Glycoengineering of host mimicking type-2 LacNAc polymers and Lewis X antigens on bacterial cell surfaces

Molecular Microbiology

Volumn 87, Issue 1, 2013, Pages 112-131

  Mally, Manuela ^a,c   Fontana, Carolina ^b   Leibundgut Landmann, Salomé ^a   Laacisse, Lamia ^a   Fan, Yao Yun ^a   Widmalm, Göran ^b   Aebi, Markus ^a  

^a ETH ZURICH   (Switzerland)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c GlycoVaxyn AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; GLYCAN DERIVATIVE; GLYCOSYLTRANSFERASE; LEWIS X ANTIGEN; LIPID A; MOLECULAR SCAFFOLD; N LINKED PROTEIN GLYCAN DERIVATIVE; O ANTIGEN; POLYMER; TYPE 2 N ACETYLLACTOSAMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BIOENGINEERING; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CELL SURFACE; CONTROLLED STUDY; ESCHERICHIA COLI; FUCOSYLATION; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS;

ANIMALS; ANTIGENS, CD15; ANTIGENS, SURFACE; BACTERIAL OUTER MEMBRANE PROTEINS; DENDRITIC CELLS; DISACCHARIDES; ESCHERICHIA COLI; HELICOBACTER PYLORI; HOST-PATHOGEN INTERACTIONS; LIPOPOLYSACCHARIDES; MICE; SALMONELLA TYPHIMURIUM; SCHISTOSOMA MANSONI;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HELICOBACTER PYLORI; MAMMALIA; MURINAE; NEGIBACTERIA; NEISSERIA MENINGITIDIS; SALMONELLA ENTERICA; SCHISTOSOMA MANSONI; VERMES;

EID: 84871455762     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12086     Document Type: Article

References (84)

1. Alaimo, C., Catrein, I., Morf, L., Marolda, C.L., Callewaert, N., Valvano, M.A., etal. (2006) Two distinct but interchangeable mechanisms for flipping of lipid-linked oligosaccharides. EMBO J 25: 967-976.
2. Appelmelk, B.J., Shiberu, B., Trinks, C., Tapsi, N., Zheng, P.Y., Verboom, T., etal. (1998) Phase variation in Helicobacter pylori lipopolysaccharide. Infect Immun 66: 70-76.
3. Bax, A., and Davis, D.G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J Magn Reson 65: 355-360.
4. Bergman, M., Del Prete, G., van Kooyk, Y., and Appelmelk, B. (2006) Helicobacter pylori phase variation, immune modulation and gastric autoimmunity. Nat Rev Microbiol 4: 151-159.
5. Bergman, M.P., Engering, A., Smits, H.H., van Vliet, S.J., van Bodegraven, A.A., Wirth, H.P., etal. (2004) Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J Exp Med 200: 979-990.
6. Bos, M.P., Tefsen, B., Geurtsen, J., and Tommassen, J. (2004) Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci USA 101: 9417-9422.
7. Comstock, L.E., and Kasper, D.L. (2006) Bacterial glycans: key mediators of diverse host immune responses. Cell 126: 847-850.
8. Crocker, P.R., Paulson, J.C., and Varki, A. (2007) Siglecs and their roles in the immune system. Nat Rev Immunol 7: 255-266.
9. Damberg, P., Jarvet, J., and Gräslund, A. (2001) Accurate measurement of translational diffusion coefficients: a practical method to account for nonlinear gradients. J Magn Reson 148: 343-348.
10. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
11. Dumon, C., Priem, B., Martin, S.L., Heyraud, A., Bosso, C., and Samain, E. (2001) In vivo fucosylation of lacto-N-neotetraose and lacto-N-neohexaose by heterologous expression of Helicobacter pylori alpha-1, 3 fucosyltransferase in engineered Escherichia coli. Glycoconj J 18: 465-474.
