Export of O-specific lipopolysaccharide

Frontiers in Bioscience

Volumn 8, Issue SUPPL., 2003, Pages

  Valvano, Miguel A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

ABC transporter; Flippase; Ligase; O antigen; Polymerization; Review; Translocation; Undecaprenol phosphate

Indexed keywords

ABC TRANSPORTER; GLYCOLIPID; ISOPRENOID PHOSPHATE SUGAR; LIPOPOLYSACCHARIDE; O ANTIGEN; POLYSACCHARIDE; SYNTHETASE; BACTERIAL PROTEIN;

BIOGENESIS; CELL MEMBRANE; CELL SURFACE; CYTOPLASM; GRAM NEGATIVE BACTERIUM; NONHUMAN; REVIEW; ACTIVE TRANSPORT; AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN CONFORMATION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; LIPOPOLYSACCHARIDES; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; O ANTIGENS; PROTEIN CONFORMATION;

EID: 1542673183     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/1079     Document Type: Review

References (172)

1. Nikaido, H: Outer Membrane. In: Escherichia coli and Salmonella: Cellular and molecular biology. Eds: 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, American Society for Microbiology Press, Washington, D. C. 29-47 (1996)
2. Whitfield, C & M A Valvano: Biosynthesis and expression of cell-surface polysaccharides in gram-negative bacteria. Adv Microb Physiol 35: 135-246 (1993)
3. Raetz, C R H: Bacterial lipopolysaccharides: a remarkable family of bioactive molecules. In: Escherichia coli and Salmonella: cellular and molecular biology. Eds: Neidhardt F C, Curtiss III R, Ingraham J L, Lin E C C, Low K B, Magasanik B, Reznikoff W S, Riley M, Schaechter M & Umbarger H E, American Society for Microbiology Press, Washington, D. C. 1035-1063. (1996)
4. Heinrichs, D E, M A Valvano & C Whitfield: Biosynthesis and genetics of lipopolysaccharide core. In: Endotoxin in health and disease. Eds: Brade H, Morrison D C, Vogel S & Opal S, Marcel Dekker, Inc., New York, N. Y. 305-330 (1999)
5. Hancock, R E W, D N Karunaratne & C Bernegger-Egli: Molecular organization and structural role of outer membrane macromolecules. In: Bacterial cell wall. Vol. 27. Eds: Ghuysen J M & Hackenbeck R, Elsevier Science, Amsterdam, New York. 263-79 (1994)
6. Ferguson, A D, W Welte, E Hofmann, B Lindner, O Holst, J W Coulton & K Diederichs: A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure Fold Des 8: 585-592. (2000)
7. Nikaido, H & M Vaara: Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49: 1-32. (1985)
8. Nikaido, H: Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264: 382-8 (1994)
9. Heinrichs, D E, J A Yethon & C Whitfield: Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol 30: 221-232. (1998)
10. Whitfield, C: Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol 3: 178-185. (1995)
11. Rick, P D & R P Silver: Enterobacterial common antigen and capsular polysaccharides. In: Escherichia coli and Salmonella: Cellular and molecular biology. Eds: Neidhardt F C, Curtiss III R, Ingraham J L, Lin E C C, Low K B, Magasanik B, Reznikoff W S, Riley M, Schaechter M & Umbarger H E, American Society for Microbiology Press, Washington, D. C. 104-122 (1996)
12. Brooke, J S & M A Valvano: Biosynthesis of inner core lipopolysaccharide in enteric bacteria identification and characterization of a conserved phosphoheptose isomerase. J Biol Chem 271: 3608-3614. (1996)
13. Valvano, M A: Biosynthesis and genetics of ADP-heptose. J Endotoxin Res 5: 90-95. (1999)
14. Valvano, M A, C L Marolda, M Bittner, M Glaskin-Clay, T L Simon & J D Klena: The rfaE gene from Escherichia coli encodes a bifunctional protein involved in the biosynthesis of the lipopolysaccharide core precursor ADP-L-glycero-D-manno-heptose. J Bacteriol 182: 488-497. (2000)
15. Schnaitman, C A & J D Klena: Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 57: 655-682 (1993)
16. Keenleyside, W J & C Whitfield: Genetics and biosynthesis of lipopolysaccharide O-antigens. In: Endotoxin in Health and Disease. Eds: Brade H, Morrison D C, Vogel S & Opal S, Marcel Dekker, Inc., New York 331-358 (1999)
17. Reeves, P R, M Hobbs, M A Valvano, M Skurnik, C Whitfield, D Coplin, N Kido, J Klena, D Maskell, C R H Raetz & P D Rick: Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol 4: 495-503 (1996)
