Literature DB >> 21606359

Convergent transcription confers a bistable switch in Enterococcus faecalis conjugation.

Anushree Chatterjee1, Christopher M Johnson, Che-Chi Shu, Yiannis N Kaznessis, Doraiswami Ramkrishna, Gary M Dunny, Wei-Shou Hu.   

Abstract

Convergent gene pairs with head-to-head configurations are widespread in both eukaryotic and prokaryotic genomes and are speculated to be involved in gene regulation. Here we present a unique mechanism of gene regulation due to convergent transcription from the antagonistic prgX/prgQ operon in Enterococcus faecalis controlling conjugative transfer of the antibiotic resistance plasmid pCF10 from donor cells to recipient cells. Using mathematical modeling and experimentation, we demonstrate that convergent transcription in the prgX/prgQ operon endows the system with the properties of a robust genetic switch through premature termination of elongating transcripts due to collisions between RNA polymerases (RNAPs) transcribing from opposite directions and antisense regulation between complementary counter-transcripts. Evidence is provided for the presence of truncated RNAs resulting from convergent transcription from both the promoters that are capable of sense-antisense interactions. A mathematical model predicts that both RNAP collision and antisense regulation are essential for a robust bistable switch behavior in the control of conjugation initiation by prgX/prgQ operons. Moreover, given that convergent transcription is conserved across species, the mechanism of coupling RNAP collision and antisense interaction is likely to have a significant regulatory role in gene expression.

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Year:  2011        PMID: 21606359      PMCID: PMC3111305          DOI: 10.1073/pnas.1101569108

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  40 in total

1.  Cell-associated pheromone peptide (cCF10) production and pheromone inhibition in Enterococcus faecalis.

Authors:  B A Buttaro; M H Antiporta; G M Dunny
Journal:  J Bacteriol       Date:  2000-09       Impact factor: 3.490

2.  Genome-wide analysis of coordinate expression and evolution of human cis-encoded sense-antisense transcripts.

Authors:  Jianjun Chen; Miao Sun; Laurence D Hurst; Gordon G Carmichael; Janet D Rowley
Journal:  Trends Genet       Date:  2005-06       Impact factor: 11.639

3.  Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis.

Authors:  Ke Shi; C Kent Brown; Zu-Yi Gu; Briana K Kozlowicz; Gary M Dunny; Douglas H Ohlendorf; Cathleen A Earhart
Journal:  Proc Natl Acad Sci U S A       Date:  2005-12-08       Impact factor: 11.205

4.  Direct evidence for control of the pheromone-inducible prgQ operon of Enterococcus faecalis plasmid pCF10 by a countertranscript-driven attenuation mechanism.

Authors:  Christopher M Johnson; Dawn A Manias; Heather A H Haemig; Sonia Shokeen; Keith E Weaver; Tina M Henkin; Gary M Dunny
Journal:  J Bacteriol       Date:  2010-01-22       Impact factor: 3.490

5.  Transcriptome complexity in a genome-reduced bacterium.

Authors:  Marc Güell; Vera van Noort; Eva Yus; Wei-Hua Chen; Justine Leigh-Bell; Konstantinos Michalodimitrakis; Takuji Yamada; Manimozhiyan Arumugam; Tobias Doerks; Sebastian Kühner; Michaela Rode; Mikita Suyama; Sabine Schmidt; Anne-Claude Gavin; Peer Bork; Luis Serrano
Journal:  Science       Date:  2009-11-27       Impact factor: 47.728

Review 6.  Tweaking biological switches through a better understanding of bistability behavior.

Authors:  Anushree Chatterjee; Yiannis N Kaznessis; Wei-Shou Hu
Journal:  Curr Opin Biotechnol       Date:  2008-10-01       Impact factor: 9.740

7.  The prgQ gene of the Enterococcus faecalis tetracycline resistance plasmid pCF10 encodes a peptide inhibitor, iCF10.

Authors:  J Nakayama; R E Ruhfel; G M Dunny; A Isogai; A Suzuki
Journal:  J Bacteriol       Date:  1994-12       Impact factor: 3.490

8.  Bistability and switching in the lysis/lysogeny genetic regulatory network of bacteriophage lambda.

Authors:  Tianhai Tian; Kevin Burrage
Journal:  J Theor Biol       Date:  2004-03-21       Impact factor: 2.691

9.  Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation.

