[en] The lipopolysaccharide (LPS) is a major component of the surface of the Gram negative bacteria. The LPS is composed of three separately synthesized entities: the lipid A, the core oligosaccharide and the O antigen, that will be linked together after their respective synthesis. The lipid A, embedded inside the outer membrane, is the proximal part of the LPS and the core is the medial part, whereas the O antigen represents the distal part free in the external environment. Amongst the Enterobacteriaceae family, the lipid A is structurally highly conserved and the variation in the structure of the core oligosaccharide is limited whereas the O antigen is the hypervariable region. Diverse biological activities have been associated with LPS, amongst which the endotoxinic activity carried by the lipid A, and the strain immunogenic specificity carried by the O antigen. In this review manuscript we summarize the state of knowledge on the structures and biosynthesis of the different components of the LPS of Escherichia coli and on their respective roles in the virulence of pathogenic bacteria.
Disciplines :
Veterinary medicine & animal health Microbiology
Author, co-author :
Szalo, Ioan Mihai ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Médecine des oiseaux, des lagomorphes et des rongeurs
Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires > Microbiologie des denrées alimentaires
Mainil, Jacques ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Bactériologie et pathologie des maladies bactériennes
Language :
French
Title :
Le lipopolysaccharide d’Escherichia coli : structure, biosynthèse et rôles
Alternative titles :
[en] Lipopolysaccharide of Escherichia coli : structure, biosynthesis and functions
Publication date :
2006
Journal title :
Annales de Médecine Vétérinaire
ISSN :
0003-4118
eISSN :
1781-3875
Publisher :
ULg - Université de Liège, Liège, Belgium
Volume :
150
Issue :
2
Pages :
108-124
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
SPF Santé - Service Public Fédéral Santé publique. Sécurité de la Chaîne alimentaire et Environnement [BE] DG RDT - Commission Européenne. Direction Générale de la Recherche et de l'Innovation [BE]
AMOR K., HEINRICHS D.E., FRIRDICH E., ZIEBELL K., JOHNSON R.P., WHITFIELD C. Distribution of core oligosaccharide types in lipopolysaccharides from Escherichia coli. Infect. Immun., 2000, 68, 1116-1124.
ANDERSON M.S., BULL H.G., GALLOWAY S.M., KELLY T.M., MOHAN S., RADIKA K., RAETZ C.R. UDP-N-acetylglucosamine acyltransferase of Escherichia coli. The first step of endotoxin biosynthesis is thermodynamically unfavorable. J. Biol. Chem., 1993, 268, 19858-19865.
ANDERSON M.S., RAETZ C.R. Biosynthesis of lipid A precursors in Escherichia coli. A cytoplasmic acyltransferase that converts UDP-N-acetylglucosamine to UDP-3-O-(R-3-hydroxymyristoyl)-N-acetylglucosamine. J. Biol. Chem., 1987, 262, 5159-5169.
ANDERSON M.S., ROBERTSON A.D., MACHER I., RAETZ C.R. Biosynthesis of lipid A in Escherichia coli : identification of UDP-3-O-[(R)-3-hydroxymyristoyl] -alpha-D-glucosamine as a precursor of UDP-N2,O3-bis[(R)-3-hydroxymyristoyl]- alpha-D-glucosamine. Biochemistry, 1988, 27, 1908-1917.
APPELMELK B.J., MONTEIRO M.A., MARTIN S.L., MORAN A.P., VANDENBROUCKE-GRAULS C.M. Why Helicobacter pylori has Lewis antigens. Trends Microbiol., 2000, 8, 565-570.
ASPINALL G.O., FUJIMOTO S., MCDONALD A.G., PANG H., KURJANCZYK L.A., PENNER J.L. Lipopolysaccharides from Campylobacter jejuni associated with Guillain-Barre syndrome patients mimic human gangliosides in structure. Infect. Immun., 1994, 62, 2122-2125.
