures of yeast carboxypeptidase Y. Proc. Natl Acad. Sci. USA, 87, 3368-3372.
6. Ballou, L., Hitzeman, R.A., Lewis, M.S., and Ballou, C.E. (1991) Vanadate-resistant yeast mutants are defective in protein glycosylation. Proc. Natl Acad. Sci. USA, 88, 3209-3212.
7. Bretthauer, R.K. and Castellino, F.J. (1999) Glycosylation of Pichia pastoris-derived proteins. Biotechnol. Appl. Biochem., 30, 193-200.
8. Dean, N. (1995) Yeast glycosylation mutants are sensitive to aminoglycosides. Proc. Natl Acad. Sci. USA, 92, 1287-1291.
9. Dean, N. (1999) Asparagine-linked glycosylation in the yeast Golgi. Biochim. Biophys. Acta, 1426, 309-322.
10. Dean, N., Zhang, Y.B., and Poster, J.B. (1997) The VRG4 gene is required for GDP-mannose transport into the lumen of the Golgi in the yeast, Saccharomyces cerevisiae. J. Biol. Chem., 272, 31908-31914.
11. Doering, T.L. (1999) A unique alpha-1,3 mannosyltransferase of the pathogenic fungus Cryptococcus neoformans. J. Bacteriol., 181, 5482-5488.
12. Gao, X.D., Kaigorodov, V., and Jigami, Y. (1999) YND1, a homologue of GDA1, encodes membrane-bound apyrase required for Golgi N- and O-glycosylation in Saccharomyces cerevisiae. J. Biol. Chem., 274, 21450-21456.
13. Gibbons, B.J., Roach, P.J., and Hurley, T.D. (2002) Crystal structure of the autocatalytic initiator of glycogen biosynthesis, glycogenin. J. Mol. Biol., 319, 463-477.
14. Guillen, E., Abeijon, C., and Hirschberg, C.B. (1999) The genes for the Golgi apparatus N-acetylglucosaminyltransferase and the UDP-N-acetylglucosamine transporter are contiguous in Kluyveromyces lactis. J. Biol. Chem., 274, 6641-6646.
15. Heinemeyer, W., Kleinschmidt, J.A., Saidowsky, J., Escher, C., and Wolf, D.H. (1991) Proteinase yscE, the yeast proteasome/multicatalytic-multifunctional proteinase: mutants unravel its function in stress induced proteolysis and uncover its necessity for cell survival. EMBO J., 10, 555-562.
16. Hernandez, L.M., Ballou, L., Alvarado, E., Tsai, P.K., and Ballou, C.E. (1989) Structure of the phosphorylated N-linked oligosaccharides from the mnn9 and mnn10 mutants of Saccharomyces cerevisiae. J. Biol. Chem., 264, 13648-13659.
17. Hernandez, L.M., Olivero, I., Alvarado, E., and Larriba, G. (1992) Oligosaccharide structures of the major exoglucanase secreted by Saccharomyces cerevisiae. Biochemistry, 31, 9823-9831.
18. Herscovics, A. (1999) Processing glycosidases of Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1426, 275-285.
19. Immervoll, T., Gentzsch, M., and Tanner, W. (1995) PMT3 and PMT4, two new members of the protein-O-mannosyltransferase gene family of Saccharomyces cerevisiae. Yeast, 11, 1345-1351.
20. Ip, C.C., Miller, W.J., Kubek, D.J., Strang, A.M., van Halbeek, H., Piesecki, S.J., and Alhadeff, J.A. (1992) Structural characterization of the N-glycans of a recombinant hepatitis B surface antigen derived from yeast. Biochemistry, 31, 285-295.
21. Jakob, C.A., Burda, P., Roth, J., and Aebi, M. (1998) Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J. Cell Biol., 142, 1223-1233.
22. Jungmann, J. and Munro, S. (1998) Multi-protein complexes in the cis Golgi of Saccharomyces cerevisiae with α-1,6-mannosyltransferase activity. EMBO J., 17, 423-434.
23. Jungmann, J., Rayner, J.C., and Munro, S. (1999) The Saccharomyces cerevisiae protein Mnn10p/Bed1p is a subunit of a Golgi mannosyltransferase complex. J. Biol. Chem., 274, 6579-6585.
24. Kalidas, C., Joshi, L., and Batt, C. (2001) Characterization of glycosylated variants of β-lactoglobulin expressed in Pichia pastoris. Protein Eng., 14, 201-207.
25. Kang, H.A., Sohn, J.H., Choi, E.S., Chung, B.H., Yu, M.H., and Rhee, S.K. (1998) Glycosylation of human alpha 1-antitrypsin in Saccharomyces cerevisiae and methylotrophic yeasts. Yeast, 14, 371-381.
