Abstract
Gram-negative bacteria express on their outer membrane lipopolysaccharide (LPS) that typically comprises of three structural components: lipid A, core oligosaccharide and the O-polysaccharide (OPS). The biosynthesis, on the other hand, takes place at the cytoplasmic face of the inner membrane via two separate pathways for lipid A-core oligosaccharide and OPS that converge physically in the periplasmic face of the inner membrane. There, the undecaprenyl-diphosphate-carried OPS is joined by a carbon-oxygen ligase onto lipid A core and the resulting completed LPS molecule is shuffled onto outer membrane by the recently delineated Lpt translocation pathway.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Raetz CR, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700
Frirdich E, Whitfield C (2005) Lipopolysaccharide inner core oligosaccharide structure and outer membrane stability in human pathogens belonging to the Enterobacteriaceae. J Endotoxin Res 11:133–144
Aspinall GO, Monteiro MA, Shaver RT, Kurjanczyk LA, Penner JL (1997) Lipopolysaccharides of Helicobacter pylori serogroups O:3 and O:6. Structures of a class of lipopolysaccharides with reference to the location of oligomeric units of d-glycero-α-d-manno-heptose residues. Eur J Biochem 248:592–601
Monteiro MA, Appelmelk BJ, Rasko DA, Moran AP, Hynes SO, MacLean LL, Chan KH, Michael FS, Logan SM, O’Rourke J, Lee A, Taylor DE, Perry MB (2000) Lipopolysaccharide structures of Helicobacter pylori genomic strains 26695 and J99, mouse model H. pylori Sydney strain, H. pylori P466 carrying sialyl Lewis X, and H. pylori UA915 expressing Lewis B classification of H. pylori lipopolysaccharides into glycotype families. Eur J Biochem 267:305–320
Stead C, Tran A, Ferguson D Jr, McGrath S, Cotter R, Trent S (2005) A novel 3-deoxy-d-manno-octulosonic acid (Kdo) hydrolase that removes the outer Kdo sugar of Helicobacter pylori lipopolysaccharide. J Bacteriol 187:3374–3383
Niedziela T, Jachymek W, Lukasiewicz J, Maciejewska A, Andersson R, Kenne L, Lugowski C (2010) Structures of two novel, serologically nonrelated core oligosaccharides of Yokenella regensburgei lipopolysaccharides differing only by a single hexose substitution. Glycobiology 20:207–214
Tsai CM, Jankowska-Stephens E, Mizanur RM, Cipollo JF (2009) The fine structure of Neisseria meningitidis lipooligosaccharide from the M986 strain and three of its variants. J Biol Chem 284:4616–4625
Mansson M, Hood DW, Moxon ER, Schweda EK (2003) Structural diversity in lipopolysaccharide expression in nontypeable Haemophilus influenzae. Identification of L-glycerol-d-manno-heptose in the outer-core region in three clinical isolates. Eur J Biochem 270:610–624
Masoud H, Moxon ER, Martin A, Krajcarski D, Richards JC (1997) Structure of the variable and conserved lipopolysaccharide oligosaccharide epitopes expressed by Haemophilus influenzae serotype b strain Eagan. Biochemistry 36:2091–2103
Li J, Bauer SH, Mansson M, Moxon ER, Richards JC, Schweda EK (2001) Glycine is a common substituent of the inner core in Haemophilus influenzae lipopolysaccharide. Glycobiology 11:1009–1015
Schweda EK, Richards JC, Hood DW, Moxon ER (2007) Expression and structural diversity of the lipopolysaccharide of Haemophilus influenzae: implication in virulence. Int J Med Microbiol 297:297–306
Pier GB (2007) Pseudomonas aeruginosa lipopolysaccharide: a major virulence factor, initiator of inflammation and target for effective immunity. Int J Med Microbiol 297:277–295
King JD, Kocincova D, Westman EL, Lam JS (2009) Lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Innate Immun 15:261–312
Bystrova OV, Shashkov AS, Kocharova NA, Knirel YA, Lindner B, Zähringer U, Pier GB (2002) Structural studies on the core and the O-polysaccharide repeating unit of Pseudomonas aeruginosa immunotype 1 lipopolysaccharide. Eur J Biochem 269:2194–2203
Sadovskaya I, Brisson JR, Thibault P, Richards JC, Lam JS, Altman E (2000) Structural characterization of the outer core and the O-chain linkage region of lipopolysaccharide from Pseudomonas aeruginosa serotype O5. Eur J Biochem 267:1640–1650
De CC, Molinaro A, Lanzetta R, Silipo A, Parrilli M (2008) Lipopolysaccharide structures from Agrobacterium and Rhizobiaceae species. Carbohydr Res 343:1924–1933
Caroff M, Aussel L, Zarrouk H, Martin A, Richards JC, Therisod H, Perry MB, Karibian D (2001) Structural variability and originality of the Bordetella endotoxins. J Endotoxin Res 7:63–68
Moll H, Knirel YA, Helbig JH, Zähringer U (1997) Identification of an α-d-Manp-(1 → 8)-Kdo disaccharide in the inner core region and the structure of the complete core region of the Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr Res 304:91–95
Vinogradov EV, Müller-Loennies S, Petersen BO, Meshkov S, Thomas-Oates JE, Holst O, Brade H (1997) Structural investigation of the lipopolysaccharide from Acinetobacter haemolyticus strain NCTC 10305 (ATCC 17906, DNA group 4). Eur J Biochem 247:82–90
Vinogradov EV, Bock K, Petersen BO, Holst O, Brade H (1997) The structure of the carbohydrate backbone of the lipopolysaccharide from Acinetobacter strain ATCC 17905. Eur J Biochem 243:122–127
Gronow S, Noah C, Blumenthal A, Lindner B, Brade H (2003) Construction of a deep-rough mutant of Burkholderia cepacia ATCC 25416 and characterization of its chemical and biological properties. J Biol Chem 278:1647–1655
Isshiki Y, Kawahara K, Zähringer U (1998) Isolation and characterisation of disodium (4-amino-4-deoxy-α-l-arabinopyranosyl)-(1 → 8)-(d-glycero-α-d-talo-oct-2-ulopyranosylonate)-(2 → 4)-(methyl 3-deoxy-d-manno-oct-2-ulopyranosid)onate from the lipopolysaccharide of Burkholderia cepacia. Carbohydr Res 313:21–27
Ortega X, Silipo A, Saldias MS, Bates CC, Molinaro A, Valvano MA (2009) Biosynthesis and structure of the Burkholderia cenocepacia K56-2 lipopolysaccharide core oligosaccharide: truncation of the core oligosaccharide leads to increased binding and sensitivity to polymyxin B. J Biol Chem 284:21738–21751
Vinogradov EV, Lindner B, Kocharova NA, Senchenkova SN, Shashkov AS, Knirel YA, Holst O, Gremyakova TA, Shaikhutdinova RZ, Anisimov AP (2002) The core structure of the lipopolysaccharide from the causative agent of plague, Yersinia pestis. Carbohydr Res 337:775–777
Vinogradov E, Lindner B, Seltmann G, Radziejewska-Lebrecht J, Holst O (2006) Lipopolysaccharides from Serratia marcescens possess one or two 4-amino-4-deoxy-l-arabinopyranose 1-phosphate residues in the lipid A and d-glycero-d-talo-oct-2-ulopyranosonic acid in the inner core region. Chem Eur J 12:6692–6700
Sonesson A, Jantzen E, Bryn K, Tangen T, Eng J, Zähringer U (1994) Composition of 2,3-dihydroxy fatty acid-containing lipopolysaccharides from Legionella israelensis, Legionella maceachernii and Legionella micdadei. Microbiology 140:1261–1271
Phillips NJ, Apicella MA, Griffiss JM, Gibson BW (1992) Structural characterization of the cell surface lipooligosaccharides from a nontypable strain of Haemophilus influenzae. Biochemistry 31:4515–4526
Phillips NJ, Apicella MA, Griffiss JM, Gibson BW (1993) Structural studies of the lipooligosaccharides from Haemophilus influenzae type b strain A2. Biochemistry 32:2003–2012