BAILEY M.J., HUGHES C., KORONAKIS V. RfaH and the ops element, components of a novel system controlling bacterial transcription elongation. Mol. Microbiol., 1997, 26, 845-851.
BASTIN D.A., STEVENSON G., BROWN P.K., HAASE A., REEVES P.R. Repeat unit polysaccharides of bacteria: a model for polymerization resembling that of ribosomes and fatty acid synthetase, with a novel mechanism for determining chain length. Mol. Microbiol., 1993, 7, 725-734.
BATCHELOR R.A., HARAGUCHI G.E., HULL R.A., HULL S.I. Regulation by a novel protein of the bimodal distribution of lipopolysaccharide in the outer membrane of Escherichia coli. J. Bacteriol., 1991, 173, 5699-5704.
BEAMER L.J., CARROLL S.F., EISENBERG D. The three-dimensional structure of human bactericidal/permeability-increasing protein: implications for understanding protein-lipopolysaccharide interactions. Biochem. Pharmacol., 1999, 57, 225-229.
BILGE S.S., VARY J.C., JR., DOWELL S.F., TARR P.I. Role of the Escherichia coli O157:H7 O side chain in adherence and analysis of an rfb locus. Infect. Immun., 1996, 64, 4795-4801.
BRAY D., ROBBINS P.W. The direction of chain growth in Salmonella anatum O-antigen biosynthesis. Biochem. Biophys. Res. Commun., 1967, 28, 334-339.
BULAWA C.E., RAETZ C.R. The biosynthesis of gram-negative endotoxin. Identification and function of UDP-2,3-diacylglucosamine in Escherichia coli. J. Biol. Chem., 1984, 259, 4846-4851.
CAROFF M., KARIBIAN D., CAVAILLON J.M., HAEFFNER-CAVAILLON N. Structural and functional analyses of bacterial lipopolysaccharides. Microbes Infect., 2002, 4, 915-926.
CARTY S.M., SREEKUMAR K.R., RAETZ C.R. Effect of cold shock on lipid A biosynthesis in Escherichia coli. Induction At 12 degrees C of an acyltransferase specific for palmitoleoyl-acyl carrier protein. J. Biol. Chem., 1999, 274, 9677-9685.
CLEMENTZ T., RAETZ C.R. A gene coding for 3-deoxy-D-mannooctulosonic-acid transferase in Escherichia coli. Identification, mapping, cloning, and sequencing. J. Biol. Chem., 1991, 266, 9687-9696.
COHEN J. The immunopathogenesis of sepsis. Nature, 2002, 420, 885-891.
COLLINS L.V., HACKETT J. Molecular cloning, characterization, and nucleotide sequence of the rfc gene, which encodes an O-antigen polymerase of Salmonella Typhimurium. J. Bacteriol., 1991, 173, 2521-2529.
CRAVEN S.E. Altered colonizing ability for the ceca of broiler chicks by lipopolysaccharide-deficient mutants of Salmonella Typhimurium. Avian Dis., 1994, 38, 401-408.
CURRIE C.G., POXTON I.R. The lipopolysaccharide core type of Escherichia coli O157:H7 and other non-O157 verotoxin-producing E. coli. FEMS Immunol. Med. Microbiol., 1999, 24, 57-62.
CZUPRYNSKI C.J. Bacterial evasion of cellular defence mechanisms: an overview. In : Roth J.A. (Ed.), Virulence mechanisms of bacterial pathogens. ASM Press : Washington, 1998, 141-160.
DIPADOVA F.E., BRADE H., BARCLAY G.R., POXTON I.R., LIEHL E., SCHUETZE E., KOCHER H.P., RAMSAY G., SCHREIER M.H., MCCLELLAND D.B.L., RIETSCHEL E.T. A Broadly Cross-Protective Monoclonal-Antibody Binding to Escherichia coli and Salmonella Lipopolysaccharides. Infect. Immun., 1993, 61, 3863-3872.
ERRIDGE C., BENNETT-GUERRERO E., POXTON I.R. Structure and function of lipopolysaccharides. Microbes Infect., 2002, 4, 837-851.
