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Volume 143, Issue 6

VlpA of O1: the first bacterial member of the α-microglobulin lipocalin superfamily Free

Abstract

We have identified a gene, which is closely linked to the locus associated with mannose-fucose-resistant haemagglutination. VlpA is an outer-membrane protein which can be labelled with [H]palmitate and whose processing is globomycin-sensitive, suggesting that it is a lipoprotein. Homology searches revealed that VlpA belongs to the group of lipocalins of the α-microglobulin superfamily which function as small hydrophobic molecule transporters, and is the first identified bacterial member of this group. Multiple copies of this gene are present in O1 and O139 and Southern hybridization reveals a biotype-specific pattern of fragment sizes. Construction of strains capable of hyperproducing VlpA suggested that it is able to bind haemin with low affinity but this may be due to a simple hydrophobic interaction. Attempts to construct specific mutants in have been unsuccessful, presumably because of the multiple copies of genes and their linkage to the VCR element.

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Keyword(s): haemin binding , lipocalin , lipoprotein , Vibrio cholerae and α2-microglobulin
© Society Society for General Microbiology 1997
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1997-06-01
2024-04-25
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References

  1. Ascencio, F.,, Ljungh, A., Wadstrom, T. 1992; Lactoferrin binding properties of Vibrio cholerae.. Microbios 70:103–117
     [Google Scholar]
  2. Barker, A.,, Clark, C. A., Manning, P. A. 1994; Identification of VCR, a repeated sequence associated with a locus encoding a hemagglutinin of Vibrio cholerae O1.. J Bacteriol 76:5450–5458
     [Google Scholar]
  3. Baumler, A. J., Hantke K. 1992; A lipoprotein of Yersinia enterocolitica facilitates ferrioxamine uptake in Escherichia coli.. J Bacteriol 174:1029–1035
     [Google Scholar]
  4. Berman, P.,, Gray, P.,, Chen, E.,, Keyser, K.,, Ehrlich, D.,, Karten, H.,, LaCorbiere, M.,, Esch, F., Schubert, D. 1987; Sequence analysis, ct:llular localization and expression of a neuroretina adhesion and cell survival molecule.. Cell 51:135–142
     [Google Scholar]
  5. Bloomfield, I. C.,, McClain, M. S., Eisenstein, B. I. 1991; Type I fimbriae mutants of Escherichia coli K-12 : characterization of recognized afimbriate strains and construction of new fim deletion mutants.. Mol Microbiol 5:1439–1445
     [Google Scholar]
  6. Brooks, D. E.,, Means, A. R., Wright, E. J.,, Singh, S. P., Tiver, K. K. 1986; Molecular cloning of the cDNA for two major androgen-dependent secretory proteins of 18⋅5 ltilodaltons synthesized by the rat epididymis.. J Biol Chem 261:4956–4961
     [Google Scholar]
  7. Chen, E. T., Seeburg, P. H. 1985; Supercoil sequencing: a fast arid simple method for sequencing plasmid :DNA.. DNA 4:165–170
     [Google Scholar]
  8. Crosa, J. H. 1989; Genetics and molecular biology of siderophore- related iron transport in bacteria.. Microbiol Rev 53:517–530
     [Google Scholar]
  9. DiRita, V. 1992; Co-ordinate expression of virulence genes by ToxR in Vibrio cholerae.. Mol Microbiol 6:451–458
     [Google Scholar]
  10. van Dongen, W. M. A. M.,, van Vlerken, M. A. M., DeGraaf, F. K. 1987; Nucleotide sequence of a DNA fragment encoding a Vibrio cholerae hemagglutinin.. Life Sci Adv 6:85–491
     [Google Scholar]
  11. Drayna, D.,, Fielding, C.,, McLean, J.,, Baer, B.,, Castro, G.,, Chen, E.,, Comstock, L.,, Henzel, W.,, Kohr, W.,, Rhee, L.,, Wion, K., Lawn, R. 1986; Cloning and expression of human apolipoproteinD cDNA.. J Biol Chem 261:16535–16539
     [Google Scholar]
  12. Drayna, D.,, McLean, J. W.,, Wion, K.L,, Trent, J. M.,, Drabkin, H. A., Lawn, R.M. 1987; Human apolipoproteinD gene: gene sequence, chromosomal localization and homology to the α2μ-globulin superfamily.. D N A 6:199–204
     [Google Scholar]
  13. Franzon V. L.,, Barker, A., Manning, P. A. 1993; Nucleotide sequence and the construction of a mutant in the mannose-fucoseresistant hemagglutinin (MFRHA) of Vibrio cholerae O1.. Infect Immun 61:3032–3037
