A detailed knowledge of LPS biosynthesis is of the utmost importance in understanding the function of the outer membrane of Gram-negative bacteria. The regulation of LPS biosynthesis affects many more compartments of the bacterial cell than the outer membrane and thus contributes to the understanding of the physiology of Gram-negative bacteria in general, on the basis of which only mechanisms of virulence and antibiotic resistance can be studied to find new targets for antibacterial treatment. The study of LPS biosynthesis is also an excellent example to demonstrate the limitations of `genomics' and `proteomics', since secondary gene products can be studied only by the combined tools of molecular genetics, enzymology and analytical structural biochemistry. Thus, the door to the field of `glycomics' is opened.
References
1.
Brade H., Opal SM, Vogel SN et al. Endotoxin in Health and Disease. New York : Marcel Dekker, 1999.
2.
Vaara M.Lipopolysaccharide and the permeability of the bacterial outer membrane. In: Brade H, Opal SM, Vogel SN et al. (eds) Endotoxin in Health and Disease. New York: Marcel Dekker, 1999; 31—38.
3.
Nikaido H.Outer membrane. In: Neidhardt FC, Curtiss III R, Ingraham JL et al. (eds) Escherichia coli and Salmonella typhimurium, Cellular and Molecular Biology. Washington DC: American Society for Microbiology, 1996; 29—47.
4.
Brandenburg K., Seydel U.Investigation into the fluidity of lipopolysaccharide and free lipid A membrane systems by Fourier-transform infrared spectroscopy and differential scanning calorimetry. Eur J Biochem1990; 191: 229—236.
5.
Labischinski H., Naumann D., Schultz C. et al. ComparativeX-ray and Fourier-transform-infrared investigations of conformational properties of bacterial and synthetic lipid A of Escherichia coli and Salmonella minnesota as well as partial structures and analogues thereof. Eur J Biochem1989; 179: 659—665.
6.
De Cock H., Brandenburg K., Wiese A. et al. Non-lamellar structure and negative charges of lipopolysaccharides required for efficient folding of outer membrane protein PhoE of Escherichia coli. J Biol Chem1999; 274: 5114—5119.
7.
Kawahara K., Seydel U., Matsuura M. et al. Chemical structure of glycosphingolipids isolated from Sphingomonas paucimobilis. FEBS Lett1991; 292: 107—110.
8.
Kawasaki S., Moriguchi R., Sekiya K. et al. The cell envelope structure of the lipopolysaccharide-lacking Gram-negative bacterium Sphingomonas paucimobilis. J Bacteriol1994; 176: 284—290.
9.
Batrakov SG, Sheichenko VI, Nikitin DIA novel glycosphingolipid from Gram-negative aquatic bacteria. Biochim Biophys Acta1999; 1440: 163—175.
10.
Steeghs L., den Hartog R., den Boer A. et al. Meningitis bacterium is viable without endotoxin. Nature1998; 392: 449—450.
11.
Zähringer U., Lindner B., Rietschel ETMolecular structure of lipid A, the endotoxic center of bacterial lipopolysaccharides . In: Horton D. (ed) Advances in Carbohydrate Chemistry and Biochemistry. San Diego, CA: Academic Press, 1994; 211—265.
12.
Zähringer U., Lindner B., Rietschel ETChemical structure of lipid A: recent advances in structural analysis of biologically active molecules. In: Brade H, Opal SM, Vogel SN et al. (eds) Endotoxin in Health and Disease. New York: Marcel Dekker, 1999; 93—114.
13.
Caroff M., Deprun C., Richards JC et al. Structural characterization of the lipid A of Bordetella pertussis 1414 endotoxin. J Bacteriol1994; 176: 5156—5159.
14.
Zähringer U. , Knirel YA, Lindner B. et al. The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog Clin Biol Res1995; 392: 113—139.
15.
Plötz BM, Lindner B., Stetter KO et al. Characterization of a novel lipid A containing D-galacturonic acid that replaces phosphate residues. The structure of the lipid a of the lipopolysaccharide from the hyperthermophilic bacterium Aquifex pyrophilus . J Biol Chem2000; 275: 11222—11228.
16.
Moran AP, Rietschel ET, Kosunen TU et al. Chemical characterization of Campylobacter jejuni lipopolysaccharides containing N-acetylneuraminic acid and 2,3-diamino-2,3-dideoxy-D-glucose. J Bacteriol1991; 173: 618—626.
17.
Bhat UR, Forsberg LS, Carlson RWStructure of lipid A component of Rhizobium leguminosarum bv. phaseoli lipopolysaccharide. Unique non-phosphorylated lipid A containing 2-amino-2-deoxygluconate, galacturonate, and glucosamine. J Biol Chem1994; 269: 14402—14410.
18.
Weintraub A. , Zähringer U., Wollenweber HW et al. Structural characterization of the lipid A component of Bacteroides fragilis strain NCTC 9343 lipopolysaccharide . Eur J Biochem1989; 183: 425—431.
19.
Rau H., Seydel U., Freudenberg M. et al. Lipopolysaccharide of Rhodospirillum salinarum 40: structural studies on the core and lipid A region. Arch Microbiol1995; 164: 280—289.
20.
Holst O., Borowiak D., Weckesser J. et al. Structural studies on the phosphate-free lipid A of Rhodomicrobium vannielii ATCC 17100. Eur J Biochem1983; 137: 325—332.
21.
