Regulatory Circuitry of the CsrA/CsrB and BarA/UvrY Systems of Escherichia coli

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Published inJournal of Bacteriology Vol. 184; no. 18; pp. 5130 - 5140
Main Authors Suzuki, Kazushi, Wang, Xin, Weilbacher, Thomas, Pernestig, Anna-Karin, Melefors, Ojar, Georgellis, Dimitris, Babitzke, Paul, Romeo, Tony
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 01.09.2002
Subjects
Bacteria
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriology
Escherichia coli - genetics
Escherichia coli - growth & development
Escherichia coli - metabolism
Escherichia coli Proteins
Gene Expression Regulation, Bacterial
Gene Regulation
Genetic Complementation Test
Medical sciences
Medicin
Medicin och hälsovetenskap
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mutation
Phosphotransferases
Proteins
Repressor Proteins
Ribonucleic acid
RNA
RNA, Long Noncoding
RNA, Untranslated - genetics
RNA, Untranslated - metabolism
RNA-Binding Proteins - genetics
RNA-Binding Proteins - metabolism
Signal Transduction
Trans-Activators - genetics
Trans-Activators - metabolism
Transcription Factors
Transcription, Genetic
Online AccessGet full text

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Abstract Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue JB About JB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0021-9193 Online ISSN: 1098-5530 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JB .asm.org, visit: JB       
AbstractList The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates central carbon metabolism, activates flagellum biosynthesis and motility, and represses biofilm formation in Escherichia coli. CsrA activity is antagonized by the untranslated RNA CsrB, to which it binds and forms a globular ribonucleoprotein complex. CsrA indirectly activates csrB transcription, in an apparent autoregulatory mechanism. In the present study, we elucidate the intermediate regulatory circuitry of this system. Mutations affecting the BarA/UvrY two-component signal transduction system decreased csrB transcription but did not affect csrA'-'lacZ expression. The uvrY defect was severalfold more severe than that of barA. Both csrA and uvrY were required for optimal barA expression. The latter observation suggests an autoregulatory loop for UvrY. Ectopic expression of uvrY suppressed the csrB-lacZ expression defects caused by uvrY, csrA, or barA mutations; csrA suppressed csrA or barA defects; and barA complemented only the barA mutation. Purified UvrY protein stimulated csrB-lacZ expression approximately sixfold in S-30 transcription-translation reactions, revealing a direct effect of UvrY on csrB transcription. Disruption of sdiA, which encodes a LuxR homologue, decreased the expression of uvrY'-'lacZ and csrB-lacZ fusions but did not affect csrA'-'lacZ. The BarA/UvrY system activated biofilm formation. Ectopic expression of uvrY stimulated biofilm formation by a csrB-null mutant, indicative of a CsrB-independent role for UvrY in biofilm development. Collectively, these results demonstrate that uvrY resides downstream from csrA in a signaling pathway for csrB and that CsrA stimulates UvrY-dependent activation of csrB expression by BarA-dependent and -independent mechanisms.
Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley Reddit StumbleUpon Twitter current issue JB About JB Subscribers Authors Reviewers Advertisers Inquiries from the Press Permissions & Commercial Reprints ASM Journals Public Access Policy JB RSS Feeds 1752 N Street N.W. • Washington DC 20036 202.737.3600 • 202.942.9355 fax • journals@asmusa.org Print ISSN: 0021-9193 Online ISSN: 1098-5530 Copyright © 2014 by the American Society for Microbiology.   For an alternate route to JB .asm.org, visit: JB       
ABSTRACT The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates central carbon metabolism, activates flagellum biosynthesis and motility, and represses biofilm formation in Escherichia coli . CsrA activity is antagonized by the untranslated RNA CsrB, to which it binds and forms a globular ribonucleoprotein complex. CsrA indirectly activates csrB transcription, in an apparent autoregulatory mechanism. In the present study, we elucidate the intermediate regulatory circuitry of this system. Mutations affecting the BarA/UvrY two-component signal transduction system decreased csrB transcription but did not affect csrA ′ - ′ lacZ expression. The uvrY defect was severalfold more severe than that of barA . Both csrA and uvrY were required for optimal barA expression. The latter observation suggests an autoregulatory loop for UvrY. Ectopic expression of uvrY suppressed the csrB-lacZ expression defects caused by uvrY , csrA , or barA mutations; csrA suppressed csrA or barA defects; and barA complemented only the barA mutation. Purified UvrY protein stimulated csrB-lacZ expression approximately sixfold in S-30 transcription-translation reactions, revealing a direct effect of UvrY on csrB transcription. Disruption of sdiA , which encodes a LuxR homologue, decreased the expression of uvrY ′ - ′ lacZ and csrB-lacZ fusions but did not affect csrA ′ - ′ lacZ . The BarA/UvrY system activated biofilm formation. Ectopic expression of uvrY stimulated biofilm formation by a csrB- null mutant, indicative of a CsrB-independent role for UvrY in biofilm development. Collectively, these results demonstrate that uvrY resides downstream from csrA in a signaling pathway for csrB and that CsrA stimulates UvrY-dependent activation of csrB expression by BarA-dependent and -independent mechanisms.
