N-linked glycosylation in bacteria: An unexpected application

Future Microbiology

Volumn 4, Issue 4, 2009, Pages 401-412

  Langdon, Rebecca H ^a   Cuccui, Jon ^a   Wren, Brendan W ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

Bacteria; Campylobacter jejuni; Glycoengineering; Glycosylation; PglB; Vaccine

Indexed keywords

BACTERIAL ENZYME; GLYCOCONJUGATE VACCINE; GLYCOPROTEIN; POLYSACCHARIDE VACCINE; PROTEIN PGLB; UNCLASSIFIED DRUG; RECOMBINANT PROTEIN;

BACTERIAL GENETICS; BACTERIAL METABOLISM; BIOSYNTHESIS; CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI; GENE MUTATION; GENETIC CONSERVATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW; VACCINE PRODUCTION; EPSILONPROTEOBACTERIA; GENETICS; GLYCOSYLATION; METABOLISM;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; EQUIDAE; ESCHERICHIA COLI; EUKARYOTA; PROTEOBACTERIA;

EPSILONPROTEOBACTERIA; ESCHERICHIA COLI; GLYCOPROTEINS; GLYCOSYLATION; RECOMBINANT PROTEINS;

EID: 66949119639     PISSN: 17460913     EISSN: None     Source Type: Journal    
DOI: 10.2217/fmb.09.10     Document Type: Review

References (80)

