Chapter 12 : Periplasmic Events in the Assembly of Bacterial Lipopolysaccharides

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Periplasmic Events in the Assembly of Bacterial Lipopolysaccharides, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815806/9781555813987_Chap12-1.gif /docserver/preview/fulltext/10.1128/9781555815806/9781555813987_Chap12-2.gif


This chapter provides an overview of the assembly pathways for lipopolysaccharide (LPS) molecules, with particular emphasis on reactions and components occurring in the periplasm. Species-specific variations on the generally conserved theme are now being identified. In the current working model, it is proposed that lipid A core binds to MsbA and the polar parts of the exported molecule enter the lumen of the transporter. WecA is an integral membrane protein that forms the undecaprenyl pyrophosphoryl-GlcNAc. The premise for the periplasmic location of the glucosylation reaction is based on studies with that first showed undecaprenyl pyrophosphate-linked intermediates provide the acceptor for glucosylation. O-Acetyltransferases also modify O-polysaccharides. Well-documented examples include OafA, which confers O:5 specificity in Oac encoded by the seroconverting bacteriophage SF6 and the O-acetyltransferase carried by bacteriophage D3. The WbdD-mediated chain termination reactions establish modal regulation in participation with the ABC transporter because the export process is coupled to chain termination. Synthases are processive glycosyltransferases that have the capacity to synthesize polymers within one or more linkages. It has been shown that peptidoglycan is also distributed in a helical arrangement along the side walls of and it will be interesting to see whether the events are coupled and whether the emerging bacterial cytoskeletal components play any role in dictating the sites of LPS insertion.

Citation: Whitfield C, Frirdich E, Reid A. 2007. Periplasmic Events in the Assembly of Bacterial Lipopolysaccharides, p 214-234. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch12
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Structure of the core oligosaccharide in and . The inner core is shown in A and the various nonstoichiometric glycose and phosphoethanolamine modifications of the base structure are represented by the dashed lines. Two representative outer core structures are shown in B.

Citation: Whitfield C, Frirdich E, Reid A. 2007. Periplasmic Events in the Assembly of Bacterial Lipopolysaccharides, p 214-234. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch12
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Allison, G. E., and, N. K.Verma. 2000. Serotypeconverting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol. 8: 1723.
2. Amer, A. O., and, M. A. Valvano. 2002. Conserved aspartic acids are essential for the enzymic activity of the WecA protein initiating the biosynthesis of O-specific lipopolysaccharide and enterobacterial common antigen in Escherichia coli. Microbiology 148: 571582.
3. Bader, M. W.,, S. Sanowar,, M. E. Daley,, A. R. Schneider,, U. Cho,, W. Xu,, R. E. Klevit,, H. Le Moual, and, S. I. Miller. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122: 461472.
4. Bastin, D. A.,, G. Stevenson,, P. K. Brown,, A. Haase, and, P. R. Reeves. 1993. Repeat unit polysaccharides of bacteria:a model for polymerization resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Mol. Microbiol. 7: 725734.
5. Bayer, M. E., 1991. Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. J. Struct. Biol. 107:268–280.
6. Bayer, M. H.,, G. P. Costello, and, M. E. Bayer. 1982. Isolation and partial characterization of membrane vesicles carrying markers of the membrane adhesion sites. J. Bacteriol. 149: 758767.
7. Bishop, R. E., 2005. The lipid A palmitoyltransferase PagP: molecular mechanisms and role in bacterial pathogenesis. Mol. Microbiol. 57: 900912.
8. Bodevin-Authelet, S.,, M. Kusche-Gullberg,, P. E. Pummill,, P. L. DeAngelis, and, U. Lindahl. 2005. Biosynthesis of hyaluronan:direction of chain elongation. J. Biol. Chem. 280: 88138818.
9. Bos, M. P.,, B. Tefsen,, J. Geurtsen, and, J. Tommassen. 2004. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc. Natl. Acad. Sci. USA 101: 94179422.
10. Bos, M. P., and, J. Tommassen. 2005. Viability of a capsule- and lipopolysaccharide-deficient mutant of Neisseria meningitidis. Infect. Immun. 73: 61946197.
11. Braun, M., and, T. J. Silhavy. 2002. Imp/OstA is required for cell envelope biogenesis in Escherichia coli. Mol. Microbiol. 45: 12891302.
12. Bray, D., and, P. W. Robbins. 1967. The direction of chain growth in Salmonella anatum O-antigen biosynthesis. Biochem. Biophys. Res. Commun. 28: 334339.
13. Breazeale, S. D.,, A. A. Ribeiro,, A. L. McClerren, and, C. R. Raetz. 2005. A formyltransferase required for polymyxin resistance in Escherichia coli and the modification of lipid A with 4-amino-4-deoxy-l-arabinose. Identification and function of UDP-4-deoxy-4-formamido-l-arabinose. J. Biol. Chem. 280: 1415414167.