FUJIHARA M., MUROI M., TANAMOTO K., SUZUKI T., AZUMA H., IKEDA H. Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol. Ther., 2003, 100, 171-194.
GIBB A.P., BARCLAY G.R., POXTON I.R., DI PADOVA F. Frequencies of lipopolysaccharide core types among clinical isolates of Escherichia coli defined with monoclonal antibodies. J. Infect. Dis., 1992, 166, 1051-1057.
GRAM C. Ueber die isolirte Farbung der Schizomyceten in SchnittÄ unt Trockenpraparaten. Fortschritte der Median, 1884, 2, 185-189.
HAMANN L., EL SAMALOUTI V., ULMER A.J., FLAD H.D., RIETSCHEL E.T. Components of gut bacteria as immunomodulators. Int. J. Food Microbiol., 1998, 41, 141-154.
HANCOCK R. E. W., KARUNARATNE, D. N., et BERNEGGER-ELI, C. Molecular organisation and structural role of outer membrane macromolecules. In : Ghuysen J.-M., Hakenbeck R. (Eds.), Bacterial cell wall, new comprehensive biochemestry. Elsevier Science : Amsterdam, 1994, 263-279.
HEINRICHS D.E., YETHON J.A., AMOR P.A., WHITFIELD C. The assembly system for the outer core portion of R1- and R4-type lipopolysaccharides of Escherichia coli. The R1 core-specific beta-glucosyltransferase provides a novel attachment site for O-polysaccharides. J. Biol. Chem., 1998, 273, 29497-29505.
HELANDER I.M., LINDNER B., BRADE H., ALTMANN K., LINDBERG A.A., RIETSCHEL E.T., ZAHRINGER U. Chemical structure of the lipopolysaccharide of Haemophilus influenzae strain I-69 Rd-/b+. Description of a novel deep-rough chemotype. Eur. J. Biochem., 1988, 177, 483-492.
HITCHCOCK P.J., LEIVE L., MAKELA P.H., RIETSCHEL E.T., STRITTMATTER W., MORRISON D.C. Lipopolysaccharide nomenclature - past, present, and future. J. Bacteriol., 1986, 166, 699-705.
HOBBS M., REEVES P.R. The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters. Mol. Microbiol., 1994, 12, 855-856.
HULL S. Escherichia coli lipopolysaccharide in pathogenesis and virulence. In : Sussman M□ (Ed.), Escherichia coli : mechanisms of virulence. Cambridge University Press : Cambridge, 1997, 145-167.
INOHARA N., OGURA Y., NUNEZ G. Nods: a family of cytosolic proteins that regulate the host response to pathogens. Curr. Opin. Microbiol., 2002, 5, 76-80.
JACKMAN J.E., RAETZ C.R., FIERKE C.A. Site-directed mutagenesis of the bacterial metalloamidase UDP-(3-O-acyl)-N-acetylglucosamine deacetylase (LpxC). Identification of the zinc binding site. Biochemistry, 2001, 40, 514-523.
JACQUES M. Role of lipo-oligosaccharides and lipopolysaccharides in bacterial adherence. Trends Microbiol., 1996, 4, 408-409.
JANN K., JANN B. Capsules of Escherichia coli. In : Sussman M. (Ed.), Escherichia coli : mechanisms of virulence. Cambridge University Press : Cambridge, 1997, 113-143.
JOINER K.A., SCHMETZ M.A., GOLDMAN R.C., LEIVE L., FRANK M.M. Mechanism of bacterial resistance to complement-mediated killing: inserted C5b-9 correlates with killing for Escherichia coli O111B4 varying in O-antigen capsule and O-polysaccharide coverage of lipid A core oligosaccharide. Infect. Immun., 1984, 45, 113-117.
KEENLEYSIDE W.J., PERRY M., MACLEAN L., POPPE C., WHITFIELD C. A plasmid-encoded rfb O:54 gene cluster is required for biosynthesis of the O:54 antigen in Salmonella enterica serovar Borreze. Mol. Microbiol., 1994, 11, 437-448.
