Guiding divisome assembly and controlling its activity

Current Opinion in Microbiology

Volumn 24, Issue , 2015, Pages 60-65

  Tsang, Mary Jane ^a   Bernhardt, Thomas G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DIVISOME; FTSA PROTEIN; FTSN PROTEIN; FTSZ PROTEIN; UNCLASSIFIED DRUG; ZIPA PROTEIN; FTSA PROTEIN, BACTERIA; NONHISTONE PROTEIN;

BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL CHROMOSOME; CELL DIVISION; CHROMOSOME REPLICATION; DNA REPLICATION; ESCHERICHIA COLI; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; METABOLISM;

BACILLUS SUBTILIS; ESCHERICHIA COLI;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL DIVISION; CHROMOSOMAL PROTEINS, NON-HISTONE; ESCHERICHIA COLI;

EID: 84921826193     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2015.01.002     Document Type: Review

References (70)

1. Bi E.F., Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature 1991, 354:161-164.
2. Szwedziak P., Wang Q., Bharat T.A.M., Tsim M., Löwe J. Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. eLife 2014, 3:e04601.
3. Lutkenhaus J., Pichoff S., Du S. Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton 2012, 69:778-790.
4. Typas A., Banzhaf M., Gross C.A., Vollmer W. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 2012, 10:123-136.
5. de Boer P.A.J. Advances in understanding E. coli cell fission. Curr Opin Microbiol 2010, 13:730-737.
6. Adams D.W., Errington J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 2009, 7:642-653.
7. de Boer P.A., Crossley R.E., Rothfield L.I. 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 1989, 56:641-649.
8. Levin P.A., Shim J.J., Grossman A.D. Effect of minCD on FtsZ ring position and polar septation in Bacillus subtilis. J Bacteriol 1998, 180:6048-6051.
9. Woldringh C.L., Mulder E., Huls P.G., Vischer N. Toporegulation of bacterial division according to the nucleoid occlusion model. Res Microbiol 1991, 142:309-320.
10. Woldringh C.L., Mulder E., Valkenburg J.A., Wientjes F.B., Zaritsky A., Nanninga N. Role of the nucleoid in the toporegulation of division. Res Microbiol 1990, 141:39-49.
11. Yu X.C., Margolin W. FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization. Mol Microbiol 1999, 32:315-326.
12. Bi E., Lutkenhaus J. Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol 1993, 175:1118-1125.
13. Raskin D.M., de Boer P.A. 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 1999, 96:4971-4976.
14. Hu Z., Lutkenhaus J. 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 1999, 34:82-90.
15. Lackner L.L., Raskin D.M., de Boer P.A.J. ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol 2003, 185:735-749.
16. Hu Z., Saez C., Lutkenhaus J. Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: role of MinD and MinE. J Bacteriol 2003, 185:196-203.
17. Ghosal D., Trambaiolo D., Amos L.A., Löwe J. MinCD cell division proteins form alternating copolymeric cytomotive filaments. Nat Commun 2014, 5:5341.
18. Raskin D.M., de Boer P.A. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 1999, 181:6419-6424.
19. Marston A.L., Errington J. Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol Microbiol 1999, 33:84-96.
20. Wu L.J., Errington J. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 2004, 117:915-925.
21. Bernhardt T.G., de Boer P.A.J. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. Mol Cell 2005, 18:555-564.
22. Tonthat N.K., Arold S.T., Pickering B.F., Van Dyke M.W., Liang S., Lu Y., Beuria T.K., Margolin W., Schumacher M.A. Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 2011, 30:154-164.
23. Cho H., Bernhardt T.G. Identification of the SlmA active site responsible for blocking bacterial cytokinetic ring assembly over the chromosome. PLOS Genet 2013, 9:e1003304.