14. Buchaklian, A. H.,, A. L. Funk, and, C. S. Klug. 2004. Resting state conformation of the MsbA homodimer as studied by site-directed spin labeling. Biochemistry 43: 86008606.
15. Buchaklian, A. H., and, C. S. Klug. 2005. Characterization of the Walker A motif of MsbA using site-directed spin labeling electron paramagnetic resonance spectroscopy. Biochemistry 44: 55035509.
16. Bulieris, P. V.,, S. Behrens,, O. Holst, and, J. H. Kleinschmidt. 2003. Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide. J. Biol. Chem. 278: 90929099.
17. Burns, S. M., and, S. I. Hull. 1998. Comparison of loss of serum resistance by defined lipopolysaccharide mutants and an acapsular mutant of uropathogenic Escherichia coli O75:K5. Infect. Immun. 66: 42444253.
18. Cabeen, M.T., and, C. Jacobs-Wagner. 2005. Bacterial cell shape. Nat. Rev. Microbiol. 3: 601610.
19. Cartee, R. T.,, W. T. Forsee,, J. W. Jensen, and, J. Yother. 2001. Expression of the Streptococcus pneumoniae type 3 synthase in Escherichia coli. Assembly of type 3 polysaccharide on a lipid primer. J. Biol. Chem. 276: 4883148839.
20. Cartee, R. T.,, W. T. Forsee,, J. S. Schutzbach, and, J. Yother. 2000. Mechanism of type 3 capsular polysaccharide synthesis in Streptococcus pneumoniae. J. Biol. Chem. 275: 39073914.
21. Carty, S. M.,, K. R. Sreekumar, and, C. R. Raetz. 1999. Effect of cold shock on lipid A biosynthesis in Escherichia coli. Induction at 12°C of an acyltransferase specific for palmitoleoyl-acyl carrier protein. J. Biol. Chem. 274: 96779685.
22. Chang, G., 2003. Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J. Mol. Biol. 330: 419430.
23. Chang, G., and, C. B. Roth. 2001. Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science 293: 17931800.
24. Charnock, S. J.,, B. Henrissat, and, G. J. Davies. 2001. Three-dimensional structures of UDP-sugar glycosyltransferases illuminate the biosynthesis of plant polysaccharides. Plant Physiol. 125: 527531.
25. Clarke, A. J.,, H. Strating, and, N. T. Blackburn. 2000. Pathways for the O-acetylation of bacterial cell wall polysaccharides, p. 187224. In R. J. Doyle, (ed)., Glycomicrobiology. Kluwer Academic/Plenum Publishers, New York, N.Y.
26. Clarke, B. R.,, L. Cuthbertson, and, C. Whitfield. 2004. Nonreducing terminal modifications determine the chain length of polymannose O antigens of Escherichia coli and couple chain termination to polymer export via an ATP-binding cassette transporter. J. Biol. Chem. 279: 3570935718.
27. Collins, L. V., and, J. Hackett. 1991. Molecular cloning, characterization, and nucleotide sequence of the rfc gene, which encodes an O-antigen polymerase of Salmonella typhimurium. J. Bacteriol. 173: 25212529.
28. Collins, R. F.,, K. Beis,, B. R. Clarke,, R. C. Ford,, M. Hulley,, J. H. Naismith, and, C. Whitfield. 2006. Periplasmic protein-protein contacts in the inner membrane protein, Wzc, form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules. J. Biol. Chem. 281: 21442150.
29. Cuthbertson, L.,, J. Powers, and, C. Whitfield. 2005. The C-terminal domain of the nucleotidebinding domain protein Wzt determines substrate specificity in the ATP-binding cassette transporter for the lipopolysaccharide O antigens in Escherichia coli serotypes 08 and 09a. J. Biol. Chem. 280: 3031030319.
30. Daniels, C.,, C. Griffiths,, B. Cowles, and, J. S. Lam. 2002. Pseudomonas aeruginosa O-antigen chain length is determined before ligation to lipid A core. Environ. Microbiol. 4: 883897.
31. Daniels, C., and, R. Morona. 1999. Analysis of Shigella flexneri Wzz (Rol) function by mutagenesis and cross-linking:Wzz is able to oligomerize. Mol. Microbiol. 34: 181194.
32. Daniels, C.,, C. Vindurampulle, and, R. Morona. 1998. Overexpression and topology of the Shigella flexneri O-antigen polymerase (Rfc/Wzy). Mol. Microbiol. 28: 12111222.
33. DeAngelis, P. L., 2002. Microbial glycosaminoglycan glycosyltransferases. Glycobiology 12: 9R16R.
34. Doerrler, W. T.,, H. S. Gibbons, and, C. R. Raetz. 2004. MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J. Biol. Chem. 279: 4510245109.
35. Doerrler, W. T.,, M. C. Reedy, and, C. R. Raetz. 2001. An Escherichia coli mutant defective in lipid export. J. Biol. Chem. 276: 1146111464.
