The Bacterial Cytoskeleton

SUMMARY In recent years it has been shown that bacteria contain a number of cytoskeletal structures. The bacterial cytoplasmic elements include homologs of the three major types of eukaryotic cytoskeletal proteins (actin, tubulin, and intermediate filament proteins) and a fourth group, the MinD-ParA group, that appears to be unique to bacteria. The cytoskeletal structures play important roles in cell division, cell polarity, cell shape regulation, plasmid partition, and other functions. The proteins self-assemble into filamentous structures in vitro and form intracellular ordered structures in vivo. In addition, there are a number of filamentous bacterial elements that may turn out to be cytoskeletal in nature. This review attempts to summarize and integrate the in vivo and in vitro aspects of these systems and to evaluate the probable future directions of this active research field.

[1]  V. Niggli,et al.  Structural properties of lipid-binding sites in cytoskeletal proteins. , 2001, Trends in biochemical sciences.

[2]  J. Lutkenhaus,et al.  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 , 1999, Molecular microbiology.

[3]  B. Spratt,et al.  Peptidoglycan synthetic activities in membranes of Escherichia coli caused by overproduction of penicillin-binding protein 2 and rodA protein. , 1986, The Journal of biological chemistry.

[4]  A. Hoffmaster,et al.  Sequence, assembly and analysis of pX01 and pX02 , 1999, Journal of applied microbiology.

[5]  Promiscuous targeting of Bacillus subtilis cell division protein DivIVA to division sites in Escherichia coli and fission yeast , 2000, The EMBO journal.

[6]  Ueli Aebi,et al.  Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. , 2003, Annual review of biochemistry.

[7]  M. Billeter,et al.  MOLMOL: a program for display and analysis of macromolecular structures. , 1996, Journal of molecular graphics.

[8]  D. Raychaudhuri ZipA is a MAP–Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division , 1999, EMBO Journal.

[9]  I. Kurtser,et al.  Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Walker,et al.  Distantly related sequences in the alpha‐ and beta‐subunits of ATP synthase, myosin, kinases and other ATP‐requiring enzymes and a common nucleotide binding fold. , 1982, The EMBO journal.

[11]  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.

[12]  S. Hiraga,et al.  Subcellular positioning of F plasmid mediated by dynamic localization of SopA and SopB. , 2006, Journal of molecular biology.

[13]  D. Bramhill,et al.  Fluorescent assay for polymerization of purified bacterial FtsZ cell-division protein. , 2002, Analytical biochemistry.

[14]  E. Bi,et al.  FtsZ ring formation in fts mutants , 1996, Journal of bacteriology.

[15]  D. Bramhill,et al.  Bacterial SOS Checkpoint Protein SulA Inhibits Polymerization of Purified FtsZ Cell Division Protein , 1998, Journal of bacteriology.

[16]  N. Wingreen,et al.  Dynamic structures in Escherichia coli: Spontaneous formation of MinE rings and MinD polar zones , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. B. Jensen,et al.  Partitioning of plasmid R1. The ParM protein exhibits ATPase activity and interacts with the centromere-like ParR-parC complex. , 1997, Journal of molecular biology.

[18]  M. de Pedro,et al.  Restricted Mobility of Cell Surface Proteins in the Polar Regions of Escherichia coli , 2004, Journal of bacteriology.

[19]  S. Maciver How ADF/cofilin depolymerizes actin filaments. , 1998, Current opinion in cell biology.

[20]  P. Graumann,et al.  Dynamic movement of actin‐like proteins within bacterial cells , 2004, EMBO reports.

[21]  J. Errington,et al.  Recruitment of penicillin‐binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates , 2004, Molecular microbiology.

[22]  L. Amos,et al.  Tubulin‐like protofilaments in Ca2+‐induced FtsZ sheets , 1999, The EMBO journal.

