Sugar and Spice Make Bacteria Not Nice: Protein Glycosylation and Its Influence in Pathogenesis

Journal of Molecular Biology

Volumn 428, Issue 16, 2016, Pages 3206-3220

  Valguarnera, Ezequiel ^a   Kinsella, Rachel L ^a,b   Feldman, Mario F ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

bacterial glycosyltransferases; bacterial pathogens; glycosyltransferase toxins; oligosaccharyltransferases; protein glycosylation

Indexed keywords

ADHESIN; BACTERIAL TOXIN; GLYCOPROTEIN; LIPOPOLYSACCHARIDE; POLYSACCHARIDE; BACTERIAL PROTEIN; GLYCOSYLTRANSFERASE;

BACTERIAL INFECTION; BACTERIUM ADHERENCE; CAMPYLOBACTER JEJUNI; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVIEW; ANIMAL; BACTERIUM; GLYCOSYLATION; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; GLYCOPROTEINS; GLYCOSYLATION; GLYCOSYLTRANSFERASES; HOST-PATHOGEN INTERACTIONS; HUMANS; POLYSACCHARIDES;

EID: 84964653566     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.04.013     Document Type: Review

References (201)

1. [1] Neuberger, A., Carbohydrates in protein: the carbohydrate component of crystalline egg albumin. Biochem. J. 32 (1938), 1435–1451.
2. [2] Apweiler, R., Hermjakob, H., Sharon, N., On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta. 1473 (1999), 4–8.
3. [3] Sleytr, U.B., Heterologous reattachment of regular arrays of glycoproteins on bacterial surfaces. Nature. 257 (1975), 400–402.
4. [4] Mescher, M.F., Strominger, J.L., Structural (shape-maintaining) role of the cell surface glycoprotein of Halobacterium salinarum. Proc. Natl. Acad. Sci. U. S. A. 73 (1976), 2687–2691.
5. [5] Zarschler, K., Janesch, B., Pabst, M., Altmann, F., Messner, P., Schaffer, C., Protein tyrosine O-glycosylation—a rather unexplored prokaryotic glycosylation system. Glycobiology. 20 (2010), 787–798.
6. [6] Ristl, R., Janesch, B., Anzengruber, J., Forsthuber, A., Blaha, J., Messner, P., et al. Description of a putative oligosaccharyl:S-layer protein transferase from the tyrosine-glycosylation system of CCM 2051. Adv. Microbiol. 2 (2012), 537–546.
7. [7] Janesch, B., Schirmeister, F., Maresch, D., Altmann, F., Messner, P., Kolarich, D., et al. Flagellin glycosylation in Paenibacillus alvei CCM 2051 T. Glycobiology. 26 (2016), 74–87.
8. [8] Hug, I., Feldman, M.F., Analogies and homologies in lipopolysaccharide and glycoprotein biosynthesis in bacteria. Glycobiology. 21 (2011), 138–151.
9. [9] Aebi, M., N-linked protein glycosylation in the ER. Biochim. Biophys. Acta. 1833 (2013), 2430–2437.
10. [10] Linton, D., Dorrell, N., Hitchen, P.G., Amber, S., Karlyshev, A.V., Morris, H.R., et al. Functional analysis of the Campylobacter jejuni N-linked protein glycosylation pathway. Mol. Microbiol. 55 (2005), 1695–1703.
11. [11] Wacker, M., Feldman, M.F., Callewaert, N., Kowarik, M., Clarke, B.R., Pohl, N.L., et al. Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 7088–7093.
12. [12] Thibault, P., Logan, S.M., Kelly, J.F., Brisson, J.R., Ewing, C.P., Trust, T.J., et al. Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem. 276:34 (2001), 862–870.
13. [13] Schirm, M., Arora, S.K., Verma, A., Vinogradov, E., Thibault, P., Ramphal, R., et al. Structural and genetic characterization of glycosylation of type a flagellin in Pseudomonas aeruginosa. J. Bacteriol. 186 (2004), 2523–2531.
14. [14] Taguchi, F., Takeuchi, K., Katoh, E., Murata, K., Suzuki, T., Marutani, M., et al. Identification of glycosylation genes and glycosylated amino acids of flagellin in Pseudomonas syringae pv. tabaci. Cell. Microbiol. 8 (2006), 923–938.
15. [15] Dell, A., Galadari, A., Sastre, F., Hitchen, P., Similarities and differences in the glycosylation mechanisms in prokaryotes and eukaryotes. Int. J. Microbiol., 2010, 2010, 148,178.
16. [16] Scott, N.E., Kinsella, R.L., Edwards, A.V., Larsen, M.R., Dutta, S., Saba, J., et al. Diversity within the O-linked protein glycosylation systems of acinetobacter species. Mol. Cell. Proteomics. 13 (2014), 2354–2370.
17. [17] Jarrell, K.F., Ding, Y., Meyer, B.H., Albers, S.V., Kaminski, L., Eichler, J., N-linked glycosylation in archaea: a structural, functional, and genetic analysis. Microbiol. Mol. Biol. Rev. 78 (2014), 304–341.
18. [18] 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 (1999), 1022–1030.
19. [19] Kaakoush, N.O., Castano-Rodriguez, N., Mitchell, H.M., Man, S.M., Global epidemiology of Campylobacter infection. Clin. Microbiol. Rev. 28 (2015), 687–720.
20. [20] Nyati, K.K., Nyati, R., Role of Campylobacter jejuni infection in the pathogenesis of Guillain–Barre syndrome: an update. Biomed. Res. Int., 2013, 2013, 852,195.
21. [21] Scott, N.E., Parker, B.L., Connolly, A.M., Paulech, J., Edwards, A.V., Crossett, B., et al. Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, higher energy collisional dissociation, and electron transfer dissociation MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol. Cell. Proteomics. 10 (2011), M000031–MMCP201.
22. [22] Szymanski, C.M., Burr, D.H., Guerry, P., Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 70 (2002), 2242–2244.
23. [23] Alemka, A., Nothaft, H., Zheng, J., Szymanski, C.M., N-glycosylation of Campylobacter jejuni surface proteins promotes bacterial fitness. Infect. Immun. 81 (2013), 1674–1682.
24. [24] Morrison, M.J., Imperiali, B., The renaissance of bacillosamine and its derivatives: pathway characterization and implications in pathogenicity. Biochemistry. 53 (2014), 624–638.