36. Dong, J.,, G. Yang, and, H. S. McHaourab. 2005. Structural basis of energy transduction in the transport cycle of MsbA. Science 308: 10231028.
37. Doublet, P.,, C. Grangeasse,, B. Obadia,, E. Vaganay, and, A. J. Cozzone. 2002. Structural organization of the protein-tyrosine autokinase Wzc within Escherichia coli cells. J. Biol. Chem. 277: 3733937348.
38. Feldman, M. F.,, C. L. Marolda,, M. A. Monteiro,, M. B. Perry,, A. J. Parodi, and, M. A. Valvano. 1999. The activity of a putative polyisoprenol-linked sugar translocase (Wzx) involved in Escherichia coli O antigen assembly is independent of the chemical structure of the O repeat. J. Biol. Chem. 274: 3512935138.
39. Forsee, W. T.,, R. T. Cartee, and, J. Yother. 2000. Biosynthesis of type 3 capsular polysaccharide in Streptococcus pneumoniae. Enzymatic chain release by an abortive translocation process. J. Biol. Chem. 275: 2597225978.
40. Franco, A. V.,, D. Liu, and, P. R. Reeves. 1998. The Wzz (Cld) protein in Escherichia coli: amino acid sequence variation determines O-antigen chain length specificity. J. Bacteriol. 180: 26702675.
41. Frirdich, E., and, C. Whitfield. 2005. Lipopolysaccharide inner core oligosaccharide structure and outer membrane stability in human pathogens belonging to the Enterobacteriaceae. J. Endotox. Res. 11: 133144.
42. Ganz, T., 2003. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3: 710720.
43. Gaspar, J. A.,, J. A. Thomas,, C. L. Marolda, and, M. A.V alvano. 2000. Surface expression of O-specific lipopolysaccharide in Escherichia coli requires the function of the TolA protein. Mol. Microbiol. 38: 262275.
44. Gatzeva-Topalova, P. Z.,, A. P. May, and, M. C. Sousa. 2004. Crystal structure of Escherichia coli ArnA (PmrI) decarboxylase domain.A key enzyme for lipid A modification with 4-amino-4-deoxy-l-arabinose and polymyxin resistance. Biochemistry 43: 1337013379.
45. Gatzeva-Topalova, P. Z.,, A. P. May, and, M. C. Sousa. 2005a. Structure and mechanism of ArnA: conformational change implies ordered dehydrogenase mechanism in key enzyme for polymyxin resistance. Structure 13: 929942.
46. Gatzeva-Topalova, P. Z.,, A. P. May, and, M. C. Sousa. 2005b. Crystal structure and mechanism of the Escherichia coli ArnA (PmrI) transformylase domain. An enzyme for lipid A modification with 4-amino-4-deoxy-l-arabinose and polymyxin resistance. Biochemistry 44: 53285338.
47. Genevrois, S.,, L. Steeghs,, P. Roholl,, J. J. Letesson, and, P. van der Ley. 2003. The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J. 22: 17801789.
48. Geurtsen, J.,, L. Steeghs,, J. T. Hove,, P. van der Ley, and, J. Tommassen. 2005. Dissemination of lipid A deacylases (pagL) among gram-negative bacteria: identification of active-site histidine and serine residues. J. Biol. Chem. 280: 82488259.
49. Ghosh, A. S., and, K. D.Y oung. 2005. Helical disposition of proteins and lipopolysaccharide in the outer membrane of Escherichia coli. J. Bacteriol. 187: 19131922.
50. Gibbons, H. S.,, S. R. Kalb,, R. J. Cotter, and, C. R. Raetz. 2005. Role of Mg 2+ and pH in the modification of Salmonella lipid A after endocytosis by macrophage tumour cells. Mol. Microbiol. 55: 425440.
51. Gibbons, H. S.,, S. Lin,, R. J. Cotter, and, C. R. Raetz. 2000. Oxygen requirement for the biosynthesis of the S-2-hydroxymyristate moiety in Salmonella typhimurium lipid A. Function of LpxO, a new Fe 2+/a-ketoglutarate-dependent dioxygenase homologue. J. Biol. Chem. 275: 3294032949.
52. Groisman, E. A., 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183: 18351842.
53. Groisman, E. A.,, J. Kayser, and, F. C. Soncini. 1997. Regulation of polymyxin resistance and adaptation to low-Mg 2+ environments. J. Bacteriol. 179: 70407045.
54. Guan, S.,, D. A. Bastin, and, N. K. Verma. 1999. Functional analysis of the O antigen glucosylation gene cluster of Shigella flexneri bacteriophage SfX. Microbiology 145: 12631273.
55. Gunn, J. S.,, K. B. Lim,, J. Krueger,, K. Kim,, L. Guo,, M. Hackett, and, S. I. Miller. 1998. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27: 11711182.