[23]  D. Ehrhardt,et al.  Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. Lutkenhaus,et al.  Membrane Binding by MinD Involves Insertion of Hydrophobic Residues within the C-Terminal Amphipathic Helix into the Bilayer , 2003, Journal of bacteriology.

[25]  D. Wirtz,et al.  The Assembly of MreB, a Prokaryotic Homolog of Actin* , 2005, Journal of Biological Chemistry.

[26]  L. Rothfield,et al.  Cell division inhibitors SulA and MinC/MinD block septum formation at different steps in the assembly of the Escherichia coli division machinery , 2000, Molecular microbiology.

[27]  James T. Staley,et al.  In vitro assembly and GTP hydrolysis by bacterial tubulins BtubA and BtubB , 2005, The Journal of cell biology.

[28]  M. de Pedro,et al.  Branching of Escherichia coli Cells Arises from Multiple Sites of Inert Peptidoglycan , 2003, Journal of bacteriology.

[29]  R. Losick,et al.  Does RNA polymerase help drive chromosome segregation in bacteria? , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  H. Erickson,et al.  FtsZ from Escherichia coli, Azotobacter vinelandii, and Thermotoga maritima--quantitation, GTP hydrolysis, and assembly. , 1998, Cell motility and the cytoskeleton.

[31]  K. Chater,et al.  Partitioning of the Linear Chromosome during Sporulation of Streptomyces coelicolor A3(2) Involves an oriC-Linked parAB Locus , 2000, Journal of bacteriology.

[32]  T. Leonard,et al.  Bacterial chromosome segregation: structure and DNA binding of the Soj dimer — a conserved biological switch , 2005, The EMBO journal.

[33]  A. Hunding,et al.  A mechanism for ParB-dependent waves of ParA, a protein related to DNA segregation during cell division in prokaryotes. , 2003, Journal of molecular biology.

[34]  M. Rosenberg,et al.  Bacterial DNA segregation dynamics mediated by the polymerizing protein ParF , 2005, The EMBO journal.

[35]  J. Poindexter,et al.  Novel peptidoglycans in Caulobacter and Asticcacaulis spp , 1982, Journal of bacteriology.

[36]  O. Espéli,et al.  SetB: an integral membrane protein that affects chromosome segregation in Escherichia coli , 2003, Molecular microbiology.

[37]  W. Cook,et al.  Compartmentalization of the periplasmic space at division sites in gram-negative bacteria , 1986, Journal of bacteriology.

[38]  J. T. Staley,et al.  Eukaryotic signature proteins of Prosthecobacter dejongeii and Gemmata sp. Wa-1 as revealed by in silico analysis. , 2005, FEMS microbiology letters.

[39]  J. Hinshaw,et al.  Dynamin Undergoes a GTP-Dependent Conformational Change Causing Vesiculation , 1998, Cell.

[40]  J. Errington,et al.  The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division , 1997, Molecular microbiology.

[41]  Wouter-Jan Rappel,et al.  Division accuracy in a stochastic model of Min oscillations in Escherichia coli. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. Görg,et al.  Defining the mycoplasma 'cytoskeleton': the protein composition of the Triton X-100 insoluble fraction of the bacterium Mycoplasma pneumoniae determined by 2-D gel electrophoresis and mass spectrometry. , 2001, Microbiology.

[43]  T D Pollard,et al.  Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. , 2000, Annual review of biophysics and biomolecular structure.

[44]  P. D. de Boer,et al.  ZipA-Induced Bundling of FtsZ Polymers Mediated by an Interaction between C-Terminal Domains , 2000, Journal of bacteriology.

[45]  S. Trachtenberg Mollicutes-wall-less bacteria with internal cytoskeletons. , 1998, Journal of structural biology.

[46]  K. Asai,et al.  A Bacillus subtilis gene‐encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition , 1998, Molecular microbiology.

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

[48]  M. Aldea,et al.  Preferential cytoplasmic location of FtsZ, a protein essential for Escherichia coli septation , 1991, Molecular Microbiology.

