Similarities and differences in the glycosylation mechanisms in prokaryotes and eukaryotes

International Journal of Microbiology

Volumn , Issue , 2010, Pages

  Dell, Anne ^a   Galadari, Alaa ^b   Sastre, Federico ^a   Hitchen, Paul ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNITED ARAB EMIRATES UNIVERSITY   (United Arab Emirates)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 80052479968     PISSN: 1687918X     EISSN: 16879198     Source Type: Journal    
DOI: 10.1155/2010/148178     Document Type: Review

References (80)

1. C. M. Szymanski and B. W. Wren, "Protein glycosylation in bacterial mucosal pathogens, " Nature Reviews Microbiology, vol. 3, no. 3, pp. 225-237, 2005. (Pubitemid 40298222)
2. M. F. Mescher and J. L. Strominger, "Purification and characterization of a prokaryotic glycoprotein from the cell envelope of Halobacterium salinarium, " Journal of Biological Chemistry, vol. 251, no. 7, pp. 2005-2014, 1976.
3. N. M. Young, J. R. Brisson, J. Kelly et al., "Structure of the N-linked glycan present on multiple glycoproteins in the gram-negative bacterium, Campylobacter jejuni, " Journal of Biological Chemistry, vol. 277, no. 45, pp. 42530-42539, 2002. (Pubitemid 35285620)
4. M. Wacker, D. Linton, P. G. Hitchen et al., "N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli, " Science, vol. 298, no. 5599, pp. 1790-1793, 2002. (Pubitemid 35404123)
5. D. Calo, L. Kaminski, and J. Eichler, "Protein glycosylation in Archaea: sweet and extreme, " Glycobiology, vol. 20, no. 9, pp. 1065-1076, 2010.
6. I. Hug and M. F. Feldman, "Analogies and homologies in lipopolysaccharide and glycoprotein biosynthesis in bacteria, " Glycobiology, vol. 21, no. 2, pp. 138-151, 2011.
7. A. Varki, R. D. Cummings, J. D. Esko et al., Essentials of Glycobiology, Cold Spring Harbor Laboratory Press, New York, NY, USA, 2nd edition, 2009.
8. M. T. Taylor and K. Drickamer, Introduction to Glycobiology, Oxford University Press, Oxford, UK, 2nd edition, 2006.
9. D. J. Kelleher, S. Banerjee, A. J. Cura, J. Samuelson, and R. Gilmore, "Dolichol-linked oligosaccharide selection by the oligosaccharyltransferase in protist and fungal organisms, " Journal of Cell Biology, vol. 177, no. 1, pp. 29-37, 2007. (Pubitemid 46588399)
10. L. Izquierdo, B. L. Schulz, J. A. Rodrigues et al., "Distinct donor and acceptor specificities of Trypanosoma brucei oligosaccharyl transferases, " The EMBO Journal, vol. 28, no. 17, pp. 2650-2661, 2009.
11. S. Sanyal and A. K. Menon, "Stereoselective transbilayer translocation of mannosyl phosphoryl dolichol by an endoplasmic reticulum flippase, " Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 25, pp. 11289-11294, 2010.
12. J. Helenius, D. T. W. Ng, C. L. Marolda, P. Walter, M. A. Valvano, and M. Aebi, "Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein, " Nature, vol. 415, no. 6870, pp. 447-450, 2002. (Pubitemid 34100957)
13. C. R. H. Raetz, C. M. Reynolds, M. S. Trent, and R. E. Bishop, "Lipid a modification systems in gram-negative bacteria, " Annual Review of Biochemistry, vol. 76, pp. 295-329, 2007.
14. C. Alaimo, I. Catrein, L. Morf et al., "Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides, " The EMBO Journal, vol. 25, no. 5, pp. 967-976, 2006. (Pubitemid 43372111)
15. L. Cuthbertson, V. Kos, and C. Whitfield, "ABC transporters involved in export of cell surface glycoconjugates, " Microbiology and Molecular Biology Reviews, vol. 74, no. 3, pp. 341-362, 2010.
