Chapter 10 : Cell Division

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Cell Division, Page 1 of 2

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In , septum assembly occurs at the midcell and involves coordinated inward growth of all three layers of the cell envelope—the cytoplasmic membrane, the peptidoglycan wall, and the outer membrane. How the division septum is assembled and how its assembly is coordinated with other events in the cell cycle, such as chromosome segregation, are the topics of this chapter. One situation is that regulation ensures that the Z ring assembles in the right place and at the right time in normally cycling cells—this sort of regulation is widely conserved among different bacterial species. Similarly, however, one could argue that FtsA too might function indirectly in recruitment as FtsA is not essential in and the normal requirement for FtsA in septal ring assembly in can be largely bypassed by artificially tethering FtsQ to the septal ring. Penicillin-binding protein 3 (PBP3) localizes to the septal ring, where it cross-links septal peptidoglycan and recruits FtsN. MgtA, in contrast, is a monofunctional transglycosylase. Curiously, overproduction of FtsN also rescues cell division in ftsK(Ts), ftsQ(Ts), ftsI(Ts), and ftsEX depletion strains too. The outer membrane is considered to invaginate simultaneously with the rest of the cell envelope in .

Citation: Arends S, Williams K, Kustusch R, Weiss D. 2007. Cell Division, p 173-197. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch10

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Outer Membrane Proteins
Integral Membrane Proteins
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Image of FIGURE 1

Regulation of Z-ring assembly. The Min system and nucleoid occlusion (NO) work together to ensure that the only permissive site for Z-ring assembly is the gap that opens up at the midcell as nucleoids segregate late in the cell cycle. (Top) In a newborn cell, nucleoid occlusion prevents the Z ring from assembling at the midcell, while the Min system prevents Z rings from forming in the DNA-free region near either pole. Nucleoid occlusion in is mediated by a DNA-binding protein named SlmA. The MinCD inhibitor complex oscillates from pole to pole under control of MinE, which is concentrated near the midcell. See text for details. (Bottom) Chromosome segregation relieves the midcell of nucleoid occlusion. MinCD continues to oscillate, but its inhibitory effects do not reach as far as the midcell because MinE limits growth of MinD polymers.

Citation: Arends S, Williams K, Kustusch R, Weiss D. 2007. Cell Division, p 173-197. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch10
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Image of FIGURE 2

Models for assembly of the septal ring. (Top) The order of assembly of proteins into the septal ring as determined by localization dependency. First, FtsZ forms the Z ring. FtsA and ZipA join next, independently of one another. Once both FtsA and ZipA have localized, the remaining proteins join the ring in the order indicated such that localization of each depends upon localization of the proteins to the left of it. ZapA and EnvC are omitted because their dependency relationships have not been established, but since neither is essential, none of the proteins shown are likely to depend on ZapA or EnvC for recruitment. Dependence of FtsK and other late proteins on FtsEX is leaky. (Bottom) Bacterial two-hybrid assays have identified a network of interactions among the division proteins. Lines connect proteins reported to interact in at least one assay, while circular arrows indicate self-interaction (e.g., dimerization). Adapted from :R514—R526 ( ), copyright 2005, with permission from Elsevier with inclusion of additional data (Arends and Weiss, unpublished).

Citation: Arends S, Williams K, Kustusch R, Weiss D. 2007. Cell Division, p 173-197. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch10
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Image of FIGURE 3

Septal targeting domains in membrane proteins involved in cell division in For clarity, proteins are not drawn to scale. Regions sufficient for septal localization are shown in black, while those known to be dispensable are white. Grey indicates a protein has not been studied in this regard. In many cases only a limited number of constructs have been characterized, so the targeting domains might be smaller than indicated. Note that targeting information can reside in any domain (cytoplasmic, transmembrane, or periplasmic) and there is no evidence that a targeting motif is shared among different proteins. These findings are consistent with the notion that division proteins localize by a cascade of protein-protein interactions rather than by binding to a common target. Because FtsL must associate with FtsB to localize to the septal ring, the targeting regions identified in FtsL probably mediate complex formation with FtsB rather than septal localization per se. Adapted with permission from the (Wissel et al. [2004]) with inclusion of new data from our lab (Arends and Weiss, unpublished).