1. Parkhill J, Wren BW, Mungall K et al.: The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665-668 (2000).
2. Guerry P, Szymanski CM: Campylobacter sugars sticking out. Trends Microbiol. 16, 428-435 (2008).
3. Linton D, Allan E, Karlyshev AV, Cronshaw AD, Wren BW: Identification of N-acetylgalactosamine-containing glycoproteins PEB3 and CgpA in Campylobacter jejuni. Mol. Microbiol. 43, 497-508 (2002).
4. Szymanski CM, Yao R, Ewing CP, Trust TJ, Guerry P: Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32, 1022-1030 (1999).
5. Thibault P, Logan SM, Kelly JF et al.: Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem. 276, 34862-34870 (2001).
6. Szymanski CM, Burr DH, Guerry P: Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 70, 2242-2244 (2002).
7. Fry BN, Korolik V, ten Brinke JA et al.: The lipopolysaccharide biosynthesis locus of Campylobacter jejuni 81116. Microbiology 144(Pt 8), 2049-2061 (1998).
8. Kakuda T, DiRita VJ: Cj1496c encodes a Campylobacter jejuni glycoprotein that influences invasion of human epithelial cells and colonization of the chick gastrointestinal tract. Infect. Immun. 74, 4715-4723 (2006).
9. Vijayakumar S, Merkx-Jacques A, Ratnayake DB et al.: Cj1121c, a novel UDP-4-keto-6-deoxy-GlcNAc C-4 aminotransferase essential for protein glycosylation and virulence in Campylobacter jejuni. J. Biol. Chem. 281, 27733-27743 (2006).
10. Wacker M, Linton D, Hitchen PG et al.: N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298, 1790-1793 (2002).
11. Wyszynska A, Zycka J, Godlewska R, Jagusztyn-Krynicka EK: The Campylobacter jejuni/coli cjaA (cj0982c) gene encodes an N-glycosylated lipoprotein localized in the inner membrane. Curr. Microbiol. 57, 181-188 (2008).
12. Young NM, Brisson JR, Kelly J et al.: Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J. Biol. Chem. 277, 42530-42539 (2002).
13. Kowarik M, Young NM, Numao S et al.: Definition of the bacterial N-glycosylation site consensus sequence. EMBO J. 25, 1957-1966 (2006).
14. Kowarik M, Numao S, Feldman MF et al.: N-linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase. Science 314, 1148-1150 (2006).
15. Slynko V, Schubert M, Numao S, Kowarik M, Aebi M, Allain FH: NMR structure determination of a segmentally labeled glycoprotein using in vitro glycosylation. J. Am. Chem. Soc. 131, 1274-1281 (2009).
16. Bacon DJ, Szymanski CM, Burr DH, Silver RP, Alm RA, Guerry P: A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 40, 769-777 (2001).
17. Dorrell N, Mangan JA, Laing KG et al.: Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. Genome Res. 11, 1706-1715 (2001).
18. Gilbert M, Karwaski MF, Bernatchez S et al.: The genetic bases for the variation in the lipo-oligosaccharide of the mucosal pathogen, Campylobacter jejuni. Biosynthesis of sialylated ganglioside mimics in the core oligosaccharide. J. Biol. Chem. 277, 327-337 (2002).
19. Guerry P, Szymanski CM, Prendergast MM et al.: Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect. Immun. 70, 787-793 (2002).
20. Hendrixson DR: A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol. Microbiol. 61, 1646-165 (2006).
21. Hendrixson DR: Restoration of flagellar biosynthesis by varied mutational events in Campylobacter jejuni. Mol. Microbiol. 70, 519-536 (2008).
22. Karlyshev AV, Linton D, Gregson NA, Wren BW: A novel paralogous gene family involved in phase-variable flagella-mediated motility in Campylobacter jejuni. Microbiology 148, 473-480 (2002).
23. Linton D, Gilbert M, Hitchen PG et al.: Phase variation of a β-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Mol. Microbiol. 37, 501-514 (2000).
24. Nuijten PJ, Marquez-Magana L, van der Zeijst BA: Analysis of flagellin gene expression in flagellar phase variants of Campylobacter jejuni 81116. Antonie van Leeuwenhoek 67, 377-383 (1995).
25. Parker CT, Gilbert M, Yuki N, Endtz HP, Mandrell RE: Characterization of lipooligosaccharide-biosynthetic loci of Campylobacter jejuni reveals new lipooligosaccharide classes: evidence of mosaic organizations. J. Bacteriol. 190, 5681-5689 (2008).
26. Prendergast MM, Tribble DR, Baqar S et al.: In vivo phase variation and serologic response to lipooligosaccharide of Campylobacter jejuni in experimental human infection. Infect. Immun. 72, 916-922 (2004).
27. Chen MM, Weerapana E, Ciepichal E et al.: Polyisoprenol specificity in the Campylobacter jejuni N-linked glycosylation pathway. Biochemistry 46, 14342-14348 (2007).
28. Glover KJ, Weerapana E, Imperiali B: In vitro assembly of the undecaprenylpyrophosphate-linked heptasaccharide for prokaryotic N-linked glycosylation. Proc. Natl Acad. Sci. USA 102, 14255-14259 (2005).