18. Tamaki, S, T Sato & M Matsuhashi: Role of lipopolysaccharides in antibiotic resistance and bacteriophage adsorption of Escherichia coli K-12. J Bacteriol 105: 968-975. (1971)
19. Curtiss, R, J Charamella, D R Stallions & J A Mays: Parental functions during conjugation. Bacteriol Rev 32: 320-348. (1968)
20. Havekes, L M, B J J Lugtenberg & W P M Hoekstra: Conjugation deficient E. coli K-12 F- mutants with heptose-less lipopolysaccharide. Mol Gen Genet 146: 43-50. (1976)
21. Sherburne, C & D E Taylor: Effect of lipopolysaccharide mutations on recipient ability of Salmonella typhimurium for incompatibility group H plasmids. J Bacteriol 179: 952-955 (1997)
22. van Alphen, W, B Eugtenberg & W Berendsen: Heptose-deficient mutants of Escherichia coli K12 deficient in up to three major outer membrane proteins. Mol Gen Genet 147: 263-269 (1976)
23. Vakharia, H & R Misra: A genetic approach for analysing surface-exposed regions of the OmpC protein of Escherichia coli K-12. Mol Microbiol 19: 881-889 (1996)
24. Verkleij, A J, E J Lugtenberg & P H Ververgaert: Freeze etch morphology of outer membrane mutants of Escherichia coli K12. Biochim Biophys Acta 426: 581-586. (1976)
25. Bayer, M E, J Koplow & H Goldfine: Alterations in envelope structure of heptose-deficient mutants of Escherichia coli as revealed by freeze-etching. Proc Natl Acad Sci USA 72: 5145-5149. (1975)
26. Koplow, J & H Goldfine: Alterations in the outer membrane of the cell envelope of heptose-deficient mutants of Escherichia coli. J Bacteriol 117: 527-543. (1974)
27. Fralick, J A & L L Burns-Keliher: Additive effect of tolC and rfa mutations on the hydrophobic barrier of the outer membrane of Escherichia coli K-12. J Bacteriol 176: 6404-6406 (1994)
28. Koronakis, V, E Koronakis, J Li & K Stauffer: Structure of TolC, the outer membrane component of the bacterial type I efflux system, derived from two-dimensional crystals. Mol Microbiol 23: 617-626. (1997)
29. Yethon, J A, E Vinogradov, M B Perry & C Whitfield: Mutation of the lipopolysaccharide core glycosyltransferase encoded by waaG destabilizes the outer membrane of Escherichia coli by interfering with core phosphorylation. J Bacteriol 182: 5620-5623. (2000)
30. Yethon, J A & C Whitfield: Purification and characterization of WaaP from Escherichia coli, a lipopolysaccharide kinase essential for outer membrane stability. J Biol Chem 276: 5498-5504. (2001)
31. Riley, L W, L N Junio, E B Libaek & G K Schoolnik: Plasmid-encoded expression of lipopolysaccharide O-antigenic polysaccharide in enteropathogenic Escherichia coli. Infect Immun 55: 2052-2056 (1987)
32. Kopecko, D J, O Washington & S B Formal: Genetic and physical evidence for plasmid control of Shigella sound form I cell surface antigen. Infect Immun 29: 207-214 (1980)
33. Sturm, S, B Jann, K Jann, P Fortnagel & K N Timmis: Genetic and biochemical analysis of Shigella dysenteriae 1 O antigen polysaccharide biosynthesis in Escherichia coli K-12: 9 kb plasmid of S. dysenteriae 1 determines addition of a galactose residue to the lipopolysaccharide core. Microb Pathog 1: 299-306. (1986)
34. Keenleyside, W J & C Whitfield: Lateral transfer of rfb genes: a mobilizable ColE1-type plasmid carries the rfbO:54 (O:54 antigen biosynthesis) gene cluster from Salmonella enterica serovar Borreze. J Bacteriol 177: 5247-5253 (1995)
35. Whitfield, C, P A Amor & R Koplin: 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 23: 629-638. (1997)
36. Daniels, C & R Morona: Analysis of Shigella flexneri wzz (Rol) function by mutagenesis and cross-linking: Wzz is able to oligomerize. Mol Microbiol 34: 181-194. (1999)
37. Morona, R, L van den Bosch & P A Manning: Molecular, genetic, and topological characterization of O-antigen chain length regulation in Shigella flexneri. J Bacteriol 177: 1059-1068. (1995)
38. Raetz, C R H & C Whitfield: Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700. (2002)
39. Whitfield, C & I S Roberts: Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol Microbiol 31: 1307-1319. (1999)
40. Valvano, M A, P Messner & P Kosma: Novel pathways for biosynthesis of nucleotide-activated glyceromanno-heptose precursors of bacterial glycoproteins and cell surface polysaccharides. Microbiology 148: 1979-1989. (2002)
