Non-sporulating ftsZ mutants in Streptomyces coelicolor reveal amino acid residues critical for FtsZ polymerization dynamics

Microbiology (United Kingdom)

Volumn 159, Issue PART 5, 2013, Pages 890-901

  Wasserstrom, Sebastian ^a   Grantcharova, Nina ^b   Ubhayasekera, Wimal ^b   Ausmees, Nora ^a   Sandblad, Linda ^c   Flärdh, Klas ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; FTSZ PROTEIN; GUANOSINE TRIPHOSPHATE;

ALLELE; ARTICLE; FILAMENTOUS ALGA; HYDROLYSIS; IN VITRO STUDY; MUTATION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PURIFICATION; SPOROGENESIS; STREPTOMYCES COELICOLOR;

MYCOBACTERIUM TUBERCULOSIS; STREPTOMYCES COELICOLOR;

EID: 84876918305     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.066480-0     Document Type: Article

References (52)

1. Adams, D. W. & Errington, J. (2009). Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7, 642-653.
2. Addinall, S. G., Small, E., Whitaker, D., Sturrock, S., Donachie, W. D. & Khattar, M. M. (2005). New temperature-sensitive alleles of ftsZ in Escherichia coli. J Bacteriol 187, 358-365.
3. Andreu, J. M., Schaffner-Barbero, C., Huecas, S., Alonso, D., Lopez-Rodriguez, M. L., Ruiz-Avila, L. B., Núñez-Ramírez, R., Llorca, O. & Martín-Galiano, A. J. (2010). The antibacterial cell division inhibitor PC190723 is an FtsZ polymer-stabilizing agent that induces filament assembly and condensation. J Biol Chem 285, 14239-14246.
4. Aylett, C. H., Löwe, J. & Amos, L. A. (2011). New insights into the mechanisms of cytomotive actin and tubulin filaments. Int Rev Cell Mol Biol 292, 1-71.
5. Bennett, J. A., Yarnall, J., Cadwallader, A. B., Kuennen, R., Bidey, P., Stadelmaier, B. & McCormick, J. R. (2009). Medium-dependent phenotypes of Streptomyces coelicolor with mutations in ftsI or ftsW. J Bacteriol 191, 661-664.
6. Buske, P. J. & Levin, P. A. (2012). Extreme C terminus of bacterial cytoskeletal protein FtsZ plays fundamental role in assembly independent of modulatory proteins. J Biol Chem 287, 10945-10957.
7. Chen, Y. & Erickson, H. P. (2005). Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J Biol Chem 280, 22549-22554.
8. Chen, Y. & Erickson, H. P. (2011). Conformational changes of FtsZ reported by tryptophan mutants. Biochemistry 50, 4675-4684.
9. Chen, Y., Bjornson, K., Redick, S. D. & Erickson, H. P. (2005). A rapid fluorescence assay for FtsZ assembly indicates cooperative assembly with a dimer nucleus. Biophys J 88, 505-514.
10. Chen, Y., Anderson, D. E., Rajagopalan, M. & Erickson, H. P. (2007). Assembly dynamics of Mycobacterium tuberculosis FtsZ. J Biol Chem 282, 27736-27743.
11. Datta, P., Dasgupta, A., Singh, A. K., Mukherjee, P., Kundu, M. & Basu, J. (2006). Interaction between FtsW and penicillin-binding protein 3 (PBP3) directs PBP3 to mid-cell, controls cell septation and mediates the formation of a trimeric complex involving FtsZ, FtsW and PBP3 in mycobacteria. Mol Microbiol 62, 1655-1673.
12. de Boer, P. A. (2010). Advances in understanding E. coli cell fission. Curr Opin Microbiol 13, 730-737.
13. Del Sol, R., Mullins, J. G., Grantcharova, N., Flärdh, K. & Dyson, P. (2006). Influence of CrgA on assembly of the cell division protein FtsZ during development of Streptomyces coelicolor. J Bacteriol 188, 1540-1550.
14. Din, N., Quardokus, E. M., Sackett, M. J. & Brun, Y. V. (1998). Dominant C-terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA. Mol Microbiol 27, 1051-1063.
15. Elsen, N. L., Lu, J., Parthasarathy, G., Reid, J. C., Sharma, S., Soisson, S. M. & Lumb, K. J. (2012). Mechanism of action of the cell-division inhibitor PC190723: modulation of FtsZ assembly cooperativity. J Am Chem Soc 134, 12342-12345.
16. Erickson, H. P., Anderson, D. E. & Osawa, M. (2010). FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74, 504-528.
17. Feucht, A. & Errington, J. (2005). ftsZ mutations affecting cell division frequency, placement and morphology in Bacillus subtilis. Microbiology 151, 2053-2064.
18. Flärdh, K. (2003). Growth polarity and cell division in Streptomyces. Curr Opin Microbiol 6, 564-571.
19. Flärdh, K. & Buttner, M. J. (2009). Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7, 36-49.
20. Flärdh, K., Leibovitz, E., Buttner, M. J. & Chater, K. F. (2000). Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol Microbiol 38, 737-749.
21. Galli, E. & Gerdes, K. (2010). Spatial resolution of two bacterial cell division proteins: ZapA recruits ZapB to the inner face of the Z-ring. Mol Microbiol 76, 1514-1526.
22. Grantcharova, N., Ubhayasekera, W., Mowbray, S. L., McCormick, J. R. & Flärdh, K. (2003). A missense mutation in ftsZ differentially affects vegetative and developmentally controlled cell division in Streptomyces coelicolor A3(2). Mol Microbiol 47, 645-656.