[49]  C. Price,et al.  The minCD locus of Bacillus subtilis lacks the minE determinant that provides topological specificity to cell division , 1993, Molecular microbiology.

[50]  Harley H. McAdams,et al.  Generating and Exploiting Polarity in Bacteria , 2002, Science.

[51]  L. Rothfield,et al.  Role Of MinD-Membrane Association in Min Protein Interactions , 2006, Journal of bacteriology.

[52]  S. Huecas,et al.  Energetics of the Cooperative Assembly of Cell Division Protein FtsZ and the Nucleotide Hydrolysis Switch* , 2003, Journal of Biological Chemistry.

[53]  Zachary Pincus,et al.  Two independent spiral structures control cell shape in Caulobacter. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[54]  ro Jorge Serment-Guerrero,et al.  The SOS response of Escherichia coli , 2005 .

[55]  R. Herrmann,et al.  Cytoskeletal elements in the bacterium Mycoplasma pneumoniae , 2002, Naturwissenschaften.

[56]  J. Gober,et al.  Cell Cycle–Dependent Polar Localization of Chromosome Partitioning Proteins in Caulobacter crescentus , 1997, Cell.

[57]  K. Schleifer,et al.  Defensive extrusive ectosymbionts of Euplotidium (Ciliophora) that contain microtubule-like structures are bacteria related to Verrucomicrobia. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  P. Graumann,et al.  Actin-like Proteins MreB and Mbl from Bacillus subtilis Are Required for Bipolar Positioning of Replication Origins , 2003, Current Biology.

[59]  N. Nanninga,et al.  Penicillin‐binding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid‐cell in comparison with the old cell pole , 2003, Molecular microbiology.

[60]  D. Lane,et al.  The parAB gene products of Pseudomonas putida exhibit partition activity in both P. putida and Escherichia coli , 2002, Molecular microbiology.

[61]  W. Cook,et al.  Membrane-murein attachment at the leading edge of the division septum: a second membrane-murein structure associated with morphogenesis of the gram-negative bacterial division septum , 1987, Journal of bacteriology.

[62]  Anthony A. Hyman,et al.  Structural Transitions at Microtubule Ends Correlate with Their Dynamic Properties in Xenopus Egg Extracts , 2000, The Journal of cell biology.

[63]  N Watanabe,et al.  The three-dimensional structure of septum site-determining protein MinD from Pyrococcus horikoshii OT3 in complex with Mg-ADP. , 2001, Structure.

[64]  M. Elowitz,et al.  Protein Mobility in the Cytoplasm ofEscherichia coli , 1999, Journal of bacteriology.

[65]  C. Walsh,et al.  Identification of vancomycin resistance protein VanA as a D-alanine:D-alanine ligase of altered substrate specificity. , 1991, Biochemistry.

[66]  S. Tamaki,et al.  Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli , 1987, Journal of bacteriology.

[67]  J. Theriot,et al.  Complex spatial distribution and dynamics of an abundant Escherichia coli outer membrane protein, LamB , 2004, Molecular microbiology.

[68]  Zemer Gitai,et al.  MreB Actin-Mediated Segregation of a Specific Region of a Bacterial Chromosome , 2005, Cell.

[69]  Achilleas S. Frangakis,et al.  Cryo-Electron Tomography Reveals the Cytoskeletal Structure of Spiroplasma melliferum , 2005, Science.

[70]  M. de Pedro,et al.  Patchiness of murein insertion into the sidewall of Escherichia coli. , 2003, Microbiology.

[71]  J. Lutkenhaus,et al.  MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation , 2003, Molecular microbiology.

[72]  G. King,et al.  Mapping the MinE Site Involved in Interaction with the MinD Division Site Selection Protein of Escherichia coli , 2003, Journal of bacteriology.

[73]  P. Levin,et al.  Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. , 2003, Annual review of microbiology.

[74]  D. Wirtz,et al.  GTPase Activity, Structure, and Mechanical Properties of Filaments Assembled from Bacterial Cytoskeleton Protein MreB , 2006, Journal of bacteriology.