26. Kniskern, P.J., Hagopian, A., Burke, P., Schultz, L.D., Montgomery, D.L., Hurni, W.M., Ip, C.Y., Schulman, C.A., Maigetter, R.Z., Wampler, D.E., and others. (1994) Characterization and evaluation of a recombinant hepatitis B vaccine expressed in yeast defective for N-linked hyperglycosylation. Vaccine, 12, 1021-1025.
27. Kobayashi, M., Ban, J., Asano, T., Utsunomiya, M., Kusumoto, S., Nishi, K., and Kato, K. (1992) The oligosaccharides in a recombinant hepatitis B virus surface antigen (HBsAg) carrying the pre-S2 region derived from yeast. FEBS Lett., 302, 129-132.
28. Kuster, B., Wheeler, S.F., Hunter, A.P., Dwek, R.A., and Harvey, D.J. (1997) Sequencing of N-linked oligosaccharides directly from protein gels: in-gel deglycosylation followed by matrix-assisted laser desorption/ionization mass spectrometry and normal-phase high-performance liquid chromatography. Anal. Biochem., 250, 82-101.
29. Kuster, B., Hunter, A.P., Wheeler, S.F., Dwek, R.A., and Harvey, D.J. (1998) Structural determination of N-linked carbohydrates by matrix-assisted laser desorption/ionization-mass spectrometry following enzymatic release within sodium dodecyl sulphate-polyacrylamide electrophoresis gels: application to species-specific glycosylation of alpha1-acid glycoprotein. Electrophoresis, 19, 1950-1959.
30. Lehle, L., Cohen, R.E., and Ballou, C.E. (1979) Carbohydrate structure of yeast invertase. Demonstration of a form with only core oligosaccharides and a form with completed polysaccharide chains. J. Biol. Chem., 254, 12209-12218.
31. Levine, T.P., Wiggins, C.A., and Munro, S. (2000) Inositol phosphorylceramide synthase is located in the Golgi apparatus of Saccharomyces cerevisiae. Mol. Biol. Cell, 11, 2267-2281.
32. Lopez-Avalos, M.D., Uccelletti, D., Abeijon, C., and Hirschberg, C.B. (2001) The UDPase activity of the Kluyveromyces lactis Golgi GDPase has a role in uridine nucleotide sugar transport into Golgi vesicles. Glycobiology, 11, 413-422.
33. Lussier, M., Sdicu, A.M., Ketela, T., and Bussey, H. (1995) Localization and targeting of the Saccharomyces cerevisiae Kre2p/Mnt1p α1,2-mannosyltransferase to a medial-Golgi compartment. J. Cell Biol., 131, 913-927.
34. Lussier, M., Sdicu, A.M., and Bussey, H. (1999) The KTR and MNN1 mannosyltransferase families of Saccharomyces cerevisiae. Biochim. Biophys. Acta, 1426, 323-334.
35. Maras, M., van Die, I., Contreras, R., and van den Hondel, C.A. (1999) Filamentous fungi as production organisms for glycoproteins of biomedical interest. Glycoconj. J., 16, 99-107.
36. McAleer, W.J., Buynak, E.B., Maigetter, R.Z., Wampler, D.E., Miller, W.J., and Hilleman, M.R. (1984) Human hepatitis B vaccine from recombinant yeast. Nature, 307, 178-180.
37. Montesino, R., Garcia, R., Quintero, O., and Cremata, J.A. (1998) Variation in N-linked oligosaccharide structures on heterologous proteins secreted by the methylotrophic yeast Pichia pastoris. Protein Expr. Purif., 14, 197-207.
38. Munro, S. (2001) What can yeast tell us about N-linked glycosylation in the Golgi apparatus? FEBS Lett., 498, 223-227.
39. Murphy, K.P. Jr., Gagne, P., Pazmany, C., and Moody, M.D. (1998) Expression of human interleukin-17 in Pichia pastoris: purification and characterization. Protein Expr. Purif., 12, 208-214.
40. Nakamura, S., Takasaki, H., Kobayashi, K., and Kato, A. (1993) Hyperglycosylation of hen egg white lysozyme in yeast. J. Biol. Chem., 268, 12706-12712.
41. Nakanishi-Shindo, Y., Nakayama, K.I., Tanaka, A., Toda, Y., and Jigami, Y. (1993) Structure of the N-linked oligosaccharides that show the complete loss of alpha-1,6-polymannose outer chain from och1, och1 mnn1, and och1 mnn1 alg3 mutants of Saccharomyces cerevisiae. J. Biol. Chem., 268, 26338-26345.
