Membrane Binding of MinE Allows for a Comprehensive Description of Min-Protein Pattern Formation

The rod-shaped bacterium Escherichia coli selects the cell center as site of division with the help of the proteins MinC, MinD, and MinE. This protein system collectively oscillates between the two cell poles by alternately binding to the membrane in one of the two cell halves. This dynamic behavior, which emerges from the interaction of the ATPase MinD and its activator MinE on the cell membrane, has become a paradigm for protein self-organization. Recently, it has been found that not only the binding of MinD to the membrane, but also interactions of MinE with the membrane contribute to Min-protein self-organization. Here, we show that by accounting for this finding in a computational model, we can comprehensively describe all observed Min-protein patterns in vivo and in vitro. Furthermore, by varying the system's geometry, our computations predict patterns that have not yet been reported. We confirm these predictions experimentally.

[1]  Victor Sourjik,et al.  Self-organized partitioning of dynamically localized proteins in bacterial cell division , 2011, Molecular systems biology.

[2]  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.

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

[4]  J. Lippincott-Schwartz,et al.  Studying protein dynamics in living cells , 2001, Nature Reviews Molecular Cell Biology.

[5]  Filipe Tostevin,et al.  A stochastic model of Min oscillations in Escherichia coli and Min protein segregation during cell division , 2005, Physical biology.

[6]  B. Matthews,et al.  A structural basis for processivity , 2001, Protein science : a publication of the Protein Society.

[7]  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.

[8]  M. Howard,et al.  Dynamic compartmentalization of bacteria: accurate division in E. coli. , 2001, Physical review letters.

[9]  K. Kruse,et al.  Surface waves of Min-proteins , 2007, Physical biology.

[10]  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.

[11]  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.

[12]  Johan Hattne,et al.  Stochastic reaction-diffusion simulation with MesoRD , 2005, Bioinform..

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

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

[15]  O. Sliusarenko,et al.  High‐throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio‐temporal dynamics , 2011, Molecular microbiology.

[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]  Wei Wu,et al.  Mechanism of the asymmetric activation of the MinD ATPase by MinE , 2012, Molecular microbiology.

[18]  J. Elf,et al.  Spontaneous separation of bi-stable biochemical systems into spatial domains of opposite phases. , 2004, Systems biology.

[19]  Burak Okumus,et al.  Segregation of molecules at cell division reveals native protein localization , 2012, Nature Methods.

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

[21]  Shigeru Kondo,et al.  Reaction-Diffusion Model as a Framework for Understanding Biological Pattern Formation , 2010, Science.

[22]  J. Liao,et al.  The N-Terminal Amphipathic Helix of the Topological Specificity Factor MinE Is Associated with Shaping Membrane Curvature , 2011, PloS one.

[23]  N. Wingreen,et al.  Pattern formation within Escherichia coli: diffusion, membrane attachment, and self-interaction of MinD molecules. , 2004, Physical review letters.

[24]  W. Margolin,et al.  Exploring intracellular space: function of the Min system in round‐shaped Escherichia coli , 2002, The EMBO journal.

[25]  Elisabeth Fischer-Friedrich,et al.  Intra- and intercellular fluctuations in Min-protein dynamics decrease with cell length , 2010, Proceedings of the National Academy of Sciences.

[26]  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.

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

[28]  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.

[29]  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.

[30]  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.

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

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

[33]  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.

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

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

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

[37]  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.

[38]  P. Schwille,et al.  Min protein patterns emerge from rapid rebinding and membrane interaction of MinE , 2011, Nature Structural &Molecular Biology.

[39]  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.

[40]  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.

[41]  Wei Wu,et al.  Determination of the structure of the MinD–ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC , 2011, Molecular microbiology.

[42]  Erwin Frey,et al.  Highly canalized MinD transfer and MinE sequestration explain the origin of robust MinCDE-protein dynamics. , 2012, Cell reports.

[43]  Masaru Tomita,et al.  A new multicompartmental reaction-diffusion modeling method links transient membrane attachment of E. coli MinE to E-ring formation , 2009, Systems and Synthetic Biology.

[44]  Nenad Pavin,et al.  Min-protein oscillations in Escherichia coli with spontaneous formation of two-stranded filaments in a three-dimensional stochastic reaction-diffusion model. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[45]  David Fange,et al.  Noise-Induced Min Phenotypes in E. coli , 2006, PLoS Comput. Biol..

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

[47]  D. Weibel,et al.  MinD and MinE Interact with Anionic Phospholipids and Regulate Division Plane Formation in Escherichia coli* , 2012, The Journal of Biological Chemistry.

[48]  Andrew D. Rutenberg,et al.  Dynamic Compartmentalization of Bacteria , 2001 .

[49]  G. Jensen,et al.  The Helical MreB Cytoskeleton in Escherichia coli MC1000/pLE7 Is an Artifact of the N-Terminal Yellow Fluorescent Protein Tag , 2012, Journal of bacteriology.

[50]  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.

[51]  K. C. Huang,et al.  The Min System as a General Cell Geometry Detection Mechanism: Branch Lengths in Y-Shaped Escherichia coli Cells Affect Min Oscillation Patterns and Division Dynamics , 2008, Journal of bacteriology.

[52]  G. Meacci,et al.  Mobility of Min-proteins in Escherichia coli measured by fluorescence correlation spectroscopy , 2006, Physical biology.

[53]  William Dowhan,et al.  Effects of Phospholipid Composition on MinD-Membrane Interactions in Vitro and in Vivo* , 2003, Journal of Biological Chemistry.

[54]  M. Zheng,et al.  Spatial control of the cell division site by the Min system in Escherichia coli. , 2013, Environmental microbiology.

[55]  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.

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

[57]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.