[75]  K. Gerdes,et al.  Bacterial mitosis: partitioning protein ParA oscillates in spiral‐shaped structures and positions plasmids at mid‐cell , 2004, Molecular microbiology.

[76]  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.

[77]  E. Nogales,et al.  Refined structure of alpha beta-tubulin at 3.5 A resolution. , 2001, Journal of molecular biology.

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

[79]  Leigh G. Monahan,et al.  Trapping of a Spiral-Like Intermediate of the Bacterial Cytokinetic Protein FtsZ , 2006, Journal of bacteriology.

[80]  R. Pfister,et al.  Intracellular structures of Mycoplasma pneumoniae revealed after membrane removal , 1980, Journal of bacteriology.

[81]  J. Gober,et al.  MreB, the cell shape‐determining bacterial actin homologue, co‐ordinates cell wall morphogenesis in Caulobacter crescentus , 2004, Molecular microbiology.

[82]  A. Grossman,et al.  Control of development by altered localization of a transcription factor in B. subtilis. , 1999, Molecular cell.

[83]  W. Margolin,et al.  FtsZ Exhibits Rapid Movement and Oscillation Waves in Helix-like Patterns in Escherichia coli , 2004, Current Biology.

[84]  K. Young,et al.  Helical Disposition of Proteins and Lipopolysaccharide in the Outer Membrane of Escherichia coli , 2005, Journal of bacteriology.

[85]  L. Rothfield,et al.  The periseptal annulus: An organelle associated with cell division in Gram-negative bacteria. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[86]  R. Valluzzi,et al.  Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Donald A. Drew,et al.  A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[88]  R. Losick,et al.  Asymmetric Cell Division in B. subtilis Involves a Spiral-like Intermediate of the Cytokinetic Protein FtsZ , 2002, Cell.

[89]  M. Goldberg,et al.  Presence of Multiple Sites Containing Polar Material in Spherical Escherichia coli Cells That Lack MreB , 2005, Journal of bacteriology.

[90]  Mark W. Maciejewski,et al.  Structural basis for the topological specificity function of MinE , 2000, Nature Structural Biology.

[91]  J. Lutkenhaus,et al.  Dynamic assembly of FtsZ regulated by GTP hydrolysis , 1998, The EMBO journal.

[92]  R. Vale,et al.  Identification of katanin, an ATPase that severs and disassembles stable microtubules , 1993, Cell.

[93]  H. Erickson,et al.  Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[94]  A. Grossman,et al.  Identification and Characterization of a Bacterial Chromosome Partitioning Site , 1998, Cell.

[95]  H. Niki,et al.  Active segregation by the Bacillus subtilis partitioning system in Escherichia coli. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[97]  A. Grossman,et al.  spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis , 1994, Journal of bacteriology.

[98]  Frederico J. Gueiros-Filho,et al.  Assembly Dynamics of FtsZ Rings in Bacillus subtilis and Escherichia coli and Effects of FtsZ-Regulating Proteins , 2004, Journal of bacteriology.

[99]  R. Losick,et al.  Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. , 1996, Genes & development.

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

[101]  E. Garner,et al.  Dynamic Instability in a DNA-Segregating Prokaryotic Actin Homolog , 2004, Science.

[102]  H. Lam,et al.  A Landmark Protein Essential for Establishing and Perpetuating the Polarity of a Bacterial Cell , 2006, Cell.

[103]  D. Bramhill,et al.  Bacterial cell division. , 1997, Annual review of cell and developmental biology.

[104]  H. Nagura,et al.  Structure-Activity Relationship of S-Benzylisothiourea Derivatives to Induce Spherical Cells in Escherichia coli , 2004, Bioscience, biotechnology, and biochemistry.

[105]  Yu-Ling Shih,et al.  Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[106]  R. P. Burchard,et al.  Intracellular, periodic structures in the gliding bacterium Myxococcus xanthus , 1977, Journal of bacteriology.