41. Anderson, M S, S S Eveland & N P Price: Conserved cytoplasmic motifs that distinguish sub-groups of the polyprenol phosphate:N-acetylhexosamine-1- phosphate transferase family. FEMS Microbiol Lett 191: 169-175. (2000)
42. Dal Nogare, A R & M A Lehrman: Conserved sequences in enzymes of the UDP-GlcNAc/MurNAc family are essential in hamster UDP-GlcNAc:dolichol-P GlcNAc-1-P transferase. Glycobiology 8: 625-632. (1988)
43. Lehrman, M A: A family of UDP-GlcNAc/MurNAc: polyisoprenol-P GlcNAc/MurNAc-1-P transferases. Glycobiology 4: 768-771. (1994)
44. Rick, P D, G L Hubbard & K Barr: Role of the rfe gene in the synthesis of the O8 antigen in Escherichia coli K-12. J Bacteriol 176: 2877-84 (1994)
45. Alexander, D C & M A Valvano: Role of the rfe gene in the biosynthesis of the Escherichia coli O7-specific lipopolysaccharide and other O-specific polysaccharides containing N-acetylglucosamine. J Bacteriol 176: 7079-7084 (1994)
46. Heifetz, A, R W Keenan & A D Elbein: Mechanism of action of tunicamycin on the UDP-GlcNAc:dolichyl phosphate GlcNAc-1-phosphate transferase. Biochemistry 18: 2186-2192. (1979)
47. Brandish, P, K Kimura, M Inukai, R Southgate, J Lonsdale & T Bugg: Modes of action of tunicamycin, liposidomycin B, and mureidomycin A: inhibition of phospho-N-acetylmuramyl-pentapeptide translocase from Escherichia coli. Antimicrob Agents Chemother 40: 1640-1644 (1996)
48. Mahoney, W C & D Duksin: Biological activities of the two major components of tunicamycin. J Biol Chem 254: 6572-6576. (1979)
49. Meier-Dieter, U, R Starman, K Barr, H Mayer & P D Rick: Biosynthesis of enterobacterial common antigen in Escherichia coli. J Biol Chem 265: 13490-13497. (1990)
50. Klena, J D & C A Schnaitman: Function of the rfb gene cluster and the rfe gene in the synthesis of O antigen by Shigella dysenteriae 1. Mol Microbiol 9: 393-402 (1993)
51. Yao, Z & M A Valvano: Genetic analysis of the O-specific lipopolysaccharide biosynthesis region (rfb) of Escherichia coli K-12 W3110: identification of genes that confer group 6 specificity to Shigella flexneri serotypes Y and 4a. J Bacteriol 176: 4133-4143 (1994)
52. Wang, L, S Huskic, A Cisterne, D Rothemund & P R Reeves: The O-antigen gene cluster of Escherichia coli O55:H7 and identification of a new UDP-GlcNAc C4 epimerase gene. J Bacteriol 184: 2620-2620. (2002)
53. Zhang, L, J Radziejewska-Lebrecht, D Krajewska-Pietrasik, P Toivanen & M Skurnik: Molecular and chemical characterization of the lipopolysaccharide O-antigen and its role in the virulence of Yersinia enterocolitica serotype O:8. Mol Microbiol 23: 63-76. (1997)
54. Wang, L & P R Reeves: Organization of the Escherichia coli O157 O antigen cluster and identification of its specific genes. Infect Immun 66: 3545-3551 (1998)
55. Clarke, B R, D Bronner, W J Keenleyside, W B Severn, J C Richards & C Whitfield: Role of Rfe and RfbF in the initiation of biosynthesis of D-galactan I, the lipopolysaccharide O antigen from Klebsiella pneumoniae serotype O1. J Bacteriol 177: 5411-5418 (1995)
56. Szabo, M, D Bronner & C Whitfield: Relationships between rfb gene clusters required for biosynthesis of identical D-galactose-containing O antigens in Klebsiella pneumoniae serotype O1 and Serratia marcescens serotype O16. Journal of Bacteriology 177: 1544-53 (1995)
57. Keenleyside, W J, M Perry, L Maclean, C Poppe & C Whitfield: A plasmid-encoded rfbO:54 gene cluster is required for biosynthesis of the O:54 antigen in Salmonella enterica serovar Borreze. Mol Microbiol 11: 437-448. (1994)
58. Rocchetta, H L, L L Burrows, J C Pacan & J S Lam: 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 28: 1103-1119. (1998)
59. Skurnik, M: Molecular genetics of Yersinia lipopolysaccharide. In: Genetics of bacterial polysaccharides. Eds: Goldberg J B, CRC Press, Boca Raton, FL. 23-51 (1999)
60. Ikeda, M, M Wachi, H K Jung, F Ishino & M Matsuhashi: The Escherichia coli mraY gene encoding UDP-N-acetylmuramoyl-pentapeptide: undecaprenylphosphate phospho-N-acetylmuramoyl-pentapeptide transferase. J Bacteriol 173: 1021-1026. (1991)