16. M. Abu-Qarn and J. Eichler, "Protein N-glycosylation in Archaea: defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation, " Molecular Microbiology, vol. 61, no. 2, pp. 511-525, 2006. (Pubitemid 44356580)
17. M. Abu-Qarn, S. Yurist-Doutsch, A. Giordano et al., "Haloferax volcanii AglB and AglD are involved in Nglycosylation of the S-layer glycoprotein and proper assembly of the surface layer, " Journal of Molecular Biology, vol. 374, no. 5, pp. 1224-1236, 2007. (Pubitemid 350122553)
18. A. J. Jervis, R. Langdon, P. Hitchen et al., "Characterization of N-linked protein glycosylation in Helicobacter pullorum, " Journal of Bacteriology, vol. 192, no. 19, pp. 5228-5236, 2010.
19. P. G. Hitchen, K. Twigger, E. Valiente, R. H. Langdon, B. W. Wren, and A. Dell, "Glycoproteomics: a powerful tool for characterizing the diverse glycoforms of bacterial pilins and flagellins, " Biochemical Society Transactions, vol. 38, no. 5, pp. 1307-1313, 2010.
20. W. J. Lennarz, "Studies on oligosaccharyl transferase in yeast, " Acta Biochimica Polonica, vol. 54, no. 4, pp. 673-677, 2007.
21. D. J. Kelleher and R. Gilmore, "An evolving view of the eukaryotic oligosaccharyl transferase, " Glycobiology, vol. 16, no. 4, pp. 47R-62R, 2006.
22. B. L. Schulz and M. Aebi, "Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency, " Molecular and Cellular Proteomics, vol. 8, no. 2, pp. 357-364, 2009.
23. F. P. Nasab, B. L. Schulz, F. Gamarro, A. J. Parodi, and M. Aebi, "All in one: leishmania major STT3 proteins substitute for the whole oligosaccharyltransferase complex in Saccharomyces cerevisiae, " Molecular Biology of the Cell, vol. 19, no. 9, pp. 3758-3768, 2008.
24. K. Hese, C. Otto, F. H. Routier, and L. Lehle, "The yeast oligosaccharyltransferase complex can be replaced by STT3 from Leishmania major, " Glycobiology, vol. 19, no. 2, pp. 160- 171, 2009.
25. C. Ruiz-Canada, D. J. Kelleher, and R. Gilmore, "Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms, " Cell, vol. 136, no. 2, pp. 272-283, 2009.
26. M. F. Feldman, M. Wacker, M. Hernandez et al., "Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli, " Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 8, pp. 3016-3021, 2005. (Pubitemid 40299908)
27. E. Peyfoon, B. Meyer, P. G. Hitchen et al., "The S-layer glycoprotein of the crenarchaeote Sulfolobus acidocaldarius is glycosylated at multiple sites with chitobiose-linked Nglycans, " Archaea. In press.
28. M. Kowarik, N. M. Young, S. Numao et al., "Definition of the bacterial N-glycosylation site consensus sequence, " The EMBO Journal, vol. 25, no. 9, pp. 1957-1966, 2006.
29. D. F. Zielinska, F. Gnad, J. R. Wísniewski, and M. Mann, "Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints, " Cell, vol. 141, no. 5, pp. 897-907, 2010.
30. H. Claus, E. Akça, T. Debaerdemaeker et al., "Molecular organization of selected prokaryotic S-layer proteins, " Canadian Journal of Microbiology, vol. 51, no. 9, pp. 731-743, 2005. (Pubitemid 43067712)
31. P. Messner, K. Steiner, K. Zarschler, and C. Scḧaffer, "S-layer nanoglycobiology of bacteria, " Carbohydrate Research, vol. 343, no. 12, pp. 1934-1951, 2008.
32. S. Grass, A. Z. Buscher, W. E. Swords et al., "The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis, " Molecular Microbiology, vol. 48, no. 3, pp. 737-751, 2003. (Pubitemid 36819059)
33. J. Gross, S. Grass, A. E. Davis, P. Gilmore-Erdmann, R. R. Townsend, and J. W. St Geme III, "The Haemophilus influenzae HMW1 adhesin is a glycoprotein with an unusual N-linked carbohydrate modification, " Journal of Biological Chemistry, vol. 283, no. 38, pp. 26010-26015, 2008.