[107]  J. Errington,et al.  Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. , 1998, Genes & development.

[108]  L. Rothfield,et al.  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 , 2004, Molecular microbiology.

[109]  D. Archer,et al.  Purification and preliminary characterization of Spiroplasma fibrils , 1980, Journal of bacteriology.

[110]  Y. Brun,et al.  Ordered expression of ftsQA and ftsZ during the Caulobacter crescentus cell cycle , 1998, Molecular microbiology.

[111]  K. Nordström,et al.  Mechanisms that contribute to the stable segregation of plasmids. , 1989, Annual review of genetics.

[112]  E. Huitema,et al.  Bacterial Birth Scar Proteins Mark Future Flagellum Assembly Site , 2006, Cell.

[113]  H. Erickson The FtsZ protofilament and attachment of ZipA--structural constraints on the FtsZ power stroke. , 2001, Current opinion in cell biology.

[114]  Judith P. Armitage,et al.  Localization of MreB in Rhodobacter sphaeroides under Conditions Causing Changes in Cell Shape and Membrane Structure , 2005, Journal of bacteriology.

[115]  J. Errington,et al.  A magnesium‐dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis , 2005, Molecular microbiology.

[116]  W. Margolin,et al.  FtsZ Dynamics during the Division Cycle of LiveEscherichia coli Cells , 1998, Journal of bacteriology.

[117]  Michio Homma,et al.  Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery , 2006, Molecular microbiology.

[118]  P. D. de Boer,et al.  MinDE-Dependent Pole-to-Pole Oscillation of Division Inhibitor MinC in Escherichia coli , 1999, Journal of bacteriology.

[119]  E V Koonin,et al.  A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif. , 1993, Journal of molecular biology.

[120]  S. Acharya,et al.  A conserved polar region in the cell division site determinant MinD is required for responding to MinE-induced oscillation but not for localization within coiled arrays. , 2005, Research in microbiology.

[121]  J. Hoch,et al.  A negative regulator linking chromosome segregation to developmental transcription in Bacillus subtilis , 1998, Molecular microbiology.

[122]  K. Gerdes,et al.  The double par locus of virulence factor pB171: DNA segregation is correlated with oscillation of ParA , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[123]  Boer,et al.  Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli , 1992, Journal of bacteriology.

[124]  Yu-Ling Shih,et al.  Division site placement in E.coli: mutations that prevent formation of the MinE ring lead to loss of the normal midcell arrest of growth of polar MinD membrane domains , 2002, The EMBO journal.

[125]  F. Neidhardt,et al.  Escherichia Coli and Salmonella: Typhimurium Cellular and Molecular Biology , 1987 .

[126]  Robert D. Goldman,et al.  Intermediate filaments mediate cytoskeletal crosstalk , 2004, Nature Reviews Molecular Cell Biology.

[127]  Ueli Aebi,et al.  Molecular mechanisms underlying the assembly of intermediate filaments. , 2004, Experimental cell research.

[128]  J. Izard,et al.  Genetic and Structural Analyses of Cytoplasmic Filaments of Wild-Type Treponema phagedenis and a Flagellar Filament-Deficient Mutant , 1999, Journal of bacteriology.

[129]  P. D. de Boer,et al.  ATP-Dependent Interactions between Escherichia coli Min Proteins and the Phospholipid Membrane In Vitro , 2003, Journal of bacteriology.

[130]  L. Amos,et al.  Bacterial ancestry of actin and tubulin. , 2001, Current opinion in microbiology.

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

[132]  P. Graumann,et al.  Bacillus subtilis actin-like protein MreB influences the positioning of the replication machinery and requires membrane proteins MreC/D and other actin-like proteins for proper localization , 2005, BMC Cell Biology.

[133]  Jan Löwe,et al.  F‐actin‐like filaments formed by plasmid segregation protein ParM , 2002, The EMBO journal.

