Protein C-mannosylation is enzyme-catalysed and uses dolichyl- phosphate-mannose as a precursor

Molecular Biology of the Cell

Volumn 9, Issue 2, 1998, Pages 291-300

  Doucey, Marie Agnès ^a   Hess, Daniel ^a   Cacan, René ^b   Hofsteenge, Jan ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DOLICHOL PHOSPHATE MANNOSE; GLYCOSYLTRANSFERASE; MANNOSE; MANNOSYLTRANSFERASE; RIBONUCLEASE; SYNTHETASE; TRYPTOPHAN;

ANIMAL CELL; ARTICLE; CATALYSIS; CHO CELL; CONTROLLED STUDY; ENZYME MECHANISM; ENZYME SPECIFICITY; LIVER MICROSOME; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; RAT;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS;

EID: 0031881719     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.2.291     Document Type: Article

References (35)

1. Abeijon, C., and Hirschberg, C.B. (1992). Topography of glycosylation reactions in the endoplasmic reticulum. Trends Biochem. Sci. 17, 32-36.
2. Alonso, M.D., Lomako, J., Lomako, W.M., and Whelan, W.J. (1995). A new look at the biogenesis of glycogen. FASEB J. 9, 1126-1137.
3. Beck, P.J., Orlean, P., Albright, C., Robbins, P.W., Gething, M.J., and Sambrook, J.F. (1990). The Saccharomyces cerevisiae DPM1 gene doli- chol-phosphate-mannose synthase is able to comlement a glycosy- lation-defective mammalian cell line. Mol. Cell. Biol. 10, 4612-4622.
4. Behrens, N.H., Carminatti, H., Staneloni, R.J., Leloir, L.F., and Cantarella, A.I. (1973). Formation of lipid-bound oligosaccharides con- taining mannose: their role in glycoprotein synthesis. Proc. Natl. Acad. Sci. USA 70, 3390-3394.
5. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Cacan, R., and Verbert, A. (1995). Gycosyltransferases of the phosphodolichol pathways. In: Methods on glycoconjugates, ed. A. Verbert, Chur, Switzerland: Harwood Academic Publishers, 191-199.
7. Chaney, W., Sundaram, S., Friedman, N., and Stanley, P. (1989). The Lec4A CHO glycosylation mutant arises from miscompartmentalization of a Golgi glycosyltransferase. J. Cell Biol. 109, 2089-2096.
8. Chaudhary, N., Freeman, D.J., Rip, J.W., and Carroll, K.K. (1982). Direct estimation of dolichyl phosphate in rat liver by high-pressure liquid chromatography. Lipids 17, 558-560.
9. de Beer, T., Vliegenthart, J.F.G., Löffler, A., and Hofsteenge, J. (1995). The hexopyranosyl residue that is C-glycosidically linked to the side chain of tryptophan-7 in human RNase Us is α-mannopyranose. Biochemistry 34, 11785-11789.
10. DeGasperi, R., Thomas, L.J., Sugiyama, E., Chang, H.M., Beck, P.J., Orlean, P., Albright, C., Waneck, G., Sambrook, J.F., Warren, C.D., and Yeh, E.T.H. (1990). Correction of a defect in mammalian GPI anchor biosynthesis by a transfected yeast gene. Science 250, 988-991.
11. Evans, P.J., and Hemming, F.W. (1973). The unambiguous characterization of dolichol phosphate mannose as a product of mannosyl transferase in pig liver endoplasmic reticulum. FEBS Lett. 31, 335-338.
12. Goochee, C.F., Gramer, M.J., Andersen, D.C., and Bahr, J.B. (1992). The oligosaccharides of glycoproteins: factors affecting their synthesis and their influence on glycoprotein properties. In: Frontiers in bioprocessing II, ed. P. Todd, S.K. Sikdar, and B. Milan, Washington, DC: American Chemical Society, 199-240.
13. Graham, J. (1992). Isolation of subcellular organelles and mebranes. In Centrifugation; a practical approach, ed. Rickwood, D., Oxford: IRL Press, 161-182.
14. Hanover, J.A., Elting, J., Mintz, G.R., and Lennarz, W.J. (1982). Temporal aspects of the N- and O-glycosylation of human chorionic gonadotropin. J. Biol. Chem. 257, 10172-10177.
15. Harlow, E., and Lane, D. (1988). Antibodies. A laboratory manual, Cold Spring Harbor Laboratory.
16. Hofsteenge, J., Müller, D.R., de Beer, T., Löffler, A., Richter, W.J., and Vliegenhart, J.F.G. (1994). New type of linkage between a carbohydrate and a protein: C-glycosylation of a specific tryptophan residue in human RNase Us. Biochemistry 33, 13524-13530.
