ATP-binding cassette transporters are targets for the development of antibacterial vaccines and therapies

Infection and Immunity

Volumn 72, Issue 12, 2004, Pages 6757-6763

  Garmory, Helen S ^a   Titball, Richard W ^a,b  

^a DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ANTIINFECTIVE AGENT; BACILLUS ANTHRACIS PROTEIN; BACILYSIN; BACTERIAL PROTEIN; BIALAPHOS; BRUCELLA OVIS PROTEIN; DNA VACCINE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS PROTEIN; N 3 (4 METHOXYFUMAROYL) 2,3 DIAMINOPROPANOIC ACID; PHOSPHINOTHRICYL DERIVATIVE; PROTEIN BSPA; PROTEIN CJAA; PROTEIN CJAC; PROTEIN EFAA; PROTEIN PIAA; PROTEIN PIUA; PROTEIN PSAA; PROTEIN PSTS; PROTEIN TROA; PROTEIN TROB; STREPTOCOCCUS AGALACTIAE PROTEIN; UNCLASSIFIED DRUG; VACCINE; VANCOMYCIN; VANCOMYCIN RESISTANT ENTEROCOCCUS FAECIUM PROTEIN;

BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CELL ADHESION; DRUG TARGETING; IMMUNOGENICITY; PRIORITY JOURNAL; SHORT SURVEY;

ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIA; BACTERIAL VACCINES; VIRULENCE;

EID: 9244241532     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.12.6757-6763.2004     Document Type: Short Survey

References (80)