25. [25] Riegert, A.S., Young, N.M., Watson, D.C., Thoden, J.B., Holden, H.M., Structure of the external aldimine form of PglE, an aminotransferase required for N,N′-diacetylbacillosamine biosynthesis. Protein Sci. 24 (2015), 1609–1616.
26. [26] Larkin, A., Imperiali, B., The expanding horizons of asparagine-linked glycosylation. Biochemistry. 50 (2011), 4411–4426.
27. [27] Nothaft, H., Szymanski, C.M., Bacterial protein N-glycosylation: new perspectives and applications. J. Biol. Chem. 288 (2013), 6912–6920.
28. [28] Perez, C., Gerber, S., Boilevin, J., Bucher, M., Darbre, T., Aebi, M., et al. Structure and mechanism of an active lipid-linked oligosaccharide flippase. Nature. 524 (2015), 433–438.
29. [29] Cullen, T.W., Trent, M.S., A link between the assembly of flagella and lipooligosaccharide of the Gram-negative bacterium Campylobacter jejuni. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 5160–5165.
30. [30] Scott, N.E., Nothaft, H., Edwards, A.V., Labbate, M., Djordjevic, S.P., Larsen, M.R., et al. Modification of the Campylobacter jejuni N-linked glycan by EptC protein-mediated addition of phosphoethanolamine. J. Biol. Chem. 287:29 (2012), 384–396.
31. [31] Golden, N.J., Acheson, D.W., Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect. Immun. 70 (2002), 1761–1771.
32. [32] Nothaft, H., Scott, N.E., Vinogradov, E., Liu, X., Hu, R., Beadle, B., et al. Diversity in the protein N-glycosylation pathways within the Campylobacter genus. Mol. Cell. Proteomics. 11 (2012), 1203–1219.
33. [33] Jervis, A.J., Butler, J.A., Lawson, A.J., Langdon, R., Wren, B.W., Linton, D., Characterization of the structurally diverse N-linked glycans of Campylobacter species. J. Bacteriol. 194 (2012), 2355–2362.
34. [34] Jervis, A.J., Langdon, R., Hitchen, P., Lawson, A.J., Wood, A., Fothergill, J.L., et al. Characterization of N-linked protein glycosylation in Helicobacter pullorum. J. Bacteriol. 192 (2010), 5228–5236.
35. [35] Hug, I., Couturier, M.R., Rooker, M.M., Taylor, D.E., Stein, M., Feldman, M.F., Helicobacter pylori lipopolysaccharide is synthesized via a novel pathway with an evolutionary connection to protein N-glycosylation. PLoS Pathog., 6, 2010, e1000819.
36. [36] Ielmini, M.V., Feldman, M.F., Desulfovibrio desulfuricans PglB homolog possesses oligosaccharyltransferase activity with relaxed glycan specificity and distinct protein acceptor sequence requirements. Glycobiology. 21 (2011), 734–742.
37. [37] Santos-Silva, T., Dias, J.M., Dolla, A., Durand, M.C., Goncalves, L.L., Lampreia, J., et al. Crystal structure of the 16 heme cytochrome from Desulfovibrio gigas: a glycosylated protein in a sulphate-reducing bacterium. J. Mol. Biol. 370 (2007), 659–673.
38. [38] Mills, D.C., Jervis, A.J., Abouelhadid, S., Yates, L.E., Cuccui, J., Linton, D., et al. Functional analysis of N-linking oligosaccharyl transferase enzymes encoded by deep-sea vent proteobacteria. Glycobiology. 26 (2016), 398–409.
39. [39] Feldman, M.F., Wacker, M., Hernandez, M., Hitchen, P.G., Marolda, C.L., Kowarik, M., et al. Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 3016–3021.
40. [40] Schwarz, F., Lizak, C., Fan, Y.Y., Fleurkens, S., Kowarik, M., Aebi, M., Relaxed acceptor site specificity of bacterial oligosaccharyltransferase in vivo. Glycobiology. 21 (2011), 45–54.
41. [41] Scott, N.E., Marzook, N.B., Cain, J.A., Solis, N., Thaysen-Andersen, M., Djordjevic, S.P., et al. Comparative proteomics and glycoproteomics reveal increased N-linked glycosylation and relaxed sequon specificity in Campylobacter jejuni NCTC11168 O. J. Proteome Res. 13 (2014), 5136–5150.
42. [42] Wacker, M., Linton, D., Hitchen, P.G., Nita-Lazar, M., Haslam, S.M., North, S.J., et al. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science. 298 (2002), 1790–1793.
43. [43] Kowarik, M., Numao, S., Feldman, M.F., Schulz, B.L., Callewaert, N., Kiermaier, E., et al. N-linked glycosylation of folded proteins by the bacterial oligosaccharyltransferase. Science. 314 (2006), 1148–1150.
44. [44] Gerber, S., Lizak, C., Michaud, G., Bucher, M., Darbre, T., Aebi, M., et al. Mechanism of bacterial oligosaccharyltransferase: in vitro quantification of sequon binding and catalysis. J. Biol. Chem. 288 (2013), 8849–8861.
45. [45] Ciocchini, A.E., Rey Serantes, D.A., Melli, L.J., Iwashkiw, J.A., Deodato, B., Wallach, J., et al. Development and validation of a novel diagnostic test for human brucellosis using a glyco-engineered antigen coupled to magnetic beads. PLoS Negl. Trop. Dis., 7, 2013, e2048.
46. [46] Iwashkiw, J.A., Fentabil, M.A., Faridmoayer, A., Mills, D.C., Peppler, M., Czibener, C., et al. Exploiting the Campylobacter jejuni protein glycosylation system for glycoengineering vaccines and diagnostic tools directed against brucellosis. Microb. Cell Factories., 11, 2012, 13.
47. [47] Melli, L.J., Ciocchini, A.E., Caillava, A.J., Vozza, N., Chinen, I., Rivas, M., et al. Serogroup-specific bacterial engineered glycoproteins as novel antigenic targets for diagnosis of shiga toxin-producing-Escherichia coli-associated hemolytic-uremic syndrome. J. Clin. Microbiol. 53 (2015), 528–538.
