Distinct glycan-charged phosphodolichol carriers are required for the assembly of the pentasaccharide N-linked to the Haloferax volcanii S-layer glycoprotein

Molecular Microbiology

Volumn 78, Issue 5, 2010, Pages 1294-1303

  Guan, Ziqiang ^a   Naparstek, Shai ^b   Kaminski, Lina ^b   Konrad, Zvia ^b   Eichler, Jerry ^b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; DOLICHOL PHOSPHATE; GLYCAN; GLYCOPROTEIN; GLYCOSYLTRANSFERASE; ISOPRENE; MANNOSE; MUTANT PROTEIN; PENTASACCHARIDE; PHOSPHATE TRANSPORTER; SUGAR NUCLEOTIDE;

ARCHAEBACTERIUM; ARTICLE; EUKARYOTE; GENE DELETION; HALOFERAX VOLCANII; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN GLYCOSYLATION;

CARRIER PROTEINS; DOLICHOL PHOSPHATES; GLYCOSYLATION; HALOFERAX VOLCANII; MEMBRANE GLYCOPROTEINS; MOLECULAR STRUCTURE; OLIGOSACCHARIDES; POLYSACCHARIDES;

EUKARYOTA; HALOBACTERIA; HALOFERAX VOLCANII;

EID: 78649546006     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07405.x     Document Type: Article

References (34)