Vinogradov EV, Bock K., Petersen BO et al. The structure of the carbohydrate backbone of the lipopolysaccharide from Acinetobacter strain ATCC 17905. Eur J Biochem1997; 243: 122—127.
22.
Holst O.Chemical structure of the core region of lipopolysaccharides. In: Brade H, Opal SM, Vogel SN et al. (eds) Endotoxin in Health and Disease. New York: Marcel Dekker , 1999; 115—154.
23.
Isshiki Y., Kawahara K., Zahringer U.Isolation and characterisation of disodium (4-amino-4-deoxy-beta-L- arabinopyranosyl)-(1-8)-(D-glycero-alpha-D-talo-oct-2-ulopyranosylonate)-(2-4)-(m ethyl 3-deoxy-D-manno-oct-2-ulopyranosid)onate from the lipopolysaccharide of Burkholderia cepacia. Carbohydr Res1998 ; 313: 21—27.
24.
Vinogradov EV, Petersen BO, Thomas-Oates JE et al. 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 Chem1998; 273: 28122—28131.
25.
Helander IM , Lindner B., Brade H. et al. Chemical structure of the lipopolysaccharide of Haemophilus influenzae strain I-69 Rd—/b+. Description of a novel deep-rough chemotype. Eur J Biochem1988; 177: 483—492.
26.
Brade H., Brabetz W., Brade L. et al. Chlamydial lipopolysaccharide. J Endotoxin Res1997; 4: 67—84.
27.
Yethon JA, Heinrichs DE, Monteiro MA et al. 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 Bacteriol1998; 175: 2534—2540.
28.
Jansson PEThe chemistry of O-polysaccharide chains in bacterial lipopolysaccharides . In: Brade H, Opal SM, Vogel SN et al. (eds) Endotoxin in Health and Disease. New York: Marcel Dekker, 1999; 155—178.
29.
Preston A., Mandrell RE, Gibson BW et al. The lipooligosaccharides of pathogenic Gram-negative bacteria . Crit Rev Microbiol1996; 22: 139—180.
30.
Brade H., Brade L., Nano FEChemical and serological investigations on the genus-specific lipopolysaccharide epitope of Chlamydia. Proc Natl Acad Sci USA1987; 84: 2508—2512.
31.
Heinrichs DE, Yethon JA, Whitfield C.Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol1998; 30: 221—232.
32.
Schnaitman CA , Klena JDGenetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev1993; 57: 655—682.
33.
Reeves PR, Hobbs M., Valvano MA et al. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol1996; 4: 495—503.
34.
Keenleyside WJ, Whitfield C.Genetics and biosynthesis of lipopolysaccharide O-antigens. In: Brade H, Opal SM, Vogel SN et al. (eds) Endotoxin in Health and Disease. New York: Marcel Dekker , 1999; 331—358.
35.
Mäkelä PH, Stocker Bad.Genetics of lipopolysaccharide. In: Rietschel ET. (ed) Chemistry of Endotoxin. Amsterdam : Elsevier Science, 1984; 59—137.
36.
Heinrichs DE, Valvano MA, Whitfield C.Biosynthesis and genetics of lipopolysaccharide core. In: Brade H, Opal SM, Vogel SN et al. (eds) Endotoxin in Health and Disease. New York: Marcel Dekker , 1999; 305—330.
37.
Raetz Crh.Enzymes of lipid A biosynthesis: targets for the design of new antibiotics . Prog Clin Biol Res1998; 397: 1—14.
38.
Polissi A., Georgopoulos C.Mutational analysis and properties of the msbA gene of Escherichia coli, coding for an essential ABC family transporter. Mol Microbiol1996; 20: 1221—1233.
39.
Zhou Z., White KA, Polissi A. et al. Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem1998; 273: 12466—12475.
40.
Kahler CM, Stephens DSGenetic basis for biosynthesis, structure, and function of meningococcal lipooligosaccharide (endotoxin). Crit Rev Microbiol1998; 24: 281—334.
41.
Raetz Crh.Bacterial lipopolysaccharides: a remarkable family of bioactive macroamphiphiles . In: Neidhardt FC. (ed) Escherichia coli and Salmonella: Cellular and Molecular Biology. Washington, DC: American Society for Microbiology, 1996; 1035—1063.
42.
Rick PD, Raetz Crh.Microbial pathways of lipid A biosynthesis. In: Brade H, Opal SM, Vogel SN et al. (eds) Endotoxin in Health and Disease. New York: Marcel Dekker , 1999; 283—304.
43.
Anderson MS , Raetz CRBiosynthesis 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 Chem1987; 262: 5159—5169.
44.
Raetz Crh, Roderick SLA left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science1995; 270: 997—1000.
45.
Anderson MS , Bull HG, Galloway SM et al. UDP-N-acetylglucosamine acyltransferase of Escherichia coli. The first step of endotoxin biosynthesis is thermodynamically unfavorable. J Biol Chem1993; 268: 19858—19865.
46.
Williamson JM, Anderson MS, Raetz Crh.Acyl-acyl carrier protein specificity of UDP-GlcNAc acyltransferases from Gram-negative bacteria: relationship to lipid A structure. J Bacteriol1991; 173: 3591—3596.
47.
Dotson GD, Kaltashov IA, Cotter RJ et al. Expression cloning of a Pseudomonas gene encoding a hydroxydecanoyl-acyl carrier protein-dependent UDP-GlcNAc acyltransferase. J Bacteriol1998; 180: 330—337.
48.