48. [48] Garcia-Quintanilla, F., Iwashkiw, J.A., Price, N.L., Stratilo, C., Feldman, M.F., Production of a recombinant vaccine candidate against Burkholderia pseudomallei exploiting the bacterial N-glycosylation machinery. Front. Microbiol., 5, 2014, 381.
49. [49] Ravenscroft, N., Haeuptle, M.A., Kowarik, M., Fernandez, F.S., Carranza, P., Brunner, A., et al. Purification and characterization of a Shigella conjugate vaccine, produced by glycoengineering Escherichia coli. Glycobiology. 26 (2016), 51–62.
50. [50] Kampf, M.M., Braun, M., Sirena, D., Ihssen, J., Thony-Meyer, L., Ren, Q., In vivo production of a novel glycoconjugate vaccine against Shigella flexneri 2a in recombinant Escherichia coli: identification of stimulating factors for in vivo glycosylation. Microb. Cell Factories., 14, 2015, 12.
51. [51] Hatz, C.F., Bally, B., Rohrer, S., Steffen, R., Kramme, S., Siegrist, C.A., et al. Safety and immunogenicity of a candidate bioconjugate vaccine against Shigella dysenteriae type 1 administered to healthy adults: a single blind, partially randomized Phase I study. Vaccine. 33 (2015), 4594–4601.
52. [52] Wacker, M., Wang, L., Kowarik, M., Dowd, M., Lipowsky, G., Faridmoayer, A., et al. Prevention of Staphylococcus aureus infections by glycoprotein vaccines synthesized in Escherichia coli. J. Infect. Dis. 209 (2014), 1551–1561.
53. [53] Wetter, M., Kowarik, M., Steffen, M., Carranza, P., Corradin, G., Wacker, M., Engineering, conjugation, and immunogenicity assessment of Escherichia coli O121 O antigen for its potential use as a typhoid vaccine component. Glycoconj. J. 30 (2013), 511–522.
54. [54] Ollis, A.A., Chai, Y., Natarajan, A., Perregaux, E., Jaroentomeechai, T., Guarino, C., et al. Substitute sweeteners: diverse bacterial oligosaccharyltransferases with unique N-glycosylation site preferences. Sci. Rep., 5, 2015, 15,237.
55. [55] Nothaft, H., Liu, X., McNally, D.J., Li, J., Szymanski, C.M., Study of free oligosaccharides derived from the bacterial N-glycosylation pathway. Proc. Natl. Acad. Sci. U. S. A. 106:15 (2009), 019–024.
56. [56] Dwivedi, R., Nothaft, H., Reiz, B., Whittal, R.M., Szymanski, C.M., Generation of free oligosaccharides from bacterial protein N-linked glycosylation systems. Biopolymers. 99 (2013), 772–783.
57. [57] Iwashkiw, J.A., Vozza, N.F., Kinsella, R.L., Feldman, M.F., Pour some sugar on it: the expanding world of bacterial protein O-linked glycosylation. Mol. Microbiol. 89 (2013), 14–28.
58. [58] Castric, P., pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology. 141:Pt 5 (1995), 1247–1254.
59. [59] Virji, M., Saunders, J.R., Sims, G., Makepeace, K., Maskell, D., Ferguson, D.J., Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol. Microbiol. 10 (1993), 1013–1028.
60. [60] Stimson, E., Virji, M., Makepeace, K., Dell, A., Morris, H.R., Payne, G., et al. Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol. Microbiol. 17 (1995), 1201–1214.
61. [61] Banerjee, A., Ghosh, S.K., The role of pilin glycan in neisserial pathogenesis. Mol. Cell. Biochem. 253 (2003), 179–190.
62. [62] Cagatay, T.I., Hickford, J.G., Glycosylation of type-IV fimbriae of Dichelobacter nodosus. Vet. Microbiol. 126 (2008), 160–167.
63. [63] Vik, A., Aas, F.E., Anonsen, J.H., Bilsborough, S., Schneider, A., Egge-Jacobsen, W., et al. Broad spectrum O-linked protein glycosylation in the human pathogen Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 4447–4452.
64. [64] Egge-Jacobsen, W., Salomonsson, E.N., Aas, F.E., Forslund, A.L., Winther-Larsen, H.C., Maier, J., et al. O-linked glycosylation of the PilA pilin protein of Francisella tularensis: identification of the endogenous protein-targeting oligosaccharyltransferase and characterization of the native oligosaccharide. J. Bacteriol. 193 (2011), 5487–5497.
65. [65] Elhenawy, W., Scott, N.E., Tondo, M.L., Orellano, E.G., Foster, L.J., Feldman, M.F., Protein O-linked glycosylation in the plant pathogen Ralstonia solanacearum. Glycobiology., 2015.
66. [66] Fletcher, C.M., Coyne, M.J., OF, V., Chatzidaki-Livanis, M., Comstock, L.E., A general O-glycosylation system important to the physiology of a major human intestinal symbiont. Cell. 137 (2009), 321–331.
67. [67] Gallagher, A., Aduse-Opoku, J., Rangarajan, M., Slaney, J.M., Curtis, M.A., Glycosylation of the Arg-gingipains of Porphyromonas gingivalis and comparison with glycoconjugate structure and synthesis in other bacteria. Curr. Protein Pept. Sci. 4 (2003), 427–441.
68. [68] Iwashkiw, J.A., Seper, A., Weber, B.S., Scott, N.E., Vinogradov, E., Stratilo, C., et al. Identification of a general O-linked protein glycosylation system in Acinetobacter baumannii and its role in virulence and biofilm formation. PLoS Pathog., 8, 2012, e1002758.
69. [69] Lithgow, K.V., Scott, N.E., Iwashkiw, J.A., Thomson, E.L., Foster, L.J., Feldman, M.F., et al. A general protein O-glycosylation system within the Burkholderia cepacia complex is involved in motility and virulence. Mol. Microbiol. 92 (2014), 116–137.
70. [70] Gebhart, C., Ielmini, M.V., Reiz, B., Price, N.L., Aas, F.E., Koomey, M., et al. Characterization of exogenous bacterial oligosaccharyltransferases in Escherichia coli reveals the potential for O-linked protein glycosylation in Vibrio cholerae and Burkholderia thailandensis. Glycobiology. 22 (2012), 962–974.
