Pseudomonas aeruginosa LptE is crucial for LptD assembly, cell envelope integrity, antibiotic resistance and virulence

References

• Silhavy TJ, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol. 2010;2:a000414.
   PubMed Web of Science ®Google Scholar
• Vollmer W, Blanot D, de Pedro MA. Peptidoglycan structure and architecture. FEMS Microbiol Rev. 2008;32:149–167.
   PubMed Web of Science ®Google Scholar
• Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev. 2003;67:593–656.
   PubMed Web of Science ®Google Scholar
• Nikaido H. Restoring permeability barrier function to outer membrane. Chem Biol. 2005;12:507–509.
   PubMedGoogle Scholar
• Ruiz N, Wu T, Khane D, et al. Probing the barrier function of the outer membrane with chemical conditionality. ACS Chem Biol. 2006;1:385–395.
   PubMed Web of Science ®Google Scholar
• Sperandeo P, Martorana AM, Polissi A. The lipopolysaccharide transport (Lpt) machinery: a non-conventional transporter for lipopolysaccharide assembly at the outer membrane of Gram-negative bacteria. J Biol Chem. 2017;292:17981–17990.
   PubMed Web of Science ®Google Scholar
• Chng SS, Gronenberg LS, Kahne D. Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry. 2010;49:4565–4567.
   PubMed Web of Science ®Google Scholar
• Wu T, McCandlish AC, Gronenberg LS, et al. Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A. 2006;103:11754–11759.
   PubMed Web of Science ®Google Scholar
• Ruiz N, Gronenberg LS, Kahne D, et al. Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A. 2008;105:5537–5542.
   PubMed Web of Science ®Google Scholar
• Sperandeo P, Lau FK, Carpentieri A, et al. Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol. 2008;190:4460–4469.
   PubMed Web of Science ®Google Scholar
• Narita S, Tokuda H. Biochemical characterization of an ABC transporter LptBFGC complex required for the outer membrane sorting of lipopolysaccharides. FEBS Lett. 2009;583:2160–2164.
   PubMed Web of Science ®Google Scholar
• Sperandeo P, Cescutti R, Villa R, et al. Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J Bacteriol. 2007;189:244–253.
   PubMed Web of Science ®Google Scholar
• Freinkman E, Okuda S, Ruiz N, et al. Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry. 2012;51:4800–4806.
   PubMed Web of Science ®Google Scholar
• Sperandeo P, Villa R, Martorana AM, et al. 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. 2011;193:1042–1053.
   PubMed Web of Science ®Google Scholar
• Okuda S, Freinkman E, Kahne D. Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E.. Coli. Science.. 2012;338:1214–1217.
   Google Scholar
• Luo Q, Yang X, Yu S, et al. Structural basis for lipopolysaccharide extraction by ABC transporter LptB(2)FG. Nat Struct Mol Biol. 2017;24:469–474.
   PubMed Web of Science ®Google Scholar
• Freinkman E, Chng SS, Kahne D. The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc Natl Acad Sci U S A. 2011;108:2486–2491.
   PubMed Web of Science ®Google Scholar
• Qiao S, Luo Q, Zhao Y, et al. Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature. 2014;511:108–111.
   PubMed Web of Science ®Google Scholar
• Dong H, Xiang Q, Gu Y, et al. Structural basis for outer membrane lipopolysaccharide insertion. Nature. 2014;511:52–56.
   PubMed Web of Science ®Google Scholar
• Chng SS, Ruiz N, Chimalakonda G, et al. Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc Natl Acad Sci U S A. 2014;107:5363–5368.
   Web of Science ®Google Scholar
• Ruiz N, Chng SS, Hiniker A, et al. Nonconsecutive disulfide bond formation in an essential integral outer membrane protein. Proc Natl Acad Sci U S A. 2010;107:12245–12250.
   PubMed Web of Science ®Google Scholar
• Chimalakonda G, Ruiz N, Chng SS, et al. 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 U S A. 2011;108:2492–2497.
   PubMed Web of Science ®Google Scholar
• Chng SS, Xue M, Garner RA, et al. Disulfide rearrangement triggered by translocon assembly controls lipopolysaccharide export. Science. 2012;337:1665–1668.
   PubMed Web of Science ®Google Scholar
• Bos MP, Tommassen J. The LptD chaperone LptE is not directly involved in lipopolysaccharide transport in Neisseria meningitidis. J Biol Chem. 2011;286:28688–28696.
   PubMed Web of Science ®Google Scholar
• Malojčić G, Andres D, Grabowicz M, et al. LptE binds to and alters the physical state of LPS to catalyze its assembly at the cell surface. Proc Natl Acad Sci U S A. 2014;111:9467–9472.
   PubMed Web of Science ®Google Scholar
• Steeghs L, Den Hartog R, Den Boer A, et al. Meningitis bacterium is viable without endotoxin. Nature. 1998;392:449–450.
