Assembly and activation of the Escherichia coli divisome

Cell division in Escherichia coli is mediated by a large protein complex called the divisome. Most of the divisome proteins have been identified, but how they assemble onto the Z ring scaffold to form the divisome and work together to synthesize the septum is not well understood. In this review, we summarize the latest findings on divisome assembly and activation as well as provide our perspective on how these two processes might be regulated.

[1]  Jie Xiao,et al.  ZapA and ZapB form an FtsZ‐independent structure at midcell , 2017, Molecular microbiology.

[2]  J. Männik,et al.  Kinetics of large-scale chromosomal movement during asymmetric cell division in Escherichia coli , 2017, PLoS genetics.

[3]  J. Errington,et al.  RodA as the missing glycosyltransferase in Bacillus subtilis and antibiotic discovery for the peptidoglycan polymerase pathway , 2017, Nature Microbiology.

[4]  Carla Coltharp,et al.  Beyond force generation: Why is a dynamic ring of FtsZ polymers essential for bacterial cytokinesis? , 2017, BioEssays : news and reviews in molecular, cellular and developmental biology.

[5]  C. Dekker,et al.  Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division , 2016, Science.

[6]  K. C. Huang,et al.  GTPase activity–coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis , 2016, Science.

[7]  J. Marto,et al.  Bacterial cell wall biogenesis is mediated by SEDS and PBP polymerase families functioning semi-autonomously , 2016, Nature Microbiology.

[8]  Shishen Du,et al.  FtsEX acts on FtsA to regulate divisome assembly and activity , 2016, Proceedings of the National Academy of Sciences.

[9]  A. Kruse,et al.  SEDS proteins are a widespread family of bacterial cell wall polymerases , 2016, Nature.

[10]  Takanari Inoue,et al.  A novel membrane anchor for FtsZ is linked to cell wall hydrolysis in Caulobacter crescentus , 2016, Molecular microbiology.

[11]  S. Walker,et al.  Cofactor bypass variants reveal a conformational control mechanism governing cell wall polymerase activity , 2016, Proceedings of the National Academy of Sciences.

[12]  Daniel P. Haeusser,et al.  A mutation in Escherichia coli ftsZ bypasses the requirement for the essential division gene zipA and confers resistance to FtsZ assembly inhibitors by stabilizing protofilament bundling , 2015, Molecular microbiology.

[13]  D. Weiss,et al.  Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides , 2015, Proceedings of the National Academy of Sciences.

[14]  T. Munder,et al.  The essential role of SepF in mycobacterial division , 2015, Molecular microbiology.

[15]  I. D. de Esch,et al.  The Soluble Periplasmic Domains of Escherichia coli Cell Division Proteins FtsQ/FtsB/FtsL Form a Trimeric Complex with Submicromolar Affinity* , 2015, The Journal of Biological Chemistry.

[16]  M. Tsang,et al.  Guiding divisome assembly and controlling its activity. , 2015, Current opinion in microbiology.

[17]  H. Hess,et al.  A Multi-layered Protein Network Stabilizes the Escherichia coli FtsZ-ring and Modulates Constriction Dynamics , 2015, PLoS genetics.

[18]  Shishen Du,et al.  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 , 2015, Molecular microbiology.

[19]  Bing Liu,et al.  Roles for both FtsA and the FtsBLQ subcomplex in FtsN‐stimulated cell constriction in Escherichia coli , 2015, Molecular microbiology.

[20]  M. Tsang,et al.  A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division , 2015, Molecular microbiology.

[21]  Jennifer R. Herricks,et al.  A thermosensitive defect in the ATP binding pocket of FtsA can be suppressed by allosteric changes in the dimer interface , 2014, Molecular microbiology.

[22]  W. Margolin,et al.  A role for FtsA in SPOR‐independent localization of the essential Escherichia coli cell division protein FtsN , 2014, Molecular microbiology.

[23]  B. de Kruijff,et al.  Specificity of the Transport of Lipid II by FtsW in Escherichia coli* , 2014, The Journal of Biological Chemistry.

[24]  S. Ishikawa,et al.  Structural and genetic analyses reveal the protein SepF as a new membrane anchor for the Z ring , 2013, Proceedings of the National Academy of Sciences.

[25]  Shishen Du,et al.  Bacterial cytokinesis: From Z ring to divisome , 2012, Cytoskeleton.

[26]  O. Espéli,et al.  A MatP–divisome interaction coordinates chromosome segregation with cell division in E. coli , 2012, The EMBO journal.