12. Dumon, C., Samain, E., and Priem, B. (2004) Assessment of the two Helicobacter pylori alpha-1, 3-fucosyltransferase ortholog genes for the large-scale synthesis of LewisX human milk oligosaccharides by metabolically engineered Escherichia coli. Biotechnol Prog 20: 412-419.
13. Dumon, C., Bosso, C., Utille, J., Heyraud, A., and Samain, E. (2006) Production of Lewis x tetrasaccharides by metabolically engineered Escherichia coli. Chembiochem 7: 359-365.
14. Dykxhoorn, D.M., St Pierre, R., and Linn, T. (1996) A set of compatible tac promoter expression vectors. Gene 177: 133-136.
15. Edwards, N.J., Monteiro, M.A., Faller, G., Walsh, E.J., Moran, A.P., Roberts, I.S., and High, N.J. (2000) Lewis X structures in the O antigen side-chain promote adhesion of Helicobacter pylori to the gastric epithelium. Mol Microbiol 35: 1530-1539.
16. Galanos, C., Luderitz, O., and Westphal, O. (1969) A new method for the extraction of R lipopolysaccharides. Eur J Biochem 9: 245-249.
17. Garcia-Vallejo, J.J., and van Kooyk, Y. (2009) Endogenous ligands for C-type lectin receptors: the true regulators of immune homeostasis. Immunol Rev 230: 22-37.
18. Geijtenbeek, T.B., and Gringhuis, S.I. (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9: 465-479.
19. Gilbert, C.W., Zaroukian, M.H., and Esselman, W.J. (1988) Poly-N-acetyllactosamine structures on murine cell surface T200 glycoprotein participate in natural killer cell binding to YAC-1 targets. J Immunol 140: 2821-2828.
20. Gringhuis, S.I., den Dunnen, J., Litjens, M., van der Vlist, M., and Geijtenbeek, T.B. (2009) Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat Immunol 10: 1081-1088.
21. Heinrichs, D.E., Yethon, J.A., and Whitfield, C. (1998) Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol 30: 221-232.
22. Holst, O. (2000) Deacylation of lipopolysaccharides and isolation of oligosaccharide phosphates. Methods Mol Biol 145: 345-353.
23. Hug, I., Zheng, B., Reiz, B., Whittal, R.M., Fentabil, M.A., Klassen, J.S., and Feldman, M.F. (2011) Exploiting bacterial glycosylation machineries for the synthesis of a Lewis antigen-containing glycoprotein. J Biol Chem 286: 37887-37894.
24. Ilg, K., Endt, K., Misselwitz, B., Stecher, B., Aebi, M., and Hardt, W.D. (2009) O-antigen-negative Salmonella enterica serovar Typhimurium is attenuated in intestinal colonization but elicits colitis in streptomycin-treated mice. Infect Immun 77: 2568-2575.
25. Ilg, K., Yavuz, E., Maffioli, C., Priem, B., and Aebi, M. (2010) Glycomimicry: display of the GM3 sugar epitope on Escherichia coli and Salmonella enterica sv Typhimurium. Glycobiology 20: 1289-1297.
26. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., etal. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176: 1693-1702.
27. Ingram, B.O., Masoudi, A., and Raetz, C.R. (2010) Escherichia coli mutants that synthesize dephosphorylated lipid A molecules. Biochemistry 49: 8325-8337.
28. 13C-N.M.R. data. Carbohydr Res 188: 169-191.
29. Knirel, Y.A., Widmalm, G., Senchenkova, S.N., Jansson, P.E., and Weintraub, A. (1997) Structural studies on the short-chain lipopolysaccharide of Vibrio cholerae O139 Bengal. Eur J Biochem 247: 402-410.
30. Knirel, Y.A., Kocharova, N.A., Hynes, S.O., Widmalm, G., Andersen, L.P., Jansson, P.E., and Moran, A.P. (1999) Structural studies on lipopolysaccharides of serologically non-typable strains of Helicobacter pylori, AF1 and 007, expressing Lewis antigenic determinants. Eur J Biochem 266: 123-131.