29. Glover KJ, 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).
30. Kelly J, Jarrell H, Millar L et al.: Biosynthesis of the N-linked glycan in Campylobacter jejuni and addition onto protein through block transfer. J. Bacteriol. 188, 2427-2434 (2006).
31. Linton D, Dorrell N, Hitchen PG et al.: Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway. Mol. Microbiol. 55, 1695-1703 (2005).
32. Reid CW, Stupak J, Chen MM, Imperiali B, Li J, Szymanski CM: Affinity-capture tandem mass spectrometric characterization of polyprenyl-linked oligosaccharides: tool to study protein N-glycosylation pathways. Anal. Chem. 80, 5468-5475 (2008).
33. Olivier NB, Chen MM, Behr JR, Imperiali B: In vitro biosynthesis of UDP-N,N′-diacetylbacillosamine by enzymes of the Campylobacter jejuni general protein glycosylation system. Biochemistry 45, 13659-13669 (2006).
34. Olivier NB, Imperiali B: Crystal structure and catalytic mechanism of PglD from Campylobacter jejuni. J. Biol. Chem. 283, 27937-27946 (2008).
35. Schoenhofen IC, McNally DJ, Vinogradov E et al.: Functional characterization of dehydratase/aminotransferase pairs from Helicobacter and Campylobacter: enzymes distinguishing the pseudaminic acid and bacillosamine biosynthetic pathways. J. Biol. Chem. 281, 723-732 (2006).
36. Rangarajan ES, Ruane KM, Sulea T et al.: Structure and active site residues of PglD, an N-acetyltransferase from the bacillosamine synthetic pathway requited for N-glycan synthesis in Campylobacter jejuni. Biochemistry 47, 1827-1836 (2008).
37. Alaimo C, Catrein I, Morf L et al.: Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J. 25, 967-976 (2006).
38. Igura M, Maita N, Kamishikiryo J et al.: Structure-guided identification of a new catalytic motif of oligosaccharyltransferase. EMBO J. 27, 234-243 (2008).
39. Nita-Lazar M, Wacker M, Schegg B, Amber S, Aebi M: The N-X-S/T consensus sequence is required but not sufficient for bacterial N-linked protein glycosylation. Glycobiology 15, 361-367 (2005).
40. Weerapana E, Imperiali B: Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems. Glycobiology 16, 91R-101R (2006).
41. Yan Q, Lennarz WJ: Studies on the function of oligosaccharyl transferase subunits. Stt3p is directly involved in the glycosylation-process. J. Biol. Chem. 277, 47692-47700 (2002).
42. Szymanski CM, Michael FS, Jarrell HC et al.: Detection of conserved N-linked glycans and phase-variable lipooligosaccharides and capsules from Campylobacter cells by mass spectrometry and high resolution magic angle spinning NMR spectroscopy. J. Biol. Chem. 278, 24509-24520 (2003).
43. Karlyshev AV, Everest P, Linton D, Cawthraw S, Newell DG, Wren BW: The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150, 1957-1964 (2004).
44. Larsen JC, Szymanski C, Guerry P: N-linked protein glycosylation is required for full competence in Campylobacter jejuni 81-176. J. Bacteriol. 186, 6508-6514 (2004).
45. Wyszynska A, Wronowska W, Lasica AM, Tomczyk K, Przanowski P, Jagusztyn-Krynicka EK: Glycosylation of C. jejuni disulfide oxidoreductase Dsbl. in zoonoses and public health. Presented at: 14th International Workshop on Campylobacter, Helicobacter and Related Organisms. Rotterdam, The Netherlands, September (2007).
46. Davis LM, Kakuda T, Dirita VJ: A Campylobacter jejuni znuA ortholog is essential for growth in low-zinc environments and chick colonization. J. Bacteriol. 191, 1631-1640 (2009).
47. Helenius A, Aebi M: Intracellular functions of N-linked glycans. Science 291, 2364-2369 (2001).
48. Herrmann JL, O'Gaora P, Gallagher A, Thole JE, Young DB: Bacterial glycoproteins: a link between glycosylation and proteolytic cleavage of a 19 kDa antigen from Mycobacterium tuberculosis. EMBO J. 15, 3547-3554 (1996).
49. Liu X, McNally DJ, Nothaft H, Szymanski CM, Brisson JR, Li J: Mass spectrometry-based glycomics strategy for exploring N-linked glycosylation in eukaryotes and bacteria. Anal. Chem. 78, 6081-6087 (2006).
50. Aebi M, Hennet T: Congenital disorders of glycosylation: genetic model systems lead the way. Trends Cell. Biol. 11, 136-141 (2001).
51. Barnes G, Hansen WJ, Holcomb CL, Rine J: Asparagine-linked glycosylation in Saccharomyces cerevisiae: genetic analysis of an early step. Mol. Cell. Biol. 4, 2381-2388 (1984).
52. Hortin G, Boime I: Inhibition of asparagine-linked glycosylation by incorporation of a threonine analog into nascent peptide chains. J. Biol. Chem. 255, 8007-8010 (1980).
