Towards a bottom-up reconstitution of bacterial cell division.

The components of the bacterial division machinery assemble to form a dynamic ring at mid-cell that drives cytokinesis. The nature of most division proteins and their assembly pathway is known. Our knowledge about the biochemical activities and protein interactions of some key division elements, including those responsible for correct ring positioning, has progressed considerably during the past decade. These developments, together with new imaging and membrane reconstitution technologies, have triggered the 'bottom-up' synthetic approach aiming at reconstructing bacterial division in the test tube, which is required to support conclusions derived from cellular and molecular analysis. Here, we describe recent advances in reconstituting Escherichia coli minimal systems able to reproduce essential functions, such as the initial steps of division (proto-ring assembly) and one of the main positioning mechanisms (Min oscillating system), and discuss future perspectives and experimental challenges.

[1]  Manouk Abkarian,et al.  Continuous droplet interface crossing encapsulation (cDICE) for high throughput monodisperse vesicle design , 2011 .

[2]  W. Margolin,et al.  Mutual effects of MinD-membrane interaction: I. Changes in the membrane properties induced by MinD binding. , 2008, Biochimica et biophysica acta.

[3]  L. Hamoen,et al.  Membrane potential is important for bacterial cell division , 2010, Proceedings of the National Academy of Sciences.

[4]  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.

[5]  Petra Schwille,et al.  Protein self-organization: lessons from the min system. , 2011, Annual review of biophysics.

[6]  P. Janmey,et al.  Biophysical properties of lipids and dynamic membranes. , 2006, Trends in cell biology.

[7]  G. Rivas,et al.  Reconstitution and Organization of Escherichia coli Proto-ring Elements (FtsZ and FtsA) inside Giant Unilamellar Vesicles Obtained from Bacterial Inner Membranes* , 2011, The Journal of Biological Chemistry.

[8]  B. Alberts A Grand Challenge in Biology , 2011, Science.

[9]  Miguel Vicente,et al.  Septum Enlightenment: Assembly of Bacterial Division Proteins , 2006, Journal of bacteriology.

[10]  G. Rivas,et al.  FtsZ polymers bound to lipid bilayers through ZipA form dynamic two dimensional networks. , 2012, Biochimica et biophysica acta.

[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]  Petra Schwille,et al.  Fluorescence correlation spectroscopy for the study of membrane dynamics and organization in giant unilamellar vesicles. , 2010, Methods in molecular biology.

[13]  P. Schwille,et al.  Surface analysis of membrane dynamics. , 2010, Biochimica et biophysica acta.

[14]  P. Tarazona,et al.  Depolymerization dynamics of individual filaments of bacterial cytoskeletal protein FtsZ , 2012, Proceedings of the National Academy of Sciences.

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

[16]  Adam J. Trexler,et al.  Single-molecule fluorescence spectroscopy using phospholipid bilayer nanodiscs. , 2010, Methods in enzymology.

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

[18]  Tiffany Lin,et al.  Direct MinE–membrane interaction contributes to the proper localization of MinDE in E. coli , 2009, Molecular microbiology.

[19]  W. Dowhan,et al.  Role of membrane lipids in bacterial division-site selection. , 2005, Current opinion in microbiology.

[20]  D. Raskin,et al.  The MinE Ring: An FtsZ-Independent Cell Structure Required for Selection of the Correct Division Site in E. coli , 1997, Cell.

[21]  Harold P. Erickson,et al.  Reconstitution of Contractile FtsZ Rings in Liposomes , 2008, Science.

[22]  L. Liz‐Marzán,et al.  Surface-Enhanced Raman scattering-based detection of the interactions between the essential cell division FtsZ protein and bacterial membrane elements. , 2012, ACS nano.

[23]  K. Yoshikawa,et al.  Cooperation between giant DNA molecules and actin filaments in a microsphere. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  G. Rivas,et al.  Isolation, Characterization and Lipid-Binding Properties of the Recalcitrant FtsA Division Protein from Escherichia coli , 2012, PloS one.

[25]  H. Erickson,et al.  Inside‐out Z rings – constriction with and without GTP hydrolysis , 2011, Molecular microbiology.

[26]  Vincent Noireaux,et al.  Development of an artificial cell, from self-organization to computation and self-reproduction , 2011 .

[27]  Karsten Kruse,et al.  Min-oscillations in Escherichia coli induced by interactions of membrane-bound proteins , 2005, Physical biology.