42. Napier, R.M., Fowke, L.C., Hawes, C., Lewis, M., and Pelham, H.R.B. (1992) Immunological evidence that plants use both HDEL and KDEL for targeting proteins to the endoplasmic reticulum. J. Cell Sci., 102, 261-271.
43. Olivero, I., Manas, P., and Hernandez, L.M. (2000) The mnn2 mutant of Saccharomyces cerevisiae is affected in phosphorylation of N-linked oligosaccharides. FEBS Lett., 475, 111-116.
44. Orlean, P. (1997) Biogenesis of yeast wall and surface components. In Pringle, J.R., Broach, J.R., and others (Eds), The molecular and cellular biology of the yeast Saccharomyces cerevisiae. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp. 229-362.
45. Peat, S., Turvey, J.R., and Doyle, D. (1961) The polysaccharides of baker's yeast. Part V. A further study of the mannan. J. Chem. Soc., 3918-3923.
46. Ram, A.F.J., Wolters, A., Tenhoopen, R., and Klis, F.M. (1994) A new approach for isolating cell wall mutants in Saccharomyces cerevisiae by screening for hypersensitivity to calcofluor white. Yeast, 10, 1019-1030.
47. Rayner, J.C. and Munro, S. (1998) Identification of the MNN2 and MNN5 mannosyltransferases required for forming and extending the mannose branches of the outer chain mannans of Saccharomyces cerevisiae. J. Biol. Chem., 273, 26836-26843.
48. Robinson, J.S., Klionsky, D.J., Banta, L.M., and Emr, S.D. (1988) Protein sorting in Saccharomyces cerevisiae - isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol., 8, 4936-4948.
49. Roy, S.K., Yoko-o, T., Ikenaga, H., and Jigami, Y. (1998) Functional evidence for UDP-galactose transporter in Saccharomyces cerevisiae through the in vivo galactosylation and in vitro transport assay. J. Biol. Chem., 273, 2583-2590.
50. Roy, S.K., Chiba, Y., Takeuchi, M., and Jigami, Y. (2000) Characterization of yeast Yea4p, a uridine diphosphate-N-acetylglucosamine transporter localized in the endoplasmic reticulum and required for chitin synthesis. J. Biol. Chem., 275, 13580-13587.
51. Scorer, C.A., Buckholz, R.G., Clare, J.J., and Romanos, M.A. (1993) The intracellular production and secretion of HIV-1 envelope protein in the methylotrophic yeast Pichia pastoris. Gene, 136, 111-119.
52. Smith, W.L., Nakajima, T., and Ballou, C.E. (1975) Biosynthesis of yeast mannan. Isolation of Kluyveromyces lactis mannan mutants and a study of the incorporation of N-acetyl-D-glucosamine into the polysaccharide side chains. J. Biol. Chem., 250, 3426-3435.
53. Stolz, J. and Munro, S. (2002) The components of the Saccharomyces cerevisiae mannosyltransferase complex M-Pol I have distinct functions in mannan synthesis. J. Biol. Chem., 277, 44801-44808.
54. Thim, L., Norris, K., Norris, F., Nielsen, P.F., Bjorn, S.E., Christensen, M., and Petersen, J. (1993) Purification and characterization of the trefoil peptide human spasmolytic polypeptide (hSP) produced in yeast. FEBS Lett., 318, 345-352.
55. 1H-NMR spectroscopy. J. Biol. Chem., 261, 9815-9824.
56. 1H NMR spectroscopic study. Glycobiology, 2, 57-75.
57. Tsai, P.K., Frevert, J., and Ballou, C.E. (1984) Carbohydrate structure of Saccharomyces cerevisiae mnn9 mannoprotein. J. Biol. Chem., 259, 3805-3811.
58. Unligil, U.M. and Rini, J.M. (2000) Glycosyltransferase structure and mechanism. Curr. Opin. Struct. Biol., 10, 510-517.
59. Wach, A., Brachat, A., AlbertiSegui, C., Rebischung, C., and Philippsen, P. (1997) Heterologous HIS3 marker and GFP reporter modules for PCR-targeting in Saccharomyces cerevisiae. Yeast, 13, 1065-1075.
60. Whyte, J.R. and Munro, S. (2001) The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev. Cell, 1, 527-537.
61. Wiggins, C.A.R. and Munro, S. (1998) Activity of the yeast MNNI α-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc. Natl Acad. Sci. USA, 95, 7945-7950.
62. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J.D., Bussey, H., and others. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science, 285, 901-906.
63. Zhu, X.P., Wu, S.X., and Letchworth, G.J. (1997) Yeast-secreted bovine herpesvirus type 1 glycoprotein D has authentic conformational structure and immunogenicity. Vaccine, 15, 679-688.