56. Gunn, J. S.,, S. S. Ryan,, J. C. Van Velkinburgh,, R. K. Ernst, and, S. I. Miller. 2000. Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 68: 61396146.
57. Guo, L.,, K. B. Lim,, J. S. Gunn,, B. Bainbridge,, R. P. Darveau,, M. Hackett, and, S. I. Miller. 1997. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276: 250253.
58. Guo, L.,, K. B. Lim,, C. M. Poduje,, M. Daniel,, J. S. Gunn,, M. Hackett, and, S. I. Miller. 1998. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95: 189198.
59. Heinrichs, D. E.,, M. A. Monteiro,, M. B. Perry, and, C. Whitfield. 1998a. The assembly system for the lipopolysaccharide R2 core-type of Escherichia coli is a hybrid of those found in Escherichia coli K-12 and Salmonella enterica.Structure and function of the R2 WaaK and WaaL homologs. J. Biol. Chem. 273: 88498859.
60. Heinrichs, D. E.,, J. A. Yethon, and, C. Whitfield. 1998b. Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol. Microbiol. 30: 221232.
61. Heldermon, C.,, P. L. DeAngelis, and, P. H. Weigel. 2001. Topological organization of the hyaluronan synthase from Streptococcus pyogenes. J. Biol. Chem. 276: 20372046.
62. Higgins, C. F., 2001. ABC transporters: physiology, structure and mechanism–an overview. Res. Microbiol. 152: 205210.
63. Kanipes, M. I.,, S. Lin,, R. J. Cotter, and, C. R. Raetz. 2001. Ca 2+-induced phosphoethanolamine transfer to the outer 3-deoxy-D-manno-octu-losonic acid moiety of Escherichia coli lipopolysaccharide. A novel membrane enzyme dependent upon phosphatidylethanolamine. J. Biol. Chem. 276: 11561163.
64. Kaniuk, N.A.,, E. Vinogradov, and, C. Whitfield. 2004. Investigation of the structural requirements in the lipopolysaccharide core acceptor for ligation of O antigens in the genus Salmonella: WaaL “ligase” is not the sole determinant of acceptor specificity. J. Biol. Chem. 279: 3647036480.
65. Karbarz, M. J.,, S. R. Kalb,, R. J. Cotter, and, C. R. Raetz. 2003. Expression cloning and biochemical characterization of a Rhizobium leguminosarum lipid A 1-phosphatase. J. Biol. Chem. 278: 3926939279.
66. Kato, A., and, E. A. Groisman. 2004. Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev 18: 23022313.
67. Kato, A.,, T. Latifi, and, E. A. Groisman. 2003. Closing the loop:the PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD. Proc. Natl. Acad. Sci. USA 100: 47064711.
68. Kawasaki, K.,, R. K. Ernst, and, S. I. Miller. 2004a. Deacylation and palmitoylation of lipid A by Salmonellae outer membrane enzymes modulate host signaling through Toll-like receptor 4. J. Endotox. Res. 10: 439444.
69. Kawasaki, K.,, R. K. Ernst, and, S. I. Miller. 2004b. 3 -O-deacylation of lipid A by PagL, a PhoP/ PhoQ-regulated deacylase of Salmonella typhimurium, modulates signaling through Toll-like receptor 4. J. Biol. Chem. 279: 2004420048.
70. Kawasaki, K.,, R. K. Ernst, and, S. I. Miller. 2005. Inhibition of Salmonella enterica serovar Typhimurium lipopolysaccharide deacylation by aminoarabinose membrane modification. J. Bacteriol. 187: 24482457.
71. Keenleyside, W. J.,, M. B. Perry,, L. L. MacLean,, C. Poppe, and, C. Whitfield. 1994. A plasmid-encoded rfb O:54 gene cluster is required for biosynthesis of the O:54 antigen in Salmonella enterica serovar Borreze. Mol. Microbiol. 11: 437448.
72. Keenleyside, W. J., and, C. Whitfield. 1995. Lateral transfer of rfb genes: a mobilizable ColE1-type plasmid carries the rfb O:54 (O:54 antigen biosynthesis) gene cluster from Salmonella enterica serovar Borreze. J. Bacteriol. 177: 52475253.
73. Keenleyside, W. J., and, C. Whitfield. 1996. A novel pathway for O-polysaccharide biosynthesis in Salmonella enterica serovar Borreze. J. Biol. Chem. 271: 2858128592.
74. Kellenberger, E., 1990. The ‘Bayer bridges’ confronted with results from improved electron microscopy methods. Mol. Microbiol. 4: 697705.
75. Kido, N.,, V. I. Torgov,, T. Sugiyama,, K. Uchiya,, H. Sugihara,, T. Komatsu,, N. Kato, and, K. Jann. 1995. Expression of the O9 polysaccharide of Escherichia coli: sequencing of the E. coli O9 rfb gene cluster, characterization of mannosyl transferases, and evidence for an ATP-binding cassette transport system. J. Bacteriol. 177: 21782187.
