Oligomerization of FtsZ converts the FtsZ tail motif (conserved carboxy-terminal peptide) into a multivalent ligand with high avidity for partners ZipA and SlmA

Molecular Microbiology

Volumn 95, Issue 2, 2015, Pages 173-188

  Du, Shishen ^a   Park, Kyung Tae ^a   Lutkenhaus, Joe ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; FTSZ PROTEIN; MAGNESIUM ION; MONOMER; SLMA PROTEIN; UNCLASSIFIED DRUG; ZIPA PROTEIN; CARRIER PROTEIN; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; ESCHERICHIA COLI PROTEIN; FTSZ PROTEIN, BACTERIA; LIGAND; MEMBRANE PROTEIN; PROTEIN BINDING; SLMA PROTEIN, E COLI; ZIPA PROTEIN, E COLI;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHIMERA; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIMERIZATION; HYDROLYSIS; IN VITRO STUDY; MUTANT; NONHUMAN; OLIGOMERIZATION; PH; PLASMID; PROTEIN PROTEIN INTERACTION; WILD TYPE; CELL DIVISION; CHEMISTRY; ESCHERICHIA COLI; METABOLISM; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION;

ESCHERICHIA COLI;

BACTERIAL PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIGANDS; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION;

EID: 84920656474     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12854     Document Type: Article

References (49)

