Mutational analysis of the major periplasmic loops of shigella flexneri wzy: Identification of the residues affecting o antigen modal chain length control, and wzz-dependent polymerization activity

Microbiology (United Kingdom)

Volumn 161, Issue 4, 2015, Pages 774-785

  Nath, Pratiti ^a   Morona, Renato ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; O ANTIGEN; BACTERIAL PROTEIN; LIPOPOLYSACCHARIDE;

ARTICLE; BACTERIOPHAGE; BIOSYNTHESIS; CONTROLLED STUDY; MUTATIONAL ANALYSIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; SHIGELLA FLEXNERI; SITE DIRECTED MUTAGENESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MUTATION; PHENOTYPE; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; VIROLOGY;

SHIGELLA FLEXNERI; TOBACCO ETCH VIRUS;

BACTERIAL PROTEINS; BACTERIOPHAGES; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPOLYSACCHARIDES; MUTATION; O ANTIGENS; PHENOTYPE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; SHIGELLA FLEXNERI;

EID: 84965000286     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000042     Document Type: Article

References (34)

1. Allison, G. E. & Verma, N. K. (2000). Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri. Trends Microbiol 8, 17–23.
2. Bardhan, P., Faruque, A. S., Naheed, A. & Sack, D. A. (2010). Decrease in shigellosis-related deaths without Shigella spp.-specific interventions, Asia. Emerg Infect Dis 16, 1718–1723.
3. Daniels, C., Vindurampulle, C. & Morona, R. (1998). Overexpression and topology of the Shigella flexneri O-antigen polymerase (Rfc/Wzy). Mol Microbiol 28, 1211–1222.
4. Islam, S. T., Gold, A. C., Taylor, V. L., Anderson, E. M., Ford, R. C. & Lam, J. S. (2011). Dual conserved periplasmic loops possess essential charge characteristics that support a catch-and-release mechanism of O-antigen polymerization by Wzy in Pseudomonas aeruginosa PAO1. J Biol Chem 286, 20600–20605.
5. Islam, S. T., Huszczynski, S. M., Nugent, T., Gold, A. C. & Lam, J. S. (2013). Conserved-residue mutations in Wzy affect O-antigen polymerization and Wzz-mediated chain-length regulation in Pseudomonas aeruginosa PAO1. Sci Rep 3, 3441.
6. Jennison, A. V. & Verma, N. K. (2004). Shigella flexneri infection: pathogenesis and vaccine development. FEMS Microbiol Rev 28, 43–58.
7. Knirel, Y. A., Bystrova, O. V., Kocharova, N. A., Zähringer, U. & Pier, G. B. (2006). Conserved and variable structural features in the lipopolysaccharide of Pseudomonas aeruginosa. J Endotoxin Res 12, 324–336.
8. Lindberg, A. A., Wollin, R., Gemski, P. & Wohlhieter, J. A. (1978). Interaction between bacteriophage Sf6 and Shigella flexneri. J Virol 27, 38–44.
9. Liu, D., Cole, R. A. & Reeves, P. R. (1996). An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J Bacteriol 178, 2102–2107.
10. Marolda, C. L., Tatar, L. D., Alaimo, C., Aebi, M. & Valvano, M. A. (2006). Interplay of the Wzx translocase and the corresponding polymerase and chain length regulator proteins in the translocation and periplasmic assembly of lipopolysaccharide O antigen. J Bacteriol 188, 5124–5135.
11. Mavris, M., Manning, P. A. & Morona, R. (1997). Mechanism of bacteriophage SfII-mediated serotype conversion in Shigella flexneri. Mol Microbiol 26, 939–950.
12. McKinney, J., Guerrier-Takada, C., Galán, J. & Altman, S. (2002). Tightly regulated gene expression system in Salmonella enterica serovar Typhimurium. J Bacteriol 184, 6056–6059.
13. Morona, R. & Van Den Bosch, L. (2003). Lipopolysaccharide O antigen chains mask IcsA (VirG) in Shigella flexneri. FEMS Microbiol Lett 221, 173–180.
