Abstract
In this chapter we will discuss how lipopolysaccharide (LPS) is transported and assembled from its site of synthesis (the cytoplasm and the inner membrane) to the cell surface. This is a remarkably complex process, as LPS must traverse three different cellular compartments to reach its final destination.
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Steeghs L, den Hartog R, den Boer A, Zomer B, Roholl P, van der Ley P (1998) Meningitis bacterium is viable without endotoxin. Nature 392:449–450
Gram HCJ (1884) Über die isolierte Färbung der Schizomyceten in Schnitt- und Trockenpräparaten. Fortschr Med 2:185–189
Beveridge TJ, Davies JA (1983) Cellular responses of Bacillus subtilis and Escherichia coli to the Gram stain. J Bacteriol 156:846–858
Glauert AM, Thornley MJ (1969) The topography of the bacterial cell wall. Annu Rev Microbiol 23:159–198
Kellenberger E, Ryter A (1958) Cell wall and cytoplasmic membrane of Escherichia coli. J Biophys Biochem Cytol 4:323–326
Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700
Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656
Narita S, Matsuyama S, Tokuda H (2004) Lipoprotein trafficking in Escherichia coli. Arch Microbiol 182:1–6
Tokuda H (2009) Biogenesis of outer membranes in Gram-negative bacteria. Biosci Biotechnol Biochem 73:465–473
Kadner RJ (1996) Cytoplasmic membrane. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC, pp 58–87
Oliver DB (1996) Periplasm. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC, pp 88–103
Holtje JV (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203
Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253
Schulz GE (2002) The structure of bacterial outer membrane proteins. Biochim Biophys Acta 1565:308–317
Dong C, Beis K, Nesper J, Brunkan-Lamontagne AL, Clarke BR, Whitfield C, Naismith JH (2006) Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444:226–229
Collins RF, Beis K, Dong C, Botting CH, McDonnell C, Ford RC, Clarke BR, Whitfield C, Naismith JH (2007) The 3D structure of a periplasm-spanning platform required for assembly of group 1 capsular polysaccharides in Escherichia coli. Proc Natl Acad Sci USA 104:2390–2395
Pettersson A, Poolman JT, van der Ley P, Tommassen J (1997) Response of Neisseria meningitidis to iron limitation. Antonie Leeuwenhoek 71:129–136
Kamio Y, Nikaido H (1976) Outer membrane of Salmonella typhimurium: accessibility of phospholipid head groups to phospholipase c and cyanogen bromide activated dextran in the external medium. Biochemistry 15:2561–2570
Gunn JS (2000) Mechanisms of bacterial resistance and response to bile. Microbes Infect 2:907–913
Ferguson AD, Welte W, Hofmann E, Lindner B, Holst O, Coulton JW, Diederichs K (2000) A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure 8:585–592
Ruiz N, Kahne D, Silhavy TJ (2006) Advances in understanding bacterial outer-membrane biogenesis. Nat Rev Microbiol 4:57–66
Young K, Silver LL (1991) Leakage of periplasmic enzymes from envA1 strains of Escherichia coli. J Bacteriol 173:3609–3614
Nikaido H (2005) Restoring permeability barrier function to outer membrane. Chem Biol 12:507–509
Jia W, El Zoeiby A, Petruzziello TN, Jayabalasingham B, Seyedirashti S, Bishop RE (2004) Lipid trafficking controls endotoxin acylation in outer membranes of Escherichia coli. J Biol Chem 279:44966–44975
Dekker N (2000) Outer-membrane phospholipase A: known structure, unknown biological function. Mol Microbiol 35:711–717
Groisman EA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183:1835–1842
Bishop RE (2008) Structural biology of membrane-intrinsic β-barrel enzymes: sentinels of the bacterial outer membrane. Biochim Biophys Acta 1778:1881–1896
Malinverni JC, Silhavy TJ (2009) An ABC transport system that maintains lipid asymmetry in the Gram-negative outer membrane. Proc Natl Acad Sci USA 106:8009–8014