The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates central carbon metabolism, activates flagellum biosynthesis and motility, and represses biofilm formation in Escherichia coli. CsrA activity is antagonized by the untranslated RNA CsrB, to which it binds and forms a globular ribonucleoprotein complex.
The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates central carbon metabolism, activates flagellum biosynthesis and motility, and represses biofilm formation in Escherichia coli . CsrA activity is antagonized by the untranslated RNA CsrB, to which it binds and forms a globular ribonucleoprotein complex. CsrA indirectly activates csrB transcription, in an apparent autoregulatory mechanism. In the present study, we elucidate the intermediate regulatory circuitry of this system. Mutations affecting the BarA/UvrY two-component signal transduction system decreased csrB transcription but did not affect csrA ′ - ′ lacZ expression. The uvrY defect was severalfold more severe than that of barA . Both csrA and uvrY were required for optimal barA expression. The latter observation suggests an autoregulatory loop for UvrY. Ectopic expression of uvrY suppressed the csrB-lacZ expression defects caused by uvrY , csrA , or barA mutations; csrA suppressed csrA or barA defects; and barA complemented only the barA mutation. Purified UvrY protein stimulated csrB-lacZ expression approximately sixfold in S-30 transcription-translation reactions, revealing a direct effect of UvrY on csrB transcription. Disruption of sdiA , which encodes a LuxR homologue, decreased the expression of uvrY ′ - ′ lacZ and csrB-lacZ fusions but did not affect csrA ′ - ′ lacZ . The BarA/UvrY system activated biofilm formation. Ectopic expression of uvrY stimulated biofilm formation by a csrB- null mutant, indicative of a CsrB-independent role for UvrY in biofilm development. Collectively, these results demonstrate that uvrY resides downstream from csrA in a signaling pathway for csrB and that CsrA stimulates UvrY-dependent activation of csrB expression by BarA-dependent and -independent mechanisms.
The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates centralcarbon metabolism, activates flagellum biosynthesis and motility, and represses biofilm formation in Escherichiacoli. CsrA activity is antagonized by the untranslated RNA CsrB, to which it binds and forms a globularribonucleoprotein complex. CsrA indirectly activates csrB transcription, in an apparent autoregulatory mechanism.In the present study, we elucidate the intermediate regulatory circuitry of this system. Mutationsaffecting the BarA/UvrY two-component signal transduction system decreased csrB transcription but did notaffect csrA-lacZ expression. The uvrY defect was severalfold more severe than that of barA. Both csrA and uvrYwere required for optimal barA expression. The latter observation suggests an autoregulatory loop for UvrY.Ectopic expression of uvrY suppressed the csrB-lacZ expression defects caused by uvrY, csrA, or barA mutations;csrA suppressed csrA or barA defects; and barA complemented only the barA mutation. Purified UvrY proteinstimulated csrB-lacZ expression approximately sixfold in S-30 transcription-translation reactions, revealing adirect effect of UvrY on csrB transcription. Disruption of sdiA, which encodes a LuxR homologue, decreased theexpression of uvrY-lacZ and csrB-lacZ fusions but did not affect csrA-lacZ. The BarA/UvrY system activatedbiofilm formation. Ectopic expression of uvrY stimulated biofilm formation by a csrB-null mutant, indicative ofa CsrB-independent role for UvrY in biofilm development. Collectively, these results demonstrate that uvrYresides downstream from csrA in a signaling pathway for csrB and that CsrA stimulates UvrY-dependentactivation of csrB expression by BarA-dependent and -independent mechanisms.