1. Bi, E.F., and Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
2. de Boer, P.A., Crossley, R.E., Hand, A.R., and Rothfield, L.I. (1991) The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J 10: 4371-4380.
3. Buckstein, M.H., He, J., and Rubin, H. (2008) Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J Bacteriol 190: 718-726.
4. Buske, P.J., and 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.
5. Buske, P.J., and Levin, P.A. (2013) A flexible C-terminal linker is required for proper FtsZ assembly in vitro and cytokinetic ring formation in vivo. Mol Microbiol 89: 249-263.
6. Camberg, J.L., Hoskins, J.R., and Wickner, S. (2009) ClpXP protease degrades the cytoskeletal protein, FtsZ, and modulates FtsZ polymer dynamics. Proc Natl Acad Sci USA 106: 10614-10619.
7. Camberg, J.L., Viola, M.G., Rea, L., Hoskins, J.R., and Wickner, S. (2014) Location of dual sites in E. coli FtsZ important for degradation by ClpXP; one at the C-terminus and one in the disordered linker. PLoS ONE 9: e94964.
8. Cho, H., McManus, H.R., Dove, S.L., and Bernhardt, T.G. (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci USA 108: 3773-3778.
9. Du, S., and Lutkenhaus, J. (2014) SlmA antagonism of FtsZ assembly employs a two-pronged mechanism like MinCD. PLoS Genet 10: e1004460.
10. Duman, R., Ishikawa, S., Celik, I., Strahl, H., Ogasawara, N., Troc, P., etal. (2013) Structural and genetic analyses reveal the protein SepF as a new membrane anchor for the Z ring. Proc Natl Acad Sci USA 110: E4601-E4610.
11. 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.
12. Erickson, H.P., Anderson, D.E., and Osawa, M. (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74: 504-528.
13. Fu, G., Huang, T., Buss, J., Coltharp, C., Hensel, Z., and Xiao, J. (2010) In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS ONE 5: e12682.
14. Gardner, K.A., Moore, D.A., and Erickson, H.P. (2013) The C-terminal linker of Escherichia coli FtsZ functions as an intrinsically disordered peptide. Mol Microbiol 89: 264-275.
15. Hale, C.A., Rhee, A.C., and de Boer, P.A. (2000) ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J Bacteriol 182: 5153-5166.
16. Haney, S.A., Glasfeld, E., Hale, C., Keeney, D., He, Z., and 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.
17. Hernandez-Rocamora, V.M., Garcia-Montanes, C., Rivas, G., and Llorca, O. (2012a) Reconstitution of the Escherichia coli cell division ZipA-FtsZ complexes in nanodiscs as revealed by electron microscopy. J Struct Biol 180: 531-538.
18. Hernandez-Rocamora, V.M., Reija, B., Garcia, C., Natale, P., Alfonso, C., Minton, A.P., etal. (2012b) Dynamic interaction of the Escherichia coli cell division ZipA and FtsZ proteins evidenced in nanodiscs. J Biol Chem 287: 30097-30104.
19. Hu, Z., Mukherjee, A., Pichoff, S., and Lutkenhaus, J. (1999) The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci USA 96: 14819-14824.
20. Hu, Z., Saez, C., and Lutkenhaus, J. (2003) Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: role of MinD and MinE. J Bacteriol 185: 196-203.
21. Krol, E., van Kessel, S.P., van Bezouwen, L.S., Kumar, N., Boekema, E.J., and Scheffers, D.J. (2012) Bacillus subtilis SepF binds to the C-terminus of FtsZ. PLoS ONE 7: e43293.
22. Kuchibhatla, A., Bhattacharya, A., and Panda, D. (2011) ZipA binds to FtsZ with high affinity and enhances the stability of FtsZ protofilaments. PLoS ONE 6: e28262.
23. Li, Y., Hsin, J., Zhao, L., Cheng, Y., Shang, W., Huang, K.C., etal. (2013) FtsZ protofilaments use a hinge-opening mechanism for constrictive force generation. Science 341: 392-395.
24. Loose, M., and Mitchison, T.J. (2014) The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 16: 38-46.
25. Lutkenhaus, J. (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-562.
26. Lutkenhaus, J., Pichoff, S., and Du, S. (2012) Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton 69: 778-790.
27. Ma, X., and Margolin, W. (1999) Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181: 7531-7544.
28. Martos, A., Alfonso, C., Lopez-Navajas, P., Ahijado-Guzmn, R., Mingorance, J., Minton, A.P., and Rivas, G. (2010) Characterization of self-association and heteroassociation of bacterial cell division proteins FtsZ and ZipA in solution by composition gradient-static light scattering. Biochemistry 49: 10780-10787.
29. Mateos-Gil, P., Marquez, I., Lopez-Navajas, P., Jimenez, M., Vicente, M., Mingorance, J., etal. (2012) FtsZ polymers bound to lipid bilayers through ZipA form dynamic two dimensional networks. Biochim Biophys Acta 1818: 806-813.
30. Mohammadi, T., Ploeger, G.E., Verheul, J., Comvalius, A.D., Martos, A., Alfonso, C., etal. (2009) The GTPase activity of Escherichia coli FtsZ determines the magnitude of the FtsZ polymer bundling by ZapA in vitro. Biochemistry 48: 11056-11066.
31. Mosyak, L., Zhang, Y., Glasfeld, E., Haney, S., Stahl, M., Seehra, J., and 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.
32. Mukherjee, A., and Lutkenhaus, J. (1998) Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J 17: 462-469.
33. Oldfield, C.J., Meng, J., Yang, J.Y., Yang, M.Q., Uversky, V.N., and Dunker, A.K. (2008) Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9 (Suppl. 1): S1.
34. 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.
35. RayChaudhuri, D. (1999) ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J 18: 2372-2383.
36. Shen, B., and Lutkenhaus, J. (2009) The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinC(C)/MinD. Mol Microbiol 72: 410-424.
37. Shen, B., and Lutkenhaus, J. (2010) Examination of the interaction between FtsZ and MinCN in E. coli suggests how MinC disrupts Z rings. Mol Microbiol 75: 1285-1298.
38. Shereda, R.D., Kozlov, A.G., Lohman, T.M., Cox, M.M., and Keck, J.L. (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit Rev Biochem Mol Biol 43: 289-318.
39. Singh, J.K., Makde, R.D., Kumar, V., and Panda, D. (2007) A membrane protein, EzrA, regulates assembly dynamics of FtsZ by interacting with the C-terminal tail of FtsZ. Biochemistry 46: 11013-11022.
40. Singh, J.K., Makde, R.D., Kumar, V., and Panda, D. (2008) SepF increases the assembly and bundling of FtsZ polymers and stabilizes FtsZ protofilaments by binding along its length. J Biol Chem 283: 31116-31124.
41. Skoog, K., and Daley, D.O. (2012) The Escherichia coli cell division protein ZipA forms homodimers prior to association with FtsZ. Biochemistry 51: 1407-1415.
42. Sossong, T.M., Jr, Brigham-Burke, M.R., Hensley, P., and Pearce, K.H., Jr. (1999) Self-activation of guanosine triphosphatase activity by oligomerization of the bacterial cell division protein FtsZ. Biochemistry 38: 14843-14850.
43. Strauss, M.P., Liew, A.T., Turnbull, L., Whitchurch, C.B., Monahan, L.G., and Harry, E.J. (2012) 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol 10: e1001389.
44. Stricker, J., Maddox, P., Salmon, E.D., and Erickson, H.P. (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci USA 99: 3171-3175.
45. Szwedziak, P., Wang, Q., Freund, S.M., and Lowe, J. (2012) FtsA forms actin-like protofilaments. EMBO J 31: 2249-2260.
46. Thanbichler, M., and Shapiro, L. (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126: 147-162.
47. Tonthat, N.K., Arold, S.T., Pickering, B.F., Van Dyke, M.W., Liang, S., Lu, Y., etal. (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30: 154-164.
48. Uversky, V.N. (2013) The most important thing is the tail: multitudinous functionalities of intrinsically disordered protein termini. FEBS Lett 587: 1891-1901.
49. Wang, X., Huang, J., Mukherjee, A., Cao, C., and Lutkenhaus, J. (1997) Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J Bacteriol 179: 5551-5559.