Casali N, Riley LW (2007) A phylogenomic analysis of the Actinomycetales mce operons. BMC Genomics 8:60–83
Alba BM, Gross CA (2004) Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol Microbiol 52:613–619
Ades SE (2008) Regulation by destruction: design of the σE envelope stress response. Curr Opin Microbiol 11:535–540
Ades SE, Connolly LE, Alba BM, Gross CA (1999) The Escherichia coli σE-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-σ factor. Genes Dev 13:2449–2461
Alba BM, Leeds JA, Onufryk C, Lu CZ, Gross CA (2002) DegS and YaeL participate sequentially in the cleavage of RseA to activate the σE-dependent extracytoplasmic stress response. Genes Dev 16:2156–2168
Inaba K, Suzuki M, Maegawa K, Akiyama S, Ito K, Akiyama Y (2008) A pair of circularly permutated PDZ domains control RseP, the S2P family intramembrane protease of Escherichia coli. J Biol Chem 283:35042–35052
Dartigalongue C, Missiakas D, Raina S (2001) Characterization of the Escherichia coli σE regulon. J Biol Chem 276:20866–20875
Johansen J, Eriksen M, Kallipolitis B, Valentin-Hansen P (2008) Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and σE-dependent CyaR-ompX regulatory case. J Mol Biol 383:1–9
Sperandeo P, Cescutti R, Villa R, Di Benedetto C, Candia D, Dehò G, Polissi A (2007) Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J Bacteriol 189:244–253
Braun M, Silhavy TJ (2002) Imp/OstA is required for cell envelope biogenesis in Escherichia coli. Mol Microbiol 45:1289–1302
Tam C, Missiakas D (2005) Changes in lipopolysaccharide structure induce the σE-dependent response of Escherichia coli. Mol Microbiol 55:1403–1412
Kol MA, de Kroon AI, Killian JA, de Kruijff B (2004) Transbilayer movement of phospholipids in biogenic membranes. Biochemistry 43:2673–2681
Bos MP, Robert V, Tommassen J (2007) Biogenesis of the Gram-negative bacterial outer membrane. Annu Rev Microbiol 61:191–214
Cronan JE (2003) Bacterial membrane lipids: where do we stand? Annu Rev Microbiol 57:203–224
Rothman JE, Kennedy EP (1977) Rapid transmembrane movement of newly synthesized phospholipids during membrane assembly. Proc Natl Acad Sci USA 74:1821–1825
Kol MA, van Dalen A, de Kroon AI, de Kruijff B (2003) Translocation of phospholipids is facilitated by a subset of membrane-spanning proteins of the bacterial cytoplasmic membrane. J Biol Chem 278:24586–24593
Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CR (1998) Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem 273:12466–12475
Doerrler WT, Gibbons HS, Raetz CR (2004) MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J Biol Chem 279:45102–45109
Tefsen B, Bos MP, Beckers F, Tommassen J, de Cock H (2005) MsbA is not required for phospholipid transport in Neisseria meningitidis. J Biol Chem 280:35961–35966
Driessen AJ, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643–667
Raetz CR (1990) Biochemistry of endotoxins. Annu Rev Biochem 59:129–170
Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, Kahne D (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235–245
Sampson BA, Misra R, Benson SA (1989) Identification and characterization of a new gene of Escherichia coli K-12 involved in outer membrane permeability. Genetics 122:491–501
Aono R, Negishi T, Aibe K, Inoue A, Horikoshi K (1994) Mapping of organic solvent tolerance gene ostA in Escherichia coli K-12. Biosci Biotechnol Biochem 58:1231–1235
Doerrler WT (2006) Lipid trafficking to the outer membrane of Gram-negative bacteria. Mol Microbiol 60:542–552
Bos MP, Tefsen B, Geurtsen J, Tommassen J (2004) Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci USA 101:9417–9422
Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, Kahne D (2006) Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103:11754–11759
