MinC, MinD, and MinE drive counter-oscillation of early-cell-division proteins prior to Escherichia coli septum formation

mBio

Volumn 4, Issue 6, 2013, Pages

  Bisicchia, Paola ^a   Arumugam, Senthil ^b   Schwille, Petra ^c   Sherratt, David ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b INSTITUT CURIE   (France)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FTSA PROTEIN; FTSZ PROTEIN; MINC PROTEIN; MIND PROTEIN; MINE PROTEIN; UNCLASSIFIED DRUG; ZAPA PROTEIN; ZAPB PROTEIN; ZIPA PROTEIN; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; CYTOSKELETON PROTEIN; ESCHERICHIA COLI PROTEIN; FTSZ PROTEIN, BACTERIA; MEMBRANE PROTEIN; MINC PROTEIN, E COLI; MIND PROTEIN, E COLI; MINE PROTEIN, E COLI;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL DIVISION; CHROMOSOME SEGREGATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EPIFLUORESCENCE MICROSCOPY; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; CELL CYCLE PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS;

EID: 84891598518     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00856-13     Document Type: Article

References (52)

1. Lutkenhaus J, Pichoff S, Du S. 2012. Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton (Hoboken) 69:778-790.
2. 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.
3. Cho H, McManus HR, Dove SL, Bernhardt TG. 2011. Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc. Natl. Acad. Sci. U. S. A. 108:3773-3778.
4. Tonthat NK, Arold ST, Pickering BF, Van Dyke MW, Liang S, Lu Y, Beuria TK, Margolin W, Schumacher MA. 2011. Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J. 30:154-164.
5. 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. U. S. A. 96: 14819-14824.
6. 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.
7. 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.
8. Hernández-Rocamora VM, García-Montañés C, Reija B, Monterroso B, Margolin W, Alfonso C, Zorrilla S, Rivas G. 2013. MinC protein shortens FtsZ protofilaments by preferentially interacting with GDP-bound subunits. J. Biol. Chem. 288:24625-24635.
9. Lutkenhaus J. 2007. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76:539-562.
10. 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. U. S. A. 98:14202-14207.
11. de Boer PA. 2010. Advances in understanding E. coli cell fission. Curr. Opin. Microbiol. 13:730-737.
12. Goehring NW, Beckwith J. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15:R514-R526.
13. Weiss DS. 2004. Bacterial cell division and the septal ring. Mol. Microbiol. 54:588-597.
14. Aarsman ME, Piette A, Fraipont C, Vinkenvleugel TM, NguyenDistèche M, den Blaauwen T. 2005. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55:1631-1645.
15. Hale CA, de Boer PA. 1999. Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J. Bacteriol. 181:167-176.
16. Hale CA, Rhee AC, de Boer PA. 2000. ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J. Bacteriol. 182:5153-5166.
17. Mateos-Gil P, Márquez I, López-Navajas P, Jiménez M, Vicente M, Mingorance J, Rivas G, Vélez M. 2012. FtsZ polymers bound to lipid bilayers through ZipA form dynamic two dimensional networks. Biochim. Biophys. Acta 1818:806-813.
18. Pazos M, Natale P, Vicente M. 2013. A specific role for the ZipA protein in cell division: stabilization of the FtsZ protein. J. Biol. Chem. 288: 3219-3226.
19. 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.
20. Low HH, Moncrieffe MC, Löwe J. 2004. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 341:839-852.
21. Small E, Marrington R, Rodger A, Scott DJ, Sloan K, Roper D, Dafforn TR, Addinall SG. 2007. FtsZ polymer-bundling by the Escherichia coli ZapA orthologue, YgfE, involves a conformational change in bound GTP. J. Mol. Biol. 369:210-221.
22. Mohammadi T, Ploeger GE, Verheul J, Comvalius AD, Martos A, Alfonso C, van Marle J, Rivas G, den Blaauwen T. 2009. The GTPase activity of Escherichia coli FtsZ determines the magnitude of the FtsZ polymer bundling by ZapA in vitro. Biochemistry 48:11056-11066.
