Transmembrane topology of the two FhuB domains representing the hydrophobic components of bacterial ABC transporters involved in the uptake of siderophores, haem and vitamin B12

Microbiology

Volumn 144, Issue 10, 1998, Pages 2759-2769

  Groeger, Wolfram ^a   Köster, Wolfgang ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b INSTITUT PASTEUR   (France)

Author keywords

ABC transporter; Escherichia coli fhu system; Integral membrane proteins; Iron; Siderophore uptake

Indexed keywords

ABC TRANSPORTER; BETA LACTAMASE; CYANOCOBALAMIN; HEME; MEMBRANE PROTEIN; SIDEROPHORE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; ESCHERICHIA COLI; HYDROPHOBICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FOLDING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0031793359     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/00221287-144-10-2759     Document Type: Article

References (57)

1. Adhikari, P., Kirby, S. D., Nowalk, A. J., Veraldi, K. L, Schryvers, A. B. & Mietzner, T. A. (1996a). Biochemical characterization of a Haemophilus influenzae periplasmic iron transport system. J Biol Chem 270, 25142-25149.
2. Adhikari, P., Berish, S. A., Nowalk, A. J., Veraldi, K. L., Morse, S. A. & Mietzner, T. A. (1996b). The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron. J Bacteriol 178, 2145-2149.
3. Ames, G. F.-L. (1986). Bacterial periplasmic transport systems: structure, mechanism and evolution. Annu Rev Biochem 55, 397-425.
4. Angerer, A., Gaisser, S. & Braun, V. (1990). Nucleotide sequences of the sfuA, sfuB, and sfuC genes of Serratia marcescens suggest a pcriplasmic-binding-protein-dependent iron transport mechanism. J Bacteriol 172, 572-578.
5. Biegel Carson, S. D. & Sparling, P. F. (1996). Gonococcal FrpB: a possible role in siderophore uptake. In Proceedings of the 10th International Pathogenic Neisseria Conference, pp. 566-567. Baltimore, MD.
6. Böhm, B., Boschert, H. & Köster, W. (1996). Conserved amino acids in the N- and C-terminal domains of integral membrane transporter FhuB define sites important for intra- and intermolecular interactions. Mol Microbiol 20, 223-232.
7. Boyd, D., Traxler, B. & Beckwith, J. (1993). Analysis of the topology of a membrane protein by using a minimum number of alkaline phosphatase fusions. J Bacteriol 175, 553-556.
8. Braun, V. & Hantke, K. (1991). Genetics of bacterial iron transport. In Handbook of Microbial Iron Chelates, pp. 107-138. Edited by G. Winkelmann. Boca Raton, FL: CRC Press.
9. Braun, V., Gross, R., Köster, W. & Zimmermann, L. (1983). Plasmid and chromosomal mutants in the iron(III)-aerobactin transport system of Escherichia coli. Use of streptonigrin for selection. Mol Gen Genet 192, 131-139.
10. Broome-Smith, J. K. & Spratt, B. G. (1986). A vector for the construction of translational fusions to TEM β-lactamase and the analysis of protein export signals and membrane protein topology. Gene 49, 341-349.
11. Bult, C. J., White, O., Olsen, G. J. & 37 other authors (1996). Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273, 1058-1073.
12. Chenault, S. S. & Earhart, C. F. (1991). Organization of genes encoding membrane proteins of the Escherichia coli ferrienterobactin permease. Mol Microbiol 5, 1405-1413.
13. Craik, C. S., Largmann, C., Fletcher, T., Roczniak, S., Barr, P. J., Fletterick, R. & Rutter, W. J. (1985). Redesigning trypsin: alteration of substrate specificity. Science 228, 291-297.
14. Dassa, E. & Muir, S. (1993). Membrane topology of MalG, an inner membrane protein from the maltose transport system of Escherichia coli. Mol Microbiol 7, 29-38.
15. Davidson, A. L., Laghaeian, S. S. & Mannering, D. E. (1996). The maltose transport system of Escherichia coli displays positive cooperativity in ATP hydrolysis. J Biol Chem 271, 4858-4863.
16. Fecker, L. & Braun, V. (1983). Cloning and expression of the fhu genes involved in iron (III) hydroxamate uptake by E. coli. J Bacteriol 156, 1301-1314.
