Asymmetric constriction of dividing Escherichia coli cells induced by expression of a fusion between two min proteins

Journal of Bacteriology

Volumn 196, Issue 11, 2014, Pages 2089-2100

  Rowlett, Veronica Wells ^a   Margolin, William ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

ARTICLE; ASYMMETRIC CELL DIVISION; BACTERIAL CELL; CELL FUSION; CELL MATURATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ESCHERICHIA COLI; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ADENOSINE TRIPHOSPHATASES; CELL DIVISION; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; RECOMBINANT PROTEINS;

EID: 84899713789     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01425-13     Document Type: Article

References (55)

1. Margolin W. 2000. Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24:531-548. http://dx.doi.org/10.1111/j.1574-6976.2000.tb00554.x.
2. Vicente M, Rico AI, Martinez-Arteaga R, Mingorance J. 2006. Septum enlightenment: assembly of bacterial division proteins. J. Bacteriol. 188: 19-27. http://dx.doi.org/10.1128/JB.188.1.19-27.2006.
3. Adams DW, Errington J. 2009. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7:642-653. http://dx.doi.org/10.1038/nrmicro2198.
4. Fu G, Huang T, Buss J, Coltharp C, Hensel Z, Xiao J. 2010. In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS One 5:e12682. http://dx.doi.org/10.1371/journal.pone.0012682.
5. PichoffS, Lutkenhaus J. 2005. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55:1722-1734. http://dx.doi.org/10.1111/j.1365-2958.2005.04522.x.
6. PichoffS, Lutkenhaus J. 2002. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21:685-693. http://dx.doi.org/10.1093/emboj/21.4.685.
7. Yu X-C, 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. http://dx.doi.org/10.1046/j.1365-2958.1999.01351.x.
8. 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. http://dx.doi.org/10.1016/0092-8674(89)90586-2.
9. Hu Z, Mukherjee A, PichoffS, 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. http://dx.doi.org/10.1073/pnas.96.26.14819.
10. Hu Z, Lutkenhaus J. 2003. A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol. Microbiol. 47:345-355. http://dx.doi.org/10.1046/j.1365-2958.2003.03321.x.
11. de Boer PAJ, Crossley RE, Hand AR, Rothfield LI. 1991. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 10:4371-4380.
12. Raskin DM, de Boer PAJ. 1997. The MinE ring: an FtsZ-independent cell structure required for selection of the correct division site in E. coli. Cell 91:685-694. http://dx.doi.org/10.1016/S0092-8674(00)80455-9.
13. Hu Z, Gogol EP, Lutkenhaus J. 2002. Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc. Natl. Acad. Sci. U. S. A. 99:6761-6766. http://dx.doi.org/10.1073/pnas.102059099.
14. 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. U. S. A. 96:4971-4976. http://dx.doi.org/10.1073/pnas.96.9.4971.
15. Fu X, Shih Y-L, Zhang Y, Rothfield LI. 2001. The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc. Natl. Acad. Sci. U. S. A. 98:980-985. http://dx.doi.org/10.1073/pnas.98.3.980.
16. Huang KC, Meir Y, Wingreen NS. 2003. Dynamic structures in Escherichia coli: spontaneous formation of MinE rings and MinD polar zones. Proc. Natl. Acad. Sci. U. S. A. 100:12724-12728. http://dx.doi.org/10.1073/pnas.2135445100.
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. http://dx.doi.org/10.1046/j.1365-2958.1999.01575.x.
18. Thanedar S, Margolin W. 2004. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14: 1167-1173. http://dx.doi.org/10.1016/j.cub.2004.06.048.
19. Tonthat NK, Milam SL, Cinnam N, Whitfill T, Margolin W, Schumacher MA. 2013. SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proc. Natl. Acad. Sci. U. S. A. 110:10586-10591. http://dx.doi.org/10.1073/pnas.1221036110.
20. Bisicchia P, Arumugam S, Schwille P, Sherratt D. 2013. MinC, MinD, and MinE drive counter-oscillation of early-cell-division proteins prior to Escherichia coli septum formation. mBio 4(6):e00856-13. http://dx.doi.org/10.1128/mBio.00856-13.
21. Cordell SC, Anderson RE, Löwe J. 2001. Crystal structure of the bacterial cell division inhibitor MinC.EMBOJ. 20:2454-2461. http://dx.doi.org/10.1093/emboj/20.10.2454.
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. http://dx.doi.org/10.1128/JB.182.14.3965-3971.2000.
23. Shiomi D, Margolin W. 2007. The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J. Bacteriol. 189:236-243. http://dx.doi.org/10.1128/JB.00666-06.
24. Shen B, Lutkenhaus J. 2009. The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinCc/MinD. Mol. Microbiol. 72:410-424. http://dx.doi.org/10.1111/j.1365-2958.2009.06651.x.
25. 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. http://dx.doi.org/10.1111/j.1365-2958.2010.07055.x.
26. 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. http://dx.doi.org/10.1016/j.cub.2008.01.042.
27. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675. http://dx.doi.org/10.1038/nmeth.2089.
28. Levin PA. 2002. Light microscopy techniques for bacterial cell biology, p 112-132. In Sansonetti P, Zychlinsky A (ed), Methods in microbiology, vol 31.Molecular cellular microbiology. Academic Press Ltd., London, United Kingdom.