Authors:  B A Leonard; A Podbielski; P J Hedberg; G M Dunny
Journal:  Proc Natl Acad Sci U S A       Date:  1996-01-09       Impact factor: 11.205

10.  Collision events between RNA polymerases in convergent transcription studied by atomic force microscopy.

Authors:  Neal Crampton; William A Bonass; Jennifer Kirkham; Claudio Rivetti; Neil H Thomson
Journal:  Nucleic Acids Res       Date:  2006-09-29       Impact factor: 16.971

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  40 in total

1.  In vivo and in vitro analyses of regulation of the pheromone-responsive prgQ promoter by the PrgX pheromone receptor protein.

Authors:  Enrico Caserta; Heather A H Haemig; Dawn A Manias; Jerneja Tomsic; Frank J Grundy; Tina M Henkin; Gary M Dunny
Journal:  J Bacteriol       Date:  2012-04-27       Impact factor: 3.490

Review 2.  Working together for the common good: cell-cell communication in bacteria.

Authors:  Ann M Stevens; Martin Schuster; Kendra P Rumbaugh
Journal:  J Bacteriol       Date:  2012-03-02       Impact factor: 3.490

3.  Effects of endogenous levels of master regulator PrgX and peptide pheromones on inducibility of conjugation in the enterococcal pCF10 system.

Authors:  Rebecca J B Erickson; Dawn A Manias; Wei-Shou Hu; Gary M Dunny
Journal:  Mol Microbiol       Date:  2019-07-18       Impact factor: 3.501

4.  Antagonistic self-sensing and mate-sensing signaling controls antibiotic-resistance transfer.

Authors:  Anushree Chatterjee; Laura C C Cook; Che-Chi Shu; Yuqing Chen; Dawn A Manias; Doraiswami Ramkrishna; Gary M Dunny; Wei-Shou Hu
Journal:  Proc Natl Acad Sci U S A       Date:  2013-04-08       Impact factor: 11.205

Review 5.  Peptide pheromone signaling in Streptococcus and Enterococcus.

Authors:  Laura C Cook; Michael J Federle
Journal:  FEMS Microbiol Rev       Date:  2013-10-31       Impact factor: 16.408

6.  Identification of a conserved branched RNA structure that functions as a factor-independent terminator.

Authors:  Christopher M Johnson; Yuqing Chen; Heejin Lee; Ailong Ke; Keith E Weaver; Gary M Dunny
Journal:  Proc Natl Acad Sci U S A       Date:  2014-02-18       Impact factor: 11.205

Review 7.  Enterococcal Sex Pheromones: Evolutionary Pathways to Complex, Two-Signal Systems.

Authors:  Gary M Dunny; Ronnie Per-Arne Berntsson
Journal:  J Bacteriol       Date:  2016-05-13       Impact factor: 3.490

Review 8.  Mechanistic Features of the Enterococcal pCF10 Sex Pheromone Response and the Biology of Enterococcus faecalis in Its Natural Habitat.

Authors:  Rebecca J Breuer; Helmut Hirt; Gary M Dunny
Journal:  J Bacteriol       Date:  2018-06-25       Impact factor: 3.490

9.  Multiscale Models of Antibiotic Probiotics.

Authors:  Yiannis N Kaznessis
Journal:  Curr Opin Chem Eng       Date:  2014-11-01       Impact factor: 5.163

10.  Antagonistic Donor Density Effect Conserved in Multiple Enterococcal Conjugative Plasmids.

Authors:  Arpan Bandyopadhyay; Sofie O'Brien; Kristi L Frank; Gary M Dunny; Wei-Shou Hu
Journal:  Appl Environ Microbiol       Date:  2016-07-15       Impact factor: 4.792

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