     [Google Scholar]
  14. Franzon V. L.,, Manning, P. A. 1986; Molecular cloning and expression in Escherichia coli K-12 of the gene for a hemagglutinin from Vibrio cholerae.. Infect Immun 52:279–284
     [Google Scholar]
  15. Godovac-Zimmermann, J. 1988; The structural motif of β-lactoglobulin and retinol binding protein : a basic framework for binding and transport of small hydrophobic molecules ?. Trends Biochem Sci 13:64–66
     [Google Scholar]
  16. Goldberg, M. B.,, DiRita, V. J., Calderwood, S. B. 1990; Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TnphoA mutagenesis.. Infect Immun 58:55–60
     [Google Scholar]
  17. Haefliger, J. A.,, Jenne, D.,, Stanley, K. K., Tschopp, J. 1987; Structural homology of human complement component C8γ and plasma protein HC: identity of the cysteine bond pattern.. Biochem Biophys Res Commun 149:750–754
     [Google Scholar]
  18. Hanson, M. S., Hansen, E. J. 1991; Molecular cloning, partial purification and characterization of a heme-binding lipoprotein from Haemophilus influenzae type B.. Mol Microbiol 5:267–278
     [Google Scholar]
  19. Henderson, D. P., Payne, S. M. 1993; Cloning and characterization of the Vibrio cholerae genes encoding the utilization of iron from hemin and hemoglobin.. Mol Microbiol 7:461–469
     [Google Scholar]
  20. Henikoff, S. 1984; Unidirectional digestion with Exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359
     [Google Scholar]
  21. Higgins, D. G., Sharp, P. M. 1988; CLUSTAL: a package for performing multiple sequence alignment on a microcomputer.. Gene 73:237–244
     [Google Scholar]
  22. Hoffman, C. S., Wright, A. 1988; Fusions of secreted proteins to alkaline phosphatase : an approach to studying protein secretion.. Proc Natl Acad Sci USA 82:5107–5111
     [Google Scholar]
  23. Holden, H. M.,, Rypniewski, W. R.,, Law, J. H., Rayment, I. 1987; The molecular structure of insecticyanin from the tobacco hornworm Manduca sexta at 2⋅6 Å resolution.. EMBO J 6:1565–1570
     [Google Scholar]
  24. Huber, R.,, Schneider, M.,, Mayr, I.,, MUller, R.,, Deutzmann, R.,, Suter, F.,, Zuber, H.,, Falk, H., Kayser, H. 1987; Molecular structure of the bilin biading protein (BBP) from Pieris brassicae after refinement at 2⋅0 Å resolution.. J Mol Biol 198:499–513
     [Google Scholar]
  25. Inukai, M.,, Takeuchi, M.,, Shimizu, K., Arai, M. 1978; Mechanism of action of globomycin.. J Antibiot 31:1203–1205
     [Google Scholar]
  26. Iredell, J. R., Manning, P. A. 1994; The toxin-coregulated pilus (TCP) of Vibrio cholerae O1: a model for type IV pilus biogenesis?. Trends Microbiol 2:187–192
     [Google Scholar]
  27. Kreutzer, K., Pratt, C. P. A., Torriani, A. 1975; Genetic analysis of regulatory mutants of alkaline phosphatase of Escherichia coli.. Genetics 81:459–468
     [Google Scholar]
  28. Manning, P. A. 1994; Surface-associated and soluble components involved in bacteria-host interactions.. Curr Top Microbiol Immunol 192:265–281
     [Google Scholar]
  29. Manoil, C., Beckwith, J. 1985; TnphoA: a transposable probe for protein export signals. Proc Natl Acad Sci USA 82:8129–8133
     [Google Scholar]
  30. Miller, J. H. 1972; Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory..
    [Google Scholar]
  31. Ng, S. C.,, Rao, A. G.,, Howard, O. M., Sodetz, J. M. 1987; The eighth component of human complement: evidence that it is an oligometric serum protein assembled from products of three different genes.. Biochemistry 26:5229–5233
     [Google Scholar]
  32. Ogierman, M. A, Manning, P. A. 1992; TCP pilus biosynthesis in Vibrio cholerae O1 : gene sequence of tcpC encoding an outer membrane lipoprotein.. FEMS Microbiol Lett 97:179–184
     [Google Scholar]
  33. Parsot, C.,, Taxman, E., Mekalanos, J. J. 1991; ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae.. Proc Natl Acad Sci USA 988:1641–1645
     [Google Scholar]
  34. Payne, S. M., Finkelstein, R. A. 1977; Detection and differentiation of iron-responsive avirulent mutants on Congo red agar.. Infect Immun 18:94–98
     [Google Scholar]
  35. Pearson, W. R. 1990; Rapid and sensitive sequence comparison with FASTP and FASTA . Methods Enzymol 183:63–98