1. Ames, B. N., G. F. Ames, J. D. Young, D. Tsuchiya, and J. Lecocq. 1973. Illicit transport: the oligopeptide permease. Proc. Natl. Acad. Sci. USA 70:456-458.
2. Ariel, N., A. Zvi, H. Grosfeld, O. Gat, Y. Inbar, B. Velan, S. Cohen, and A. Shafferman. 2002. Search for potential vaccine candidate open reading frames in the Bacillus anthracis virulence plasmid pXO1: in silico and in vitro screening. Infect. Immun. 70:6817-6827.
3. Bannantine, J. P., and D. D. Rockey. 1999. Use of a primate model system to identify Chlamydia trachomatis protein antigens recognized uniquely in the context of infection. Microbiology 145:2077-2085.
4. Bearden, S. W., and R. D. Perry. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403-414.
5. Berry, A. M., and J. C. Paton. 1996. Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect. Immun. 64:5255-5262.
6. Blanco, D. R., C. I. Champion, M. M. Exner, H. Erdjument-Bromage, R. E. Hancock, P. Tempst, J. N. Miller, and M. A. Lovett. 1995. Porin activity and sequence analysis of a 31-kilodalton Treponema pallidum subsp. pallidum rare outer membrane protein (Tromp1). J. Bacteriol. 177:3556-3562.
7. Boyer, E., I. Bergevin, D. Malo, P. Gros, and M. F. M. Cellier. 2002. Acquisition of Mn(II) in addition to Fe(II) is required for full virulence in Salmonella enterica serovar Typhimurium. Infect. Immun. 70:6032-6042.
8. Briles, D. E., E. Ades, J. C. Paton, J. S. Sampson, G. M. Carlone, R. C. Huebner, A. Virolainen, E. Swiatlo, and S. K. Hollingshead. 2000. Intranasal immunization of mice with a mixture of the pneumococcal proteins PsaA and PspA is highly protective against nasopharyngeal carriage of Streptococcus pneumoniae. Infect. Immun. 68:796-800.
9. Brown, J. S., S. M. Gilliland, and D. W. Holden. 2001. A Streptococcus pneumoniae pathogenicity island encoding ABC transporter involved in iron uptake and virulence. Mol. Microbiol. 40:572-585.
10. Brown, J. S., A. D. Ogunniyi, M. C. Woodrow, D. W. Holden, and J. C. Paton. 2001. Immunization with components of two iron uptake ABC transporters protects mice against systemic Streptococcus pneumoniae infection. Infect. Immun. 69:6702-6706.
11. Burnette-Curley, D., V. Wells, H. Viscount, C. L. Munro, J. C. Fenno, P. Fives-Taylor, and F. L. Macrina. 1995. FimA, a major virulence factor associated with Streptococcus parasanguis endocarditis. Infect. Immun. 63: 4669-4674.
12. Burnie, J. P., R. C. Matthews, T. Carter, E. Beaulieu, M. Donohoe, C. Chapman, P. Williamson, and S. J. Hodgetts. 2000. Identification of an immunodominant ABC transporter in methicillin-resistant Staphylococcus aureus infections. Infect. Immun. 68:3200-3209.
13. Burnie, J. P., T. Carter, G. Rigg, S. Hodgetts, M. Donohoe, and R. Matthews. 2002. Identification of ABC transporters in vancomycin-resistant Enterococcusfaecium as potential targets for antibody therapy. FEMS Immunol. Med. Microbiol. 33:179-189.
14. Chakraburity, K. 2001. Translational regulation by ABC systems. Res. Microbiol. 152:391-400.
15. Claesson, A., A. M. Jansson, B. G. Pring, S. M. Hammond, and B. Ekstrom. 1987. Design and synthesis of peptide derivatives of a 3-deoxy-D-manno-2- octulosonic acid (KDO) analogue as novel antibacterial agents acting upon lipopolysaccharide biosynthesis. J. Med. Chem. 30:2309-2313.
16. Claverys, J.-P. 2001. A new family of high-affinity ABC manganese and zinc permeases. Res. Microbiol. 152:231-243.
17. Coulter, S. N., W. R. Schwan, E. Y. Ng, M. H. Langhorne, H. D. Ritchie, S. Westbrock-Wadman, W. O. Hufnagle, K. R. Folger, A. S. Bayer, and C. K. Stover. 1998. Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments. Mol. Microbiol. 30:393-404.
18. Darwin, A. J., and V. L. Miller. 1999. Identification of Yersinia enterocolitica genes affecting survival in an animal host using signature-tagged transposon mutagenesis. Mol. Microbiol. 32:51-62.
19. Dassa, E., and P. Bouige. 2001. The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Res. Microbiol. 152:211-229.
