The rfaE gene from Escherichia coli encodes a bifunctional protein involved in biosynthesis of the lipopolysaccharide core precursor ADP-L- glycero-D-manno-heptose

Journal of Bacteriology

Volumn 182, Issue 2, 2000, Pages 488-497

  Valvano, Miguel A ^a   Marolda, Cristina L ^a   Bittner, Mauricio ^a,b   Glaskin Clay, Mike ^a   Simon, Tania L ^a   Klena, John D ^c  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSITY OF CANTERBURY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; HEPTOSE; LIPOPOLYSACCHARIDE;

AMINO ACID SEQUENCE; ARTICLE; CARBOHYDRATE SYNTHESIS; DNA SEQUENCE; ESCHERICHIA COLI; GENE ACTIVATION; GENE EXPRESSION; GENE MUTATION; GENETIC RECOMBINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ADENOSINE DIPHOSPHATE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI; GLYCOSYLTRANSFERASES; HEPTOSES; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; SEQUENCE ALIGNMENT;

EID: 0033987369     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.182.2.488-497.2000     Document Type: Article

References (60)

1. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Blattner, F. R., G. Plunkett, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden. D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
3. Bolivar, F. 1978. Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique EcoR1 sites for selection of EcoR1 generated recombinant DNA molecules. Gene 4:121-136.
4. Bork, P., L. Holm, E. V. Koonin, and C. Sander. 1995. The cytidylyltransferase superfamily: identification of the nucleotide-binding site and fold prediction. Proteins 22:259-266.
5. Bork, P., C. Sander, and A. Valencia. 1993. Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Protein Sci. 2:31-40.
6. Brick, P., T. N. Bhat, and D. M. Blow. 1989. Structure of the tyrosyl tRNA synthetase refined at 2.3 Ångströms resolution. Interaction of the enzyme with the tyrosyl adenylate intermediate. J. Mol. Biol. 208:83-98.
7. Brooke, J. S., and M. A. Valvano. 1996. Biosynthesis of inner core lipopolysaccharide in enteric bacteria identification and characterization of a conserved phosphoheptose isomerase. J. Biol. Chem. 271:3608-3614.
8. Brooke, J. S., and M. A. Valvano. 1996. Molecular cloning of the Haemophilus influenzae gmhA (lpcA) gene encoding a phosphoheptose isomerase required for lipooligosaccharide biosynthesis. J. Bacteriol. 178:3339-3341.
9. Chang, A. C. Y., and S. N. Cohen. 1978. Construction and characterization of amplifiable DNA cloning vectors derived from P15A cryptic plasmid. J. Bacteriol. 134:1141-1156.
10. Coleman, W. G., Jr. 1983. The rfaD gene codes for ADP-L-glycero-D-mannoheptose-6-epimerase. An enzyme required for lipopolysaccharide core biosynthesis. J. Biol. Chem. 258:1985-1990.
11. Curtiss, R., III, J. Charamella, D. R. Stallions, and J. A. Mays. 1968. Parental functions during conjugation. Bacteriol. Rev. 32:320-348.
12. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
13. Dower, W. J., J. F. Miller, and C. W. Ragsdale. 1988. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16:6127-6145.
14. Drazek, E. S., D. C. Stein, and C. D. Deal. 1995. A mutation in the Neisseria gonorrhoeae rfaD homolog results in altered lipooligosaccharide expression. J. Bacteriol. 177:2321-2327.
15. Eidels, L., and M. J. Osborn. 1971. Lipopolysaccharide and aldoheptose biosynthesis in transketolase mutants of Salmonella typhimurium. J. Biol. Chem. 68:1673-1677.
16. Eidels, L., and M. J. Osborn. 1974. Phosphoheptose isomerase, first enzyme in the biosynthesis of aldoheptose in Salmonella typhimurium. J. Biol. Chem. 249:5642-5648.
17. Freter, A., and O. Bowien. 1994. Identification of a novel gene, aut, involved in autotrophic growth of Alcaligenes eutrophus. J. Bacteriol. 176:5401-5408.
18. Havekes, L. M., B. J. J. Lugtenberg, and W. P. M. Hoekstra. 1976. Conjugation deficient E. coli K-12 F-mutants with heptose-less lipopolysaccharide. Mol. Gen. Genet. 146:43-50.
