Sialic acid transport in Haemophilus influenzae is essential for lipopolysaccharide sialylation and serum resistance and is dependent on a novel tripartite ATP-independent periplasmic transporter

Molecular Microbiology

Volumn 58, Issue 4, 2005, Pages 1173-1185

  Severi, Emmanuele ^a   Randle, Gaynor ^b   Kivlin, Polly ^a   Whitfield, Kate ^a   Young, Rosie ^a   Moxon, Richard ^b   Kelly, David ^c   Hood, Derek ^b   Thomas, Gavin H ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; LIPOPOLYSACCHARIDE; N ACETYLNEURAMINIC ACID; SIALIC ACID;

ARTICLE; BACTERIAL STRAIN; BINDING SITE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; GENETIC CODE; HAEMOPHILUS INFLUENZAE; MUTANT; NONHUMAN; NUTRITION; PRIORITY JOURNAL; SIALYLATION; STOICHIOMETRY;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; BLOOD BACTERICIDAL ACTIVITY; GENE DELETION; GENE ORDER; GENES, BACTERIAL; HAEMOPHILUS INFLUENZAE; LIPOPOLYSACCHARIDES; MEMBRANE TRANSPORT PROTEINS; MUTAGENESIS, INSERTIONAL; N-ACETYLNEURAMINIC ACID; PROTEIN BINDING; PROTEIN SUBUNITS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SYNTENY;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE;

EID: 27944469933     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04901.x     Document Type: Article

References (51)