[27]  J. Löwe,et al.  FtsA forms actin‐like protofilaments , 2012, The EMBO journal.

[28]  E. Rivkin,et al.  Identification of ZapD as a Cell Division Factor That Promotes the Assembly of FtsZ in Escherichia coli , 2012, Journal of bacteriology.

[29]  W. Margolin,et al.  The Early Divisome Protein FtsA Interacts Directly through Its 1c Subdomain with the Cytoplasmic Domain of the Late Divisome Protein FtsN , 2012, Journal of bacteriology.

[30]  J. Lutkenhaus,et al.  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 , 2012, Molecular microbiology.

[31]  T. Bernhardt,et al.  An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring , 2011, Proceedings of the National Academy of Sciences.

[32]  Eduardo Abeliuk,et al.  Assembly of the Caulobacter cell division machine , 2011, Molecular microbiology.

[33]  T. Vernet,et al.  Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane , 2011, The EMBO journal.

[34]  Helen Yu,et al.  Identification and Characterization of ZapC, a Stabilizer of the FtsZ Ring in Escherichia coli , 2011, Journal of bacteriology.

[35]  P. D. de Boer,et al.  Identification of Escherichia coli ZapC (YcbW) as a Component of the Division Apparatus That Binds and Bundles FtsZ Polymers , 2011, Journal of bacteriology.

[36]  Waldemar Vollmer,et al.  Regulation of peptidoglycan synthesis by outer membrane proteins , 2010, Cell.

[37]  S. Walker,et al.  Lipoprotein Cofactors Located in the Outer Membrane Activate Bacterial Cell Wall Polymerases , 2010, Cell.

[38]  H. Erickson,et al.  FtsZ in Bacterial Cytokinesis: Cytoskeleton and Force Generator All in One , 2010, Microbiology and Molecular Biology Reviews.

[39]  Nelly Dubarry,et al.  Multiple regions along the Escherichia coli FtsK protein are implicated in cell division , 2010, Molecular microbiology.

[40]  J. Lutkenhaus FtsN—Trigger for Septation , 2009, Journal of bacteriology.

[41]  P. D. de Boer,et al.  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 , 2009, Journal of bacteriology.

[42]  M. Marbouty,et al.  Characterization of the FtsZ-Interacting Septal Proteins SepF and Ftn6 in the Spherical-Celled Cyanobacterium Synechocystis Strain PCC 6803 , 2009, Journal of bacteriology.

[43]  Ryan J. Kustusch,et al.  ATP-Binding Site Lesions in FtsE Impair Cell Division , 2009, Journal of bacteriology.

[44]  R. D. Makde,et al.  A membrane protein, EzrA, regulates assembly dynamics of FtsZ by interacting with the C-terminal tail of FtsZ. , 2007, Biochemistry.

[45]  J. Lutkenhaus,et al.  Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. , 2007, Annual review of biochemistry.

[46]  W. Margolin,et al.  Interaction between Cell Division Proteins FtsE and FtsZ , 2007, Journal of bacteriology.

[47]  M. Reddy Role of FtsEX in Cell Division of Escherichia coli: Viability of ftsEX Mutants Is Dependent on Functional SufI or High Osmotic Strength , 2006, Journal of bacteriology.

[48]  J. Beckwith,et al.  Premature targeting of cell division proteins to midcell reveals hierarchies of protein interactions involved in divisome assembly , 2006, Molecular microbiology.

[49]  S. Ishikawa,et al.  A new FtsZ‐interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis , 2006, Molecular microbiology.

[50]  L. Hamoen,et al.  SepF, a novel FtsZ‐interacting protein required for a late step in cell division , 2006, Molecular microbiology.

[51]  W. Margolin,et al.  Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK , 2005, Molecular microbiology.

[52]  J. Beckwith,et al.  Diverse Paths to Midcell: Assembly of the Bacterial Cell Division Machinery , 2005, Current Biology.

[53]  D. Ladant,et al.  Interaction Network among Escherichia coli Membrane Proteins Involved in Cell Division as Revealed by Bacterial Two-Hybrid Analysis , 2005, Journal of bacteriology.

[54]  J. Lutkenhaus,et al.  Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA , 2005, Molecular microbiology.

[55]  T. den Blaauwen,et al.  Maturation of the Escherichia coli divisome occurs in two steps , 2005, Molecular microbiology.

[56]  J. Beckwith,et al.  A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region , 2004, Molecular microbiology.