71. [71] Harding, C.M., Nasr, M.A., Kinsella, R.L., Scott, N.E., Foster, L.J., Weber, B.S., et al. Acinetobacter strains carry two functional oligosaccharyltransferases, one devoted exclusively to type IV pilin, and the other one dedicated to O-glycosylation of multiple proteins. Mol. Microbiol. 96 (2015), 1023–1041.
72. [72] Power, P.M., Seib, K.L., Jennings, M.P., Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli. Biochem. Biophys. Res. Commun. 347 (2006), 904–908.
73. [73] Lees-Miller, R.G., Iwashkiw, J.A., Scott, N.E., Seper, A., Vinogradov, E., Schild, S., et al. A common pathway for O-linked protein-glycosylation and synthesis of capsule in Acinetobacter baumannii. Mol. Microbiol. 89 (2013), 816–830.
74. [74] Castric, P., Cassels, F.J., Carlson, R.W., Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J. Biol. Chem. 276:26 (2001), 479–485.
75. [75] Faridmoayer, A., Fentabil, M.A., Mills, D.C., Klassen, J.S., Feldman, M.F., Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J. Bacteriol. 189 (2007), 8088–8098.
76. [76] Horzempa, J., Comer, J.E., Davis, S.A., Castric, P., Glycosylation substrate specificity of Pseudomonas aeruginosa 1244 pilin. J. Biol. Chem. 281 (2006), 1128–1136.
77. [77] Horzempa, J., Dean, C.R., Goldberg, J.B., Castric, P., Pseudomonas aeruginosa 1244 pilin glycosylation: glycan substrate recognition. J. Bacteriol. 188 (2006), 4244–4252.
78. [78] Qutyan, M., Paliotti, M., Castric, P., PilO of Pseudomonas aeruginosa 1244: subcellular location and domain assignment. Mol. Microbiol. 66 (2007), 1444–1458.
79. [79] Faridmoayer, A., Fentabil, M.A., Haurat, M.F., Yi, W., Woodward, R., Wang, P.G., et al. Extreme substrate promiscuity of the Neisseria oligosaccharyl transferase involved in protein O-glycosylation. J. Biol. Chem. 283:34 (2008), 596–604.
80. [80] Musumeci, M.A., Ielmini, M.V., Feldman, M.F., In vitro glycosylation assay for bacterial oligosaccharyltransferases. Methods Mol. Biol. 1022 (2013), 161–171.
81. [81] Musumeci, M.A., Faridmoayer, A., Watanabe, Y., Feldman, M.F., Evaluating the role of conserved amino acids in bacterial O-oligosaccharyltransferases by in vivo, in vitro and limited proteolysis assays. Glycobiology. 24 (2014), 39–50.
82. [82] Musumeci, M.A., Hug, I., Scott, N.E., Ielmini, M.V., Foster, L.J., Wang, P.G., et al. In vitro activity of Neisseria meningitidis PglL O-oligosaccharyltransferase with diverse synthetic lipid donors and a UDP-activated sugar. J. Biol. Chem. 288:10 (2013), 578–587.
83. [83] Fletcher, C.M., Coyne, M.J., Comstock, L.E., Theoretical and experimental characterization of the scope of protein O-glycosylation in Bacteroides fragilis. J. Biol. Chem. 286 (2011), 3219–3226.
84. [84] Posch, G., Pabst, M., Brecker, L., Altmann, F., Messner, P., Schaffer, C., Characterization and scope of S-layer protein O-glycosylation in Tannerella forsythia. J. Biol. Chem. 286:38 (2011), 714–724.
85. [85] Posch, G., Pabst, M., Neumann, L., Coyne, M.J., Altmann, F., Messner, P., et al. “Cross-glycosylation” of proteins in Bacteroidales species. Glycobiology. 23 (2013), 568–577.
86. [86] Jennings, M.P., Jen, F.E., Roddam, L.F., Apicella, M.A., Edwards, J.L., Neisseria gonorrhoeae pilin glycan contributes to CR3 activation during challenge of primary cervical epithelial cells. Cell. Microbiol. 13 (2011), 885–896.
87. [87] McCann, J.R., St Geme, J.W. 3rd., The HMW1C-like glycosyltransferases—an enzyme family with a sweet tooth for simple sugars. PLoS Pathog., 10, 2014, e1003977.
88. [88] Leo, J.C., Grin, I., Linke, D., Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 367 (2012), 1088–1101.
89. [89] Sijbrandi, R., Urbanus, M.L., ten Hagen-Jongman, C.M., Bernstein, H.D., Oudega, B., Otto, B.R., et al. Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J. Biol. Chem. 278 (2003), 4654–4659.
90. [90] Brandon, L.D., Goehring, N., Janakiraman, A., Yan, A.W., Wu, T., Beckwith, J., et al. IcsA, a polarly localized autotransporter with an atypical signal peptide, uses the Sec apparatus for secretion, although the Sec apparatus is circumferentially distributed. Mol. Microbiol. 50 (2003), 45–60.
91. [91] Peterson, J.H., Szabady, R.L., Bernstein, H.D., An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J. Biol. Chem. 281 (2006), 9038–9048.
92. [92] Konieczny, M.P.J., Benz, I., Hollinderbaumer, B., Beinke, C., Niederweis, M., Schmidt, M.A., Modular organization of the AIDA autotransporter translocator: the N-terminal beta1-domain is surface-exposed and stabilizes the transmembrane beta2-domain. Antonie Van Leeuwenhoek. 80 (2001), 19–34.
93. [93] Oomen, C.J., van Ulsen, P., van Gelder, P., Feijen, M., Tommassen, J., Gros, P., Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23 (2004), 1257–1266.
94. [94] Grass, S., Buscher, A.Z., Swords, W.E., Apicella, M.A., Barenkamp, S.J., Ozchlewski, N., et al. The Haemophilus influenzae HMW1 adhesin is glycosylated in a process that requires HMW1C and phosphoglucomutase, an enzyme involved in lipooligosaccharide biosynthesis. Mol. Microbiol. 48 (2003), 737–751.
95. [95] Grass, S., Lichti, C.F., Townsend, R.R., Gross, J., St Geme, J.W. 3rd., The Haemophilus influenzae HMW1C protein is a glycosyltransferase that transfers hexose residues to asparagine sites in the HMW1 adhesin. PLoS Pathog., 6, 2010, e1000919.