Sperandeo P, Lau FK, Carpentieri A, De Castro C, Molinaro A, Dehò G, Silhavy TJ, Polissi A (2008) Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190:4460–4469
Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ (2008) Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 105:5537–5542
Chng SS, Ruiz N, Chimalakonda G, Silhavy TJ, Kahne D (2010) Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc Natl Acad Sci USA 107:5363–5368
Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364
Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10:218–227
Karow M, Georgopoulos C (1993) The essential Escherichia coli msbA gene, a multicopy suppressor of null mutations in the htrB gene, is related to the universally conserved family of ATP-dependent translocators. Mol Microbiol 7:69–79
Clementz T, Bednarski JJ, Raetz CR (1996) Function of the htrB high temperature requirement gene of Escherchia coli in the acylation of lipid A: HtrB catalyzed incorporation of laurate. J Biol Chem 271:12095–12102
Karow M, Fayet O, Georgopoulos C (1992) The lethal phenotype caused by null mutations in the Escherichia coli htrB gene is suppressed by mutations in the accBC operon, encoding two subunits of acetyl coenzyme A carboxylase. J Bacteriol 174:7407–7418
Polissi A, Georgopoulos C (1996) Mutational analysis and properties of the msbA gene of Escherichia coli, coding for an essential ABC family transporter. Mol Microbiol 20:1221–1233
Doerrler WT, Reedy MC, Raetz CR (2001) An Escherichia coli mutant defective in lipid export. J Biol Chem 276:11461–11464
Raetz CR, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in Gram-negative bacteria. Annu Rev Biochem 76:295–329
Doerrler WT, Raetz CR (2002) ATPase activity of the MsbA lipid flippase of Escherichia coli. J Biol Chem 277:36697–36705
Eckford PD, Sharom FJ (2008) Functional characterization of Escherichia coli MsbA: interaction with nucleotides and substrates. J Biol Chem 283:12840–12850
Siarheyeva A, Sharom FJ (2009) The ABC transporter MsbA interacts with lipid A and amphipathic drugs at different sites. Biochem J 419:317–328
Eckford PD, Sharom FJ (2010) The reconstituted Escherichia coli MsbA protein displays lipid flippase activity. Biochem J 429:195–203
Ward A, Reyes CL, Yu J, Roth CB, Chang G (2007) Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc Natl Acad Sci USA 104:19005–19010
Chang G, Roth CB, Reyes CL, Pornillos O, Chen YJ, Chen AP (2006) Retraction. Science 314:1875
Dawson RJ, Locher KP (2006) Structure of a bacterial multidrug ABC transporter. Nature 443:180–185
Rosenberg MF, Callaghan R, Modok S, Higgins CF, Ford RC (2005) Three-dimensional structure of P-glycoprotein: the transmembrane regions adopt an asymmetric configuration in the nucleotide-bound state. J Biol Chem 280:2857–2862
Narita S, Tokuda H (2009) Biochemical characterization of an ABC transporter LptBFGC complex required for the outer membrane sorting of lipopolysaccharides. FEBS Lett 583:2160–2164
Chng SS, Gronenberg LS, Kahne D (2010) Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49:4565–4567
Stenberg F, Chovanec P, Maslen SL, Robinson CV, Ilag LL, von Heijne G, Daley DO (2005) Protein complexes of the Escherichia coli cell envelope. J Biol Chem 280:34409–34419
Tran AX, Trent MS, Whitfield C (2008) The LptA protein of Escherichia coli is a periplasmic lipid A-binding protein involved in the lipopolysaccharide export pathway. J Biol Chem 283:20342–20349
Serina S, Nozza F, Nicastro G, Faggioni F, Mottl H, Dehò G, Polissi A (2004) Scanning the Escherichia coli chromosome by random transposon mutagenesis and multiple phenotypic screening. Res Microbiol 155:692–701
Meredith TC, Woodard RW (2003) Escherichia coli YrbH is a d-arabinose 5-phosphate isomerase. J Biol Chem 278:32771–32777