1. Abu-Qarn, M., and Eichler, J. (2006) Protein N-glycosylation in Archaea: defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation. Mol Microbiol 61: 511-525.
2. Abu-Qarn, M., Yurist-Doutsch, S., Giordano, A., Trauner, A., Morris, H.R., Hitchen, P., et al. (2007) Haloferax volcanii AglB and AglD are involved in N-glycosylation of the S-layer glycoprotein and proper assembly of the surface layer. J Mol Biol 14: 1224-1236.
3. Abu-Qarn, M., Giordano, A., Battaglia, F., Trauner, A., Morris, H.R., Hitchen, P., et al. (2008) Identification of AglE, a second glycosyltransferase involved in N-glycosylation of the Haloferax volcanii S-layer glycoprotein. J Bacteriol 190: 3140-3146.
4. Burda, P., and Aebi, M. (1999) The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta 1426: 239-257.
5. Calo, D., Kaminski, L., and Eichler, J. (2010) Protein glycosylation in Archaea: sweet and extreme. Glycobiology 20: 1065-1079.
6. Cantagrel, V., Lefeber, D.J., Ng, B.G., Guan, Z., Silhavy, J.L., Bielas, S.L., et al. (2010) SRD5A3 is required for converting polyprenol to dolichol and is mutated in a congenital glycosylation disorder. Cell 142: 1-15.
7. Eichler, J., and Adams, M.W.W. (2005) Posttranslational protein modification in Archaea. Microbiol Mol Biol Rev 69: 393-425.
8. Hartmann, E., and Konig, H. (1989) Uridine and dolichyl diphosphate activated oligosaccharides are intermediates in the biosynthesis of the S-layer glycoprotein of Methanothermus fervidus. Arch Microbiol 151: 274-281.
9. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-1049.
10. Jones, M.B., Rosenberg, J.N., Betenbaugh, M.J., and Krag, S.S. (2009) Structure and synthesis of polyisoprenoids used in N-glycosylation across the three domains of life. Biochim Biophys Acta 1790: 485-494.
11. Kaminski, L., Abu-Qarn, M., Guan, Z., Naparstek, S., Ventura, V.V., Raetz, C.R.H., et al. (2010) AglJ adds the first sugar of the N-linked pentasaccharide decorating the Haloferax volcanii S-layer glycoprotein. J Bacteriol doi:10.1128/JB.00705-10.
12. Kärcher, U., Schröder, H., Haslinger, E., Allmaier, G., Schreiner, R., Wieland, F., et al. (1993) Primary structure of the heterosaccharide of the surface glycoprotein of Methanothermus fervidus. J Biol Chem 268: 26821-26826.
13. Kuntz, C., Sonnenbichler, J., Sonnenbichler, I., Sumper, M., and Zeitler, R. (1997) Isolation and characterization of dolichol-linked oligosaccharides from Haloferax volcanii. Glycobiology 7: 897-904.
14. Lechner, J., and Wieland, F. (1989) Structure and biosynthesis of prokaryotic glycoproteins. Annu Rev Biochem 58: 173-194.
15. Lechner, J., Wieland, F., and Sumper, M. (1985a) Biosynthesis of sulfated saccharides N-glycosidically linked to the protein via glucose. Purification and identification of sulfated dolichyl monophosphoryl tetrasaccharides from halobacteria. J Biol Chem 260: 860-866.
16. Lechner, J., Wieland, F., and Sumper, M. (1985b) Transient methylation of dolichyl oligosaccharides is an obligatory step in halobacterial sulfated glycoprotein biosynthesis. J Biol Chem 260: 8984-8989.
17. Magidovich, H., Yurist-Doutsch, S., Konrad, Z., Ventura, V.V., Hitchen, P.G., Dell, A., and Eichler, J. (2010) AglP is a S-adenosyl-l-methionine-dependent methyltransferase that participates in the N-glycosylation pathway of Haloferax volcanii. Mol Microbiol 76: 190-199.
18. Mengele, R., and Sumper, M. (1992) Drastic differences in glycosylation of related S-layer glycoproteins from moderate and extreme halophiles. J Biol Chem 267: 8182-8185.
19. Mescher, M.F., and Strominger, J.L. (1978) Glycosylation of the surface glycoprotein of Halobacterium salinarium via a cyclic pathway of lipid-linked intermediates. FEBS Lett 89: 37-41.
20. Mescher, M.F., Hansen, U., and Strominger, J.L. (1976) Formation of lipid-linked sugar compounds in Halobacterium salinarium. Presumed intermediates in glycoprotein synthesis. J Biol Chem 251: 7289-7294.
21. Mevarech, M., and Werczberger, R. (1985) Genetic transfer in Halobacterium volcanii. J Bacteriol 162: 461-462.
22. Plavner, N., and Eichler, J. (2008) Defining the topology of the N-glycosylation pathway in the halophilic archaeon Haloferax volcanii. J Bacteriol 190: 8045-8052.
23. Sprott, G.D., Larocque, S., Cadotte, N., Dicaire, C.J., McGee, M., and Brisson, J.R. (2003) Novel polar lipids of halophilic eubacterium Planococcus H8 and archaeon Haloferax volcanii. Biochim Biophys Acta 1633: 179-188.
24. Sumper, M. (1987) Halobacterial glycoprotein biosynthesis. Biochim Biophys Acta 906: 69-79.
25. Sumper, M., Berg, E., Mengele, R., and Strobel, I. (1990) Primary structure and glycosylation of the S-layer protein of Haloferax volcanii. J Bacteriol 172: 7111-7118.
26. Szymanski, C.M., and Wren, B.W. (2005) Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3: 225-237.
27. Weerapana, E., and Imperiali, B. (2006) Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16: 91R-101R.
28. Wieland, F., Dompert, W., Bernhardt, G., and Sumper, M. (1980) Halobacterial glycoprotein saccharides contain covalently linked sulphate. FEBS Lett 120: 110-114.
29. Wieland, F., Paul, G., and Sumper, M. (1985) Halobacterial flagellins are sulfated glycoproteins. J Biol Chem 260: 15180-15185.
30. Yurist-Doutsch, S., and Eichler, J. (2009) Manual annotation, transcriptional analysis and protein expression studies reveal novel genes in the agl cluster responsible for N-glycosylation in the halophilic archaeon Haloferax volcanii. J Bacteriol 191: 3068-3075.
31. Yurist-Doutsch, S., Chaban, B., VanDyke, D., Jarrell, K.F., and Eichler, J. (2008a) Sweet to the extreme: protein glycosylation in Archaea. Mol Microbiol 68: 1079-1084.
32. Yurist-Doutsch, S., Abu-Qarn, M., Battaglia, F., Morris, H.R., Hitchen, P.G., Dell, A., and Eichler, J. (2008b) aglF, aglG and aglI, novel members of a gene cluster involved in the N-glycosylation of the Haloferax volcanii S-layer glycoprotein. Mol Microbiol 69: 1234-1245.
33. Yurist-Doutsch, S., Magidovich, H., Ventura, V.V., Hitchen, P.G., Dell, A., and Eichler, J. (2010) N-glycosylation in Archaea: on the coordinated actions of Haloferax volcanii AglF and AglM. Mol Microbiol 75: 1047-1058.
34. Zhu, B.C., Drake, R.R., Schweingruber, H., and Laine, R.A. (1995) Inhibition of glycosylation by amphomycin and sugar nucleotide analogs PP36 and PP55 indicates that Haloferax volcanii beta-glucosylates both glycoproteins and glycolipids through lipid-linked sugar intermediates: evidence for three novel glycoproteins and a novel sulfated dihexosyl-archaeol glycolipid. Arch Biochem Biophys 319: 355-364.