96. [96] Gross, J., Grass, S., Davis, A.E., Gilmore-Erdmann, P., Townsend, R.R., St Geme, J.W. 3rd., The Haemophilus influenzae HMW1 adhesin is a glycoprotein with an unusual N-linked carbohydrate modification. J. Biol. Chem. 283:26 (2008), 010–015.
97. [97] St Geme, J.W. 3rd, Falkow, S., Barenkamp, S.J., High-molecular-weight proteins of nontypable Haemophilus influenzae mediate attachment to human epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 2875–2879.
98. [98] St Geme, J.W. 3rd, Grass, S., Secretion of the Haemophilus influenzae HMW1 and HMW2 adhesins involves a periplasmic intermediate and requires the HMWB and HMWC proteins. Mol. Microbiol. 27 (1998), 617–630.
99. [99] Fleckenstein, J.M., Roy, K., Fischer, J.F., Burkitt, M., Identification of a two-partner secretion locus of enterotoxigenic Escherichia coli. Infect. Immun. 74 (2006), 2245–2258.
100. [100] Nelson, K.M., Young, G.M., Miller, V.L., Identification of a locus involved in systemic dissemination of Yersinia enterocolitica. Infect. Immun. 69 (2001), 6201–6208.
101. [101] Schwarz, F., Fan, Y.Y., Schubert, M., Aebi, M., Cytoplasmic N-glycosyltransferase of Actinobacillus pleuropneumoniae is an inverting enzyme and recognizes the NX(S/T) consensus sequence. J. Biol. Chem. 286:35 (2011), 267–274.
102. [102] Kawai, F., Grass, S., Kim, Y., Choi, K.J., St Geme, J.W. 3rd, Yeo, H.J., Structural insights into the glycosyltransferase activity of the Actinobacillus pleuropneumoniae HMW1C-like protein. J. Biol. Chem. 286:38 (2011), 546–557.
103. [103] Naegeli, A., Michaud, G., Schubert, M., Lin, C.W., Lizak, C., Darbre, T., et al. Substrate specificity of cytoplasmic N-glycosyltransferase. J. Biol. Chem. 289:24 (2014), 521–532.
104. [104] Naegeli, A., Neupert, C., Fan, Y.Y., Lin, C.W., Poljak, K., Papini, A.M., et al. Molecular analysis of an alternative N-glycosylation machinery by functional transfer from Actinobacillus pleuropneumoniae to Escherichia coli. J. Biol. Chem. 289 (2014), 2170–2179.
105. [105] Rempe, K.A., Spruce, L.A., Porsch, E.A., Seeholzer, S.H., Norskov-Lauritsen, N., St Geme, J.W. 3rd., Unconventional N-Linked glycosylation promotes trimeric autotransporter function in Kingella kingae and Aggregatibacter aphrophilus. MBio, 6, 2015.
106. [106] Chaban, B., Hughes, H.V., Beeby, M., The flagellum in bacterial pathogens: for motility and a whole lot more. Semin. Cell Dev. Biol. 46 (2015), 91–103.
107. [107] Rossez, Y., Wolfson, E.B., Holmes, A., Gally, D.L., Holden, N.J., Bacterial flagella: twist and stick, or dodge across the kingdoms. PLoS Pathog., 11, 2015, e1004483.
108. [108] Logan, S.M., Flagellar glycosylation—a new component of the motility repertoire?. Microbiology. 152 (2006), 1249–1262.
109. [109] Schirm, M., Kalmokoff, M., Aubry, A., Thibault, P., Sandoz, M., Logan, S.M., Flagellin from Listeria monocytogenes is glycosylated with beta-O-linked N-acetylglucosamine. J. Bacteriol. 186 (2004), 6721–6727.
110. [110] Twine, S.M., Paul, C.J., Vinogradov, E., McNally, D.J., Brisson, J.R., Mullen, J.A., et al. Flagellar glycosylation in Clostridium botulinum. FEBS J. 275 (2008), 4428–4444.
111. [111] Twine, S.M., Reid, C.W., Aubry, A., McMullin, D.R., Fulton, K.M., Austin, J., et al. Motility and flagellar glycosylation in Clostridium difficile. J. Bacteriol. 191 (2009), 7050–7062.
112. [112] Schirm, M., Schoenhofen, I.C., Logan, S.M., Waldron, K.C., Thibault, P., Identification of unusual bacterial glycosylation by tandem mass spectrometry analyses of intact proteins. Anal. Chem. 77 (2005), 7774–7782.
113. [113] Scott, A.E., Twine, S.M., Fulton, K.M., Titball, R.W., Essex-Lopresti, A.E., Atkins, T.P., et al. Flagellar glycosylation in Burkholderia pseudomallei and Burkholderia thailandensis. J. Bacteriol. 193 (2011), 3577–3587.
114. [114] Josenhans, C., Vossebein, L., Friedrich, S., Suerbaum, S., The neuA/flmD gene cluster of Helicobacter pylori is involved in flagellar biosynthesis and flagellin glycosylation. FEMS Microbiol. Lett. 210 (2002), 165–172.
115. [115] Schirm, M., Soo, E.C., Aubry, A.J., Austin, J., Thibault, P., Logan, S.M., Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori. Mol. Microbiol. 48 (2003), 1579–1592.
116. [116] Merino, S., Tomas, J.M., Gram-negative flagella glycosylation. Int. J. Mol. Sci. 15 (2014), 2840–2857.
117. [117] Nothaft, H., Szymanski, C.M., Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8 (2010), 765–778.
118. [118] Takeuchi, K., Taguchi, F., Inagaki, Y., Toyoda, K., Shiraishi, T., Ichinose, Y., Flagellin glycosylation island in Pseudomonas syringae pv. glycinea and its role in host specificity. J. Bacteriol. 185 (2003), 6658–6665.
119. [119] Ewing, C.P., Andreishcheva, E., Guerry, P., Functional characterization of flagellin glycosylation in Campylobacter jejuni 81–176. J. Bacteriol. 191 (2009), 7086–7093.
120. [120] Arora, S.K., Neely, A.N., Blair, B., Lory, S., Ramphal, R., Role of motility and flagellin glycosylation in the pathogenesis of Pseudomonas aeruginosa burn wound infections. Infect. Immun. 73 (2005), 4395–4398.
121. [121] Fulton, K.M., Mendoza-Barbera, E., Twine, S.M., Tomas, J.M., Merino, S., Polar glycosylated and lateral non-glycosylated flagella from Aeromonas hydrophila strain AH-1 (serotype O11). Int. J. Mol. Sci. 16:28 (2015), 255–269.