Wu J, Woodard RW (2003) Escherichia coli YrbI is 3-deoxy-d-manno-octulosonate 8-phosphate phosphatase. J Biol Chem 278:18117–18123
Sperandeo P, Pozzi C, Dehò G, Polissi A (2006) Non-essential KDO biosynthesis and new essential cell envelope biogenesis genes in the Escherichia coli yrbG-yhbG locus. Res Microbiol 157:547–558
Ma B, Reynolds CM, Raetz CR (2008) Periplasmic orientation of nascent lipid A in the inner membrane of an Escherichia coli LptA mutant. Proc Natl Acad Sci USA 105:13823–13828
Linton KJ, Higgins CF (2007) Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch 453:555–567
Gil R, Silva FJ, Zientz E, Delmotte F, Gonzalez-Candelas F, Latorre A, Rausell C, Kamerbeek J, Gadau J, Holldobler B, van Ham RC, Gross R, Moya A (2003) The genome sequence of Blochmannia floridanus: comparative analysis of reduced genomes. Proc Natl Acad Sci USA 100:9388–9393
Tefsen B, Geurtsen J, Beckers F, Tommassen J, de Cock H (2005) Lipopolysaccharide transport to the bacterial outer membrane in spheroplasts. J Biol Chem 280:4504–4509
Matsuyama S, Tajima T, Tokuda H (1995) A novel periplasmic carrier protein involved in the sorting and transport of Escherichia coli lipoproteins destined for the outer membrane. EMBO J 14:3365–3372
Bayer ME (1968) Areas of adhesion between wall and membrane of Escherichia coli. J Gen Microbiol 53:395–404
Bayer ME (1991) Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. J Struct Biol 107:268–280
Muhlradt PF, Menzel J, Golecki JR, Speth V (1973) Outer membrane of Salmonella. Sites of export of newly synthesised lipopolysaccharide on the bacterial surface. Eur J Biochem 35:471–481
Ishidate K, Creeger ES, Zrike J, Deb S, Glauner B, MacAlister TJ, Rothfield LI (1986) Isolation of differentiated membrane domains from Escherichia coli and Salmonella typhimurium, including a fraction containing attachment sites between the inner and outer membranes and the murein skeleton of the cell envelope. J Biol Chem 261:428–443
Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62:379–433
Nikaido H, Zgurskaya HI (2001) AcrAB and related multidrug efflux pumps of Escherichia coli. J Mol Microbiol Biotechnol 3:215–218
Suits MD, Sperandeo P, Dehò G, Polissi A, Jia Z (2008) Novel structure of the conserved Gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J Mol Biol 380:476–488
Tran AX, Dong C, Whitfield C (2010) Structure and functional analysis of LptC, a conserved membrane protein involved in the lipopolysaccharide export pathway in Escherichia coli. J Biol Chem 285:33529–33539
Rossi P, Xiao R, Acton TB, Montelione GT (2007) Solution NMR structure of uncharacterized lipoprotein B from Nitrosomonas europaea. PDB ID: 2JXP doi:10.2210/pdb2jxp/pdb
Vorobiev SM, Abashidze M, Seetharaman J, Cunningham K, Maglaqui M, Owens L, Fang Y, Xiao R, Acton TB, Montelione GT, Tong L, Hunt JF (2007) Crystal structure of the A1KSW9_NEIMF protein from Neisseria meningitidis. PDB ID: 3BF2 doi:10.2210/pdb3bf2/pdb
Meredith TC, Aggarwal P, Mamat U, Lindner B, Woodard RW (2006) Redefining the requisite lipopolysaccharide structure in Escherichia coli. ACS Chem Biol 1:33–42
Mamat U, Meredith TC, Aggarwal P, Kuhl A, Kirchhoff P, Lindner B, Hanuszkiewicz A, Sun J, Holst O, Woodard RW (2008) Single amino acid substitutions in either YhjD or MsbA confer viability to 3-deoxy-d-manno-oct-2-ulosonic acid-depleted Escherichia coli. Mol Microbiol 67:633–648
Klein G, Lindner B, Brabetz W, Brade H, Raina S (2009) Escherichia coli K-12 suppressor-free mutants lacking early glycosyltransferases and late acyltransferases: minimal lipopolysaccharide structure and induction of envelope stress response. J Biol Chem 284:15369–15389
Fischbach MA, Walsh CT (2009) Antibiotics for emerging pathogens. Science 325:1089–1093