Citation: Arends S, Williams K, Kustusch R, Weiss D. 2007. Cell Division, p 173-197. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch10
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1. Aarsman, M. E.,, A. Piette,, C. Fraipont,, T. M. Vinkenvleugel,, M. Nguyen-Distèche, and, T. den Blaauwen. 2005. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55:16311645.
2. Adam, M.,, C. Fraipont,, N. Rhazi,, M. NguyenDistèche,, B. Lakaye,, J. M. Frere,, B. Devreese,, J. Van Beeumen,, Y. van Heijenoort,, J. van Heijenoort, and, J. M. Ghuysen. 1997.The bimodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes peptide bond formation from thiolesters and does not catalyze glycan chain polymerization from the lipid II intermediate. J. Bacteriol. 179:60056009.
3. Addinall, S. G.,, C. Cao, and, J. Lutkenhaus. 1997. FtsN, a late recruit to the septum in Escherichia coli. Mol. Microbiol. 25:303309.
4. Addinall, S. G., and, J. Lutkenhaus. 1996. FtsA is localized to the septum in an FtsZ-dependent manner.J. Bacteriol. 178:71677172.
5. Anderson, D. E.,, F. J. Gueiros-Filho, and, H. P. Erickson. 2004. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186:57755781.
6. Arends, S. J., and, D. S. Weiss. 2004.Inhibiting cell division in Escherichia coli has little if any effect on gene expression. J. Bacteriol. 186:880884.
7. Aussel, L.,, F. X. Barre,, M. Aroyo,, A. Stasiak,, A. Z. Stasiak, and, D. Sherratt. 2002. FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108:195205.
8. Bath, J.,, L. J. Wu,, J. Errington, and, J. C. Wang. 2000. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290:995997.
9. Beall, B., and, J. Lutkenhaus. 1992. Impaired cell division and sporulation of a Bacillus subtilis strain with the ftsA gene deleted. J. Bacteriol. 174:23982403.
10. Begg, K. J.,, S. J. Dewar, and, W. D. Donachie. 1995. A new Escherichia coli cell division gene, ftsK. J. Bacteriol. 177:62116222.
11. Ben-Yehuda, S., and, R. Losick. 2002.Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109:257266.
12. Bernhardt, T. G., and, P. A. de Boer. 2003.The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol. 48:11711182.
13. Bernhardt, T. G., and, P. A. de Boer. 2004. Screening for synthetic lethal mutants in Escherichia coli and identification of EnvC (YibP) as a periplasmic septal ring factor with murein hydrolase activity. Mol. Microbiol. 52:12551269.
14. Bernhardt, T. G., and, P. A. de Boer. 2005. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18:555564.
15. Bigot, S.,, J. Corre,, J. M. Louarn,, F. Cornet, and, F. X. Barre. 2004. FtsK activities in Xer recombination, DNA mobilization and cell division involve overlapping and separate domains of the protein. Mol. Microbiol. 54:876886.
16. Bigot, S.,, O. A. Saleh,, C. Lesterlin,, C. Pages,, M. El Karoui,, C. Dennis,, M. Grigoriev,, J. F. Allemand,, F. X. Barre, and, F. Cornet. 2005. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J. 24:37703780.
17. Bork, P.,, C. Sander, and, A. Valencia. 1992. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl. Acad. Sci. USA 89:72907294.
18. Botta, G. A., and, J. T. Park. 1981. Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation but not during cell elongation. J. Bacteriol. 145:333340.
19. Bouige, P.,, D. Laurent,, L. Piloyan, and, E. Dassa. 2002. Phylogenetic and functional classification of ATP-binding cassette (ABC) systems. Curr. Protein Peptide Sci. 3:541559.
20. Bowler, L. D., and, B. G. Spratt. 1989. Membrane topology of penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 3:12771286.
21. Broome-Smith, J. K.,, P. J. Hedge, and, B. G. Spratt. 1985. Production of thiol-penicillin-binding protein 3 of Escherichia coli using a two primer method of site-directed mutagenesis. EMBO J. 4:231235.
22. Buddelmeijer, N., and, J. Beckwith. 2002. Assembly of cell division proteins at the E. coli cell center. Curr. Opin. Microbiol. 5:553557.
23. Buddelmeijer, N., and, J. Beckwith. 2004. A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol. Microbiol. 52:13151327.
24. Buddelmeijer, N.,, N. Judson,, D. Boyd,, J. J. Mekalanos, and, J. Beckwith. 2002. 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. USA 99:63166321.