[134]  R. B. Jensen,et al.  Mechanism of DNA segregation in prokaryotes: ParM partitioning protein of plasmid R1 co‐localizes with its replicon during the cell cycle , 1999, The EMBO journal.

[135]  J. Mingorance,et al.  Concentration and Assembly of the Division Ring Proteins FtsZ, FtsA, and ZipA during the Escherichia coli Cell Cycle , 2003, Journal of bacteriology.

[136]  William Dowhan,et al.  Visualization of Phospholipid Domains inEscherichia coli by Using the Cardiolipin-Specific Fluorescent Dye 10-N-Nonyl Acridine Orange , 2000, Journal of bacteriology.

[137]  J. Lutkenhaus,et al.  A conserved sequence at the C‐terminus of MinD is required for binding to the membrane and targeting MinC to the septum , 2003, Molecular microbiology.

[138]  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.

[139]  M. Goldberg,et al.  Evidence for polar positional information independent of cell division and nucleoid occlusion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[140]  Robert Landick,et al.  RNA Polymerase as a Molecular Motor , 1998, Cell.

[141]  D. H. Snyder,et al.  MICROTUBULES: EVIDENCE FOR 13 PROTOFILAMENTS , 1973, The Journal of cell biology.

[142]  O. Espéli,et al.  A Physical and Functional Interaction between Escherichia coli FtsK and Topoisomerase IV* , 2003, Journal of Biological Chemistry.

[143]  H. Meinhardt,et al.  Pattern formation in Escherichia coli: A model for the pole-to-pole oscillations of Min proteins and the localization of the division site , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[144]  C. Jacobs-Wagner,et al.  The Bacterial Cytoskeleton An Intermediate Filament-Like Function in Cell Shape , 2003, Cell.

[145]  A. Hoffmaster,et al.  Sequence and Organization of pXO1, the Large Bacillus anthracis Plasmid Harboring the Anthrax Toxin Genes , 1999, Journal of bacteriology.

[146]  S. Rowland,et al.  Membrane Redistribution of the Escherichia coli MinD Protein Induced by MinE , 2000, Journal of bacteriology.

[147]  D. Barillà,et al.  Architecture of the ParF•ParG protein complex involved in prokaryotic DNA segregation , 2003, Molecular microbiology.

[148]  J. Lutkenhaus,et al.  Interaction between FtsZ and inhibitors of cell division , 1996, Journal of bacteriology.

[149]  F. Hartl,et al.  Crystal structure of an archaeal actin homolog. , 2006, Journal of molecular biology.

[150]  J. Gober,et al.  The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[151]  R. B. Jensen,et al.  Mechanism of DNA segregation in prokaryotes: replicon pairing by parC of plasmid R1. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[152]  J. Lutkenhaus,et al.  Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. , 2001, Molecular cell.

[153]  J. Errington,et al.  Cytokinesis in Bacteria , 2003, Microbiology and Molecular Biology Reviews.

[154]  G. Rivas,et al.  Visualization of Single Escherichia coli FtsZ Filament Dynamics with Atomic Force Microscopy* , 2005, Journal of Biological Chemistry.

[155]  J. Errington,et al.  Selection of the midcell division site in Bacillus subtilis through MinD‐dependent polar localization and activation of MinC , 1999, Molecular microbiology.

[156]  Y. Brun,et al.  Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. , 1998, Genes & development.

[157]  Ruifeng Yang,et al.  AglZ Is a Filament-Forming Coiled-Coil Protein Required for Adventurous Gliding Motility of Myxococcus xanthus , 2004, Journal of bacteriology.

[158]  D. Wirtz,et al.  The rapid onset of elasticity during the assembly of the bacterial cell-division protein FtsZ. , 2005, Biochemical and biophysical research communications.

[159]  J. Pogliano,et al.  Bacterial DNA segregation by dynamic SopA polymers. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[160]  Jan Löwe,et al.  Prokaryotic origin of the actin cytoskeleton , 2001, Nature.