29. Raskin DM, de Boer PAJ. 1999. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181:6419-6424.
30. Johnson JE, Lackner LL, de Boer PAJ. 2002. Targeting of DMinC/MinD and DMinC/DicB complexes to septal rings in Escherichia coli suggests a multistep mechanism for MinC-mediated destruction of nascent FtsZ rings. J. Bacteriol. 184:2951-2962. http://dx.doi.org/10.1128/JB.184.11.2951-2962.2002.
31. Sun Q, Margolin W. 1998. FtsZ dynamics during the division cycle of live Escherichia coli cells. J. Bacteriol. 180:2050-2056.
32. 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 Dev. 22:3475-3488. http://dx.doi.org/10.1101/gad.1732408.
33. Zhou H, Lutkenhaus J. 2005. MinC mutants deficient in MinD- and DicB-mediated cell division inhibition due to loss of interaction with MinD, DicB, or a septal component. J. Bacteriol. 187:2846-2857. http://dx.doi.org/10.1128/JB.187.8.2846-2857.2005.
34. Szeto TH, Rowland SL, Rothfield LI, King GF. 2002. Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc. Natl. Acad. Sci. U. S. A. 99: 15693-15698. http://dx.doi.org/10.1073/pnas.232590599.
35. Ma L, King GF, Rothfield L. 2004. Positioning of the MinE binding site on the MinD surface suggests a plausible mechanism for activation of the Escherichia coli MinD ATPase during division site selection. Mol. Microbiol. 54:99-108. http://dx.doi.org/10.1111/j.1365-2958.2004.04265.x.
36. Robinson AC, Kenan DJ, Hatfull GF, Sullivan NF, Spiegelberg R, Donachie WD. 1984. DNA sequence and transcriptional organization of essential cell division genes ftsQ and ftsA of Escherichia coli: evidence for overlapping transcriptional units. J. Bacteriol. 160:546-555.
37. Robinson AC, Kenan DJ, Sweeny J, Donachie WD. 1986. Further evidence for overlapping transcriptional units in an Escherichia coli cell envelope-cell division gene cluster: DNA sequence and transcriptional organization of the ddl ftsQ region. J. Bacteriol. 167:809-817.
38. Yi Q-M, Rockenbach S, Ward JE, Jr, Lutkenhaus J. 1985. Structure and expression of the cell division genes ftsQ, ftsA and ftsZ. J. Mol. Biol. 184: 399-412. http://dx.doi.org/10.1016/0022-2836(85)90290-6.
39. PichoffS, Lutkenhaus J. 2001. Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J. Bacteriol. 183:6630-6635. http://dx.doi.org/10.1128/JB.183.22.6630-6635.2001.
40. Begg K, Nikolaichik Y, Crossland N, Donachie WD. 1998. Roles of FtsA and FtsZ in activation of division sites. J. Bacteriol. 180:881-884.
41. Bi E, Lutkenhaus J. 1990. FtsZ regulates frequency of cell division in Escherichia coli. J. Bacteriol. 172:2765-2768.
42. Dai K, Lutkenhaus J. 1992. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J. Bacteriol. 174:6145-6151.
43. Geissler B, Shiomi D, Margolin W. 2007. The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology 153:814-825. http://dx.doi.org/10.1099/mic.0.2006/001834-0.
44. PichoffS, Shen B, Sullivan B, Lutkenhaus J. 2012. FtsA mutants impaired for self-interaction bypass ZipA suggesting a model in which FtsA's self-interaction competes with its ability to recruit downstream division proteins. Mol. Microbiol. 83:151-167. http://dx.doi.org/10.1111/j.1365-2958.2011.07923.x.
45. Thanky NR, Young DB, Robertson BD. 2007. Unusual features of the cell cycle in mycobacteria: polar-restricted growth and the snapping-model of cell division. Tuberculosis 87:231-236. http://dx.doi.org/10.1016/j.tube.2006.10.004.
46. Katzmann E, Müller FD, Lang C, Messerer M, Winklhofer M, Plitzko JM, Schüler D. 2011. Magnetosome chains are recruited to cellular division sites and split by asymmetric septation. Mol. Microbiol. 82:1316-1329. http://dx.doi.org/10.1111/j.1365-2958.2011.07874.x.
47. Addinall SG, Bi E, Lutkenhaus J. 1996. FtsZ ring formation in fts mutants. J. Bacteriol. 178:3877-3884.
48. Corbin BD, Yu X-C, Margolin W. 2002. Exploring intracellular space: function of the Min system in round-shaped Escherichia coli. EMBO J. 21:1998-2008. http://dx.doi.org/10.1093/emboj/21.8.1998.
49. Bendezú FO, de Boer PAJ. 2008. Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli. J. Bacteriol. 190:1792-1811. http://dx.doi.org/10.1128/JB.01322-07.
50. Busiek KK, Eraso JM, Wang Y, Margolin W. 2012. The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J. Bacteriol. 194:1989-2000. http://dx.doi.org/10.1128/JB.06683-11.
51. Sun Q, Margolin W. 2001. Influence of the nucleoid on placement of FtsZ and MinE rings in Escherichia coli. J. Bacteriol. 183:1413-1422. http://dx.doi.org/10.1128/JB.183.4.1413-1422.2001.
52. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006. 0008. http://dx.doi.org/10.1038/msb4100050.
53. Geissler B, Elraheb D, Margolin W. 2003. A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 100:4197-4202. http://dx.doi.org/10.1073/pnas.0635003100.
54. Weiss DS, Chen JC, Ghigo J-M, Boyd D, Beckwith J. 1999. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J. Bacteriol. 181:508-520.
55. 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. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01705.x.