17. Fiss, E. H., Yu, S. & Jacobs, W. R., Jr (1994). Identification of genes involved in the sequestration of iron in mycobacteria : the ferric exochelin biosynthetic and uptake pathways. Mol Microbiol 14, 557-569.
18. Fleischmann, R. D., Adams, M. D., White, O. & 37 other authors (1995). Whole-genome random sequencing and assembly of Haemophilus influenzae. Science 269, 496-512.
19. Friedrich, M. J., DeVeaux, L. C. & Kadner, R. J. (1986). Nucleotide sequence of the btuCED genes involved in vitamin B12 transport in Escherichia coli and homology with components of periplasmic binding protein-dependent transport systems. J Bacteriol 167, 928-934.
20. Froshauer, S., Green, G. N., Boyd, D., McGovern, K. & Beckwith, J. (1988). Genetic analysis of the membrane insertion and topology of MalF, a cytoplasmic membrane protein of E. coli. J Mol Biol 200, 501-511.
21. Haardt, M. & Bremer, E. (1996). Use of phoA and lacZ fusions to study the membrane topology of ProW, a component of the osmoregulated ProU transport system of Escherichia coli. J Bacteriol 178, 5370-5381.
22. Hanahan, D. (1985). DNA Cloning: a Practical Approach, vol. 1, p. 109. Edited by S. W. Glover. Oxford: IRL Press.
23. von Heijne, G. (1986). The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J 5, 3021-3025.
24. Higgins, C. F. (1992). ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8, 67-113.
25. Hubacek, J. & Glover, S. W. (1970). Complementation analysis of temperature-sensitive host specificity mutations in Escherichia coli. J Mal Biol 50, 111-127.
26. Kaneko, T., Sato, S., Kotani, H. & 21 other authors (1996). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3, 109-136.
27. Kerppola, R. E. & Ames, G. F.-L. (1992). Topology of the hydrophobic membrane-bound components of the histidine periplasmic permease. Comparison with other members of the family. J Biol Chem 267, 2329-2336.
28. Klenk, H.-P., Clayton, R. A., Tomb, J. F. & 48 other authors (1997). The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidns. Nature 390, 364-370.
29. Köster, W. (1991). Iron (III) hydroxamate transport across the cytoplasmic membrane of Escherichia coli. Biol Metals 4, 23-32.
30. Köster, W. & Böhm, B. (1992). Point mutations in two conserved glycine residues within the integral membrane protein FhuB affect iron(III) hydroxamate transport. Mol Gen Genet 232, 399-407.
31. Köster, W. & Braun, V. (1986). Iron hydroxamate transport of Escherichia coli: nucleotide sequence of the fhuB gene and identification of the protein. Mol Gen Genet 204, 435-442.
32. Köster, W. & Braun, V. (1989). Iron hydroxamate transport into Escherichia coli K12: localization of FhuD in the periplasm and of FhuB in the cytoplasmic membrane. Mol Gen Genet 217, 435-442.
33. Köster, W. & Braun, V. (1990). Iron(III) hydroxamate transport of Escherichia coli: restoration of iron supply by coexpression of the N- and C-terminal halves of the cytoplasmic membrane protein FhuB cloned on separate plasmids. Mol Gen Genet 223, 379-384.
34. Köster, W. L., Actis, L. A., Waldbeser, L. S., Tolmasky, M. E. & Crosa, J. H. (1991). Molecular characterization of the iron transport system mediated by the pJM1 plasmid in Vibrio anguillarum 775. J Biol Chem 266, 23829-23833.
35. Kunst, F., Ogasawara, N., Moszer, I. & 148 other authors (1997). The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature 390, 249-256.
36. Lugtenberg, B., Meijers, J., Peters, R., van der Hoek, P. & van Alphen, L. (1975). Electrophoretic resolution of the major outer membrane protein of Escherichia coli K-12 into four bands. FEBS Lett 58, 254-258.
37. McGovern, K., Ehrmann, M. & Beckwith, J. (1991). Decoding signals for membrane protein assembly using alkaline phosphatase fusions. EMBO J 10, 2773-2782.
38. Mané, B., Masclaux, C., Rauscher, L., Enard, C. & Expert, D. (1995). Differential expression of two siderophore-dependent iron-acquisition pathways in Erwinia chrysanthemi 3937: characterization of a novel ferrisiderophore permease of the ABC transporter family. Mol Microbiol 18, 33-43.