19. Heinrichs, D. E., M. A. Valvano, and C. Whitfield. 1999. Biosynthesis and genetics of lipopolysaccharide core. p. 305-330. In H. Brade, D. C. Morrison, S. Vogel, and S. Opal (ed.), Endotoxin in health and disease. Marcel Dekker, Inc., New York, N.Y.
20. Helander, I. M., B. Lindner, H. Brade, K. Altmann, A. A. Lindberg, E. T. Rietschel, and U. Zahringer. 1988. Chemical structure of the lipopolysaccharide of Haemophilus influenzae strain 1-69 Rd-/B+: description of a novel deep-rough chemotype. Eur. J. Biochem. 177:483-492.
21. Izard, T., and A. Geerlof. 1999. The crystal structure of a novel bacterial adenylyltransferase reveals half of sites reactivity. EMBO J. 18:2021-2030.
22. Klena, J. D., R. S. Ashford, and C. A. Schnaitman. 1992. 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.
23. Knauf, V. C., and E. W. Nester. 1982. Wide host range cloning vectors: a cosmid clone hank of an Agrobacterium Ti plasmid. Plasmid 8:45-54.
24. Kocsis, B., and T. Kontrohr. 1984. 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. Chem. 259:11858-11860.
25. Kontrohr, T., and B. Kocsis. 1981. Isolation of adenosine 5′-diphosphate-i> glycero-D-mannoheptose. An intermediate in lipopolysaccharide biosynthesis of Shigella sonnei. J. Biol. Chem. 256:7715-7718.
26. Koronakis, V., E. Koronakis, J. Li, and K. Stauffer. 1997. Structure of To1C, the outer membrane component of the bacterial type I efflux system, derived from two-dimensional crystals. Mol. Microbiol. 23:617-626.
27. Kovach, M. E., R. W. Phillips, P. H. Elzer, R. M. Roop, and K. M. Peterson. 1994. pBBR1MCS: a broad-host-range cloning vector. BioTechniques 16: 800-802.
28. Lee, N.-G., M. G. Sunshine, and M. A. Apicella. 1995. Molecular cloning and characterization of the nontypeable Haemophilus influenzae 2019 rfaE gene required for lipopolysaccharide biosynthesis. Infect. Immun. 63:818-824.
29. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, N.Y.
30. Marolda, C. L., and M. A. Valvano. 1993. Identification, expression, and DNA sequence of the GDP-mannose biosynthesis genes encoded by the O7 rfb gene cluster of strain VW187 (Escherichia coli O7:K1). J. Bacteriol. 175:148-158.
31. Marolda, C. L., J. Welsh, L. Dafoe, and M. A. Valvano. 1990. Genetic analysis of the O7-polysaccharide biosynthesis region from the Escherichia coli O7:K1 strain VW187. J. Bacteriol. 172:3590-3599.
32. Metcalf, W. W., W. Jiang, and B. L. Wanner. 1994. Use of the rep technique for allele replacement to construct new Escherichia coli hosts for maintenance of R6K gamma origin plasmids at different copy numbers. Gene 138:1-7.
33. Mushegian, A. 1999. The purloined letter: bacterial orthologs of archeal NMN adenylyltransferase are domains within multifunctional transcription regulator NadR. J. Mol. Microbiol. Biotechnol. 1:127-128.
34. Nichols, W. A., B. W. Gibson, W. Melaugh, N.-G. Lee, M. Sunshine, and M. A. Apicella. 1997. Identification of the ADP-L-glycero-D-manno-heptose-6-epimerase (rfaD) and heptosyltransferase II (rfaF) biosynthesis genes from nontypeable Haemophilus influenzae 2019. Infect. Immun. 65:1377-1386.
35. Nikaido, H., and M. Vaara. 1985. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49:1-32.
36. Parker, C. T., A. W. Kloser, C. A. Schnaitman, M. A. Stein, S. Gottesman, and B. W. Gibson. 1992. Role of the rfaG and rfaP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli K-12. J. Bacteriol. 174:2525-2538.
37. Passador, L., and T. Linn. 1989. Autogenous regulation of the RNA polymerase β subunit of Escherichia coli occurs at the translational level in vivo. J. Bacteriol. 171:6234-6242.
38. Raetz, C. R. H. 1996. Bacterial lipopolysaccharides: a remarkable family of bioactive molecules, p. 1035-1063. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, D.C.
39. Reeves, P. R. 1992. Variation in O-antigens, niche-specific selection and bacterial populations. FEMS Microbiol. Lett. 79:509-516.