Wyckoff TJ, Lin SH, Cotter RJ et al. Hydrocarbon rulers in UDP-N-acetylglucosamine acyltransferases . J Biol Chem1998; 273: 32369—32372.
49.
Qureshi N., Kaltashov I., Walker K. et al. Structure of the monophosphoryl lipid A moiety obtained from the lipopolysaccharide of Chlamydia trachomatis. J Biol Chem1997; 272: 10594-10600.
50.
Galloway SM , Raetz Crh.A mutant of Escherichia coli defective in the first step of endotoxin biosynthesis. J Biol Chem1990; 265: 6394—6402.
51.
Vuorio R., Vaara M.The lipid A biosynthesis mutation lpxA2 of Escherichia coli results in drastic antibiotic supersusceptibility. Antimicrob Agents Chemother1992; 36: 826—829.
52.
Young K., Silver LL, Bramhill D. et al. 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 Chem1995; 270: 30384—30391.
53.
Hyland SA, Eveland SS, Anderson MSCloning, expression, and purification of UDP-3-O-acyl-GlcNAc deacetylase from Pseudomonas aeruginosa: a metalloamidase of the lipid A biosynthesis pathway . J Bacteriol1997; 179 : 2029—2037.
54.
Jackman JE, Fierke CA, Tumey LN et al. Antibacterial agents that target lipid A biosynthesis in Gram-negative bacteria. Inhibition of diverse UDP-3-O-(R-3-hydroxymyristoyl)-N-acetylglucosamine deacetylases by substrate analogs containing zinc binding motifs. J Biol Chem2000; 275: 11002—11009.
55.
Jackman JE, Raetz Crh, Fierke CAUDP-3-O-(R-3-hydroxymyristoyl)-N-acetylglucosamine deacetylase of Escherichia coli is a zinc metalloenzyme. Biochemistry1999; 38: 1902—1911.
56.
Onishi HR, Pelak BA, Gerckens LS et al. Antibacterial agents that inhibit lipid A biosynthesis. Science1996; 274: 980—982.
57.
Anderson MS , Robertson AD, Macher I. et al. Biosynthesis of lipid A in Escherichia coli: identification of UDP-3-O-[(R)-3-hydroxymyristoyl]-α-D-glucosamine as a precursor of UDP-N2, O3bis[(R)-3-hydroxymyristoyl]-α-D-glucosamine . Biochemistry1988; 27: 1908—1917.
58.
Kelly TM, Stachula SA, Raetz Crh et al. The firA gene of Escherichia coli encodes UDP-3-O-(R-3-hydroxymyristoyl)-glucosamine N-acyltransferase. The third step of endotoxin biosynthesis. J Biol Chem1993; 268: 19866—19874.
59.
Babinski KJ , Raetz Crh.Identification of a gene encoding a novel Escherichia coli UDP-2,3-diacylglucosamine hydrolase. FASEB J1998; 12: L63.
60.
Crowell DN, Anderson MS, Raetz Crh.Molecular cloning of the genes for lipid A disaccharide synthase and UDP-N-acetylglucosamine acyltransferase in Escherichia coli. J Bacteriol1986; 168: 152—159.
61.
Radika K., Raetz Crh.Purification and properties of lipid A disaccharide synthase of Escherichia coli. J Biol Chem1988; 263: 14859—14867.
62.
Raetz Crh.Molecular genetics of membrane phospholipid synthesis. Annu Rev Genet1986; 20: 253—295.
63.
Ray BL, Raetz Crh.The biosynthesis of Gram-negative endotoxin. A novel kinase in Escherichia coli membranes that incorporates the 4′-phosphate of lipid A. J Biol Chem1987; 262: 1122—1128.
64.
Hansen-Hagge T., Lehmann V., Seydel U. et al. Isolation and structural analysis of two lipid A-precursors from a Kdo-deficient mutant of Salmonella typhimurium differing in their hexadecanoic acid content. Arch Microbiol1985; 141: 353—358.
65.
Raetz Crh, Purcell S., Meyer MV et al. Isolation and characterization of eight lipid A precursors from a 3-deoxy-D-manno-octylosonic acid-deficient mutant of Salmonella typhimurium . J Biol Chem1985; 260: 16080—16088.
66.
Imoto M., Yoshimura H., Yamamoto M. et al. Chemical synthesis of phosphorylated tetraacyl disaccharide corresponding to a biosynthetic precursor of lipid A. Tetrahedron Lett1984; 25: 2667—2670.
67.
Garrett TA, Kadrmas JL, Raetz Crh.Identification of the gene encoding the Escherichia coli lipid a 4′-kinase — facile phosphorylation of endotoxin analogs with recombinant LpxK. J Biol Chem1997; 272: 21855—21864.
68.
Price NP, Kelly TM, Raetz Crh et al. Biosynthesis of a structurally novel lipid A in Rhizobium leguminosarum: identification and characterization of six metabolic steps leading from UDP-GlcNAc to 3-deoxy-D-manno-2-octulosonic acid2-lipid IVA. J Bacteriol1994; 176: 4646—4655.
69.
Price NP, Jeyaretnam B., Carlson RW et al. Lipid A biosynthesis in Rhizobium leguminosarum: role of a 2-keto-3-deoxyoctulosonateactivated 4′ phosphatase. Proc Natl Acad Sci USA1995; 92: 7352—7356.
70.