25. Butland, G.,, J. M. Peregrin-Alvarez,, J. Li,, W. Yang,, X. Yang,, V. Canadien,, A. Starostine,, D. Richards,, B. Beattie,, N. Krogan,, M. Davey,, J. Parkinson,, J. Greenblatt, and, A. Emili. 2005. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433:531537.
26. Capiaux, H.,, C. Lesterlin,, K. Perals,, J. M. Louarn, and, F. Cornet. 2002.A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep. 3:532536.
27. Chen, J. C., and, J. Beckwith. 2001. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42:395413.
28. Chen, J. C.,, D. S.W eiss,, J. M. Ghigo, and, J. Beckwith. 1999. Septal localization of FtsQ, an essential cell division protein in Escherichia coli. J. Bacteriol. 181:521530.
29. Corbin, B. D.,, B. Geissler,, M. Sadasivam, and, W. Margolin. 2004. Z-ring-independent interaction between a subdomain of FtsA and late septation proteins as revealed by a polar recruitment assay.J. Bacteriol. 186:77367744.
30. Cordell, S. C.,, E. J. H. Robinson, and, J. Lowe. 2003. Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc. Natl. Acad. Sci. USA 100:78897894.
31. Corre, J., and, J. M. Louarn. 2002. Evidence from terminal recombination gradients that FtsK uses replichore polarity to control chromosome terminus positioning at division in Escherichia coli. J. Bacteriol. 184:38013807.
32. Courcelle, J.,, A. Khodursky,, B. Peter,, P. O. Brown, and, P. C. Hanawalt. 2001. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158:4164.
33. Dai, K.,, Y. Xu, and, J. Lutkenhaus. 1993. Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J. Bacteriol. 175:37903797.
34. Dai, K.,, Y. Xu, and, J. Lutkenhaus. 1996. Topological characterization of the essential Escherichia coli cell division protein FtsN. J. Bacteriol. 178:13281334.
35. Daniel, R. A., and, J. Errington. 2000. Intrinsic instability of the essential cell division protein FtsL of Bacillus subtilis and a role for DivIB protein in FtsL turnover. Mol. Microbiol. 36:278289.
36. Daniel, R. A.,, E. J. Harry,, V. L. Katis,, R. G. Wake, and, J. Errington. 1998. Characterization of the essential cell division gene ftsL(yIID) of Bacillus subtilis and its role in the assembly of the division apparatus. Mol. Microbiol. 29:593604.
37. de Boer, P. A.,, R. E. Crossley, and, L. I. Rothfield. 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 56:641649.
38. de Jonge, B. L.,, F. B. Wientjes,, I. Jurida,, F. Driehuis,, J. T. Wouters, and, N. Nanninga. 1989. Peptidoglycan synthesis during the cell cycle of Escherichia coli:composition and mode of insertion. J. Bacteriol. 171:57835794.
39. de Leeuw, E.,, B. Graham,, G. J. Phillips,, C. M. ten Hagen-Jongman,, B. Oudega, and, J. Luirink. 1999. Molecular characterization of Escherichia coli FtsE and FtsX. Mol. Microbiol. 31:983993.
40. Den Blaauwen, T.,, M. E. Aarsman,, N. O. Vischer, and, N. Nanninga. 2003. Penicillin-binding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid-cell in comparison with the old cell pole. Mol. Microbiol. 47:539547.
41. Den Blaauwen, T.,, N. Buddelmeijer,, M. E. Aarsman,, C. M. Hameete, and, N. Nanninga. 1999. Timing of FtsZ assembly in Escherichia coli. J. Bacteriol. 181:51675175.
42. Denome, S. A.,, P. K. Elf,, T. A. Henderson,, D. E. Nelson, and, K. D.Y oung. 1999. Escherichia coli mutants lacking all possible combinations of eight penicillin binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J. Bacteriol. 181:39813993.
43. de Pedro, M. A.,, J. C. Quintela,, J.V. Holtje, and, H. Schwarz. 1997. Murein segregation in Escherichia coli. J. Bacteriol. 179:28232834.
44. Dessen, A.,, N. Mouz,, E. Gordon,, J. Hopkins, and, O. Dideberg. 2001. Crystal structure of PBP2x from a highly penicillin-resistant Streptococcus pneumoniae clinical isolate: a mosaic framework containing 83 mutations. J. Biol. Chem. 276:4510645112.
45. Diez, A. A.,, A. Farewell,, U. Nannmark, and, T. Nystrom. 1997. A mutation in the ftsK gene of Escherichia coli affects cell-cell separation, stationaryphase survival, stress adaptation, and expression of the gene encoding the stress protein UspA. J. Bacteriol. 179:58785883.
46. Di Lallo, G.,, M. Fagioli,, D. Barionovi,, P. Ghelardini, and, L. Paolozzi. 2003. Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery:bacterial septosome differentiation. Microbiology 149:33533359.
