Relationship between O-antigen chain length and resistance to colicin E2 in Shigella flexneri

Microbiology (United Kingdom)

Volumn 160, Issue PART 3, 2014, Pages 589-601

  Hoa Tran, Elizabeth Ngoc ^a   Papadopoulos, Magdalene ^a   Morona, Renato ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COLICIN; COLICIN E2; LIPOPOLYSACCHARIDE; O ANTIGEN; POLYSACCHARIDE CO POLYMERASE CLASS 1A; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; SHIGELLA FLEXNERI; WILD TYPE;

BACTERIAL PROTEINS; COLICINS; DRUG RESISTANCE, BACTERIAL; LIPOPOLYSACCHARIDES; MICROBIAL SENSITIVITY TESTS; MUTATION; O ANTIGENS; RECEPTORS, CELL SURFACE; SHIGELLA FLEXNERI;

EID: 84896835022     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.074955-0     Document Type: Article

References (39)

1. Achtman, M., Mercer, A., Kusecek, B., Pohl, A., Heuzenroeder, M., Aaronson, W., Sutton, A. & Silver, R. P. (1983). Six widespread bacterial clones among Escherichia coli K1 isolates. Infect Immun 39, 315-335.
2. al-Hendy, A., Toivanen, P. & Skurnik, M. (1992). Lipopolysaccharide O side chain of Yersinia enterocolitica O:3 is an essential virulence factor in an orally infected murine model. Infect Immun 60, 870-875.
3. Bowman, C. M., Sidikaro, J. & Nomura, M. (1971). Specific inactivation of ribosomes by colicin E3 in vitro and mechanism of immunity in colicinogenic cells. Nat New Biol 234, 133-137.
4. Bravo, D., Silva, C., Carter, J. A., Hoare, A., Alvarez, S. A., Blondel, C. J., Zaldívar, M., Valvano, M. A. & Contreras, I. (2008). Growth-phase regulation of lipopolysaccharide O-antigen chain length influences serumresistance in serovars of Salmonella. JMed Microbiol 57, 938-946.
5. Crawford, R. W., Keestra, A. M., Winter, S. E., Xavier, M. N., Tsolis, R. M., Tolstikov, V. & Bäumler, A. J. (2012). Very long O-antigen chains enhance fitness during Salmonella-induced colitis by increasing bile resistance. PLoS Pathog 8, e1002918.
6. Crawford, R. W., Wangdi, T., Spees, A. M., Xavier, M. N., Tsolis, R. M. & Bäumler, A. J. (2013). Loss of very-long O-antigen chains optimizes capsule-mediated immune evasion by Salmonella enterica serovar Typhi. MBio 4, e00232-13.
7. Daniels, C. & Morona, R. (1999). Analysis of Shigella flexneri wzz (Rol) function by mutagenesis and cross-linking: wzz is able to oligomerize. Mol Microbiol 34, 181-194.
8. Davies, J. K. & Reeves, P. (1975). Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A. J Bacteriol 123, 102-117.
9. Franco, A. V., Liu, D. & Reeves, P. R. (1998). The wzz (cld) protein in Escherichia coli: amino acid sequence variation determines O-antigen chain length specificity. J Bacteriol 180, 2670-2675.
10. Hong, M. & Payne, S. M. (1997). Effect of mutations in Shigella flexneri chromosomal and plasmid-encoded lipopolysaccharide genes on invasion and serum resistance. Mol Microbiol 24, 779-791.
11. Kalynych, S., Yao, D., Magee, J. & Cygler, M. (2012). Structural characterization of closely related O-antigen lipopolysaccharide (LPS) chain length regulators. J Biol Chem 287, 15696-15705.
12. Kintz, E., Scarff, J. M., DiGiandomenico, A. & Goldberg, J. B. (2008). Lipopolysaccharide O-antigen chain length regulation in Pseudomonas aeruginosa serogroup O11 strain PA103. J Bacteriol 190, 2709-2716.
13. Lugtenberg, B., Meijers, J., Peters, R., van der Hoek, P. & van Alphen, L. (1975). Electrophoretic resolution of the "major outer membrane protein" of Escherichia coli K12 into four bands. FEBS Lett 58, 254-258.
14. Masi, M., Vuong, P., Humbard, M., Malone, K. & Misra, R. (2007). Initial steps of colicin E1 import across the outer membrane of Escherichia coli. J Bacteriol 189, 2667-2676.
15. May, J. F. & Groisman, E. A. (2013). Conflicting roles for a cell surface modification in Salmonella. Mol Microbiol 88, 970-983.
16. Morona, R., Macpherson, D. F., Van Den Bosch, L., Carlin, N. I. & Manning, P. A. (1995). Lipopolysaccharide with an altered O-antigen produced in Escherichia coli K-12 harbouring mutated, cloned Shigella flexneri rfb genes. Mol Microbiol 18, 209-223.
17. Morona, R., Daniels, C. & VanDenBosch, L. (2003). Genetic modulation of Shigella flexneri 2a lipopolysaccharide O antigen modal chain length reveals that it has been optimized for virulence. Microbiology 149, 925-939.