Goldman RC, Doran CC, Kadam SK et al. Lipid A precursor from Pseudomonas aeruginosa is completely acylated prior to addition of 3-deoxy-D-manno-octulosonate. J Biol Chem1988; 263: 5217—5223.
71.
Ray PH, Kelsey JE, Bigham EC et al. Synthesis and use of 3-deoxy-D-manno-2-octulosonate (Kdo) in Escherichia coli. In: Anderson L, Unger FM. (eds) Bacterial Lipopolysaccharides — Structure, Synthesis, and Biochemical Activities. Washington DC: American Chemical Society, 1983 ; 141—169.
72.
Ray PHPurification and characterization of 3-deoxy-D-manno-octulosonate 8-phosphate synthetase from Escherichia coli. J Bacteriol1980; 141: 635—644.
73.
Levin DH, Racker E.Condensation of arabinose 5-phosphate and phosphorylenol pyruvate by 2-keto-3-deoxy-8-phosphooctonic acid synthase. J Biol Chem1959; 234: 2532—2539.
74.
Ghalambor MA , Heath ECThe biosynthesis of cell wall lipopolysaccharide in Escherichia coli. V. Purification and properties of 3-deoxy-D-manno-octulosonate aldolase. J Biol Chem1966; 241: 3222—3227.
75.
Woisetschläger M., Högenauer G.Cloning and characterization of the gene encoding 3-deoxy-D-manno-octulosonate 8-phosphate synthetase from Escherichia coli . J Bacteriol1986; 168: 437—439.
76.
Radaev S., Dastidar P., Patel M. et al. Structure and mechanism of 3-deoxy-D-manno-octulosonate 8-phosphate synthase. J Biol Chem2000; 275: 9476—9484.
77.
Radaev S., Dastidar P., Patel M. et al. Preliminary X-ray analysis of a new crystal form of the Escherichia coli KDO8P synthase. Acta Crystallogr D Biol Crystallogr2000; 56: 516—519.
78.
Ray PH, Benedict CDPurification and characterization of specific 3-deoxy-D-manno-octulosonate 8-phosphate phosphatase from Escherichia coli B. J Bacteriol1980; 142: 60—68.
79.
Goldman RC, Bolling TJ, Kohlbrenner WE et al. Primary structure of CTP:CMP-3-deoxy-D-manno-octulosonate cytidylyltransferase (CMP-KDO synthetase) from Escherichia coli. J Biol Chem1986; 261: 15831—15835.
80.
Tipples G., McClarty G.Cloning and expression of the Chlamydia trachomatis gene for CTP synthetase . J Biol Chem1995; 270: 7908—7914.
81.
Goldman RC, Kohlbrenner WEMolecular cloning of the structural gene coding for CTP: CMP-3-deoxy-manno-octulosonate cytidylyltransferase from Escherichia coli K-12. J Bacteriol1985; 163: 256—261.
82.
Lin CH, Murray BW, Ollmann IR et al. Why is CMPketodeoxyoctonate highly unstable?Biochemistry1997; 36: 780—785.
83.
Kohlbrenner WE, Fesik SWDetermination of the anomeric specificity of the Escherichia coli CTP: CMP-3-deoxy-D-manno-octulosonate cytidylyltransferase by 13C NMR spectroscopy. J Biol Chem1985; 260: 14695—14700.
84.
Cosgrove DJAssembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol1997 ; 13: 171-201.
85.
Royo J., Gomez E., Hueros G.A maize homologue of the bacterial CMP-KDO synthetases: similar pathways operate in plants and bacteria for the activation of KDO prior to its incorporation into outer cellular envelopes. J Biol Chem2000; 275: 24993—24999.
86.
Hammond SM, Claesson A., Jansson AM et al. A new class of synthetic antibacterials acting on lipopolysaccharide biosynthesis. Nature1987; 327: 730—732.
87.
Goldman R., Kohlbrenner W., Lartey P. et al. Antibacterial agents specifically inhibiting lipopolysaccharide synthesis. Nature1987; 329: 162—164.
88.
Clementz T. , Raetz Crh.A gene coding for 3-deoxy-D-manno-octulosonic-acid transferase in Escherichia coli. Identification, mapping, cloning, and sequencing . J Biol Chem1991; 266: 9687—9696.
89.
Belunis CJ, Raetz Crh.Biosynthesis of endotoxins. Purification and catalytic properties of 3- deoxy-D-manno-octulosonic acid transferase from Escherichia coli. J Biol Chem1992; 267 : 9988—9997.
90.
Belunis CJ, Mdluli KE, Raetz Crh et al. A novel 3-deoxy-D-manno-octulosonic acid transferase from Chlamydia trachomatis required for expression of the genus-specific epitope. J Biol Chem1992; 267: 18702—18707.
91.
Mamat U., Baumann M., Schmidt G. et al. The genus-specific lipopolysaccharide epitope of Chlamydia is assembled in C. psittaci and C. trachomatis by glycosyltransferases of low homology. Mol Microbiol1993; 10: 935—941.
92.
Löbau S., Mamat U., Brabetz W. et al. Molecular cloning, sequence analysis, and functional characterization of the lipopolysaccharide biosynthetic gene kdtA encoding 3-deoxy-alpha- D-manno-octulosonic acid transferase of Chlamydia pneumoniae strain TW-183. Mol Microbiol1995; 18: 391—399.
93.
Bode CE, Brabetz W., Brade H.Cloning and characterization of 3-deoxy-D-manno-oct-2-ulosonic acid (Kdo) transferase genes (kdtA) from Acinetobacter baumannii and Acinetobacter haemolyticus . Eur J Biochem1998; 254: 404—412.