34. S. Grass, C. F. Lichti, R. R. Townsend, J. Gross, and J. W. St Geme III, "The haemophilus influenzae HMW1c protein is a glycosyltransferase that transfers hexose residues to asparagine sites in the HMW1 adhesin, " PLoS Pathogens, vol. 6, no. 5, Article ID e1000919, 9 pages, 2010.
35. R. Schreiner, E. Schnabel, and F. Wieland, "Novel Nglycosylation in eukaryotes: laminin contains the linkage unit β-glucosylasparagine, " Journal of Cell Biology, vol. 124, no. 6, pp. 1071-1081, 1994.
36. E. Stimson, M. Virji, K. Makepeace et al., "Meningococcal pilin: a glycoprotein substituted with digalactosyl 2, 4- diacetamido-2, 4, 6-trideoxyhexose, " Molecular Microbiology, vol. 17, no. 6, pp. 1201-1214, 1995.
37. F. T. Hegge, P. G. Hitchen, F. E. Aas et al., "Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili, " Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 29, pp. 10798-10803, 2004. (Pubitemid 38955822)
38. P. M. Power, K. L. Seib, and M. P. Jennings, "Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli, " Biochemical and Biophysical Research Communications, vol. 347, no. 4, pp. 904-908, 2006. (Pubitemid 44118204)
39. A. Faridmoayer, M. A. Fentabil, D. C. Mills, J. S. Klassen, and M. F. Feldman, "Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation, " Journal of Bacteriology, vol. 189, no. 22, pp. 8088- 8098, 2007. (Pubitemid 350178920)
40. M. Qutyan, M. Paliotti, and P. Castric, "PilO of Pseudomonas aeruginosa 1244: subcellular location and domain assignment, " Molecular Microbiology, vol. 66, no. 6, pp. 1444-1458, 2007. (Pubitemid 350179678)
41. J. G. Smedley III, E. Jewell, J. Roguskie et al., "Influence of pilin glycosylation on Pseudomonas aeruginosa 1244 pilus function, " Infection and Immunity, vol. 73, no. 12, pp. 7922- 7931, 2005. (Pubitemid 41740276)
42. A. Vik, F. E. Aas, J. H. Anonsen et al., "Broad spectrum Olinked protein glycosylation in the human pathogen Neisseria gonorrhoeae, " Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 11, pp. 4447-4452, 2009.
43. S. C. Ku, B. L. Schulz, P. M. Power, and M. P. Jennings, "The pilin O-glycosylation pathway of pathogenic Neisseria is a general system that glycosylates AniA, an outer membrane nitrite reductase, " Biochemical and Biophysical Research Communications, vol. 378, no. 1, pp. 84-89, 2009.
44. A. Faridmoayer, M. A. Fentabil, M. F. Haurat et al., "Extreme substrate promiscuity of the Neisseria oligosaccharyl transferase involved in protein O-glycosylation, " Journal of Biological Chemistry, vol. 283, no. 50, pp. 34596-34604, 2008.
45. M. J. Coyne, B. Reinap, M. M. Lee, and L. E. Comstock, "Human symbionts use a host-like pathway for surface fucosylation, " Science, vol. 307, no. 5716, pp. 1778-1781, 2005. (Pubitemid 40388619)
46. C. M. Fletcher, M. J. Coyne, O. F. Villa, M. Chatzidaki-Livanis, and L. E. Comstock, "A general O-glycosylation system important to the physiology of a major human intestinal symbiont, " Cell, vol. 137, no. 2, pp. 321-331, 2009.
47. A. E. Zeituni, W. McCaig, E. Scisci, D. G. Thanassi, and C. W. Cutler, "The native 67-kilodalton minor fimbria of Porphyromonas gingivalis is a novel glycoprotein with DCSIGN- targeting motifs, " Journal of Bacteriology, vol. 192, no. 16, pp. 4103-4110, 2010.
48. M. Sumper, E. Berg, R. Mengele, and I. Strobel, "Primary structure and glycosylation of the S-layer protein of Haloferax volcanii, " Journal of Bacteriology, vol. 172, no. 12, pp. 7111- 7118, 1990.
49. C. Scḧaffer, M. Graninger, and P. Messner, "Prokaryotic glycosylation, " Proteomics, vol. 1, no. 2, pp. 248-261, 2001. (Pubitemid 33586720)
50. M. Abu-Qarn, J. Eichler, and N. Sharon, "Not just for Eukarya anymore: protein glycosylation in Bacteria and Archaea, " Current Opinion in Structural Biology, vol. 18, no. 5, pp. 544- 550, 2008.
