Protein N-glycosylation in Archaea: Defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation

Molecular Microbiology

Volumn 61, Issue 2, 2006, Pages 511-525

  Abu Qarn, Mehtap ^a   Eichler, Jerry ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLYCOPROTEIN; OLIGOSACCHARIDE TRANSFERASE; TRANSFERASE; UNCLASSIFIED DRUG;

ALG11 GENE; ALG5 GENE; ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BIOINFORMATICS; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; GENE DELETION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HALOFERAX VOLCANII; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STT3 GENE;

ARCHAEAL PROTEINS; BACTERIAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, ARCHAEAL; GLYCOSYLATION; HALOFERAX VOLCANII; HEXOSYLTRANSFERASES; LIPIDS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; OPEN READING FRAMES; POLYSACCHARIDES; PROTEIN SUBUNITS;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; HALOBACTERIA; HALOFERAX VOLCANII;

EID: 33748517628     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05252.x     Document Type: Article

References (54)

1. Allers, T., Ngo, H.P., Mevarech, M., and Lloyd, R.G. (2004) Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl Environ Microbiol 70: 943-953.
2. Apweiler, R., Hermjakob, H., and Sharon, N. (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta 1473: 48.
3. Baliga, N.S., Bonneau, R., Facciotti, M.T., Pan, M., Glusman, G., Deutsch, E.W., et al. (2004) Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 14: 2221-2234.
4. Bayley, D.P., Kalmokoff, M.L., and Jarrell, K.F. (1993) Effect of bacitracin on flagellar assembly and presumed glycosylation of the flagellins of Methanococcus deltae. Arch Microbiol 160: 179-185.
5. Bitan-Banin, G., Ortenberg, R., and Mevarech, M. (2003) Development of a gene knockout system for the halophilic archaeon Haloferax volcanii by use of the pyrE gene. J Bacteriol 185: 772-778.
6. Burda, P., and Aebi, M. (1999) The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta 1426: 239-257.
7. Coutinho, P.M., Deleury, E., Davies, G.J., and Henrissat, B. (2003) An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328: 307-317.
8. Dubray, G., and Bezard, G. (1982) A highly sensitive periodic acid-silver stain for 1,2-diol groups of glycoproteins and polysaccharides in polyacrylamide gels. Anal Biochem 119: 325-329.
9. Eichler, J., and Adams, M.W.W. (2005) Post-translational protein modification in Archaea. Microbiol Mol Biol Rev 69: 393-425.
10. Falb, M., Pfeiffer, F., Palm, P., Rodewald, K., Hickmann, V., Tittor, J., and Oesterhelt, D. (2005) Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res 15: 1336-1343.
11. Feldman, M.F., Wacker, M., Hernandez, M., Hitchen, P.G., Marolda, C.L., Kowarik, M., et al. (2005) Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc Natl Acad Sci USA 102: 3016-3021.
12. Fine, A., Irihimovitch, V., Dahan, I., Konrad, Z., and Eichler, J. (2006) Cloning, expression and purification of functional Sec11a and Sec11b, type I signal peptidases of the archaeon Haloferax volcanii. J Bacteriol 188: 1911-1919.
13. Grogan, D.W. (1996) Organization and interactions of cell envelope proteins of the extreme thermoacidophile Sulfolobus acidocaldarius. Can J Microbiol 42: 1163-1171.
14. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-1049.
15. Helenius, J., Ng, D.T.W., Marolda, C.L., Walter, P., Valvano, M.A., and Aebi, M. (2002) Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature 415: 447-450.
16. Irihimovitch, V., and Eichler, J. (2003) Post-translational secretion of fusion proteins in the halophilic archaea Haloferax volcanii. J Biol Chem 278: 12881-12887.
17. Karcher, U., Schroder, 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.
18. Konrad, Z., and Eichler, J. (2002) Lipid modification of proteins in Archaea: attachment of a mevalonic acid-based lipid moiety to the surface-layer glycoprotein of Haloferax volcanii follows protein translocation. Biochem J 366: 959-964.
19. Kornfeld, R., and Kornfeld, S. (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54: 631-664.
20. 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.
21. Lechner, J., and Sumper, M. (1987) The primary structure of a procaryotic glycoprotein. Cloning and sequencing of the cell surface glycoprotein gene of halobacteria. J Biol Chem 262: 9724-9729.
22. Lechner, J., and Wieland, F. (1989) Structure and biosynthesis of prokaryotic glycoproteins. Annu Rev Biochem 58: 173-194.
23. Lechner, J., Wieland, F., and Sumper, M. (1985) Transient methylation of dolichyl oligosaccharides is an obligatory step in halobacterial sulfated glycoprotein biosynthesis. J Biol Chem 260: 8984-8989.