1. Bardor, M., Nguyen, D.H., Diaz, S., and Varki, A. (2005) Mechanism of uptake and incorporation of the non-human sialic acid N-glycolylneuraminic acid into human cells. J Biol Chem 280: 4228-4237.
2. Blakey, D., Leech, A., Thomas, G.H., Coutts, G., Findlay, K., and Merrick, M. (2002) Purification of the Escherichia coli ammonium transporter AmtB reveals a trimeric stoichiometry. Biochem J 364: 527-535.
3. Bouchet, V., Hood, D.W., Li, J., Brisson, J.R., Randle, G.A., Martin, A., et al. (2003) Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. Proc Natl Acad Sci USA 100: 8898-8903.
4. Bulai, T., Bratosin, D., Pons, A., Montreuil, J., and Zanetta, J.P. (2003) Diversity of the human erythrocyte membrane sialic acids in relation with blood groups. FEBS Lett 534: 185-189.
5. Byers, H.L., Homer, K.A., Tarelli, E., and Beighton, D. (1999) N-acetylneuraminic acid transport by Streptococcus oralis strain AR3. J Med Microbiol 48: 375-381.
6. Cash, P., Argo, E., and Bruce, K.D. (1995) Characterisation of Haemophilus influenzae proteins by two-dimensional gel electrophoresis. Electrophoresis 16: 135-148.
7. Coleman, H.N., Daines, D.A., Jarisch, J., and Smith, A.L. (2003) Chemically defined media for growth of Haemophilus influenzae strains. J Clin Microbiol 41: 4408-4410.
8. Condemine, G., Berrier, C., Plumbridge, J., and Ghazi, A. (2005) Function and expression of an N-acetylneuraminic acid-inducible outer membrane channel in Escherichia coli. J Bacteriol 187: 1959-1965.
9. Coulton, J.W., Chin, A.C., and Vachon, V. (1992) Recombinant porin of Haemophilus influenzae type b. J Infect Dis 165(Suppl. 1): S188-S191.
10. Cox, A.D., Hood, D.W., Martin, A., Makepeace, K.M., Deadman, M.E., Li, J., et al. (2002) Identification and structural characterization of a sialylated lacto-N-neotetraose structure in the lipopolysaccharide of Haemophilus influenzae. Eur J Biochem 269: 4009-4019.
11. Doeven, M.K., Abele, R., Tampe, R., and Poolman, B. (2004) The binding specificity of OppA determines the selectivity of the oligopeptide ATP-binding cassette transporter. J Biol Chem 279: 32301-32307.
12. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
13. Forward, J.A., Behrendt, M.C., Wyborn, N.R., Cross, R., and Kelly, D.J. (1997) TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse Gram-negative bacteria. J Bacteriol 179: 5482-5493.
14. Fuller, T.E., Kennedy, M.J., and Lowery, D.E. (2000) Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature-tagged mutagenesis. Microb Pathog 29: 25-38.
15. Grammann, K., Volke, A., and Kunte, H.J. (2002) New type of osmoregulated solute transporter identified in halophilic members of the bacteria domain: TRAP transporter TeaABC mediates uptake of ectoine and hydroxyectoine in Halomonas elongate DSM 2581 (T). J Bacteriol 184: 3078-3085.
16. Herriott, R.M., Meyer, E.M., and Vogt, M. (1970) Defined nongrowth media for stage II development of competence in Haemophilus influenzas. J Bacteriol 101: 517-524.
17. Hood, D.W., and Moxon, E.R. (1999) Lipopolysaccharide phase variation in Haemophilus and Neisseria. In Endotoxin in Health and Disease. Brade, H., Opal, S., Vogel, S., and Morrison, D. (eds). New York: Marcel Dekker, pp. 39-54.
18. Hood, D.W., Makepeace, K., Deadman, M.E., Rest, R.F., Thibault, P., Martin, A., et al. (1999a) Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol Microbiol 33: 679-692.
19. Hood, D.W., Richards, J.C., and Moxon, E.R. (1999b) Haemophilus influenzae lipopolysaccharide. Biochem Soc Trans 27: 493-498.
20. Hood, D.W., Cox, A.D., Gilbert, M., Makepeace, K., Walsh, S., Deadman, M.E., et al. (2001) Identification of a lipopolysaccharide alpha-2,3- sialyltransferase from Haemophilus influenzae. Mol Microbiol 39: 341-350.
21. Inoue, S., Kitajima, K., and Inoue, Y. (1996) Identification of 2-keto-3-deoxy-D-glycero - galactonononic acid (KDN, deaminoneuraminic acid) residues in mammalian tissues and human lung carcinoma cells. Chemical evidence of the occurrence of KDN glycoconjugates in mammals. J Biol Chem 271: 24341-24344.
22. Jermyn, W.S., and Boyd, E.F. (2002) Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 148: 3681-3693.
23. Jermyn, W.S., and Boyd, E.F. (2005) Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates. Microbiology 151: 311-322.
24. Jurcisek, J., Greiner, L., Watanabe, H., Zaleski, A., Apicella, M.A., and Bakaletz, L.O. (2005) Role of sialic acid and complex carbohydrate biosynthesis in biofilm formation by nontypeable Haemophilus influenzae in the chinchilla middle ear. Infect Immun 73: 3210-3218.
