Browse > Article
http://dx.doi.org/10.14348/molcells.2016.0202

Structural and Biochemical Studies Reveal a Putative FtsZ Recognition Site on the Z-ring Stabilizer ZapD  

Choi, Hwajung (Department of Chemistry, College of Natural Sciences, Seoul National University)
Min, Kyungjin (Department of Chemistry, College of Natural Sciences, Seoul National University)
Mikami, Bunzo (Laboratory of Quality Design and Exploitation, Division of Agronomy and Horticultural Science, Graduate School of Agriculture, Kyoto University)
Yoon, Hye-Jin (Department of Chemistry, College of Natural Sciences, Seoul National University)
Lee, Hyung Ho (Department of Chemistry, College of Natural Sciences, Seoul National University)
Publication Information
Molecules and Cells / v.39, no.11, 2016 , pp. 814-820 More about this Journal
Abstract
FtsZ, a tubulin homologue, is an essential protein of the Z-ring assembly in bacterial cell division. It consists of two domains, the N-terminal and C-terminal core domains, and has a conserved C-terminal tail region. Lateral interactions between FtsZ protofilaments and several Z-ring associated proteins (Zaps) are necessary for modulating Z-ring formation. ZapD, one of the positive regulators of Z-ring assembly, directly binds to the C-terminal tail of FtsZ and promotes stable Z-ring formation during cytokinesis. To gain structural and functional insights into how ZapD interacts with the C-terminal tail of FtsZ, we solved two crystal structures of ZapD proteins from Salmonella typhimurium (StZapD) and Escherichia coli (EcZapD) at a 2.6 and $3.1{\AA}$ resolution, respectively. Several conserved residues are clustered on the concave sides of the StZapD and EcZapD dimers, the suggested FtsZ binding site. Modeled structures of EcZapD-EcFtsZ and subsequent binding studies using bio-layer interferometry also identified the EcFtsZ binding site on EcZapD. The structural insights and the results of bio-layer interferometry assays suggest that the two FtsZ binding sites of ZapD dimer might be responsible for the binding of ZapD dimer to two protofilaments to hold them together.
Keywords
cell division; cytokinesis; FtsZ; ZapD;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Dundas, J., Ouyang, Z., Tseng, J., Binkowski, A., Turpaz, Y., and Liang, J. (2006). CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res. 34, W116-118.   DOI
2 Durand-Heredia, J., Rivkin, E., Fan, G., Morales, J., and Janakiraman, A. (2012). Identification of ZapD as a cell division factor that promotes the assembly of FtsZ in Escherichia coli. J. Bacteriol. 194, 3189-3198.   DOI
3 Ebersbach, G., Galli, E., Moller-Jensen, J., Lowe, J., and Gerdes, K. (2008). Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol. Microbiol. 68, 720-735.   DOI
4 Osawa, M., Anderson, D.E., and Erickson, H.P. (2009). Curved FtsZ protofilaments generate bending forces on liposome membranes. EMBO J. 28, 3476-3484.   DOI
5 Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. Part A 276, 307-326.   DOI
6 Pichoff, S., and Lutkenhaus, J. (2002). Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21, 685-693.   DOI
7 Roach, E.J., Wroblewski, C., Seidel, L., Berezuk, A.M., Brewer, D., Kimber, M.S., and Khursigara, C.M. (2016). Structure and mutational analyses of Escherichia coli ZapD reveal charged residues involved in FtsZ filament bundling. J. Bacteriol. 198, 1683-1693.   DOI
8 Schumacher, M.A., Zeng, W., Huang, K.H., Tchorzewski, L., and Janakiraman, A. (2016). Structural and functional analyses reveal insights into the molecular properties of the Escherichia coli Z ring stabilizing protein, ZapC. J. Biol. Chem. 291, 2485-2498.   DOI
9 Sheffield, P., Garrard, S., and Derewenda, Z. (1999). Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Exp. Purif. 15, 34-39.   DOI
