Role of Microbial Glycosylation in Host Cell Invasion

Microbial Glycobiology

Volumn , Issue , 2010, Pages 871-883

  Kanipes, Margaret I ^a   Guerry, Patricia ^b  

^a NORTH CAROLINA A AND T STATE UNIVERSITY   (United States)

^b NAVAL MEDICAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882904905     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-374546-0.00044-4     Document Type: Chapter

References (86)

1. Aspinall G.O., Lynch C.M., Pang H., Shaver R.T., Moran A.P. Chemical structures of the core region of Campylobacter jejuni O:3 lipopolysaccharide and an associated polysaccharide. Eur. J. Biochem. 1995, 231:570-578.
2. Bachtiar B.M., Coloe P.J., Fry B.N. Knockout mutagenesis of the kpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium-host interactions. FEMS Immunol. Med. Microbiol. 2007, 49:149-154.
3. Bacon D.J., Szymanski C.M., Burr D.H., Silver R.P., Alm R.A., Guerry P. A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 2001, 40:769-777.
4. Bauer B.A., Stevens M.K., Hansen E.J. Involvement of the Haemophilus ducreyi gmhA gene product in lipooligosaccharide expression and virulence. Infect. Immun. 1998, 66:4290-4298.
5. Bauer B.A., Lumbley S.R., Hansen E.J. Characterization of a WaaF (RfaF) homolog expressed by Haemophilus ducreyi. Infect. Immun. 1999, 67:899-907.
6. 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. 2001, 40:1403-1413.
7. Benz I., Schmidt M.A. Never say never again: protein glycosylation in pathogenic bacteria. Mol. Microbiol. 2002, 45:267-276.
8. Bernatchez S., Szymanski C.M., Ishiyama N., et al. A single bifunctional UDP-GlcNAc/Glc 4-epimerase supports the synthesis of three cell surface glycoconjugates in Campylobacter jejuni. J. Biol. Chem. 2005, 280:4792-4802.
9. Campos M.A., Vargas M.A., Regueiro V., Llompart C.M., Alberti S., Bengoechea J.A. Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect. Immun. 2004, 72:7107-7114.
10. Castric P., Cassels F.J., Carlson R.W. Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J. Biol. Chem. 2001, 276:26479-26485.
11. Chandan V., Logan S.M., Harrison B.A., et al. Characterization of a waaF mutant of Helicobacter pylori strain 26695 provides evidence that an extended polysaccharide structure has a limited role in the invasion of gastric cancer cells. Biochem. Cell. Biol. 2007, 85:582-590.
12. Clement M.-J., Imberty A., Phalipon A., et al. Conformational studies of the O-specific polysaccharide of Shigella flexneri 5a and of four related synthetic pentasaccharide fragments using NMR and molecular modeling. J. Biol. Chem. 2003, 278:47928-47936.
13. Cope L.D., Yogev R., Mertsola J., Argyle J.C., McCracken G.H., Hansen E.J. Effect of mutations in lipooligosaccharide biosynthesis genes on virulence of Haemophilus influenzae type b. Infect. Immun. 1990, 58:2343-2351.
14. Dobos K.M., Swiderek K., Khoo K.H., Brennan P.J., Belisle J.T. Evidence for glycosylation sites on the 45-kilodalton glycoprotein of Mycobacterium tuberculosis. Infect. Immun. 1995, 63:2846-2853.
15. Dzieciatkowska M., Brochu D., van Belkum A., et al. Mass spectrometric analysis of intact lipooligosaccharide: direct evidence for O-acetylated sialic acids and discovery of O-linked glycine expressed by Campylobacter jejuni. Biochemistry 2007, 46:14704-14714.
16. Ernst R.K., Guina T., Miller S.I. How intracellular bacteria survive: surface modifications that promote resistance to host innate immune responses. J. Infect. Dis. 1999, 179(Suppl. 2):S326-S330.
17. Finlay B.B., Starnbach M.N., Francis C.L., et al. Identification and characterization of TnphoA mutants of Salmonella that are unable to pass through a polarized MDCK epithelial cell monolayer. Mol. Microbiol. 1988, 2:757-766.
18. Friedman C., Neiman J., Wegener H., Tauxe R. Epidemiology of Campylobacter jejuni infections in the United States and other industrilaized nations. Campylobacter 2000, 121-138. ASM Press, Washington, DC. 2nd edn. I. Nachamkin, M. Blaser (Eds.).