94.
Isobe T., White KA, Allen AG et al. Bordetella pertussis waaA encodes a monofunctional 2-keto-3-deoxy-D-manno-octulosonic acid transferase that can complement an Escherichia coli waaA mutation. J Bacteriol1999; 181: 2648—2651.
95.
Brabetz W., Schirmer C., Brade H.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 Bacteriol2000; 182: 4654—4657.
96.
White KA, Lin S., Cotter RJ et al. 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 Chem1999; 274: 31391—31400.
97.
Brabetz W., Müller-Loennies S., Brade H.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 Chem2000; 275: 34954—34962.
98.
Noah C., Brabetz W., Gronow S. et al. Cloning, sequencing, and functional analysis of three glycosyltransferases involved in the biosynthesis of the inner core region of Klebsiella pneumoniae lipopolysaccharide. J Endotoxin Res2001; 7: 25—33.
99.
Rund S., Lindner B., Brade H. et al. Structural analysis of the lipopolysaccharide from Chlamydophila psittaci strain 6BC. Eur J Biochem2000; 267: 5717—5726.
100.
Brabetz W. , Lindner B., Brade H.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 Biochem2000; 267: 5458—5465.
101.
White KA, Kaltashov IA, Cotter RJ et al. A mono-functional 3-deoxy-D-manno-octulosonic acid (Kdo) transferase and a Kdo kinase in extracts of Haemophilus influenzae. J Biol Chem1997; 272: 16555—16563.
102.
White KA, Raetz Crh.Complementation of a genomic disruption of the E. coli bifunctional Kdo transferase by the H. influenzae mono-functional Kdo transferase. FASEB J1998; 12: L44.
103.
Geerlof A. , Lewendon A., Shaw WVPurification and characterization of phosphopantetheine adenylyltransferase from Escherichia coli. J Biol Chem1999; 274: 27105—27111.
104.
Karow M., Georgopoulos C.Isolation and characterization of the Escherichia coli msbB gene, a multicopy suppressor of null mutations in the high-temperature requirement gene htrB . J Bacteriol1992; 174: 702—710.
105.
Brozek KA, Raetz Crh.Biosynthesis of lipid A in Escherichia coli. Acyl carrier protein-dependent incorporation of laurate and myristate. J Biol Chem1990; 265: 15410—15417.
106.
Clementz T., Bednarski JJ, Raetz Crh.Function of the htrB high temperature requirement gene of Escherichia coli in the acylation of lipid A: HtrB catalyzed incorporation of laurate. J Biol Chem1996; 271: 12095—12102.
107.
Clementz T., Zhou ZM, Raetz Crh.Function of the Escherichia coli msbB gene, a multicopy suppressor of htrB knockouts, in the acylation of lipid A — acylation by MsbB follows laurate incorporation by HtrB. J Biol Chem1997; 272: 10353—10360.
108.
Lehmann V. , Rupprecht E., Osborn MJIsolation of mutants conditionally blocked in the biosynthesis of the 3-deoxy-D-manno-octulosonic-acid—lipid-A part of lipopolysaccharides derived from Salmonella typhimurium. Eur J Biochem1977; 76: 41—49.
109.
Rick PD, Fung LW, Ho C. et al. Lipid A mutants of Salmonella typhimurium. Purification and characterization of a lipid A precursor produced by a mutant in 3-deoxy-D-mannooctulosonate-8-phosphate synthetase. J Biol Chem1977; 252: 4904—4912.
110.
Karow M., Fayet O., Cegielska A. et al. Isolation and characterization of the Escherichia coli htrB gene, whose product is essential for bacterial viability above 33 degrees C in rich media. J Bacteriol1991; 173: 741—750.
111.
Karow M., Fayet O., Georgopoulos C.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 Bacteriol1992; 174: 7407—7418.
112.
Sunshine M. , Gibson BW, Engstrom JJ et al. Mutation of the htrB gene in a virulent Salmonella typhimurium strain by intergeneric transduction: strain construction and phenotypic characterization. J Bacteriol1997; 179: 5521—5533.
113.
Wollenweber HW, Schlecht S., Luderitz O. et al. Fatty acid in lipopolysaccharides of Salmonella species grown at low temperature. Identification and position. Eur J Biochem1983; 130: 167—171.
114.
Carty SM, Sreekumar KR, Raetz Crh.A cold-induced, palmitoleoyl transferase involved in lipid A biosynthesis in Escherichia coli. FASEB J1997; 11: A1423.
115.
Carty SM, Sreekumar KR, Raetz Crh.Effect of cold shock on lipid A biosynthesis in Escherichia coli — induction at 12°C of an acyltransferase specific for palmitoleoyl-acyl carrier protein . J Biol Chem1999; 274: 9677—9685.
116.
Lee NG, Sunshine MG, Engstrom JJ et al. Mutation of the htrB locus of Haemophilus influenzae non-typable strain 2019 is associated with modifications of lipid A and phosphorylation of the lipo-oligosaccharide. J Biol Chem1995 ; 270: 27151—27159.
117.
Fleischmann RD, Adams MD, White O. et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science1995; 269: 496—512.
118.
Somerville JE, Cassiano L., Bainbridge B. et al. A novel Escherichia coli lipid A mutant that produces an anti-inflammatory lipopolysaccharide. J Clin Invest1996; 97: 359—365.
119.