Lebbar S, Caroff M, Szabo L, Merienne C, Szilogyi L (1994) Structure of a hexasaccharide proximal to the hydrophobic region of lipopolysaccharides present in Bordetella pertussis endotoxin preparations. Carbohydr Res 259:257–275
Holst O (1999) Chemical structure of the core region of lipopolysaccharides. In: Brade H, Opal SM, Vogel SN, Morrison DC (eds) Endotoxin in health and disease. Marcel Dekker, New York, pp 115–154
Edebrink P, Jansson P-E, Bogwald J, Hoffman J (1996) Structural studies of the Vibrio salmonicida lipopolysaccharide. Carbohydr Res 287:225–245
Kondo S, Zähringer U, Seydel U, Sinnwell V, Hisatsune K, Rietschel ET (1991) Chemical structure of the carbohydrate backbone of Vibrio parahaemolyticus serotype O12 lipopolysaccharide. Eur J Biochem 200:689–698
Vinogradov EV, Bock K, Holst O, Brade H (1995) The structure of the lipid A-core region of the lipopolysaccharides from Vibrio cholerae O1 smooth strain 569B (Inaba) and rough mutant strain 95R (Ogawa). Eur J Biochem 233:152–158
Brade H, Brabetz W, Brade L, Holst O, Löbau S, Lucakova M, Mamat U, Rozalski A, Zych K, Kosma P (1997) Chlamydial lipopolysaccharide. J Endotoxin Res 4:67–84
Heine H, Müller-Loennies S, Brade L, Lindner B, Brade H (2003) Endotoxic activity and chemical structure of lipopolysaccharides from Chlamydia trachomatis serotypes E and L2 and Chlamydophila psittaci 6BC. Eur J Biochem 270:440–450
Rund S, Lindner B, Brade H, Holst O (1999) Structural analysis of the lipopolysaccharide from Chlamydia trachomatis serotype L2. J Biol Chem 274:16819–16824
Rund S, Lindner B, Brade H, Holst O (2000) Structural analysis of the lipopolysaccharide from Chlamydophila psittaci strain 6BC. Eur J Biochem 267:5717–5726
Hanuszkiewicz A, Hubner G, Vinogradov E, Lindner B, Brade L, Brade H, Debarry J, Heine H, Holst O (2008) Structural and immunochemical analysis of the lipopolysaccharide from Acinetobacter lwoffii F78 located outside Chlamydiaceae with a Chlamydia-specific lipopolysaccharide epitope. Chem Eur J 14:10251–10258
Meredith TC, Woodard RW (2003) Escherichia coli YrbH is a d-arabinose 5-phosphate isomerase. J Biol Chem 278:32771–32777
Sommaruga S, Gioia LD, Tortora P, Polissi A (2009) Structure prediction and functional analysis of KdsD, an enzyme involved in lipopolysaccharide biosynthesis. Biochem Biophys Res Commun 388:222–227
Tan L, Darby C (2006) Yersinia pestis YrbH is a multifunctional protein required for both 3-deoxy-d-manno-oct-2-ulosonic acid biosynthesis and biofilm formation. Mol Microbiol 61:861–870
Tzeng YL, Datta A, Strole C, Kolli VS, Birck MR, Taylor WP, Carlson RW, Woodard RW, Stephens DS (2002) KpsF is the arabinose-5-phosphate isomerase required for 3-deoxy-d-manno-octulosonic acid biosynthesis and for both lipooligosaccharide assembly and capsular polysaccharide expression in Neisseria meningitidis. J Biol Chem 277:24103–24113
Meredith TC, Woodard RW (2005) Identification of GutQ from Escherichia coli as a d-arabinose 5-phosphate isomerase. J Bacteriol 187:6936–6942
Cieslewicz M, Vimr E (1997) Reduced polysialic acid capsule expression in Escherichia coli K1 mutants with chromosomal defects in kpsF. Mol Microbiol 26:237–249
Meredith TC, Woodard RW (2006) Characterization of Escherichia coli d-arabinose 5-phosphate isomerase encoded by kpsF: implications for group 2 capsule biosynthesis. Biochem J 395:427–432
Bateman A (1999) The SIS domain: a phosphosugar-binding domain. Trends Biochem Sci 24:94–95
Bateman A (1997) The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem Sci 22:12–13
Dotson GD, Nanjappan P, Reily MD, Woodard RW (1993) Stereochemistry of 3-deoxyoctulosonate 8-phosphate synthase. Biochemistry 32:12392–12397
Dotson GD, Dua RK, Clemens JC, Wooten EW, Woodard RW (1995) Overproduction and one-step purification of Escherichia coli 3-deoxy-d-manno-octulosonic acid 8-phosphate synthase and oxygen transfer studies during catalysis using isotopic-shifted heteronuclear NMR. J Biol Chem 270:13698–13705
Radaev S, Dastidar P, Patel M, Woodard RW, Gatti DL (2000) Structure and mechanism of 3-deoxy-d-manno-octulosonate 8-phosphate synthase. J Biol Chem 275:9476–9484
Radaev S, Dastidar P, Patel M, Woodard RW, Gatti DL (2000) Preliminary X-ray analysis of a new crystal form of the Escherichia coli KDO8P synthase. Acta Crystallogr D Biol Crystallogr 56:516–519
Birck MR, Woodard RW (2001) Aquifex aeolicus 3-deoxy-d-manno-2-octulosonic acid 8-phosphate synthase: a new class of KDO 8-P synthase? J Mol Evol 52:205–214
Duewel HS, Woodard RW (2000) A metal bridge between two enzyme families. 3-Deoxy-d-manno-octulosonate-8-phosphate synthase from Aquifex aeolicus requires a divalent metal for activity. J Biol Chem 275:22824–22831
Vainer R, Belakhov V, Rabkin E, Baasov T, Adir N (2005) Crystal structures of Escherichia coli KDO8P synthase complexes reveal the source of catalytic irreversibility. J Mol Biol 351:641–652
Wagner T, Kretsinger RH, Bauerle R, Tolbert WD (2000) 3-Deoxy-d-manno-octulosonate-8-phosphate synthase from Escherichia coli. Model of binding of phosphoenolpyruvate and d-arabinose-5-phosphate. J Mol Biol 301:233–238
Cochrane FC, Cookson TV, Jameson GB, Parker EJ (2009) Reversing evolution: re-establishing obligate metal ion dependence in a metal-independent KDO8P synthase. J Mol Biol 390:646–661
Duewel HS, Radaev S, Wang J, Woodard RW, Gatti DL (2001) Substrate and metal complexes of 3-deoxy-d-manno-octulosonate-8-phosphate synthase from Aquifex aeolicus at 1.9-Å resolution. Implications for the condensation mechanism. J Biol Chem 276:8393–8402
Kona F, Tao P, Martin P, Xu X, Gatti DL (2009) Electronic structure of the metal center in the Cd2+, Zn2+, and Cu2+ substituted forms of KDO8P synthase: implications for catalysis. Biochemistry 48:3610–3630
Li J, Wu J, Fleischhacker AS, Woodard RW (2004) Conversion of Aquifex aeolicus 3-deoxy-d-manno-octulosonate 8-phosphate synthase, a metalloenzyme, into a nonmetalloenzyme. J Am Chem Soc 126:7448–7449
Shulami S, Yaniv O, Rabkin E, Shoham Y, Baasov T (2003) Cloning, expression, and biochemical characterization of 3-deoxy-d-manno-2-octulosonate-8-phosphate (KDO8P) synthase from the hyperthermophilic bacterium Aquifex pyrophilus. Extremophiles 7:471–481
Krosky DJ, Alm R, Berg M, Carmel G, Tummino PJ, Xu B, Yang W (2002) Helicobacter pylori 3-deoxy-d-manno-octulosonate-8-phosphate (KDO-8-P) synthase is a zinc-metalloenzyme. Biochim Biophys Acta 1594:297–306
Sau AK, Li Z, Anderson KS (2004) Probing the role of metal ions in the catalysis of Helicobacter pylori 3-deoxy-d-manno-octulosonate-8-phosphate synthase using a transient kinetic analysis. J Biol Chem 279:15787–15794
Allison TM, Yeoman JA, Hutton RD, Cochrane FC, Jameson GB, Parker EJ (2010) Specificity and mutational analysis of the metal-dependent 3-deoxy-d-manno-octulosonate 8-phosphate synthase from Acidithiobacillus ferrooxidans. Biochim Biophys Acta 1804:1526–1536
Kona F, Xu X, Martin P, Kuzmic P, Gatti DL (2007) Structural and mechanistic changes along an engineered path from metallo to nonmetallo 3-deoxy-d-manno-octulosonate 8-phosphate synthases. Biochemistry 46:4532–4544