47. Draper, G. C.,, N. McLennan,, K. Begg,, M. Masters, and, W. D. Donachie. 1998. Only the Nterminal domain of FtsK functions in cell division. J. Bacteriol. 180:46214627.
48. Eberhardt, C.,, L. Kuerschner, and, D. S. Weiss. 2003. Probing the catalytic activity of a cell division-specific transpeptidase in vivo with betalactams. J. Bacteriol. 185:37263734.
49. Ehlert, K., and, J. V. Holtje. 1996. Role of precursor translocation in coordination of murein and phospholipid synthesis in Escherichia coli. J. Bacteriol. 178:67666771.
50. Errington, J.,, J. Bath, and, L. J. Wu. 2001. DNA transport in bacteria. Nat. Rev. Mol. Cell Biol. 2:538545.
51. Errington, J.,, R. A. Daniel, and, D. J. Scheffers. 2003. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67:5265.
52. Espeli, O.,, C. Lee, and, K. J. Marians. 2003. A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J. Biol. Chem. 278:4463944644.
53. Feucht, A.,, I. Lucet,, M. D. Yudkin, and, J. Errington. 2001. Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis. Mol. Microbiol. 40:115125.
54. Fung, J.,, T. J. MacAlister, and, L. I. Rothfield. 1978. Role of murein lipoprotein in morphogenesis of the bacterial division septum:phenotypic similarity of lkyD and lpo mutants. J. Bacteriol. 133:14671471.
55. Geissler, B.,, D. Elraheb, and, W. Margolin. 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. USA 100:41974202.
56. Geissler, B., and, W. Margolin. 2005. Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol. Microbiol. 58:596612.
57. Gerard, P.,, T. Vernet, and, A. Zapun. 2002. Membrane topology of the Streptococcus pneumoniae FtsW division protein. J. Bacteriol. 184:19251931.
58. Ghigo, J. M.,, D. S. Weiss,, J. C. Chen,, J. C. Yarrow, and, J. Beckwith. 1999. Localization of FtsL to the Escherichia coli septal ring. Mol. Microbiol. 31:725737.
59. Ghuysen, J. M., 1991. Serine beta-lactamases and penicillin-binding proteins. Annu. Rev. Microbiol. 45:3767.
60. Gibbs, T. W.,, D. R. Gill, and, G. P. Salmond. 1992. Localised mutagenesis of the fts YEX operon: conditionally lethal missense substitutions in the FtsE cell division protein of Escherichia coli are similar to those found in the cystic fibrosis transmembrane conductance regulator protein (CFTR) of human patients. Mol. Gen. Genet. 234:121128.
61. Gill, D. R.,, G. F. Hatfull, and, G. P. Salmond. 1986. A new cell division operon in Escherichia coli. Mol. Gen. Genet. 205:134145.
62. Goehring, N. W., and, J. Beckwith. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15:R514R526.
63. Goehring, N. W.,, F. Gueiros-Filho, and, J. Beckwith. 2005. Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli. Genes Dev. 19:127137.
64. Gueiros-Filho, F. J., and, R. Losick. 2002. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev. 16:25442556.
65. Guzman, L. M.,, J. J. Barondess, and, J. Beckwith. 1992. FtsL, an essential cytoplasmic membrane protein involved in cell division in Escherichia coli. J. Bacteriol. 174:77167728.
66. Hale, C. A., and, P. A. de Boer. 1997. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88:175185.
67. Hale, C. A., and, P. A. de Boer. 1999. Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ and independent of FtsA. J. Bacteriol. 181:167176.
68. Hale, C. A.,, A. C. Rhee, and, P. A. de Boer. 2000. ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J. Bacteriol. 182:51535166.
69. Heidrich, C.,, M. F. Templin,, A. Ursinus,, M. Merdanovic,, J. Berger,, H. Schwarz,, M. A. de Pedro, and, J. V. Holtje. 2001. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167178.
70. Heidrich, C.,, A. Ursinus,, J. Berger,, H. Schwarz, and, J. V. Holtje. 2002. Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J. Bacteriol. 184:60936099.
71. Henriques, A. O.,, P. Glaser,, P. J. Piggot, and, C. P. Moran, Jr., 1998. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 28:235247.
72. Holtje, J. V., 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichiacoli. Microbiol. Mol. Biol. Rev. 62:181203.
73. Houba-Herin, N.,, H. Hara,, M. Inouye, and, Y. Hirota. 1985. Binding of penicillin to thiol-penicillinbinding protein 3 of Escherichia coli:identification of its active site. Mol. Gen. Genet. 201:499504.
74. Hu, Z., and, J. Lutkenhaus. 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. 34:8290.