Eidels L., Osborn MJLipopolysaccharide and aldoheptose biosynthesis in transketolase mutants of Salmonella typhimurium. Proc Natl Acad Sci USA1971; 68: 1673—1677.
120.
Kocsis B., Kontrohr T.Isolation of adenosine 5′-diphosphate-L-glycero-D-mannoheptose, the assumed substrate of heptose transferase(s), from Salmonella minnesota R595 and Shigella sonnei Re mutants. J Biol Chem1984; 259: 11858—11860.
121.
Brooke JS, Valvano MAMolecular cloning of the Haemophilus influenzae gmhA (lpcA) gene encoding a phosphoheptose isomerase required for lipooligosaccharide biosynthesis. J Bacteriol1996; 178: 3339—3341.
122.
Valvano MA , Marolda CL, Bittner M. et al. 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 Bacteriol2000; 182: 488—497.
123.
Coleman Jr WGThe rfaD gene codes for ADP-L-glycero-D-mannoheptose-6-epimerase. An enzyme required for lipopolysaccharide core biosynthesis. J Biol Chem1983; 258: 1985—1990.
124.
Kontrohr T. , Kocsis B.Isolation of adenosine 5′-diphosphate-D-glycero-D-mannoheptose. An intermediate in lipopolysaccharide biosynthesis of Shigella sonnei. J Biol Chem1981; 256: 7715—7718.
125.
Sirisena DM , Brozek KA, MacLachlan PR et al. The rfaC gene of Salmonella typhimurium. Cloning, sequencing, and enzymatic function in heptose transfer to lipopolysaccharide . J Biol Chem1992; 267: 18874—18884.
126.
Brabetz W. , Müller-Loennies S., Holst O. et al. 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 Biochem1997; 247: 716—724.
127.
Chen L., Coleman Jr WGCloning and characterization of the Escherichia coli K-12 rfa-2 (rfaC) gene, a gene required for lipopolysaccharide inner core synthesis. J Bacteriol1993; 175: 2534—2540.
128.
Kadrmas JL , Raetz Crh.Enzymatic synthesis of lipopolysaccharide in Escherichia coli — purification and properties of heptosyltransferase 1. J Biol Chem1998; 273: 2799—2807.
129.
Zamyatina A., Gronow S., Oertelt C. et al. 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 Engl2000; 39: 4150—4153.
130.
Gronow S., Oertelt C., Zamyatina A. et al. ADP-L-glycero-beta-D-manno-heptopyranose is the physiological sugar donor for heptosyltransferases I and II in Escherichia coli lipopolysaccharide core region biosynthesis. J Endotoxin Res2001; 7: In Press.
131.
Sirisena DM , MacLachlan PR, Liu SL et al. Molecular analysis of the rfaD gene, for heptose synthesis, and the rfaF gene, for heptose transfer, in lipopolysaccharide synthesis in Salmonella typhimurium. J Bacteriol1994; 175: 2379—2385.
132.
Schwan ET, Robertson BD, Brade H. et al. Gonococcal rfaF mutants express Rd2 chemotype LPS and do not enter epithelial host cells. Mol Microbiol1995; 15: 267—275.
133.
Bauer BA, Lumbley SR, Hansen EJCharacterization of a WaaF (RfaF) homolog expressed by Haemophilus ducreyi . Infect Immun1999; 67: 899—907.
134.
Nichols WA , Gibson BW, Melaugh W. et al. Identification of the ADP-L-glycero-D-manno-heptose-6-epimerase (rfaD) and heptosyltransferase II (rfaF) biosynthesis genes from nontypeable Haemophilus influenzae 2019. Infect Immun1997; 65: 1377—1386.
135.
Allen AG, Isobe T., Maskell DJIdentification and cloning of waaF (rfaF) from Bordetella pertussis and use to generate mutants of Bordetella spp. with deep rough lipopolysaccharide . J Bacteriol1998; 180: 35—40.
136.
de Kievit TR, Lam JSIsolation and characterization of two genes, waaC (rfaC) and waaF (rfaF), involved in Pseudomonas aeruginosa serotype O5 inner-core biosynthesis. J Bacteriol1997; 179: 3451—3457.
137.
Jennings MP , Bisercic M., Dunn Klr et al. 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 Pathog1995; 19: 391—407.
138.
Titarenko E., Lptosyl-2-transferase involved in Let al. Mutants of Ralstonia (Pseudomonas) solanacearum sensitive to antimicrobial peptides are altered in their lipopolysaccharide structure and are avirulent in tobacco. J Bacteriol1997; 179: 6699—6704.
139.
Gronow S., Brabetz W., Brade H.Comparative functional characterization in vitro of heptosyltransferase I (WaaC) and II (WaaF) from Escherichia coli. Eur J Biochem2000; 267: 6602—6611.
140.
Parker CT, Pradel E., Schnaitman CAIdentification and sequences of the lipopolysaccharide core biosynthetic genes rfaQ, rfaP, and rfaG of Escherichia coli K-12. J Bacteriol1992; 174: 930—934.
141.
Filiatrault MJ , Gibson BW, Schilling B. et al. Construction and characterization of Haemophilus ducreyi lipooligosaccharide (LOS) mutants defective in expression of heptosyltransferase III and beta-1,4-glucosyltransferase: identification of LOS glycoforms containing lactosamine repeats. Infect Immun2000; 68: 3352—3361.
142.