Oliynyk Z, Briseno-Roa L, Janowitz T, Sondergeld P, Fersht AR (2004) Designing a metal-binding site in the scaffold of Escherichia coli KDO8PS. Protein Eng Des Sel 17:383–390
Shulami S, Furdui C, Adir N, Shoham Y, Anderson KS, Baasov T (2004) A reciprocal single mutation affects the metal requirement of 3-deoxy-d-manno-2-octulosonate-8-phosphate (KDO8P) synthases from Aquifex pyrophilus and Escherichia coli. J Biol Chem 279:45110–45120
Ray PH, Benedict CD (1982) 3-Deoxy-d-manno-octulosonate-8-phosphate (KDO-8-P) phosphatase. Method Enzymol 83:530–535
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, Deho 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
Chng SS, Gronenberg LS, Kahne D (2010) Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49:4565–4567
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
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
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
Sperandeo P, Cescutti R, Villa R, Di Benedetto C, Candia D, Deho 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
Sperandeo P, Lau FK, Carpentieri A, De Castro C, Molinaro A, Deho 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
Suits MD, Sperandeo P, Deho 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, 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
Biswas T, Yi L, Aggarwal P, Wu J, Rubin JR, Stuckey JA, Woodard RW, Tsodikov OV (2009) The tail of KdsC: conformational changes control the activity of a haloacid dehalogenase superfamily phosphatase. J Biol Chem 284:30594–30603
Parsons JF, Lim K, Tempczyk A, Krajewski W, Eisenstein E, Herzberg O (2002) From structure to function: YrbI from Haemophilus influenzae (HI1679) is a phosphatase. Proteins 46:393–404
Allen KN, Dunaway-Mariano D (2004) Phosphoryl group transfer: evolution of a catalytic scaffold. Trends Biochem Sci 29:495–503
Burroughs AM, Allen KN, Dunaway-Mariano D, Aravind L (2006) Evolutionary genomics of the HAD superfamily: understanding the structural adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes. J Mol Biol 361:1003–1034
Lu Z, Wang L, Dunaway-Mariano D, Allen KN (2009) Structure-function analysis of 2-keto-3-deoxy-d-glycero-d-galacto-nononate-9-phosphate phosphatase defines specificity elements in type C0 haloalkanoate dehalogenase family members. J Biol Chem 284:1224–1233
Lin CH, Murray BW, Ollmann IR, Wong CH (1997) Why is CMP-ketodeoxyoctonate highly unstable? Biochemistry 36:780–785
Ray PH, Benedict CD (1982) CTP:CMP-3-deoxy-d-manno-octulosonate cytidylyltransferase (CMP-KDO synthetase). Method Enzymol 83:535–540
Brade H, Zähringer U, Rietschel ET, Christian R, Schulz G, Unger FM (1984) Spectroscopic analysis of a 3-deoxy-d-manno-2-octulosonic acid (Kdo)-disaccharide from the lipopolysaccharide of a Salmonella godesberg Re mutant. Carbohydr Res 134:157–166
Kohlbrenner WE, Fesik SW (1985) Determination of the anomeric specificity of the Escherichia coli CTP:CMP-3-deoxy-d-manno-octulosonate cytidylyltransferase by 13C NMR spectroscopy. J Biol Chem 260:14695–14700
Finke A, Roberts I, Boulnois G, Pzzani C, Jann K (1989) Activity of CMP-2-keto-3-deoxyoctulosonic acid synthetase in Escherichia coli strains expressing the capsular K5 polysaccharide implication for K5 polysaccharide biosynthesis. J Bacteriol 171:3074–3079
Rosenow C, Roberts IS, Jann K (1995) Isolation from recombinant Escherichia coli and characterization of CMP-Kdo synthetase, involved in the expression of the capsular K5 polysaccharide (K-CKS). FEMS Microbiol Lett 125:159–164
Jann B, Jann K (1990) Structure and biosynthesis of the capsular antigens of Escherichia coli. Curr Top Microbiol Immunol 150:19–42
Finke A, Jann B, Jann K (1990) CMP-KDO-synthetase activity in Escherichia coli expressing capsular polysaccharides. FEMS Microbiol Lett 57:129–133
Strohmaier H, Remler P, Renner W, Hogenauer G (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 177:4488–4500
Jelakovic S, Jann K, Schulz GE (1996) The three-dimensional structure of capsule-specific CMP: 2-keto-3-deoxy-manno-octonic acid synthetase from Escherichia coli. FEBS Lett 391:157–161
Jelakovic S, Schulz GE (2001) The structure of CMP:2-keto-3-deoxy-manno-octonic acid synthetase and of its complexes with substrates and substrate analogs. J Mol Biol 312:143–155
Jelakovic S, Schulz GE (2002) Catalytic mechanism of CMP:2-keto-3-deoxy-manno-octonic acid synthetase as derived from complexes with reaction educt and product. Biochemistry 41:1174–1181
Heyes DJ, Levy C, Lafite P, Roberts IS, Goldrick M, Stachulski AV, Rossington SB, Stanford D, Rigby SE, Scrutton NS, Leys D (2009) Structure-based mechanism of CMP-2-keto-3-deoxy-manno-octulonic acid synthetase: convergent evolution of a sugar-activating enzyme with DNA/RNA polymerases. J Biol Chem 284:35514–35523
Yoon HJ, Ku MJ, Mikami B, Suh SW (2008) Structure of 3-deoxy-manno-octulosonate cytidylyltransferase from Haemophilus influenzae complexed with the substrate 3-deoxy-manno-octulosonate in the β-configuration. Acta Crystallogr D Biol Crystallogr 64:1292–1294
Nudler E (2009) RNA polymerase active center: the molecular engine of transcription. Annu Rev Biochem 78:335–361
Rothwell PJ, Waksman G (2005) Structure and mechanism of DNA polymerases. Adv Protein Chem 71:401–440
Holst O (2002) Chemical structure of the core region of lipopolysaccharides – an update. Trends Glycosci Glyc 14:87–103
Carlson RW, Reuhs B, Chen TB, Bhat UR, Noel KD (1995) Lipopolysaccharide core structures in Rhizobium etli and mutants deficient in O-antigen. J Biol Chem 270:11783–11788
Kannenberg EL, Reuhs B, Forsberg LS, Carlson RW (1998) Lipopolysaccharides and K-antigens: their structures, biosynthesis, and functions in Rhizobium-legume interactions. In: Spaink HH, Kondrosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Kluwer, Amsterdam, pp 119–154
Knirel YA, Moll H, Zähringer U (1996) Structural study of a highly O-acetylated core of Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr Res 293:223–234
Edebrink P, Jansson P-E, Widmalm G, Holme T, Rahman M (1996) The structures of oligosaccharides isolated from the lipopolysaccharide of Moraxella catarrhalis serotype B, strain CCUG 3292. Carbohydr Res 295:127–146
Vinogradov EV, Petersen BO, Thomas-Oates JE, Duus J, Brade H, Holst O (1998) Characterization of a novel branched tetrasaccharide of 3-deoxy-d-manno-oct-2-ulopyranosonic acid. The structure of the carbohydrate backbone of the lipopolysaccharide from Acinetobacter baumannii strain NCTC 10303 (ATCC 17904). J Biol Chem 273:28122–28131
Brooke JS, Valvano MA (1996) Molecular cloning of the Haemophilus influenzae gmhA (lpcA) gene encoding a phosphoheptose isomerase required for lipooligosaccharide biosynthesis. J Bacteriol 178:3339–3341
Brooke JS, Valvano MA (1996) Biosynthesis of inner core lipopolysaccharide in enteric bacteria identification and characterization of a conserved phosphoheptose isomerase. J Biol Chem 271:3608–3614
Eidels L, Osborn MJ (1974) Phosphoheptose isomerase, first enzyme in the biosynthesis of aldoheptose in Salmonella typhimurium. J Biol Chem 249:5642–5648