24. Linton, D., Allan, E., Karlyshev, A.V., Cronshaw, A.D., and Wren, B.W. (2002) Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol Microbiol 43: 497-508.
25. Linton, D., Dorrell, N., Hitchen, P.G., Amber, S., Karlyshev, A.V., Morris, H.R., et al. (2005) Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway. Mol Microbiol 55: 1695-1703.
26. 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.
27. Mescher, M.F., and Strominger, J.L. (1976a) Purification and characterization of a prokaryotic glycoprotein from the cell envelope of Halobacterium salinarium. J Biol Chem 251: 2005-2014.
28. Mescher, M.F., and Strominger, J.L. (1976b) Structural (shape-maintaining) role of the cell surface glycoprotein of Halobacterium salinarium. Proc Natl Acad Sci USA 73: 2687-2691.
29. 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.
30. Mevarech, M., and Werczberger, R. (1985) Genetic transfer in Halobacterium volcanii. J Bacteriol 162: 461-462.
31. Meyer, W., and Schafer, G. (1992) Characterization and purification of a membrane-bound archaebacterial pyrophosphatase from Sulfolobus acidocaldarius. Eur J Biochem 207: 741-746.
32. Mullakhanbhai, M.F., and Larsen, H. (1975) Halobacterium volcanii spec. nov., a Dead Sea halobacterium with a moderate salt requirement. Arch Microbiol 104: 207-214.
33. Ng, W.V., Kennedy, S.P., Mahairas, G.G., Berquist, B., Pan, M., Shukla, H.D., et al. (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci USA 97: 12176-12181.
34. Nilsson, I., Kelleher, D.J., Miao, Y., Shao, Y., Kreibich, G., Gilmore, R., et al. (2003) Photocross-linking of nascent chains to the STT3 subunit of the oligosaccharyltransferase complex. J Cell Biol 161: 715-725.
35. Oren, A., Ginzburg, M., Ginzburg, B.Z., Hochstein, L.I., and Volcani, B.E. (1990) Haloarcula marismortui (Volcani) sp. nov., nom. rev., an extremely halophilic bacterium from the Dead Sea. Int J Syst Bacteriol 40: 209-210.
36. Ortenberg, R., and Mevarech, M. (2000) Evidence for post-translational membrane insertion of the integral membrane protein bacterioopsin expressed in the heterologous halophilic archaeon Haloferax volcanii. J Biol Chem 275: 22839-22846.
37. Ring, G., and Eichler, J. (2004) In the Archaea Haloferax volcanii, membrane protein biogenesis and protein synthesis rates are affected by decreased ribosomal-binding to the translocon. J Biol Chem 279: 53160-53166.
38. Silberstein, S., and Gilmore, R. (1996) Biochemistry, molecular biology, and genetics of the oligosaccharyltransferase. FASEB J 10: 849-858.
39. Spiro, R.G. (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12: 43R-56R.
40. 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.
41. Szymanski, C.M., and Wren, B.W. (2005) Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3: 225-237.
42. Szymanski, C.M., Yao, R., Ewing, C.P., Trust, T.J., and Guerry, P. (1999) Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol Microbiol 32: 1022-1030.
43. Szymanski, C.M., Logan, S.M., Linton, D., and Wren, B.W. (2003) Campylobacter - a tale of two protein glycosylation systems. Trends Microbiol 11: 233-238.
44. Varki, A. (1998) Factors controlling the glycosylation potential of the Golgi apparatus. Trends Cell Biol 8: 34-40.
45. Wacker, M., Linton, D., Hitchen, P.G., Nita-Lazar, M., Haslam, S.M., North, S.J., et al. (2002) N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298: 1790-1793.
46. Wieland, F., Dompert, W., Bernhardt, G., and Sumper, M. (1980) Halobacterial glycoprotein saccharides contain covalently linked sulphate. FEBS Lett 120: 110-114.
47. Yan, A., and Lennarz, W.J. (2002) Studies on the function of oligosaccharyl transferase subunits. Stt3p is directly involved in the glycosylation process. J Biol Chem 277: 47692-44700.
48. Yan, A., and Lennarz, W.J. (2005) Unraveling the mechanism of protein N-glycosylation. J Biol Chem 280: 3121-3124.
49. Young, N.M., Brisson, J.R., Kelly, J., Watson, D.C., Tessier, L., Lanthier, P.H., et al. (2002) Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J Biol Chem 277: 42530-42539.
50. Zaigler, A., Schuster, S.C., and Soppa, J. (2003) Construction and usage of a onefold-coverage shotgun DNA microarray to characterize the metabolism of the archaeon Haloferax volcanii. Mol Microbiol 48: 1089-1105.
51. Zeitler, R., Hochmuth, E., Deutzmann, R., and Sumper, M. (1998) Exchange of Ser-4 for Val, Leu or Asn in the sequon Asn-Ala-Ser does not prevent N-glycosylation of the cell surface glycoprotein from Halobacterium halobium. Glycobiology 8: 1157-1164.
52. Zhu, B.C., and Laine, R.A. (1996) Dolichyl-phosphomannose synthase from the archae Thermoplasma acidophilum. Glycobiology 6: 811-816.
53. 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.
54. 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.