75. Hu, Z.,, A. Mukherjee,, S. Pichoff, and, J. Lutkenhaus. 1999. The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc. Natl. Acad. Sci. USA 96:1481914824.
76. Huisman, O.,, R. D’Ari, and, S. Gottesman. 1984. Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc. Natl. Acad. Sci. USA 81:44904494.
77. Ikeda, M.,, T. Sato,, M. Wachi,, H. K. Jung,, F. Ishino,, Y. Kobayashi, and, M. Matsuhashi. 1989. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J. Bacteriol. 171:63756378.
78. Ishidate, K.,, A. Ursinus,, J. V. Holtje, and, L. Roth-field. 1998. Analysis of the length distribution of murein glycan strands in ftsZ and ftsI mutants of E. coli. FEMS Microbiol. Lett. 168:7175.
79. Jensen, S. O.,, L. S. Thompson, and, E. J. Harry. 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. 187:65366544.
80. Johnson, J. E.,, L. L. Lackner,, C. A. Hale, and, P. A. de Boer. 2004. ZipA is required for targeting of DMinC/DicB, but not DMinC/MinD, complexes to septal ring assemblies in Escherichia coli. J. Bacteriol. 186:24182429.
81. Joris, B.,, G. Dive,, A. Henriques,, P. J. Piggot, and, J. M. Ghuysen. 1990. The life-cycle proteins RodA of Escherichia coli and SpoVE of Bacillus subtilis have very similar primary structures. Mol. Microbiol. 4:513517.
82. Judd, E. M.,, L. R. Comolli,, J. C. Chen,, K. H. Downing,, W. E. Moerner, and, H. H. McAdams. 2005. Distinct constrictive processes, separated in time and space, divide caulobacter inner and outer membranes. J. Bacteriol. 187:68746882.
83. Karimova, G.,, N. Dautin, and, D. Ladant. 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 187:22332243.
84. Katis, V. L.,, R. G. Wake, and, E. J. Harry. 2000. Septal localization of the membrane-bound division proteins of Bacillus subtilis DivIB and DivIC is codependent only at high temperatures and requires FtsZ. J. Bacteriol. 182:36073611.
85. Keck, W.,, B. Glauner,, U. Schwarz,, J. K. BroomeSmith, and, B. G. Spratt. 1985. Sequences of the active-site peptides of three of the high-Mr penicillin-binding proteins of Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 82:19992003.
86. Kobayashi, N.,, K. Nishino, and, A. Yamaguchi. 2001. Novel macrolide-specific ABC-type efflux transporter in Escherichia coli. J. Bacteriol. 183:56395644.
87. Lara, B., and, J. A. Ayala. 2002. Topological characterization of the essential Escherichia coli cell division protein FtsW. FEMS Microbiol. Lett. 216:2332.
88. Lara, B.,, D. Mengin-Lecreulx,, J. A. Ayala, and, J. van Heijenoort. 2005a. Peptidoglycan precursor pools associated with MraY and FtsW deficiencies or antibiotic treatments. FEMS Microbiol. Lett. 250:195200.
89. Lara, B.,, A. I. Rico,, S. Petruzzelli,, A. Santona,, J. Dumas,, J. Biton,, M. Vicente,, J. Mingorance, and, O. Massidda. 2005b. Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol. Microbiol. 55:699711.
90. Levy, O.,, J. L. Ptacin,, P. J. Pease,, J. Gore,, M. B. Eisen,, C. Bustamante, and, N. R. Cozzarelli. 2005. Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc. Natl. Acad. Sci. USA 102:1761817623.
91. Liu, N.-J. L.,, R. J. Dutton, and, K. Pogliano. 2006. Evidence that the SpoIIIE DNA translocase participates in membrane fusion during cytokinesis and engulftment. Mol. Microbiol. 59:10971113.
92. Liu, Z.,, A. Mukherjee, and, J. Lutkenhaus. 1999. Recruitment of ZipA to the division site by interaction with FtsZ. Mol. Microbiol. 31:18531861.
93. Low, H. H.,, M. C. Moncrieffe, and, J. Lowe. 2004. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 341:839852.
94. Lu, C.,, M. Reedy, and, H. P. Erickson. 2000. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182:164170.
95. Macheboeuf, P.,, A. M. Di Guilmi,, V. Job,, T. Vernet,, O. Dideberg, and, A. Dessen. 2005. Active site restructuring regulates ligand recognition in class A penicillin-binding proteins. Proc. Natl. Acad. Sci. USA 102:577582.
96. Margolin, W., 2000. Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24:531548.
97. Marrec-Fairley, M.,, A. Piette,, X. Gallet,, R. Brasseur,, H. Hara,, C. Fraipont,, J. M. Ghuysen, and, M. Nguyen-Distèche. 2000. Differential functionalities of amphiphilic peptide segments of the cell-septation penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 37:10191031.