[28]  S. Sligar,et al.  Chapter 11 - Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. , 2009, Methods in enzymology.

[29]  Maïté Marguet,et al.  Polymersomes in "gelly" polymersomes: toward structural cell mimicry. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[30]  M. Elowitz,et al.  Synthetic Biology: Integrated Gene Circuits , 2011, Science.

[31]  C. Keating,et al.  Dynamic microcompartmentation in synthetic cells , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Pasquale Stano,et al.  Approaches to chemical synthetic biology , 2012, FEBS letters.

[33]  W. Margolin,et al.  The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. , 2007, Microbiology.

[34]  G. Rivas,et al.  Essential Cell Division Protein FtsZ Assembles into One Monomer-thick Ribbons under Conditions Resembling the Crowded Intracellular Environment* , 2003, Journal of Biological Chemistry.

[35]  Ned S. Wingreen,et al.  A Curvature-Mediated Mechanism for Localization of Lipids to Bacterial Poles , 2006, PLoS Comput. Biol..

[36]  G. Rivas,et al.  Lipid domains and mechanical plasticity of Escherichia coli lipid monolayers. , 2010, Chemistry and physics of lipids.

[37]  M. Record,et al.  Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments. , 1998, Trends in biochemical sciences.

[38]  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.

[39]  Antoine Danchin,et al.  Synthetic biology: discovering new worlds and new words , 2008, EMBO reports.

[40]  P. Devaux,et al.  Specificity of lipid-protein interactions as determined by spectroscopic techniques. , 1985, Biochimica et biophysica acta.

[41]  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.

[42]  Andreas Henkel,et al.  Single unlabeled protein detection on individual plasmonic nanoparticles. , 2012, Nano letters.

[43]  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.

[44]  P. Schwille,et al.  Spatial Regulators for Bacterial Cell Division Self-Organize into Surface Waves in Vitro , 2008, Science.

[45]  Petra Schwille,et al.  Synthetic biology of minimal systems , 2009, Critical reviews in biochemistry and molecular biology.

[46]  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.

[47]  Wei Wu,et al.  The Min Oscillator Uses MinD-Dependent Conformational Changes in MinE to Spatially Regulate Cytokinesis , 2011, Cell.

[48]  P. D. de Boer,et al.  ZipA Is Required for Recruitment of FtsK, FtsQ, FtsL, and FtsN to the Septal Ring in Escherichia coli , 2002, Journal of bacteriology.

[49]  H. Erickson,et al.  The straight and curved conformation of FtsZ protofilaments-evidence for rapid exchange of GTP into the curved protofilament. , 1999, Cell structure and function.

[50]  P. Schwille,et al.  Geometry sensing by self-organized protein patterns , 2012, Proceedings of the National Academy of Sciences.

[51]  P. Schwille,et al.  Protein–membrane interactions: the virtue of minimal systems in systems biology , 2011, Wiley interdisciplinary reviews. Systems biology and medicine.

[52]  P. Schwille,et al.  Minimal systems to study membrane-cytoskeleton interactions. , 2012, Current opinion in biotechnology.

[53]  Jeff Errington,et al.  Bacterial cell division: assembly, maintenance and disassembly of the Z ring , 2009, Nature Reviews Microbiology.

[54]  P. D. de Boer,et al.  Structural Evidence that the P/Q Domain of ZipA Is an Unstructured, Flexible Tether between the Membrane and the C-Terminal FtsZ-Binding Domain , 2002, Journal of bacteriology.

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

[56]  Daniel A. Fletcher,et al.  Biology under construction: in vitro reconstitution of cellular function , 2009, Nature Reviews Molecular Cell Biology.

[57]  Priscilla E. M. Purnick,et al.  The second wave of synthetic biology: from modules to systems , 2009, Nature Reviews Molecular Cell Biology.

[58]  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.

[59]  Huan‐Xiang Zhou,et al.  Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. , 2008, Annual review of biophysics.

[60]  H. Erickson,et al.  Curved FtsZ protofilaments generate bending forces on liposome membranes , 2009, The EMBO journal.

[61]  Françoise Brochard-Wyart,et al.  Inkjet formation of unilamellar lipid vesicles for cell-like encapsulation. , 2009, Lab on a chip.

[62]  Michio Homma,et al.  Transformation of ActoHMM Assembly Confined in Cell-Sized Liposome , 2011, Langmuir : the ACS journal of surfaces and colloids.

[63]  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.

[64]  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.