Taylor PL, Blakely KM, de Leon GP, Walker JR, McArthur F, Evdokimova E, Zhang K, Valvano MA, Wright GD, Junop MS (2008) Structure and function of sedoheptulose-7-phosphate isomerase, a critical enzyme for lipopolysaccharide biosynthesis and a target for antibiotic adjuvants. J Biol Chem 283:2835–2845
Seetharaman J, Rajashankar KR, Solorzano V, Kniewel R, Lima CD, Bonanno JB, Burley SK, Swaminathan S (2006) Crystal structures of two putative phosphoheptose isomerases. Proteins 63:1092–1096
Kneidinger B, Graninger M, Puchberger M, Kosma P, Messner P (2001) Biosynthesis of nucleotide-activated d-glycero-d-manno-heptose. J Biol Chem 276:20935–20944
McArthur F, Andersson CE, Loutet S, Mowbray SL, Valvano MA (2005) Functional analysis of the glycero-manno-heptose 7-phosphate kinase domain from the bifunctional HldE protein, which is involved in ADP-l-glycero-d-manno-heptose biosynthesis. J Bacteriol 187:5292–5300
Valvano MA, Marolda CL, Bittner M, Glaskin-Clay M, Simon TL, Klena JD (2000) The rfaE gene from Escherichia coli encodes a bifunctional protein involved in biosynthesis of the lipopolysaccharide core precursor ADP-l-glycero-d-manno-heptose. J Bacteriol 182:488–497
Loutet SA, Flannagan RS, Kooi C, Sokol PA, Valvano MA (2006) A complete lipopolysaccharide inner core oligosaccharide is required for resistance of Burkholderia cenocepacia to antimicrobial peptides and bacterial survival in vivo. J Bacteriol 188:2073–2080
Valvano MA, Messner P, Kosma P (2002) Novel pathways for biosynthesis of nucleotide-activated glycero-manno-heptose precursors of bacterial glycoproteins and cell surface polysaccharides. Microbiology 148:1979–1989
Kneidinger B, Marolda C, Graninger M, Zamyatina A, McArthur F, Kosma P, Valvano MA, Messner P (2002) Biosynthesis pathway of ADP-l-glycero-β-d-manno-heptose in Escherichia coli. J Bacteriol 184:363–369
Nguyen HH, Wang L, Huang H, Peisach E, Dunaway-Mariano D, Allen KN (2010) Structural determinants of substrate recognition in the HAD superfamily member d-glycero-d-manno-heptose-1,7-bisphosphate phosphatase (GmhB). Biochemistry 49:1082–1092
Taylor PL, Sugiman-Marangos S, Zhang K, Valvano MA, Wright GD, Junop MS (2010) Structural and kinetic characterization of the LPS biosynthetic enzyme d-α, β-d-heptose-1,7-bisphosphate phosphatase (GmhB) from Escherichia coli. Biochemistry 49:1033–1041
Wang L, Huang H, Nguyen HH, Allen KN, Mariano PS, Dunaway-Mariano D (2010) Divergence of biochemical function in the HAD superfamily: d-glycero-d-manno-heptose-1,7-bisphosphate phosphatase (GmhB). Biochemistry 49:1072–1081
Morrison JP, Read JA, Coleman WG Jr, Tanner ME (2005) Dismutase activity of ADP-l-glycero-d-manno-heptose 6-epimerase: evidence for a direct oxidation/reduction mechanism. Biochemistry 44:5907–5915
Morrison JP, Tanner ME (2007) A two-base mechanism for Escherichia coli ADP-l-glycero-d-manno-heptose 6-epimerase. Biochemistry 46:3916–3924
Lee NG, Sunshine MG, Apicella MA (1995) Molecular cloning and characterization of the nontypeable Haemophilus influenzae 2019 rfaE gene required for lipopolysaccharide biosynthesis. Infect Immun 63:818–824
Nichols WA, Gibson BW, Melaugh W, Lee NG, Sunshine M, Apicella MA (1997) Identification of the ADP-l-glycero-d-manno-heptose-6-epimerase (rfaD) and heptosyltransferase II (rfaF) biosynthesis genes from nontypeable Haemophilus influenzae 2019. Infect Immun 65:1377–1386
Drazek ES, Stein DC, Deal CD (1995) A mutation in the Neisseria gonorrhoeae rfaD homolog results in altered lipooligosaccharide expression. J Bacteriol 177:2321–2327
Levin JC, Stein DC (1996) Cloning, complementation, and characterization of an rfaE homolog from Neisseria gonorrhoeae. J Bacteriol 178:4571–4575
Provost M, Harel J, Labrie J, Sirois M, Jacques M (2003) Identification, cloning and characterization of rfaE of Actinobacillus pleuropneumoniae serotype 1, a gene involved in lipopolysaccharide inner-core biosynthesis. FEMS Microbiol Lett 223:7–14
Jin UH, Chung TW, Lee YC, Ha SD, Kim CH (2001) Molecular cloning and functional expression of the rfaE gene required for lipopolysaccharide biosynthesis in Salmonella typhimurium. Glycoconj J 18:779–787
Sirisena DM, MacLachlan PR, Liu SL, Hessel A, Sanderson KE (1994) Molecular analysis of the rfaD gene, for heptose synthesis, and the rfaF gene, for heptose transfer, in lipopolysaccharide synthesis in Salmonella typhimurium. J Bacteriol 176:2379–2385
Stroeher UH, Karageorgos LE, Morona R, Manning PA (1995) In Vibrio cholerae serogroup O1, rfaD is closely linked to the rfb operon. Gene 155:67–72
Andrä J, de Cock H, Garidel P, Howe J, Brandenburg K (2005) Investigation into the interaction of the phosphoporin PhoE with outer membrane lipids: physicochemical characterization and biological activity. Med Chem 1:537–546
de Cock H, Brandenburg K, Wiese A, Holst O, Seydel U (1999) Non-lamellar structure and negative charges of lipopolysaccharides required for efficient folding of outer membrane protein PhoE of Escherichia coli. J Biol Chem 274:5114–5119
Hagge SO, de Cock H, Gutsmann T, Beckers F, Seydel U, Wiese A (2002) Pore formation and function of phosphoporin PhoE of Escherichia coli are determined by the core sugar moiety of lipopolysaccharide. J Biol Chem 277:34247–34253
Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656
Qu J, Behrens-Kneip S, Holst O, Kleinschmidt JH (2009) Binding regions of outer membrane protein A in complexes with the periplasmic chaperone Skp. A site-directed fluorescence study. Biochemistry 48:4926–4936
Brabetz W, Müller-Loennies S, Brade H (2000) 3-Deoxy-d-manno-oct-2-ulosonic acid (Kdo) transferase (WaaA) and Kdo kinase (KdkA) of Haemophilus influenzae are both required to complement a waaA knockout mutation of Escherichia coli. J Biol Chem 275:34954–34962
Hankins JV, Trent MS (2009) Secondary acylation of Vibrio cholerae lipopolysaccharide requires phosphorylation of Kdo. J Biol Chem 284:25804–25812
Harper M, Boyce JD, Cox AD, St Michael F, Wilkie IW, Blackall PJ, Adler B (2007) Pasteurella multocida expresses two lipopolysaccharide glycoforms simultaneously, but only a single form is required for virulence: identification of two acceptor-specific heptosyl I transferases. Infect Immun 75:3885–3893
Harper M, Cox AD, St Michael F, Ford M, Wilkie IW, Adler B, Boyce JD (2010) Natural selection in the chicken host identifies Kdo kinase residues essential for phosphorylation of Pasteurella multocida LPS. Infect Immun 78:3669–3677
White KA, Kaltashov IA, Cotter RJ, Raetz CR (1997) A mono-functional 3-deoxy-d-manno-octulosonic acid (Kdo) transferase and a Kdo kinase in extracts of Haemophilus influenzae. J Biol Chem 272:16555–16563
White KA, Lin S, Cotter RJ, Raetz CR (1999) A Haemophilus influenzae gene that encodes a membrane bound 3-deoxy-d-manno-octulosonic acid (Kdo) kinase. Possible involvement of Kdo phosphorylation in bacterial virulence. J Biol Chem 274:31391–31400
Krupa A, Srinivasan N (2002) Lipopolysaccharide phosphorylating enzymes encoded in the genomes of gram-negative bacteria are related to the eukaryotic protein kinases. Protein Sci 11:1580–1584
Yethon JA, Heinrichs D, Monteiro MA, Perry MB, Whitfield C (1998) Involvement of waaY, waaQ, and waaP in the modification of Escherichia coli lipopolysaccharide and their role in the formation of a stable outer membrane. J Biol Chem 273:26310–26316
Yethon JA, Gunn JS, Ernst RK, Miller SI, Laroche L, Malo D, Whitfield C (2000) Salmonella enterica serovar typhimurium waaP mutants show increased susceptibility to polymyxin and loss of virulence in vivo. Infect Immun 68:4485–4491
Yethon JA, Whitfield C (2001) Purification and characterization of WaaP from Escherichia coli, a lipopolysaccharide kinase essential for outer membrane stability. J Biol Chem 276:5498–5504
Kooistra O, Bedoux G, Brecker L, Lindner B, Sanchez CP, Haras D, Zähringer U (2003) Structure of a highly phosphorylated lipopolysaccharide core in the ΔalgC mutants derived from Pseudomonas aeruginosa wild-type strains PAO1 (serogroup O5) and PAC1R (serogroup O3). Carbohydr Res 338:2667–2677
Walsh AG, Matewish MJ, Burrows LL, Monteiro MA, Perry MB, Lam JS (2000) Lipopolysaccharide core phosphates are required for viability and intrinsic drug resistance in Pseudomonas aeruginosa. Mol Microbiol 35:718–727
Zhao X, Lam JS (2002) WaaP of Pseudomonas aeruginosa is a novel eukaryotic type protein-tyrosine kinase as well as a sugar kinase essential for the biosynthesis of core lipopolysaccharide. J Biol Chem 277:4722–4730
Cox AD, Wright JC, Li J, Hood DW, Moxon ER, Richards JC (2003) Phosphorylation of the lipid A region of meningococcal lipopolysaccharide: identification of a family of transferases that add phosphoethanolamine to lipopolysaccharide. J Bacteriol 185:3270–3277
Mackinnon FG, Cox AD, Plested JS, Tang CM, Makepeace K, Coull PA, Wright JC, Chalmers R, Hood DW, Richards JC, Moxon ER (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 43:931–943
O’Connor ET, Piekarowicz A, Swanson KV, Griffiss JM, Stein DC (2006) Biochemical analysis of Lpt3, a protein responsible for phosphoethanolamine addition to lipooligosaccharide of pathogenic Neisseria. J Bacteriol 188:1039–1048
Wright JC, Hood DW, Randle GA, Makepeace K, Cox AD, Li J, Chalmers R, Richards JC, Moxon ER (2004) lpt6, a gene required for addition of phosphoethanolamine to inner-core lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae. J Bacteriol 186:6970–6982
Brabetz W, Müller-Loennies S, Holst O, Brade H (1997) Deletion of the heptosyltransferase genes rfaC and rfaF in Escherichia coli K-12 results in an Re-type lipopolysaccharide with a high degree of 2-aminoethanol phosphate substitution. Eur J Biochem 247:716–724
Reynolds CM, Kalb SR, Cotter RJ, Raetz CR (2005) A phosphoethanolamine transferase specific for the outer 3-deoxy-d-manno-octulosonic acid residue of Escherichia coli lipopolysaccharide. Identification of the eptB gene and Ca2+ hypersensitivity of an eptB deletion mutant. J Biol Chem 280:21202–21211
Forsberg LS, Carlson RW (1998) The structures of the lipopolysaccharides from Rhizobium etli strains CE358 and CE359. The complete structure of the core region of R. etli lipopolysaccharides. J Biol Chem 273:2747–2757
Niedziela T, Lukasiewicz J, Jachymek W, Dzieciatkowska M, Lugowski C, Kenne L (2002) Core oligosaccharides of Plesiomonas shigelloides O54:H2 (strain CNCTC 113/92): structural and serological analysis of the lipopolysaccharide core region, the O-antigen biological repeating unit, and the linkage between them. J Biol Chem 277:11653–11663
Severn WB, Kelly RF, Richards JC, Whitfield C (1996) Structure of the core oligosaccharide in the serotype O8 lipopolysaccharide from Klebsiella pneumoniae. J Bacteriol 178:1731–1741
Süsskind M, Brade L, Brade H, Holst O (1998) Identification of a novel heptoglycan of α1 → 2-linked d-glycero-d-manno-heptopyranose. Chemical and antigenic structure of lipopolysaccharides from Klebsiella pneumoniae ssp. pneumoniae rough strain R20 (O1−:K20−). J Biol Chem 273:7006–7017
Vinogradov E, Perry MB (2001) Structural analysis of the core region of the lipopolysaccharides from eight serotypes of Klebsiella pneumoniae. Carbohydr Res 335:291–296
Frirdich E, Bouwman C, Vinogradov E, Whitfield C (2005) The role of galacturonic acid in outer membrane stability in Klebsiella pneumoniae. J Biol Chem 280:27604–27612
Regue M, Hita B, Pique N, Izquierdo L, Merino S, Fresno S, Benedi VJ, Tomas JM (2004) A gene, uge, is essential for Klebsiella pneumoniae virulence. Infect Immun 72:54–61
Fresno S, Jimenez N, Canals R, Merino S, Corsaro MM, Lanzetta R, Parrilli M, Pieretti G, Regue M, Tomas JM (2007) A second galacturonic acid transferase is required for core lipopolysaccharide biosynthesis and complete capsule association with the cell surface in Klebsiella pneumoniae. J Bacteriol 189:1128–1137
Izquierdo L, Coderch N, Pique N, Bedini E, Corsaro MM, Merino S, Fresno S, Tomas JM, Regue M (2003) The Klebsiella pneumoniae wabG gene: role in biosynthesis of the core lipopolysaccharide and virulence. J Bacteriol 185:7213–7221
Kanjilal-Kolar S, Raetz CR (2006) Dodecaprenyl phosphate-galacturonic acid as a donor substrate for lipopolysaccharide core glycosylation in Rhizobium leguminosarum. J Biol Chem 281:12879–12887
Kanjilal-Kolar S, Basu SS, Kanipes MI, Guan Z, Garrett TA, Raetz CR (2006) Expression cloning of three Rhizobium leguminosarum lipopolysaccharide core galacturonosyltransferases. J Biol Chem 281:12865–12878
Belunis CJ, Raetz CR (1992) Biosynthesis of endotoxins. Purification and catalytic properties of 3-deoxy-d-manno-octulosonic acid transferase from Escherichia coli. J Biol Chem 267:9988–9997
Raetz CR, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76:295–329
Bode CE, Brabetz W, Brade H (1998) Cloning and characterization of 3-deoxy-d-manno-oct-2-ulosonic acid (Kdo) transferase genes (kdtA) from Acinetobacter baumannii and Acinetobacter haemolyticus. Eur J Biochem 254:404–412
Brabetz W, Schirmer CE, Brade H (2000) 3-Deoxy-d-manno-oct-2-ulosonic acid (Kdo) transferase of Legionella pneumophila transfers two Kdo residues to a structurally different lipid A precursor of Escherichia coli. J Bacteriol 182:4654–4657
Mamat U, Schmidt H, Munoz E, Lindner B, Fukase K, Hanuszkiewicz A, Wu J, Meredith TC, Woodard RW, Hilgenfeld R, Mesters JR, Holst O (2009) WaaA of the hyperthermophilic bacterium Aquifex aeolicus is a monofunctional 3-deoxy-d-manno-oct-2-ulosonic acid transferase involved in lipopolysaccharide biosynthesis. J Biol Chem 284:22248–22262
Noah C, Brabetz W, Gronow S, Brade H (2001) Cloning, sequencing, and functional analysis of three glycosyltransferases involved in the biosynthesis of the inner core region of Klebsiella pneumoniae lipopolysaccharide. J Endotoxin Res 7:25–33
Belunis CJ, Mdluli KE, Raetz CR, Nano FE (1992) A novel 3-deoxy-d-manno-octulosonic acid transferase from Chlamydia trachomatis required for expression of the genus-specific epitope. J Biol Chem 267:18702–18707
Brabetz W, Lindner B, Brade H (2000) Comparative analyses of secondary gene products of 3-deoxy-d-manno-oct-2-ulosonic acid transferases from Chlamydiaceae in Escherichia coli K-12. Eur J Biochem 267:5458–5465
Löbau S, Mamat U, Brabetz W, Brade H (1995) Molecular cloning, sequence analysis, and functional characterization of the lipopolysaccharide biosynthetic gene kdtA encoding 3-deoxy-α-d-manno-octulosonic acid transferase of Chlamydia pneumoniae strain TW-183. Mol Microbiol 18:391–399