10 Son, S.H., and Lee, H.H. (2013). The N-terminal domain of EzrA binds to the C terminus of FtsZ to inhibit Staphylococcus aureus FtsZ polymerization. Biochem. Biophys. Res. Commun. 433, 108-114.   DOI
11 Son, S.H., and Lee, H.H. (2015). Crystallization and preliminary Xray crystallographic analysis of Z-ring-associated protein (ZapD). from Escherichia coli. Acta Crystallogr. F Struct. Biol. Commun. 71, 194-198.   DOI
12 Sureshan, V., Deshpande, C.N., Boucher, Y., Koenig, J.E., Stokes, H.W., Harrop, S.J., Curmi, P.M., and Mabbutt, B.C. (2013). Integron gene cassettes: a repository of novel protein folds with distinct interaction sites. PLoS One 8, e52934.   DOI
13 Weiss, M.S. (2001). Global indicators of X-ray data quality. J. Appl. Cryst. 34, 130-135.   DOI
14 Huang, K.H., Durand-Heredia, J., and Janakiraman, A. (2013). FtsZ ring stability: of bundles, tubules, crosslinks, and curves. J. Bacteriol. 195, 1859-1868.   DOI
15 Egan, A.J., and Vollmer, W. (2013). The physiology of bacterial cell division. Ann. N Y Acad. Sci. 1277, 8-28.   DOI
16 Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.   DOI
17 Galli, E., and Gerdes, K. (2012). FtsZ-ZapA-ZapB interactome of Escherichia coli. J. Bacteriol. 194, 292-302.   DOI
18 Hale, C.A., and de Boer, P.A. (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.   DOI
19 Holm, L., and Rosenstrom, P. (2010). Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-549.   DOI
20 Huang, K.H., Mychack, A., Tchorzewski, L., and Janakiraman, A. (2016). Characterization of the FtsZ C-Terminal Variable (CTV). region in Z-Ring assembly and interaction with the Z-Ring stabilizer ZapD in E.coli cytokinesis. PLoS One 11, e0153337.   DOI
21 Krissinel, E., and Henrick, K. (2007). Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.   DOI
22 London, N., Raveh, B., Cohen, E., Fathi, G. and Schueler-Furman, O. (2011). Rosetta FlexPepDock web server--high resolution modeling of peptide-protein interactions. Nucleic Acids Res. 39, W249-253.   DOI
23 Low, H.H., Moncrieffe, M.C., and Lowe, J. (2004). The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 341, 839-852.   DOI
24 Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255.   DOI
25 Erickson, H.P. (2009). Modeling the physics of FtsZ assembly and force generation. Proc. Natl. Acad. Sci. USA 106, 9238-9243.   DOI
26 Lowe, J., and van den Ent, F. (2001). Conserved sequence motif at the C-terminus of the bacterial cell-division protein FtsA. Biochimie 83, 117-120.   DOI
27 Ma, X., Sun, Q., Wang, R., Singh, G., Jonietz, E.L., and Margolin, W. (1997). Interactions between heterologous FtsA and FtsZ proteins at the FtsZ ring. J. Bacteriol. 179, 6788-6797.   DOI
28 Margolin, W. (2000). Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24, 531-548.   DOI
29 McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007). Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674.   DOI
30 Ortiz, C., Kureisaite-Ciziene, D., Schmitz, F., McLaughlin, S.H., Vicente, M., and Lowe, J. (2015). Crystal structure of the Z-ring associated cell division protein ZapC from Escherichia coli. FEBS Lett. 589, 3822-3828.   DOI
31 Diederichs, K., and Karplus, P.A. (1997). Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat. Struct. Biol. 4, 269-275.   DOI
32 Adams, D.W., and Errington, J. (2009). Bacterial cell division:assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7, 642-653.   DOI
33 Brunger, A.T. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.   DOI
34 de Boer, P., Crossley, R., and Rothfield, L. (1992). The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359, 254-256.   DOI
35 Diederichs, K., and Karplus, P.A. (2013). Better models by discarding data? Acta Crystallogr. D Biol. Crystallogr. 69, 1215-1222.   DOI