[161]  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.

[162]  A. Grossman,et al.  The chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillus subtilis , 2006, Molecular microbiology.

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

[164]  L. Rothfield,et al.  Spatial control of bacterial division-site placement , 2005, Nature Reviews Microbiology.

[165]  P. D. de Boer,et al.  SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. , 2005, Molecular cell.

[166]  P. Coulombe,et al.  Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds , 2004, Nature Cell Biology.

[167]  J. Errington,et al.  A role for division‐site‐selection protein MinD in regulation of internucleoid jumping of Soj (ParA) protein in Bacillus subtilis , 2002, Molecular microbiology.

[168]  O. Massidda,et al.  Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein , 2004, Molecular microbiology.

[169]  G. King,et al.  The MinD Membrane Targeting Sequence Is a Transplantable Lipid-binding Helix* , 2003, Journal of Biological Chemistry.

[170]  D. Barillà,et al.  The bacterial segrosome: a dynamic nucleoprotein machine for DNA trafficking and segregation , 2006, Nature Reviews Microbiology.

[171]  J. Lutkenhaus,et al.  Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[172]  L. Rothfield New Insights into the Developmental History of the Bacterial Cell Division Site , 2003, Journal of bacteriology.

[173]  G. King,et al.  Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[174]  G. Stewart,et al.  The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants , 1992, Journal of bacteriology.

[175]  Cassie Aldridge,et al.  The molecular biology of plastid division in higher plants. , 2005, Journal of experimental botany.

[176]  J. Löwe,et al.  Crystal structure of the bacterial cell division regulator MinD , 2001, FEBS letters.

[177]  Y. Brun,et al.  Cell cycle regulation and cell type-specific localization of the FtsZ division initiation protein in Caulobacter. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[178]  J. Errington,et al.  Control of Cell Morphogenesis in Bacteria Two Distinct Ways to Make a Rod-Shaped Cell , 2003, Cell.

[179]  R. B. Jensen,et al.  Prokaryotic DNA segregation by an actin‐like filament , 2002, The EMBO journal.

[180]  Jan Löwe,et al.  Structural insights into FtsZ protofilament formation , 2004, Nature Structural &Molecular Biology.

[181]  D. Williams,et al.  The structure and mode of action of glycopeptide antibiotics of the vancomycin group. , 1984, Annual review of microbiology.

[182]  J. Hurley,et al.  Endocytosis Driving Membranes around the Bend , 2002, Cell.

[183]  Ram Samudrala,et al.  Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[184]  Grant J. Jensen,et al.  Magnetosomes Are Cell Membrane Invaginations Organized by the Actin-Like Protein MamK , 2006, Science.

[185]  J. Sawitzke,et al.  Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[186]  J. Errington,et al.  Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. , 1999, Molecular cell.

[187]  J. Lutkenhaus,et al.  Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[188]  Y. Ishii,et al.  Functional dissection of a cell-division inhibitor, SulA, of Escherichia coli and its negative regulation by Lon , 1997, Molecular and General Genetics MGG.

[189]  P. Gómez-Puertas,et al.  Escherichia coli FtsZ polymers contain mostly GTP and have a high nucleotide turnover , 2001, Molecular microbiology.

[190]  J. Errington,et al.  RacA and the Soj‐Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis , 2003, Molecular microbiology.

[191]  G. Stewart,et al.  Bacillus subtilis possesses a second determinant with extensive sequence similarity to the Escherichia coli mreB morphogene , 1995, Journal of bacteriology.

[192]  Yu-Ling Shih,et al.  The MreB and Min cytoskeletal‐like systems play independent roles in prokaryotic polar differentiation , 2005, Molecular microbiology.

[193]  J. Davies,et al.  Molecular Biology of the Cell , 1983, Bristol Medico-Chirurgical Journal.

[194]  K. Morikawa,et al.  Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus , 2001, The EMBO journal.