Falagas ME, Bliziotis IA, Kasiakou SK, Samonis G, Athanassopoulou P, Michalopoulos A (2005) Outcome of infections due to pandrug-resistant (PDR) Gram-negative bacteria. BMC Infect Dis 5:24
Walsh C (2003) Where will new antibiotics come from? Nat Rev Microbiol 1:65–70
Patel U, Yan YP, Hobbs FW Jr, Kaczmarczyk J, Slee AM, Pompliano DL, Kurilla MG, Bobkova EV (2001) Oxazolidinones mechanism of action: inhibition of the first peptide bond formation. J Biol Chem 276:37199–37205
Yan K, Madden L, Choudhry AE, Voigt CS, Copeland RA, Gontarek RR (2006) Biochemical characterization of the interactions of the novel pleuromutilin derivative retapamulin with bacterial ribosomes. Antimicrob Agents Chemother 50:3875–3881
Jung D, Rozek A, Okon M, Hancock RE (2004) Structural transitions as determinants of the action of the calcium-dependent antibiotic daptomycin. Chem Biol 11:949–957
Saenz HL, Dehio C (2005) Signature-tagged mutagenesis: technical advances in a negative selection method for virulence gene identification. Curr Opin Microbiol 8:612–619
Arigoni F, Talabot F, Peitsch M, Edgerton MD, Meldrum E, Allet E, Fish R, Jamotte T, Curchod ML, Loferer H (1998) A genome-based approach for the identification of essential bacterial genes. Nat Biotechnol 16:851–856
Akerley BJ, Rubin EJ, Camilli A, Lampe DJ, Robertson HM, Mekalanos JJ (1998) Systematic identification of essential genes by in vitro mariner mutagenesis. Proc Natl Acad Sci USA 95:8927–8932
Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL (2007) Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat Rev Drug Discov 6:29–40
Weber A, Casini A, Heine A, Kuhn D, Supuran CT, Scozzafava A, Klebe G (2004) Unexpected nanomolar inhibition of carbonic anhydrase by COX-2-selective celecoxib: new pharmacological opportunities due to related binding site recognition. J Med Chem 47:550–557
Kinnings SL, Liu N, Buchmeier N, Tonge PJ, Xie L, Bourne PE (2009) Drug discovery using chemical systems biology: repositioning the safe medicine Comtan to treat multi-drug and extensively drug resistant tuberculosis. PLoS Comput Biol 5:e1000423
Gronenberg LS, Kahne D (2010) Development of an activity assay for discovery of inhibitors of lipopolysaccharide transport. J Am Chem Soc 132:2518–2519
Srinivas N, Jetter P, Ueberbacher BJ, Werneburg M, Zerbe K, Steinmann J, Van der MB, Bernardini F, Lederer A, Dias RL, Misson PE, Henze H, Zumbrunn J, Gombert FO, Obrecht D, Hunziker P, Schauer S, Ziegler U, Kach A, Eberl L, Riedel K, DeMarco SJ, Robinson JA (2010) Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science 327:1010–1013
Kokryakov VN, Harwig SS, Panyutich EA, Shevchenko AA, Aleshina GM, Shamova OV, Korneva HA, Lehrer RI (1993) Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins. FEBS Lett 327:231–236
Takase I, Ishino F, Wachi M, Kamata H, Doi N, Asoh S, Matsuzawa H, Ohta T, Matsuhashi M (1987) Genes encoding two lipoproteins in the leuS-dacA region of the Escherichia coli chromosome. J Bacteriol 169:5692–5699
Acknowledgements
This work was in part supported by Regione Lombardia “Cooperazione scientifica e tecnologica internazionale” grant 16876 SAL-18 (to A.P) and “Fondazione per la Ricerca sulla Fibrosi Cistica” grant FFC#13/2010 (to A.P.).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer-Verlag/Wien
About this chapter
Cite this chapter
Sperandeo, P., Dehò, G., Polissi, A. (2011). Lipopolysaccharide Export to the Outer Membrane. In: Knirel, Y., Valvano, M. (eds) Bacterial Lipopolysaccharides. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0733-1_10
Download citation
DOI: https://doi.org/10.1007/978-3-7091-0733-1_10
Published:
Publisher Name: Springer, Vienna
Print ISBN: 978-3-7091-0732-4
Online ISBN: 978-3-7091-0733-1
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)