Identification of the SlmA Active Site Responsible for Blocking Bacterial Cytokinetic Ring Assembly over the Chromosome

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Cho, Hongbaek ^a   Bernhardt, Thomas G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; FTSZ PROTEIN; PROTEIN SLMA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL PHENOMENA AND FUNCTIONS; CYTOKINETIC RING ASSEMBLY; DNA BINDING MOTIF; ENZYME ACTIVE SITE; GENETIC VARIABILITY; NONHUMAN; POLYMERIZATION; PROTEIN CONFORMATION;

BACTERIAL PROTEINS; BINDING SITES; CARRIER PROTEINS; CELL DIVISION; CHROMOSOMES, BACTERIAL; CYTOSKELETAL PROTEINS; DNA REPLICATION; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS;

EID: 84874784097     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003304     Document Type: Article

References (42)

1. de Boer PAJ, (2010) Advances in understanding E. coli cell fission. Curr Opin Microbiol 13: 730-737 doi:10.1016/j.mib.2010.09.015.
2. Bi EF, Lutkenhaus J, (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164 doi:10.1038/354161a0.
3. Durand-Heredia JM, Yu HH, De Carlo S, Lesser CF, Janakiraman A, (2011) Identification and characterization of ZapC, a stabilizer of the FtsZ ring in Escherichia coli. J Bacteriol 193: 1405-1413 doi:10.1128/JB.01258-10.
4. Hale CA, Shiomi D, Liu B, Bernhardt TG, Margolin W, et al. (2011) Identification of Escherichia coli ZapC (YcbW) as a component of the division apparatus that binds and bundles FtsZ polymers. J Bacteriol 193: 1393-1404 doi:10.1128/JB.01245-10.
5. Durand-Heredia J, Rivkin E, Fan G, Morales J, 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:10.1128/JB.00176-12.
6. Aarsman MEG, Piette A, Fraipont C, Vinkenvleugel TMF, Nguyen-Distèche M, et al. (2005) Maturation of the Escherichia coli divisome occurs in two steps. Mol Microbiol 55: 1631-1645 doi:10.1111/j.1365-2958.2005.04502.x.
7. de Boer PA, Crossley RE, Rothfield LI, (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56: 641-649.
8. Yu XC, Margolin W, (1999) FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization. Mol Microbiol 32: 315-326.
9. Woldringh CL, Mulder E, Huls PG, Vischer N, (1991) Toporegulation of bacterial division according to the nucleoid occlusion model. Res Microbiol 142: 309-320.
10. Levin PA, Shim JJ, Grossman AD, (1998) Effect of minCD on FtsZ ring position and polar septation in Bacillus subtilis. J Bacteriol 180: 6048-6051.
11. Wu LJ, Errington J, (2011) Nucleoid occlusion and bacterial cell division. Nat Rev Microbiol 10: 8-12 doi:10.1038/nrmicro2671.
12. Levin PA, Margolis PS, Setlow P, Losick R, Sun D, (1992) Identification of Bacillus subtilis genes for septum placement and shape determination. J Bacteriol 174: 6717-6728.
13. Lutkenhaus J, (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-562 doi:10.1146/annurev.biochem.75.103004.142652.
14. Park K-T, Wu W, Battaile KP, Lovell S, Holyoak T, et al. (2011) The Min oscillator uses MinD-dependent conformational changes in MinE to spatially regulate cytokinesis. Cell 146: 396-407 doi:10.1016/j.cell.2011.06.042.
15. Raskin DM, de Boer PA, (1999) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA 96: 4971-4976.
16. Raskin DM, de Boer PA, (1999) MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 181: 6419-6424.
17. Hu Z, Lutkenhaus J, (1999) Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol 34: 82-90.
18. Marston AL, Errington J, (1999) Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol Microbiol 33: 84-96.
19. Bramkamp M, Emmins R, Weston L, Donovan C, Daniel RA, et al. (2008) A novel component of the division-site selection system of Bacillus subtilis and a new mode of action for the division inhibitor MinCD. Mol Microbiol 70: 1556-1569 doi:10.1111/j.1365-2958.2008.06501.x.
