1887

Chapter 11 : Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance

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

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap11-1.gif /docserver/preview/fulltext/10.1128/9781555818524/9781555816766_Chap11-2.gif

Abstract:

Lipopolysaccharide (LPS) is the major component of the outer membrane of gram-negative bacteria and consists of three distinct structural domains: lipid A, a nonrepeating “core” oligosaccharide, and a distal repeated O-antigen polysaccharide. This chapter discusses the structure of the three regions, in order, as they extend out from the outer membrane, focusing on regulated alterations, modifications, and/or substitutions. The biosynthetic enzymes are either constitutively active or regulated by a variety of two-component regulatory systems, including PhoR/PhoB, PmrA/PmrB and/or PhoP/PhoQ. Deletion of IpxT in resulted in an increase in sensitivity to the cationic antimicrobial peptides (AMPs) polymyxin B, although experiments elucidating roles for lpxT in overall pathogenesis have yet to be undertaken. The chapter explores the regulation of one particular modification, that of phosphorylcholine (ChoP), on and lipooligosaccharide (LOS). Regulation of LPS core biosynthesis is not well understood, although some of the regulatory mechanisms for biosynthesis of Kdo and inner and outer core are emerging. The current evidence based on genetic and biophysical interaction studies of the Lpt proteins supports the transenvelope model. Further studies into the regulation of LPS should help provide a link between signals in the environment and the resulting outer membrane composition that are likely to have the most impact on host-pathogen interactions.

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Schematic representation of modifications of terminal residues of lipid A. The diagram shows the possible modifications outside of the terminal residues of lipid A. Chemical groups are color coded by the enzyme responsible for their action; a plus sign indicates an addition to the base structure, and a minus sign indicates a removal. Under each enzyme is the regulatory system that controls each its action; an upward-pointing arrow indicates a positive regulator, and a downward-pointing arrow indicates a negative regulator. doi:10.1128/9781555818524.ch11f1

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Pathway for the synthesis of Kdo. KdsD converts dribulose 5-phosphate to d-arabinose 5-phosphate. d-Arabinose 5-phosphate and phosphoenolpyruvate are combined by KdsA to form Kdo 8-phosphate. KdsC cleaves Kdo 8-phosphate to Kdo and inorganic phosphate. KdsB mediates the reaction of Kdo and CTP to form the activated sugar CMP-Kdo and PP. This active sugar is added to lipid IV in the inner membrane. doi:10.1128/9781555818524.ch11f2

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Structures of LPS core. Structures of known inner and outer cores for serovar Typhimurium (A), K-12 (B), and R1 (C), R2 (D), R3 (E), and R4 (F). All genes with known/proposed activities are indicated with gray arrows at the sites of activity. Adapted from A. Silipo and A. Molinaro, 2010. doi:10.1128/9781555818524.ch11f3

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Genetic organization of LPS core and LPS transport genes. (A) K-12 operon and known promoters. All promoters are indicated with interacting sigma factors. Genes for LPS transport are in white; the gene, part of the cation antiporter family, is shown in dark blue, and inner core genes are shown in black. (B) K-12 and operons with the gene and indicated promoters. Promoters are labeled with interacting sigma factors; promoters in black indicate active promoters, while blue promoters have not been proven active. Genes implicated in O-antigen synthesis are displayed in white, outer core genes are shown in blue, and inner core genes are shown in black. doi:10.1128/9781555818524.ch11f4

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Structure and visualization of LPS. (A) The typical gram-negative membrane is comprised of the inner membrane, the periplasm, and the outer membrane. The inner membrane is a phospholipid bilayer with integral and peripheral membrane proteins. (B) Representation of LPS structure showing the O antigen in blue, core in purple, and lipid A in yellow. Phosphates are shown as black circles. (C) LPS from Typhimurium strain 14028s and its isogenic Δ mutant. The lower-molecularweight bands demonstrate the banding pattern associated with increasing O-antigen side chains. The loss of long chain lengths due to the absence of is evident in the deletion mutant strain. Since is still contained in the genome of both strains, the very long chain length is still detected at the top of the gel. LPS was detected using Salmonella O Antiserum Factor 4 from Difco Laboratories. doi:10.1128/9781555818524.ch11f5

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

O-antigen loci from different gram-negative bacteria. Organizations of loci were obtained from the Genome home of NCBI (http://www.ncbi.nlm.nih.gov/sites/genome). Strains are as follows: PAO1; Typhimurium LT2, and 2a str 301. Locus tag numbers are provided underneath genes at the beginning and end of the operons. For reference, some of the other O-antigen-associated genes are as follows: , = PA4999 and = PA0938; Typhimurium, () = STM1332 and (second gene) = STM0589; and , = SF3666. doi:10.1128/9781555818524.ch11f6

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 7
Figure 7

Wzy-dependent pathway for O-antigen synthesis and transfer across the inner membrane. The diagram shows that O antigens are synthesized on the Und-P and transferred via the Wzx, O-antigen flippase. The Wzy, O-antigen polymerase, extends the chains, the length of which is controlled by the Wzz O-antigen regulator. (Adapted from ) doi:10.1128/9781555818524.ch11f7

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 8
Figure 8

ABC transporter-dependent pathway for transfer across the inner membrane. The diagram shows the transfer of the Und- P-linked O antigen across the inner membrane by the ABC transporter, Wzm and Wzt. (Adapted from ) doi:10.1128/9781555818524.ch11f8

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 9
Figure 9

Diagram of the two proposed LptA transport mechanisms. In both models, MsbA transports the lipid A-core across the inner membrane. The completed Und-linked O antigen is transferred to the lipid A-core via the WaaL, O-antigen ligase (not shown). The left model shows that LptA docks with LptC and picks up the lipid A-core-O antigen and transports it across the periplasmic space, where it docks with the LptDE complex before being translocated across the outer membrane. In the right model, LptA oligomerizes to form a scaffold that allows the LPS to be transported across the periplasmic space. (Adapted from ) doi:10.1128/9781555818524.ch11f9

