MinDE-Dependent Pole-to-Pole Oscillation of Division Inhibitor MinC in Escherichia coli

ABSTRACT By inhibiting FtsZ ring formation near the cell ends, the MinC protein plays a critical role in proper positioning of the division apparatus in Escherichia coli. MinC activity requires that of MinD, and the MinE peptide provides topological specificity by suppressing MinC-MinD-mediated division inhibition specifically at the middle of the cell. We recently presented evidence that MinE not only accumulates in an FtsZ-independent ring structure at the cell’s middle but also imposes a unique dynamic localization pattern upon MinD in which the latter accumulates alternately in either one of the cell halves in what appears to be a rapidly oscillating membrane association-dissociation cycle. Here we show that functional green fluorescent protein-MinC displays a very similar oscillatory behavior which is dependent on both MinD and MinE and independent of FtsZ. The results support a model in which MinD recruits MinC to its site of action and in which FtsZ ring assembly at each of the cell ends is blocked in an intermittent and alternate fashion.

[1]  E. Boye,et al.  Rule governing the division pattern in Escherichia coli minB and wild-type filaments , 1990, Journal of bacteriology.

[2]  P. D. de Boer,et al.  Central role for the Escherichia coli minC gene product in two different cell division-inhibition systems. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[3]  W. Cook,et al.  Nucleoid-Independent Identification of Cell Division Sites in Escherichia coli , 1999, Journal of bacteriology.

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

[5]  L. Rothfield,et al.  A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli , 1989, Cell.

[6]  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.

[7]  P. D. de Boer,et al.  Proper placement of the Escherichia coli division site requires two functions that are associated with different domains of the MinE protein. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[8]  C. Woldringh,et al.  Actively replicating nucleoids influence positioning of division sites in Escherichia coli filaments forming cells lacking DNA , 1989, Journal of bacteriology.

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

[10]  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.

[11]  F. Jacob,et al.  On the process of cellular division in Escherichia coli. I. Asymmetrical cell division and production of deoxyribonucleic acid-less bacteria. , 1968, Journal of molecular biology.

[12]  E. Bi,et al.  Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring , 1993, Journal of bacteriology.

[13]  C. Touriol,et al.  Deletion analysis of gene minE which encodes the topological specificity factor of cell division in Escherichia coli , 1995, Molecular microbiology.

[14]  A. Higashitani,et al.  A cell division inhibitor SulA of Escherichia coli directly interacts with FtsZ through GTP hydrolysis. , 1995, Biochemical and biophysical research communications.

[15]  K. Nordström,et al.  Effects of chromosome underreplication on cell division in Escherichia coli. , 1998, Journal of bacteriology.

[16]  J. Lutkenhaus,et al.  Bacterial cell division and the Z ring. , 1997, Annual review of biochemistry.

[17]  Nanne Nanninga,et al.  Morphogenesis of Escherichia coli , 1998, Microbiology and Molecular Biology Reviews.

[18]  W. D. Fisher,et al.  MINIATURE escherichia coli CELLS DEFICIENT IN DNA. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[19]  J. Errington,et al.  Postseptational chromosome partitioning in bacteria. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[20]  W. Donachie,et al.  Quantal Behavior of a Diffusible Factor Which Initiates Septum Formation at Potential Division Sites in Escherichia coli , 1974, Journal of bacteriology.

[21]  K. Nordström,et al.  Cell division in Escherichia coli minB mutants , 1992, Molecular microbiology.

[22]  L. Rothfield,et al.  Bacterial Cell Division: The Cycle of the Ring , 1997, Cell.

[23]  A. Grossman,et al.  Effect of minCD on FtsZ Ring Position and Polar Septation in Bacillus subtilis , 1998, Journal of bacteriology.

[24]  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.

[25]  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.

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

[27]  L. Shapiro,et al.  Bacterial cell division: a moveable feast. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[28]  T. Hill,et al.  sfi-independent filamentation in Escherichia coli Is lexA dependent and requires DNA damage for induction , 1997, Journal of bacteriology.

[29]  N Nanninga,et al.  Role of the nucleoid in the toporegulation of division. , 1990, Research in microbiology.

[30]  W. Donachie,et al.  "Division potential" in Escherichia coli , 1996, Journal of bacteriology.

[31]  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.

[32]  C. Woldringh,et al.  Toporegulation of bacterial division according to the nucleoid occlusion model. , 1991, Research in microbiology.

[33]  P. D. de Boer,et al.  Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli , 1988, Journal of bacteriology.

[34]  W. Margolin,et al.  A green light for the bacterial cytoskeleton. , 1998, Trends in microbiology.

[35]  W. Margolin,et al.  Assembly of the FtsZ ring at the central division site in the absence of the chromosome , 1998, Molecular microbiology.

[36]  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.

[37]  S Falkow,et al.  FACS-optimized mutants of the green fluorescent protein (GFP). , 1996, Gene.

[38]  W. Margolin,et al.  FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization , 1999, Molecular microbiology.

[39]  G. Salmond,et al.  ParD: a new gene coding for a protein required for chromosome partitioning and septum localization in Escherichia coli , 1987, Molecular microbiology.

[40]  L. Rothfield,et al.  The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. , 1991, The EMBO journal.