   PubMed Web of Science ®Google Scholar
• Steeghs L, de Cock H, Evers E, et al. Outer membrane composition of a lipopolysaccharide-deficient Neisseria meningitidis mutant. Embo J. 2001;20:6937–6945.
   PubMed Web of Science ®Google Scholar
• Bos MP, Tommassen J. Viability of a capsule- and lipopolysaccharide-deficient mutant of Neisseria meningitidis. Infect Immun. 2005;73:6194–6197.
   PubMed Web of Science ®Google Scholar
• Bos MP, Tefsen B, Geurtsen J, et al. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci U S A. 2004;101:9417–9422.
   PubMed Web of Science ®Google Scholar
• Tefsen B, Bos MP, Beckers F, et al. MsbA is not required for phospholipid transport in Neisseria meningitidis. J Biol Chem. 2005;280:35961–35966.
   PubMed Web of Science ®Google Scholar
• Poole K. Pseudomonas aeruginosa: resistance to the max. Front Microbiol. 2011;2:65.
   PubMed Web of Science ®Google Scholar
• Srinivas N, Jetter P, Ueberbacher BJ, et al. Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science. 2010;327:1010–1013.
   PubMed Web of Science ®Google Scholar
• Werneburg M, Zerbe K, Juhas M, et al. Inhibition of lipopolysaccharide transport to the outer membrane in Pseudomonas aeruginosa by peptidomimetic antibiotics. Chembiochem. 2012;13:1767–1775.
   PubMed Web of Science ®Google Scholar
• Bollati M, Villa R, Gourlay LJ, et al. Crystal structure of LptH, the periplasmic component of the lipopolysaccharide transport machinery from Pseudomonas aeruginosa. FEBS J. 2015;282:1980–1997.
   PubMed Web of Science ®Google Scholar
• Fernández-Piñar R, Lo Sciuto A, Rossi A, et al. In vitro and in vivo screening for novel essential cell-envelope proteins in Pseudomonas aeruginosa. Sci Rep. 2015;5:17593.
   PubMed Web of Science ®Google Scholar
• Mdluli KE, Witte PR, Kline T, et al. Molecular validation of LpxC as an antibacterial drug target in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2006;50:2178–2184.
   PubMed Web of Science ®Google Scholar
• Delucia AM, Six DA, Caughlan RE, et al. Lipopolysaccharide (LPS) inner-core phosphates are required for complete LPS synthesis and transport to the outer membrane in Pseudomonas aeruginosa PAO1. MBio. 2011;2:pii: e00142–11.
   PubMed Web of Science ®Google Scholar
• Jacobs MA, Alwood A, Thaipisuttikul I, et al. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2003;100:14339–14344.
   PubMed Web of Science ®Google Scholar
• Liberati NT, Urbach JM, Miyata S, et al. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A. 2006;103:2833–2838.
   PubMed Web of Science ®Google Scholar
• Lee SA, Gallagher LA, Thongdee M, et al. General and condition-specific essential functions of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2015;112:5189–5194.
   PubMed Web of Science ®Google Scholar
• Turner KH, Wessel AK, Palmer GC, et al. Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum. Proc Natl Acad Sci U S A. 2015;112:4110–4115.
   PubMed Web of Science ®Google Scholar
• Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: a Laboratory Manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1989.
   Google Scholar
• Heeb S, Blumer C, Haas D. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J Bacteriol. 2002;84:1046–1056.
   Web of Science ®Google Scholar
• Lo Sciuto A, Fernández-Piñar R, Bertuccini L, et al. The periplasmic protein TolB as a potential drug target in Pseudomonas aeruginosa. PLoS One. 2014;9:e103784.
   PubMed Web of Science ®Google Scholar
• Milton DL, O’Toole R, Horstedt P, et al. Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol. 1996;178:1310–1319.
   PubMed Web of Science ®Google Scholar
• Hoang TT, Kutchma AJ, Becher A, et al. Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid. 2000;43:59–72.
   PubMed Web of Science ®Google Scholar
• Volokhina EB, Beckers F, Tommassen J, et al. The beta-barrel outer membrane protein assembly complex of Neisseria meningitidis. J Bacteriol. 2009;191:7074–7085.
   PubMed Web of Science ®Google Scholar
• Liu YY, Chandler CE, Leung LM, et al. Structural modification of lipopolysaccharide conferred by mcr-1 in gram-negative ESKAPE pathogens. Antimicrob Agents Chemother. 2017;61:pii: e00580-17.
   Web of Science ®Google Scholar
• Hitchcock PJ, Brown TM. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol. 1983;154:269–277.
   PubMed Web of Science ®Google Scholar
• Lam JS, Anderson EM, Hao Y. LPS quantitation procedures. Methods Mol Biol. 2014;1149:375–402.
   PubMedGoogle Scholar
• Michel G, Bleves S, Ball G, et al. Mutual stabilization of the XcpZ and XcpY components of the secretory apparatus in Pseudomonas aeruginosa. Microbiology. 1998;144:3379–3386.