20. Detmers, F. J. M., F. C. Lanfermeijer, and B. Poolman. 2001. Peptides and ATP binding cassette peptide transporters. Res. Microbiol. 152:245-258.
21. Fetherston, J. D., J. W. Lillard, Jr., and R. D. Perry. 1995. Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J. Bacteriol. 177:1824-1833.
22. Fetherston, J. D., V. J. Bertolino, and R. D. Perry. 1999. YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol. Microbiol. 32:289-299.
23. Fickel, T. E., and C. Gilvarg. 1973. Transport of impermeant substances in E. coli by way of oligopeptide permease. Nat. New Biol. 241:161-163.
24. Garduno, R. A., E. Garduno, and P. S. Hoffman. 1998. Surface-associated Hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect. Immun. 66:4602-4610.
25. Goosen, N., and G. F. Moolenaar. 2001. Role of ATP hydrolysis by UvrA and UvrB during nucleotide excision repair. Res. Microbiol. 152:401-409.
26. Hammond, S. M., A. Claesson, A. M. Jansson, L. G. Larsson, B. G. Pring, C. M. Town, and B. Ekstrom. 1987. A new class of synthetic antibacterials acting on lipopolysaccharide biosynthesis. Nature 327:730-732.
27. Hardham, J. M., L. V. Stamm, S. F. Porcella, J. G. Frye, N. Y. Barnes, J. K. Howell, S. L. Mueller, J. D. Radolf, G. M. Weinstock, and S. J. Norris. 1997. Identification and transcriptional analysis of a Treponema pallidum operon encoding a putative ABC transport system, an iron-activated repressor protein homolog, and a glycolytic pathway enzyme homolog. Gene 197:47-64.
28. Havlasova, J., L. Hernychova, P. Halada, V. Pellantova, J. Krejsek, J. Stulik, A. Macela, P. R. Jungblut, P. Larsson, and M. Forsman. 2002. Mapping of immunoreactive antigens of Francisella tularensis live vaccine strain. Proteomics 2:857-867.
29. Hennequin, C., F. Porcheray, A. Waligora-Dupriet, A. Collignon, M. Barc, P. Bourlioux, and T. Karjalainen. 2001. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 147:87-96.
30. Hensel, M., J. E. Shea, C. Gleeson, M. D. Jones, E. Dalton, and D. W. Holden. 1995. Simultaneous identification of bacterial virulence genes by negative selection. Science 269:400-403.
31. Higgins, C. 1987. Microbiology-synthesizing designer drugs. Nature 327: 655-656.
32. Higgins, C. F. 2001. ABC transporters: physiology, structure and mechanism-an overview. Res. Microbiol. 152:205-210.
33. Hosie, A. H. F., and P. S. Poole. 2001. Bacterial ABC transporters of amino acids. Res. Microbiol. 152:259-270.
34. Hughes, M. J., R. Wilson, J. C. Moore, J. D. Lane, R. J. Dobson, P. Muckett, Z. Younes, P. Pribul, A. Topping, R. G. Feldman, and J. D. Santangelo. 2003. Novel protein vaccine candidates against group B streptococcal infection identified using alkaline phosphatase fusions. FEMS Microbiol. Lett. 222: 263-271.
35. Igarashi, K., K. Ito, and K. Kashiwagi. 2001. Polyamine uptake systems in Escherichia coli. Res. Microbiol. 152:271-278.
36. Janakiraman, A., and J. M. Slauch. 2000. The putative iron transport system sitABCD encoded on SPII is required for full virulence of Salmonella typhimurium. Mol. Microbiol. 35:1146-1155.
37. Janulczyk, R., S. Ricci, and L. Bjorck. 2003. MtsABC is important for manganese and iron transport, oxidative stress resistance, and virulence of Streptococcus pyogenes. Infect. Immun. 71:2656-2664.
38. Jones, P. M., and A. M. George. 1999. Subunit interactions in ABC transporters: towards a functional architecture. FEMS Microbiol. Lett. 179:187-202.
39. Jungblut, P. R., and D. Bumann. 2002. Immunoproteome of Helicobacter pylori. Methods Enzymol. 358:307-316.
40. Karylshev, A. V., P. C. F. Oyston, K. Williams, G. C. Clark, R. W. Titball, E. A. Winzeler, and B. W. Wren. 2001. Application of high-density array-based signature-tagged mutagenesis to discover novel Yersinia virulence-associated genes. Infect. Immun. 69:7810-7819.
41. Kerr, I. D. 2002. Structure and association of ATP-binding cassette transporter nucleotide-binding domains. Biochim. Biophys. Acta 1561:47-64.
