Tyrosine phosphorylation enhances activity of pneumococcal autolysin LytA

Microbiology (United Kingdom)

Volumn 160, Issue , 2014, Pages 2745-2754

  Standish, Alistair J ^a   Whittall, Jonathan J ^a   Morona, Renato ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIETHYLAMINOETHANOL; AUTOLYSIN; BACTERIAL POLYSACCHARIDE; PROTEIN CPSB; PROTEIN CPSC; PROTEIN CPSD; PROTEIN LYTA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; N ACETYLMURAMOYLALANINE AMIDASE; TYROSINE; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; AUTOLYSIS; BACTERIAL MUTATION; BIOSYNTHESIS; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; STREPTOCOCCUS PNEUMONIAE; TURBIDIMETRY; BACTERIOLYSIS; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING;

BACTERIAL PROTEINS; BACTERIOLYSIS; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; STREPTOCOCCUS PNEUMONIAE; TYROSINE; VIRULENCE FACTORS;

EID: 84915748033     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.080747-0     Document Type: Article

References (42)

1. Beard, S. J., Salisbury, V., Lewis, R. J., Sharpe, J. A. & MacGowan, A. P. (2002). Expression of lux genes in a clinical isolate of Streptococcus pneumoniae: using bioluminescence to monitor gemifloxacin activity. Antimicrob Agents Chemother 46, 538-542.
2. Bender, M. H. & Yother, J. (2001). CpsB is a modulator of capsuleassociated tyrosine kinase activity in Streptococcus pneumoniae. J Biol Chem 276, 47966-47974.
3. Berry, A. M. & Paton, J. C. (2000). Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect Immun 68, 133-140.
4. Byrne, J. P., Morona, J. K., Paton, J. C. & Morona, R. (2011). Identification of Streptococcus pneumoniae Cps2C residues that affect capsular polysaccharide polymerization, cell wall ligation, and Cps2D phosphorylation. J Bacteriol 193, 2341-2346.
5. Dalia, A. B. & Weiser, J. N. (2011). Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody. Cell Host Microbe 10, 486-496.
6. De Las Rivas, B., García, J. L., López, R. & García, P. (2002). Purification and polar localization of pneumococcal LytB, a putative endo-b-N-acetylglucosaminidase: the chain-dispersing murein hydrolase. J Bacteriol 184, 4988-5000.
7. Eldholm, V., Johnsborg, O., Haugen, K., Ohnstad, H. S. & Håvarstein, L. S. (2009). Fratricide in Streptococcus pneumoniae: contributions and role of the cell wall hydrolases CbpD, LytA and LytC. Microbiology 155, 2223-2234.
8. Ericsson, D. J., Standish, A., Kobe, B. & Morona, R. (2012). Wzydependent bacterial capsules as potential drug targets. Curr Drug Targets 13, 1421-1431.
9. Fernández-Tornero, C., López, R., García, E., Giménez-Gallego, G. & Romero, A. (2001). A novel solenoid fold in the cell wall anchoring domain of the pneumococcal virulence factor LytA. Nat Struct Biol 8, 1020-1024.
10. Fernández-Tornero, C., García, E., López, R., Giménez-Gallego, G. & Romero, A. (2002). Two new crystal forms of the choline-binding domain of the major pneumococcal autolysin: insights into the dynamics of the active homodimer. J Mol Biol 321, 163-173.
11. Fernebro, J., Andersson, I., Sublett, J., Morfeldt, E., Novak, R., Tuomanen, E., Normark, S. & Normark, B. H. (2004). Capsular expression in Streptococcus pneumoniae negatively affects spontaneous and antibiotic-induced lysis and contributes to antibiotic tolerance. J Infect Dis 189, 328-338.
12. García, E., García, J. L., Ronda, C., García, P. & López, R. (1985). Cloning and expression of the pneumococcal autolysin gene in Escherichia coli. Mol Gen Genet 201, 225-230.
13. García, P., García, J. L., García, E. & López, R. (1986). Nucleotide sequence and expression of the pneumococcal autolysin gene from its own promoter in Escherichia coli. Gene 43, 265-272.
14. Giudicelli, S. & Tomasz, A. (1984). Attachment of pneumococcal autolysin to wall teichoic acids, an essential step in enzymatic wall degradation. J Bacteriol 158, 1188-1190.
15. Goebel, W. F. & Avery, O. T. (1929). A study of pneumococcus autolysis. J Exp Med 49, 267-286.
16. Hansen, A. M., Chaerkady, R., Sharma, J., Díaz-Mejía, J. J., Tyagi, N., Renuse, S., Jacob, H. K., Pinto, S. M., Sahasrabuddhe, N. A. & other authors (2013). The Escherichia coli phosphotyrosine proteome relates to core pathways and virulence. PLoS Pathog 9, e1003403.
17. Henriques, M. X., Rodrigues, T., Carido, M., Ferreira, L. & Filipe, S. R. (2011). Synthesis of capsular polysaccharide at the division septum of Streptococcus pneumoniae is dependent on a bacterial tyrosine kinase. Mol Microbiol 82, 515-534.
18. Kelley, L. A. & Sternberg, M. J. (2009). Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4, 363-371.
19. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
