Characterization of a novel sialic acid transporter of the sodium solute symporter (SSS) family and in vivo comparison with known bacterial sialic acid transporters

FEMS Microbiology Letters

Volumn 304, Issue 1, 2010, Pages 47-54

  Severi, Emmanuele ^a   Hosie, Arthur H F ^b   Hawkhead, Judith A ^a   Thomas, Gavin H ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Salmonella typhumurium; Sialic acid; Transporter

Indexed keywords

CARRIER PROTEIN; COTRANSPORTER; SIALIC ACID TRANSPORTER; SODIUM SOLUTE SYMPORTER; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; COMPARATIVE STUDY; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE;

BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HAEMOPHILUS INFLUENZAE; HUMANS; MEMBRANE TRANSPORT PROTEINS; N-ACETYLNEURAMINIC ACID; ORGANIC ANION TRANSPORTERS; SALMONELLA TYPHIMURIUM; SYMPORTERS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 76349112697     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2009.01881.x     Document Type: Article

References (29)

1. Allen S, Zaleski A, Johnston JW, Gibson BW Apicella MA (2005) Novel sialic acid transporter of Haemophilus influenzae. Infect Immun 73 : 5291 5300.
2. Almagro-Moreno S Boyd EF (2009) Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 9 : 118.
3. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2 : 2006.0008.
4. Bouchet V, Hood DW, Li J et al 2003) Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. P Natl Acad Sci USA 100 : 8898 8903.
5. Brigham C, Caughlan R, Gallegos R, Dallas MB, Godoy VG Malamy MH (2009) Sialic acid (N-acetyl neuraminic acid) utilization by Bacteroides fragilis requires a novel N-acetyl mannosamine epimerase. J Bacteriol 191 : 3629 3638.
6. Chang DE, Smalley DJ, Tucker DL et al 2004) Carbon nutrition of Escherichia coli in the mouse intestine. P Natl Acad Sci USA 101 : 7427 7432.
7. Condemine G, Berrier C, Plumbridge J Ghazi A (2005) Function and expression of an N-acetylneuraminic acid-inducible outer membrane channel in Escherichia coli. J Bacteriol 187 : 1959 1965.
8. Datsenko KA Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. P Natl Acad Sci USA 97 : 6640 6645.
9. Johnston JW, Zaleski A, Allen S, Mootz JM, Armbruster D, Gibson BW, Apicella MA Munson RS Jr. (2007) Regulation of sialic acid transport and catabolism in Haemophilus influenzae. Mol Microbiol 66 : 26 39.
10. Johnston JW, Coussens NP, Allen S, Houtman JC, Turner KH, Zaleski A, Ramaswamy S, Gibson BW Apicella MA (2008) Characterization of the N-acetyl-5-neuraminic acid-binding site of the extracytoplasmic solute receptor (SiaP) of nontypeable Haemophilus influenzae strain 2019. J Biol Chem 283 : 855 865.
11. Kelly DJ Thomas GH (2001) The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol Rev 25 : 405 424.
12. Martinez J, Steenbergen S 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.
13. Muller A, Severi E, Mulligan C, Watts AG, Kelly DJ, Wilson KS, Wilkinson AJ Thomas GH (2006) Conservation of structure and mechanism in primary and secondary transporters exemplified by SiaP, a sialic acid binding virulence factor from Haemophilus influenzae. J Biol Chem 281 : 22212 22222.
14. Mulligan C, Geertsma ER, Severi E, Kelly DJ, Poolman B Thomas GH (2009) The substrate-binding protein imposes directionality on an electrochemical sodium gradient-driven TRAP transporter. P Natl Acad Sci USA 106 : 1778 1783.
15. Neidhardt FC, Bloch PL Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119 : 736 747.
16. Nikaido H Vaara M (1985) Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49 : 1 32.
17. Poolman B Konings WN (1993) Secondary solute transport in bacteria. Biochim Biophys Acta 1183 : 5 39.
18. Post DM, Mungur R, Gibson BW Munson RS Jr. (2005) Identification of a novel sialic acid transporter in Haemophilus ducreyi. Infect Immun 73 : 6727 6735.
19. Sampson BA, Misra R Benson SA (1989) Identification and characterization of a new gene of Escherichia coli K-12 involved in outer membrane permeability. Genetics 122 : 491 501.
20. Schauer R (2004) Sialic acids: fascinating sugars in higher animals and man. Zoology (Jena) 107 : 49 64.
21. Severi E, Randle G, Kivlin P, Whitfield K, Young R, Moxon R, Kelly D, Hood D Thomas GH (2005) 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. Mol Microbiol 58 : 1173 1185.
22. Severi E, Hood DW Thomas GH (2007) Sialic acid utilization by bacterial pathogens. Microbiology 153 : 2817 2822.
23. Severi E, Muller A, Potts JR, Leech A, Williamson D, Wilson KS Thomas GH (2008) Sialic acid mutarotation is catalyzed by the Escherichia coli {beta}-propeller protein YjhT. J Biol Chem 283 : 4841 4849.
24. Sperandeo P, Lau FK, Carpentieri A, De Castro C, Molinaro A, Deho G, Silhavy TJ Polissi A (2008) Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190 : 4460 4469.
25. Teplyakov A, Obmolova G, Toedt J, Galperin MY Gilliland GL (2005) Crystal structure of the bacterial YhcH protein indicates a role in sialic acid catabolism. J Bacteriol 187 : 5520 5527.
26. Thompson H, Homer KA, Rao S, Booth V Hosie AH (2009) An orthologue of Bacteroides fragilis NanH is the principal sialidase in Tannerella forsythia. J Bacteriol 191 : 3623 3628.
27. Vimr ER Troy FA (1985) Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J Bacteriol 164 : 845 853.
28. Vimr ER, Kalivoda KA, Deszo EL Steenbergen SM (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol R 68 : 132 153.
29. Wang RF Kushner SR (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100 : 195 199.