Mamat U, Löbau S, Persson K, Brade H (1994) Nucleotide sequence variations within the lipopolysaccharide biosynthesis gene gseA (Kdo transferase) among the Chlamydia trachomatis serovars. Microb Pathog 17:87–97
Nano FE, Caldwell HD (1985) Expression of the chlamydial genus-specific lipopolysaccharide epitope in Escherichia coli. Science 228:742–744
Isobe T, White KA, Allen AG, Peacock M, Raetz CR, Maskell DJ (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 181:2648–2651
Moran AP, Knirel YA, Senchenkova SN, Widmalm G, Hynes SO, Jansson P-E (2002) Phenotypic variation in molecular mimicry between Helicobacter pylori lipopolysaccharides and human gastric epithelial cell surface glycoforms. Acid-induced phase variation in Lewisx and Lewisy expression by H. pylori lipopolysaccharides. J Biol Chem 277:5785–5795
Vinogradov E, Perry MB, Conlan JW (2002) Structural analysis of Francisella tularensis lipopolysaccharide. Eur J Biochem 269:6112–6118
Zhao J, Raetz CR (2010) A two-component Kdo hydrolase in the inner membrane of Francisella novicida. Mol Microbiol 78:820–836
Stead CM, Zhao J, Raetz CR, Trent MS (2010) Removal of the outer Kdo from Helicobacter pylori lipopolysaccharide and its impact on the bacterial surface. Mol Microbiol 78:837–852
Chung HS, Raetz CR (2010) Interchangeable domains in the Kdo transferases of Escherichia coli and Haemophilus influenzae. Biochemistry 49:4126–4137
Chen L, Coleman WG Jr (1993) Cloning and characterization of the Escherichia coli K-12 rfa-2 (rfaC) gene, a gene required for lipopolysaccharide inner core synthesis. J Bacteriol 175:2534–2540
Gronow S, Brabetz W, Brade H (2000) Comparative functional characterization in vitro of heptosyltransferase I (WaaC) and II (WaaF) from Escherichia coli. Eur J Biochem 267:6602–6611
Kadrmas JL, Raetz CR (1998) Enzymatic synthesis of lipopolysaccharide in Escherichia coli. Purification and properties of heptosyltransferase I. J Biol Chem 273:2799–2807
Schnaitman CA, Klena JD (1993) Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 57:655–682
Sirisena DM, Brozek KA, MacLachlan PR, Sanderson KE, Raetz CR (1992) The rfaC gene of Salmonella typhimurium. Cloning, sequencing, and enzymatic function in heptose transfer to lipopolysaccharide. J Biol Chem 267:18874–18884
de Kievit TR, Lam JS (1997) Isolation and characterization of two genes, waaC (rfaC) and waaF (rfaF), involved in Pseudomonas aeruginosa serotype O5 inner-core biosynthesis. J Bacteriol 179:3451–3457
Petricoin EF III, Danaher RJ, Stein DC (1991) Analysis of the lsi region involved in lipooligosaccharide biosynthesis in Neisseria gonorrhoeae. J Bacteriol 173:7896–7902
Schwan ET, Robertson BD, Brade H, van Putten JP (1995) Gonococcal rfaF mutants express Rd2 chemotype LPS and do not enter epithelial host cells. Mol Microbiol 15:267–275
Zhou D, Lee NG, Apicella MA (1994) Lipooligosaccharide biosynthesis in Neisseria gonorrhoeae: cloning, identification and characterization of the α1,5 heptosyltransferase I gene (rfaC). Mol Microbiol 14:609–618
Jennings MP, Bisercic M, Dunn KL, Virji M, Martin A, Wilks KE, Richards JC, Moxon ER (1995) Cloning and molecular analysis of the Isi1 (rfaF) gene of Neisseria meningitidis which encodes a heptosyl-2-transferase involved in LPS biosynthesis: evaluation of surface exposed carbohydrates in LPS mediated toxicity for human endothelial cells. Microb Pathog 19:391–407
Stojiljkovic I, Hwa V, Larson J, Lin L, So M, Nassif X (1997) Cloning and characterization of the Neisseria meningitidis rfaC gene encoding α-1,5 heptosyltransferase I. FEMS Microbiol Lett 151:41–49
Allen AG, Isobe T, Maskell DJ (1998) Identification and cloning of waaF (rfaF) from Bordetella pertussis and use to generate mutants of Bordetella spp. with deep rough lipopolysaccharide. J Bacteriol 180:35–40
Jimenez N, Canals R, Lacasta A, Kondakova AN, Lindner B, Knirel YA, Merino S, Regue M, Tomas JM (2008) Molecular analysis of three Aeromonas hydrophila AH-3 (serotype O34) lipopolysaccharide core biosynthesis gene clusters. J Bacteriol 190:3176–3184
Jimenez N, Lacasta A, Vilches S, Reyes M, Vazquez J, Aquillini E, Merino S, Regue M, Tomas JM (2009) Genetics and proteomics of Aeromonas salmonicida lipopolysaccharide core biosynthesis. J Bacteriol 191:2228–2236
Kanipes MI, Papp-Szabo E, Guerry P, Monteiro MA (2006) Mutation of waaC, encoding heptosyltransferase I in Campylobacter jejuni 81–176, affects the structure of both lipooligosaccharide and capsular carbohydrate. J Bacteriol 188:3273–3279
Klena JD, Gray SA, Konkel ME (1998) Cloning, sequencing, and characterization of the lipopolysaccharide biosynthetic enzyme heptosyltransferase I gene (waaC) from Campylobacter jejuni and Campylobacter coli. Gene 222:177–185
Coderch N, Pique N, Lindner B, Abitiu N, Merino S, Izquierdo L, Jimenez N, Tomas JM, Holst O, Regue M (2004) Genetic and structural characterization of the core region of the lipopolysaccharide from Serratia marcescens N28b (serovar O4). J Bacteriol 186:978–988
Hood DW, Deadman ME, Allen T, Masoud H, Martin A, Brisson JR, Fleischmann R, Venter JC, Richards JC, Moxon ER (1996) Use of the complete genome sequence information of Haemophilus influenzae strain Rd to investigate lipopolysaccharide biosynthesis. Mol Microbiol 22:951–965
Gronow S, Oertelt C, Ervelä E, Zamyatina A, Kosma P, Skurnik M, Holst O (2001) Characterization of the physiological substrate for lipopolysaccharide heptosyltransferases I and II. J Endotoxin Res 7:263–270
Zamyatina A, Gronow S, Oertelt C, Puchberger M, Brade H, Kosma P (2000) Efficient chemical synthesis of the two anomers of ADP-l-glycero- and d-glycero-d-manno-heptopyranose allows the determination of the substrate specificities of bacterial heptosyltransferases. Angew Chem Int Ed Engl 39:4150–4153
Grizot S, Salem M, Vongsouthi V, Durand L, Moreau F, Dohi H, Vincent S, Escaich S, Ducruix A (2006) Structure of the Escherichia coli heptosyltransferase WaaC: binary complexes with ADP and ADP-2-deoxy-2-fluoro heptose. J Mol Biol 363:383–394
Hiratsuka K, Logan SM, Conlan JW, Chandan V, Aubry A, Smirnova N, Ulrichsen H, Chan KH, Griffith DW, Harrison BA, Li J, Altman E (2005) Identification of a d-glycero-d-manno-heptosyltransferase gene from Helicobacter pylori. J Bacteriol 187:5156–5165
Gronow S, Brabetz W, Lindner B, Brade H (2005) OpsX from Haemophilus influenzae represents a novel type of heptosyltransferase I in lipopolysaccharide biosynthesis. J Bacteriol 187:6242–6247
Kingsley MT, Gabriel DW, Marlow GC, Roberts PD (1993) The opsX locus of Xanthomonas campestris affects host range and biosynthesis of lipopolysaccharide and extracellular polysaccharide. J Bacteriol 175:5839–5850
Brozek KA, Kadrmas JL, Raetz CR (1996) Lipopolysaccharide biosynthesis in Rhizobium leguminosarum. Novel enzymes that process precursors containing 3-deoxy-d-manno-octulosonic acid. J Biol Chem 271:32112–32118
Kadrmas JL, Brozek KA, Raetz CR (1996) Lipopolysaccharide core glycosylation in Rhizobium leguminosarum. An unusual mannosyl transferase resembling the heptosyl transferase I of Escherichia coli. J Biol Chem 271:32119–32125