98. Marston, A. L., and, J. Errington. 1999. Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol. Microbiol. 33:8496.
99. Marston, A. L.,, H. B. Thomaides,, D. H. Edwards,, M. E. Sharpe, and, J. Errington. 1998. Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev. 12:34193430.
100. Massey, T. H.,, L. Aussel,, F. X. Barre, and, D. J. Sherratt. 2004. Asymmetric activation of Xer site specific recombination by FtsK. EMBO Rep. 5:399404.
101. Meisel, U.,, J. V. Holtje, and, W. Vollmer. 2003. Overproduction of inactive variants of the murein synthase PBP1B causes lysis in Escherichia coli. J. Bacteriol. 185:53425348.
102. Mercer, K. L., and, D. S. Weiss. 2002. The Escherichia coli cell division protein FtsW is required to recruitits cognate transpeptidase, FtsI (PBP3), to the division site. J. Bacteriol. 184:904912.
103. Miller, C.,, L. E. Thomsen,, C. Gaggero,, R. Mosseri,, H. Ingmer, and, S. N. Cohen. 2004. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305:16291631.
104. Mizusawa, S., and, S. Gottesman. 1983. Protein degradation in Escherichia coli: the lon gene controls the stability of sulA protein. Proc. Natl. Acad. Sci. USA 80:358362.
105. Mosyak, L.,, Y. Zhang,, E. Glasfeld,, S. Haney,, M. Stahl,, J. Seehra, and, W. S. Somers. 2000. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBOJ. 19:31793191.
106. Mukherjee, A.,, C. Cao, and, J. Lutkenhaus. 1998. Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc. Natl. Acad. Sci. USA 95:28852890.
107. Nanninga, N., 1991. Cell division and peptidoglycan assembly in Escherichia coli. Mol Microbiol. 5:791795.
108. Narita, S. I., and, H. Tokuda. 2005. An ABC transporter mediating the membrane detachment of bacterial lipoproteins depending on their sorting signals. FEBS Lett. 580:11641170.
109. Newman, E. B.,, L. I. Budman,, E. C. Chan,, R. C. Greene,, R. T. Lin,, C. L. Woldringh, and, R. D’Ari. 1998. Lack of S-adenosylmethionine results in a cell division defect in Escherichia coli. J. Bacteriol. 180:36143619.
110. Nguyen-Distèche, M.,, C. Fraipont,, N. Buddelmeijer, and, N. Nanninga. 1998. The structure and function of Escherichia coli penicillin-binding protein 3. Cell. Mol. Life Sci. 54:309316.
111. Nicholas, R. A.,, J. L. Strominger,, H. Suzuki, and, Y. Hirota. 1985. Identification of the active site in penicillin-binding protein 3 of Escherichia coli. J. Bacteriol. 164:456460.
112. Noirclerc-Savoye, M.,, A. Le Gouellec,, C. Morlot,, O. Dideberg,, T. Vernet, and, A. Zapun. 2005. In vitro reconstitution of a trimeric complex of DivIB, DivIC and FtsL, and their transient co-localization at the division site in Streptococcus pneumoniae. Mol. Microbiol. 55:413424.
113. Obermann, W., and, J. V. Höltje. 1994. Alterations of murein structure and of penicillin-binding proteins in minicells from Escherichia coli. Microbiology 140:7987.
114. O’Reilly, E. K., and, K. N. Kreuzer. 2004. Isolation of SOS constitutive mutants of Escherichia coli. J. Bacteriol. 186:71497160.
115. Paradis-Bleau, C.,, F. Sanschagrin, and, R. C. Levesque. 2005. Peptide inhibitors of the essential cell division protein FtsA. Protein Eng. Des. Sel. 18:8591.
116. Pares, S.,, N. Mouz,, Y. Petillot,, R. Hakenbeck, and, O. Dideberg. 1996. X-ray structure of Streptococcus pneumoniae PBP2x, a primary penicillin target enzyme. Nat. Struct. Biol. 3:284289.
117. Pastoret, S.,, C. Fraipont,, T. den Blaauwen,, B. Wolf,, M. E. Aarsman,, A. Piette,, A. Thomas,, R. Brasseur, and, M. Nguyen-Disteche. 2004. Functional analysis of the cell division protein FtsW of Escherichia coli. J. Bacteriol. 186:83708379.
118. Pease, P. J.,, O. Levy,, G. J. Cost,, J. Gore,, J. L. Ptacin,, D. Sherratt,, C. Bustamante, and, N. R. Cozzarelli. 2005. Sequence-directed DNA translocation by purified FtsK. Science 307:586590.
119. Pedersen, L. B.,, E. R. Angert, and, P. Setlow. 1999. Septal localization of penicillin-binding protein 1 in Bacillus subtilis. J. Bacteriol. 181:32013211.
120. Pichoff, S., and, J. Lutkenhaus. 2002. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21:685693.
121. Pichoff, S., and, J. Lutkenhaus. 2005. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55:17221734.
122. Piette, A.,, C. Fraipont,, T. Den Blaauwen,, M. E. Aarsman,, S. Pastoret, and, M. Nguyen-Disteche. 2004. Structural determinants required to target penicillin-binding protein 3 to the septum of Escherichia coli. J. Bacteriol. 186:61106117.