17. Hofsteenge, J., Löffler, A., Müller, D.R., Richter, W.J., de Beer, T., and Vliegenthart, J.F.G. (1996). Protein C-glycosylation. In: Techniques in protein chemistry VII, ed. D.R. Marshak, New York: Academic Press, 163-171.
18. Kerscher, F., and Franz, G. (1987). Biosynthesis of vitexin and isovitexin: enzymatic synthesis of the C-glucosylflavones vitexin and isovittexin with an enzyme preparation from Fagopyrum esculentum m. seedlings. Z. Naturforsch. 42, 519-524.
19. Kerscher, F., and Franz, G. (1988). Isolation and some properties of an UDP-glucose: 2-hydroxyflavanone-6 (or 8)-C-glucosyltransferase from Fagopyrum esculentum m. cotyledons. J. Plant Physiol. 132, 110-115.
20. Krieg, J., Gläsner, W., Vincentini, A., Doucey, M.-A., Löffler, A., Hess, D., and Hofsteenge, J. (1997a). Protein C-mannosylation is an intracellular process, performed by a variety of cultured cells. J. Biol. Chem. 272, 26687-26692.
21. Krieg, J., Hartmann, S., Vicentini, A., Gläsner, W., Hess, D., and Hofsteenge, J. (1998). Recognition signal for C-mannosylation of Trp-7 in RNase 2 consists of the sequence Trp-Xaa-Xaa-Trp. Mol. Biol. Cell 9, 301-309.
22. Löffler, A., Doucey, M.-A., Jansson, A.M., Müller, D.R., de Beer, T., Hess, D., Meldal, M., Richter, W.J., Vliegenthart, J.F.G., and Hofsteenge, J. (1996). Spectroscopic and protein chemical analyses demonstrate the presence of C-mannosylated tryptophan in intact human RNase 2 and its isoforms. Biochemistry 35, 12005-12014.
23. Mosimann, S.C., Newton, D.L., Youle, R.J., and James, M.N.G. (1996). X-ray crystallographic structure of recombinant eosinophil-derived neurotoxin at 1.83 Å resolution. J. Mol. Biol. 260, 540-552.
24. Oliver, G.J.A., Harrison, J., and Hemming, F.W. (1975). The mannosylation of dolichol-diphosphate oligosaccharides in relation to the formation of oligosaccharides and glycoprteins in pig-liver endoplasmic reticulum. Eur. J. Biochem. 58, 223-229.
25. Pisano, A., Redmond, J.W., Williams, K.L., and Gooley, A.A. (1993). Glycosylation sites identified by solid-phase edman degradation: O-linked glycosylation motifs on human glycophorin A. Glycobiol- ogy 3, 429-435.
26. Rosenwald, A.G., Stoll, J., and Krag, S.S. (1990). Regulation of glycosylation. J. Biol. Chem. 265, 14544-14553.
27. Singh, D.G., Lomako, J., Lomako, W.M., Whelan, W.J., Meyer, H.E., Serwe, M., and Metzger, J.W. (1995). Beta-Glucosylarginine: a new glucose-protein bond in a self-glucosylating protein from sweet corn. FEBS Lett. 376, 61-64.
28. Singh, N., and Tartakoff, A.M. (1991). Two different mutants blocked in synthesis of dolichol-phosphoryl-mannose do not add glycolipid anchors to membrane proteins: quantitative correction of the phenotype of a CHO cell mutant with tunicamycin. Mol. Cell. Biol. 11, 391-400.
29. Stoll, J., Robbins, A.R., and Krag, S.S. (1982). Mutant of Chinese hamster ovary cells with altered mannose 6-phosphate receptor activity is unable to synthesize mannosylphosphoryldolichol. Proc. Natl. Acad. Sci. USA 79, 2296-2300.
30. Stoll, J., Rosenberg, L., Carson, D.D., Lennarz, W.J., and Krag, S.S. (1985). A single enzyme catalyzes the synthesis of the mannosylphosphoryl derivative of dolichol and retinol in rat liver and Chinese hamster ovary cells. J. Biol. Chem. 260, 232-236.
31. Stoll, J., Cacan, R., Verbert, A., and Krag, S.S. (1992). Lec15 cells transfer glucosylated oligosaccharides to protein. Arch. Biochem. Biophys. 299, 225-231.
32. Vicentini, A., Hemmings, B.A., and Hofsteenge, J. (1994). Residues 36-42 of liver RNase PL3 contribute to its uridine-preferring substrate specificity. Protein Sci. 3, 459-466.
33. Waechter, C.J., Lucas, J.J., and Lennarz, W.J. (1973). Membrane glycoproteins. J. Biol. Chem. 248, 7570-7579.
34. Waechter, C.J., and Lennarz, W.J. (1976). The role of polyprenol-linked sugars in glycoprotein synthesis. Annu. Rev. Biochem. 45, 95-111.
35. Wilm, M., and Mann, M. (1996). Analytical properties of the nanoelectrospray ion source. Anal. Chem. 68, 1-8.