19. Fry B.N., Feng S., Chen Y.Y., Newell D.G., Coloe P.J., Korolik V. The galE gene of Campylobacter jejuni is involved in lipopolysaccharide synthesis and virulence. Infect. Immun. 2000, 68:2594-2601.
20. Gibson B.W., Campagnari A.A., Melaugh W., et al. Characterization of a transposon Tn916-generated mutant of Haemophilus ducreyi 35000 defective in lipooligosaccharide biosynthesis. J. Bacteriol. 1997, 179:5062-5071.
21. Gilbert M., Karwaski M.F., 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. 2002, 277:327-337.
22. Gronow S., Noah C., Blumenthal A., Lindner B., Brade H. Construction of a deep-rough mutant of Burkholderia cepacia ATCC 25416 and characterization of its chemical and biological properties. J. Biol. Chem. 2003, 278:1647-1655.
23. Guerry P. Campylobacter flagella: not just for motility. Trends Microbiol. 2007, 15:456-461.
24. Guerry P., Ewing C.P., Hickey T.E., Prendergast M.M., Moran A.P. Sialylation of lipooligosaccharide cores affects immunogenicity and serum resistance of Campylobacter jejuni. Infect. Immun. 2000, 68:6656-6662.
25. Guerry P., Szymanski C.M., Prendergast M.M., et al. Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect. Immun. 2002, 70:787-793.
26. Guerry P., Ewing C.P., Schirm M., et al. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 2006, 60:299-311.
27. Guo L., Lim K.B., Poduje C.M., et al. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 1998, 95:189-198.
28. Hendrixson D.R., DiRita V.J. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 2004, 52:471-484.
29. Hoare A., Bittner M., Carter J., et al. The outer core lipopolysaccharide of Salmonella enterica serovar Typhi is required for bacterial entry into epithelial cells. Infect. Immun. 2006, 74:1555-1564.
30. Hoffman J.A., Wass C., Stins M.F., Kim K.S. The capsule supports survival but not traversal of Escherichia coli K1 across the blood-brain barrier. Infect. Immun. 1999, 67:3566-3570.
31. Houliston R.S., Endtz H.P., Yuki N., et al. Identification of a sialate O-acetyltransferase from Campylobacter jejuni: demonstration of direct transfer to the C-9 position of terminal alpha-2, 8-linked sialic acid. J. Biol. Chem. 2006, 281:11480-11486.
32. Jones M.A., Marston K.L., Woodall C.A., et al. Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 2004, 72:3769-3776.
33. Kakuda T., DiRita V.J. Cj1496c encodes a Campylobacter jejuni glycoprotein that influences invasion of human epithelial cells and colonization of the chick gastrointestinal tract. Infect. Immun. 2006, 74:4715-4723.
34. Kanipes M.I., Holder L.C., Corcoran A.T., Moran A.P., Guerry P. A deep-rough mutant of Campylobacter jejuni 81-176 is noninvasive for intestinal epithelial cells. Infect. Immun. 2004, 72:2452-2455.
35. Kanipes M.I., Papp-Szabo E., Guerry P., Monteiro M.A. Mutation of waaC, encoding heptosyltransferase I in Campylobacter jejuni 81-176, affects the structure of both lipooligosaccharide and capsular carbohydrate. J. Bacteriol. 2006, 188:3273-3279.
36. Kanipes M.I., Tan X., Akelaitis A., et al. Genetic analysis of lipooligosaccharide core biosynthesis in Campylobacter jejuni 81-176. J. Bacteriol. 2008, 190:1568-1574.
37. Kihlstrom E., Edebo L. Association of viable and inactivated Salmonella typhimurium 395 MS and MR 10 with HeLa cells. Infect. Immun. 1976, 14:851-857.
38. Kim C.-H. A Salmonella typhimurium rfaE mutant recovers invasiveness for human epithelial cells when complemented by wild type rfaE (controlling biosynthesis of ADP-l-glycero-d-manno-Heptose-containing lipopolysaccharide). Mol. Cells 2003, 15:226-232.
39. Konkel M.E., Klena J.D., Rivera-Amill V., et al. Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J. Bacteriol. 2004, 176:3296-3303.