   PubMed Web of Science ®Google Scholar
• Basto AP, Piedade J, Ramalho R, et al. A new cloning system based on the OprI lipoprotein for the production of recombinant bacterial cell wall-derived immunogenic formulations. J Biotechnol. 2012;157:50–63.
   PubMed Web of Science ®Google Scholar
• Jander G, Rahme LG, Ausubel FM. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol. 2000;182:3843–3845.
   PubMed Web of Science ®Google Scholar
• Antunes LC, Imperi F, Carattoli A, et al. Deciphering the multifactorial nature of Acinetobacter baumannii pathogenicity. PLoS One. 2011;6:e22674.
   PubMed Web of Science ®Google Scholar
• Meisner J, Goldberg JB. The Escherichia coli rhaSR-PrhaBAD Inducible promoter system allows tightly controlled gene expression over a wide range in Pseudomonas aeruginosa. Appl Environ Microbiol. 2016;82:6715–6727.
   PubMed Web of Science ®Google Scholar
• Bishop RE. Structural biology of membrane-intrinsic beta-barrel enzymes: sentinels of the bacterial outer membrane. Biochim Biophys Acta. 2008;1778:1881–1896.
   PubMed Web of Science ®Google Scholar
• Knirel YA, Bystrova OV, Kocharova NA, et al. Conserved and variable structural features in the lipopolysaccharide of Pseudomonas aeruginosa. J Endotoxin Res. 2006;12:324–336.
   PubMedGoogle Scholar
• King JD, Kocíncová D, Westman EL, et al. Review: lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Innate Immun. 2009;15:261–312.
   PubMed Web of Science ®Google Scholar
• Pasqua M, Visaggio D, Lo Sciuto A, et al. The ferric uptake regulator Fur is conditionally essential in Pseudomonas aeruginosa. J Bacteriol. 2017;199:pii: e00472–17.
   PubMed Web of Science ®Google Scholar
• Putker F, Bos MP, Tommassen J. Transport of lipopolysaccharide to the Gram-negative bacterial cell surface. FEMS Microbiol Rev. 2015;39:985–1002.
   PubMed Web of Science ®Google Scholar
• May JM, Sherman DJ, Simpson BW, et al. Lipopolysaccharide transport to the cell surface: periplasmic transport and assembly into the outer membrane. Philos Trans R Soc Lond B Biol Sci. 2015;370:pii: 20150027.
   Web of Science ®Google Scholar
• Simpson BW, May JM, Sherman DJ, et al. Lipopolysaccharide transport to the cell surface: biosynthesis and extraction from the inner membrane. Philos Trans R Soc Lond B Biol Sci. 2015;370:pii: 20150029.
   Web of Science ®Google Scholar
• Okuda S, Sherman DJ, Silhavy TJ, et al. Lipopolysaccharide transport and assembly at the outer membrane: the PEZ model. Nat Rev Microbiol. 2016;14:337–345.
   PubMed Web of Science ®Google Scholar
• Botos I, Noinaj N, Buchanan SK. Insertion of proteins and lipopolysaccharide into the bacterial outer membrane. Philos Trans R Soc Lond B Biol Sci. 2017;372:pii: 20160224.
   PubMed Web of Science ®Google Scholar
• Moehle K, Kocherla H, Bacsa B, et al. Solution Structure and Dynamics of LptE from Pseudomonas aeruginosa. Biochemistry. 2016;55:2936–2943.
   PubMed Web of Science ®Google Scholar
• Grabowicz M, Yeh J, Silhavy TJ. Dominant negative lptE mutation that supports a role for LptE as a plug in the LptD barrel. J Bacteriol. 2013;195:1327–1334.
   PubMed Web of Science ®Google Scholar
• Balibar CJ, Grabowicz M. Mutant Alleles of lptD increase the permeability of Pseudomonas aeruginosa and define determinants of intrinsic resistance to antibiotics. Antimicrob Agents Chemother. 2015;60:845–854.
   PubMed Web of Science ®Google Scholar
• Botos I, Majdalani N, Mayclin SJ, et al. Structural and functional characterization of the LPS transporter LptDE from Gram-negative pathogens. Structure. 2016;24:965–976.
   PubMed Web of Science ®Google Scholar
• Gibbons HS, Reynolds CM, Guan Z, et al. An inner membrane dioxygenase that generates the 2-hydroxymyristate moiety of Salmonella lipid A. Biochemistry. 2008;47:2814–2825.
   PubMed Web of Science ®Google Scholar
• Hittle LE, Powell DA, Jones JW, et al. Site-specific activity of the acyltransferases HtrB1 and HtrB2 in Pseudomonas aeruginosa lipid A biosynthesis. Pathog Dis. 2015;73:ftv053.
   PubMed Web of Science ®Google Scholar