Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Oct;177(20):6005–6010. doi: 10.1128/jb.177.20.6005-6010.1995

Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain.

J Martinez 1, S Steenbergen 1, E Vimr 1
PMCID: PMC177433  PMID: 7592358

Abstract

Catabolism of sialic acids by Escherichia coli requires the genes nanA and nanT, which were previously mapped between argG and rpoN (E.R. Vimr and F.A. Troy, J. Bacteriol. 164:845-853, 1985). This organization is confirmed and extended by physical mapping techniques. An open reading frame beginning 135 bp from the nanA translational stop codon could code for a 53,547-Da hydrophobic polypeptide predicted to contain 14 transmembrane segments. Complementation analysis confirmed that nanT is required for sialic acid uptake when expressed in trans. NanT is homologous to a putative permease encoded by open reading frame 425, which maps between leuX and fecE in the E. coli chromosome. However, unlike this hypothetical permease or previously reported monosaccharide transporters, NanT contains a centrally located domain with two additional potential membrane-spanning segments plus one amphiphilic alpha-helix that may be important for the structure and function of sialic acid-permease.

Full Text

The Full Text of this article is available as a PDF (299.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Baldwin S. A., Henderson P. J. Homologies between sugar transporters from eukaryotes and prokaryotes. Annu Rev Physiol. 1989;51:459–471. doi: 10.1146/annurev.ph.51.030189.002331. [DOI] [PubMed] [Google Scholar]
  3. Baldwin S. A. Mammalian passive glucose transporters: members of an ubiquitous family of active and passive transport proteins. Biochim Biophys Acta. 1993 Jun 8;1154(1):17–49. doi: 10.1016/0304-4157(93)90015-g. [DOI] [PubMed] [Google Scholar]
  4. Corfield T. Bacterial sialidases--roles in pathogenicity and nutrition. Glycobiology. 1992 Dec;2(6):509–521. doi: 10.1093/glycob/2.6.509. [DOI] [PubMed] [Google Scholar]
  5. Godoy V. G., Dallas M. M., Russo T. A., Malamy M. H. A role for Bacteroides fragilis neuraminidase in bacterial growth in two model systems. Infect Immun. 1993 Oct;61(10):4415–4426. doi: 10.1128/iai.61.10.4415-4426.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Griffith J. K., Baker M. E., Rouch D. A., Page M. G., Skurray R. A., Paulsen I. T., Chater K. F., Baldwin S. A., Henderson P. J. Membrane transport proteins: implications of sequence comparisons. Curr Opin Cell Biol. 1992 Aug;4(4):684–695. doi: 10.1016/0955-0674(92)90090-y. [DOI] [PubMed] [Google Scholar]
  7. Gunn F. J., Tate C. G., Henderson P. J. Identification of a novel sugar-H+ symport protein, FucP, for transport of L-fucose into Escherichia coli. Mol Microbiol. 1994 Jun;12(5):799–809. doi: 10.1111/j.1365-2958.1994.tb01066.x. [DOI] [PubMed] [Google Scholar]
  8. Henderson P. J., Baldwin S. A., Cairns M. T., Charalambous B. M., Dent H. C., Gunn F., Liang W. J., Lucas V. A., Martin G. E., McDonald T. P. Sugar-cation symport systems in bacteria. Int Rev Cytol. 1992;137:149–208. [PubMed] [Google Scholar]
  9. Henderson P. J. The 12-transmembrane helix transporters. Curr Opin Cell Biol. 1993 Aug;5(4):708–721. doi: 10.1016/0955-0674(93)90144-f. [DOI] [PubMed] [Google Scholar]
  10. Hoyer L. L., Hamilton A. C., Steenbergen S. M., Vimr E. R. Cloning, sequencing and distribution of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol Microbiol. 1992 Apr;6(7):873–884. doi: 10.1111/j.1365-2958.1992.tb01538.x. [DOI] [PubMed] [Google Scholar]
  11. Izard T., Lawrence M. C., Malby R. L., Lilley G. G., Colman P. M. The three-dimensional structure of N-acetylneuraminate lyase from Escherichia coli. Structure. 1994 May 15;2(5):361–369. doi: 10.1016/s0969-2126(00)00038-1. [DOI] [PubMed] [Google Scholar]
  12. Kawakami B., Kudo T., Narahashi Y., Horikoshi K. Genetic and molecular analyses of Escherichia coli N-acetylneuraminate lyase gene. J Bacteriol. 1986 Jul;167(1):404–406. doi: 10.1128/jb.167.1.404-406.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  14. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  15. Lilley G. G., von Itzstein M., Ivancic N. High-level production and purification of Escherichia coli N-acetylneuraminic acid aldolase (EC 4.1.3.3). Protein Expr Purif. 1992 Oct;3(5):434–440. doi: 10.1016/s1046-5928(05)80047-6. [DOI] [PubMed] [Google Scholar]