Citation: Ernst R, Powell D, Hittle L, GOLDBERG J, KINTZ E. 2013. Regulation of Lipopolysaccharide Modifications and Antimicrobial Peptide Resistance , p 209-238. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch11
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818524.chap11
1. Allison, G. E.,, and N. K. Verma. 2000. Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol. 81:1723.
2. Alpuche Aranda, C. M.,, J. A. Swanson,, W. P. Loomis,, and S. I. Miller. 1992. Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc. Natl. Acad. Sci. USA 89:1007910083.
3. Asensio, C. J.,, M. E. Gaillard,, G. Moreno,, D. Bottero,, E. Zurita,, M. Rumbo,, P. van derLey,, A. van der Ark,, and D. Hozbor. 2011. Outer membrane vesicles obtained from Bordetella pertussis Tohama expressing the lipid A deacylase PagL as a novel acellular vaccine candidate. Vaccine 29:16491656.
4. 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.
5. Bailey, M. J.,, C. Hughes,, and V. Koronakis. 2000. In vitro recruitment of the RfaH regulatory protein into a specialised transcription complex, directed by the nucleic acid ops element. Mol. Gen. Genet. 262:10521059.
6. 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.
7. Belden, W. J.,, and S. I. Miller. 1994. Further characterization of the PhoP regulon: identification of new PhoP-activated virulence loci. Infect. Immun. 62:50955101.
8. Belunis, C. J.,, T. Clementz,, S. M. Carty,, and C. R. Raetz. 1995. Inhibition of lipopolysaccharide biosynthesis and cell growth following inactivation of the kdtA gene in Escherichia coli. J. Biol. Chem. 270:2764627652.
9. Bengoechea, J. A.,, L. Zhang,, P. Toivanen,, and M. Skurnik. 2002. Regulatory network of lipopolysaccharide O-antigen biosynthesis in Yersinia enterocolitica includes cell envelope-dependent signals. Mol. Microbiol. 44:10451062.
10. Beutler, B. 2005. The Toll-like receptors: analysis by forward genetic methods. Immunogenetics 57:385392.
11. Bishop, R. E. 2008. Structural biologyof membrane-intrinsic beta-barrel enzymes: sentinels of the bacterial outermembrane. Biochim. Biophys. Acta 1778:18811896.
12. Bishop, R. E.,, H. S. Gibbons,, T. Guina,, M. S. Trent,, S. I. Miller,, and C. R. Raetz. 2000. Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J. 19:50715080.
13. Biswas, T.,, L. Yi,, P. Aggarwal,, J. Wu,, J. R. Rubin,, J. A. Stuckey,, R. W. Woodard,, and O. V. Tsodikov. 2009. The tail of KdsC: conformational changes control the activity of a haloacid dehalogenase superfamily phosphatase. J. Biol. Chem. 284:3059430603.
14. Bittner, M.,, S. Saldias,, F. Altamirano,, M. A. Valvano,, and I. Contreras. 2004. RpoS and RpoN are involved in the growth-dependent regulation of rfaH transcription and O antigen expression in Salmonella enterica serovar Typhi. Microb. Pathog. 36:1924.
15. Bittner, M.,, S. Saldias,, C. Estevez,, M. Zaldivar,, C. L. Marolda,, M. A. Valvano,, and I. Contreras. 2002. O-antigen expressionin Salmonella enterica serovar Typhi is regulated by nitrogen availability through RpoN-mediated transcriptional control of the rfaH gene. Microbiology 148(Pt. 12):37893799.
16. Bos, M. P.,, and J. Tommassen. 2011. The LptD chaperone LptE is not directly involved in lipopolysaccharide transport in Neisseria meningitidis. J. Biol. Chem. 286:2868828696.
17. Bowyer, A.,, J. Baardsnes,, E. Ajamian,, L. Zhang,, and M. Cygler. 2011. Characterization of interactions between LPS transport proteins of the Lpt system. Biochem. Biophys. Res. Commun. 404:10931098.
18. Broadbent, S. E.,, M. R. Davies,, and M. W. van der Woude. 2010. Phase variationcontrols expression of Salmonella lipopolysaccharide modification genes by a DNAmethylation-dependent mechanism. Mol. Microbiol. 77:337353.
19. Bronner, D.,, B. R. Clarke,, and C. Whitfield. 1994. Identification of an ATP-binding cassette transport system required for translocation of lipopolysaccharide O-antigen side-chains across the cytoplasmic membrane of Klebsiella pneumoniae serotype O1. Mol. Microbiol. 14:505519.
20. Brozek, K. A.,, and C. R. Raetz. 1990. Biosynthesis of lipid A in Escherichia coli. Acyl carrier protein-dependent incorporation of laurate and myristate. J. Biol. Chem. 265:1541015417.
21. 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.
22. Carter, J. A.,, C. J. Blondel,, M. Zaldivar,, S. A. Alvarez,, C. L. Marolda,, M. A. Valvano,, and I. Contreras. 2007. O-antigen modal chainlength in Shigella flexneri 2a is growth-regulated through RfaH-mediatedtranscriptional control of the wzy gene. Microbiology 153(Pt. 10):34993507.
23. Carter, J. A.,, J. C. Jimenez,, M. Zaldivar,, S. A. Alvarez,, C. L. Marolda,, M. A. Valvano,, and I. Contreras. 2009. The cellular level ofO-antigen polymerase Wzy determines chain length regulation by WzzB and WzzpHS-2 in Shigellaflexneri 2a. Microbiology 155(Pt.10):32603269.
24. Chalabaev, S.,, T. H. Kim,, R. Ross,, A. Derian,, and D. L. Kasper. 2010. 3-Deoxy-D-manno-octulosonic acid (Kdo) hydrolase identified in Francisella tularensis, Helicobacter pylori, and Legionella pneumophila. J. Biol. Chem. 285:3433034336.
25. Chimalakonda, G.,, N. Ruiz,, S. S. Chng,, R. A. Garner,, D. Kahne,, and T. J. Silhavy. 2011. Lipoprotein LptE is required for the assembly of LptD by the beta-barrel assembly machine in the outer membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA 108:24922497.
26. Chng, S. S.,, L. S. Gronenberg,, and D. Kahne. 2010a. Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49:45654567.
27. Chng, S. S.,, N. Ruiz,, G. Chimalakonda,, T. J. Silhavy,, and D. Kahne. 2010b. Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc. Natl. Acad. Sci. USA107:53635368.
28. Cipolla, L.,, A. Polissi,, C. Airoldi,, P. Galliani,, P. Sperandeo,, and F. Nicotra. 2009. The Kdo biosynthetic pathway toward OM biogenesis as target in antibacterial drug design and development. Curr. Drug Discov. Technol. 6:1933.
29. Clementz, T. 1992. The gene coding for 3-deoxy-manno-octulosonic acid transferase and the rfaQ gene are transcribed from divergently arranged promoters in Escherichia coli. J. Bacteriol. 174:77507756.
30. Clementz, T.,, J. J. Bednarski,, and C. R. Raetz. 1996. Function of the htrB high temperature requirement gene of Escherchia coli in theacylation of lipid A: HtrB catalyzed incorporation of laurate. J. Biol.Chem. 271:1209512102.