20. Martner, A., Dahlgren, C., Paton, J. C. & Wold, A. E. (2008). Pneumolysin released during Streptococcus pneumoniae autolysis is a potent activator of intracellular oxygen radical production in neutrophils. Infect Immun 76, 4079-4087.
21. McAllister, L. J., Tseng, H. J., Ogunniyi, A. D., Jennings, M. P., McEwan, A. G. & Paton, J. C. (2004). Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Mol Microbiol 53, 889-901.
22. Mellroth, P., Daniels, R., Eberhardt, A., Rönnlund, D., Blom, H., Widengren, J., Normark, S. & Henriques-Normark, B. (2012). LytA, major autolysin of Streptococcus pneumoniae, requires access to nascent peptidoglycan. J Biol Chem 287, 11018-11029.
23. Mellroth, P., Sandalova, T., Kikhney, A., Vilaplana, F., Hesek, D., Lee, M., Mobashery, S., Normark, S., Svergun, D. & other authors (2014). Structural and functional insights into peptidoglycan access for the lytic amidase LytA of Streptococcus pneumoniae. MBio 5, e01120-13.
24. 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.
25. Morona, J. K., Paton, J. C., Miller, D. C. & Morona, R. (2000). Tyrosine phosphorylation of CpsD negatively regulates capsular polysaccharide biosynthesis in Streptococcus pneumoniae. Mol Microbiol 35, 1431- 1442.
26. Morona, J. K., Morona, R.,Miller,D. C. & Paton, J. C. (2002). Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganesedependent phosphotyrosine-protein phosphatase. J Bacteriol 184, 577- 583.
27. Morona, J. K., Miller, D. C., Morona, R. & Paton, J. C. (2004). The effect that mutations in the conserved capsular polysaccharide biosynthesis genes cpsA, cpsB, and cpsD have on virulence of Streptococcus pneumoniae. J Infect Dis 189, 1905-1913.
28. Morona, J. K., Morona, R. & Paton, J. C. (2006). Attachment of capsular polysaccharide to the cell wall of Streptococcus pneumoniae type 2 is required for invasive disease. Proc Natl Acad Sci U S A 103, 8505-8510.
29. Olivares-Illana, V., Meyer, P., Bechet, E., Gueguen-Chaignon, V., Soulat, D., Lazereg-Riquier, S., Mijakovic, I., Deutscher, J., Cozzone, A. J. & other authors (2008). Structural basis for the regulation mechanism of the tyrosine kinase CapB from Staphylococcus aureus. PLoS Biol 6, e143.
30. Romero, P., López, R. & García, E. (2007). Key role of amino acid residues in the dimerization and catalytic activation of the autolysin LytA, an important virulence factor in Streptococcus pneumoniae. J Biol Chem 282, 17729-17737.
31. Rosenow, C., Ryan, P.,Weiser, J. N., Johnson, S., Fontan, P., Ortqvist, A. & Masure, H. R. (1997). Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol Microbiol 25, 819-829.
32. Sanz, J. M., Lopez, R. & Garcia, J. L. (1988). Structural requirements of choline derivatives for 'conversion' of pneumococcal amidase. A new single-step procedure for purification of this autolysin. FEBS Lett 232, 308-312.
33. Soulat, D., Jault, J. M., Duclos, B., Geourjon, C., Cozzone, A. J. & Grangeasse, C. (2006). Staphylococcus aureus operates proteintyrosine phosphorylation through a specific mechanism. J Biol Chem 281, 14048-14056.
34. Standish, A. J. & Morona, R. (2014). The role of bacterial protein tyrosine phosphatases in the regulation of the biosynthesis of secreted polysaccharides. Antioxid Redox Signal 20, 2274-2289.
35. Standish, A. J., Stroeher, U. H. & Paton, J. C. (2005). The twocomponent signal transduction system RR06/HK06 regulates expression of cbpA in Streptococcus pneumoniae. Proc Natl Acad Sci U S A 102, 7701-7706.
36. Standish, A. J., Salim, A. A., Zhang, H., Capon, R. J. & Morona, R. (2012). Chemical inhibition of bacterial protein tyrosine phosphatase suppresses capsule production. PLoS ONE 7, e36312.
37. Standish, A. J., Salim, A. A., Capon, R. J. & Morona, R. (2013). Dual inhibition of DNA polymerase PolC and protein tyrosine phosphatase CpsB uncovers a novel antibiotic target. Biochem Biophys Res Commun 430, 167-172.
38. Sun, X., Ge, F., Xiao, C. L., Yin, X. F., Ge, R., Zhang, L. H. & He, Q. Y. (2010). Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. J Proteome Res 9, 275-282.
39. Sung, C. K., Li, H., Claverys, J. P. & Morrison, D. A. (2001). An rpsL cassette, Janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl Environ Microbiol 67, 5190- 5196.
40. Tomasz, A. & Westphal, M. (1971). Abnormal autolytic enzyme in a pneumococcus with altered teichoic acid composition. Proc Natl Acad Sci U S A 68, 2627-2630.
41. Trappetti, C., Potter, A. J., Paton, A. W., Oggioni, M. R. & Paton, J. C. (2011). LuxS mediates iron-dependent biofilm formation, competence, and fratricide in Streptococcus pneumoniae. Infect Immun 79, 4550-4558.
42. Whitmore, S. E. & Lamont, R. J. (2012). Tyrosine phosphorylation and bacterial virulence. Int J Oral Sci 4, 1-6.