1887

Abstract

The outer membrane (OM) of almost all Gram-negative bacteria is composed of phospholipids, lipopolysaccharide, proteins and capsular or loosely adherent polysaccharides that together mediate cellular interactions with diverse environments. Most OM components are synthesized intracellularly or at the inner membrane (IM) and thus require an export mechanism. This mini-review focuses on recent progress in understanding how synthesis of one kind of capsular polysaccharide (group 2) is coupled to the export apparatus located in the IM and spanning the periplasmic space, thus providing a transport channel to the cell surface. Although the model system for these investigations is the medically important extraintestinal pathogen K1 and its polysialic acid capsule, the conclusions are general for other group 2 and group 2-like polysaccharides synthesized by many different bacterial species.

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2009-01-01
2024-10-05
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References

  1. Andreischeva E. N., Vann W. F. 2006; Gene products required for de novo synthesis of polysialic acid in Escherichia coli K1. J Bacteriol 188:1786–1797
    [Google Scholar]
  2. Annunziato P. W., Wright L. F., Vann W. F., Silver R. P. 1995; Nucleotide sequence and genetic analysis of the neuD and neuB genes in region 2 of the polysialic acid gene cluster of Escherichia coli K1. J Bacteriol 177:312–319
    [Google Scholar]
  3. Azurmendi H. F., Vionnet J., Wrightson L., Trinh L. B., Shiloach J., Freedberg D. I. 2007; Extracellular structure of polysialic acid explored by on cell solution NMR. Proc Natl Acad Sci U S A 104:11557–11561
    [Google Scholar]
  4. Bos M. P., Robert V., Tommassen J. 2007; Biogenesis of the gram-negative bacterial outer membrane. Annu Rev Microbiol 61:191–214
    [Google Scholar]
  5. Bronner D., Sieberth V., Pazzanik C., Roberts I. S., Boulnois G., Jann B., Jann K. 1993; Expression of the capsular K5 polysaccharide of Escherichia coli: biochemical and electron microscopic analyses of mutants with defects in region 1 of the K5 gene cluster. J Bacteriol 175:5984–5992
    [Google Scholar]
  6. Cieslewicz M., Vimr E. 1996; Thermoregulation of kpsF, the first region 1 gene in the kps locus for polysialic acid biosynthesis in Escherichia coli K1. J Bacteriol 178:3212–3220
    [Google Scholar]
  7. Cieslewicz M., Vimr E. 1997; Reduced polysialic acid capsule expression in Escherichia coli K1 mutants with chromosomal defects in kpsF . Mol Microbiol 26:237–249
    [Google Scholar]
  8. Cuthbertson L., Kimber M. S., Whitfield C. 2007; Substrate binding by a bacterial ABC transporter involved in polysaccharide export. Proc Natl Acad Sci U S A 104:19529–19534
    [Google Scholar]
  9. Daines D. A., Silver R. P. 2000; Evidence for multimerization of Neu proteins involved in polysialic acid synthesis in Escherichia coli K1 using improved LexA-based vectors. J Bacteriol 182:5267–5270
    [Google Scholar]
  10. Finke A., Bronner D., Nikolaev A. V., Jann B., Jann K. 1991; Biosynthesis of the Escherichia coli K5 polysaccharide, a representative of group II capsular polysaccharides: polymerization in vitro and characterization of the product. J Bacteriol 173:4088–4094
    [Google Scholar]
  11. Jann K., Jann B. 1987; Polysaccharide antigens of Escherichia coli . Rev Infect Dis 9:S517–S526
    [Google Scholar]
  12. Karimova G., Pidoux J., Ullmann A., Ladant D. 1998; A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 95:5752–5756
    [Google Scholar]
  13. Karimova G., Dautin N., Ladant D. 2005; Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187:2233–2243
    [Google Scholar]
  14. McNulty C., Thompson J., Barrett B., Lord L., Anderson C., Roberts I. A. 2006; The cell surface expression of group 2 capsular polysaccharides in Escherichia coli: the role of KpsD, RhsA and a multi-protein complex at the pole of the cell. Mol Microbiol 59:907–922
    [Google Scholar]
  15. Ørskov I., Ørskov F., Jann B., Jann K. 1977; Serology, chemistry, and genetics of O and K antigens of Escherichia coli . Bacteriol Rev 41:667–710
    [Google Scholar]
  16. Severi E., Hood D. W., Thomas G. H. 2007; Sialic acid utilization by bacterial pathogens. Microbiology 153:2817–2822
    [Google Scholar]
  17. Silver R. P., Prior K., Nsahlai C., Wright L. F. 2001; ABC transporters and the export of capsular polysaccharides from gram-negative bacteria. Res Microbiol 152:357–364
    [Google Scholar]
  18. Steenbergen S. M., Vimr E. R. 2008; Biosynthesis of the Escherichia coli K1 group 2 polysialic acid capsule occurs within a protected cytoplasmic compartment. Mol Microbiol 68:1252–1267
    [Google Scholar]
  19. Steenbergen S. M., Lee Y. C., Vann W. F., Vionnet J., Wright L. F., Vimr E. R. 2006; Separate pathways for O acetylation of polymeric and monomeric sialic acids and identification of sialyl O-acetyl esterase in Escherichia coli K1. J Bacteriol 188:6195–6206
    [Google Scholar]
  20. Thanabalu T., Koronakis E., Hughes C., Koronakis V. 1998; Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J 17:6487–6496
    [Google Scholar]
  21. Troy F. A., Vijay I. K., Tesche N. 1975; Role of undecaprenyl phosphate in synthesis of polymers containing sialic acid in Escherichia coli . J Biol Chem 250:156–163
    [Google Scholar]
  22. Vimr E. R. 1992; Selective synthesis and labeling of the polysialic acid capsule in Escherichia coli K1 strains with mutations in nanA and neuB . J Bacteriol 174:6191–6197
    [Google Scholar]
  23. Vimr E. R., Steenbergen S. M. 2006; Targeting microbial sialic acid metabolism for new drug development. In Protein–Carbohydrate Interactions in Infectious Disease, pp. 125–150 Edited by C. A. Bewley. London, UK: Royal Society of Chemistry.
    [Google Scholar]
  24. Vimr E. R., Kalivoda K. A., Deszo E. L., Steenbergen S. M. 2004; Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68:132–153
    [Google Scholar]
  25. Vionnet J., Kempner E. S., Vann W. F. 2006; Functional molecular mass of Escherichia coli K92 polysialyltransferase as determined by radiation target analysis. Biochemistry 45:13511–13516
    [Google Scholar]
  26. Weigel P. H., DeAngelis P. L. 2007; Hyaluronan synthases: a decade-plus of novel glycosyltransferases. J Biol Chem 282:36777–36781
    [Google Scholar]
  27. Weisgerber C., Troy F. A. 1990; Biosynthesis of the polysialic acid capsule in Escherichia coli K1. The endogenous acceptor of polysialic acid is a membrane protein of 20 kDa. J Biol Chem 265:1578–1587
    [Google Scholar]
  28. Whitfield C. 2006; Biosynthesis and assembly of capsular polysaccharides in Escherichia coli . Annu Rev Biochem 75:39–68
    [Google Scholar]
  29. Whitfield C., Naismith J. H. 2008; Periplasmic export machines for outer membrane assembly. Curr Opin Struct Biol 18:466–474
    [Google Scholar]
  30. Whitfield C., Paiment A. 2003; Biosynthesis and assembly of group 1 capsular polysaccharides in Escherichia coli and related extracellular polysaccharides in other bacteria. Carbohydr Res 338:2491–2502
    [Google Scholar]
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