61. Bouhss, A, D Mengin-Lecreulx, D Le Beller & J Van Heijenoort: Topological analysis of the MraY protein catalysing the first membrane step of peptidoglycan synthesis. Mol Microbiol 34: 576-585. (1999)
62. Amer, A O & M A Valvano: Conserved aspartic acids are essential for the enzymatic activity of the WecA protein initiating the biosynthesis of O-specific lipopolysaccharide and enterobacterial common antigen in Escherichia coli. Microbiology 148: 571-582. (2002)
63. Amer, A O & M A Valvano: The N-terminal region of the Escherichia coli WecA (Rfe) protein containing three predicted transmembrane helices is required for function but not for membrane insertion. J Bacteriol 182: 498-503. (2000)
64. Amer, A O & M A Valvano: Conserved amino acid residues found in a predicted cytosolic domain of WecA (UDP-N-acetyl glucosamine:undecaprenol- phosphate N-acetylglucosamine-1-phosphate transferase) are implicated in the recognition of UDP-N-acetylglucosamine. Microbiology 147: 3015-3025. (2001)
65. Allingham, J S, P A Pribil & D B Haniford: All three residues of the Tn10 transposase DDE catalytic triad function in divalent metal ion binding. J Mol Biol 289: 1195-1206. (1999)
66. Sekine, S, A Shimada, O Nureki, J Cavarelli, D Moras, D G Vassylyev & S Yokoyama: Crucial Role of the HIGH-loop Lysine for the Catalytic Activity of Arginyl-tRNA Synthetase. J Biol Chem 276: 3723-3726 (2001)
67. Jiang, X M, B Neal, F Santiago, S J Lee, L K Romana & P R Reeves: Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2) Mol Microbiol 5: 695-713. (1991)
68. Arakawa, Y, R Wacharotayankun, T Nagatsula, H Ito, N Kato & M Ohta: Genomic organization of the Klebsiella pneumoniae cps region responsible for serotype K2 capsular polysaccharide synthesis in the virulent strain Chedid. J Bacteriol 177: 1788-1796. (1995)
69. Bugert, P & K Geider: Molecular analysis of the ams operon required for exopolysaccharide synthesis in Erwinia amylovora. Mol Microbiol 15: 917-933 (1995)
70. Stevenson, G, K Andrianopoulos, M Hobbs & P R Reeves: Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J Bacteriol 178: 4885-4893 (1996)
71. Katzen, F, D U Ferreiro, C G Oddo, M V Ielmini, A Becker, A Puhler & L Ielpi: Xanthomonas campestris pv. campestris gum mutants: effects on xanthan biosynthesis and plant virulence. J Bacteriol 180: 1607-1617. (1998)
72. Reuber, T L & G C Walker: Biosynthesis of succinoglycan, a symbolically important exopolysaccharide of Rhizobium meliloti. Cell 74: 269-280. (1993)
73. Wang, L, D Liu & P R Reeves: 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 178: 2598-2604. (1996)
74. Campbell, J A, G J Davies, V Bulone & B Henrissat: A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem J 326: 929-939. (1997)
75. McGrath, B C & M J Osborn: Localization of the terminal steps of O-antigen synthesis in Salmonella typhimurium. J Bacteriol 173: 649-654 (1991)
76. Mulford, C A & M J Osborn: An intermediate step in translocation of lipopolysaccharide to the outer membrane of Salmonella typhimurium. Proc Natl Acad Sci U S A 80: 1159-1163. (1983)
77. Marino, P A, B C McGrath & M J Osborn: Energy dependence of O-antigen synthesis in Salmonella typhimurium. J Bacteriol 173: 3128-3133 (1991)
78. Bronner, D, B R Clarke & C Whitfield: Identification of an ATP-binding cassette transport system required for translocation of lipopolysaccharide O-antigen side-chains across the cytoplasmic membrane of Klebsiella pneumoniae serotype O1. Mol Microbiol 14: 505-519. (1994)
79. Clarke, B R & C Whitfield: Molecular cloning of the rfb region of Klebsiella pneumoniae serotype O1:K20: the rfb gene cluster is responsible for synthesis of the D-galactan I O polysaccharide. J Bacteriol 174: 4614-21 (1992)
80. Bugg, T D & P E Brandish: From peptidoglycan to glycoproteins: common features of lipid-linked oligosaccharide biosynthesis. FEMS Microbiol Lett 119: 255-262. (1994)
81. Burda, P & M Aebi: The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta 1426: 239-257. (1999)
82. Hirschberg, C B & M D Snider: Topography of glycosylation in the rough endoplasmic reticulum and Golgi apparatus. Annu Rev Biochem 54: 63-87 (1987)
83. McCloskey, M A & F A Troy: Paramagnetic isoprenoid carrier lipids. 1. Chemical synthesis and incorporation into model membranes. Biochemistry 19: 2061-2066 (1980)
84. Hanover, J A & W J Lennarz: The topological orientation of N,N′-diacetylchitobiosylpyrophosphoryldolichol in artificial and natural membranes. J Biol Chem 254: 9237-9246 (1978)
85. Rush, J S & C J Waechter: Transmembrane movement of a water-soluble analogue of mannosylphosphoryldolichol is mediated by an endoplasmic reticulum protein. J Cell Biol 130: 529-536 (1995)
86. Rush, J S, K van Leyen, O Ouerfelli, B Wolucka & C J Waechter: Transbilayer movement of Glc-P-dolichol and its function as a glucosyl donor: protein-mediated transport of a water-soluble analog into sealed ER vesicles from pig brain. Glycobiology 8: 1195-1205. (1998)
87. Liu, D, R A Cole & P R Reeves: An O-antigen processing function for Wzx (RfbX): A promising candidate for O-unit flippase. J Bacteriol 178: 2102-2107. (1996)
88. Paulsen, I T, A M Beness & M H Saier: Computer-based analyses of the protein constituents of transport systems catalysing export of complex carbohydrates in bacteria. Microbiology 143: 2685-2699 (1997)
89. Marolda, C L, M F Feldman & M A Valvano: Genetic organization of the O7-specific lipopolysaccharide biosynthesis cluster of Escherichia coli VW187 (O7:K1) Microbiology 145: 2485-2496. (1999)
90. Feldman, M F, C L Marolda, M A Monteiro, M B Perry, A J Parodi & M A Valvano: The activity of a putative polyisoprenol-linked sugar translocase(Wzx) involved in Escherichia coil O antigen assembly is independent of the chemical structure of the O repeat. J Biol Chem 274: 35129-35138. (1999)
91. Bray, D & P W Robbins: The direction of chain growth in Salmonella anatum O-antigen biosynthesis. Biochem Biophys Res Commun 28: 334-339. (1967)
92. Robbins, P W, D Bray, B M Dankert & A Wright: Direction of chain growth in polysaccharide synthesis. Science 158: 1536-142. (1967)
93. Collins, L V, S Attridge & J Hackett: Mutations at rfc or pmi attenuate Salmonella typhimurium virulence for mice. Infection & Immunity 59: 1079-85 (1991)
94. Jann, K & B Jann: Structure and biosynthesis of O antigens. In: Handbook of Endotoxin vol 1: Chemistry of endotoxin. Eds: Rietschel E T, Elsevier Science Publishers, Amsterdam, The Netherlands 138-186 (1984)
95. Morona, R, M Mavris, A Fallarino & P A Manning: Characterization of the rfc region of Shigella flexneri. J Bacteriol 176: 733-747. (1994)
96. Daniels, C, C Vindurampulle & R Morona: Overexpression and topology of the Shigella flexneri O-antigen polymerase (Rfc/Wzy) Mol Microbiol 28: 1211-1222. (1998)
97. Batchelor, R A, G E Haraguchi, R A Hull & S I Hull: Regulation by a novel protein of the bimodal distribution of lipopolysaccharide in the outer membrane of Escherichia coli. J Bacteriol 173: 5699-5704. (1991)
98. Bastin, D A, G Stevenson, P K Brown, A Haase & P R Reeves: 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 7: 725-734. (1993)
99. Rocchetta, H L, L L Burrows & J S Lam: Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 63: 523-553. (1999)
100. Stevenson, G, A Kessler & P R Reeves: A plasmid-borne O-antigen chain length determinant and its relationship to other chain length determinants. FEMS Microbiol Lett 125: 23-30. (1995)
101. Morona, R, L Van Den Bosch & C Daniels: Evaluation of Wzz/MPA1/MPA2 proteins based on the presence of coiled-coil regions. Microbiology 146: 1-4. (2000)
102. Franco, A V, D Liu & P R Reeves: The wzz (cld) protein in Escherichia coli: amino acid sequence variation determines O-antigen chain length specificity. J Bacteriol 180: 2670-2675. (1998)
103. Helenius, J, D T Ng, C L Marolda, P Walter, M A Valvano & M Aebi: Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature 415: 447-450. (2002)
104. Ng, D T W, E D Spear & P Walter: The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J Cell Biol 150: 77-88 (2000)
105. Sprang, H, P van der Sluijs & G van Meer: How proteins move lipids and lipid move proteins. Nat Rev Mol Cell Biol 2: 504-513. (2001)
106. Davidson, E A & D C Gowda: Glycobiology of Plasmodium falciparum. Biochimie 83: 601-604. (2001)
107. Süsskind, M, L Brade, H Brade & O Holst: Identification of a novel heptoglycan of a1®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. (1998)
108. Kido, N, V I Torgov, T Sugiyama, K Uchiya, H Sugihara, T Komatsu, N Kato & K Jann: Expression of the O9 polysaccharide of Escherichia coli: sequencing of the E. coli O9 rfb gene cluster, characterization of mannosyl transferases, and evidence for an ATP-binding cassette transport system. J Bacteriol 177: 2178-2187. (1995)
109. Guan, S, A J Clarke & C Whitfield: Functional analysis of the galactosyltransferases required for biosynthesis of D-galactan I, a component of the lipopolysaccharide O1 antigen of Klebsiella pneumoniae. J Bacteriol 183: 3318-3327. (2001)
110. Weisgerber, C & K Jann: Glucosyldiphosphoundecaprenol, the mannose acceptor in the synthesis of the O9 antigen of Escherichia coli. Biosynthesis and characterization. Eur J Biochem 127: 165-168. (1982)
111. Kido, N & H Kobayashi: A single amino acid substitution in a mannosyltransferase, WbdA, converts the Escherichia coli O9 polysaccharide into O9a: generation of a new O-serotype group. J Bacteriol 182: 2567-2573. (2000)
112. Kido, N, T Sugiyama, T Yokochi, H Kobayashi & Y Okawa: Synthesis of Escherichia coli O9a polysaccharide requires the participation of two domains of WbdA, a mannosyltransferase encoded within the wb* gene cluster. Mol Microbiol 27: 1213-1221. (1998)
113. Reizer, J, A Reizer & M H Saier, Jr.: A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Protein Sci 1: 1326-1332. (1992)
114. Jansson, P E, J Lonngren, G Widmalm, K Leontein, K Slettengren, S B Svenson, G Wrangsell, A Dell & P R Tiller: Structural studies of the O-antigen polysaccharides of Klebsiella O5 and Escherichia coli O8. Carbohydr Res 145: 59-66. (1985)
115. Olsthoorn, M M, J Haverkamp & J E Thomas-Oates: Mass spectrometric analysis of Klebsiella pneumoniae ssp. pneumoniae rough strain R20 (O1-: K20-) lipopolysaccharide preparations: identification of novel core oligosaccharide components and three 3-deoxy-D-manno-oct-2-ulopyranosonic artifacts. J Mass Spectrom 34: 622-36 (1999)
116. Vinogradov, E, E Frirdich, L L MacLean, M B Perry, B O Petersen, J O Duus & C Whitfield: Structures of Lipopolysaccharides from Klebsiella pneumoniae. Elucidation of the structure of the linkage region between core and polysaccharide O chain and identification of the residues at the non-reducing termini of the O chains. J Biol Chem 277: 25070-25081. (2002)
117. Vinogradov, E, M S Peppler & M B Perry: The structure of the nonreducing terminal groups in the O-specific polysaccharides from two strains of Bordetella bronchiseptica. Eur J Biochem 267: 7230-7237. (2000)
118. Preston, A, A G Allen, J Cadisch, R Thomas, K Stevens, C M Churcher, K L Badcock, J Parkhill, B Barrell & D J Maskell: Genetic basis for lipopolysaccharide O-antigen biosynthesis in bordetellae. Infect Immun 67: 3763-3767. (1999)
119. Keenleyside, W J & C Whitfield: A novel pathway for O-polysaccharide biosynthesis in Salmonella enterica serovar Borreze. J Biol Chem 271: 28581-28592. (1996)
120. Keenleyside, W J, A J Clarke & C Whitfield: Identification of residues involved in catalytic activity of the inverting glycosyl transferase WbbE from Salmonella enterica serovar borreze. J Bacteriol 183: 77-85. (2001)
121. DeAngelis, P L: Microbial glycosaminoglycan glycosyltransferases. Glycobiology 12: 9R-16R. (2002)
122. DeAngelis, P L: Hyaluronan synthases: fascinating glycosyltransferases from vertebrates, bacterial pathogens, and algal viruses. Cell Mol Life Sci 56: 670-682. (1999)
123. Cartee, R T, W T Forsee, J S Schutzbach & J Yother: Mechanism of type 3 capsular polysaccharide synthesis in Streptococcus pneumoniae. J Biol Chem 275: 3907-3914. (2000)
124. Forsee, W T, R T Cartee & J Yother: Biosynthesis of type 3 capsular polysaccharide in Streptococcus pneumoniae. Enzymatic chain release by an abortive translocation process. J Biol Chem 275: 25972-25978. (2000)
125. Klena, J D, R S Ashford & C A Schnaitman: Role of the Escherichia coli K-12 rfa genes and the rfp gene of Shigella dysenteriae 1 in generation of lipopolysaccharide core heterogeneity and attachment of O antigen. J Bacteriol 174: 7297-7307. (1992)
126. Zhou, Z, K A White, A Polissi, C Georgopoulos & C R Raetz: Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem 273: 12466-12475. (1998)