24. Cho H., McManus H.R., Dove S.L., Bernhardt T.G. Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci U S A 2011, 108:3773-3778.
25. Tonthat N.K., Milam S.L., Chinnam N., Whitfill T., Margolin W., Schumacher M.A. SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proc Natl Acad Sci U S A 2013, 110:10586-10591.
26. Du S., Park K.-T., Lutkenhaus J. Oligomerization of FtsZ converts the FtsZ tail motif (conserved carboxy-terminal peptide) into a multivalent ligand with high avidity for partners ZipA and SlmA. Mol Microbiol 2014, 10.1111/mmi.12854.
27. Du S., Lutkenhaus J. SlmA antagonism of FtsZ assembly employs a two-pronged mechanism like MinCD. PLOS Genet 2014, 10:e1004460.
28. Wu L.J., Ishikawa S., Kawai Y., Oshima T., Ogasawara N., Errington J. Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J 2009, 28:1940-1952.
29. Bailey M.W., Bisicchia P., Warren B.T., Sherratt D.J., Männik J. Evidence for divisome localization mechanisms independent of the Min system and SlmA in Escherichia coli. PLOS Genet 2014, 10:e1004504.
30. Mercier R., Petit M.-A., Schbath S., Robin S., Karoui El M., Boccard F., Espéli O. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 2008, 135:475-485.
31. Dupaigne P., Tonthat N.K., Espéli O., Whitfill T., Boccard F., Schumacher M.A. Molecular basis for a protein-mediated DNA-bridging mechanism that functions in condensation of the E. coli chromosome. Mol Cell 2012, 48:560-571.
32. Espéli O., Borne R., Dupaigne P., Thiel A., Gigant E., Mercier R., Boccard F. A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 2012, 31:3198-3211.
33. Galli E., Gerdes K. Spatial resolution of two bacterial cell division proteins: ZapA recruits ZapB to the inner face of the Z-ring. Mol Microbiol 2010, 76:1514-1526.
34. Gueiros-Filho F.J., Losick R. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 2002, 16:2544-2556.
35. Buss J., Coltharp C., Huang T., Pohlmeyer C., Wang S.-C., Hatem C., Xiao J. In vivo organization of the FtsZ-ring by ZapA and ZapB revealed by quantitative super-resolution microscopy. Mol Microbiol 2013, 89:1099-1120.
36. Rodrigues C.D.A., Harry E.J. The Min system and nucleoid occlusion are not required for identifying the division site in Bacillus subtilis but ensure its efficient utilization. PLoS Genet 2012, 8:e1002561.
37. Moriya S., Rashid R.A., Rodrigues C.D.A., Harry E.J. Influence of the nucleoid and the early stages of DNA replication on positioning the division site in Bacillus subtilis. Mol Microbiol 2010, 76:634-647.
38. Harry E.J., Rodwell J., Wake R.G. Co-ordinating DNA replication with cell division in bacteria: a link between the early stages of a round of replication and mid-cell Z ring assembly. Mol Microbiol 1999, 33:33-40.
39. Regamey A., Harry E.J., Wake R.G. Mid-cell Z ring assembly in the absence of entry into the elongation phase of the round of replication in bacteria: co-ordinating chromosome replication with cell division. Mol Microbiol 2000, 38:423-434.
40. Arjes H.A., Kriel A., Sorto N.A., Shaw J.T., Wang J.D., Levin P.A. Failsafe mechanisms couple division and DNA replication in bacteria. Curr Biol 2014, 24:2149-2155.
41. Pichoff S., Lutkenhaus J. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J 2002, 21:685-693.
42. Hale C.A., de Boer P.A. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 1997, 88:175-185.
43. Goehring N.W., Beckwith J. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 2005, 15:R514-R526.
44. Chen J.C., Beckwith J. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol Microbiol 2001, 42:395-413.
45. Buddelmeijer N., Judson N., Boyd D., Mekalanos J.J., Beckwith J. YgbQ, a cell division protein in Escherichia coli and Vibrio cholerae, localizes in codependent fashion with FtsL to the division site. Proc Natl Acad Sci U S A 2002, 99:6316-6321.