[65]  P. Schwille,et al.  Biomimetic membrane systems to study cellular organization. , 2009, Journal of structural biology.

[66]  J. Lutkenhaus Min oscillation in bacteria. , 2008, Advances in experimental medicine and biology.

[67]  G. Rivas,et al.  Dynamic Interaction of the Escherichia coli Cell Division ZipA and FtsZ Proteins Evidenced in Nanodiscs* , 2012, The Journal of Biological Chemistry.

[68]  Andrew D Rutenberg,et al.  Self-organization of the MinE protein ring in subcellular Min oscillations. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[69]  Vincent Noireaux,et al.  Assembly of MreB filaments on liposome membranes: a synthetic biology approach. , 2012, ACS synthetic biology.

[70]  G. Rivas,et al.  Active membrane viscoelasticity by the bacterial FtsZ-division protein. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[71]  Judith Herzfeld,et al.  Life in a crowded world , 2004, EMBO reports.

[72]  D. Brooks,et al.  Phase separation in cytoplasm, due to macromolecular crowding, is the basis for microcompartmentation , 1995, FEBS letters.

[73]  Damien Larivière,et al.  An inventory of the bacterial macromolecular components and their spatial organization. , 2011, FEMS microbiology reviews.

[74]  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.

[75]  J. Errington,et al.  Crucial role for membrane fluidity in proliferation of primitive cells. , 2012, Cell reports.

[76]  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.

[77]  S. Zimmerman,et al.  Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. , 1991, Journal of molecular biology.

[78]  M. Vicente,et al.  The order of the ring: assembly of Escherichia coli cell division components , 2006, Molecular microbiology.

[79]  D. Endy Foundations for engineering biology , 2005, Nature.

[80]  Ji Yu,et al.  The dynamic nature of the bacterial cytoskeleton , 2009, Cellular and Molecular Life Sciences.

[81]  S. Eom,et al.  Crystal structure of Helicobacter pylori MinE, a cell division topological specificity factor , 2010, Molecular microbiology.

[82]  Sean X. Sun,et al.  MinC Spatially Controls Bacterial Cytokinesis by Antagonizing the Scaffolding Function of FtsZ , 2008, Current Biology.

[83]  G. Rivas,et al.  Independence between GTPase active sites in the Escherichia coli cell division protein FtsZ , 2011, FEBS letters.

[84]  Nicole Liska,et al.  Forming giant vesicles with controlled membrane composition, asymmetry, and contents , 2011, Proceedings of the National Academy of Sciences.

[85]  Miguel Vicente,et al.  Strong FtsZ is with the force: mechanisms to constrict bacteria. , 2010, Trends in microbiology.

[86]  Andreas Janshoff,et al.  Protein-membrane interaction probed by single plasmonic nanoparticles. , 2008, Nano letters.

[87]  Eugenia Mileykovskaya,et al.  A hypothesis to explain division site selection in Escherichia coli by combining nucleoid occlusion and Min , 2004, FEBS letters.

[88]  H. Erickson Modeling the physics of FtsZ assembly and force generation , 2009, Proceedings of the National Academy of Sciences.

[89]  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.

[90]  J. Errington,et al.  Nucleoid occlusion and bacterial cell division , 2011, Nature Reviews Microbiology.

[91]  G. King,et al.  The Dimerization Function of MinC Resides in a Structurally Autonomous C-Terminal Domain , 2001, Journal of bacteriology.

[92]  Olivier Jacquet,et al.  Cover Picture: A Diagonal Approach to Chemical Recycling of Carbon Dioxide: Organocatalytic Transformation for the Reductive Functionalization of CO2 (Angew. Chem. Int. Ed. 1/2012) , 2012 .

[93]  G. Jensen,et al.  The structure of FtsZ filaments in vivo suggests a force‐generating role in cell division , 2007, The EMBO journal.

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

[95]  Pasquale Stano,et al.  The Minimal Size of Liposome‐Based Model Cells Brings about a Remarkably Enhanced Entrapment and Protein Synthesis , 2009, Chembiochem : a European journal of chemical biology.

[96]  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.

[97]  J. Errington,et al.  Life without a wall or division machine in Bacillus subtilis , 2009, Nature.

[98]  P. Schwille,et al.  Surface topology engineering of membranes for the mechanical investigation of the tubulin homologue FtsZ. , 2012, Angewandte Chemie.

[99]  M. Casanova,et al.  Role of Escherichia coli FtsN protein in the assembly and stability of the cell division ring , 2010, Molecular microbiology.