KEENLEYSIDE W.J., WHITFIELD C. Lateral transfer of rfb genes: a mobilizable ColE1-type plasmid carries the rfb O:54 (O:54 antigen biosynthesis) gene cluster from Salmonella enterica serovar Borreze. J. Bacteriol., 1995, 177, 5247-5253.
KEENLEYSIDE W.J., WHITFIELD C. A novel pathway for O-polysaccharide biosynthesis in Salmonella enterica serovar Borreze. J. Biol. Chem., 1996, 271, 28581-28592.
KELLY T.M., STACHULA S.A., RAETZ C.R., ANDERSON M.S. The firA gene of Escherichia coli encodes UDP-3-O-(R-3-hydroxymyristoyl)-glucosamine N-acyl-transferase : the third step of endotoxin biosynthesis. J. Biol. Chem., 1993, 268, 19866-19874.
KLENA J.D., PRADEL E., SCHNAITMAN C.A. The rfaS gene, which is involved in production of a rough form of lipopolysaccharide core in Escherichia coli K-12, is not present in the rfa cluster of Salmonella Typhimurium LT2. J. Bacteriol., 1993, 175, 1524-1527.
KNEIDINGER B., MAROLDA C., GRANINGER M., ZAMYATINA A., MCARTHUR F., KOSMA P., VALVANO M.A., MESSNER P. Biosynthesis pathway of ADP-L-glycero-beta-D- manno-heptose in Escherichia coli. J. Bacteriol., 2002, 184, 363-369.
KUHN H.M., MEIER-DIETER U., MAYER H. ECA, the enterobacterial common antigen. FEMS Microbiol. Rev., 1988, 4, 195-222.
LIANG-TAKASAKI C.J., MAKELA P.H., LEIVE L. Phagocytosis of bacteria by macrophages: changing the carbohydrate of lipopolysaccharide alters interaction with complement and macrophages. J. Immunol., 1982, 128, 1229-1235.
LIU D., COLE R.A., REEVES P.R. An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J. Bacteriol., 1996, 178, 2102-2107.
MCGRATH B.C., OSBORN M.J. Localization of the terminal steps of O-antigen synthesis in Salmonella Typhimurium. J. Bacteriol., 1991, 173, 649-654.
MEIER-DIETER U., BARR K., STARMAN R., HATCH L., RICK P.D. Nucleotide sequence of the Escherichia coli rfe gene involved in the synthesis of enterobacterial common antigen. Molecular cloning of the rfe-rff gene cluster. J. Biol. Chem., 1992, 267, 746-753.
MORAN A.P. The role of lipopolysaccharide in Helicobacter pylori pathogenesis. Aliment Pharmacol. Ther., 1996, 10 Suppl 1, 39-50.
NATARO J.P., LEVINE M.M. Escherichia coli diseases in humans. In : Gyles C.L (Ed.), Escherichia coli in domestic animals and humans. CAB International : Wallingford, 1994, 285-333.
NIKAIDO H. Outer membrane. In : Neidhardt F.C., Ingraham J.L., Low K.B., Magasanik B., Umbarger H.E (Eds.), Escherichia coli and Salmonella Typhimurium : cellular and molecular biology. American Society for Microbiology : Washington, 1994, 29-47.
NIKAIDO H., VAARA M. Outer membrane. In : Neidhardt F.C., Ingraham J.L., Low K.B., Magasanik B., Umbarger H.E (Eds.), Escherichia coli and Salmonella Typhimurium : cellular and molecular biology. American Society for Microbiology : Washington, 1987, 7-22.
O'NEILL L.A., BROWN Z., WARD S.G. Toll-like receptors in the spotlight. Nat. Immunol., 2003, 4, 299-
OSBORN M.J., RICK P.D., RASMUSSEN N.S. Mechanism of assembly of the outer membrane of Salmonella Typhimurium. Translocation and integration of an incomplete mutant lipid A into the outer membrane. J. Biol. Chem., 1980, 255, 4246-4251.