51. H.Wu, M. Zeng, and P. Fives-Taylor, "The glycan moieties and the N-terminal polypeptide backbone of a fimbria-associated adhesin, Fap1, play distinct roles in the biofilm development of Streptococcus parasanguinis, " Infection and Immunity, vol. 75, no. 5, pp. 2181-2188, 2007. (Pubitemid 46744304)
52. Z. Peng, P. Fives-Taylor, T. Ruiz et al., "Identification of critical residues in Gap3 of Streptococcus parasanguinis involved in Fap1 glycosylation, fimbrial formation and in vitro adhesion, " BMC Microbiology, vol. 8, article 52, 2008.
53. M. Zhou and H.Wu, "Glycosylation and biogenesis of a family of serine-rich bacterial adhesins, " Microbiology, vol. 155, no. 2, pp. 317-327, 2009.
54. S. Ramboarina, J. A. Garnett, M. Zhou et al., "Structural insights into serine-rich fimbriae from gram-positive bacteria, " Journal of Biological Chemistry, vol. 285, no. 42, pp. 32446-32457, 2010.
55. B. A. Bensing, B. W. Gibson, and P. M. Sullam, "The Streptococcus gordonii platelet binding protein GspB undergoes glycosylation independently of export, " Journal of Bacteriology, vol. 186, no. 3, pp. 638-645, 2004. (Pubitemid 38129640)
56. N. M. van Sorge, D. Quach, M. A. Gurney, P. M. Sullam, V. Nizet, and K. S. Doran, "The group B streptococcal serinerich repeat 1 glycoprotein mediates penetration of the bloodbrain barrier, " Journal of Infectious Diseases, vol. 199, no. 10, pp. 1479-1487, 2009.
57. P. Shivshankar, C. Sanchez, L. F. Rose, and C. J. Orihuela, "The Streptococcus pneumoniae adhesin PsrP binds to Keratin 10 on lung cells, " Molecular Microbiology, vol. 73, no. 4, pp. 663- 679, 2009.
58. SU. Bu, Y. Li, M. Zhou et al., "Interaction between two putative glycosyltransferases is required for glycosylation of a serinerich streptococcal adhesin, " Journal of Bacteriology, vol. 190, no. 4, pp. 1256-1266, 2008. (Pubitemid 351215006)
59. R. Wu, M. Zhou, and H. Wu, "Purification and characterization of an active N-acetylglucosaminyltransferase enzyme complex from Streptococci, " Applied and Environmental Microbiology, vol. 76, no. 24, pp. 7966-7971, 2010.
60. Q. Zeidan and G. W. Hart, "The intersections between OGlcNAcylation and phosphorylation: implications for multiple signaling pathways, " Journal of Cell Science, vol. 123, no. 1, pp. 13-22, 2010.
61. M. Zhou, F. Zhu, S. Dong, D. G. Pritchard, and H. Wu, "A novel glucosyltransferase is required for glycosylation of a serine-rich adhesin and biofilm formation by Streptococcus parasanguinis, " Journal of Biological Chemistry, vol. 285, no. 16, pp. 12140-12148, 2010.
62. M. Lommel and S. Strahl, "Protein O-mannosylation: conserved from bacteria to humans, " Glycobiology, vol. 19, no. 8, pp. 816-828, 2009.
63. T. Endo, "O-Mannosyl glycans in mammals, " Biochimica et Biophysica Acta, vol. 1473, no. 1, pp. 237-246, 1999.
64. N. Nakamura, D. Lyalin, and V. M. Panin, "Protein Omannosylation in animal development and physiology: from human disorders to Drosophila phenotypes, " Seminars in Cell and Developmental Biology, vol. 21, no. 6, pp. 622-630, 2010.
65. C. Espitia, L. Serv́in-Gonźalez, and R.Mancilla, "New insights into protein O-mannosylation in actinomycetes, " Molecular Bio Systems, vol. 6, no. 5, pp. 775-781, 2010.
