Literature DB >> 20023035

MreB drives de novo rod morphogenesis in Caulobacter crescentus via remodeling of the cell wall.

Constantin N Takacs1, Sebastian Poggio, Godefroid Charbon, Mathieu Pucheault, Waldemar Vollmer, Christine Jacobs-Wagner.   

Abstract

MreB, the bacterial actin-like cytoskeleton, is required for the rod morphology of many bacterial species. Disruption of MreB function results in loss of rod morphology and cell rounding. Here, we show that the widely used MreB inhibitor A22 causes MreB-independent growth inhibition that varies with the drug concentration, culture medium conditions, and bacterial species tested. MP265, an A22 structural analog, is less toxic than A22 for growth yet equally efficient for disrupting the MreB cytoskeleton. The action of A22 and MP265 is enhanced by basic pH of the culture medium. Using this knowledge and the rapid reversibility of drug action, we examined the restoration of rod shape in lemon-shaped Caulobacter crescentus cells pretreated with MP265 or A22 under nontoxic conditions. We found that reversible restoration of MreB function after drug removal causes extensive morphological changes including a remarkable cell thinning accompanied with elongation, cell branching, and shedding of outer membrane vesicles. We also thoroughly characterized the composition of C. crescentus peptidoglycan by high-performance liquid chromatography and mass spectrometry and showed that MreB disruption and recovery of rod shape following restoration of MreB function are accompanied by considerable changes in composition. Our results provide insight into MreB function in peptidoglycan remodeling and rod shape morphogenesis and suggest that MreB promotes the transglycosylase activity of penicillin-binding proteins.

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Year:  2009        PMID: 20023035      PMCID: PMC2832515          DOI: 10.1128/JB.01311-09

Source DB:  PubMed          Journal:  J Bacteriol        ISSN: 0021-9193            Impact factor:   3.490


  66 in total

Review 1.  Morphogenesis of rod-shaped sacculi.

Authors:  Tanneke den Blaauwen; Miguel A de Pedro; Martine Nguyen-Distèche; Juan A Ayala
Journal:  FEMS Microbiol Rev       Date:  2008-03       Impact factor: 16.408

Review 2.  Peptidoglycan structure and architecture.

Authors:  Waldemar Vollmer; Didier Blanot; Miguel A de Pedro
Journal:  FEMS Microbiol Rev       Date:  2008-01-08       Impact factor: 16.408

3.  Identification of the L,D-transpeptidases for peptidoglycan cross-linking in Escherichia coli.

Authors:  Sophie Magnet; Lionel Dubost; Arul Marie; Michel Arthur; Laurent Gutmann
Journal:  J Bacteriol       Date:  2008-05-02       Impact factor: 3.490

4.  Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli.

Authors:  Felipe O Bendezú; Piet A J de Boer
Journal:  J Bacteriol       Date:  2007-11-09       Impact factor: 3.490

5.  Identification of the binding of sceptrin to MreB via a bidirectional affinity protocol.

Authors:  Abimael D Rodríguez; Martin J Lear; James J La Clair
Journal:  J Am Chem Soc       Date:  2008-05-14       Impact factor: 15.419

6.  Anti-infectious effect of S-benzylisothiourea compound A22, which inhibits the actin-like protein, MreB, in Shigella flexneri.

Authors:  Norihisa Noguchi; Keita Yanagimoto; Hidemasa Nakaminami; Moeru Wakabayashi; Noritaka Iwai; Masaaki Wachi; Masanori Sasatsu
Journal:  Biol Pharm Bull       Date:  2008-07       Impact factor: 2.233

Review 7.  Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli.

Authors:  Waldemar Vollmer; Ute Bertsche
Journal:  Biochim Biophys Acta       Date:  2007-06-16

8.  Growth of Escherichia coli: significance of peptidoglycan degradation during elongation and septation.

Authors:  Tsuyoshi Uehara; James T Park
Journal:  J Bacteriol       Date:  2008-04-04       Impact factor: 3.490

Review 9.  The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis.

Authors:  Eric Sauvage; Frédéric Kerff; Mohammed Terrak; Juan A Ayala; Paulette Charlier
Journal:  FEMS Microbiol Rev       Date:  2008-02-11       Impact factor: 16.408

10.  A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus.

Authors:  Martin Thanbichler; Antonio A Iniesta; Lucy Shapiro
Journal:  Nucleic Acids Res       Date:  2007-10-24       Impact factor: 16.971

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  64 in total

Review 1.  Physics of bacterial morphogenesis.

Authors:  Sean X Sun; Hongyuan Jiang
Journal:  Microbiol Mol Biol Rev       Date:  2011-12       Impact factor: 11.056

2.  Polar growth in the Alphaproteobacterial order Rhizobiales.

Authors:  Pamela J B Brown; Miguel A de Pedro; David T Kysela; Charles Van der Henst; Jinwoo Kim; Xavier De Bolle; Clay Fuqua; Yves V Brun
Journal:  Proc Natl Acad Sci U S A       Date:  2012-01-17       Impact factor: 11.205

Review 3.  The structure and function of bacterial actin homologs.

Authors:  Joshua W Shaevitz; Zemer Gitai
Journal:  Cold Spring Harb Perspect Biol       Date:  2010-07-14       Impact factor: 10.005

4.  Mechanical control of bacterial cell shape.

Authors:  Hongyuan Jiang; Fangwei Si; William Margolin; Sean X Sun
Journal:  Biophys J       Date:  2011-07-20       Impact factor: 4.033

5.  Coarse-grained simulations of bacterial cell wall growth reveal that local coordination alone can be sufficient to maintain rod shape.

Authors:  Lam T Nguyen; James C Gumbart; Morgan Beeby; Grant J Jensen
Journal:  Proc Natl Acad Sci U S A       Date:  2015-06-30       Impact factor: 11.205

Review 6.  Polar localization of MreB actin is inhibited by anionic phospholipids in the rod-shaped bacterium Escherichia coli.

Authors:  Daisuke Shiomi
Journal:  Curr Genet       Date:  2017-04-24       Impact factor: 3.886

Review 7.  Cytoskeletal Proteins in Caulobacter crescentus: Spatial Orchestrators of Cell Cycle Progression, Development, and Cell Shape.

Authors:  Kousik Sundararajan; Erin D Goley
Journal:  Subcell Biochem       Date:  2017

8.  A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole.

Authors:  Yoshiharu Yamaichi; Raphael Bruckner; Simon Ringgaard; Andrea Möll; D Ewen Cameron; Ariane Briegel; Grant J Jensen; Brigid M Davis; Matthew K Waldor
Journal:  Genes Dev       Date:  2012-10-15       Impact factor: 11.361

Review 9.  Modes of cell wall growth differentiation in rod-shaped bacteria.

Authors:  Felipe Cava; Erkin Kuru; Yves V Brun; Miguel A de Pedro
Journal:  Curr Opin Microbiol       Date:  2013-10-01       Impact factor: 7.934

10.  De novo morphogenesis in L-forms via geometric control of cell growth.

Authors:  Gabriel Billings; Nikolay Ouzounov; Tristan Ursell; Samantha M Desmarais; Joshua Shaevitz; Zemer Gitai; Kerwyn Casey Huang
Journal:  Mol Microbiol       Date:  2014-07-23       Impact factor: 3.501

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