53. Parodi AJ, Behrens NH, Leloir LF, Carminatti H: The role of polyprenol-bound saccharides as intermediates in glycoprotein synthesis in liver. Proc. Natl Acad. Sci. USA 69, 3268-3272 (1972).
54. Alton G, Hasilik M, Niehues R et al.: Direct utilization of mannose for mammalian glycoprotein biosynthesis. Glycobiology 8, 285-295 (1998).
55. Westphal V, Srikrishna G, Freeze HH: Congenital disorders of glycosylation: have you encountered them? Genet. Med. 2, 329-337 (2000).
56. Kelleher DJ, Gilmore R: An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16, 47R-62R (2006).
57. Plavner N, Eichler J: Defining the topology of the N-glycosylation pathway in the halophilic archaeon Haloferax volcanii. J. Bacteriol. 190, 8045-8052 (2008).
58. 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).
59. Zhu BC, Drake RR, Schweingruber H, Laine RA: Inhibition of glycosylation by amphomycin and sugar nucleotide analogs PP36 and PP55 indicates that Haloferax volcanii β-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 (1995).
60. Zeitler R, Hochmuth E, Deutzmann R, Sumper M: 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 (1998).
61. O'Connor SE, Imperiali B: Modulation of protein structure and function by asparagine-linked glycosylation. Chem. Biol. 3, 803-812 (1996).
62. Schulz BL, Aebi M: Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency. Mol. Cell. Proteomics 8(2), 357-364 (2008).
63. Rangarajan ES, Bhatia S, Watson DC et al.: Structural context for protein N-glycosylation in bacteria: the structure of PEB3, an adhesin from Campylobacter jejuni. Protein Sci. 16, 990-995 (2007).
64. Petrescu AJ, Milac AL, Petrescu SM, Dwek RA, Wormald MR: Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology 14, 103-114 (2004).
65. Chen MM, Glover KJ, Imperiali B: From peptide to protein: comparative analysis of the substrate specificity of N-linked glycosylation in C. jejuni. Biochemistry 46, 5579-5585 (2007).
66. Weerapana E, Glover KJ, Chen MM, Imperiali B: Investigating bacterial N-linked glycosylation: synthesis and glycosyl acceptor activity of the undecaprenyl pyrophosphate-linked bacillosamine. J. Am. Chem. Soc. 127, 13766-13767 (2005).
67. Leonard EE 2nd, Takata T, Blaser MJ, Falkow S, Tompkins LS, Gaynor EC: Use of an open-reading frame-specific Campylobacter jejuni DNA microarray as a new genotyping tool for studying epidemiologically related isolates. J. Infect. Dis. 187, 691-694 (2003).
68. Pearson BM, Pin C, Wright J, I'Anson K, Humphrey T, Wells JM: Comparative genome analysis of Campylobacter jejuni using whole genome DNA microarrays. FEBS Lett. 554, 224-230 (2003).
69. Taboada EN, Acedillo RR, Carrillo CD et al.: Large-scale comparative genomics meta-analysis of Campylobacter jejuni isolates reveals low level of genome plasticity. J. Clin. Microbiol. 42, 4566-4576 (2004).
70. Baar C, Eppinger M, Raddatz G et al.: Complete genome sequence and analysis of Wolinella succinogenes. Proc. Natl Acad. Sci. USA 100, 11690-11695 (2003).
71. Burnens AP, Stanley J, Morgenstern R, Nicolet J: Gastroenteritis associated with Helicobacter pullorum. Lancet 344, 1569-1570 (1994).
72. Stanley J, Linton D, Burnens AP et al.: Helicobacter pullorum sp. nov.-genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology 140(Pt 12), 3441-3449 (1994).
73. Steinbrueckner B, Haerter G, Pelz K et al.: Isolation of Helicobacter pullorum from patients with enteritis. Scand. J. Infect. Dis. 29, 315-318 (1997).
74. Fox JG, Chien CC, Dewhirst FE et al.: Helicobacter canadensis sp. nov. isolated from humans with diarrhea as an example of an emerging pathogen. J. Clin. Microbiol. 38, 2546-2549 (2000).
75. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K: Deep-sea vent -̇proteobacterial genomes provide insights into emergence of pathogens. Proc. Natl Acad. Sci. USA 104, 12146-12150 (2007).
76. Campbell BJ, Engel AS, Porter ML, Takai K: The versatile -̇proteobacteria: key players in snlphidic habitats. Nat. Rev. Microbiol. 4, 458-468 (2006).
77. Feldman MF, Wacker M, Hernandez M et al.: Engineering N-linked protein glycosylation with diverse O-antigen lipopolysaccharide structures in Escherichia coli. Proc. Natl Acad. Sci. USA 102, 3016-3021 (2005).
78. Wacker M, Feldman MF, Callewaert N et al.: Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems. Proc. Natl Acad. Sci. USA 103, 7088-7093 (2006).
79. Adderson EE: Antibody repertoires in infants and adults: effects of T-independent and T-dependent immunizations. Springer Semin. Immunopathol. 23, 387-403 (2001).
80. Faridmoayer A, Fentabil MA, Mills DC, Klassen JS, Feldman MF: Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J. Bacteriol. 189, 8088-8098 (2007).