Kanipes MI, Ribeiro AA, Lin S, Cotter RJ, Raetz CR (2003) A mannosyl transferase required for lipopolysaccharide inner core assembly in Rhizobium leguminosarum. Purification, substrate specificity, and expression in Salmonella waaC mutants. J Biol Chem 278:16356–16364
Schwingel JM, St Michael F, Cox AD, Masoud H, Richards JC, Campagnari AA (2008) A unique glycosyltransferase involved in the initial assembly of Moraxella catarrhalis lipooligosaccharides. Glycobiology 18:447–455
Geurtsen J, Dzieciatkowska M, Steeghs L, Hamstra HJ, Boleij J, Broen K, Akkerman G, El Hassan H, Li J, Richards JC, Tommassen J, van der Ley P (2009) Identification of a novel lipopolysaccharide core biosynthesis gene cluster in Bordetella pertussis, and influence of core structure and lipid A glucosamine substitution on endotoxic activity. Infect Immun 77:2602–2611
Kanipes MI, Tan X, Akelaitis A, Li J, Rockabrand D, Guerry P, Monteiro MA (2008) Genetic analysis of lipooligosaccharide core biosynthesis in Campylobacter jejuni 81-176. J Bacteriol 190:1568–1574
Tullius MV, Phillips NJ, Scheffler NK, Samuels NM, Munson JR Jr, Hansen EJ, Stevens-Riley M, Campagnari AA, Gibson BW (2002) The lbgAB gene cluster of Haemophilus ducreyi encodes a β-1,4-galactosyltransferase and an α-1,6-d,d-heptosyltransferase involved in lipooligosaccharide biosynthesis. Infect Immun 70:2853–2861
St Michael F, Vinogradov E, Li J, Cox AD (2005) Structural analysis of the lipopolysaccharide from Pasteurella multocida genome strain Pm70 and identification of the putative lipopolysaccharide glycosyltransferases. Glycobiology 15:323–333
Pinta E, Duda KA, Hanuszkiewicz A, Salminen TA, Bengoechea JA, Hyytiäinen H, Lindner B, Radziejewska-Lebrecht J, Holst O, Skurnik M (2010) Characterization of the six glycosyltransferases involved in the biosynthesis of Yersinia enterocolitica serotype O:3 lipopolysaccharide outer core. J Biol Chem 285:28333–28342
Austin EA, Graves JF, Hite LA, Parker CT, Schnaitman CA (1990) Genetic analysis of lipopolysaccharide core biosynthesis by Escherichia coli K-12: insertion mutagenesis of the rfa locus. J Bacteriol 172:5312–5325
Kadam SK, Rehemtulla A, Sanderson KE (1985) Cloning of rfaG, B, I, and J genes for glycosyltransferase enzymes for synthesis of the lipopolysaccharide core of Salmonella typhimurium. J Bacteriol 161:277–284
Martinez-Fleites C, Proctor M, Roberts S, Bolam DN, Gilbert HJ, Davies GJ (2006) Insights into the synthesis of lipopolysaccharide and antibiotics through the structures of two retaining glycosyltransferases from family GT4. Chem Biol 13:1143–1152
Muller E, Hinckley A, Rothfield L (1972) Studies of phospholipid-requiring bacterial enzymes. Purification and properties of uridine diphosphate glucose:lipopolysaccharide glucosyltransferase I. J Biol Chem 247:2614–2622
Parker CT, Pradel E, Schnaitman CA (1992) Identification and sequences of the lipopolysaccharide core biosynthetic genes rfaQ, rfaP, and rfaG of Escherichia coli K-12. J Bacteriol 174:930–934
Heinrichs DE, Yethon JA, Whitfield C (1998) Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol 30:221–232
Heinrichs DE, Whitfield C, Valvano MA (1999) Biosynthesis and genetics of lipopolysaccharide core. In: Brade H, Opal SM, Vogel SN, Morrison DC (eds) Endotoxin in health and disease. Marcel Dekker, New York, pp 305–330
Kaniuk NA, Monteiro MA, Parker CT, Whitfield C (2002) Molecular diversity of the genetic loci responsible for lipopolysaccharide core oligosaccharide assembly within the genus Salmonella. Mol Microbiol 46:1305–1318
Carstenius P, Flock JI, Lindberg A (1990) Nucleotide sequence of rfaI and rfaJ genes encoding lipopolysaccharide glycosyl transferases from Salmonella typhimurium. Nucleic Acids Res 18:6128
Endo A, Rothfield L (1969) Studies of a phospholipid-requiring bacterial enzyme. I. Purification and properties of uridine diphosphate galactose: lipopolysaccharide α-3-galactosyl transferase. Biochemistry 8:3500–3507
Pradel E, Parker CT, Schnaitman CA (1992) Structures of the rfaB, rfaI, rfaJ, and rfaS genes of Escherichia coli K-12 and their roles in assembly of the lipopolysaccharide core. J Bacteriol 174:4736–4745
Whitfield C, Kaniuk N, Frirdich E (2003) Molecular insights into the assembly and diversity of the outer core oligosaccharide in lipopolysaccharides from Escherichia coli and Salmonella. J Endotoxin Res 9:244–249
Heinrichs DE, Yethon JA, Amor PA, Whitfield C (1998) The assembly system for the outer core portion of R1- and R4-type lipopolysaccharides of Escherichia coli. The R1 core-specific β-glucosyltransferase provides a novel attachment site for O-polysaccharides. J Biol Chem 273:29497–29505
Heinrichs DE, Monteiro MA, Perry MB, Whitfield C (1998) 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 273:8849–8859
Leipold MD, Vinogradov E, Whitfield C (2007) Glycosyltransferases involved in biosynthesis of the outer core region of Escherichia coli lipopolysaccharides exhibit broader substrate specificities than is predicted from lipopolysaccharide structures. J Biol Chem 282:26786–26792
Leipold MD, Kaniuk NA, Whitfield C (2007) The C-terminal domain of the Escherichia coli WaaJ glycosyltransferase is important for catalytic activity and membrane association. J Biol Chem 282:1257–1264
Persson K, Ly HD, Dieckelmann M, Wakarchuk WW, Withers SG, Strynadka NC (2001) Crystal structure of the retaining galactosyltransferase LgtC from Neisseria meningitidis in complex with donor and acceptor sugar analogs. Nat Struct Biol 8:166–175
MacLachlan PR, Kadam SK, Sanderson KE (1991) Cloning, characterization, and DNA sequence of the rfaLK region for lipopolysaccharide synthesis in Salmonella typhimurium LT2. J Bacteriol 173:7151–7163
Banerjee A, Wang R, Uljon SN, Rice PA, Gotschlich EC, Stein DC (1998) Identification of the gene (lgtG) encoding the lipooligosaccharide β chain synthesizing glucosyl transferase from Neisseria gonorrhoeae. Proc Natl Acad Sci USA 95:10872–10877
Erwin AL, Haynes PA, Rice PA, Gotschlich EC (1996) Conservation of the lipooligosaccharide synthesis locus lgt among strains of Neisseria gonorrhoeae: requirement for lgtE in synthesis of the 2C7 epitope and of the β chain of strain 15253. J Exp Med 184:1233–1241
Gotschlich EC (1994) Genetic locus for the biosynthesis of the variable portion of Neisseria gonorrhoeae lipooligosaccharide. J Exp Med 180:2181–2190
Kahler CM, Carlson RW, Rahman MM, Martin LE, Stephens DS (1996) Two glycosyltransferase genes, lgtF and rfaK, constitute the lipooligosaccharide ice (inner core extension) biosynthesis operon of Neisseria meningitidis. J Bacteriol 178:6677–6684
Wakarchuk W, Martin A, Jennings MP, Moxon ER, Richards JC (1996) Functional relationships of the genetic locus encoding the glycosyltransferase enzymes involved in expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. J Biol Chem 271:19166–19173
Hood DW, Deadman ME, Cox AD, Makepeace K, Martin A, Richards JC, Moxon ER (2004) Three genes, lgtF, lic2C and lpsA, have a primary role in determining the pattern of oligosaccharide extension from the inner core of Haemophilus influenzae LPS. Microbiology 150:2089–2097