31. Coats, S. R.,, C. T. Do,, L. M. Karimi-Naser,, P. H. Braham,, and R. P. Darveau. 2007. Antagonistic lipopolysaccharides block E. coli lipopolysaccharide function at human TLR4 via interaction with the human MD-2 lipopolysaccharide binding site. Cell. Microbiol. 9:11911202.
32. Comstock, L. E.,, and D. L. Kasper. 2006. Bacterial glycans: key mediators of diverse host immune responses. Cell 126:847850.
33. Corsaro, M. M.,, E. Parrilli,, R. Lanzetta,, T. Naldi,, G. Pieretti,, B. Lindner,, A. Carpentieri,, M. Parrilli,, and M. L. Tutino. 2009. The presence of OMP inclusion bodies in a Escherichia coli K-12 mutated strain is not related to lipopolysaccharide structure. J. Biochem. 146:231240.
34. Cox, A. D.,, J. C. Wright,, J. Li,, D. W. Hood,, E. R. Moxon,, and J. C. Richards. 2003. Phosphorylation of the lipid A region of meningococcal lipopolysaccharide: identification of a family of transferases that add phosphoethanolamine to lipopolysaccharide. J. Bacteriol. 185:32703277.
35. Creeger, E. S.,, and L. I. Rothfield. 1979. Cloning of genes for bacterial glycosyltransferases. I. Selection of hybrid plasmids carrying genes for two glucosyltransferases. J. Biol. Chem. 254:804810.
36. Cullen, T. W.,, and M. S. Trent. 2010. A link between the assembly of flagella and lipooligosaccharide of the Gram-negative bacterium Campylobacter jejuni. Proc. Natl. Acad. Sci. USA 107:51605165.
37. 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.
38. 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.
39. Dartigalongue, C.,, D. Missiakas,, and S. Raina. 2001. Characterization of the Escherichia coli sigma E regulon. J. Biol. Chem. 276:20866-20875.
40. Darveau, R. P.,, T. T. Pham,, K. Lemley,, R. A. Reife,, B. W. Bainbridge,, S. R. Coats,, W. N. Howald,, S. S. Way,, and A. M. Hajjar. 2004. Porphyromonas gingivalis lipopolysaccharide contains multiple lipid A species that functionally interact with both Toll-like receptors 2 and 4. Infect. Immun. 72:50415051.
41. de Cock, H.,, K. Brandenburg,, A. Wiese,, O. Holst,, and U. Seydel. 1999. Non-lamellar structure and negative charges of lipopolysaccharides required for efficient folding of outer membrane protein PhoE of Escherichia coli. J. Biol. Chem. 274:51145119.
42. de Cock, H.,, and J. Tommassen. 1996. Lipopolysaccharides and divalent cations are involved in the formation of an assembly-competent intermediate of outer-membrane protein PhoE of E. coli. EMBO J. 15:55675573.
43. Delgado, M. A.,, C. Mouslim,, and E. A. Groisman. 2006. The PmrA/PmrB and RcsC/YojN/RcsB systems control expression of the Salmonella O-antigen chain length determinant. Mol. Microbiol. 60:3950.
44. Derzelle, S.,, E. Turlin,, E. Duchaud,, S. Pages,, F. Kunst,, A. Givaudan,, and A. Danchin. 2004. The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J. Bacteriol. 186:12701279.
45. 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.
46. El Ghachi, M.,, A. Derbise,, A. Bouhss,, and D. Mengin-Lecreulx. 2005. Identificationof multiple genes encoding membrane proteins with undecaprenyl pyrophosphate phosphatase (UppP)activity in Escherichia coli. J. Biol. Chem. 280:1868918695.
47. Ernst, R. K.,, E. C. Yi,, L. Guo,, K. B. Lim,, J. L. Burns,, M. Hackett,, and S. I. Miller. 1999. Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286:15611565.
48. Fox, K. L.,, J. Li,, E. K. Schweda,, V. Vitiazeva,, K. Makepeace,, M. P. Jennings,, E. R. Moxon,, and D. W. Hood. 2008. Duplicate copies of lic1 direct the addition of multiple phosphocholine residues in the lipopolysaccharide of Haemophilus influenzae. Infect. Immun. 76:588600.
49. 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.
50. Frirdich, E.,, B. Lindner,, O. Holst,, and C. Whitfield. 2003. Overexpression of the waaZ gene leads to modification of the structure of the inner core region of Escherichia coli lipopolysaccharide, truncation of the outer core, and reduction of the amount of O polysaccharide on the cell surface. J. Bacteriol. 185:16591671.
51. Frirdich, E.,, and C. Whitfield. 2005. Lipopolysaccharide inner core oligosaccharide structure and outer membrane stability in human pathogens belonging to the Enterobacteriaceae. J. Endotoxin Res. 11:133144.
52. Garcia Vescovi, E.,, F. C. Soncini,, and E. A. Groisman. 1996. Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84:165174.
53. Gibbons, H. S.,, S. R. Kalb,, R. J. Cotter,, and C. R. Raetz. 2005. Role of Mg2+ and pH in the modification of Salmonella lipid A after endocytosis by macrophage tumour cells. Mol. Microbiol. 55:425440.
54. 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 Fe2+/alpha-ketoglutarate-dependent dioxygenase homologue. J. Biol. Chem. 275:3294032949.
55. Golden, N. J.,, and D. W. Acheson. 2002. Identification of motility and autoagglutination Campylobacter jejuni mutants by random transposon mutagenesis. Infect. Immun. 70:17611771.
56. Grizot, S.,, M. Salem,, V. Vongsouthi,, L. Durand,, F. Moreau,, H. Dohi,, S. Vincent,, S. Escaich,, and A. Ducruix. 2006. Structure of the Escherichia coli heptosyltransferase WaaC: binary complexes with ADP and ADP-2-deoxy-2-fluoro heptose. J. Mol. Biol. 363:383394
57. Groisman, E. A.,, E. Chiao,, C. J. Lipps,, and F. Heffron. 1989. Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc. Natl. Acad. Sci. USA 86:70777081.
58. Gronow, S.,, W. Brabetz,, and H. Brade. 2000. Comparative functional characterization in vitro of heptosyltransferase I (WaaC) and II (WaaF) from Escherichia coli. Eur. J. Biochem. 267:66026611.
59. 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.
60. Gunn, J. S.,, and S. I. Miller. 1996. PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J. Bacteriol. 178:68576864.
61. 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.
62. Guo, H.,, K. Lokko,, Y. Zhang,, W. Yi,, Z. Wu,, and P. G. Wang. 2006. Overexpression and characterization of Wzz of Escherichia coli O86:H2. Protein Expr. Purif. 48:4955.
63. 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.
64. Hajjar, A. M.,, R. K. Ernst,, J. H. Tsai,, C. B. Wilson,, and S. I. Miller. 2002. Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nat. Immunol. 3:354359.
65. Hankins, J. V.,, J. A. Madsen,, D. K. Giles,, B. M. Childers,, K. E. Klose,, J. S. Brodbelt,, and M. S. Trent. 2011. Elucidation of a novel Vibrio cholerae lipid A secondary hydroxy-acyltransferase and its role in innate immune recognition. Mol. Microbiol. 81:13131329.