40. Reeves, P. R., M. Hobbs, M. A. Valvano, M. Skurnik, C. Whitfield, D. Coplin, N. Kido, J. Klena, D. Maskell, C. R. H. Raetz, and P. D. Rick. 1996. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol. 4:495-503.
41. Rossmann, M. G., A. Liljas, C. I. Branden, and L. J. Banaszak. 1975. Evolutionary and structural relationships among dehydrogenases, p. 62-102. In P. D. Boyer (ed.), The enzymes, 3rd ed., vol. 11. Academic Press, New York, N.Y.
42. Schagger, H., and G. van Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
43. Schnaitman, C. A., and J. D. Klena. 1993. Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol. Rev. 57:655-682.
44. Sherburne, C., and D. E. Taylor. 1997. Effect of lipopolysaccharide mutations on recipient ability of Salmonella typhimurium for incompatibility group H plasmids. J. Bacteriol. 179:952-955.
45. Sigrell, J. A., A. D. Cameron, T. A. Jones, and S. L. Mowbray. 1998. Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 Å resolution: insights into a new family of kinase structures. Structure 6:183-193.
46. Sirisena, D. M., P. R. MacLachlan, S. L. Liu, A. Hessel, and K. E. Sanderson. 1994. Molecular analysis of the rfaD gene, for heptose synthesis, and the rfaF gene, for heptose transfer, in lipopolysaccharide synthesis in Salmonella typhimurium. J. Bacteriol. 176:2379-2385.
47. Tamaki, S., T. Sato, and M. Matsuhashi. 1971. Role of lipopolysaccharides in antibiotic resistance and bacteriophage adsorption of Escherichia coli K-12. J. Bacteriol. 105:968-975.
48. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
49. Valvano, M. A. 1999. Biosynthesis and genetics of ADP-heptose. J. Endotoxin Res. 5:90-95.
50. Valvano, M. A., and J. H. Crosa. 1984. Aerobactin iron transport genes commonly encoded by certain CoIV plasmids occur in the chromosome of a human invasive strain of Escherichia coli K1. Infect. Immun. 46:159-167.
51. Valvano, M. A., and J. H. Crosa. 1988. Molecular cloning, expression, and regulation in Escherichia coli K-12 of a chromosome-mediated aerohactin iron transport system from a human invasive isolate of E. coli K1. J. Bacteriol. 170:5529-5538.
52. Valvano, M. A., R. P. Silver, and J. H. Crosa. 1986. Occurrence of chromosome-or plasmid-mediated aerobactin iron transport systems and hemolysin production among clonal groups of human invasive strains of Eschcrichia coli K1. Infect. Immun. 52:192-199.
53. van Heeswijk, W. C., M. Rabenberg, H. V. Westerhoff, and D. Kahn. 1993. The genes of the glutamine synthetase adenylylation cascade are not regulated by nitrogen in Escherichia coli. Mol. Microbiol. 9:443-457.
54. Venkatachalam, K. V., H. Fuda, E. V. Koonin, and C. A. Strott. 1999. Site-selected mutagenesis of a conserved nucleotide binding HXGH motif located in ATP sulfurylase domain of a human bifunctional 3′-phosphoadenosine 5′-phosphosulfate synthase. J. Biol. Chem. 274:2601-2604.
55. Vimont, S., S. Dumontier, V. Escuyer, and P. Berche. 1997. The rfaD locus: a region of rearrangement in Vibrio cholerae O139. Gene 185:43-47.
56. Watson, G., and K. Paigen. 1971. Isolation and characterization of an Escherichia coli bacteriophage requiring cell wall galactose. J. Virol. 8:669-674.
57. Whitfield, C., and M. A. Valvano. 1993. Biosynthesis and expression of cell-surface polysaccharides in gram-negative bacteria. Adv. Micron. Physiol. 35:135-246.
58. Wilkinson, R. G., P. Gemski, and B. A. D. Stocker. 1972. Non-smooth mutants ni Salmonella typhimurium: differentiation by phage sensitivity and genetic mapping. J. Gen. Microbiol. 70:527-554.
59. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
60. Zwahlen, A., L. G. Rubin, C. J. Connelly, T. J. Inzana, and E. R. Moxon. 1985. Alteration of the cell wall in Haemophilus influenzae type b by transformation with cloned DNA: association with attenuated virulence. J. Infect. Dis. 152:485-492.