Biochemical evidence for an alternate pathway in N-linked glycoprotein biosynthesis

Nature Chemical Biology

Volumn 9, Issue 6, 2013, Pages 367-373

  Larkin, Angelyn ^a,b   Chang, Michelle M ^a   Whitworth, Garrett E ^a   Imperiali, Barbara ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; BETA GLUCOSYLTRANSFERASE; DOLICHOL PHOSPHATE; DOLICHYL MONOPHOSPHATE GLYCAN; GLYCOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; EUKARYOTE; GLYCOSYLATION; IN VITRO STUDY; METHANOCOCCUS VOLTAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

ARCHAEAL PROTEINS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GLUCOSYLTRANSFERASES; GLYCOPEPTIDES; GLYCOPROTEINS; GLYCOSYLATION; LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; METHANOCOCCUS; PLASMIDS; POLYSACCHARIDES;

ARCHAEA; EUKARYOTA; METHANOCOCCUS VOLTAE;

EID: 84879126165     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1249     Document Type: Article

References (54)

1. Nothaft, H. & Szymanski, C.M. Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8, 765-778 (2010).
2. Eichler, J. Extreme sweetness: protein glycosylation in archaea. Nat. Rev. Microbiol. 11, 151-156 (2013).
3. Larkin, A. & Imperiali, B. The expanding horizons of asparagine-linked glycosylation. Biochemistry 50, 4411-4426 (2011).
4. Szymanski, C.M., Yao, R., Ewing, C.P., Trust, T.J. & Guerry, P. Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32, 1022-1030 (1999).
5. Magidovich, H. & Eichler, J. Glycosyltransferases and oligosaccharyltransferases in archaea: putative components of the N-glycosylation pathway in the third domain of life. FEMS Microbiol. Lett. 300, 122-130 (2009).
6. Chaban, B., Voisin, S., Kelly, J., Logan, S.M. & Jarrell, K.F. Identification of genes involved in the biosynthesis and attachment of Methanococcus voltae N-linked glycans: insight into N-linked glycosylation pathways in archaea. Mol. Microbiol. 61, 259-268 (2006).
7. Abu-Qarn, M. & Eichler, J. Protein N-glycosylation in archaea: defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation. Mol. Microbiol. 61, 511-525 (2006).
8. Mescher, M.F. & Strominger, J.L. Purification and characterization of a prokaryotic glucoprotein from the cell envelope of Halobacterium salinarium. J. Biol. Chem. 251, 2005-2014 (1976).
9. Mescher, M.F., Hansen, U. & Strominger, J.L. Formation of lipid-linked sugar compounds in Halobacterium salinarium. Presumed intermediates in glycoprotein synthesis. J. Biol. Chem. 251, 7289-7294 (1976).
10. Lechner, J., Wieland, F. & Sumper, M. 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 (1985).
11. Burda, P. & Aebi, M. The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426, 239-257 (1999).
12. Calo, D., Guan, Z., Naparstek, S. & Eichler, J. Different routes to the same ending: comparing the N-glycosylaton processes of Haloferax volcanii and Haloarcula morismortui, two halophilic archaea from the Dead Sea. Mol. Microbiol. 81, 1166-1177 (2011).
13. Kuntz, C., Sonnenbichler, J., Sonnenbichler, I., Sumper, M. & Zeitler, R. Isolation and characterization of dolichol-linked oligosaccharides from Haloferax volcanii. Glycobiology 7, 897-904 (1997).
14. Guan, Z. et al. Distinct glycan-charged phosphodolichol carriers are required for the assembly of the pentasaccharide N-linked to the Haloferax volcanii S-layer glycoprotein. Mol. Microbiol. 78, 1294-1303 (2010).
