PhpA, a tyrosine phosphatase of Myxococcus xanthus, is involved in the production of exopolysaccharide

Microbiology (United Kingdom)

Volumn 158, Issue 10, 2012, Pages 2546-2555

  Mori, Yumi ^a   Maeda, Miri ^a   Takegawa, Kaoru ^b   Kimura, Yoshio ^a  

^a KAGAWA UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BTKA PROTEIN; EXOPOLYSACCHARIDE; MUTANT PROTEIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; TYROSINE PHOSPHATASE PHPA; UNCLASSIFIED DRUG; VANADATE SODIUM;

ARTICLE; CELL ADHESION; CELL AGGLUTINATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FRUITING BODY; MYXOCOCCUS XANTHUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

BACTERIAL ADHESION; BACTERIAL PROTEINS; KINETICS; MUTATION; MYXOCOCCUS XANTHUS; POLYSACCHARIDES; PROTEIN TYROSINE PHOSPHATASES; SPORES, BACTERIAL;

BACTERIA (MICROORGANISMS); MYXOCOCCUS XANTHUS;

EID: 84867135500     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.059824-0     Document Type: Article

References (49)

1. Aravind, L. & Koonin, E. V. (1998). Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res 26, 3746-3752.
2. Bechet, E., Guiral, S., Torres, S., Mijakovic, I., Cozzone, A. J. & Grangeasse, C. (2009). Tyrosine-kinases in bacteria: from a matter of controversy to the status of key regulatory enzymes. Amino Acids 37, 499-507.
3. Behmlander, R. M. & Dworkin, M. (1994). Biochemical and structural analyses of the extracellular matrix fibrils of Myxococcus xanthus. J Bacteriol 176, 6295-6303.
4. Berleman, J. E., Vicente, J. J., Davis, A. E., Jiang, S. Y., Seo, Y.-E. & Zusman, D. R. (2011). FrzS regulates social motility in Myxococcus xanthus by controlling exopolysaccharide production. PLoS ONE 6, e23920.
5. Bialojan, C. & Takai, A. (1988). Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J 256, 283-290.
6. Black, W. P. & Yang, Z. (2004). Myxococcus xanthus chemotaxis homologs DifD and DifG negatively regulate fibril polysaccharide production. J Bacteriol 186, 1001-1008.
7. Black, W. P., Xu, Q. & Yang, Z. (2006). Type IV pili function upstream of the Dif chemotaxis pathway in Myxococcus xanthus EPS regulation. Mol Microbiol 61, 447-456.
8. Black, W. P., Schubot, F. D., Li, Z. & Yang, Z. (2010). Phosphorylation and dephosphorylation among Dif chemosensory proteins essential for exopolysaccharide regulation in Myxococcus xanthus. J Bacteriol 192, 4267-4274.
9. Bowden, M. G. & Kaplan, H. B. (1998). The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol Microbiol 30, 275-284.
10. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
11. Copeland, R. A. (1996). Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis, pp. 195-197. New York: VCH Publishers.
12. Cozzone, A. J., Grangeasse, C., Doublet, P. & Duclos, B. (2004). Protein phosphorylation on tyrosine in bacteria. Arch Microbiol 181, 171-181.
13. Dabour, N. & LaPointe, G. (2005). Identification and molecular characterization of the chromosomal exopolysaccharide biosynthesis gene cluster from Lactococcus lactis subsp. cremoris SMQ-461. Appl Environ Microbiol 71, 7414-7425.
14. Dana, J. R. & Shimkets, L. J. (1993). Regulation of cohesiondependent cell interactions in Myxococcus xanthus. J Bacteriol 175, 3636-3647.
15. Doublet, P., Grangeasse, C., Obadia, B., Vaganay, E. & Cozzone, A. J. (2002). Structural organization of the protein-tyrosine autokinase Wzc within Escherichia coli cells. J Biol Chem 277, 37339-37348.
16. DuBois, K., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Anal Chem 28, 350-356.
17. Dworkin, M. & Gibson, S. M. (1964). A system for studying microbial morphogenesis: rapid formation of microcysts in Myxococcus xanthus. Science 146, 243-244.
18. Grangeasse, C., Obadia, B., Mijakovic, I., Deutscher, J., Cozzone, A. J. & Doublet, P. (2003). Autophosphorylation of the Escherichia coli protein kinase Wzc regulates tyrosine phosphorylation of Ugd, a UDP-glucose dehydrogenase. J Biol Chem 278, 39323-39329.
19. Grangeasse, C., Cozzone, A. J., Deutscher, J. & Mijakovic, I. (2007). Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem Sci 32, 86-94.
20. Hagelueken, G., Huang, H., Mainprize, I. L., Whitfield, C. & Naismith, J. H. (2009). Crystal structures of Wzb of Escherichia coli and CpsB of Streptococcus pneumoniae, representatives of two families of tyrosine phosphatases that regulate capsule assembly. J Mol Biol 392, 678-688.
21. Hagen, C. D., Bretscher, P. A. & Kaiser, D. (1978). Synergism between morphogenic mutants of Myxococcus xanthus. Dev Biol 64, 284-296.
22. Hodgkin, J. & Kaiser, D. (1979a). Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): genes controlling movement of single cells. Mol Gen Genet 171, 167-176.
23. Hodgkin, J. & Kaiser, D. (1979b). Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): two gene systems control movement. Mol Gen Genet 171, 177-191.