31. van Kooyk, Y., and Rabinovich, G.A. (2008) Protein-glycan interactions in the control of innate and adaptive immune responses. Nat Immunol 9: 593-601.
32. Kostlanova, N., Mitchell, E.P., Lortat-Jacob, H., Oscarson, S., Lahmann, M., Gilboa-Garber, N., etal. (2005) The fucose-binding lectin from Ralstonia solanacearum. A new type of beta-propeller architecture formed by oligomerization and interacting with fucoside, fucosyllactose, and plant xyloglucan. J Biol Chem 280: 27839-27849.
33. Kumar, A., Ernst, R.R., and Wüthrich, K. (1980) A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem Biophys Res Commun 95: 1-6.
34. Kupče, Ē. (2002) Applications of adiabatic pulses in biomolecular nuclear magnetic resonance. In Nuclear Magnetic Resonance of Biological Macromolecules Part A. James, T.L., Dötsch, V., and Schmitz, U. (eds). San Diego: Academic Press, pp. 82-111.
35. Lefebre, M.D., and Valvano, M.A. (2002) Construction and evaluation of plasmid vectors optimized for constitutive and regulated gene expression in Burkholderia cepacia complex isolates. Appl Environ Microbiol 68: 5956-5964.
36. Lundborg, M., and Widmalm, G. (2011) Structural analysis of glycans by NMR chemical shift prediction. Anal Chem 83: 1514-1517.
37. Mandrell, R.E., and Apicella, M.A. (1993) Lipo-oligosaccharides (LOS) of mucosal pathogens: molecular mimicry and host-modification of LOS. Immunobiology 187: 382-402.
38. Marionneau, S., Cailleau-Thomas, A., Rocher, J., Le Moullac-Vaidye, B., Ruvoen, N., Clement, M., and Le Pendu, J. (2001) ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83: 565-573.
39. Masoud, H., Urbanik-Sypniewska, T., Lindner, B., Weckesser, J., and Mayer, H. (1991) The structure of the lipid A component of Sphaerotilus natans. Arch Microbiol 156: 167-175.
40. Masoud, H., Ferry, M.B., and Richards, J.C. (1994) Characterization of the lipopolysaccharide of Moraxella catarrhalis. Structural analysis of the lipid A from M. catarrhalis serotype-A lipopolysaccharide. Eur J Biochem 220: 209-216.
41. Mastroeni, P., Vazquez-Torres, A., Fang, F.C., Xu, Y., Khan, S., Hormaeche, C.E., and Dougan, G. (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J Exp Med 192: 237-248.
42. Mayer, H., Krauss, J.H., Yokota, A., and Weckesser, J. (1990) Natural variants of lipid A. Adv Exp Med Biol 256: 45-70.
43. Meredith, T.C., Mamat, U., Kaczynski, Z., Lindner, B., Holst, O., and Woodard, R.W. (2007) Modification of lipopolysaccharide with colanic acid (M-antigen) repeats in Escherichia coli. J Biol Chem 282: 7790-7798.
44. Miller, K.E., Mukhopadhyay, C., Cagas, P., and Bush, C.A. (1992) Solution structure of the Lewis X oligosaccharide determined by NMR spectroscopy and molecular dynamics simulations. Biochemistry 31: 6703-6709.
45. Miller, S.I., Ernst, R.K., and Bader, M.W. (2005) LPS, TLR4 and infectious disease diversity. Nat Rev Microbiol 3: 36-46.
46. Mills, R. (1973) Self-diffusion in normal and heavy water in the range 1-45° J Phys Chem 77: 685-688.
47. Moran, A.P. (2008) Relevance of fucosylation and Lewis antigen expression in the bacterial gastroduodenal pathogen Helicobacter pylori. Carbohydr Res 343: 1952-1965.