     [Google Scholar]
  36. Peitsch, M. C., Boguski, M. S. 1990; Is apolipoprotein D a mammalian bilin-binding protein ?. Nature New Biol 2:197–206
     [Google Scholar]
  37. Pervaiz, S., Brew K. 1987; Homology and structure-function correlations between α1-acid glycoprotein and serum retinolbinding protein and its relatives.. FASEB J 1:209–214
     [Google Scholar]
  38. Pugsley, A. P. 1989; San Diego, CA: Academic Press.. Protein Targeting
     [Google Scholar]
  39. Richardson, A.,, Butler, J. A,, Rutherford, M. S.,, Sensei, I.,, Gu, M. Z.,, Fernandez, G., Chiang, W. H. 1987; Effect of age and dietary restriction on the expression of α2 μ-globulin.. J Biol Chem 262:12821–12825
     [Google Scholar]
  40. Riley, C. T.,, Barbean, B. K.,, Kein, P. S.,, Kedzy, F. J.,, Heinrikson. R. L., Law, J. H. 1984; The covalent protein structure of insecticyanin, a blue biliprotein from the hemolymph of the tobacco hornworm Manduca sexta L.. J Biol Chem 259:13159–13165
     [Google Scholar]
  41. Sambrook, J.,, Fritsch, E. F., Maniatis, T. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory..
    [Google Scholar]
  42. Sanger, F.,, Nicklen, S., Coulson, A. R. 1977; DNA sequencing with chain-terminating inhibitors.. Proc Natl Acad Sci USA 74:5463–5467
     [Google Scholar]
  43. Sawyer, L. 1987; One fold among many.. Nature 327:659
     [Google Scholar]
  44. Schneider, R., Hantke, K. 1993; Iron-hydroxamate uptake systems in Bacillus subtilis : identification of a lipoprotein as part of a binding protein-dependent transport system.. Mol Microbiol 8:111–121
     [Google Scholar]
  45. Schubert, D.,, LaCorbiere, M., Esch, F. 1993; A chick neural retina adhesion and survival molecule is a retinol binding protein.. J Cell Biol 102:2295–2301
     [Google Scholar]
  46. Snyder, S. H.,, Sklar, P. B., Pevsner, J. 1988; Molecular mechanisms of olfaction.. J Biol Chem 263:13971–13974
     [Google Scholar]
  47. Spreyer, P.,, Schaal, H.,, Kuhn, G.,, Rothe, T.,, Unterbeck, A.,, Olek, K., MUller, H. W. 1990; Regeneration-associated high level expression of apolipoproteinD mRNA in endoneural fibroblasts of peripheral nerve.. EMBO J 9:2479–2484
     [Google Scholar]
  48. Stugard, C. E.,, Daskaleros, P. A., Payne, S. M. 1989; A 101- kilodalton heme-binding protein associated with Congo red 5463-5467. binding and virulence in Shigella flexneri and enteroinvasive Escherichia coli strains.. Infect Immun 57:3534–3539
     [Google Scholar]
  49. Suter, .,, Kayser, H., Zuber H. 1988; The complete amino acid sequence of the bilin-binding protein from Pieris brassicae and its similar,ty to a family of Serum transport proteins like the retinal binding proteins. Biol Chem Hoppe-Seyler 369:497–505
     [Google Scholar]
  50. Tabor, S., Richardson, C. C. 1985; A bacteriophage T 7 RNA polymerase/promoter system for controlled exclusive expression of specific genes.. Proc Natl Acad Sci USA 82:1074–1078
     [Google Scholar]
  51. Vieira, J., Messing J. 1982; The pUC plasmids, an M13mp7- derived system for insertion mutagenesis and sequencing with synthetic universal primers.. Gene 19:259–268
     [Google Scholar]
  52. Williams, P. H., Roberts, M. 1982; Iron scavenging in the pathogenesis of Escherichia coli. In Genetics of Bacterial Diversity,. Edited by D. A. Hopwood & K. F. Chater. London : Academic Press. pp:331–350
     [Google Scholar]
  53. Williams, S. G.,, Attridge, S. R., Manning, P. A. 1993; The transcriptional activator HlyU of Vibrio cholerae : nucleotide sequence and role in virulence gene expression.. Mol Microbiol 9:751–760
     [Google Scholar]
  54. Yamaguchi, K.,, Yu, F., Inouye, M. 1988; A single amino acid determinant of the membrane localization of lipoproteins in E. coli .. Cell 53:423–432
     [Google Scholar]
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VlpA of Vibrio cholerae O1: the first bacterial member of the α2-microglobulin lipocalin superfamily
Microbiology 143, 1805 (1997); https://doi.org/10.1099/00221287-143-6-1805
/content/journal/micro/10.1099/00221287-143-6-1805
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