123. Raskin, D. M., and, P. A. de Boer. 1999a. MinDEdependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181:64196424.
124. Raskin, D. M., and, P. A. de Boer. 1999b. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. USA 96:49714976.
125. RayChaudhuri, D., 1999. ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J. 18:23722383.
126. Rico, A. I.,, M. Garcia-Ovalle,, J. Mingorance, and, M. Vicente. 2004. Role of two essential domains of Escherichia coli FtsA in localization and progression of the division ring. Mol. Microbiol. 53:13591371.
127. Robson, S. A.,, K. A. Michie,, J. P. Mackay,, E. Harry, and, G. F. King. 2002. The Bacillus subtilis cell division proteins FtsL and DivIC are intrinsically unstable and do not interact with one another in the absence of other septasomal components. Mol. Microbiol. 44:663674.
128. Romberg, L., and, P. A. Levin. 2003. Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. Annu. Rev. Microbiol. 57:125154.
129. Rothfield, L.,, A. Taghbalout, and, Y. L. Shih. 2005. Spatial control of bacterial division-site placement. Nat. Rev. Microbiol. 3:959968.
130. Rueda, S.,, M. Vicente, and, J. Mingorance. 2003. Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J. Bacteriol. 185:33443351.
131. Ryan, K. R., and, L. Shapiro. 2003. Temporal and spatial regulation in prokaryotic cell cycle progression and development. Annu. Rev. Biochem. 72:367394.
132. Sanchez, M.,, A. Valencia,, M. J. Ferrandiz,, C. Sander, and, M. Vicente. 1994. Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J. 13:49194925.
133. Scheffers, D. J.,, L. J. Jones, and, J. Errington. 2004. Several distinct localization patterns for penicillinbinding proteins in Bacillus subtilis. Mol. Microbiol. 51:749764.
134. Schiffer, G., and, J. V. Holtje. 1999. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J. Biol. Chem. 274:3203132039.
135. Schmidt, K. L.,, N. D. Peterson,, R. J. Kustusch,, M. C. Wissel,, B. Graham,, G. J. Phillips, and, D. S. Weiss. 2004. A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J. Bacteriol. 186:785793.
136. Sharp, M. D., and, K. Pogliano. 2002. Role of cellspecific SpoIIIE assembly in polarity of DNA transfer. Science 295:137139.
137. Sharp, M. D., and, K. Pogliano. 2003. The membrane domain of SpoIIIE is required for membrane fusion during Bacillus subtilis sporulation. J Bacteriol. 185:2005–2008.
138. Sievers, J., and, J. Errington. 2000. The Bacillus subtilis cell division protein FtsL localizes to sites of septation and interacts with DivIC. Mol. Microbiol. 36:846855.
139. Spratt, B. G., and, A. B. Pardee. 1975. Penicillinbinding proteins and cell shape in E. coli. Nature 254:516517.
140. Steiner, W.,, G. Liu,, W. D. Donachie, and, P. Kuempel. 1999. The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol. Microbiol. 31:579583.
141. Stenberg, F.,, P. Chovanec,, S. L. Maslen,, C. V. Robinson,, L. L. Ilag,, G. von Heijne, and, D. O. Daley. 2005. Protein complexes of the Escherichia coli cell envelope. J. Biol. Chem. 280:3440934419.
142. Stricker, J.,, P. Maddox,, E. D. Salmon, and, H. P. Erickson. 2002. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. USA 99:31713175.
143. Taschner, P. E.,, P. G. Huls,, E. Pas, and, C. L. Woldringh. 1988. Division behavior and shape changes in isogenic jtsZ, jtsQ, jtsA, pbpB, and ftsE cell division mutants of Escherichia coli during temperature shift experiments. J. Bacteriol. 170:15331540.
144. Thanedar, S., and, W. Margolin. 2004. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14:11671173.
145. Trusca, D.,, S. Scott,, C. Thompson, and, D. Bramhill. 1998. Bacterial SOS checkpoint protein SulA inhibits polymerization of purified FtsZ cell division protein. J. Bacteriol. 180:39463953.
146. Ursinus, A.,, F. van den Ent,, S. Brechtel,, M. de Pedro,, J. V. Holtje,, J. Lowe, and, W. Vollmer. 2004. Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichi acoli. J. Bacteriol. 186:67286737.
147. van den Ent, F., and, J. Lowe. 2000. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J. 19:53005307.
148. Varma, A., and, K. D.Y oung. 2004. FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J. Bacteriol. 186: 67686774.