76. Klee, S. R.,, B. D. Tzschaschel,, K. N. Timmis, and, C. A. Guzman. 1997. Influence of different rol gene products on the chain length of Shigella dysenteriae type 1 lipopolysaccharide O antigen expressed by Shigella flexneri carrier strains. J. Bacteriol. 179: 24212425.
77. Korres, H.,, M. Mavris,, R. Morona,, P. A. Manning, and, N. K.V erma. 2005. Topological analysis of GtrA and GtrB proteins encoded by the serotype-converting cassette of Shigella flexneri. Biochem. Biophys. Res. Commun. 328: 12521260.
78. Korres, H., and, N. K. Verma. 2004. Topological analysis of glucosyltransferase GtrV of Shigella flexneri by a dual reporter system and identification of a unique reentrant loop. J. Biol. Chem. 279: 2246922476.
79. Kox, L. F.,, M. M. Wosten, and, E. A. Groisman. 2000. A small protein that mediates the activation of a two-component system by another two-component system. EMBO J. 19: 18611872.
80. Lee, H.,, F. F. Hsu,, J. Turk, and, E. A. Groisman. 2004. The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J. Bacteriol. 186: 41244133.
81. Lehane, A. M.,, H. Korres, and, N. K.V erma. 2005. Bacteriophage-encoded glucosyltransferase GtrII of Shigella flexneri: membrane topology and identification of critical residues. Biochem. J. 389: 137143.
82. Liu, D.,, R. Cole, and, P. R. Reeves. 1996. An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J. Bacteriol. 178: 21022107.
83. Losick, R., and, P. W. Robbins. 1967. Mechanism of epsilon-15 conversion studies with a bacterial mutant. J. Mol. Biol. 30: 445455.
84. Mackinnon, F. G.,, A. D. Cox,, J. S. Plested,, C. M. Tang,, K. Makepeace,, P. A. Coull,, J. C. Wright,, R. Chalmers,, D. W. Hood,, J. C. Richards, and, E. R. Moxon. 2002. Identification of a gene (lpt-3) required for the addition of phosphoethanolamine to the lipopolysaccharide inner core of Neisseria meningitidis and its role in mediating susceptibility to bactericidal killing and opsonophagocytosis. Mol. Microbiol. 43: 931943.
85. Mäkelä, P. H., and, B. A. D. Stocker. 1984. Genetics of lipopolysaccharide, p. 59137. In E. T. Rietschel, (ed.), Handbook of Endotoxin, vol. I. Elsevier Science Publishers, B.V., Amsterdam, The Netherlands.
86. Marolda, C. L.,, L. D. Tatar,, C. Alaimo,, M. Aebi, and, M. A. Valvano. 2006. Interplay of the Wzx translocase and the corresponding polymerase and chain length regulator proteins in the translocation and periplasmic assembly of lipopolysaccharide O antigen. J. Bacteriol. 188: 51245135.
87. Marolda, C. L.,, J. Vicarioli, and, M. A. Valvano. 2004. Wzx proteins involved in biosynthesis of O antigen function in association with the first sugar of the O-specific lipopolysaccharide subunit. Microbiology 150: 40954105.
88. Mavris, M.,, P. A. Manning, and, R. Morona. 1997. Mechanism of bacteriophage SfII-mediated serotype conversion in Shigella flexneri. Mol. Microbiol. 26: 939950.
89. Morona, R.,, C. Daniels, and, L. Van Den Bosch. 2003. Genetic modulation of Shigella flexneri 2a lipopolysaccharide O antigen modal chain length reveals that it has been optimized for virulence. Microbiology 149: 925939.
90. Morona, R.,, M. Mavris,, A. Fallarino, and, P. A. Manning. 1994. Characterization of the rfc region of Shigella flexneri. J. Bacteriol. 176: 733747.
91. Morona, R., and, L. Van Den Bosch. 2003. Multicopy icsA is able to suppress the virulence defect caused by the wzz(SF) mutation in Shigella flexneri. FEMS Microbiol. Lett. 221: 213219.
92. Morona, R.,, L. Van Den Bosch, and, C. Daniels. 2000. Evaluation of Wzz/MPA1/MPA2 proteins based on the presence of coiled-coil regions. Microbiology 146: 14.
93. Morona, R.,, L. Van Den Bosch, and, P. A. Manning. 1995. Molecular, genetic, and topological characterization of O-antigen chain length regulation in Shigella flexneri. J. Bacteriol. 177: 10591068.
94. Mouslim, C.,, T. Latifi, and, E. A. Groisman. 2003. Signal-dependent requirement for the co-activator protein RcsA in transcription of the RcsB-regulated ugd gene. J. Biol. Chem. 278: 5058850595.
95. Mühlradt, P. F.,, J. Menzel,, J. R. Golecki, and, V. Speth. 1973. Outer membrane of Salmonella. Sites of export of newly synthesized lipopolysaccharide on the bacterial surface. Eur. J. Biochem. 35: 471481.