122. [122] Mahdavi, J., Pirinccioglu, N., Oldfield, N.J., Carlsohn, E., Stoof, J., Aslam, A., et al. A novel O-linked glycan modulates Campylobacter jejuni major outer membrane protein-mediated adhesion to human histo-blood group antigens and chicken colonization. Open Biol., 4, 2014, 130,202.
123. [123] Charbonneau, M.E., Girard, V., Nikolakakis, A., Campos, M., Berthiaume, F., Dumas, F., et al. O-linked glycosylation ensures the normal conformation of the autotransporter adhesin involved in diffuse adherence. J. Bacteriol. 189 (2007), 8880–8889.
124. [124] Diderichsen, B., flu, a metastable gene controlling surface properties of Escherichia coli. J. Bacteriol. 141 (1980), 858–867.
125. [125] Klemm, P., Hjerrild, L., Gjermansen, M., Schembri, M.A., Structure–function analysis of the self-recognizing Antigen 43 autotransporter protein from Escherichia coli. Mol. Microbiol. 51 (2004), 283–296.
126. [126] Knudsen, S.K., Stensballe, A., Franzmann, M., Westergaard, U.B., Otzen, D.E., Effect of glycosylation on the extracellular domain of the Ag43 bacterial autotransporter: enhanced stability and reduced cellular aggregation. Biochem. J. 412 (2008), 563–577.
127. [127] Sherlock, O., Dobrindt, U., Jensen, J.B., Munk Vejborg, R., Klemm, P., Glycosylation of the self-recognizing Escherichia coli Ag43 autotransporter protein. J. Bacteriol. 188 (2006), 1798–1807.
128. [128] Sherlock, O., Vejborg, R.M., Klemm, P., The TibA adhesin/invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect. Immun. 73 (2005), 1954–1963.
129. [129] Benz, I., Schmidt, M.A., Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol. Microbiol. 40 (2001), 1403–1413.
130. [130] Lu, Q., Yao, Q., Xu, Y., Li, L., Li, S., Liu, Y., et al. An iron-containing dodecameric heptosyltransferase family modifies bacterial autotransporters in pathogenesis. Cell Host Microbe. 16 (2014), 351–363.
131. [131] Moormann, C., Benz, I., Schmidt, M.A., Functional substitution of the TibC protein of enterotoxigenic Escherichia coli strains for the autotransporter adhesin heptosyltransferase of the AIDA system. Infect. Immun. 70 (2002), 2264–2270.
132. [132] Cote, J.P., Charbonneau, M.E., Mourez, M., Glycosylation of the Escherichia coli TibA self-associating autotransporter influences the conformation and the functionality of the protein. PLoS ONE., 8, 2013, e80739.
133. [133] Cote, J.P., Mourez, M., Structure–function analysis of the TibA self-associating autotransporter reveals a modular organization. Infect. Immun. 79 (2011), 1826–1832.
134. [134] Charbonneau, M.E., Cote, J.P., Haurat, M.F., Reiz, B., Crepin, S., Berthiaume, F., et al. A structural motif is the recognition site for a new family of bacterial protein O-glycosyltransferases. Mol. Microbiol. 83 (2012), 894–907.
135. [135] Bensing, B.A., Sullam, P.M., An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol. Microbiol. 44 (2002), 1081–1094.
136. [136] Lizcano, A., Sanchez, C.J., Orihuela, C.J., A role for glycosylated serine-rich repeat proteins in Gram-positive bacterial pathogenesis. Mol. Oral Microbiol. 27 (2012), 257–269.
137. [137] Plummer, C., Wu, H., Kerrigan, S.W., Meade, G., Cox, D., Ian Douglas, C.W., A serine-rich glycoprotein of Streptococcus sanguis mediates adhesion to platelets via GPIb. Br. J. Haematol. 129 (2005), 101–109.
138. [138] Samen, U., Eikmanns, B.J., Reinscheid, D.J., Borges, F., The surface protein Srr-1 of Streptococcus agalactiae binds human keratin 4 and promotes adherence to epithelial HEp-2 cells. Infect. Immun. 75 (2007), 5405–5414.
139. [139] Shivshankar, P., Sanchez, C., Rose, L.F., Orihuela, C.J., The Streptococcus pneumoniae adhesin PsrP binds to Keratin 10 on lung cells. Mol. Microbiol. 73 (2009), 663–679.
140. [140] Zhou, M., Wu, H., Glycosylation and biogenesis of a family of serine-rich bacterial adhesins. Microbiology. 155 (2009), 317–327.
141. [141] Bu, S., Li, Y., Zhou, M., Azadin, P., Zeng, M., Fives-Taylor, P., et al. Interaction between two putative glycosyltransferases is required for glycosylation of a serine-rich streptococcal adhesin. J. Bacteriol. 190 (2008), 1256–1266.
142. [142] Zhou, M., Zhu, F., Dong, S., Pritchard, D.G., Wu, H., A novel glucosyltransferase is required for glycosylation of a serine-rich adhesin and biofilm formation by Streptococcus parasanguinis. J. Biol. Chem. 285:12 (2010), 140–148.
143. [143] Nobbs, A.H., Lamont, R.J., Jenkinson, H.F., Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 73 (2009), 407–450 (Table of Contents).
144. [144] Zhang, H., Zhu, F., Yang, T., Ding, L., Zhou, M., Li, J., et al. The highly conserved domain of unknown function 1792 has a distinct glycosyltransferase fold. Nat. Commun., 5, 2014, 4339.
145. [145] Tang, G., Kitten, T., Munro, C.L., Wellman, G.C., Mintz, K.P., EmaA, a potential virulence determinant of Aggregatibacter actinomycetemcomitans in infective endocarditis. Infect. Immun. 76 (2008), 2316–2324.
146. [146] Tang, G., Mintz, K.P., Glycosylation of the collagen adhesin EmaA of Aggregatibacter actinomycetemcomitans is dependent upon the lipopolysaccharide biosynthetic pathway. J. Bacteriol. 192 (2010), 1395–1404.
147. [147] Tang, G., Ruiz, T., Mintz, K.P., O-polysaccharide glycosylation is required for stability and function of the collagen adhesin EmaA of Aggregatibacter actinomycetemcomitans. Infect. Immun. 80 (2012), 2868–2877.