23. Grantcharova, N., Lustig, U. & Flärdh, K. (2005). Dynamics of FtsZ assembly during sporulation in Streptomyces coelicolor A3(2). J Bacteriol 187, 3227-3237.
24. Hale, C. A. & de Boer, P. A. J. (1997). Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88, 175-185.
25. Hanahan, D. (1983). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557-580.
26. Haney, S. A., Glasfeld, E., Hale, C., Keeney, D., He, Z. & de Boer, P. (2001). Genetic analysis of the Escherichia coli FtsZ.ZipA interaction in the yeast two-hybrid system. Characterization of FtsZ residues essential for the interactions with ZipA and with FtsA. J Biol Chem 276, 11980-11987.
27. Haydon, D. J., Stokes, N. R., Ure, R., Galbraith, G., Bennett, J. M., Brown, D. R., Baker, P. J., Barynin, V. V., Rice, D. W. & other authors (2008). An inhibitor of FtsZ with potent and selective antistaphylococcal activity. Science 321, 1673-1675.
28. Jakimowicz, D. & van Wezel, G. P. (2012). Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol Microbiol 85, 393-404.
29. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47, 110-119.
30. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. A. (2000). Practical Streptomyces Genetics. Norwich, UK: The John Innes Foundation.
31. Kleywegt, G. J., Zou, J. Y., Kjeldgaard, M. & Jones, T. A. (2001). Around O. In International Tables for Crystallography, pp. 353-356. Edited by M. G. Rossmann & E. Arnold. Dordrecht: Kluwer.
32. Leung, A. K., Lucile White, E., Ross, L. J., Reynolds, R. C., DeVito, J. A. & Borhani, D. W. (2004). Structure of Mycobacterium tuberculosis FtsZ reveals unexpected, G protein-like conformational switches. J Mol Biol 342, 953-970.
33. Löwe, J. & Amos, L. A. (1998). Crystal structure of the bacterial celldivision protein FtsZ. Nature 391, 203-206.
34. Lutkenhaus, J., Pichoff, S. & Du, S. (2012). Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton (Hoboken) 69, 778-790.
35. Ma, X. & Margolin, W. (1999). Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181, 7531-7544.
36. Martín-Galiano, A. J., Buey, R. M., Cabezas, M. & Andreu, J. M. (2010). Mapping flexibility and the assembly switch of cell division protein FtsZ by computational and mutational approaches. J Biol Chem 285, 22554-22565.
37. McCormick, J. R. (2009). Cell division is dispensable but not irrelevant in Streptomyces. Curr Opin Microbiol 12, 689-698.
38. McCormick, J. R. & Flärdh, K. (2012). Signals and regulators that govern Streptomyces development. FEMS Microbiol Rev 36, 206-231.
39. McCormick, J. R., Su, E. P., Driks, A. & Losick, R. (1994). Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol Microbiol 14, 243-254
40. Mistry, B. V., Del Sol, R., Wright, C., Findlay, K. & Dyson, P. (2008). FtsW is a dispensable cell division protein required for Z-ring stabilization during sporulation septation in Streptomyces coelicolor. J Bacteriol 190, 5555-5566.
41. Mosyak, L., Zhang, Y., Glasfeld, E., Haney, S., Stahl, M., Seehra, J. & Somers, W. S. (2000). The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J 19, 3179-3191.
42. Oliva, M. A., Cordell, S. C. & Löwe, J. (2004). Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11, 1243-1250.
43. Oliva, M. A., Trambaiolo, D. & Löwe, J. (2007). Structural insights into the conformational variability of FtsZ. J Mol Biol 373, 1229-1242.
44. Pichoff, S. & Lutkenhaus, J. (2005). Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 55, 1722-1734.
45. Plocinski, P., Ziolkiewicz, M., Kiran, M., Vadrevu, S. I., Nguyen, H. B., Hugonnet, J., Veckerle, C., Arthur, M., Dziadek, J. & other authors (2011). Characterization of CrgA, a new partner of the Mycobacterium tuberculosis peptidoglycan polymerization complexes. J Bacteriol 193, 3246-3256.
46. Sambrook, J. & Russel, D. W. (2001). Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
47. Schwedock, J., McCormick, J. R., Angert, E. R., Nodwell, J. R. & Losick, R. (1997). Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol Microbiol 25, 847-858.
48. Shen, B. & Lutkenhaus, J. (2009). The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinCC/MinD. Mol Microbiol 72, 410-424.
49. Tan, C. M., Therien, A. G., Lu, J., Lee, S. H., Caron, A., Gill, C. J., Lebeau-Jacob, C., Benton-Perdomo, L., Monteiro, J. M. & other authors (2012). Restoring methicillin-resistant Staphylococcus aureus susceptibility to b-lactam antibiotics. Sci Transl Med 4, 26ra35.
50. Wang, Y., Jones, B. D. & Brun, Y. V. (2001). A set of ftsZ mutants blocked at different stages of cell division in Caulobacter. Mol Microbiol 40, 347-360.
51. White, E. L., Ross, L. J., Reynolds, R. C., Seitz, L. E., Moore, G. D. & Borhani, D. W. (2000). Slow polymerization of Mycobacterium tuberculosis FtsZ. J Bacteriol 182, 4028-4034.
52. Willemse, J., Borst, J. W., de Waal, E., Bisseling, T. & van Wezel, G. P. (2011). Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev 25, 89-99.