96. Murray, G. L.,, S. R. Attridge, and, R. Morona. 2003. Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. Mol. Microbiol. 47: 13951406.
97. Murray, G. L.,, S. R. Attridge, and, R. Morona. 2005. Inducible serum resistance in Salmonella typhimurium is dependent on wzz(fepE)-regulated very long O antigen chains. Microb. Infect. 7: 12961304.
98. Najdenski, H.,, E. Golkocheva,, A. Vesselinova,, J. A. Bengoechea, and, M. Skurnik. 2003. Proper expression of the O-antigen of lipopolysaccharide is essential for the virulence of Yersinia enterocolitica O:8 in experimental oral infection of rabbits. FEMS Immunol. Med. Microbiol. 38: 97106.
99. Navarre, W. W.,, T. A. Halsey,, D. Walthers,, J. Frye,, M. McClelland,, J. L. Potter,, L. J. Kenney,, J. S. Gunn,, F. C. Fang, and, S. J. Libby. 2005. Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol. Microbiol. 56: 492508.
100. Newton, G. J.,, C. Daniels,, L. L. Burrows,, A. M. Kropinski,, A. J. Clarke, and, J. S. Lam. 2001. Three-component-mediated serotype conversion in Pseudomonas aeruginosa by bacteriophage D3. Mol. Microbiol. 39: 12371247.
101. Nikaido, H., 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67: 593656.
102. Nikaido, H.,, K. Nikaido,, T. Nakae, and, P. H. Makela. 1971. Glucosylation of lipopolysaccharide in Salmonella: biosynthesis of O antigen factor 12 2. I. Over-all reaction. J. Biol. Chem. 246: 39023911.
103. Nikaido, K., and, H. Nikaido. 1971. Glucosylation of lipopolysaccharide in Salmonella: biosynthesis of O antigen factor 12 2. II. Structure of the lipid intermediate. J. Biol. Chem. 246: 39123919.
104. Ørskov, I.,, F. Ørskov,, B. Jann, and, K. Jann. 1977. Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Bacteriol. Rev. 41: 667710.
105. Osborn, M. J.,, M. A. Cynkin,, J. M. Gilbert,, L. Müller, and, M. Singh. 1972. Synthesis of bacterial O-antigens. Methods Enzymol. 28: 583601.
106. Pelosi, L.,, M. Boumedienne,, N. Saksouk,, J. Geiselmann, and, R. A. Geremia. 2005. The glucosyl-1-phosphate transferase WchA (Cap8E) primes the capsular polysaccharide repeat unit biosynthesis of Streptococcus pneumoniae serotype 8. Biochem. Biophys. Res. Commun. 327: 857865.
107. Peng, D.,, W. Hong,, B. P. Choudhury,, R. W. Carlson, and, X. X. Gu. 2005. Moraxella catarrhalis bacterium without endotoxin, a potential vaccine candidate. Infect. Immun. 73: 75697577.
108. Price, N. P., and, F. A. Momany. 2005. Modeling bacterial UDP-HexNAc:polyprenol-P HexNAc1-P transferases. Glycobiology 15: 29R42R.
109. Raetz, C. R., and, C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71: 635700.
110. Reyes, C. L., and, G. Chang. 2005. Structure of the ABC transporter MsbA in complex with ADP vanadate and lipopolysaccharide. Science 308: 10281031.
111. Reynolds, C. M.,, S. R. Kalb,, R. J. Cotter, and, C. R. Raetz. 2005. A phosphoethanolamine transferase specific for the outer 3-deoxy-D-mannooctulosonic acid residue of Escherichia coli lipopolysaccharide. Identification of the eptB gene and Ca 2+ hypersensitivity of an eptB deletion mutant. J. Biol. Chem. 280: 2120221211.
112. Rick, P. D.,, K. Barr,, K. Sankaran,, J. Kajimura,, J. S. Rush, and, C. J. Waechter. 2003. Evidence that the wzxE gene of Escherichia coli K-12 encodes a protein involved in the transbilayer movement of a trisaccharide-lipid intermediate in the assembly of enterobacterial common antigen. J. Biol. Chem. 278: 1653416542.
113. Rick, P. D.,, G. L. Hubbard, and, K. Barr. 1994. Role of the rfe gene in the synthesis of the O8 antigen in Escherichia coli K-12. J. Bacteriol. 176: 28772884.
114. Robbins, P. W.,, D. Bray,, M. Dankert, and, A. Wright. 1967. Direction of chain growth in polysaccharide synthesis. Science 158: 15361542.
115. Schild, S.,, A. K. Lamprecht, and, J. Reidl. 2005. Molecular and functional characterization of O antigen transfer in Vibrio cholerae. J. Biol. Chem. 280: 2593625947.
116. Schnaitman, C. A., and, J. D. Klena. 1993. Genet-ics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol. Rev. 57: 655682.