48. Moran, A.P., Knirel, Y.A., Senchenkova, S.N., Widmalm, G., Hynes, S.O., and Jansson, P.-E. (2002) Phenotypic variation in molecular mimicry between Helicobacter pylori lipopolysaccharides and human gastric epithelial cell surface glycoforms. J Biol Chem 277: 5785-5795.
49. Muramatsu, T. (1988) Alterations of cell-surface carbohydrates during differentiation and development. Biochimie 70: 1587-1596.
50. Nilsson, C., Skoglund, A., Moran, A., Annuk, H., Engstrand, L., and Normark, S. (2006) An enzymatic ruler modulates Lewis antigen glycosylation of Helicobacter pylori LPS during persistent infection. Proc Natl Acad Sci USA 103: 2863-2868.
51. Pang, P.C., Chiu, P.C., Lee, C.L., Chang, L.Y., Panico, M., Morris, H.R., etal. (2011) Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida. Science 333: 1761-1764.
52. Paton, A.W., Morona, R., and Paton, J.C. (2000) A new biological agent for treatment of Shiga toxigenic Escherichia coli infections and dysentery in humans. Nat Med 6: 265-270.
53. Paton, A.W., Jennings, M., Morona, R., Wang, H., Focareta, A., Roddam, L.F., and Paton, J.C. (2005) Recombinant probiotics for treatment and prevention of enterotoxigenic Escherichia coli diarrhea. Gastroenterology 128: 1219-1228.
54. Perez, J.M., McGarry, M.A., Marolda, C.L., and Valvano, M.A. (2008) Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase. Mol Microbiol 70: 1424-1440.
55. x. Science 250: 1130-1132.
56. Preston, A., Mandrell, R.E., Gibson, B.W., and Apicella, M.A. (1996) The lipooligosaccharides of pathogenic gram-negative bacteria. Crit Rev Microbiol 22: 139-180.
57. van Putten, J.P., and Robertson, B.D. (1995) Molecular mechanisms and implications for infection of lipopolysaccharide variation in Neisseria. Mol Microbiol 16: 847-853.
58. Rabinovich, G.A., and Toscano, M.A. (2009) Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol 9: 338-352.
59. Raetz, C.R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700.
60. Raetz, C.R., Reynolds, C.M., Trent, M.S., and Bishop, R.E. (2007) Lipid A modification systems in Gram-negative bacteria. Annu Rev Biochem 76: 295-329.
61. Ruiz, N., Kahne, D., and Silhavy, T.J. (2009) Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat Rev Microbiol 7: 677-683.
62. Sauerzapfe, B., Krenek, K., Schmiedel, J., Wakarchuk, W.W., Pelantova, H., Kren, V., and Elling, L. (2009) Chemo-enzymatic synthesis of poly-N-acetyllactosamine (poly-LacNAc) structures and their characterization for CGL2-galectin-mediated binding of ECM glycoproteins to biomaterial surfaces. Glycoconj J 26: 141-159.
63. Schagger, H. (2006) Tricine-SDS-PAGE. Nat Protoc 1: 16-22.
64. Schleucher, J., Schwendinger, M., Sattler, M., Schmidt, P., Schedletzky, O., Glaser, S.J., etal. (1994) A general enhancement scheme in heteronuclear multidimensional NMR employing pulsed-field gradients. J Biomol NMR 4: 301-306.
65. Schneider, M.C., Exley, R.M., Ram, S., Sim, R.B., and Tang, C.M. (2007) Interactions between Neisseria meningitidis and the complement system. Trends Microbiol 15: 233-240.
66. Schwarz, F., Huang, W., Li, C., Schulz, B.L., Lizak, C., Palumbo, A., etal. (2010) A combined method for producing homogeneous glycoproteins with eukaryotic N-glycosylation. Nat Chem Biol 6: 264-266.
67. Stead, C.M., Zhao, J., Raetz, C.R., and Trent, M.S. (2010) Removal of the outer Kdo from Helicobacter pylori lipopolysaccharide and its impact on the bacterial surface. Mol Microbiol 78: 837-852.