14. Morona, R., Mavris, M., Fallarino, A. & Manning, P. A. (1994). Characterization of the rfc region of Shigella flexneri. J Bacteriol 176, 733–747.
15. Morona, R., van den Bosch, L. & Manning, P. A. (1995). Molecular, genetic, and topological characterization of O-antigen chain length regulation in Shigella flexneri. J Bacteriol 177, 1059–1068.
16. Morona, R., Van Den Bosch, L. & Daniels, C. (2000). Evaluation of Wzz/MPA1/MPA2 proteins based on the presence of coiled-coil regions. Microbiology 146, 1–4.
17. Morona, R., Daniels, C. & Van Den Bosch, 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. 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.
19. Nath, P., Tran, E. N. & Morona, R. (2015). Mutational analysis of the Shigella flexneri O-antigen polymerase Wzy: identification of Wzzdependent Wzy mutants. J Bacteriol 197, 108–119.
20. Raetz, C. R. & Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu Rev Biochem 71, 635–700.
21. Ruiz, N., Gronenberg, L. S., Kahne, D. & Silhavy, T. J. (2008). Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci U S A 105, 5537–5542.
22. Sperandeo, P., Dehò, G. & Polissi, A. (2009). The lipopolysaccharide transport system of Gram-negative bacteria. Biochim Biophys Acta 1791, 594–602.
23. Stagg, R. M., Tang, S. S., Carlin, N. I., Talukder, K. A., Cam, P. D. & Verma, N. K. (2009). A novel glucosyltransferase involved in Oantigen modification of Shigella flexneri serotype 1c. J Bacteriol 191, 6612–6617.
24. Sun, Q., Knirel, Y. A., Lan, R., Wang, J., Senchenkova, S. N., Jin, D., Shashkov, A. S., Xia, S., Perepelov, A. V. & other authors (2012). A novel plasmid-encoded serotype conversion mechanism through addition of phosphoethanolamine to the O-antigen of Shigella flexneri. PLoS ONE 7, e46095.
25. Sun, Q., Lan, R., Wang, Y., Wang, J., Wang, Y., Li, P., Du, P. & Xu, J. (2013). Isolation and genomic characterization of SfI, a serotypeconverting bacteriophage of Shigella flexneri. BMC Microbiol 13, 39.
26. Taylor, V. L., Udaskin, M. L., Islam, S. T. & Lam, J. S. (2013). The D3 bacteriophage a-polymerase inhibitor (Iap) peptide disrupts Oantigen biosynthesis through mimicry of the chain length regulator Wzz in Pseudomonas aeruginosa. J Bacteriol 195, 4735–4741.
27. 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 Struct Mol Biol 15, 130–138.
28. Tran, E. N., Papadopoulos, M. & Morona, R. (2014). Relationship between O-antigen chain length and resistance to colicin E2 in Shigella flexneri. Microbiology 160, 589–601.
29. 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.
30. Waldo, G. S., Standish, B. M., Berendzen, J. & Terwilliger, T. C. (1999). Rapid protein-folding assay using green fluorescent protein. Nat Biotechnol 17, 691–695.
31. Wang, P. G., Guo, H., Yi, W. & Song, J. K. (2008). Current understanding on biosynthesis of microbial polysaccharides. Curr Top Med Chem 8, 141–151.
32. Wang, X., Zhang, C., Shi, F. & Hu, X. (2010). Purification and characterization of lipopolysaccharides. Subcell Biochem 53, 27–51.
33. Woodward, R., Yi, W., Li, L., Zhao, G., Eguchi, H., Sridhar, P. R., Guo, H., Song, J. K., Motari, E. & other authors (2010). In vitro bacterial polysaccharide biosynthesis: defining the functions of Wzy and Wzz. Nat Chem Biol 6, 418–423.
34. Zhao, G., Wu, B., Li, L. & Wang, P. G. (2014). O-antigen polymerase adopts a distributive mechanism for lipopolysaccharide biosynthesis. Appl Microbiol Biotechnol 98, 4075–4081.