148. [148] Espitia, C., Mancilla, R., Identification, isolation and partial characterization of Mycobacterium tuberculosis glycoprotein antigens. Clin. Exp. Immunol. 77 (1989), 378–383.
149. [149] Espitia, C., Servin-Gonzalez, L., Mancilla, R., New insights into protein O-mannosylation in actinomycetes. Mol. BioSyst. 6 (2010), 775–781.
150. [150] Herrmann, J.L., O'Gaora, P., Gallagher, A., Thole, J.E., Young, D.B., Bacterial glycoproteins: a link between glycosylation and proteolytic cleavage of a 19 kDa antigen from Mycobacterium tuberculosis. EMBO J. 15 (1996), 3547–3554.
151. [151] Michell, S.L., Whelan, A.O., Wheeler, P.R., Panico, M., Easton, R.L., Etienne, A.T., et al. The MPB83 antigen from Mycobacterium bovis contains O-linked mannose and (1–> 3)-mannobiose moieties. J. Biol. Chem. 278:16 (2003), 423–432.
152. [152] Sartain, M.J., Belisle, J.T., N-Terminal clustering of the O-glycosylation sites in the Mycobacterium tuberculosis lipoprotein SodC. Glycobiology. 19 (2009), 38–51.
153. [153] Cooper, H.N., Gurcha, S.S., Nigou, J., Brennan, P.J., Belisle, J.T., Besra, G.S., et al. Characterization of mycobacterial protein glycosyltransferase activity using synthetic peptide acceptors in a cell-free assay. Glycobiology. 12 (2002), 427–434.
154. [154] VanderVen, B.C., Harder, J.D., Crick, D.C., Belisle, J.T., Export-mediated assembly of mycobacterial glycoproteins parallels eukaryotic pathways. Science. 309 (2005), 941–943.
155. [155] Liu, C.F., Tonini, L., Malaga, W., Beau, M., Stella, A., Bouyssie, D., et al. Bacterial protein-O-mannosylating enzyme is crucial for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 6560–6565.
156. [156] Mahne, M., Tauch, A., Puhler, A., Kalinowski, J., 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 Microbiol. Lett. 259 (2006), 226–233.
157. [157] Wehmeier, S., Varghese, A.S., Gurcha, S.S., Tissot, B., Panico, M., Hitchen, P., et al. Glycosylation of the phosphate binding protein, PstS, in Streptomyces coelicolor by a pathway that resembles protein O-mannosylation in eukaryotes. Mol. Microbiol. 71 (2009), 421–433.
158. [158] Hartmann, M., Barsch, A., Niehaus, K., Puhler, A., Tauch, A., Kalinowski, J., The glycosylated cell surface protein Rpf2, containing a resuscitation-promoting factor motif, is involved in intercellular communication of Corynebacterium glutamicum. Arch. Microbiol. 182 (2004), 299–312.
159. [159] Lu, Q., Li, S., Shao, F., Sweet talk: protein glycosylation in bacterial interaction with the host. Trends Microbiol. 23 (2015), 630–641.
160. [160] Jank, T., Belyi, Y., Aktories, K., Bacterial glycosyltransferase toxins. Cell. Microbiol. 17 (2015), 1752–1765.
161. [161] Just, I., Selzer, J., Wilm, M., von Eichel-Streiber, C., Mann, M., Aktories, K., Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature. 375 (1995), 500–503.
162. [162] Just, I., Wilm, M., Selzer, J., Rex, G., von Eichel-Streiber, C., Mann, M., et al. The enterotoxin from Clostridium difficile (ToxA) monoglucosylates the Rho proteins. J. Biol. Chem. 270:13 (1995), 932–936.
163. [163] Just, I., Gerhard, R., Large clostridial cytotoxins. Rev. Physiol. Biochem. Pharmacol. 152 (2004), 23–47.
164. [164] Leffler, D.A., Lamont, J.T., Clostridium difficile infection. N. Engl. J. Med. 372 (2015), 1539–1548.
165. [165] Johanesen, P.A., Mackin, K.E., Hutton, M.L., Awad, M.M., Larcombe, S., Amy, J.M., et al. Disruption of the gut microbiome: Clostridium difficile infection and the threat of antibiotic resistance. Genes 6 (2015), 1347–1360.
166. [166] Yuan, P., Zhang, H., Cai, C., Zhu, S., Zhou, Y., Yang, X., et al. Chondroitin sulfate proteoglycan 4 functions as the cellular receptor for Clostridium difficile toxin B. Cell Res. 25 (2015), 157–168.
167. [167] LaFrance, M.E., Farrow, M.A., Chandrasekaran, R., Sheng, J., Rubin, D.H., Lacy, D.B., Identification of an epithelial cell receptor responsible for Clostridium difficile TcdB-induced cytotoxicity. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 7073–7078.
168. [168] Barth, H., Pfeifer, G., Hofmann, F., Maier, E., Benz, R., Aktories, K., Low pH-induced formation of ion channels by Clostridium difficile toxin B in target cells. J. Biol. Chem. 276:10 (2001), 670–676.
169. [169] Papatheodorou, P., Zamboglou, C., Genisyuerek, S., Guttenberg, G., Aktories, K., Clostridial glucosylating toxins enter cells via clathrin-mediated endocytosis. PLoS ONE, 5, 2010, e10673.
170. [170] Jaffe, A.B., Hall, A., Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21 (2005), 247–269.
171. [171] Selzer, J., Hofmann, F., Rex, G., Wilm, M., Mann, M., Just, I., et al. Clostridium novyi alpha-toxin-catalyzed incorporation of GlcNAc into Rho subfamily proteins. J. Biol. Chem. 271:25 (1996), 173–177.
172. [172] Nagahama, M., Ohkubo, A., Oda, M., Kobayashi, K., Amimoto, K., Miyamoto, K., et al. Clostridium perfringens TpeL glycosylates the Rac and Ras subfamily proteins. Infect. Immun. 79 (2011), 905–910.
173. [173] Jank, T., Bogdanovic, X., Wirth, C., Haaf, E., Spoerner, M., Bohmer, K.E., et al. A bacterial toxin catalyzing tyrosine glycosylation of Rho and deamidation of Gq and Gi proteins. Nat. Struct. Mol. Biol. 20 (2013), 1273–1280.