[57]  Kari L. Schmidt,et al.  A Predicted ABC Transporter, FtsEX, Is Needed for Cell Division in Escherichia coli , 2004, Journal of bacteriology.

[58]  W. Margolin,et al.  A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Beckwith,et al.  Assembly of cell division proteins at the E. coli cell center. , 2002, Current opinion in microbiology.

[60]  Frederico J. Gueiros-Filho,et al.  A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. , 2002, Genes & development.

[61]  J. Beckwith,et al.  YgbQ, a cell division protein in Escherichia coli and Vibrio cholerae, localizes in codependent fashion with FtsL to the division site , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[62]  E. Salmon,et al.  Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Lutkenhaus,et al.  Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli , 2002, The EMBO journal.

[64]  J. Beckwith,et al.  FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co‐localization with FtsZ during Escherichia coli cell division , 2001, Molecular microbiology.

[65]  Yan Zhang,et al.  The bacterial cell‐division protein ZipA and its interaction with an FtsZ fragment revealed by X‐ray crystallography , 2001, The EMBO journal.

[66]  Jan Löwe,et al.  Crystal structure of the cell division protein FtsA from Thermotoga maritima , 2000, The EMBO journal.

[67]  W. Margolin,et al.  Genetic and Functional Analyses of the Conserved C-Terminal Core Domain of Escherichia coli FtsZ , 1999, Journal of bacteriology.

[68]  W. Donachie,et al.  The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers , 1999, Molecular microbiology.

[69]  W. Margolin,et al.  Role of the C Terminus of FtsK in Escherichia coli Chromosome Segregation , 1998, Journal of bacteriology.

[70]  W. Donachie,et al.  Only the N-Terminal Domain of FtsK Functions in Cell Division , 1998, Journal of bacteriology.

[71]  J. Lutkenhaus,et al.  FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response , 1998, Molecular microbiology.

[72]  W. Donachie,et al.  FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli , 1998, Molecular microbiology.

[73]  W. Margolin,et al.  Localization of Cell Division Protein FtsK to theEscherichia coli Septum and Identification of a Potential N-Terminal Targeting Domain , 1998, Journal of bacteriology.

[74]  L. Amos,et al.  Crystal structure of the bacterial cell-division protein FtsZ , 1998, Nature.

[75]  J. Beckwith,et al.  Domain-swapping analysis of FtsI, FtsL, and FtsQ, bitopic membrane proteins essential for cell division in Escherichia coli , 1997, Journal of bacteriology.

[76]  J. Lutkenhaus,et al.  FtsN, a late recruit to the septum in Escherichia coli , 1997, Molecular microbiology.

[77]  C. Hale,et al.  Direct Binding of FtsZ to ZipA, an Essential Component of the Septal Ring Structure That Mediates Cell Division in E. coli , 1997, Cell.

[78]  J. Lutkenhaus,et al.  FtsZ‐spirals and ‐arcs determine the shape of the invaginating septa in some mutants of Escherichia coli , 1996, Molecular microbiology.

[79]  J. Lutkenhaus,et al.  Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[80]  D. Raychaudhuri,et al.  Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein , 1992, Nature.

[81]  L. Rothfield,et al.  The essential bacterial cell-division protein FtsZ is a GTPase , 1992, Nature.

[82]  P Bork,et al.  An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[83]  J. Lutkenhaus,et al.  Impaired cell division and sporulation of a Bacillus subtilis strain with the ftsA gene deleted , 1992, Journal of bacteriology.

[84]  E. Bi,et al.  FtsZ ring structure associated with division in Escherichia coli , 1991, Nature.

[85]  J. Beckwith,et al.  The FtsQ protein of Escherichia coli: membrane topology, abundance, and cell division phenotypes due to overproduction and insertion mutations , 1991, Journal of bacteriology.

[86]  J. Lutkenhaus,et al.  Nucleotide sequence and insertional inactivation of a Bacillus subtilis gene that affects cell division, sporulation, and temperature sensitivity , 1989, Journal of bacteriology.

[87]  M. Ikeda,et al.  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 , 1989, Journal of bacteriology.

[88]  G. Salmond,et al.  A new cell division operon inEscherichia coli , 1986, Molecular and General Genetics MGG.

[89]  James T. Park,et al.  Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation but not during cell elongation , 1981, Journal of bacteriology.

[90]  P. D. de Boer,et al.  Advances in understanding E. coli cell fission. , 2010, Current opinion in microbiology.

[91]  Frederico J. Gueiros-Filho,et al.  Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli. , 2005, Genes & development.