40. Kowarik M., Young N.M., Numao S., et al. Definition of the bacterial N-glycosylation site consensus sequence. EMBO J. 2006, 25:1957-1966.
41. Larsen J.C., Szymanski C., Guerry P. N-linked protein glycosylation is required for full competence in Campylobacter jejuni 81-176. J. Bacteriol. 2004, 186:6508-6514.
42. Lindenthal C., Elsinghorst E.A. Enterotoxigenic Escherichia coli TibA glycoprotein adheres to human intestine epithelial cells. Infect. Immun. 2001, 69:52-57.
43. 1-like lipo-oligosaccharide of Campylobacter jejuni. Mol. Microbiol. 2000, 37:501-514.
44. Locke J.B., Colvin K.M., Datta A.K., et al. Streptococcus iniae capsule impairs phagocytic clearance and contributes to virulence in fish. J. Bacteriol. 2007, 189:1279-1287.
45. Logan S.M., Kelly J.F., Thibault P., Ewing C.P., Guerry P. Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins. Mol. Microbiol. 2002, 46:587-597.
46. Magee A.D., Yother J. Requirement for capsule in colonization by Streptococcus pneumoniae. Infect. Immun. 2001, 69:3755-3761.
47. Mandrell R.E., Parker C.T., Bates A.H., et al. Campylobacter jejuni strain RM1221 lipooligosaccharide mimics globo- and lactoneo-series P blood group antigens. Abstracts of the 107th General Meeting of the American Society for Microbiology (ASM) 2008, 53. ASM Press, Washington, DC, Boston, Massachusetts.
48. Masoud H., Moxon E.R., Martin A., Krajcarski D., Richards J.C. Structure of the variable and conserved lipopolysaccharide oligosaccharide epitopes expressed by Haemophilus influenzae serotype b strain Eagan. Biochemistry 1997, 36:2091-2103.
49. McBride J.W., Yu X.-J., Walker D.H. Glycosylation of homologous immunodominant proteins of Ehrlichia chaffeensis and Ehrlichia canis. Infect. Immun. 2000, 68:13-18.
50. McBride J.W., Doyle C.K., Zhang X., et al. Identification of a glycosylated Ehrlichia canis 19-kilodalton major immunoreactive protein with a species-specific serine-rich glycopeptide epitope. Infect. Immun. 2007, 75:74-82.
51. McNally D.J., Hui J.P.M., Aubry A.J., et al. Functional characterization of the flagellar glycosylation locus in Campylobacter jejuni 81-176 using a focused metabolomics approach. J. Biol. Chem. 2006, 281:18489-18498.
52. McNally D.J., Lamoureux M.P., Karlyshev A.V., et al. Commonality and biosynthesis of the O-methyl phosphoramidate capsule modification in Campylobacter jejuni. J. Biol. Chem. 2007, 282:28566-28576.
53. Moran A., Penner J., Aspinall G. Campylobacter lipopolysaccharides. Campylobacter 2000, 241-257. ASM Press, Washington, DC. 2nd edn. I. Nachamkin, M. Blaser (Eds.).
54. Mroczenski-Wildey M.J., Di Fabio J.L., Cabello F.C. Invasion and lysis of HeLa cell monolayers by Salmonella typhi: the role of lipopolysaccharide. Microb. Path. 1989, 6:143-152.
55. Nelson A.L., Roche A.M., Gould J.M., Chim K., Ratner A.J., Weiser J.N. Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect. Immun. 2007, 75:83-90.
56. Nikaido H., et al. Outer membrane. Escherichia coli and Salmonella: Cellular and Molecular Biology 1996, 29-47. ASM Press, Washington, DC. R.C. Curtiss, J.L. Ingraham, E.C.C. Lin (Eds.).
57. O'Riordan K., Lee J.C. Staphylococcus aureus capsular polysaccharides. Clin. Microbiol. Rev. 2004, 17:218-234.
58. Oberhelman R., Taylor D. Campylobacter infections in developing countries. Campylobacter 2000, 139-153. ASM Press, Washington, DC. 2nd edn. I. Nachamkin, M. Blaser (Eds.).
59. Poly F., Ewing C., Goon S., et al. Heterogeneity of a Campylobacter jejuni protein that is secreted through the flagellar filament. Infect. Immun. 2007, 75:3859-3867.
60. Poly F., Read T.D., Chen Y.-H., et al. Characterization of two Campylobacter jejuni strains for use in experimental infection studies. Infect. Immun. 2008, 76:5655-5667.
61. Raetz C.R., Whitfield C. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 2002, 71:635-700.