PERERA P.Y., MAYADAS T.N., TAKEUCHI O., AKIRA S., ZAKSZILBERMAN M., GOYERT S.M., VOGEL S.N. CD11b/CD18 acts in concert with CD14 and Toll-like receptor (TLR) 4 to elicit full lipopolysaccharide and taxol-inducible gene expression. J. Immunol., 2001, 166, 574-581.
POLTORAK A., HE X., SMIRNOVA L, LIU M.Y., VAN HUFFEL C., DU X., BIRDWELL D., ALEJOS E., SILVA M., GALANOS C., FREUDENBERG M., RICCIARDI-CASTAGNOLI P., LAYTON B., BEUTLER B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science, 1998, 282, 2085-2088.
POPOFF M.Y., LE MINOR L. Expression of antigenic factor O:54 is associated with the presence of a plasmid in Salmonella. Ann. Inst. Pasteur Microbiol., 1985, 136B, 169-179.
PRESCOTT L.M., HARLEY J.P., KLEIN D.A. Microbiologie. De Boeck Université : Bruxelles, 2003, 1136 p.
PRESTON A., MANDRELL R.E., GIBSON B.W., APICELLA M.A. The lipooligosaccharides of pathogenic gram-negative bacteria. Crit. Rev. Microbiol., 1996, 22, 139-180.
RAETZ C.R.H. Bacterial Lipopolysaccharides : a remarkable family of bioactive macroamphiphiles. In : Neidhardt F.C., Curtiss R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., Umbarger H.E (Eds.), Escherichia coli and Salmonella Typhimurium : cellular and molecular biology. American Society for Microbiology : Washington, 1994, 1035-1063.
RAY B.L., PAINTER G., RAETZ C.R. The biosynthesis of gram-negative endotoxin. Formation of lipid A disaccharides from monosaccharide precursors in extracts of Escherichia coli. J. Biol. Chem., 1984, 259, 4852-4859.
RAY B.L., RAETZ C.R. The biosynthesis of gram-negative endotoxin. A novel kinase in Escherichia coli membranes that incorporates the 4′-phosphate of lipid A. J. Biol. Chem., 1987, 262, 1122-1128.
REEVES P. Biosynthesis and assembly of lipopolysaccharides. In : Ghuysen J.-M., Hakenbeck R. (Eds.), Bacterial cell wall, new comprehensive biochemistry. Elsevier Science : Amsterdam, 1994, 281-317.
REEVES P.R., HOBBS M., VALVANO M.A., SKURNIK M., WHITFIELD C., COPLIN D., KIDO N., KLENA J., MASKELL D., RAETZ C.R., RICK P.D. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol., 1996, 4, 495-503.
RICK P.D., SILVER R.P Enterobacterial Common Antigen and Capsular Polysaccharides. In : Neidhardt F.C., Curtiss R., Ingraham J.L., Low K.B., Magasanik B., Schaechter M., Umbarger H.E (Eds.), Escherichia coli and Salmonella Typhimurium : cellular and molecular biology. American Society for Microbiology : Washington, 1987, 648-662.
RIETSCHEL E.T., KIRIKAE T., SCHADE F.U., ULMER A.J., HOLST O., BRADE H., SCHMIDT G., MAMAT U., GRIMMECKE H.D., KUSUMOTO S. The chemical structure of bacterial endotoxin in relation to bioactivity. Immunobiology, 1993, 187, 169-190.
ROBBINS P.W., BRAY D., DANKERT B.M., WRIGHT A. Direction of chain growth in polysaccharide synthesis. Science, 1967, 158, 1536-1542.
ROCCHETTA H.L., BURROWS L.L., PACAN J.C., LAM J.S. Three rhamnosyltransferases responsible for assembly of the A-band D-rhamnan polysaccharide in Pseudomonas aeruginosa: a fourth transferase, WbpL, is required for the initiation of both A-band and B-band lipopolysaccharide synthesis. Mol. Microbiol., 1998, 28, 1103-1119.
