Literature DB >> 9512521

Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter.

A J Kelly1, M J Sackett, N Din, E Quardokus, Y V Brun.   

Abstract

In the differentiating bacterium Caulobacter crescentus, the cell division initiation protein FtsZ is present in only one of the two cell types. Stalked cells initiate a new round of DNA replication immediately after cell division and contain FtsZ, whereas the progeny swarmer cells are unable to initiate DNA replication and do not contain FtsZ. We show that FtsZ expression is controlled by cell cycle-dependent transcription and proteolysis. Transcription of ftsZ is repressed in swarmer cells and is activated concurrently with the initiation of DNA replication. At the end of the DNA replication period, transcription of ftsZ decreases substantially. We show that the global cell cycle regulator CtrA is involved in the cell cycle control of ftsZ transcription. CtrA binds to a site that overlaps the ftsZ transcription start site. Removal of the CtrA-binding site results in transcription of the ftsZ promoter in swarmer cells. Decreasing the cellular concentration of CtrA increases ftsZ transcription and conversely, increasing the concentration of CtrA decreases ftsZ transcription. Because CtrA is present in swarmer cells, is degraded at the same time as ftsZ transcription begins, and reappears when ftsZ transcription decreases at the end of the cell cycle, we propose that CtrA is a repressor of ftsZ transcription. We show that proteolysis is an important determinant of cell type-specific distribution and cell cycle variation of FtsZ. FtsZ is stable when it is synthesized and assembles into the cytokinetic ring at the beginning of the cell cycle. After the initiation of cell division, the rate of FtsZ degradation increases as both the constriction site and the FtsZ ring decrease in diameter. When ftsZ is expressed constitutively from inducible promoters, the abundance of FtsZ still varies during the cell cycle. The coupling of transcription and proteolysis to cell division ensures that FtsZ is inherited only by the progeny cell that will begin DNA replication immediately after cell division.

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Year:  1998        PMID: 9512521      PMCID: PMC316630          DOI: 10.1101/gad.12.6.880

Source DB:  PubMed          Journal:  Genes Dev        ISSN: 0890-9369            Impact factor:   11.361


  61 in total

1.  A temporally controlled sigma-factor is required for polar morphogenesis and normal cell division in Caulobacter.

Authors:  Y V Brun; L Shapiro
Journal:  Genes Dev       Date:  1992-12       Impact factor: 11.361

Review 2.  Bacterial cell division: the cycle of the ring.

Authors:  L I Rothfield; S S Justice
Journal:  Cell       Date:  1997-03-07       Impact factor: 41.582

3.  Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells.

Authors:  M Evinger; N Agabian
Journal:  J Bacteriol       Date:  1977-10       Impact factor: 3.490

4.  Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis.

Authors:  M R Alley; J R Maddock; L Shapiro
Journal:  Science       Date:  1993-03-19       Impact factor: 47.728

5.  Polar location of the chemoreceptor complex in the Escherichia coli cell.

Authors:  J R Maddock; L Shapiro
Journal:  Science       Date:  1993-03-19       Impact factor: 47.728

6.  Localization of surface structures during procaryotic differentiation: role of cell division in Caulobacter crescentus.

Authors:  E D Huguenel; A Newton
Journal:  Differentiation       Date:  1982       Impact factor: 3.880

7.  Isolation of spontaneously derived mutants of Caulobacter crescentus.

Authors:  R C Johnson; B Ely
Journal:  Genetics       Date:  1977-05       Impact factor: 4.562

Review 8.  The cell cycle of Escherichia coli.

Authors:  W D Donachie
Journal:  Annu Rev Microbiol       Date:  1993       Impact factor: 15.500

9.  A Caulobacter DNA methyltransferase that functions only in the predivisional cell.

Authors:  G Zweiger; G Marczynski; L Shapiro
Journal:  J Mol Biol       Date:  1994-01-14       Impact factor: 5.469

10.  Transcription of ftsZ oscillates during the cell cycle of Escherichia coli.

Authors:  T Garrido; M Sánchez; P Palacios; M Aldea; M Vicente
Journal:  EMBO J       Date:  1993-10       Impact factor: 11.598

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  89 in total

Review 1.  Bacterial DNA methylation: a cell cycle regulator?

Authors:  A Reisenauer; L S Kahng; S McCollum; L Shapiro
Journal:  J Bacteriol       Date:  1999-09       Impact factor: 3.490

2.  Developmental regulation of the cell division protein FtsZ in Anabaena sp. strain PCC 7120, a cyanobacterium capable of terminal differentiation.

Authors:  I Kuhn; L Peng; S Bedu; C C Zhang
Journal:  J Bacteriol       Date:  2000-08       Impact factor: 3.490

3.  Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle.

Authors:  Michael T Laub; Swaine L Chen; Lucy Shapiro; Harley H McAdams
Journal:  Proc Natl Acad Sci U S A       Date:  2002-04-02       Impact factor: 11.205

Review 4.  Cytokinesis in prokaryotes and eukaryotes: common principles and different solutions.

Authors:  N Nanninga
Journal:  Microbiol Mol Biol Rev       Date:  2001-06       Impact factor: 11.056

5.  CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus.

Authors:  M Wortinger; M J Sackett; Y V Brun
Journal:  EMBO J       Date:  2000-09-01       Impact factor: 11.598

6.  Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle.

Authors:  C Jacobs; D Hung; L Shapiro
Journal:  Proc Natl Acad Sci U S A       Date:  2001-03-13       Impact factor: 11.205

7.  DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter.

Authors:  Ann Reisenauer; Lucy Shapiro
Journal:  EMBO J       Date:  2002-09-16       Impact factor: 11.598

8.  Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins.

Authors:  Whitman B Schofield; Hoong Chuin Lim; Christine Jacobs-Wagner
Journal:  EMBO J       Date:  2010-08-27       Impact factor: 11.598

9.  Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus.

Authors:  A S Lang; J T Beatty
Journal:  Proc Natl Acad Sci U S A       Date:  2000-01-18       Impact factor: 11.205

10.  Mycobacterium tuberculosis ftsZ expression and minimal promoter activity.

Authors:  Manjot Kiran; Erin Maloney; Hava Lofton; Ashwini Chauhan; Rasmus Jensen; Renata Dziedzic; Murty Madiraju; Malini Rajagopalan
Journal:  Tuberculosis (Edinb)       Date:  2009-12       Impact factor: 3.131

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