Author Xin Wang
Thomas Weilbacher
Anna-Karin Pernestig
Paul Babitzke
Tony Romeo
Öjar Melefors
Dimitris Georgellis
Kazushi Suzuki
AuthorAffiliation Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322, 1 Microbiology and Tumorbiology Center, Karolinska Institutet, SE-171 77 Stockholm, Sweden, 2 Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico, 3 Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802 4
AuthorAffiliation_xml – name: Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322, 1 Microbiology and Tumorbiology Center, Karolinska Institutet, SE-171 77 Stockholm, Sweden, 2 Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico, 3 Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802 4
Author_xml – sequence: 1
  givenname: Kazushi
  surname: Suzuki
  fullname: Suzuki, Kazushi
  organization: Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322, USA
– sequence: 2
  givenname: Xin
  surname: Wang
  fullname: Wang, Xin
– sequence: 3
  givenname: Thomas
  surname: Weilbacher
  fullname: Weilbacher, Thomas
– sequence: 4
  givenname: Anna-Karin
  surname: Pernestig
  fullname: Pernestig, Anna-Karin
– sequence: 5
  givenname: Ojar
  surname: Melefors
  fullname: Melefors, Ojar
– sequence: 6
  givenname: Dimitris
  surname: Georgellis
  fullname: Georgellis, Dimitris
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  givenname: Paul
  surname: Babitzke
  fullname: Babitzke, Paul
– sequence: 8
  givenname: Tony
  surname: Romeo
  fullname: Romeo, Tony
BackLink https://www.ncbi.nlm.nih.gov/pubmed/12193630$$D View this record in MEDLINE/PubMed
https://urn.kb.se/resolve?urn=urn:nbn:se:his:diva-10417$$DView record from Swedish Publication Index
http://kipublications.ki.se/Default.aspx?queryparsed=id:1950559$$DView record from Swedish Publication Index
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Corresponding author. Mailing address: Department of Microbiology and Immunology, Emory University School of Medicine, 3133 Rollins Research Center, 1510 Clifton Rd. N.E., Atlanta, GA 30322. Phone: (404) 727-5950. Fax: (404) 727-8250. E-mail: romeo@microbio.emory.edu.
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Snippet Article Usage Stats Services JB Citing Articles Google Scholar PubMed Related Content Social Bookmarking CiteULike Delicious Digg Facebook Google+ Mendeley...
The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates central carbon metabolism, activates flagellum biosynthesis and...
ABSTRACT The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates central carbon metabolism, activates flagellum...
The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates centralcarbon metabolism, activates flagellum biosynthesis and...
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StartPage 5130
SubjectTerms Bacteria
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriology
Escherichia coli - genetics
Escherichia coli - growth & development
Escherichia coli - metabolism
Escherichia coli Proteins
Gene Expression Regulation, Bacterial
Gene Regulation
Genetic Complementation Test
Medical sciences
Medicin
Medicin och hälsovetenskap
Membrane Proteins - genetics
Membrane Proteins - metabolism
Mutation
Phosphotransferases
Proteins
Repressor Proteins
Ribonucleic acid
RNA
RNA, Long Noncoding
RNA, Untranslated - genetics
RNA, Untranslated - metabolism
RNA-Binding Proteins - genetics
RNA-Binding Proteins - metabolism
Signal Transduction
Trans-Activators - genetics
Trans-Activators - metabolism
Transcription Factors
Transcription, Genetic
Title Regulatory Circuitry of the CsrA/CsrB and BarA/UvrY Systems of Escherichia coli
URI http://jb.asm.org/content/184/18/5130.abstract
https://www.ncbi.nlm.nih.gov/pubmed/12193630
https://www.proquest.com/docview/227086508
https://search.proquest.com/docview/18576515
https://search.proquest.com/docview/72022316
https://pubmed.ncbi.nlm.nih.gov/PMC135316
https://urn.kb.se/resolve?urn=urn:nbn:se:his:diva-10417
http://kipublications.ki.se/Default.aspx?queryparsed=id:1950559
Volume 184
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