ROCCHETTA H.L., LAM J.S. Identification and functional characterization of an ABC transport system involved in polysaccharide export of A-band lipopolysaccharide in Pseudomonas aeruginosa. J. Bacteriol., 1997, 179, 4713-4724.
SALYERS A.A., WHITT D.D. Bacterial pathogenesis : a molecular approach. ASM Press : Washington, 1994, 418 p.
SALYERS A.A., WHITT D.D. Bacterial pathogenesis : a molecular approach. 2nd Ed. ASM Press : Washington, 2002, 539 p.
SANDKVIST M. Biology of type II secretion. Mol. Microbiol., 2001, 40, 271-283.
SCHNAITMAN C.A., KLENA J.D. Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol. Rev., 1993, 57, 655-682.
SORENSEN P.G., LUTKENHAUS J., YOUNG K., EVELAND S.S., ANDERSON M.S., RAETZ C.R. Regulation of UDP-3-O-[R-3-hydroxymyristoyl]-N-acetylglucosamine deacetylase in Escherichia coli. The second enzymatic step of lipid a biosynthesis. J. Biol. Chem., 1996, 271, 25898-25905.
SZALO I.M., TAMINIAU B., GOFFAUX F., PIRSON V., MCCAPPIN J., BALL H.J., MAINIL J.G. 2F3 monoclonal antibody recognizes the O26 O-antigen moiety of the lipopolysaccharide of enterohemorrhagic Escherichia coli strain 4276. Clin. Diagn. Lab. Immunol., 2004, 11, 532-537.
TANAMOTO K., ZAHRINGER U., MCKENZIE G.R., GALANOS C., RIETSCHEL E.T., LUDERITZ O., KUSUMOTO S., SHIBA T. Biological activities of synthetic lipid A analogs: pyrogenicity, lethal toxicity, anticomplement activity, and induction of gelation of Limulus amoebocyte lysate. Infect. Immun., 1984, 44, 421-426.
TRIANTAFILOU M., MIYAKE K., GOLENBOCK D.T., TRIANTAFILOU K. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci., 2002, 115, 2603-2611.
WANG L., LIU D., REEVES P.R. C-terminal half of Salmonella enterica WbaP (RfbP) is the galactosyl-1-phosphate transferase domain catalyzing the first step of O-antigen synthesis. J. Bacteriol., 1996, 178, 2598-2604.
WANG L., REEVES P.R. Organization of Escherichia coli 0157 O antigen gene cluster and identification of its specific genes. Infect. Immun., 1998, 66, 3545-3551.
WHITFIELD C. Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol., 1995, 3, 178-185.
WHITFIELD C., AMOR P.A., KOPLIN R. Modulation of the surface architecture of gram-negative bacteria by the action of surface polymer:lipid A-core ligase and by determinants of polymer chain length. Mol. Microbiol., 1997, 23, 629-638.
WHITFIELD, C., KENLEYSIDE, W. J., et CLARKE, B. R. Structure, function and synthesis of surface polysaccharides in Escherichla coli. In : Gyles, C (Ed.), Escherichia coli in domestic animals and humans. CAB International : Wallingford, 1994, 437-494.
WHITFIELD C., ROBERTS I.S. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol., 1999, 31, 1307-1319.
WRIGHT S.D., RAMOS R.A., TOBIAS P.S., ULEVITCH R.J., MATHISON J.C. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science, 1990, 249, 1431-1433.
YOUNG K., SILVER L.L., BRAMHILL D., CAMERON P., EVELAND S.S., RAETZ C.R., HYLAND S.A., ANDERSON M.S. The envA permeability/cell division gene of Escherichia coli encodes the second enzyme of lipid A biosynthesis. UDP-3-O-(R-3-hydroxymyristoyl)-N-acetylglucosamine deacetylase. J. Biol. Chem., 1995, 270, 30384-30391.