20. Patrick JE, Kearns DB, (2008) MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol Microbiol 70: 1166-1179 doi:10.1111/j.1365-2958.2008.06469.x.
21. Meinhardt H, de Boer PA, (2001) Pattern formation in Escherichia coli: a model for the pole-to-pole oscillations of Min proteins and the localization of the division site. Proc Natl Acad Sci USA 98: 14202-14207 doi:10.1073/pnas.251216598.
22. Wu LJ, Errington J, (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915-925 doi:10.1016/j.cell.2004.06.002.
23. Bernhardt TG, de Boer PAJ, (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. Mol Cell 18: 555-564 doi:10.1016/j.molcel.2005.04.012.
24. Wu LJ, Ishikawa S, Kawai Y, Oshima T, Ogasawara N, et al. (2009) Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J 28: 1940-1952 doi:10.1038/emboj.2009.144.
25. Cho H, McManus HR, Dove SL, Bernhardt TG, (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci USA 108: 3773-3778 doi:10.1073/pnas.1018674108.
26. Tonthat NK, Arold ST, Pickering BF, Van Dyke MW, Liang S, et al. (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30: 154-164 doi:10.1038/emboj.2010.288.
27. Schumacher MA, Miller MC, Grkovic S, Brown MH, Skurray RA, et al. (2001) Structural mechanisms of QacR induction and multidrug recognition. Science 294: 2158-2163 doi:10.1126/science.1066020.
28. Orth P, Schnappinger D, Hillen W, Saenger W, Hinrichs W, (2000) Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat Struct Biol 7: 215-219 doi:10.1038/73324.
29. Mukherjee A, Lutkenhaus J, (1998) Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J 17: 462-469 doi:10.1093/emboj/17.2.462.
30. Karimova G, Pidoux J, Ullmann A, Ladant D, (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
31. Erickson HP, Taylor DW, Taylor KA, Bramhill D, (1996) Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci USA 93: 519-523.
32. Mukherjee A, Lutkenhaus J, (1994) Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 176: 2754-2758.
33. Mukherjee A, Lutkenhaus J, (1999) Analysis of FtsZ assembly by light scattering and determination of the role of divalent metal cations. J Bacteriol 181: 823-832.
34. Yu XC, Margolin W, (1997) Ca2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. EMBO J 16: 5455-5463 doi:10.1093/emboj/16.17.5455.
35. González JM, Jiménez M, Vélez M, Mingorance J, Andreu JM, et al. (2003) Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment. J Biol Chem 278: 37664-37671 doi:10.1074/jbc.M305230200.
36. Shen B, 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 doi:10.1111/j.1365-2958.2010.07055.x.
37. Ramos JL, Martínez-Bueno M, Molina-Henares AJ, Terán W, Watanabe K, et al. (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69: 326-356 doi:10.1128/MMBR.69.2.326-356.2005.
38. Routh MD, Su C-C, Zhang Q, Yu EW, (2009) Structures of AcrR and CmeR: insight into the mechanisms of transcriptional repression and multi-drug recognition in the TetR family of regulators. Biochim Biophys Acta 1794: 844-851 doi:10.1016/j.bbapap.2008.12.001.
39. Miller J (1972) Experiments in Molecular Genetics. New York: Cold Spring Harbor Laboratory.
40. Johnson JE, Lackner LL, Hale CA, de Boer PAJ, (2004) ZipA is required for targeting of DMinC/DicB, but not DMinC/MinD, complexes to septal ring assemblies in Escherichia coli. J Bacteriol 186: 2418-2429.
41. Haldimann A, Wanner BL, (2001) Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J Bacteriol 183: 6384-6393 doi:10.1128/JB.183.21.6384-6393.2001.
42. Gueiros-Filho FJ, Losick R, (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16: 2544-2556 doi:10.1101/gad.1014102.