174. [174] Forst, S., Dowds, B., Boemare, N., Stackebrandt, E., Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51 (1997), 47–72.
175. [175] Rucker, R.R., Redmouth disease of rainbow trout (Salmo gairdneri). Bull. Off. Int. Epizoot. 65 (1966), 825–830.
176. [176] Kumar, G., Menanteau-Ledouble, S., Saleh, M., El-Matbouli, M., Yersinia ruckeri, the causative agent of enteric redmouth disease in fish. Vet. Res., 46, 2015, 103.
177. [177] Heymann, J.B., Bartho, J.D., Rybakova, D., Venugopal, H.P., Winkler, D.C., Sen, A., et al. Three-dimensional structure of the toxin-delivery particle antifeeding prophage of Serratia entomophila. J. Biol. Chem. 288:25 (2013), 276–284.
178. [178] Hurst, M.R., Beard, S.S., Jackson, T.A., Jones, S.M., Isolation and characterization of the Serratia entomophila antifeeding prophage. FEMS Microbiol. Lett. 270 (2007), 42–48.
179. [179] Jank, T., Eckerle, S., Steinemann, M., Trillhaase, C., Schimpl, M., Wiese, S., et al. Tyrosine glycosylation of Rho by Yersinia toxin impairs blastomere cell behaviour in zebrafish embryos. Nat. Commun., 6, 2015, 7807.
180. [180] Fields, B.S., Benson, R.F., Besser, R.E., Legionella and Legionnaires' disease: 25 years of investigation. Clin. Microbiol. Rev. 15 (2002), 506–526.
181. [181] Hoffmann, C., Harrison, C.F., Hilbi, H., The natural alternative: protozoa as cellular models for Legionella infection. Cell. Microbiol. 16 (2014), 15–26.
182. [182] Jjemba, P.K., Johnson, W., Bukhari, Z., LeChevallier, M.W., Occurrence and control of Legionella in recycled water systems. Pathogens (Basel, Switzerland). 4 (2015), 470–502.
183. [183] Ensminger, A.W., Legionella pneumophila, armed to the hilt: justifying the largest arsenal of effectors in the bacterial world. Curr. Opin. Microbiol. 29 (2015), 74–80.
184. [184] Rolando, M., Buchrieser, C., Legionella pneumophila type IV effectors hijack the transcription and translation machinery of the host cell. Trends Cell Biol. 24 (2014), 771–778.
185. [185] Belyi, I., Popoff, M.R., Cianciotto, N.P., Purification and characterization of a UDP-glucosyltransferase produced by Legionella pneumophila. Infect. Immun. 71 (2003), 181–186.
186. [186] Belyi, Y., Niggeweg, R., Opitz, B., Vogelsgesang, M., Hippenstiel, S., Wilm, M., et al. Legionella pneumophila glucosyltransferase inhibits host elongation factor 1 A. Proc. Natl. Acad. Sci. U. S. A. 103:16 (2006), 953–958.
187. [187] Belyi, Y., Stahl, M., Sovkova, I., Kaden, P., Luy, B., Aktories, K., Region of elongation factor 1 A1 involved in substrate recognition by Legionella pneumophila glucosyltransferase Lgt1: identification of Lgt1 as a retaining glucosyltransferase. J. Biol. Chem. 284:20 (2009), 167–174.
188. [188] Belyi, Y., Tabakova, I., Stahl, M., Aktories, K., Lgt: a family of cytotoxic glucosyltransferases produced by Legionella pneumophila. J. Bacteriol. 190 (2008), 3026–3035.
189. [189] Ramakrishnan, V., Ribosome structure and the mechanism of translation. Cell. 108 (2002), 557–572.
190. [190] Heidtman, M., Chen, E.J., Moy, M.Y., Isberg, R.R., Large-scale identification of Legionella pneumophila Dot/Icm substrates that modulate host cell vesicle trafficking pathways. Cell. Microbiol. 11 (2009), 230–248.
191. [191] Huang, L., Boyd, D., Amyot, W.M., Hempstead, A.D., Luo, Z.Q., O'Connor, T.J., et al. The E Block motif is associated with Legionella pneumophila translocated substrates. Cell. Microbiol. 13 (2011), 227–245.
192. [192] Jank, T., Bohmer, K.E., Tzivelekidis, T., Schwan, C., Belyi, Y., Aktories, K., Domain organization of Legionella effector SetA. Cell. Microbiol. 14 (2012), 852–868.
193. [193] Hu, J., Torres, A.G., Enteropathogenic Escherichia coli: foe or innocent bystander?. Clin. Microbiol. Infect. 21 (2015), 729–734.
194. [194] Santos, A.S., Finlay, B.B., Bringing down the host: enteropathogenic and enterohaemorrhagic Escherichia coli effector-mediated subversion of host innate immune pathways. Cell. Microbiol. 17 (2015), 318–332.
195. [195] Wong, A.R., Pearson, J.S., Bright, M.D., Munera, D., Robinson, K.S., Lee, S.F., et al. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol. Microbiol. 80 (2011), 1420–1438.
196. [196] Gao, X., Wang, X., Pham, T.H., Feuerbacher, L.A., Lubos, M.L., Huang, M., et al. NleB, a bacterial effector with glycosyltransferase activity, targets GAPDH function to inhibit NF-kappaB activation. Cell Host Microbe. 13 (2013), 87–99.
197. [197] Li, S., Zhang, L., Yao, Q., Li, L., Dong, N., Rong, J., et al. Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature. 501 (2013), 242–246.
198. [198] Pearson, J.S., Hartland, E.L., A surprising sweetener from enteropathogenic Escherichia coli. Gut Microbes. 5 (2014), 766–769.
199. [199] Lizak, C., Gerber, S., Numao, S., Aebi, M., Locher, K.P., X-ray structure of a bacterial oligosaccharyltransferase. Nature. 474 (2011), 350–355.
200. [200] Lizak, C., Gerber, S., Michaud, G., Schubert, M., Fan, Y.Y., Bucher, M., et al. Unexpected reactivity and mechanism of carboxamide activation in bacterial N-linked protein glycosylation. Nat. Commun., 4, 2013, 2627.
201. [201] Xu, H., Yang, J., Gao, W., Li, L., Li, P., Zhang, L., et al. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature. 513 (2014), 237–241.