42. Kertesz, M. A. 2001. Bacterial transporters for sulfate and organosulfur compounds. Res. Microbiol. 152:279-290.
43. Kitten, T., C. L. Munro, S. M. Michalek, and F. L. Macrina. 2002. Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect. Immun. 68:4441-4451.
44. 12. Res. Microbiol. 152:291-301.
45. Lefèvre, P., M. Braibant, L. De Wit, M. Kalai, D. Röeper, J. Grötzinger, J.-P. Delville, P. Peirs, J. Ooms, K. Huygen, and J. Content. 1997. Three different putative phosphate transport receptors are encoded by the Mycobacterium tuberculosis genome and are present at the surface of Mycobacterium bovis BCG. J. Bacteriol. 179:2900-2906.
46. Lewis, D. A., J. Klesney-Tait, S. R. Lumbley, C. K. Ward, J. L. Latimer, C. A. Ison, and E. J. Hanson. 1999. Identification of the znuA-encoded periplasmic zinc transport protein of Haemophilus ducreyi. Infect. Immun. 67:5060-5068.
47. Linton, K. J., and C. T. Higgins. 1998. The Escherichia coli ATP-binding cassette (ABC) proteins. Mol. Microbiol. 28:5-13.
48. Lock, R. A., G. W. Coombs, T. M. McWilliams, J. W. Pearman, W. B. Grubb, G. J. Melrose, and G. M. Forbes. 2002. Proteome analysis of highly immunoreactive proteins of Helicobacter pylori. Helicobacter 7:175-182.
49. Marshall, N. J., R. Andruszkiewicz, S. Gupta, S. Milewski, and J. W. Payne. 2003. Structure-activity relationships for a series of peptidomimetic antimicrobial prodrugs containing glutamine analogues. J. Antimicrob. Chemother. 51:821-831.
50. Martin, P. R., and M. H. Hulks. 1999. Cloning and characterization of a gene encoding an antigenic membrane protein from Actinobacillus pleuropneumoniae with homology to ABC transporters. FEMS Immunol. Med. Microbiol. 25:245-254.
51. Matthysse, A. G., H. A. Yarnall, and N. Young. 1996. Requirement for genes with homology to ABC transport systems for attachment and virulence of Agrobacterium tumefaciens. J. Bacteriol. 178:5302-5308.
52. Mei, J.-M., F. Nourbakhsh, C. W. Ford, and D. W. Holden. 1997. Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Mol. Microbiol. 26:399-407.
53. Méndez, C., and J. A. Salas. 2001. The role of ABC transporters in antibiotic-producing organisms: drug secretion and resistance mechanisms. Res. Microbiol. 152:341-350.
54. Nachin, L., M. El Hassouni, L. Loiseau, D. Expert, and F. Barras. 2001. SoxR-dependant response to oxidative stress and virulence of Erwinia chrysanthemi: the key role of SufC, an orphan ABC ATPase. Mol. Microbiol. 39:960-972.
55. Nachin, L., L. Loiseau, D. Expert, and F. Barras. 2003. SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress. EMBO J. 22:427-437.
56. Ogunniyi, A. D., R. L. Folland, D. E. Briles, S. K. Hollingshead, and J. C. Paton. 2000. Immunization of mice with combinations of pneumococcal virulence proteins elicits enhanced protection against challenge with Streptococcus pneumoniae. Infect. Immun. 68:3028-3033.
57. Paik, S., A. Brown, C. L. Munro, C. N. Conrelissen, and T. Kitten. 2003. The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J. Bacteriol. 185:5967-5975.
58. Pawelec, D., E. Rozynek, J. Popowski, and E. K. Jagusztyn-Krynicka. 1997. Cloning and characterization of a Campylobacterjejuni 72Dz/92 gene encoding a 30 kDa immunopositive protein component of the ABC transporter system; expression of the gene in avirulent Salmonella typhimurium. FEMS Immunol. Med. Microbiol. 19:137-150.
59. Pawelec, D., J. Jakubowska-Mróz, and E. K. Jagusztyn-Krynicka. 1998. Campylobacter jejuni 72Dz/92 cjaC gene coding 28 kDa immunopositive protein, a homologue of the solute-binding components of the ABC transport system. Lett. Appl. Microbiol. 26:69-76.
60. Payne, J. W. 1976. Peptides and micro-organisms. Adv. Microb. Physiol. 13:55-113.
61. Polissi, A., A. Pontiggia, G. Feger, M. Altieri, H. Mottl, L. Ferrari, and D. Simon. 1998. Large-scale identification of virulence genes from Streptococcus pneumoniae. Infect. Immun. 66:5620-5629.