15. Guan, Z., Meyer, B., Albers, S.-V. & Eichler, J. The thermoacidophilic archaeaon Sulfolobus acidocaldarius contains an unusually short, highly reduced dolichol phosphate. Biochim. Biophys. Acta 1811, 607-616 (2011).
16. Yurist-Doutsch, S., Chaban, B., Van Dyke, D.J., Jarrell, K.F. & Eichler, J. Sweet to the extreme: protein glycosylation in archaea. Mol. Microbiol. 68, 1079-1084 (2008).
17. Van Dyke, D.J. et al. Identification of genes involves in the assembly and attachment of a novel flagellin N-linked tetrasaccharide important for motility in the archaeon Methanococcus maripaludis. Mol. Microbiol. 72, 633-644 (2009).
18. Voisin, S. et al. Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae. J. Biol. Chem. 280, 16586-16593 (2005).
19. Chaban, B., Logan, S.M., Kelly, J.F. & Jarrell, K.F. AglC and AglK are involved in biosynthesis and attachment of diacetylated glucuronic acid to the N-glycan in Methanococcus voltae. J. Bacteriol. 191, 187-195 (2009).
20. Shams-Eldin, H., Chaban, B., Niehus, S., Schwarz, R.T. & Jarrell, K.F. Identification of the archaeal alg7 gene homolog (encoding N-acetylglucosamine-1-phosphate transferase) of the N-linked glycosylation system by cross-domain complementation in Saccharomyces cerevisiae. J. Bacteriol. 190, 2217-2220 (2008).
21. Jones, M.B., Rosenburg, J.N., Betenbaugh, M.J. & Krag, S.S. Structure and synthesis of polyisoprenoids used in N-glycosylation across the three domains of life. Biochim. Biophys. Acta 1790, 485-494 (2009).
22. Naparstek, S., Guan, Z. & Eichler, J. A predicted geranylgeranyl reductase reduces the ω-position isoprene of dolichol phosphate in the halophilic archaeon, Haloferax volcanii. Biochim. Biophys. Acta 1821, 923-933 (2012).
23. Heesen, S., Lehle, L., Weissmann, A. & Aebi, M. Isolation of the ALG5 locus encoding the UDP-glucose:dolichyl-phosphate glucosyltransferase from Saccharomyces cerevisiae. Eur. J. Biochem. 224, 71-79 (1994).
24. Kaminski, L. et al. AglJ adds the first sugar of the N-linked pentasaccharide decorating the Haloferax volcanii S-layer glycoprotein. J. Bacteriol. 192, 5572-5579 (2010).
25. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580 (2001).
26. Hartley, M.D. & Imperiali, B. At the membrane frontier: a prospectus on the remarkable evolutionary conservation of polyprenols and polyprenyl-phosphates. Arch. Biochem. Biophys. 517, 83-97 (2012).
27. Kelly, J., Logan, S.M., Jarrell, K.F., Van Dyke, D.J. & Vinogradov, E.V. A novel N-linked flagellar glycan from Methanococcus maripaludis. Carbohydr. Res. 344, 648-653 (2009).
28. Behrens, N.H. & Leloir, L.F. Dolichyl monophosphate glucose: an intermediate in glucose transfer in liver. Proc. Natl. Acad. Sci. USA 66, 153-159 (1970).
29. 14C-labeled mannolipid with properties of dolichyl mannopyranosyl phosphate. J. Biol. Chem. 249, 6372-6381 (1974).
30. Herscovics, A., Warren, C.D. & Jeanloz, R.W. Anomeric configuration of the dolichyl-d-mannosyl phosphate formed in calf pancreas microsomes. J. Biol. Chem. 250, 8079-8084 (1975).
31. 1H NMR. Biochemistry 18, 500-507 (1979).
32. Larkin, A. & Imperiali, B. Biosynthesis of UDP-GlcNAc(3NAc)A by WbpB, WbpE, and WbpD: enzymes in the Wbp pathway responsible for O-antigen assembly in Pseudomonas aeruginosa PAO1. Biochemistry 48, 5446-5455 (2009).
33. Sharma, C.B., Lehle, L. & Tanner, W. N-Glycosylation of yeast proteins. Characterization of the solubilized oligosaccharyl transferase. Eur. J. Biochem. 116, 101-108 (1981).
34. Imperiali, B. & Hendrickson, T.L. Asparagine-linked glycosylation: specificity and function of oligosaccharyl transferase. Bioorg. Med. Chem. 3, 1565-1578 (1995).
35. Glover, K.J., Weerapana, E., Numao, S. & Imperiali, B. Chemoenzymatic synthesis of glycopeptides with PglB, a bacterial oligosaccharyl transferase from Campylobacter jejuni. Chem. Biol. 12, 1311-1315 (2005).
36. Jaffee, M.B. & Imperiali, B. Exploiting topological constraints to reveal buried sequence motifs in the membrane-bound N-linked oligosaccharyl transferases. Biochemistry 50, 7557-7567 (2011).
37. Lizak, C., Gerber, S., Numao, S., Aebi, M. & Locher, K.P. X-ray structure of a bacterial oligosaccharyltransferase. Nature 474, 350-355 (2011).
38. Ferrante, G., Ekiel, I. & Sprott, G.D. Structural characterization of the lipids of Methanococcus voltae, including a novel N-acetylglucosamine 1-phosphate diether. J. Biol. Chem. 261, 17062-17066 (1986).
39. Charnock, S.J. & Davies, G.J. Structural analysis of the nucleotide-diphospho-sugar transferase, SpsA from Bacillus subtilis, in native and nucleotide-complexed forms. Biochemistry 38, 6380-6385 (1999).
40. Coutinho, P.M., Deleury, E., Davies, G.J. & Henrissat, B. An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328, 307-317 (2003).
41. Lairson, L.L., Henrissat, B., Davies, G.J. & Withers, S.G. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555 (2008).
42. Flint, J. et al. Structural dissection and high-throughput screening of mannosylglycerate synthase. Nat. Struct. Mol. Biol. 12, 608-614 (2005).
43. Ramirez, F. & Marecek, J.F. Coordination of magnesium with adenosine 5′-diphosphate and triphosphate. Biochim. Biophys. Acta 589, 21-29 (1980).
44. Igura, M. et al. Structure-guided identification of a new catalytic motif of oligosaccharyltransferase. EMBO J. 27, 234-243 (2008).
45. Matsumoto, S. et al. Crystal structure of the C-terminal globular domain of oligosaccharyltransferase from Archaeoglobus fulgidus at 1.75 Åresolution. Biochemistry 51, 4157-4166 (2012).
46. Świeżewska, E. et al. The search for plant polyprenols. Acta Biochim. Pol. 41, 221-260 (1994).
47. Wu, R., Beauchamps, M.G., Laquidara, J.M. & Sowa, J.R. Jr. Ruthenium-catalyzed asymmetric transfer hydrogenation of allylic alcohols by an enantioselective isomerization/transfer hydrogenation mechanism. Angew. Chem. Int. Ed. Engl. 51, 2106-2110 (2012).
48. Suzuki, S. et al. Synthesis of mammalian dolichols from plant polyprenols. Tetrahedr. Lett. 24, 5103-5106 (1983).
49. Branch, C.L., Burton, G. & Moss, S.F. An expedient synthesis of allylic polyprenol phosphates. Synth. Commun. 29, 2639-2644 (1999).
50. Imperiali, B. & Zimmerman, J.W. Synthesis of dolichylpyrophosphate- linked oligosaccharides. Tetrahedr. Lett. 31, 6485-6488 (1990).
51. Tai, V.W.F. & Imperiali, B. Substrate specificity of the glycosyl donor for oligosaccharyl transferase. J. Org. Chem. 66, 6217-6228 (2001).
52. Sim, M.M., Kondo, H. & Wong, C.-H. Synthesis and use of glycosyl phosphites: an effective route to glycosyl phosphates, sugar nucleotides, and glycosides. J. Am. Chem. Soc. 115, 2260-2267 (1993).
53. Folch, J., Lees, M. & Stanley, G.H.S. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509 (1957).
54. Troutman, J.M. & Imperiali, B. Campylobacter jejuni PglH is a single active site processive polymerase that utilizes product inhibition to limit sequential glycosyl transfer reactions. Biochemistry 48, 2807-2816 (2009).