Parker CT, Kloser AW, Schnaitman CA et al. Role of the rfaG and rfaP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli K-12. J Bacteriol1992; 174: 2525—2538.
143.
Vaara M., Nurminen M.Outer membrane permeability barrier in Escherichia coli mutants that are defective in the late acyltransferases of lipid A biosynthesis. Antimicrob Agents Chemother1999; 43: 1459—1462.
144.
Mühlradt PFBiosynthesis of Salmonella lipopolysaccharide. Studies on the transfer of glucose, galactose, and phosphate to the core in a cell free system. Eur J Biochem1971; 18: 20—27.
145.
Vaara M.Antibiotic-supersusceptible mutants of Escherichia coli and Salmonella typhimurium . Antimicrob Agents Chemother1993; 37: 2255—2260.
146.
Mohan S., Kelly TM, Eveland SS et al. An Escherichia coli gene (fabZ) encoding (3R)-hydroxymyristoyl acyl carrier protein dehydrase. Relation to fabA and suppression of mutations in lipid A biosynthesis. J Biol Chem1994; 269: 32896—32903.
147.
Helander IM , Lindner B., Seydel U. et al. Defective biosynthesis of the lipid A component of temperature-sensitive firA (omsA) mutant of Escherichia coli . Eur J Biochem1993; 212: 363—369.
148.
Brozek KA, Bulawa CE, Raetz Crh.Biosynthesis of lipid A precursors in Escherichia coli. A membrane-bound enzyme that transfers a palmitoyl residue from a glycerophospholipid to lipid X. J Biol Chem1987; 262: 5170—5179.
149.
Sorensen PG , Lutkenhaus J., Young K. et al. Regulation of UDP-3-0-[R-3-hydroxymyristoyl]-N-acetylglucosamine deacetylase in Escherichia coli — the second enzymatic step of lipid A biosynthesis. J Biol Chem1996; 271: 25898—25905.
150.
Kloser A., Laird M., Deng M. et al. Modulations in lipid A and phospholipid biosynthesis pathways influence outer membrane protein assembly in Escherichia coli K-12. Mol Microbiol1998; 27: 1003—1008.
151.
Ogura T., Inoue K., Tatsuta T. et al. Balanced biosynthesis of major membrane components through regulated degradation of the committed enzyme of lipid A biosynthesis by the AAA protease FtsH (HflB) in Escherichia coli. Mol Microbiol1999; 31: 833—844.
152.
Tomoyasu T. , Yuki T., Morimura S. et al. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J Bacteriol1993; 175: 1344—1351.
153.
Tomoyasu T. , Gamer J., Bukau B. et al. Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J1995; 14: 2551—2560.
154.
Patel S., Latterich M.The AAA team: related ATPases with diverse functions. Trends Cell Biol1998; 8: 65—71.
155.
Deuerling E., Mogk A., Richter C. et al. The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol Microbiol1997; 23: 921—933.
156.
Van Alphen L, Lugtenberg B., Rietschel ET et al. Architecture of the outer membrane of Escherichia coli K12. Phase transitions of the bacteriophage K3 receptor complex. Eur J Biochem1979; 101: 571—579.
157.
Karow M., Georgopoulos C.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 Microbiol1993; 7: 69—79.
158.
Mdluli KE, Anthony LS, Baron GS et al. Serum-sensitive mutation of Francisella novicida: association with an ABC transporter gene. Microbiology1994; 140: 3309—3318.
159.
Storm DR, Rosenthal KS, Swanson PEPolymyxin and related peptide antibiotics. Annu Rev Biochem1977; 46: 723—763.
160.
Peterson AA , Hancock RE, McGroarty EJBinding of polycationic antibiotics and polyamines to lipopolysaccharides of Pseudomonas aeruginosa. J Bacteriol1985; 164: 1256—1261.
161.
Schindler PR, Teuber M.Action of polymyxin B on bacterial membranes: morphological changes in the cytoplasm and in the outer membrane of Salmonella typhimurium and Escherichia coli B. Antimicrob Agents Chemother1975; 8: 95—104.
162.
Vaara M., Vaara T., Sarvas M.Decreased binding of polymyxin by polymyxin-resistant mutants of Salmonella typhimurium. J Bacteriol1979; 139: 664—667.
163.
Vaara M., Vaara T., Jensen M. et al. Characterization of the lipopolysaccharide from the polymyxin-resistant pmrA mutants of Salmonella typhimurium. FEBS Lett1981; 129: 145—149.
164.
Helander IM , Kilpelainen I., Vaara M.Increased substitution of phosphate groups in lipopolysaccharides and lipid A of the polymyxin-resistant pmrA mutants of Salmonella typhimurium: a 31P-NMR study. Mol Microbiol1994; 11: 481—487.
165.
Nummila K. , Kilpelainen I., Zähringer U. et al. Lipopolysaccharides of polymyxin B-resistant mutants of Escherichia coli are extensively substituted by 2-aminoethyl pyrophosphate and contain aminoarabinose in lipid A. Mol Microbiol1995; 16: 271—278.
166.
Sidorczyk Z., Zähringer U., Rietschel ETChemical structure of the lipid A component of the lipopolysaccharide from a Proteus mirabilis Re-mutant. Eur J Biochem1983; 137: 15—22.
167.
Farrar WEAntimicrobial susceptibility of clinical isolates, synergistic effects, and beta-lactamases of Serratia. In: Von Graevenitz A, Rubin SJ. (eds) The Genus Serratia. Boca Raton: CRC Press, 1980; 121—138.