62. Rapola, S., V. Jantti, R. Haikala, R. Syrjanen, G. M. Carlone, J. S. Sampson, D. E. Briles, J. C. Paton, A. K. Takala, T. M. Kilpi, and H. Kayhty. 2000. Natural development of antibodies to pneumococcal surface protein A, pneumococcal surface adhesin A, and pneumolysin in relation to pneumococcal carriage and acute otitis media. J. Infect. Dis. 182:1146-1152.
63. Rosinha, G. M. S., D. A. Freitas, A. Miyoshi, V. Azevedo, E. Campos, S. L. Cravero, G. Rossetti, G. Splitter, and S. C. Oliveira. 2002. Identification and characterization of a Brucella abortus ATP-binding cassette transporter homolog to Rhizobium meliloti ExsA and its role in virulence and protection in mice. Infect. Immun. 70:5036-5044.
64. Schneider, E. 2001. ABC transporters catalyzing carbohydrate uptake. Res. Microbiol. 152:303-310.
65. Schneider, E., and S. Hunke. 1998. ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/ domains. FEMS Microbiol. Rev. 22:1-20.
66. Self, W. T., A. M. Grunden, A. Hasona, and K. T. Shanmugam. 2001. Molybdate transport. Res. Microbiol. 152:311-321.
67. Silver, R. P., K. Prior, C. Nsalai, and L. F. Wright. 2001. ABC transporters and the export of capsular polysaccharides from Gram-negative bacteria. Res. Microbiol. 152:357-364.
68. Singh, K. V., T. M. Coque, G. M. Weinstock, and B. E. Murray. 1998. In vivo testing of an Enterococcusfaecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol. Med. Microbiol. 21:323-331.
69. Smith, M. W., and J. W. Payne. 1990. Simultaneous exploitation of different peptide permeases by combinations of synthetic peptide smugglins can lead to enhanced antibacterial activity. FEMS Microbiol. Lett. 70:311-316.
70. Tai, S. S., C. Yu, and J. K. Lee. 2003. A solute binding protein of Streptococcus pneumoniae iron transport. FEMS Microbiol. Lett. 220:303-308.
71. Tame, J. R., G. N. Murshudov, E. J. Dodson, T. K. Neil, G. G. Dodson, C. F. Higgins, and A. J. Wilkinson. 1994. The structural basis of sequence-independent peptide binding by OppA protein. Science 264:1578-1581.
72. Tame, J. R., E. J. Dodson, G. Murshudov, C. F. Higgins, and A. J. Wilkinson. 1995. The crystal structures of the oligopeptide-binding protein OppA complexed with tripeptide and tetrapeptide ligands. Structure 3:1395-1406.
73. Tamura, G. S., A. Nittayajarn, and D. L. Schoentag. 2002. A glutamine transport gene, glnQ, is required for fibronectin adherence and virulence of group B streptococci. Infect. Immun. 70:2877-2885.
74. Tanghe, A., P. Lefèvre, O. Denis, S. D'Souza, M. Braibant, E. Lozes, M. Singh, D. Montgomery, J. Content, and K. Huygen. 1999. Immunogenicity and protective efficacy of tuberculosis DNA vaccines encoding putative phosphate transport receptor. J. Immunol. 162:1113-1119.
75. Teixeira-Gomes, A. P., A. Cloeckaert, G. Bezard, R. A. Bowden, G. Dubray, and M. S. Zygmunt. 1997. Identification and characterization of Brucella ovis immunogenic proteins using two-dimensional electrophoresis and immunoblotting. Electrophoresis 18:1491-1497.
76. Turner, M. S., P. Timms, L. M. Hafner, and P. M. Giffard. 1997. Identification and characterization of a basic cell surface-located protein from Lactobacillus fermentum BR11. J. Bacteriol. 179:3310-3316.
77. van Veen, H. W., C. F. Higgins, and W. N. Konings. 2001. Multidrug transport by ATP binding cassette transporters: a proposed two-cylinder engine mechanism. Res. Microbiol. 152:265-274.
78. Vytvytska, O., E. Nagy, M. Bluggel, H. E. Meyer, R. Kurzbauer, L. A. Huber, C., and S. Klade. 2002. Identification of vaccine candidate antigens of Staphylococcus aureus by serological proteome analysis. Proteomics 2:580-590.
79. Wouters, J. 2003. Crystallography of membrane proteins, major targets in drug design. Mini-Rev. Med. Chem. 3:439-448.
80. Young, J., and I. B. Holland. 1999. ABC transporters: bacterial exporters-revisited five years on. Biochim. Biophys. Acta 1461:177-200.