18. Morona, R., Purins, L., Tocilj, A., Matte, A. & Cygler, M. (2009). Sequence-structure relationships in polysaccharide co-polymerase (PCP) proteins. Trends Biochem Sci 34, 78-84.
19. Murray, G. L., Attridge, S. R. & Morona, R. (2003). Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. Mol Microbiol 47, 1395-1406.
20. Murray, G. L., Attridge, S. R. & Morona, R. (2005). Inducible serum resistance in Salmonella typhimurium is dependent on wzz(fepE)-regulated very long O antigen chains. Microbes Infect 7, 1296-1304.
21. Murray, G. L., Attridge, S. R. & Morona, R. (2006). Altering the length of the lipopolysaccharide O antigen has an impact on the interaction of Salmonella enterica serovar Typhimurium with macrophages and complement. J Bacteriol 188, 2735-2739.
22. Najdenski, H., Golkocheva, E., Vesselinova, A., Bengoechea, J. A. & Skurnik, M. (2003). Proper expression of the O-antigen of lipopolysaccharide is essential for the virulence of Yersinia enterocolitica O:8 in experimental oral infection of rabbits. FEMS Immunol Med Microbiol 38, 97-106.
23. Nomura, M. (1964). Mechanism of action of colicines. Proc Natl Acad Sci U S A 52, 1514-1521.
24. Papadopoulos, M. & Morona, R. (2010). Mutagenesis and chemical cross-linking suggest that Wzz dimer stability and oligomerization affect lipopolysaccharide O-antigen modal chain length control. J Bacteriol 192, 3385-3393.
25. Purins, L., Van Den Bosch, L., Richardson, V. & Morona, R. (2008). Coiled-coil regions play a role in the function of the Shigella flexneri O-antigen chain length regulatorWzzpHS2. Microbiology 154, 1104-1116.
26. Raetz, C. R. & Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu Rev Biochem 71, 635-700.
27. Riley, M. A. & Gordon, D. M. (1999). The ecological role of bacteriocins in bacterial competition. Trends Microbiol 7, 129-133.
28. Samuel, G. & Reeves, P. (2003). Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res 338, 2503-2519.
29. Sharma, O., Yamashita, E., Zhalnina, M. V., Zakharov, S. D., Datsenko, K. A., Wanner, B. L. & Cramer, W. A. (2007). Structure of the complex of the colicin E2 R-domain and its BtuB receptor. The outer membrane colicin translocon. J Biol Chem 282, 23163-23170.
30. Sharma, O., Datsenko, K. A., Ess, S. C., Zhalnina, M. V., Wanner, B. L. & Cramer, W. A. (2009). Genome-wide screens: novel mechanisms in colicin import and cytotoxicity. Mol Microbiol 73, 571-585.
31. Smajs, D., Pilsl, H. & Braun, V. (1997). Colicin U, a novel colicin produced by Shigella boydii. J Bacteriol 179, 4919-4928.
32. Stevenson, G., Kessler, A. & Reeves, P. R. (1995). A plasmid-borne O-antigen chain length determinant and its relationship to other chain length determinants. FEMS Microbiol Lett 125, 23-30.
33. Tocilj, A., Munger, C., Proteau, A., Morona, R., Purins, L., Ajamian, E., Wagner, J., Papadopoulos, M., Van Den Bosch, L. & other authors (2008). Bacterial polysaccharide co-polymerases share a common framework for control of polymer length. Nat StructMol Biol 15, 130-138.
34. Tran, E. N. & Morona, R. (2013). Residues located inside the Escherichia coli FepE protein oligomer are essential for lipopolysaccharide Oantigen modal chain length regulation. Microbiology 159, 701-714.
35. Van Den Bosch, L. & Morona, R. (2003). The actin-based motility defect of a Shigella flexneri rmlD rough LPS mutant is not due to loss of IcsA polarity. Microb Pathog 35, 11-18.
36. Van Den Bosch, L., Manning, P. A. & Morona, R. (1997). Regulation of O-antigen chain length is required for Shigella flexneri virulence. Mol Microbiol 23, 765-775.
37. van der Ley, P., de Graaff, P. & Tommassen, J. (1986). Shielding of Escherichia coli outer membrane proteins as receptors for bacteriophages and colicins by O-antigenic chains of lipopolysaccharide. J Bacteriol 168, 449-451.
38. Wang, R. F. & Kushner, S. R. (1991). Construction of versatile lowcopy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100, 195-199.
39. Zhang, L., Radziejewska-Lebrecht, J., Krajewska-Pietrasik, D., Toivanen, P. & Skurnik, M. (1997). Molecular and chemical characterization of the lipopolysaccharide O-antigen and its role in the virulence of Yersinia enterocolitica serotype O:8. Mol Microbiol 23, 63-76.