62. Raetz C.R., Reynolds C.M., Trent M.S., Bishop R.E. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 2007, 76:295-329.
63. Raffatellu M., Chessa D., Wilson R.P., Dusold R., Rubino S., Baumler A.J. The Vi capsular antigen of Salmo-nella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect. Immun. 2005, 73:3367-3374.
64. Rao V.K., Krasan G.P., Hendrixson D.R., Dawid S., Geme J.W. Molecular determinants of the pathogenesis of disease due to non-typable Haemophilus influenzae. FEMS Microb. Rev. 1999, 23:99-129.
65. Sambri V., Stefanelli C., Cevenini R. Detection of glycoproteins in Borrelia burgdorferi. Arch. Microbiol. 1992, 157:205-208.
66. Sambri V., Massaria F., Ardizzoni M., Stefanelli C., Cevenini R. Glycoprotein patterns in Borrelia spp. Zentralbl. Bakteriol. 1993, 279:330-335.
67. Schrager H.M., Rheinwald J.G., Wessels M.R. Hyaluronic acid capsule and the role of streptococcal entry into keratinocytes in invasive skin infection. J. Clin. Invest. 1996, 98:1954-1958.
68. Sharma A., Qadri A. Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. Proc. Natl. Acad. Sci. USA 2004, 101:17492-17497.
69. Sisti F., Fernandez J., Rodriguez M.E., Lagares A., Guiso N., Hozbor D.F. In vitro and in vivo characterization of a Bordetella bronchiseptica mutant strain with a deep rough lipopolysaccharide structure. Infect. Immun. 2002, 70:1791-1798.
70. Song Y.C., Jin S., Louie H., et al. FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol. Microbiol. 2004, 53:541-553.
71. Spinosa M.R., Progida C., Tala A., Cogli L., Alifano P., Bucci C. The Neisseria meningitidis capsule is important for intracellular survival in human cells. Infect. Immun. 2007, 75:3594-3603.
72. Stevens M.K., Klesney-Tait J., Lumbley S., et al. Identification of tandem genes involved in lipooligosaccharide expression by Haemophilus ducreyi. Infect. Immun. 1997, 65:651-660.
73. Swanson A.F., Kuo C.C. Identification of lectin-binding proteins in Chlamydia species. Infect. Immun. 1990, 58:502-507.
74. Swanson A.F., Kuo C.C. Evidence that the outer membrane protein of Chlamydia trachomatis is glycosylated. Infect. Immun. 1991, 59:2120-2125.
75. Swanson A.F., Kuo C.C. Binding of the glycan of the major outer membrane protein of Chlamydia trachomatis to HeLa cells. Infect. Immun. 1994, 62:24-28.
76. Swords W.E., Buscher B.A., Ver Steeg Ii K., et al. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 2000, 37:13-27.
77. 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. 1999, 32:1022-1030.
78. Szymanski C.M., Burr D., Guerry P. Campylobacter protein glycosylation affects immunogenicity and host cell interactions. Infect. Immun. 2002, 70:2242-2244.
79. Szymanski C.M., Michael F.S., Jarrell H.C., 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. 2003, 278:24509-24520.
80. Thibault P., Logan S.M., Kelly J.F., et al. Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem. 2001, 276:34862-34870.
81. Wacker M., Linton D., Hitchen P.G., et al. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 2002, 298:1790-1793.
82. Wacker M., Feldman M.F., 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 2006, 103:7088-7093.
83. West N.P., Sansonetti P.J., Mounier R.M., et al. Optimization of virulence functions through glucosylation of Shigella LPS. Science 2005, 307:1313-1317.
84. Young N.M., Brisson J.-R., Kelly J., et al. Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J. Biol. Chem. 2002, 277:42530-42539.
85. Zaidi T.S., Fleiszig S.M., Preston M.J., Goldberg J.B., Pier G.B. Lipopolysaccharide outer core is a ligand for corneal cell binding and ingestion of Pseudomonas aeruginosa. Invest. Ophthalmol. Vis. Sci. 1996, 37:976-986.
86. Zilbauer M., Dorrell N., Boughan P.K., et al. Intestinal innate immunity to Campylobacter jejuni results in induction of bactericidal human beta-defensins 2 and 3. Infect. Immun. 2005, 73:7281-7289.