168.
Hase S., Rietschel ETThe chemical structure of the lipid A component of lipopolysaccharides from Chromobacterium violaceum NCTC 9694. Eur J Biochem1977; 75: 23—34.
169.
Gunn JS, Lim KB, Krueger J. et al. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol1998; 27: 1171—1182.
170.
Zhou Z., Lin S., Cotter RJ et al. Lipid A modifications characteristic of Salmonella typhimurium are induced by NH4VO3 in Escherichia coli K12. Detection of 4-amino-4-deoxy-L-arabinose, phosphoethanolamine and palmitate. J Biol Chem1999; 274: 18503—18514.
171.
Groisman EA , Kayser J., Soncini FCRegulation of polymyxin resistance and adaptation to low-Mg2+ environments. J Bacteriol1997 ; 179: 7040—7045.
172.
Fields PI, Groisman EA, Heffron F.A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science1989; 243: 1059—1062.
Garcia Vescovi E, Soncini FC, Groisman EAThe role of the PhoP/PhoQ regulon in Salmonella virulence. Res Microbiol1994; 145: 473—480.
175.
Soncini FC , Groisman EATwo-component regulatory systems can interact to process multiple environmental signals. J Bacteriol1996; 178: 6796—6801.
176.
Ernst RK, Guina T., Miller SIHow intracellular bacteria survive: surface modifications that promote resistance to host innate immune responses. J Infect Dis1999; 179: S326—S330.
177.
Garcia Vescovi E., Soncini FC, Groisman EAMg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell1996 ; 84: 165—174.
178.
Castelli ME, Garcia Vescovi E., Soncini FCThe phosphatase activity is the target for Mg2+ regulation of the sensor protein PhoQ in Salmonella. J Biol Chem2000; 275: 22948—22954.
179.
Gunn JS, Hohmann EL, Miller SITranscriptional regulation of Salmonella virulence: a PhoQ periplasmic domain mutation results in increased net phosphotransfer to PhoP. J Bacteriol1996; 178: 6369—6373.
180.
Guo L., Lim KB, Gunn JS et al. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science1997; 276: 250—253.
181.
Guo L., Lim KB, Poduje CM et al. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell1998; 95: 189—198.
182.
Gunn JS, Ernst RK, McCoy AJ et al. Constitutive mutations of the Salmonella enterica serovar Typhimurium transcriptional virulence regulator phoP. Infect Immun2000; 68: 3758—3762.
183.
Roland KL, Martin LE, Esther CR et al. Spontaneous pmrA mutants of Salmonella typhimurium LT2 define a new two-component regulatory system with a possible role in virulence. J Bacteriol1993; 175: 4154—4164.
184.
Mäkelä PH, Sarvas M., Calcagno S. et al. Isolation and characterization of polymyxin-resistant mutants of Salmonella. FEMS Microbiol Lett1978; 3: 323—326.
185.
Kox LF, Wosten MM, Groisman EAA small protein that mediates the activation of a two-component system by another two-component system. EMBO J2000; 19: 1861—1872.
186.
Soncini FC , Garcia Vescovi E., Solomon F. et al. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes . J Bacteriol1996; 178: 5092—5099.
187.
Groisman EAThe ins and outs of virulence gene expression: Mg2+ as a regulatory signal. Bioessays1998 ; 20: 96—101.
188.
Zhou Z., Ribeiro AA, Raetz CRHigh-resolution NMR spectroscopy of lipid A molecules containing 4-amino-4-deoxy-L-arabinose and phosphoethanolamine substituents. Different attachment sites on lipid A molecules from NH4VO3-treated Escherichia coli versus kdsA mutants of Salmonella typhimurium. J Biol Chem2000; 275: 13542—13551.
189.
Levinson G. , Gutman GASlipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol1987; 4: 203—221.
190.
Hood DW, Deadman ME, Jennings MP et al. DNA repeats identify novel virulence genes in Haemophilus influenzae . Proc Natl Acad Sci USA1996; 93: 11121—11125.
191.
Jarosik GP , Hansen EJIdentification of a new locus involved in expression of Haemophilus influenzae type b lipooligosaccharide. Infect Immun1994; 62: 4861—4867.
192.
High NJ, Jennings MP, Moxon ERTandem repeats of the tetramer 5′-CAAT-3′ present in lic2A are required for phase variation but not lipopolysaccharide biosynthesis in Haemophilus influenzae. Mol Microbiol1996; 20: 165—174.
193.
Weiser JN, Love JM, Moxon ERThe molecular mechanism of phase variation of H. influenzae lipopolysaccharide . Cell1989; 59: 657—665.
194.
Jonsson AB , Nyberg G., Normark S.Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J1991; 10: 477—488.
195.
Yang QL, Gotschlich ECVariation of gonococcal lipooligosaccharide structure is due to alterations in poly-G tracts in lgt genes encoding glycosyl transferases. J Exp Med1996; 183: 323—327.
196.
Jennings MP , Srikhanta YN, Moxon ER et al. The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. Microbiology1999; 145: 3013—3021.
197.
Danaher RJ , Levin JC, Arking D. et al. Genetic basis of Neisseria gonorrhoeae lipooligosaccharide antigenic variation. J Bacteriol1995; 177: 7275—7279.
198.
Burch CL, Danaher RJ, Stein DCAntigenic variation in Neisseria gonorrhoeae: production of multiple lipooligosaccharides . J Bacteriol1997; 179: 982—986.