66. Hankins, J. V.,, and M. S. Trent. 2009. Secondary acylation of Vibrio cholerae lipopolysaccharide requires phosphorylation of Kdo. J. Biol. Chem. 284:2580425812.
67. Hegge, F. T.,, P. G. Hitchen,, F. E. Aas,, H. Kristiansen,, C. Lovold,, W. Egge-Jacobsen,, M. Panico,, W. Y. Leong,, V. Bull,, M. Virji,, H. R. Morris,, A. Dell,, and M. Koomey. 2004. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc. Natl. Acad. Sci. USA 101:1079810803.
68. 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.
69. Heinrichs, D. E.,, J. A. Yethon,, P. A. Amor,, and C. Whitfield. 1998b. The assembly system for the outer core portion of R1- and R4-type lipopolysaccharides of Escherichia coli. The R1 core-specific beta-glucosyltransferase provides a novel attachment site for O-polysaccharides. J. Biol. Chem. 273:2949729505.
70. Heinrichs, D. E.,, J. A. Yethon,, and C. Whitfield. 1998c. Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol. Microbiol. 30:221232.
71. Helander, I. M.,, I. Kilpelainen,, and M. Vaara. 1994. Increased substitution of phosphate groups in lipopolysaccharides and lipid A of the polymyxin-resistant pmrA mutants of Salmonella typhimurium: a 31P-NMR study. Mol. Microbiol. 11:481487.
72. Herrera, C. M.,, J. V. Hankins,, and M. S. Trent. 2010. Activation of PmrA inhibits LpxT-dependent phosphorylation of lipid A promoting resistance to antimicrobial peptides. Mol. Microbiol. 76:14441460.
73. Hitchen, P. G.,, J. L. Prior,, P. C. Oyston,, M. Panico,, B. W. Wren,, R.W. Titball,, H. R. Morris,, and A. Dell. 2002. Structural characterization of lipo-oligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system. Mol. Microbiol. 44:16371650.
74. Hobbs, M.,, and P. R. Reeves. 1994. The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters. Mol. Microbiol. 12:855856.
75. Hong, W.,, B. Pang,, S. West-Barnette,, and W. E. Swords. 2007. Phosphorylcholine expression by nontypeable Haemophilus influenzae correlates with maturation of biofilm communities in vitro and in vivo. J. Bacteriol. 189:83008307.
76. Hwang, P. M.,, W. Y. Choy,, E. I. Lo,, L. Chen,, J. D. Forman-Kay,, C.R. Raetz,, G. G. Prive,, R. E. Bishop,, and L. E. Kay. 2002. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl. Acad. Sci. USA 99:1356013565.
77. Ingram, B. O.,, C. Sohlenkamp,, O. Geiger,, and C. R. Raetz. 2010. Altered lipid A structuresand polymyxin hypersensitivity of Rhizobium etli mutants lacking the LpxE and LpxFphosphatases. Biochim. Biophys. Acta 1801:593604.
78. Isobe, T.,, K. A. White,, A. G. Allen,, M. Peacock,, C. R. Raetz,, and D. J. Maskell. 1999. Bordetella pertussis waaA encodes a monofunctional 2-keto-3-deoxy-D-manno-octulosonic acid transferase that can complement an Escherichia coli waaA mutation. J. Bacteriol. 181:26482651.
79. Ivanov, I. E.,, E. N. Kintz,, L. A. Porter,, J. B. Goldberg,, N. A. Burnham,, and T. A. Camesano. 2011. Relating the physical properties of Pseudomonas aeruginosa lipopolysaccharides to virulence by atomic force microscopy. J. Bacteriol. 193:12591266.
80. Jimenez, N.,, R. Canals,, M. T. Salo,, S. Vilches,, S. Merino,, and J.M. Tomas. 2008. The Aeromonas hydrophila wb*O34 gene cluster: genetics and temperature regulation. J. Bacteriol. 190:41984209.
81. Joiner, K. A.,, C. H. Hammer,, E. J. Brown,, R. J. Cole,, and M.M. Frank. 1982. Studies on the mechanism of bacterial resistance to complement-mediated killing. I. Terminal complement components are deposited and released from Salmonella minnesota S218 without causing bacterial death. J. Exp. Med. 155:797808.
82. Kadam, S. K.,, A. Rehemtulla,, and K. E. Sanderson. 1985. Cloning of rfaG, B, I, and J genes for glycosyltransferase enzymes for synthesis of the lipopolysaccharide core of Salmonella typhimurium. J. Bacteriol. 161:277284.
83. Kaluzny, K.,, P. D. Abeyrathne,, and J. S. Lam. 2007. Coexistence of two distinct versions of O-antigen polymerase, Wzy-alpha and Wzy-beta, in Pseudomonas aeruginosa serogroup O2 and their contributions to cell surface diversity. J. Bacteriol. 189:41414152.
84. Kalynych, S.,, X. Ruan,, M. A. Valvano,, and M. Cygler. 2011. Structure-guided investigation of lipopolysaccharide O-antigen chain length regulators reveals regions critical for modal length control. J. Bacteriol. 193:37103721.
85. Kaniuk, N. A.,, E. Vinogradov,, J. Li,, M. A. Monteiro,, and C. Whitfield. 2004. Chromosomal and plasmid-encoded enzymes are required for assembly of the R3-type core oligosaccharide in the lipopolysaccharide of Escherichia coli O157:H7. J. Biol. Chem. 279:3123731250.
86. 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.
87. Karow, M.,, O. Fayet,, A. Cegielska,, T. Ziegelhoffer,, and C. Georgopoulos. 1991a. Isolation and characterization of the Escherichia coli htrB gene, whose product is essential for bacterial viability above 33°C in rich media. J. Bacteriol. 173:741750.
88. Karow, M.,, S. Raina,, C. Georgopoulos,, and O. Fayet. 1991b. Complex phenotypes of null mutations in the htr genes, whose products are essential for Escherichia coli growth at elevated temperatures. Res. Microbiol. 142:289294.
89. Karow, M.,, and C. Georgopoulos. 1991. Sequencing, mutational analysis, and transcriptional regulation of the Escherichia coli htrB gene. Mol. Microbiol. 5:22852292.
90. 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.
91. Kawano, M.,, T. Manabe,, and K. Kawasaki. 2010. Salmonella enterica serovar Typhimurium lipopolysaccharide deacylation enhances its intracellular growth within macrophages. FEBS Lett. 584:207212.
92. Kawasaki, K.,, K. China,, and M. Nishijima. 2007. Release of the lipopolysaccharide deacylase PagL from latency compensates for a lack of lipopolysaccharide aminoarabinose modification-dependent resistance to the antimicrobial peptide polymyxin B in Salmonella enterica. J. Bacteriol. 189:49114919.
93. Kawasaki, K.,, R. K. Ernst,, and S. I. Miller. 2004a. 3-O-deacylation of lipidA by PagL, a PhoP/PhoQ-regulated deacylase of Salmonella typhimurium, modulatessignaling through Toll-like receptor 4. J. Biol. Chem. 279:2004420048.
94. Kawasaki, K.,, R. K. Ernst,, and S. I. Miller. 2004b. Deacylation and palmitoylation of lipid A by Salmonellae outer membrane enzymes modulate host signaling through Toll-like receptor 4. J. Endotoxin Res. 10:439444.