  16. Mancini G. M., Beerens C. E., Galjaard H., Verheijen F. W. Functional reconstitution of the lysosomal sialic acid carrier into proteoliposomes. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6609–6613. doi: 10.1073/pnas.89.14.6609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mancini G. M., de Jonge H. R., Galjaard H., Verheijen F. W. Characterization of a proton-driven carrier for sialic acid in the lysosomal membrane. Evidence for a group-specific transport system for acidic monosaccharides. J Biol Chem. 1989 Sep 15;264(26):15247–15254. [PubMed] [Google Scholar]
  18. Manoil C., Beckwith J. TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129–8133. doi: 10.1073/pnas.82.23.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Marger M. D., Saier M. H., Jr A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem Sci. 1993 Jan;18(1):13–20. doi: 10.1016/0968-0004(93)90081-w. [DOI] [PubMed] [Google Scholar]
  20. Nowak R. Getting the bugs worked out. Science. 1995 Jan 13;267(5195):172–174. doi: 10.1126/science.7809621. [DOI] [PubMed] [Google Scholar]
  21. Ohta Y., Watanabe K., Kimura A. Complete nucleotide sequence of the E. coli N-acetylneuraminate lyase. Nucleic Acids Res. 1985 Dec 20;13(24):8843–8852. doi: 10.1093/nar/13.24.8843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Petter J. G., Vimr E. R. Complete nucleotide sequence of the bacteriophage K1F tail gene encoding endo-N-acylneuraminidase (endo-N) and comparison to an endo-N homolog in bacteriophage PK1E. J Bacteriol. 1993 Jul;175(14):4354–4363. doi: 10.1128/jb.175.14.4354-4363.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Renlund M., Tietze F., Gahl W. A. Defective sialic acid egress from isolated fibroblast lysosomes of patients with Salla disease. Science. 1986 May 9;232(4751):759–762. doi: 10.1126/science.3961501. [DOI] [PubMed] [Google Scholar]
  24. Rodríguez-Aparicio L. B., Reglero A., Luengo J. M. Uptake of N-acetylneuraminic acid by Escherichia coli K-235. Biochemical characterization of the transport system. Biochem J. 1987 Sep 1;246(2):287–294. doi: 10.1042/bj2460287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Saier M. H., Jr Convergence and divergence in the evolution of transport proteins. Bioessays. 1994 Jan;16(1):23–29. doi: 10.1002/bies.950160104. [DOI] [PubMed] [Google Scholar]
  26. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vimr E. R., Aaronson W., Silver R. P. Genetic analysis of chromosomal mutations in the polysialic acid gene cluster of Escherichia coli K1. J Bacteriol. 1989 Feb;171(2):1106–1117. doi: 10.1128/jb.171.2.1106-1117.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vimr E. R. Microbial sialidases: does bigger always mean better? Trends Microbiol. 1994 Aug;2(8):271–277. doi: 10.1016/0966-842x(94)90003-5. [DOI] [PubMed] [Google Scholar]
  29. Vimr E. R. Selective synthesis and labeling of the polysialic acid capsule in Escherichia coli K1 strains with mutations in nanA and neuB. J Bacteriol. 1992 Oct;174(19):6191–6197. doi: 10.1128/jb.174.19.6191-6197.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Vimr E. R., Troy F. A. Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J Bacteriol. 1985 Nov;164(2):845–853. doi: 10.1128/jb.164.2.845-853.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Vimr E. R., Troy F. A. Regulation of sialic acid metabolism in Escherichia coli: role of N-acylneuraminate pyruvate-lyase. J Bacteriol. 1985 Nov;164(2):854–860. doi: 10.1128/jb.164.2.854-860.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. WARREN L. THE DISTRIBUTION OF SIALIC ACIDS IN NATURE. Comp Biochem Physiol. 1963 Oct;10:153–171. doi: 10.1016/0010-406x(63)90238-x. [DOI] [PubMed] [Google Scholar]
  33. von Heijne G. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol. 1992 May 20;225(2):487–494. doi: 10.1016/0022-2836(92)90934-c. [DOI] [PubMed] [Google Scholar]
  34. von Itzstein M., Wu W. Y., Kok G. B., Pegg M. S., Dyason J. C., Jin B., Van Phan T., Smythe M. L., White H. F., Oliver S. W. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature. 1993 Jun 3;363(6428):418–423. doi: 10.1038/363418a0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES