Characterization of ftsZ mutations that render Bacillus subtilis resistant to MinC

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  de Oliveira, Inês Filipa Fernandes ^a   Borges, Anabela de Sousa ^a   Kooij, Viola ^b,d   Bartosiak Jentys, Jeremy ^c,e   Luirink, Joen ^b   Scheffers, Dirk Jan ^a,b,c  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FTSZ PROTEIN; GUANOSINE TRIPHOSPHATE; MINC PROTEIN; MIND PROTEIN; MUTANT PROTEIN; PROTEIN INHIBITOR; BACTERIAL PROTEIN; CYTOSKELETON PROTEIN; FTSZ PROTEIN, BACTERIA; MINC PROTEIN, BACTERIA;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; CONTROLLED STUDY; GENE MUTATION; GENE OVEREXPRESSION; GENETIC RESISTANCE; GENETIC SCREENING; GROWTH RATE; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PH; PROTEIN POLYMERIZATION; PROTEIN PURIFICATION; TEMPERATURE SENSITIVITY; BIOSYNTHESIS; CELL DIVISION; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; GENETICS; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

BACILLUS SUBTILIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY;

EID: 77957782485     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012048     Document Type: Article

References (48)

1. Adams DW, Errington J (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7: 642-53.
2. Rothfield L, Taghbalout A, Shih YL (2005) Spatial control of bacterial divisionsite placement. Nat Rev Microbiol 3: 959-968.
3. Wu LJ, Errington J (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915-925.
4. Bernhardt TG, de Boer PA (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18: 555-564.
5. de Boer PAJ, 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.
6. Lutkenhaus J (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-62.
7. Hu Z, Mukherjee A, Pichoff S, 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.
8. Edwards DH, Errington J (1997) The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24: 905-915.
9. Marston AL, Thomaides HB, Edwards DH, Sharpe ME, Errington J (1998) Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Devel 12: 3419-3430.
10. Bramkamp M, Emmins R, Weston L, Donovan C, Daniel RA, Errington J (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: 1556-69.
11. Patrick JE, Kearns DB (2008) MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol Microbiol 70: 1166-79.
12. Raskin DM, De Boer PAJ (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.
13. Raskin DM, De Boer PAJ (1999) MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 181: 6419-6424.
14. Hu Z, Lutkenhaus J (2001) Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol Cell 7: 1337-1343.
15. Hu Z, Saez C, 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.
16. Suefuji K, Valluzzi R, RayChaudhuri D (2002) Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE. Proc Natl Acad Sci USA 99: 16776-16781.
17. Howard M (2004) A mechanism for polar protein localization in bacteria. J Mol Biol 335: 655-663.
18. 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.
19. Gregory JA, Becker EC, Pogliano K (2008) Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes & Development 22: 3475-3488.
20. Dajkovic A, Lan G, Sun SX, Wirtz D, Lutkenhaus J (2008) MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr Biol 18: 235-244.
21. Scheffers DJ (2008) The effect of MinC on FtsZ polymerization is pH dependent and can be counteracted by ZapA. FEBS Lett 582: 2601-2608.
22. Hu Z, Lutkenhaus J (2000) Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J Bacteriol 182: 3965-3971.
23. Shiomi D, Margolin W (2007) The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J Bacteriol 189: 236-43.
24. Cordell SC, Anderson RE, Löwe J (2001) Crystal structure of the bacterial cell division inhibitor MinC. EMBO J 20: 2454-2461.
25. Löwe J, Amos LA (1998) Crystal structure of the bacterial cell-division protein FtsZ. Nature 391: 203-206.
26. Bi E, Lutkenhaus J (1990) Interaction between the min locus and ftsZ. J Bacteriol 172: 5610-6.
27. Bi E, Lutkenhaus J (1990) Analysis of ftsZ mutations that confer resistance to the cell division inhibitor SulA (SfiA). J Bacteriol 172: 5602-9.
28. Cordell SC, Robinson EJ, Löwe J (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci USA 100: 7889-7894.
29. Mukherjee A, Saez C, Lutkenhaus J (2001) Assembly of an FtsZ mutant deficient in GTPase activity has implications for FtsZ assembly and the role of the Z ring in cell division. J Bacteriol 183: 7190-7197.
30. Shen B, 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: 410-24.
31. 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.
32. Haney SA, 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.
33. Singh JK, Makde RD, Kumar V, Panda D (2007) A membrane protein, EzrA, regulates assembly dynamics of FtsZ by interacting with the C-terminal tail of FtsZ. Biochem 46: 11013-11022.
34. Ishikawa S, Kawai Y, Hiramatsu K, Kuwano M, Ogasawara N (2006) A new FtsZ-interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis. Mol Microbiol 60: 1364-80.
35. 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.
36. Feucht A, Errington J (2005) FtsZ mutations affecting cell division frequency, placement and morphology in Bacillus subtilis. Microbiol 151: 2053-2064.
37. Haydon DJ, et al. (2008) An inhibitor of FtsZ with potent and selective antistaphylococcal activity. Science 321: 1673-5.
38. 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.
39. 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.
40. Jensen SO, Thompson LS, Harry EJ (2005) Cell division in Bacillus subtilis: FtsZ and FtsA association is Z-ring independent, and FtsA is required for efficient midcell Z-Ring assembly. J Bacteriol 187: 6536-44.
41. Kunst F, Rapoport G (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177: 2403-2407.
42. Anagnostopoulos C, Spizizen J (1961) Requirements for transformation in Bacillus subtilis. J Bacteriol 81: 741-746.
43. Jenkinson HF (1983) Altered arrangement of proteins in the spore coat of a germination mutant of Bacillus subtilis. J Gen Microbiol 129: 1945-1958.
44. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, Cold Spring Harbor Laboratory Press. Cold Spring Harbor.
45. Wang X, Lutkenhaus J (1993) The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration. Mol Microbiol 9: 435-442.
46. Den Blaauwen T, Aarsman ME, Vischer NO, Nanninga N (2003) Penicillinbinding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid-cell in comparison with the old cell pole. Mol Microbiol 47: 539-547.
47. Kobayashi K, et al. (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100: 4678-4683.
48. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Meth Enzymol 185: 60-89.