Weiser JN, Lindberg AA, Manning EJ, Hansen EJ, Moxon ER (1989) Identification of a chromosomal locus for expression of lipopolysaccharide epitopes in Haemophilus influenzae. Infect Immun 57:3045–3052
Yildirim HH, Li J, Richards JC, Hood DW, Moxon ER, Schweda EK (2005) An alternate pattern for globoside oligosaccharide expression in Haemophilus influenzae lipopolysaccharide: structural diversity in nontypeable strain 1124. Biochemistry 44:5207–5224
Edwards KJ, Allen S, Gibson BW, Campagnari AA (2005) Characterization of a cluster of three glycosyltransferase enzymes essential for Moraxella catarrhalis lipooligosaccharide assembly. J Bacteriol 187:2939–2947
Preston A, Mandrell RE, Gibson BW, Apicella MA (1996) The lipooligosaccharides of pathogenic Gram-negative bacteria. Crit Rev Microbiol 22:139–180
van Putten JP, Robertson BD (1995) Molecular mechanisms and implications for infection of lipopolysaccharide variation in Neisseria. Mol Microbiol 16:847–853
Griffiss JM, Schneider H (1999) The chemistry and biology of lipooligosaccharides: the endotoxins of bacteria of the respiratory and genital mucosae. In: Brade H, Opal SM, Vogel SN, Morrison DC (eds) Endotoxin in health and disease. Marcel Dekker, New York, pp 179–193
Schneider H, Hale TL, Zollinger WD, Seid RC Jr, Hammack CA, Griffiss JM (1984) Heterogeneity of molecular size and antigenic expression within lipooligosaccharides of individual strains of Neisseria gonorrhoeae and Neisseria meningitidis. Infect Immun 45:544–549
Filiatrault MJ, Gibson BW, Schilling B, Sun S, Munson RS Jr, Campagnari AA (2000) Construction and characterization of Haemophilus ducreyi lipooligosaccharide (LOS) mutants defective in expression of heptosyltransferase III and β1,4-glucosyltransferase: identification of LOS glycoforms containing lactosamine repeats. Infect Immun 68:3352–3361
Gilbert M, Karwaski MF, Bernatchez S, Young NM, Taboada E, Michniewicz J, Cunningham AM, Wakarchuk WW (2002) The genetic bases for the variation in the lipo-oligosaccharide of the mucosal pathogen. Campylobacter jejuni. Biosynthesis of sialylated ganglioside mimics in the core oligosaccharide. J Biol Chem 277:327–337
Faglin I, Tiralongo J, Wilson JC, Collins PM, Peak IR (2010) Biochemical analysis of Lgt3, a glycosyltransferase of the bacterium Moraxella catarrhalis. Biochem Biophys Res Commun 393:609–613
Regue M, Climent N, Abitiu N, Coderch N, Merino S, Izquierdo L, Altarriba M, Tomas JM (2001) Genetic characterization of the Klebsiella pneumoniae waa gene cluster, involved in core lipopolysaccharide biosynthesis. J Bacteriol 183:3564–3573
Deadman ME, Lundstrom SL, Schweda EK, Moxon ER, Hood DW (2006) Specific amino acids of the glycosyltransferase LpsA direct the addition of glucose or galactose to the terminal inner core heptose of Haemophilus influenzae lipopolysaccharide via alternative linkages. J Biol Chem 281:29455–29467
Wilkinson RG, Stocker BA (1968) Genetics and cultural properties of mutants of Salmonella typhimurium lacking glucosyl or galactosyl lipopolysaccharide transferases. Nature 217:955–957
Lindberg AA, Hellerqvist C-G (1980) Rough mutants of Salmonella typhimurium: immunochemical and structural analysis of lipopolysaccarides from rfaH mutants. J Gen Microbiol 116:25–32
Bailey MJA, Hughes C, Koronakis V (1997) RfaH and the ops element, components of a novel system controlling bacterial transcription elongation. Mol Microbiol 26:845–851
Nieto JM, Bailey MJA, Hughes C, Koronakis V (1996) Suppression of transcription polarity in the Escherichia coli haemolysin operon by a short upstream element shared by polysaccharide and DNA transfer determinants. Mol Microbiol 19:705–713
Hobbs M, Reeves PR (1994) The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters. Mol Microbiol 12:855–856
Marolda CL, Valvano MA (1998) Promoter region of the Escherichia coli O7-specific lipopolysaccharide gene cluster: structural and functional characterization of an upstream untranslated mRNA sequence. J Bacteriol 180:3070–3079
Artsimovitch I, Landick R (2002) The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109:193–203
Belogurov GA, Mooney RA, Svetlov V, Landick R, Artsimovitch I (2009) Functional specialization of transcription elongation factors. EMBO J 28:112–122
Belogurov GA, Sevostyanova A, Svetlov V, Artsimovitch I (2010) Functional regions of the N-terminal domain of the antiterminator RfaH. Mol Microbiol 76:286–301
Karow M, Raina S, Georgopoulos C, Fayet O (1991) Complex phenotypes of null mutations in the htr genes, whose products are essential for Escherichia coli growth at elevated temperatures. Res Microbiol 142:289–294
Hoffman J, Lindberg B, Brubaker RR (1980) Structural studies of the O-specific side-chains of the lipopolysaccharide from Yersinia enterocolitica Ye 128. Carbohydr Res 78:212–214
Skurnik M, Venho R, Toivanen P, Al-Hendy A (1995) A novel locus of Yersinia enterocolitica serotype O:3 involved in lipopolysaccharide outer core biosynthesis. Mol Microbiol 17:575–594
Skurnik M, Venho R, Bengoechea J-A, Moriyón I (1999) The lipopolysaccharide outer core of Yersinia enterocolitica serotype O:3 is required for virulence and plays a role in outer membrane integrity. Mol Microbiol 31:1443–1462
Nizet V (2006) Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr Issues Mol Biol 8:11–26
Monreal D, Grillo MJ, Gonzalez D, Marin CM, De Miguel MJ, Lopez-Goni I, Blasco JM, Cloeckaert A, Moriyon I (2003) Characterization of Brucella abortus O-polysaccharide and core lipopolysaccharide mutants and demonstration that a complete core is required for rough vaccines to be efficient against Brucella abortus and Brucella ovis in the mouse model. Infect Immun 71:3261–3271
Ramjeet M, Deslandes V, St MF, Cox AD, Kobisch M, Gottschalk M, Jacques M (2005) Truncation of the lipopolysaccharide outer core affects susceptibility to antimicrobial peptides and virulence of Actinobacillus pleuropneumoniae serotype 1. J Biol Chem 280:39104–39114
Fresno S, Jimenez N, Izquierdo L, Merino S, Corsaro MM, De CC, Parrilli M, Naldi T, Regue M, Tomas JM (2006) The ionic interaction of Klebsiella pneumoniae K2 capsule and core lipopolysaccharide. Microbiology 152:1807–1818
Cortes G, Borrell N, de Astorza B, Gomez C, Sauleda J, Alberti S (2002) Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infect Immun 70:2583–2590
Regue M, Izquierdo L, Fresno S, Pique N, Corsaro MM, Naldi T, De CC, Waidelich D, Merino S, Tomas JM (2005) A second outer-core region in Klebsiella pneumoniae lipopolysaccharide. J Bacteriol 187:4198–4206
Sahly H, Keisari Y, Crouch E, Sharon N, Ofek I (2008) Recognition of bacterial surface polysaccharides by lectins of the innate immune system and its contribution to defense against infection: the case of pulmonary pathogens. Infect Immun 76:1322–1332
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
Mamat, U., Skurnik, M., Bengoechea, J.A. (2011). Lipopolysaccharide Core Oligosaccharide Biosynthesis and Assembly. In: Knirel, Y., Valvano, M. (eds) Bacterial Lipopolysaccharides. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0733-1_8
Download citation
DOI: https://doi.org/10.1007/978-3-7091-0733-1_8
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)