23. Dajkovic A, Pichoff S, Lutkenhaus J, Wirtz D. 2010. Cross-linking FtsZ polymers into coherent Z rings. Mol. Microbiol. 78:651-668.
24. 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.
25. Ebersbach G, Galli E, Møller-Jensen J, Löwe J, Gerdes K. 2008. Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol. Microbiol. 68:720-735.
26. Mercier R, Petit MA, Schbath S, Robin S, El Karoui M, Boccard F, Espéli O. 2008. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135: 475-485.
27. Espéli O, Borne R, Dupaigne P, Thiel A, Gigant E, Mercier R, Boccard F. 2012. A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J. 31:3198-3211.
28. Wang X, Huang J, Mukherjee A, Cao C, Lutkenhaus J. 1997. Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J. Bacteriol. 179: 5551-5559.
29. Den Blaauwen T, Buddelmeijer N, Aarsman ME, Hameete CM, Nanninga N. 1999. Timing of FtsZ assembly in Escherichia coli. J. Bacteriol. 181:5167-5175.
30. Rueda S, Vicente M, Mingorance J. 2003. Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J. Bacteriol. 185:3344-3351.
31. Galli E, Gerdes K. 2012. FtsZ-ZapA-ZapB interactome of Escherichia coli. J. Bacteriol. 194:292-302.
32. Wang X, Possoz C, Sherratt DJ. 2005. Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev. 19: 2367-2377.
33. Juarez JR, Margolin W. 2010. Changes in the Min oscillation pattern before and after cell birth. J. Bacteriol. 192:4134-4142.
34. Thanedar S, Margolin W. 2004. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14: 1167-1173.
35. Cordell SC, Robinson EJ, Lowe J. 2003. Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc. Natl. Acad. Sci. U. S. A. 100:7889-7894.
36. Dajkovic A, Mukherjee A, Lutkenhaus J. 2008. Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. J. Bacteriol. 190:2513-2526.
37. Erickson HP, Anderson DE, Osawa M. 2010. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol. Mol. Biol. Rev. 74:504-528.
38. Anderson DE, Gueiros-Filho FJ, Erickson HP. 2004. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZregulating proteins. J. Bacteriol. 186:5775-5781.
39. Loose M, Fischer-Friedrich E, Ries J, Kruse K, Schwille P. 2008. Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320:789-792.
40. Arumugam S, Chwastek G, Fischer-Friedrich E, Ehrig C, Mönch I, Schwille P. 2012. Surface topology engineering of membranes for the mechanical investigation of the tubulin homologue FtsZ. Angew. Chem. Int. Ed. Engl. 19:11858-11862.
41. Loose M, Fischer-Friedrich E, Herold C, Kruse K, Schwille P. 2011. Min protein patterns emerge from rapid rebinding and membrane interaction of MinE. Nat. Struct. Mol. Biol. 18:577-583.
42. Scheffers DJ. 2008. The effect of MinC on FtsZ polymerization is pH dependent and can be counteracted by ZapA. FEBS Lett. 582: 2601-2608.
43. Chen Y, Bjornson K, Redick SD, Erickson HP. 2005. A rapid fluorescence assay for FtsZ assembly indicates cooperative assembly with a dimer nucleus. Biophys. J. 88:505-514.
44. Mukherjee A, Lutkenhaus J. 1998. Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J. 17:462-469.
45. Romberg L, Mitchison TJ. 2004. Rate-limiting guanosine 5=triphosphate hydrolysis during nucleotide turnover by FtsZ, a prokaryotic tubulin homologue involved in bacterial cell division. Biochemistry 43: 282-288.
46. Chen Y, Erickson HP. 2009. FtsZ filament dynamics at steady state: subunit exchange with and without nucleotide hydrolysis. Biochemistry 48:6664-6673.
47. 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.
48. Bachmann BJ. 1972. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol. Rev. 36:525-557.
49. Reyes-Lamothe R, Sherratt DJ, Leake MC. 2010. Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328:498-501.
50. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
51. 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.
52. Osawa M, Anderson DE, Erickson HP. 2008. Reconstitution of contrac tile FtsZ rings in liposomes. Science 320:792-794.