127. Doerrler, W T, M C Reedy & C R H Raetz: An Escherichia coli mutant defective in lipid export. J Biol Chem 276: 11461-11464. (2001)
128. Chang, G & C B Roth: Structure of MsbA from E. coli: A Homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science 293: 1793-1800. (2001)
129. Doerrler, W T & C R H Raetz: ATPase activity of the MsbA lipid flippase of Escherichia coli. J Biol Chem 277: 36697-36705. (2002)
130. Boucher, Y & W Ford Doolittle: The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol Microbiol 37: 703-716. (2000)
131. White, R H: Biosynthesis of isoprenoids in bacteria. In: Escherichia coli and Salmonella: cellular and molecular biology. Eds: Neidhardt F C, Curtiss III R, Ingraham J L, Lin E C C, Low K B, Magasanik B, Reznikoff W S, Riley M, Schaechter M & Umbarger H E, American Society for Microbiology Press, Washington, D. C. 637-641. (1996)
132. Shimizu, N, T Koyama & K Ogura: Molecular cloning, expression, and purification of undecaprenyl diphosphate synthase. No sequence similarity between E-and Z-prenyl diphosphate synthases. J Biol. Chem 273: 19476-19481. (1998)
133. Apfel, C M, B Takacs, M Fountoulakis, M Stieger & W Keck: Use of genomics to identify bacterial undecaprenyl pyrophosphate synthetase: cloning, expression, and characterization of the essential uppS gene. J Bacteriol 181: 483-492. (1999)
134. Goldman, R & J L Strominger: Purification and properties of C 55 -isoprenylpyrophosphate phosphatase from Micrococcus lysodeikticus. J Biol Chem 247: 5116-5122. (1972)
135. Storm, D R & J L Strominger: Complex formation between bacitracin peptides and isoprenyl pyrophosphates. The specificity of lipid-peptide interactions. J Biol. Chem 248: 3940-3945. (1973)
136. Stone, K J & J L Strominger: Mechanism of action of bacitracin: complexation with metal ion and C 55-isoprenyl pyrophosphate. Proc Natl Acad Sci USA 68: 3223-3227. (1971)
137. Harkness, R E & V Braun: Colicin M inhibits peptidoglycan biosynthesis by interfering with lipid carrier recycling. J Biol Chem 264: 6177-6182. (1989)
138. Harkness, R E & V Braun: Inhibition of lipopolysaccharide O-antigen synthesis by colicin M. J Biol Chem 264: 14716-22 (1989)
139. Cain, B D, P J Norton, W Eubanks, H S Nick & C M Allen: Amplification of the bacA gene confers bacitracin resistance to Escherichia coli. J Bacteriol 175: 3784-3789. (1993)
140. Pollock, T J, L Thorne, M Yamazaki, M J Mikolajczak & R W Armentrout: Mechanism of bacitracin resistance in gram-negative bacteria that synthesize exopolysaccharides. J Bacteriol 176: 6229-6237. (1994)
141. Cao, M & J D Helmann: Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function s factors. J Bacteriol 184: 6123-6129. (2002)
142. Abeijon, C & C B Hirschberg: Topography of glycosylation reactions in the endoplasmic reticulum. Trends Biochem Sci 17: 32-36 (1992)
143. Fernandez, F, J S Rush, D A Toke, G Han, J E Quinn, G M Carman, J-Y Choi, D R Voelker, M Aebi & C J Waechter: The CWH8 gene encodes a dolichyl pyrophosphate phosphatase with a luminally oriented active site in the endoplasmic reticulum of Saccharomyces cerevisiae. J Biol Chem 276: 41455-41464. (2001)
144. van Berkel, M A, M Rieger, S te Heesen, A F Ram, H van den Ende, M Aebi & F M Klis. Glycobiology 9: 243-253 (1999)
145. Kulpa, C F, Jr. & L Leive: Mode of insertion of lipopolysaccharide into the outer membrane of Escherichia coli. J Bacteriol 126: 467-477. (1976)
146. Muhlradt, P F, J Menzel, J R Golecki & V Speth: Outer membrane of Salmonella. Sites of export of newly synthesised lipopolysaccharide on the bacterial surface. Eur J Biochem 35: 471-481. (1973)
147. Bayer, M E: Areas of adhesion between wall and membrane of Escherichia coli. J Gen Microbiol 53: 395-404. (1968)
148. Kellenberger, E: The 'Bayer bridges' confronted with results from improved electron microscopy methods. Mol Microbiol 4: 697-705. (1990)
149. Bayer, M E: Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. J Struct Biol 107: 268-280 (1991)
150. Ishidate, K, E S Creeger, J Zrike, S Deb, B Glauner, T J MacAlister & L I Rothfield: Isolation of differentiated membrane domains from Escherichia coli and Salmonella typhimurium, including a fraction containing attachment sites between the inner and outer membranes and the murein skeleton of the cell envelope. J Biol. Chem 261: 428-443. (1986)