117. Shi, Y.,, M. J. Cromie,, F. F. Hsu,, J. Turk, and, E. A. Groisman. 2004. PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B. Mol. Microbiol. 53: 229241.
118. Slauch, J. M.,, A. A. Lee,, M. J. Mahan, and, J. J. Mekalanos. 1996. Molecular characterization of the oafA locus responsible for acetylation of Salmonella typhimurium O-antigen: oafA is a member of a family of integral membrane trans-acylases. J. Bacteriol. 178: 59045909.
119. Sperandeo, P.,, C. Pozzi,, G. Dehó, and, A. Polissi. 2006. Non-essential KDO biosynthesis and new essential cell envelope biogenesis genes in the Escherichia coli yrbG-yhbG locus. Res. Microbiol. 157: 547558.
120. Stead, C.,, A. Tran,, D. Ferguson, Jr.,, S. McGrath,, R. Cotter, and, S. Trent. 2005. A novel 3-de-oxy-D-manno-octulosonic acid (Kdo) hydrolase that removes the outer Kdo sugar of Helicobacter pylori lipopolysaccharide. J. Bacteriol. 187: 33743383.
121. Steeghs, L.,, R. den Hartog,, A. den Boer,, B. Zomer,, P. Roholl, and, P. van der Ley. 1998. Meningitis bacterium is viable without endotoxin. Nature (Lond.) 392: 449450.
122. Takeshita, M., and, P. H. Makela. 1971. Glucosylation of lipopolysaccharide in Salmonella: biosynthesis of O antigen factor 12 2.3.The presence of 12 2 determinants in haptenic polysaccharides. J. Biol. Chem. 246: 39203927.
123. Tamayo, R.,, B. Choudhury,, A. Septer,, M. Merighi,, R. Carlson, and, J. S. Gunn. 2005. Identification of cptA, a PmrA-regulated locus required for phosphoethanolamine modification of the Salmonella enterica serovar Typhimurium lipopolysaccharide core. J. Bacteriol. 187: 33913399.
124. Tefsen, B.,, M. P. Bos,, F. Beckers,, J. Tommassen, and, H. de Cock. 2005a. MsbA is not required for phospholipid transport in Neisseria meningitidis. J. Biol. Chem. 280: 3596135966.
125. Tefsen, B.,, J. Geurtsen,, F. Beckers,, J. Tommassen, and, H. de Cock. 2005b. Lipopolysaccharide transport to the bacterial outer membrane in spheroplasts. J. Biol. Chem. 280: 45044509.
126. Tlapak-Simmons, V. L.,, C. A. Baron,, R. Gotschall,, D. Haque,, W. M. Canfield, and, P. H. Weigel. 2005. Hyaluronan biosynthesis by class I streptococcal hyaluronan synthases occurs at the reducing end. J. Biol. Chem. 280: 1301213018.
127. Tran, A. X.,, M. J. Karbarz,, X. Wang,, C. R. Raetz,, S. C. McGrath,, R. J. Cotter, and, M. S. Trent. 2004. Periplasmic cleavage and modification of the 1-phosphate group of Helicobacter pylori lipid A. J. Biol. Chem. 279: 5578055791.
128. Tran, A. X.,, M. E. Lester,, C. M. Stead,, C. R. Raetz,, D. J. Maskell,, S. C. McGrath,, R. J. Cotter, and, M. S. Trent. 2005. Resistance to the antimicrobial peptide polymyxin requires myristoylation of Escherichia coli and Salmonella typhimurium lipid A. J. Biol. Chem. 280: 2818628194.
129. Trent, M. S., 2004. Biosynthesis, transport, and modification of lipid A. Biochem. Cell Biol. 82: 7186.
130. Trent, M. S.,, W. Pabich,, C. R. Raetz, and, S. I. Miller. 2001a. A PhoP/PhoQ-induced lipase (PagL) that catalyzes 3-O-deacylation of lipid A precursors in membranes of Salmonella typhimurium. J. Biol. Chem. 276: 90839092.
131. Trent, M. S.,, A. A. Ribeiro,, W. T. Doerrler,, S. Lin,, R. J. Cotter, and, C. R. Raetz. 2001b. Accumulation of a polyisoprene-linked amino sugar in polymyxin-resistant Salmonella typhimurium and Escherichia coli: structural characterization and transfer to lipid A in the periplasm. J. Biol. Chem. 276: 4313243144.
132. Trent, M. S.,, A. A. Ribeiro,, S. Lin,, R. J. Cotter, and, C. R. Raetz. 2001c. An inner membrane enzyme in Salmonella and Escherichia coli that transfers 4-amino-4-deoxy-l-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipid-linked donor. J. Biol. Chem. 276: 4312243131.
133. Vaara, M., 1992. Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56: 395411.
134. Valvano, M. A., 2003. Export of O-specific lipopolysaccharide. Front. Biosci. 8: s452s471.
135. Vander Byl, C., and, A. M. Kropinski. 2000. Sequence of the genome of Salmonella bacteriophage P22. J.Bacteriol. 182: 64726481.