39. Maniatis, T., Fritsch, E. F. & Sambrook, J. (1982). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
40. Mourez, M., Hofnung, M. & Dassa, E. (1997). Subunit interactions in ABC transporters: a conserved sequence in hydrophobic membrane proteins of periplasmic permeases defines an important site of interaction with the ATPase subunits. EMBO J 16, 3066-3077.
41. Pearce, S. R., Mimmack, M. L., Gallagher, M. P., Gileadi, U., Hyde, S. C. & Higgins, C. F. (1992). Membrane topology of the integral membrane components, OppB and OppC, of the oligopeptide permease of Salmonella typhimurium. Mol Microbiol 6, 47-57.
42. Quirk, P. G., Guffanti, A. A., Clejan, S., Cheng, J. & Krulwich, T. A. (1994). Isolation of Tn917 insertional mutants of Bacillus subtilis that are resistant to the protonophore carbonyl cyanide mchlorophenylhydrazone. Biochim Biophys Acta 1186, 27-34.
43. Richardson, P. T. & Park, S. F. (1995). Enterochelin acquisition in Campylobacter coli: characterization of components of a binding-protein-dependent transport system. Microbiology 141, 3181-3191.
44. Sanger, F., Nicklen, S. & Coulson, A. R. (1977). DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74, 5463-5467.
45. Saurin, W., Köster, W. & Dassa, E. (1994). Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral membrane proteins. Mol Microbiol 12, 993-1004.
46. Schultz-Hauser, G., Köster, W., Schwarz, H. & Braun, V. (1992). Iron (III) hydroxamate transport in Escherichia coli K-12: FhuB-mediated membrane association of the FhuC protein and negative complementation of fhuC mutants. J Bacteriol 174, 2305-2311.
47. Shea, C. M. & Mclntosh, M. A. (1991). Nucleotide sequence and genetic organization of the ferric enterobactin transport system -homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol Microbiol 5, 1415-1428.
48. Short, J. M., Fernandez, J. M., Sorge, J. A. & Huse, W. D. (1988). ZAP: a bacteriophage expression vector with in vivo excision properties. Nucleic Acids Res 16, 7583-7600.
49. Stanssens, P., Opsomer, C., McKeown, Y. M., Kramer, W., Zabeau, M. & Fritz, H. J. (1989). Efficient oligonucleotide-directed construction of mutations in expression vectors by the gapped duplex DNA method using alternating selectable markers. Nucleic Acids Res 17, 4441-4454.
50. Staudenmaier, H., Van Hove, B., Yaraghi, Z. & Braun, V. (1989). Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic binding protein-dependent transport mechanism for iron (III) dicitrate in Escherichia coli. J Bacteriol 171, 2626-2633.
51. Stojiljkovic, I. & Hantke, K. (1994). Transport of haemin across the cytoplasmic membrane through a haemin specific periplasmic binding protein-dependent transport system in Yersinia enterocolitica. Mol Microbiol 13, 719-732.
52. Studier, F. W. & Moffatt, B. A. (1986). Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189, 113-130.
53. Tabor, S. & Richardson, C. C. (1985). A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 82, 1074-1078.
54. Tomb, J.-F., White, O., Kerlavage, A. R. & 39 other authors (1997). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539-547.
55. Whitley, P., Zander, T., Ehrmann, M., Haardt, M., Bremer, E. & von Heijne, G. (1994). Sec-independent translocation of a 100-residue periplasmic N-terminal tail in the E. coli inner membrane protein Pro W. EMBO J 13, 4653-4661.
56. Wilken, S., Schmees, G. & Schneider, E. (1996). A putative helical domain in the MalK subunit of the ATP-binding-cassette transport system for maltose of Salmonella typhimurium (MalFGK2) is crucial for interaction with MalF and MalG. A study using the LacK protein of Agrobacterium radiobacter as a tool. Mol Microbiol 22, 655-666.
57. Yamane, K., Kumano, M. & Kurita, K. (1996). The 25 °-36 °region of the Bacillus subtilis chromosome: determination of the sequence of a 146 kb segment and identification of 113 genes. Microbiology 142, 3047-3056.