[195]  J. Lutkenhaus,et al.  The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli , 1992, Journal of bacteriology.

[196]  E. Nogales,et al.  Tubulin and FtsZ form a distinct family of GTPases , 1998, Nature Structural Biology.

[197]  Y. Okada,et al.  New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells , 1989, Journal of bacteriology.

[198]  T. Ogura,et al.  Positioning of replicated chromosomes in Escherichia coli , 1990, Journal of bacteriology.

[199]  Zemer Gitai,et al.  An actin-like gene can determine cell polarity in bacteria. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[200]  T. Kruse,et al.  Dysfunctional MreB inhibits chromosome segregation in Escherichia coli , 2003, The EMBO journal.

[201]  Brian T Helfand,et al.  Intermediate filaments are dynamic and motile elements of cellular architecture , 2004, Journal of Cell Science.

[202]  Jan Löwe,et al.  Structure of bacterial tubulin BtubA/B: evidence for horizontal gene transfer. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[203]  U. Schwarz,et al.  Autolytic enzymes and cell division of Escherichia coli. , 1969, Journal of molecular biology.

[204]  Daniel P. Haeusser,et al.  EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ , 2004, Molecular microbiology.

[205]  J. Errington,et al.  Roles for MreC and MreD proteins in helical growth of the cylindrical cell wall in Bacillus subtilis , 2005, Molecular microbiology.

[206]  P A de Boer,et al.  Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[207]  S. Trachtenberg,et al.  A bacterial linear motor: cellular and molecular organization of the contractile cytoskeleton of the helical bacterium Spiroplasma melliferum BC3 , 2001, Molecular microbiology.

[208]  R. Losick,et al.  Identification of Bacillus subtilis genes for septum placement and shape determination , 1992, Journal of bacteriology.

[209]  W. Margolin Bacterial Mitosis: Actin in a New Role at the Origin , 2005, Current Biology.

[210]  S. Khan,et al.  A Novel FtsZ-Like Protein Is Involved in Replication of the Anthrax Toxin-Encoding pXO1 Plasmid in Bacillus anthracis , 2006, Journal of bacteriology.

[211]  Thomas Kruse,et al.  The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane‐bound complex , 2004, Molecular microbiology.

[212]  B. Spratt,et al.  Identification of the rodA gene product of Escherichia coli , 1983, Journal of bacteriology.

[213]  J. Errington,et al.  Control of Cell Shape in Bacteria Helical, Actin-like Filaments in Bacillus subtilis , 2001, Cell.

[214]  Peter Roepstorff,et al.  Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. , 2003, Molecular cell.

[215]  Zemer Gitai,et al.  The New Bacterial Cell Biology: Moving Parts and Subcellular Architecture , 2005, Cell.

[216]  M. Mann,et al.  Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. , 2006, Genes & development.

[217]  Jan Kok,et al.  Subcellular sites for bacterial protein export , 2004, Molecular microbiology.

[218]  P. Lenzi,et al.  ‘Epixenosomes’: Peculiar epibionts of the protozoon ciliate Euplotidium itoi: Do their cytoplasmic tubules consist of tubulin? , 1993 .

[219]  J. Errington,et al.  Several distinct localization patterns for penicillin‐binding proteins in Bacillus subtilis , 2003, Molecular microbiology.

[220]  M. de Pedro,et al.  Murein segregation in Escherichia coli , 1997, Journal of bacteriology.

[221]  Jeff Errington,et al.  The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. , 2003, Developmental cell.

[222]  Karsten Kruse,et al.  A dynamic model for determining the middle of Escherichia coli. , 2002, Biophysical journal.

[223]  J. Lutkenhaus,et al.  The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[224]  K. Gerdes,et al.  Plasmid segregation mechanisms. , 2005, Annual review of genetics.

[225]  S. Almo,et al.  The structure of nonvertebrate actin: Implications for the ATP hydrolytic mechanism , 2003, Proceedings of the National Academy of Sciences of the United States of America.