136. Verma, N. K.,, J. M. Brandt,, D. J. Verma, and, A. A. Lindberg. 1991. Molecular characterization of the O-acetyl transferase gene of converting bacteriophage SF6 that adds group antigen 6 to Shigella flexneri. Mol. Microbiol. 5: 7175.
137. Vines, E. D.,, C. L. Marolda,, A. Balachandran, and, M. A. Valvano. 2005. Defective O-antigen polymerization in tolA and pal mutants of Escherichia coli in response to extracytoplasmic stress. J. Bacteriol. 187: 33593368.
138. Vinogradov, E.,, E. Frirdich,, L. L. MacLean,, M. B. Perry,, B. O. Petersen,, J. O. Duus, and, C. Whitfield., 2002. Structures of lipopolysaccharides from Klebsiella pneumoniae. Elucidation of the structure of the linkage region between core and polysaccharide O chain and identification of the residues at the non-reducing termini of the O chains. J. Biol. Chem. 277: 2507025081.
139. Vollmer, W., and, J. V. Holtje. 2001. Morphogenesis of Escherichia coli. Curr. Opin. Microbiol. 4: 625633.
140. Voulhoux, R.,, M. P. Bos,, J. Geurtsen,, M. Mols, and, J. Tommassen. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299: 262265.
141. Wang, L.,, D. Liu, and, P. R. Reeves. 1996. C-terminal half of Salmonella enterica WbaP (RfbP) is a galactosyl-1-phosphate transferase domain catalyzing the first step of O-antigen synthesis. J. Bacteriol. 178: 25982604.
142. Wang, X.,, M. J. Karbarz,, S. C. McGrath,, R. J. Cotter, and, C. R. Raetz. 2004. MsbA transporter-dependent lipid A 1-dephosphorylation on the periplasmic surface of the inner membrane: topography of Francisella novicida LpxE expressed in Escherichia coli. J. Biol. Chem. 279: 4947049478.
143. Whitfield, C., 1995. Biosynthesis of lipopolysaccharide O-antigens. Trends Microbiol. 3: 178185.
144. Whitfield, C., 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75: 3968.
145. Whitfield, C.,, P. A. Amor, and, R. Köplin. 1997. Modulation of surface architecture of gram-negative bacteria by the action of surface polymer:lipid A-core ligase and by determinants of polymer chain length. Mol. Microbiol. 23: 629638.
146. Whitfield, C.,, N. Kaniuk, and, E. Frirdich. 2003. Molecular insights into the assembly and diversity of the outer core oligosaccharide in lipopolysaccharides from Escherichia coli and Salmonella. J. Endotox. Res. 9: 244249.
147. Whitfield, C., and, A. Paiment. 2003. Biosynthesis and assembly of group 1 capsular polysaccharides in Escherichia coli and related extracellular polysaccharides in other bacteria. Carbohydr. Res. 338: 24911502.
148. Williams, G. J.,, S. D. Breazeale,, C. R. Raetz, and, J. H. Naismith. 2005. Structure and function of both domains of ArnA, a dual function decarboxylase and a formyltransferase, involved in 4-amino-4-deoxy-l-arabinose biosynthesis. J. Biol. Chem. 280: 2300023008.
149. Wosten, M. M.,, L. F. Kox,, S. Chamnongpol,, F. C. Soncini, and, E. A. Groisman. 2000. A signal transduction system that responds to extracellular iron. Cell 103: 113125.
150. Wu, T.,, J. Malinverni,, N. Ruiz,, S. Kim,, T. J. Silhavy, and, D. Kahne. 2005. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121: 235245.
151. Wu, T.,, A. C. McCandlish,, L. S. Gronenberg,, S. S. Chang,, T. J. Silhavy, and, D. Kahne. 2006. Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA 103: 1175411759.
152. Wugeditsch, T.,, A. Paiment,, J. Hocking,, J. Drummelsmith,, C. Forrester, and, C. Whitfield. 2001. Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J. Biol. Chem. 276: 23612371.
153. Zhou, Z.,, S. Lin,, R. J. Cotter, and, C. R. Raetz. 1999. Lipid A modifications characteristic of Salmonella typhimurium are induced by NH 4VO 3 in Escherichia coli K12.Detection of 4-amino-4-deoxy-l-arabinose, phosphoethanolamine and palmitate. J. Biol. Chem. 274: 1850318514.
154. Zhou, Z.,, A. A. Ribeiro,, S. Lin,, R. J. Cotter,, S. I. Miller, and, C. R. Raetz. 2001. Lipid A modifications in polymyxin-resistant Salmonella typhimurium: PMRA-dependent 4-amino-4-deoxy-l-arabinose, and phosphoethanolamine incorporation. J. Biol. Chem. 276: 4311143121.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error