149. Vicente, M.,, A. I. Rico,, R. Martinez-Arteaga, and, J. Mingorance. 2006. Septum enlightenment: assembly of bacterial division proteins. J. Bacteriol. 188:1927.
150. Vollmer, W.,, M. von Rechenberg, and, J. V. Höltje. 1999. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol. Chem. 274:67266734.
151. von Rechenberg, M.,, A. Ursinus, and, J. V. Höltje. 1996. Affinity chromatography as a means to study multienzyme complexes involved in murein synthesis. Microb. Drug Resist. 2:155157.
152. Wang, H., and, R. C. Gayda,, Wang, H., and, R. C. Gayda,, Wang, H., and, R. C. Gayda. 1992. Quantitative determination of FtsA at different growth rates in Escherichia coli using monoclonal antibodies. Mol. Microbiol. 6:25172524.
153. Wang, L., and, J. Lutkenhaus. 1998. FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response. Mol. Microbiol. 29:731740.
154. Wang, S.,, S. J. Arends,, D. S. Weiss, and, E. B. Newman. 2005. A deficiency in S-adenosylmethionine synthetase interrupts assembly of the septal ring in Escherichia coli K-12. Mol. Microbiol. 58:791799.
155. Weigand, R. A.,, K. D.V inci, and, L. I. Rothfield. 1976. Morphogenesis of the bacterial division sep tum: a new class of septation-defective mutants. Proc. Natl. Acad. Sci. USA 73:18821886.
156. Weiss, D. S., 2004. Bacterial cell division and the septal ring. Mol. Microbiol. 54:588597.
157. Weiss, D. S.,, J. C. Chen,, J. M. Ghigo,, D. Boyd, and, J. Beckwith. 1999. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL.J. Bacteriol. 181:508520.
158. Weiss, D. S.,, K. Pogliano,, M. Carson,, L. M. Guzman,, C. Fraipont,, M. Nguyen-Disteche,, R. Losick, and, J. Beckwith. 1997. Localization of the Escherichia coli cell division protein Ftsl (PBP3) to the division site and cell pole. Mol. Microbiol. 25:671681.
159. Wientjes, F. B., and, N. Nanninga. 1989. Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J. Bacteriol. 171:34123419.
160. Wientjes, F. B., and, N. Nanninga. 1991. On the role of the high molecular weight penicillin-binding proteins in the cell cycle of Escherichia coli. Res. Microbiol. 142:333344.
161. Wissel, M. C., and, D. S. Weiss. 2004. Genetic analysis of the cell division protein FtsI (PBP3): amino acid substitutions that impair septal localization of FtsI and recruitment of FtsN.J. Bacteriol. 186:490502.
162. Wissel, M. C.,, J. L. Wendt,, C. J. Mitchell, and, D. S. Weiss. 2005. The transmembrane helix of the Escherichia coli division protein FtsI localizes to the septal ring. J. Bacteriol. 187:320328.
163. Woldringh, C. L.,, E. Mulder,, P. G. Huls, and, N. Vischer. 1991. Toporegulation of bacterial division according to the nucleoid occlusion model. Res. Microbiol. 142:309320.
164. Wu, L. J., and, J. Errington. 2004. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915925.
165. Yang, J. C.,, F. Van Den Ent,, D. Neuhaus,, J. Brevier, and, J. Lowe. 2004. Solution structure and domain architecture of the divisome protein FtsN. Mol. Microbiol. 52:651660.
166. Yates, J.,, M. Aroyo,, D. J. Sherratt, and, F. X. Barre. 2003. Species specificity in the activation of Xer recombination at dif by FtsK. Mol. Microbiol. 49:241249.
167. Yim, L.,, G. Vandenbussche,, J. Mingorance,, S. Rueda,, M. Casanova,, J. M. Ruysschaert, and, M. Vicente. 2000. Role of the carboxy terminus of Escherichia coli FtsA in self-interaction and cell division. J. Bacteriol. 182:63666373.
168. Yousif, S. Y.,, J. K. Broome-Smith, and, B. G. Spratt. 1985. Lysis of Escherichia coli by beta-lactam antibiotics: deletion analysis of the role of penicillin-binding proteins 1A and 1B. J. Gen. Microbiol. 131:28392845.
169. Yu, X. C.,, A. H. Tran,, Q. Sun, and, W. Margolin. 1998. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J. Bacteriol. 180:12961304.


Generic image for table

Proteins found in the septal ring of

Citation: Arends S, Williams K, Kustusch R, Weiss D. 2007. Cell Division, p 173-197. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch10
Generic image for table

Proteins that regulate cell division in

Citation: Arends S, Williams K, Kustusch R, Weiss D. 2007. Cell Division, p 173-197. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch10

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