46. Hale C.A., de Boer P.A. Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J Bacteriol 1999, 181:167-176.
47. Schmidt K.L., Peterson N.D., Kustusch R.J., Wissel M.C., Graham B., Phillips G.J., Weiss D.S. A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J Bacteriol 2004, 186:785-793.
48. Wang L., Khattar M.K., Donachie W.D., Lutkenhaus J. FtsI and FtsW are localized to the septum in Escherichia coli. J Bacteriol 1998, 180:2810-2816.
49. Weiss D.S., Chen J.C., Ghigo J.M., Boyd D., Beckwith J. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J Bacteriol 1999, 181:508-520.
50. Mercer K.L.N., Weiss D.S. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J Bacteriol 2002, 184:904-912.
51. Hale C.A., de Boer P.A.J. ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J Bacteriol 2002, 184:2552-2556.
52. Addinall S.G., Cao C., Lutkenhaus J. FtsN, a late recruit to the septum in Escherichia coli. Mol Microbiol 1997, 25:303-309.
53. Corbin B.D., Geissler B., Sadasivam M., Margolin W. Z-ring-independent interaction between a subdomain of FtsA and late septation proteins as revealed by a polar recruitment assay. J Bacteriol 2004, 186:7736-7744.
54. Gerding M.A., Liu B., Bendezú F.O., Hale C.A., Bernhardt T.G., de Boer P.A.J. Self-enhanced accumulation of FtsN at Division Sites and Roles for Other Proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction. J Bacteriol 2009, 191:7383-7401.
55. Lutkenhaus J. FtsN-trigger for septation. J Bacteriol 2009, 191:7381-7382.
56. Busiek K.K., Eraso J.M., Wang Y., Margolin W. The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J Bacteriol 2012, 194:1989-2000.
57. Busiek K.K., Margolin W. A role for FtsA in SPOR-independent localization of the essential Escherichia coli cell division protein FtsN. Mol Microbiol 2014, 92:1212-1226.
58. Geissler B., Margolin W. Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol Microbiol 2005, 58:596-612.
59. Geissler B., Elraheb D., Margolin W. 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 2003, 100:4197-4202.
60. Bernard C.S., Sadasivam M., Shiomi D., Margolin W. An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol Microbiol 2007, 64:1289-1305.
61. Goehring N.W., Petrovska I., Boyd D., Beckwith J. Mutants, suppressors, and wrinkled colonies: mutant alleles of the cell division gene ftsQ point to functional domains in FtsQ and a role for domain 1C of FtsA in divisome assembly. J Bacteriol 2007, 189:633-645.
62. Pichoff S., Shen B., Sullivan B., Lutkenhaus J. 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 2012, 83:151-167.
63. Szwedziak P., Wang Q., Freund S.M.V., Löwe J. FtsA forms actin-like protofilaments. EMBO J 2012, 31:2249-2260.
64. Pichoff S., Du S., Lutkenhaus J. The bypass of ZipA by overexpression of FtsN requires a previously unknown conserved FtsN motif essential for FtsA-FtsN interaction supporting a model in which FtsA monomers recruit late cell division proteins to the Z ring. Mol Microbiol 2014, (in press).
65. Herricks J.R., Nguyen D., Margolin W. A thermosensitive defect in the ATP binding pocket of FtsA can be suppressed by allosteric changes in the dimer interface. Mol Microbiol 2014, 94:713-727.
66. Tsang M.-J., Bernhardt T.G. A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division. Mol Microbiol 2014, (in press).
67. Liu B., Persons L., Lee L., de Boer P.A.J. Roles for both FtsA and the FtsQLB subcomplex in FtsN-stimulated cell constriction in Escherichia coli. Mol Microbiol 2014, (in press).
68. Loose M., Mitchison T.J. The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat Cell Biol 2013, 16:38-46.
69. Dai K., Lutkenhaus J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol 1992, 174:6145-6151.
70. Dewar S.J., Begg K.J., Donachie W.D. Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J Bacteriol 1992, 174:6314-6316.