24. Huyer, G., Lin, S., Kelly, J., Moffat, J., Payette, P., Kennedy, B., Tsapralisis, C., Gresser, M. J. & Ramachandran, C. (1997). Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J Biol Chem 272, 843-851.
25. Jaumot, M. & Hancock, J. F., (2001). Protein phosphatases 1 and 2A promote Raf-1 activation by regulating 14-3-3 interactions. Oncogene 20, 3949-3958.
26. Kamibayashi, C., Estes, R., Slaughter, C. & Mumby, M. C. (1991). Subunit interactions control protein phosphatase 2A. Effects of limited proteolysis, N-ethylmaleimide, and heparin on the interaction of the B subunit. J Biol Chem 266, 13251-13260.
27. Kim, H. S., Lee, S. J., Yoon, H. J., An, D. R., Kim, J., Kim, S. J. & Suh, S. W. (2011). Crystal structures of YwqE from Bacillus subtilis and CpsB from Streptococcus pneumoniae, unique metal-dependent tyrosine phosphatases. J Struct Biol 175, 442-450.
28. Kimura, Y., Ishida, S., Matoba, H. & Okahisa, N. (2004). RppA, a transducer homologue, and MmrA, a multidrug transporter homologue, are involved in the biogenesis and/or assembly of polysaccharide in Myxococcus xanthus. Microbiology 150, 631-639.
29. Kimura, Y., Yamashita, S., Mori, Y., Kitajima, Y. & Takegawa, K. (2011). A Myxococcus xanthus bacterial tyrosine kinase, BtkA, is required for the formation of mature spores. J Bacteriol 193, 5853-5857.
30. Kimura, Y., Kato, T. & Mori, Y. (2012). Function analysis of a bacterial tyrosine kinase, BtkB, in Myxococcus xanthus. FEMS Microbiol Lett. (in press).
31. LaPointe, G., Atlan, D. & Gilbert, C. (2008). Characterization and sitedirected mutagenesis of Wzb, an O-phosphatase from Lactobacillus rhamnosus. BMC Biochem 9, 10-21.
32. Mijakovic, I., Poncet, S., Boël, G., Mazé, A., Gillet, S., Jamet, E., Decottignies, P., Grangeasse, C., Doublet, P. &other authors (2003). Transmembrane modulator-dependent bacterial tyrosine kinase activates UDP-glucose dehydrogenases. EMBO J 22, 4709-4718.
33. Mijakovic, I., Musumeci, L., Tautz, L., Petranovic, D., Edwards, R. A., Jensen, P. R., Mustelin, T., Deutscher, J. & Bottini, N. (2005). In vitro characterization of the Bacillus subtilis protein tyrosine phosphatase YwqE. J Bacteriol 187, 3384-3390.
34. Minic, Z., Marie, C., Delorme, C., Faurie, J.-M., Mercier, G., Ehrlich, D. & Renault, P. (2007). Control of EpsE, the phosphoglycosyltransferase initiating exopolysaccharide synthesis in Streptococcus thermophilus, by EpsD tyrosine kinase. J Bacteriol 189, 1351-1357.
35. Morona, J. K., Morona, R., Miller, D. C. & Paton, J. C. (2002). Streptococcus pneumoniae capsule biosynthesis protein CpsB is a novel manganese-dependent phosphotyrosine-protein phosphatase. J Bacteriol 184, 577-583.
36. 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.
37. Müller, F. D., Schink, C. W., Hoiczyk, E., Cserti, E. & Higgs, P. I. (2012). Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol Microbiol 83, 486-505.
38. Paiment, A., Hocking, J. & Whitfield, C. (2002). Impact of phosphorylation of specific residues in the tyrosine autokinase, Wzc, on its activity in assembly of group 1 capsules in Escherichia coli. J Bacteriol 184, 6437-6447.
39. Petters, T., Zhang, X., Nesper, J., Treuner-Lange, A., Gomez-Santos, N., Hoppert, M., Jenal, U. & Søgaard-Andersen, L. (2012). The orphan histidine protein kinase SgmT is a c-di-GMP receptor and regulates composition of the extracellular matrix together with the orphan DNA binding response regulator DigR in Myxococcus xanthus. Mol Microbiol 84, 147-165.
40. Plamann, L., Kuspa, A. & Kaiser, D. (1992). The Myxococcus xanthus asgA gene encodes a novel signal transduction protein required for multicellular development. J Bacteriol 174, 3311-3318.
41. Shi, Y. (2009). Serine/threonine phosphatases: mechanism through structure. Cell 139, 468-484.
42. Shi, L., Kobir, A., Jers, C. & Mijakovic, I. (2010). Bacterial protein- tyrosine kinases. Curr Proteomics 7, 188-194.
43. Velicer, G. J. & Vos, M. (2009). Sociobiology of the myxobacteria. Annu Rev Microbiol 63, 599-623.
44. Vincent, C., Doublet, P., Grangeasse, C., Vaganay, E., Cozzone, A. J. & Duclos, B. (1999). Cells of Escherichia coli contain a proteintyrosine kinase, Wzc, and a phosphotyrosine-protein phosphatase, Wzb. J Bacteriol 181, 3472-3477.
45. Weimer, R. M., Creighton, C., Stassinopoulos, A., Youderian, P. & Hartzell, P. L. (1998). A chaperone in the HSP70 family controls production of extracellular fibrils in Myxococcus xanthus. J Bacteriol 180, 5357-5368.
46. Whitworth, D. E. (2007). Myxobacteria: Multicellularity and Differentiation. Washington, DC: American Society for Microbiology.
47. Wu, S. S. & Kaiser, D. (1995). Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol Microbiol 18, 547-558.
48. Wu, S. S., Wu, J. & Kaiser, D. (1997). The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol Microbiol 23, 109-121.
49. Zusman, D. R., Scott, A. E., Yang, Z. & Kirby, J. R. (2007). Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5, 862-872.