66. K. M. Dobos, K. H. Khoo, K.M. Swiderek, P. J. Brennan, and J. T. Belisle, "Definition of the full extent of glycosylation of the 45-kilodalton glycoprotein of Mycobacterium tuberculosis, " Journal of Bacteriology, vol. 178, no. 9, pp. 2498-2506, 1996. (Pubitemid 26134471)
67. M. J. Sartain and J. T. Belisle, "N-Terminal clustering of the O-glycosylation sites in the Mycobacterium tuberculosis lipoprotein SodC, " Glycobiology, vol. 19, no. 1, pp. 38-51, 2009.
68. S. L. Michell, A. O. Whelan, P. R. Wheeler et al., "The MPB83 antigen fromMycobacterium bovis contains O-linked mannose and (1 → 3)-mannobiose moieties, " Journal of Biological Chemistry, vol. 278, no. 18, pp. 16423-16432, 2003. (Pubitemid 36799770)
69. M. Mahne, A. Tauch, A. P̈uhler, and J. Kalinowski, "The Corynebacterium glutamicum gene pmt encoding a glycosyltransferase related to eukaryotic protein-O-mannosyltransferases is essential for glycosylation of the resuscitation promoting factor (Rpf2) and other secreted proteins, " FEMS Microbiology Letters, vol. 259, no. 2, pp. 226-233, 2006. (Pubitemid 43828744)
70. S.Wehmeier, A. S. Varghese, S. S. Gurcha et al., "Glycosylation of the phosphate binding protein, PstS, in Streptomyces coelicolor by a pathway that resembles protein O-mannosylation in eukaryotes, "Molecular Microbiology, vol. 71, no. 2, pp. 421- 433, 2009.
71. I. Benz and M. A. Schmidt, "Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin, "Molecular Microbiology, vol. 40, no. 6, pp. 1403-1413, 2001. (Pubitemid 32635308)
72. O. Sherlock, U. Dobrindt, J. B. Jensen, R. M. Vejborg, and P. Klemm, "Glycosylation of the self-recognizing Escherichia coli Ag43 autotransporter protein, " Journal of Bacteriology, vol. 188, no. 5, pp. 1798-1807, 2006. (Pubitemid 43346858)
73. S. Reidl, A. Lehmann, R. Schiller, A. Salam Khan, and U. Dobrindt, "Impact of O-glycosylation on the molecular and cellular adhesion properties of the Escherichia coli autotransporter protein Ag43, " International Journal of Medical Microbiology, vol. 299, no. 6, pp. 389-401, 2009.
74. S. K. Knudsen, A. Stensballe, M. Franzmann, U. B. Westergaard, and D. E. Otzen, "Effect of glycosylation on the extracellular domain of the Ag43 bacterial autotransporter: enhanced stability and reduced cellular aggregation, " Biochemical Journal, vol. 412, no. 3, pp. 563-577, 2008. (Pubitemid 351846422)
75. P. G. Hitchen, K. Twigger, E. Valiente, R. H. Langdon, B. W. Wren, and A. Dell, "Glycoproteomics: a powerful tool for characterizing the diverse glycoforms of bacterial pilins and flagellins, " Biochemical Society Transactions, vol. 38, no. 5, pp. 1307-1313, 2010.
76. S. M. Logan, "Flagellar glycosylation-a new component of the motility repertoire?" Microbiology, vol. 152, no. 5, pp. 1249-1262, 2006.
77. W. L. Miller, M. J. Matewish, D. J. McNally et al., "Flagellin glycosylation in Pseudomonas aeruginosa PAK requires the O-antigen biosynthesis enzyme WbpO, " Journal of Biological Chemistry, vol. 283, no. 6, pp. 3507-3518, 2008.
78. S. M. Twine, C.W. Reid, A. Aubry et al., "Motility and flagellar glycosylation in Clostridium difficile, " Journal of Bacteriology, vol. 191, no. 22, pp. 7050-7062, 2009.
79. K. Julenius, A. Mølgaard, R. Gupta, and S. Brunak, "Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites, " Glycobiology, vol. 15, no. 2, pp. 153-164, 2005. (Pubitemid 40227920)
80. J. L. Herrmann, R. Delahay, A. Gallagher, B. Robertson, and D. Young, "Analysis of post-translational modification of mycobacterial proteins using a cassette expression system, " FEBS Letters, vol. 473, no. 3, pp. 358-362, 2000. (Pubitemid 30249154)