151. Braun, V & M Braun: Active transport of iron and siderophore antibiotics. Curr Opin Microbiol 5: 194-201. (2002)
152. Lloubes, R, E Cascales, A Walburger, E Bouveret, C Lazdunski, A Bernadac & L Journet: The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152: 523-529. (2001)
153. Bliss, J M & R P Silver: Coating the surface: a model for expression of capsular polysialic acid in Escherichia coli K1. Mol Microbiol 21: 221-231. (1996)
154. Gaspar, J A, J A Thomas, C L Marolda & M A Valvano: Surface expression of O-specific lipopolysaccharide in Escherichia coli requires the function of the TolA protein. Mol Microbiol 38: 262-275 (2000)
155. Webster, R E: The tol gene products and the import of macromolecules into Escherichia coli. Mol Microbiol 5: 1005-1011. (1991)
156. Lazdunski, C J, E Bouveret, A Rigal, L Journet, R Lloubès & H Bénédetti: Colicin Import into Escherichia coli Cells. J Bacteriol 180: 4993-5002 (1998)
157. Vianney, A, M M Muller, T Clavel, J C Lazzaroni, R Portalier & R E Webster: Characterization of the tol-pal region of Escherichia coli K-12: Translational control of tolR expression by TolQ and identification of a new open reading frame downstream of pal encoding a periplasmic protein. J Bacteriol 178: 4031-4038. (1996)
158. Lazzaroni, J C, P Germon, M C Ray & A Vianney: The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 177: 191-197 (1999)
159. Derouiche, R, H Benedetti, J C Lazzaroni, C Lazdunski & R Lloubes: Protein complex within Escherichia coli inner membrane. TolA N-terminal domain interacts with TolQ and TolR proteins. J Biol Chem 270: 11078-11084. (1995)
160. Guihard, G, P Boulanger, H Benedetti, R Lloubes, M Besnard & L Letellier: Colicin A and the Tol proteins involved in its translocation are preferentially located in the contact sites between the inner and outer membranes of Escherichia coli cells. J Biol Chem 269: 5874-5880. (1994)
161. Levengood, S K, W F Beyer & R E Webster: TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc Natl Acad Sci USA 88: 5939-5943. (1991)
162. Derouiche, R, M Gavioli, H Benedetti, A Prilipov, C Lazdunski & R Lloubes: Tol A central domain interacts with Escherichia coli porins. EMBO J 15: 6408-6415. (1996)
163. Clavel, T, P Germon, A Vianney, R Portalier & J C Lazzaroni: TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol 29: 359-367 (1998)
164. Cascales, E, M Gavioli, J N Sturgis & R Lloubes: Proton motive force drives the interaction of the inner membrane TolA and outer membrane Pal proteins in Escherichia coli. Mol Microbiol 38: 904-915. (2000)
165. Liu, D & P R Reeves: Escherichia coli K12 regains its O antigen. Microbiology 140: 49-57. (1994)
166. Bengoechea, J A, E Pinta, T Salminen, C Oertelt, O Holst, J Radziejewska-Lebrecht, Z Piotrowska-Seget, R Venho & M Skurnik: Functional Characterization of Gne (UDP-N-Acetylglucosamine- 4-Epimerase), Wzz (Chain Length Determinant), and Wzy (O-Antigen Polymerase) of Yersinia enterocolitica Serotype O:8. J Bacteriol 184: 4277-4287. (2002)
167. Helenius, J & M Aebi: Transmembrane movement of dolichol linked carbohydrates during N-glycoprotein biosynthesis in the endoplasmic reticulum. Semin Cell Dev Biol 13: 171-178. (2002)
168. Knauer, R & L Lehle: The oligosaccharyltransferase complex from yeast. Biochim Biophys Acta 1426: 259-273. (1999)
169. Yan, Q & W J Lennarz: Oligosaccharyltransferase: a complex multisubunit enzyme of the endoplasmic reticulum. Biochem Biophys Res Commun 266: 684-689. (1999)
170. Parodi, A J: Protein glucosylation and its role in protein folding. Annu Rev Biochem 69: 69-93. (2000)
171. Sonnhammer, E L L, G von Heijne & A Krogh: A hidden Markov model for predicting transmembrane helices in protein sequences. In: Proceedings of Sixth International Conference on Intelligent Systems for Molecular Biology. Eds: Glasgow J, Littlejohn T, Major F, Lathrop R, Sankoff D & Sensen C, AAAI Press, Menlo Park, Ca 175-182. (1998)
172. Cserzo, M, E Wallin, I Simon, G von Heijne & A Elofsson: Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the Dense Alignment Surface method. Prot Eng 10: 673-676 (1997)