95. 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.
96. Keenleyside, W. J.,, and C. Whitfield. 1996. A novel pathway for O-polysaccharide biosynthesis in Salmonella enterica serovar Borreze. J. Biol. Chem. 271:2858128592.
97. Keenleyside, W. J.,, and C. Whitfield,. 1999. Genetics andbiosynthesis of lipopolysaccharide O-antigens, p. 331358. In C. M. H. Brade,, S. M. Opal,, and S. N. Vogel (ed.), Endotoxin in Health and Disease. Marcel Dekker, Inc., New York, NY.
98. Kim, S. H.,, K. S. Kim,, S. R. Lee,, E. Kim,, M. S. Kim,, E. Y. Lee,, Y. S. Gho,, J. W. Kim,, R. E. Bishop,, and K. T. Chang. 2009. Structural modifications of outer membrane vesicles to refine them as vaccine delivery vehicles. Biochim. Biophys. Acta 1788:21502159.
99. Kintz, E.,, and J. B. Goldberg. 2008. Regulation of lipopolysaccharide O antigen expression in Pseudomonas aeruginosa. Future Microbiol. 3:191203.
100. Kintz, E.,, J. M. Scarff,, A. DiGiandomenico,, and J. B. Goldberg. 2008. Lipopolysaccharide O-antigen chain length regulation in Pseudomonas aeruginosa serogroup O11 strain PA103. J. Bacteriol. 190:27092716.
101. Knirel, Y. A.,, B. Lindner,, E. Vinogradov,, R. Z. Shaikhutdinova,, S. N. Senchenkova,, N. A. Kocharova,, O. Holst,, G. B. Pier,, and A. P. Anisimov. 2005. Cold temperature-induced modifications to the composition and structure of the lipopolysaccharide of Yersinia pestis. Carbohydr. Res. 340:16251630.
102. Koprivnjak, T.,, and A. Peschel. 2011. Bacterial resistance mechanisms against host defense peptides. Cell. Mol. Life Sci. 68:22432254.
103. Koretke, K. K.,, A. N. Lupas,, P. V. Warren,, M. Rosenberg,, and J. R. Brown. 2000. Evolution of two-componentsignal transduction. Mol. Biol. Evol. 17:19561970.
104. Kox, L. F.,, M. M. Wosten,, and E. A. Groisman. 2000. A small protein thatmediates the activation of a two-component system by another two-component system. EMBO J. 19:18611872.
105. Kulshin, V. A.,, U. Zahringer,, B. Lindner,, C. E. Frasch,, C. M. Tsai,, B.A. Dmitriev,, and E. T. Rietschel. 1992. Structural characterization of the lipid A component of pathogenic Neisseria meningitidis. J. Bacteriol. 174:17931800.
106. Kuzio, J.,, and A. M. Kropinski. 1983. O-antigen conversion in Pseudomonas aeruginosa PAO1 by bacteriophage D3. J. Bacteriol. 155:203212.
107. Lamarche, M. G.,, S. H. Kim,, S. Crepin,, M. Mourez,, N. Bertrand,, R. E. Bishop,, J. D. Dubreuil,, and J. Harel. 2008a. Modulation of hexa-acyl pyrophosphate lipid A population under Escherichia coli phosphate (Pho) regulon activation. J. Bacteriol. 190:52565264.
108. Lamarche, M. G.,, B. L. Wanner,, S. Crepin,, and J. Harel. 2008b. The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol. Rev. 32:461473.
109. Larue, K.,, M. S. Kimber,, R. Ford,, and C. Whitfield. 2009. Biochemical and structural analysis of bacterial O-antigen chain length regulator proteins reveals a conserved quaternary structure. J. Biol. Chem. 284:73957403.
110. 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.
111. Lee, J. H.,, K. L. Lee,, W. S. Yeo,, S. J. Park,, and J. H. Roe. 2009a. SoxRS-mediated lipopolysaccharide modification enhances resistance against multiple drugs in Escherichia coli. J. Bacteriol. 191:44414450.
112. Lee, S. R.,, S. H. Kim,, K. J. Jeong,, K. S. Kim,, Y. H. Kim,, S. J. Kim,, E. Kim,, J. W. Kim,, and K. T. Chang. 2009b. Multi-immunogenic outer membrane vesicles derived from an MsbB-deficient Salmonella enterica serovar Typhimurium mutant. J. Microbiol. Biotechnol. 19:12711279.
113. Lewis, L. A.,, B. Choudhury,, J. T. Balthazar,, L. E. Martin,, S. Ram,, P. A. Rice,, D. S. Stephens,, R. Carlson,, and W. M. Shafer. 2009. Phosphoethanolamine substitution of lipid A and resistance of Neisseria gonorrhoeae to cationic antimicrobial peptides and complement-mediated killing by normal human serum. Infect. Immun. 77:11121120.
114. Lippa, A. M.,, and M. Goulian. 2009. Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet. 5:e1000788.
115. Llama-Palacios, A.,, E. Lopez-Solanilla,, and P. Rodriguez-Palenzuela. 2005. Role of the PhoP-PhoQ system in the virulence of Erwinia chrysanthemi strain 3937: involvement in sensitivity to plant antimicrobial peptides, survival at acid pH, and regulation of pectolytic enzymes. J. Bacteriol. 187:21572162.
116. Loomis, W. F.,, A. Kuspa,, and G. Shaulsky. 1998. Two-component signal transduction systems in eukaryotic microorganisms. Curr. Opin. Microbiol. 1:643648.
117. Lysenko, E. S.,, J. Gould,, R. Bals,, J. M. Wilson,, and J. N. Weiser. 2000. Bacterial phosphorylcholine decreases susceptibility to the antimicrobial peptide LL-37/hCAP18 expressed in the upper respiratory tract. Infect. Immun. 68:16641671.
118. Macarthur, I.,, J. W. Jones,, D. R. Goodlett,, R. K. Ernst,, and A. Preston. 2011. The role of pagL and lpxO in Bordetella bronchiseptica lipid A biosynthesis. J. Bacteriol. 193:47264735.
119. Macfarlane, E. L.,, A. Kwasnicka,, and R. E. Hancock. 2000. Role of Pseudomonas aeruginosa PhoP-PhoQ in resistance to antimicrobial cationic peptidesand aminoglycosides. Microbiology 146(Pt.10):25432554.
120. Macfarlane, E. L.,, A. Kwasnicka,, M. M. Ochs,, and R. E. Hancock. 1999. PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol. Microbiol. 34:305316.
121. 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.
122. Marchal, K.,, S. De Keersmaecker,, P. Monsieurs,, N. van Boxel,, K. Lemmens,, G. Thijs,, J. Vanderleyden,, and B. De Moor. 2004. In silico identification and experimental validation of PmrAB targets in Salmonella typhimurium by regulatory motif detection. Genome Biol. 5:R9.
123. Marolda, C. L.,, and M. A. Valvano. 1998. Promoter region of the Escherichia coli O7-specific lipopolysaccharide gene cluster: structural and functional characterization of an upstream untranslated mRNA sequence. J. Bacteriol. 180:30703079.
124. Martorana, A. M.,, P. Sperandeo,, A. Polissi,, and G. Deho. 2011. Complex transcriptional organization regulates an Escherichia coli locus implicated in lipopolysaccharide biogenesis. Res. Microbiol. 162:470482.
125. McGee, D. J.,, A. E. George,, E. A. Trainor,, K. E. Horton,, E. Hildebrandt,, and T. L. Testerman. 2011. Cholesterol enhances Helicobacter pylori resistance to antibiotics and LL-37. Antimicrob. Agents Chemother. 55:28972904.