68. Stewart, A., Bernlind, C., Martin, A., Oscarson, S., Richards, J.C., and Schweda, E.K.H. (1998) Studies of alkaline mediated phosphate migration in synthetic phosphoethanolamine L-glycero-D-manno-heptoside derivatives. Carbohydr Res 313: 193-202.
69. van Stijn, C.M., Meyer, S., van den Broek, M., Bruijns, S.C., van Kooyk, Y., Geyer, R., and van Die, I. (2010) Schistosoma mansoni worm glycolipids induce an inflammatory phenotype in human dendritic cells by cooperation of TLR4 and DC-SIGN. Mol Immunol 47: 1544-1552.
70. Szymanski, C.M., and Wren, B.W. (2005) Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3: 225-237.
71. Tannús, A., and Garwood, M. (1997) Adiabatic pulses. NMR Biomed 10: 423-434.
72. Togayachi, A., Kozono, Y., Ishida, H., Abe, S., Suzuki, N., Tsunoda, Y., etal. (2007) Polylactosamine on glycoproteins influences basal levels of lymphocyte and macrophage activation. Proc Natl Acad Sci USA 104: 15829-15834.
73. Tsai, C.M., and Frasch, C.E. (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119: 115-119.
74. Valderrama-Rincon, J.D., Fisher, A.C., Merritt, J.H., Fan, Y.Y., Reading, C.A., Chhiba, K., etal. (2012) An engineered eukaryotic protein glycosylation pathway in Escherichia coli. Nat Chem Biol 8: 434-436.
75. Varki, A. (1994) Selectin ligands. Proc Natl Acad Sci USA 91: 7390-7397.
76. Viel, S., Capitani, D., Mannina, L., and Segre, A. (2003) Diffusion-ordered NMR spectroscopy: a versatile tool for the molecular weight determination of uncharged polysaccharides. Biomacromolecules 4: 1843-1847.
77. van Vliet, S.J., Steeghs, L., Bruijns, S.C., Vaezirad, M.M., Snijders Blok, C., Arenas Busto, J.A., etal. (2009) Variation of Neisseria gonorrhoeae lipooligosaccharide directs dendritic cell-induced T helper responses. PLoS Pathog 5: e1000625.
78. Wacker, M., Linton, D., Hitchen, P.G., Nita-Lazar, M., Haslam, S.M., North, S.J., etal. (2002) N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298: 1790-1793.
79. Walser, P.J., Haebel, P.W., Kunzler, M., Sargent, D., Kues, U., Aebi, M., and Ban, N. (2004) Structure and functional analysis of the fungal galectin CGL2. Structure 12: 689-702.
80. Wang, G., Ge, Z., Rasko, D.A., and Taylor, D.E. (2000) Lewis antigens in Helicobacter pylori: biosynthesis and phase variation. Mol Microbiol 36: 1187-1196.
81. van der Woude, M.W., and Baumler, A.J. (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17: 581-611, table of contents.
82. Yavuz, E., Maffioli, C., Ilg, K., Aebi, M., and Priem, B. (2011) Glycomimicry: display of fucosylation on the lipo-oligosaccharide of recombinant Escherichia coli K12. Glycoconj J 28: 39-47.
83. Yethon, J.A., Heinrichs, D.E., Monteiro, M.A., Perry, M.B., and Whitfield, C. (1998) Involvement of waaY, waaQ, and waaP in the modification of Escherichia coli lipopolysaccharide and their role in the formation of a stable outer membrane. J Biol Chem 273: 26310-26316.
84. Yethon, J.A., Vinogradov, E., Perry, M.B., and Whitfield, C. (2000) Mutation of the lipopolysaccharide core glycosyltransferase encoded by waaG destabilizes the outer membrane of Escherichia coli by interfering with core phosphorylation. J Bacteriol 182: 5620-5623.