25. Kapatral, V., Anderson, I., Ivanova, N., Reznik, G., Los, T., Lykidis, A., et al. (2002) Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 184: 2005-2018.
26. Kelly, D.J., and Thomas, G.H. (2001) The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol Rev 25: 405-424.
27. Kolker, E., Purvine, S., Galperin, M.Y., Stolyar, S., Goodlett, D.R., Nesvizhskii, A.I., et al. (2003) Initial proteome analysis of model microorganism Haemophilus influenzae strain Rd KW20. J Bacteriol 185: 4593-4602.
28. Kolker, E., Makarova, K.S., Shabalina, S., Picone, A.F., Purvine, S., Holzman, T., et al. (2004) Identification and functional analysis of 'hypothetical' genes expressed in Haemophilus influenzae. Nucleic Acids Res 32: 2353-2361.
29. Lesse, A.J., Campagnari, A.A., Bittner, W.E., and Apicella, M.A. (1990) Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J Immunol Methods 126: 109-117.
30. Macfadyen, L.P., and Redfield, R.J. (1996) Life in mucus: sugar metabolism in Haemophilus influenzae. Res Microbiol 147: 541-551.
31. Markwell, M.A., Haas, S.M., Bieber, L.L., and Tolbert, N.E. (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87: 206-210.
32. Martinez, J., Steenbergen, S., and Vimr, E. (1995) Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain. J Bacteriol 177: 6005-6010.
33. Moxon, E.R., and Murphy, T.F. (2000) Haemophilus influenzae. In Mandell, Douglas and Bennett's Principles and Practice of Infectious Disease. Mandell, G.K., Bennett, J.E., and Dolin, R. (eds). Philadelphia, PA: Churchill Livingstone, pp. 2369-2378.
34. Nakano, T., and Ozimek, L. (1999) Determination of sialic acid by the thiobarbituric acid reaction in sweet whey and its fractions. J Agric Food Chem 47: 2613-2616.
35. Neidhardt, F.C., Bloch, P.L., and Smith, D.F. (1974) Culture medium for enterobacteria. J Bacteriol 119: 736-747.
36. Prakash, S., Cooper, G., Singhi, S., and Saier, M.H., Jr (2003) The ion transporter superfamily. Biochim Biophys Acta 1618: 79-92.
37. Quintero, M.J., Montesinos, M.L., Herrero, A., and Flores, E. (2001) Identification of genes encoding amino acid permeases by inactivation of selected ORFs from the Synechocystis genomic sequence. Genome Res 11: 2034-2040.
38. Rabus, R., Jack, D.L., Kelly, D.J., and Saier, M.H., Jr (1999) TRAP transporters: an ancient family of extracytoplasmic solute-receptor-dependent secondary active transporters. Microbiology 145: 3431-3445.
39. Redfield, R.J., Cameron, A.D., Qian, Q., Hinds, J., Ali, T.R., Kroll, J.S., and Langford, P.R. (2005) A novel CRP-dependent regulon controls expression of competence genes in Haemophilus influenzae. J Mol Biol 347: 735-747.
40. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbour, NY: Cold Spring Harbour Press.
41. Shakhnovich, E.A., King, S.J., and Weiser, J.N. (2002) Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect Immun 70: 7161-7164.
42. Solana, S., Reglero, A.A., Martinez-Blanco, H., Revilla-Nuin, B., Bravo, I.G., Rodriguez-Aparicio, L.B., and Ferrero, M.A. (2001) N-Acetylneuraminic acid uptake in Pasteurella (Mannheimia) haemolytica A2 occurs by an inducible and specific transport system. FEBS Lett 509: 41-46.
43. Steenbergen, S.M., Lichtensteiger, C.A., Caughlan, R., Garfinkle, J., Fuller, T.E., and Vimr, E.R. (2005) Sialic Acid metabolism and systemic pasteurellosis. Infect Immun 73: 1284-1294.
44. Tan, K., Moreno-Hagelsieb, G., Collado-Vides, J., and Stormo, G.D. (2001) A comparative genomics approach to prediction of new members of regulons. Genome Res 11: 566-584.
45. Vimr, E.R., and Troy, F.A. (1985) Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J Bacteriol 164: 845-853.
46. Vimr, E., and Lichtensteiger, C. (2002) To sialylate, or not to sialylate: that is the question. Trends Microbiol 10: 254-257.
47. Vimr, E., Lichtensteiger, C., and Steenbergen, S. (2000) Sialic acid metabolism's dual function in Haemophilus influenzae. Mol Microbiol 36: 1113-1123.
48. Vimr, E.R., Kalivoda, K.A., Deszo, E.L., and Steenbergen, S.M. (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68: 132-153. table.
49. Warren, L. (1959) The thiobarbituric acid assay of sialic acids. J Biol Chem 234: 1971-1975.
50. Wilkinson, A.J., and Verschueren, K.H.G. (2003) Crystal structures of periplasmic solute-binding proteins in ABC transport complexes illuminate their function. In ABC Proteins: from Bacteria to Man. Holland, I.B., Cole, S.P.C., Kuchler, K., and Higgins, C.F. (eds). Amsterdam: Elsevier, pp. 187-208.
51. Wyborn, N.R., Alderson, J., Andrews, S.C., and Kelly, D.J. (2001) Topological analysis of DctQ, the small integral membrane protein of the C4-dicarboxylate TRAP transporter of Rhodobacter capsulatus. FEMS Microbiol Lett 194: 13-17.