126. Miller, S. I.,, A. M. Kukral,, and J. J. Mekalanos. 1989. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc. Natl. Acad. Sci. USA 86:50545058.
127. Mohan, S.,, and C. R. Raetz. 1994. Endotoxin biosynthesis in Pseudomonas aeruginosa: enzymatic incorporation of laurate before 3-deoxy-D-manno-octulosonate. J. Bacteriol. 176:69446951.
128. Moran, A. P.,, B. Lindner,, and E. J. Walsh. 1997. Structural characterization of the lipid A component of Helicobacter pylori rough- and smooth-form lipopolysaccharides. J. Bacteriol. 179:64536463.
129. Morona, R.,, L. Purins,, A. Tocilj,, A. Matte,, and M. Cygler. 2009. Sequence-structure relationships in polysaccharide co-polymerase (PCP) proteins. Trends Biochem. Sci. 34:7884.
130. Morona, R.,, L. vanden Bosch,, and P. A. Manning. 1995. Molecular, genetic, andtopological characterization of O-antigen chain length regulation in Shigellaflexneri. J. Bacteriol. 177:10591068.
131. Moss, J. E.,, P. E. Fisher,, B. Vick,, E. A. Groisman,, and A. Zychlinsky. 2000. The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell. Microbiol. 2:443452.
132. Mosser, J. L.,, and A. Tomasz. 1970. Choline-containing teichoic acid as a structural component of pneumococcal cell wall and its role in sensitivity to lysis by an autolytic enzyme. J. Biol. Chem. 245:287298.
133. Munford, R. S. 2008. Sensing gram-negative bacterial lipopolysaccharides: a human disease determinant? Infect. Immun. 76:454465.
134. Murata, T.,, W. Tseng,, T. Guina,, S. I. Miller,, and H. Nikaido. 2007. PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189:72137222.
135. 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.
136. 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. Microbes Infect. 7:12961304.
137. Murray, G. L.,, S. R. Attridge,, and R. Morona. 2006. Altering the length of the lipopolysaccharide O antigen has an impact on the interaction of Salmonella enterica serovar Typhimurium with macrophages and complement. J. Bacteriol. 188:27352739.
138. Nagy, G.,, T. Palkovics,, A. Otto,, H. Kusch,, B. Kocsis,, U. Dobrindt,, S. Engelmann,, M. Hecker,, L. Emody,, T. Pal,, and J. Hacker. 2008. “Gently rough”: the vaccine potential of a Salmonella enterica regulatory lipopolysaccharide mutant. J. Infect. Dis. 198:16991706.
139. 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.
140. Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:593656.
141. Oertelt, C.,, B. Lindner,, M. Skurnik,, and O. Holst. 2001. Isolation and structural characterization of an R-form lipopolysaccharide from Yersinia enterocolitica serotype O:8. Eur. J. Biochem. 268:554564.
142. O’Neill, L. A. 2008a. The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol. Rev. 226:1018.
143. O’Neill, L. A. 2008b. When signaling pathways collide: positive and negative regulation of Toll-like receptor signal transduction. Immunity 29:1220.
144. Oyston, P. C.,, N. Dorrell,, K. Williams,, S. R. Li,, M. Green,, R. W. Titball,, and B. W. Wren. 2000. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68:34193425.
145. Papadopoulos, M.,, and R. Morona. 2010. Mutagenesis and chemical cross-linking suggest that Wzz dimer stability and oligomerization affect lipopolysaccharide O-antigen modal chain length control. J. Bacteriol. 192:33853393.
146. Perez-Gutierrez, C.,, E. Llobet,, C. M. Llompart,, M. Reines,, and J. A. Bengoechea. 2010. Role of lipid A acylation in Yersinia enterocolitica virulence. Infect. Immun. 78: 27682781.
147. Pescaretti, M. M.,, F. E. Lopez,, R. D. Morero,, and M. A. Delgado. 2011. The PmrA/PmrB regulatorysystem controls the expression of wzzfepE gene involvedin the O-antigen synthesis of Salmonella enterica serovarTyphimurium. Microbiology 157:25152521
148. Pilione, M. R.,, E. J. Pishko,, A. Preston,, D. J. Maskell,, and E. T. Harvill. 2004. pagP is required for resistance to antibody-mediated complement lysis during Bordetella bronchiseptica respiratory infection. Infect. Immun. 72:28372842.
149. Plested, J. S.,, K. Makepeace,, M. P. Jennings,, M. A. Gidney,, S. Lacelle,, J. Brisson,, A. D. Cox,, A. Martin,, A. G. Bird,, C. M. Tang,, F. M. Mackinnon,, J. C. Richards,, and E. R. Moxon. 1999. Conservation and accessibility of an inner core lipopolysaccharide epitope of Neisseria meningitidis. Infect. Immun. 67:54175426.
150. Preston, A.,, E. Maxim,, E. Toland,, E. J. Pishko,, E. T. Harvill,, M. Caroff,, and D. J. Maskell. 2003. Bordetella bronchiseptica PagP is a Bvg-regulated lipid A palmitoyl transferase that is required for persistent colonization of the mouse respiratory tract. Mol. Microbiol. 48:725736.
151. Raetz, C. R.,, C. M. Reynolds,, M. S. Trent,, and R. E. Bishop. 2007. Lipid A modification systems in Gram-negative bacteria. Annu. Rev. Biochem. 76:295329.
152. Raetz, C. R.,, and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635700.
153. Raina, S.,, and C. Georgopoulos. 1991. The htrM gene, whose product is essential for Escherichia coli viability only at elevated temperatures, is identical to the rfaD gene. Nucleic Acids Res. 19:38113819.
154. Ranallo, R. T.,, R. W. Kaminski,, T. George,, A. A. Kordis,, Q. Chen,, K. Szabo,, and M. M. Venkatesan. 2010. Virulence, inflammatory potential, and adaptive immunity induced by Shigella flexneri msbB mutants. Infect. Immun. 78:400412.
155. Ray, P. H.,, C. D. Benedict,, and H. Grasmuk. 1981. Purification and characterization of cytidine 5'-triphosphate:cytidine 5'-monophosphate-3-deoxy-D-manno-octulosonate cytidylyltransferase. J. Bacteriol. 145:12731280.
156. Raymond, C. K.,, E. H. Sims,, A. Kas,, D. H. Spencer,, T. V. Kutyavin,, R. G. Ivey,, Y. Zhou,, R. Kaul,, J. B. Clendenning,, and M. V. Olson. 2002. Genetic variation at the O-antigen biosynthetic locus in Pseudomonas aeruginosa. J. Bacteriol. 184:36143622.
157. Rebeil, R.,, R. K. Ernst,, B. B. Gowen,, S. I. Miller,, and B. J. Hinnebusch. 2004. Variation in lipid A structure in the pathogenic Yersiniae. Mol. Microbiol. 52:13631373.
158. Reynolds, C. M.,, A. A. Ribeiro,, S. C. McGrath,, R. J. Cotter,, C. R. Raetz,, and M. S. Trent. 2006. An outer membrane enzymeencoded by Salmonella typhimurium lpxR that removes the 3'-acyloxyacyl moiety of lipid A. J. Biol. Chem. 281:2197421987.
159. Robey, M.,, W. O’Connell,, and N. P. Cianciotto. 2001. Identification of Legionella pneumophila rcp, a pagP-like gene that confers resistance to cationic antimicrobial peptides and promotes intracellular infection. Infect. Immun. 69:42764286.
160. Rojas, G.,, S. Saldias,, M. Bittner,, M. Zaldivar,, and I. Contreras. 2001. The rfaH gene, which affects lipopolysaccharide synthesis in Salmonella enterica serovar Typhi, is differentially expressed during the bacterial growth phase. FEMS Microbiol. Lett. 204:123128.
161. Ruiz, N.,, D. Kahne,, and T. J. Silhavy. 2009. Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat. Rev. Microbiol. 7:677683.
162. Rutten, L.,, J. P. Mannie,, C. M. Stead,, C. R. Raetz,, C. M. Reynolds,, A. M. Bonvin,, J. P. Tommassen,, M. R. Egmond,, M. S. Trent,, and P. Gros. 2009. Active-site architecture and catalytic mechanism of the lipid A deacylase LpxR of Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 106:19601964.
163. Sarnacki, S. H.,, C. L. Marolda,, M. Noto Llana,, M. N. Giacomodonato,, M. A. Valvano,, and M. C. Cerquetti. 2009. Dam methylation controls O-antigen chain length in Salmonella enterica serovar Enteritidis by regulating the expression of Wzz protein. J. Bacteriol. 191: 66946700.
164. Serino, L.,, and M. Virji. 2000. Phosphorylcholine decoration of lipopolysaccharide differentiates commensal Neisseriae from pathogenic strains: identification of licA-type genes in commensal Neisseriae. Mol. Microbiol. 35:15501559.
165. Serino, L.,, and M. Virji. 2002. Genetic and functional analysis of the phosphorylcholine moiety of commensal Neisseria lipopolysaccharide. Mol. Microbiol. 43:437448.
166. Sevostyanova, A.,, V. Svetlov,, D. G. Vassylyev,, and I. Artsimovitch. 2008. The elongation factor RfaH and the initiation factor sigma bind to the same site on the transcription elongation complex. Proc. Natl. Acad. Sci. USA 105:865870.
167. Silipo, A.,, and A. Molinaro. 2010. The diversity of the core oligosaccharide in lipopolysaccharides. Subcell. Biochem. 53:6999.
168. Snyder, L. A.,, S. A. Butcher,, and N. J. Saunders. 2001. Comparativewhole-genome analyses reveal over 100 putative phase-variable genes in the pathogenic Neisseria spp. Microbiology 147(Pt. 8):23212332.
169. Somerville, J. E., Jr.,, L. Cassiano,, B. Bainbridge,, M. D. Cunningham,, and R. P. Darveau. 1996. A novel Escherichia coli lipid A mutant that produces an antiinflammatory lipopolysaccharide. J. Clin. Investig. 97:359365.
170. Somerville, J. E., Jr.,, L. Cassiano,, and R. P. Darveau. 1999. Escherichia coli msbB gene as a virulence factor and a therapeutic target. Infect. Immun. 67:65836590.
171. Soncini, F. C.,, E. Garcia Vescovi,, F. Solomon,, and E. A. Groisman. 1996. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J. Bacteriol. 178:50925099.
172. Sperandeo, P.,, R. Cescutti,, R. Villa,, C. Di Benedetto,, D. Candia,, G. Deho,, and A. Polissi. 2007. Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J. Bacteriol. 189:244253.
173. Sperandeo, P.,, C. Pozzi,, G. Deho,, 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.
174. Sperandeo, P.,, R. Villa,, A. M. Martorana,, M. Samalikova,, R. Grandori,, G. Deho,, and A. Polissi. 2011. New insights into the Lpt machinery for lipopolysaccharide transport to the cell surface: LptA-LptC interaction and LptA stability as sensors of a properly assembled transenvelope complex. J. Bacteriol. 193:10421053.
175. Spitznagel, J. K. 1990. Antibiotic proteins of human neutrophils. J. Clin. Investig. 86:13811386.
176. Stead, C. M.,, A. Beasley,, R. J. Cotter,, and M. S. Trent. 2008. Deciphering the unusual acylation pattern of Helicobacter pylori lipid A. J. Bacteriol. 190:70127021.
177. Stead, C. M.,, J. Zhao,, C. R. Raetz,, and M. S. Trent. 2010. Removal of the outer Kdo from Helicobacter pylori lipopolysaccharide and its impact on the bacterial surface. Mol. Microbiol. 78:837852.
178. Steeghs, L.,, H. deCock,, E. Evers,, B. Zomer,, J. Tommassen,, and P. van der Ley. 2001. Outer membranecomposition of a lipopolysaccharide-deficient Neisseria meningitidis mutant. EMBO J. 20:69376945.
179. Steeghs, L.,, M. P. Jennings,, J. T. Poolman,, and P. van der Ley. 1997. Isolation andcharacterization of the Neisseria meningitidis lpxD-fabZ-lpxA gene cluster involvedin lipid A biosynthesis. Gene 190:263270.
180. Stenutz, R.,, A. Weintraub,, and G. Widmalm. 2006. The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol. Rev. 30:382403.
181. Stevenson, G.,, A. Kessler,, and P. R. Reeves. 1995. A plasmid-borne O-antigen chain length determinant and its relationship to other chain length determinants. FEMS Microbiol. Lett. 125:2330.
182. Strohmaier, H.,, P. Remler,, W. Renner,, and G. Hogenauer. 1995. Expression of genes kdsA and kdsB involved in 3-deoxy-D-manno- octulosonic acid metabolism and biosynthesis of enterobacterial lipopolysaccharide is growth phase regulated primarily at the transcriptional level in Escherichia coli K-12. J. Bacteriol. 177:44884500.
183. Svetlov, V.,, G. A. Belogurov,, E. Shabrova,, D. G. Vassylyev,, and I. Artsimovitch. 2007. Allosteric control of the RNA polymerase by the elongation factor RfaH. Nucleic Acids Res. 35:56945705.
184. Swords, W. E.,, B. A. Buscher,, K. VerSteeg Ii,, A. Preston,, W. A. Nichols,, J. N. Weiser,, B. W. Gibson,, and M. A. Apicella. 2000. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 37:1327.
185. Swords, W. E.,, M. R. Ketterer,, J. Shao,, C. A. Campbell,, J. N. Weiser,, and M. A. Apicella. 2001. Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cell. Microbiol. 3:525536.
186. 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.
187. Tamayo, R.,, S. S. Ryan,, A. J. McCoy,, and J. S. Gunn. 2002. Identification and genetic characterization of PmrA-regulated genes and genes involved in polymyxin B resistance in Salmonella enterica serovar Typhimurium. Infect. Immun. 70:67706778.
188. Tang, K. H.,, H. Guo,, W. Yi,, M. D. Tsai,, and P. G. Wang. 2007. Investigation of the conformational states of Wzz and the Wzz.O-antigen complex under near-physiological conditions. Biochemistry 46:1174411752.
189. Tocilj, A.,, C. Munger,, A. Proteau,, R. Morona,, L. Purins,, E. Ajamian,, J. Wagner,, M. Papadopoulos,, L. Van Den Bosch,, J. L. Rubinstein,, J. Fethiere,, A. Matte,, and M. Cygler. 2008. Bacterial polysaccharide co-polymerases share a common framework for control of polymer length. Nat. Struct. Mol. Biol. 15:130138.
190. Touze, T.,, A. X. Tran,, J. V. Hankins,, D. Mengin-Lecreulx,, and M.S. Trent. 2008. Periplasmic phosphorylation of lipid A is linked to the synthesis of undecaprenyl phosphate. Mol. Microbiol. 67:264277.
191. Tran, A. X.,, J. D. Whittimore,, P. B. Wyrick,, S. C. McGrath,, R. J. Cotter,, and M. S. Trent. 2006. The lipid A 1-phosphatase of Helicobacter pylori is required for resistance to the antimicrobial peptide polymyxin. J. Bacteriol. 188:45314541.
192. 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.
193. Trent, M. S.,, A. A. Ribeiro,, S. Lin,, R. J. Cotter,, and C. R. Raetz. 2001b. 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.
194. Trent, M. S.,, C. M. Stead,, A. X. Tran,, and J. V. Hankins. 2006. Diversity of endotoxin and its impact on pathogenesis. J. Endotoxin Res. 12:205223.
195. Tzeng, Y. L.,, K. D. Ambrose,, S. Zughaier,, X. Zhou,, Y. K. Miller,, W. M. Shafer,, and D. S. Stephens. 2005. Cationic antimicrobial peptide resistance in Neisseria meningitidis. J. Bacteriol. 187:53875396.
196. Tzeng, Y. L.,, A. Datta,, V. K. Kolli,, R. W. Carlson,, and D. S. Stephens. 2002. Endotoxin of Neisseria meningitidis composed only of intact lipid A: inactivation of the meningococcal 3-deoxy-D-manno-octulosonic acid transferase. J. Bacteriol. 184:23792388.
197. Vaara, M.,, and M. Nurminen. 1999. Outer membrane permeability barrier in Escherichia coli mutants that are defective in the late acyltransferases of lipid A biosynthesis. Antimicrob. Agents Chemother. 43:14591462.
198. Valvano, M. A. 2008. Undecaprenyl phosphate recycling comes out of age. Mol. Microbiol. 67:232235.
199. Viau, C.,, V. Le Sage,, D. K. Ting,, J. Gross,, and H. Le Moual. 2011. Absence of PmrAB-mediated phosphoethanolamine modifications of Citrobacter rodentium lipopolysaccharide affects outer membrane integrity. J. Bacteriol. 193:21682176.
200. 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.
201. Vinogradov, E.,, M. B. Perry,, and J. W. Conlan. 2002. Structural analysis of Francisella tularensis lipopolysaccharide. Eur. J. Biochem. 269:61126118.
202. Vorachek-Warren, M. K.,, S. Ramirez,, R. J. Cotter,, and C. R. Raetz. 2002. A triple mutant of Escherichia coli lacking secondary acyl chains on lipid A. J. Biol. Chem. 277:1419414205.
203. Wang, L.,, S. Jensen,, R. Hallman,, and P. R. Reeves. 1998. Expression of the O antigen gene cluster is regulated by RfaH through the JUMPstart sequence. FEMS Microbiol. Lett. 165:201206.
204. 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.
205. Warren, M. J.,, and M. P. Jennings. 2003. Identification and characterization of pptA: a gene involved in the phase-variable expression of phosphorylcholine on pili of Neisseria meningitidis. Infect. Immun. 71:68926898.
206. Weiser, J. N.,, J. B. Goldberg,, N. Pan,, L. Wilson,, and M. Virji. 1998. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 66:42634267.
207. Weiser, J. N.,, A. A. Lindberg,, E. J. Manning,, E. J. Hansen,, and E. R. Moxon. 1989a. Identification of a chromosomal locus for expression of lipopolysaccharide epitopes in Haemophilus influenzae. Infect. Immun. 57:30453052.
208. Weiser, J. N.,, J. M. Love,, and E. R. Moxon. 1989b. The molecular mechanism of phase variation of H. influenzae lipopolysaccharide. Cell 59:657665.
209. Weiser, J. N.,, M. Shchepetov,, and S. T. Chong. 1997. Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect. Immun. 65:943950.
210. West, A. H.,, and A. M. Stock. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26:369376.
211. White, K. A.,, I. A. Kaltashov,, R. J. Cotter,, and C. R. Raetz. 1997. A mono-functional 3-deoxy-D-manno-octulosonic acid (Kdo) transferase and a Kdo kinase in extracts of Haemophilus influenzae. J. Biol. Chem. 272:1655516563.
212. Whitfield, C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75:3968.
213. Whitfield, C.,, P. A. Amor,, and R. Koplin. 1997. Modulation of the 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.
214. Wilkinson, S. G.,, and L. Galbrath. 1975. Studies of lipopolysaccharides from Pseudomonas aeruginosa. Eur. J. Biochem. 52:331343.
215. Woisetschlager, M.,, and G. Hogenauer. 1986. Cloning and characterization of the gene encoding 3-deoxy-D-manno-octulosonate 8-phosphate synthetase from Escherichia coli. J. Bacteriol. 168: 437439.
216. Wollin, R.,, E. S. Creeger,, L. I. Rothfield,, B. A. Stocker,, and A. A. Lindberg. 1983. Salmonella typhimurium mutants defective in UDP-D-galactose:lipopolysaccharide alpha 1,6-D-galactosyltransferase. Structural, immunochemical, and enzymologic studies of rfaB mutants. J. Biol. Chem. 258:37693774.
217. Wong, S. M.,, and B. J. Akerley. 2005. Environmental and genetic regulation of the phosphorylcholine epitope of Haemophilus influenzae lipooligosaccharide. Mol. Microbiol. 55:724738.
218. Woodward, R.,, W. Yi,, L. Li,, G. Zhao,, H. Eguchi,, P. R. Sridhar,, H. Guo,, J. K. Song,, E. Motari,, L. Cai,, P. Kelleher,, X. Liu,, W. Han,, W. Zhang,, Y. Ding,, M. Li,, and P. G. Wang. 2010. In vitro bacterial polysaccharide biosynthesis: defining the functions of Wzy and Wzz. Nat. Chem. Biol. 6:418423.
219. 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.
220. Wren, B. W. 2003. The Yersiniae—a model genus to study the rapid evolution of bacterial pathogens. Nat. Rev. Microbiol. 1:5564.
221. Yethon, J. A.,, D. E. Heinrichs,, M. A. Monteiro,, M. B. Perry,, and C. Whitfield. 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. 273:2631026316.
222. Zaslaver, A.,, A. Bren,, M. Ronen,, S. Itzkovitz,, I. Kikoin,, S. Shavit,, W. Liebermeister,, M. G. Surette,, and U. Alon. 2006. A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat. Methods 3:623628.
223. Zhang, J. R.,, I. Idanpaan-Heikkila,, W. Fischer,, and E. I. Tuomanen. 1999. Pneumococcal licD2 gene is involved in phosphorylcholine metabolism. Mol. Microbiol. 31:14771488.
224. Zhao, J.,, and C. R. Raetz. 2010. A two-component Kdo hydrolase in the inner membrane of Francisella novicida. Mol. Microbiol. 78:820836.
225. Zhou, Z.,, S. Lin,, R. J. Cotter,, and C. R. Raetz. 1999. Lipid A modificationscharacteristic of Salmonella typhimurium are induced by NH4VO3 in Escherichia coli K12. Detection of 4-amino-4-deoxy-L-arabinose, phosphoethanolamineand palmitate. J. Biol. Chem. 274:1850318514.