The Pseudomonas aeruginosa Vfr Regulator Controls Global Virulence Factor Expression through Cyclic AMP-Dependent and -Independent Mechanisms

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Published inJournal of Bacteriology Vol. 192; no. 14; pp. 3553 - 3564
Main Authors Fuchs, Erin L., Brutinel, Evan D., Jones, Adriana K., Fulcher, Nanette B., Urbanowski, Mark L., Yahr, Timothy L., Wolfgang, Matthew C.
Format Journal Article
LanguageEnglish
Published Washington, DC American Society for Microbiology 01.07.2010
American Society for Microbiology (ASM)
Subjects
Amino Acid Sequence
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriology
Base Sequence
Biological and medical sciences
Cyclic AMP - metabolism
Cyclic AMP Receptor Protein - genetics
Cyclic AMP Receptor Protein - metabolism
DNA, Bacterial
Fundamental and applied biological sciences. Psychology
Gene Expression Regulation, Bacterial - physiology
Microbiology
Miscellaneous
Molecular Biology of Pathogens
Molecular Sequence Data
Promoter Regions, Genetic
Protein Binding
Pseudomonas aeruginosa
Pseudomonas aeruginosa - genetics
Pseudomonas aeruginosa - metabolism
Virulence Factors - genetics
Virulence Factors - metabolism
Pseudomonadales
Virulence
Cyclic AMP
Bacteria
Pseudomonadaceae
Pseudomonas aeruginosa
Mechanism
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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 Vfr is a global regulator of virulence factor expression in the human pathogen Pseudomonas aeruginosa. Although indirect evidence suggests that Vfr activity is controlled by cyclic AMP (cAMP), it has been hypothesized that the putative cAMP binding pocket of Vfr may accommodate additional cyclic nucleotides. In this study, we used two different approaches to generate apo-Vfr and examined its ability to bind a representative set of virulence gene promoters in the absence and presence of different allosteric effectors. Of the cyclic nucleotides tested, only cAMP was able to restore DNA binding activity to apo-Vfr. In contrast, cGMP was capable of inhibiting cAMP-Vfr DNA binding. Further, we demonstrate that vfr expression is autoregulated and cAMP dependent and involves Vfr binding to a previously unidentified site within the vfr promoter region. Using a combination of in vitro and in vivo approaches, we show that cAMP is required for Vfr-dependent regulation of a specific subset of virulence genes. In contrast, we discovered that Vfr controls expression of the lasR promoter in a cAMP-independent manner. In summary, our data support a model in which Vfr controls virulence gene expression by distinct (cAMP-dependent and -independent) mechanisms, which may allow P. aeruginosa to fine-tune its virulence program in response to specific host cues or environments.Vfr is a global regulator of virulence factor expression in the human pathogen Pseudomonas aeruginosa. Although indirect evidence suggests that Vfr activity is controlled by cyclic AMP (cAMP), it has been hypothesized that the putative cAMP binding pocket of Vfr may accommodate additional cyclic nucleotides. In this study, we used two different approaches to generate apo-Vfr and examined its ability to bind a representative set of virulence gene promoters in the absence and presence of different allosteric effectors. Of the cyclic nucleotides tested, only cAMP was able to restore DNA binding activity to apo-Vfr. In contrast, cGMP was capable of inhibiting cAMP-Vfr DNA binding. Further, we demonstrate that vfr expression is autoregulated and cAMP dependent and involves Vfr binding to a previously unidentified site within the vfr promoter region. Using a combination of in vitro and in vivo approaches, we show that cAMP is required for Vfr-dependent regulation of a specific subset of virulence genes. In contrast, we discovered that Vfr controls expression of the lasR promoter in a cAMP-independent manner. In summary, our data support a model in which Vfr controls virulence gene expression by distinct (cAMP-dependent and -independent) mechanisms, which may allow P. aeruginosa to fine-tune its virulence program in response to specific host cues or environments.
Vfr is a global regulator of virulence factor expression in the human pathogen Pseudomonas aeruginosa . Although indirect evidence suggests that Vfr activity is controlled by cyclic AMP (cAMP), it has been hypothesized that the putative cAMP binding pocket of Vfr may accommodate additional cyclic nucleotides. In this study, we used two different approaches to generate apo-Vfr and examined its ability to bind a representative set of virulence gene promoters in the absence and presence of different allosteric effectors. Of the cyclic nucleotides tested, only cAMP was able to restore DNA binding activity to apo-Vfr. In contrast, cGMP was capable of inhibiting cAMP-Vfr DNA binding. Further, we demonstrate that vfr expression is autoregulated and cAMP dependent and involves Vfr binding to a previously unidentified site within the vfr promoter region. Using a combination of in vitro and in vivo approaches, we show that cAMP is required for Vfr-dependent regulation of a specific subset of virulence genes. In contrast, we discovered that Vfr controls expression of the lasR promoter in a cAMP-independent manner. In summary, our data support a model in which Vfr controls virulence gene expression by distinct (cAMP-dependent and -independent) mechanisms, which may allow P. aeruginosa to fine-tune its virulence program in response to specific host cues or environments.
Vfr is a global regulator of virulence factor expression in the human pathogen Pseudomonas aeruginosa. Although indirect evidence suggests that Vfr activity is controlled by cyclic AMP (cAMP), it has been hypothesized that the putative cAMP binding pocket of Vfr may accommodate additional cyclic nucleotides. In this study, we used two different approaches to generate apo-Vfr and examined its ability to bind a representative set of virulence gene promoters in the absence and presence of different allosteric effectors. Of the cyclic nucleotides tested, only cAMP was able to restore DNA binding activity to apo-Vfr. In contrast, cGMP was capable of inhibiting cAMP-Vfr DNA binding. Further, we demonstrate that vfr expression is autoregulated and cAMP dependent and involves Vfr binding to a previously unidentified site within the vfr promoter region. Using a combination of in vitro and in vivo approaches, we show that cAMP is required for Vfr-dependent regulation of a specific subset of virulence genes. In contrast, we discovered that Vfr controls expression of the lasR promoter in a cAMP-independent manner. In summary, our data support a model in which Vfr controls virulence gene expression by distinct (cAMP-dependent and -independent) mechanisms, which may allow P. aeruginosa to fine-tune its virulence program in response to specific host cues or environments.
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       
Author Evan D. Brutinel
Matthew C. Wolfgang
Nanette B. Fulcher
Erin L. Fuchs
Mark L. Urbanowski
Timothy L. Yahr
Adriana K. Jones
AuthorAffiliation Cystic Fibrosis/Pulmonary Research and Treatment Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, 1 Department of Microbiology, University of Iowa, Iowa City, Iowa 52242, 2 Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599 3
AuthorAffiliation_xml – name: Cystic Fibrosis/Pulmonary Research and Treatment Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, 1 Department of Microbiology, University of Iowa, Iowa City, Iowa 52242, 2 Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599 3
Author_xml – sequence: 1
  givenname: Erin L.
  surname: Fuchs
  fullname: Fuchs, Erin L.
  organization: Cystic Fibrosis/Pulmonary Research and Treatment Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599
– sequence: 2
  givenname: Evan D.
  surname: Brutinel
  fullname: Brutinel, Evan D.
  organization: Department of Microbiology, University of Iowa, Iowa City, Iowa 52242
– sequence: 3
  givenname: Adriana K.
  surname: Jones
  fullname: Jones, Adriana K.
  organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599
– sequence: 4
  givenname: Nanette B.
  surname: Fulcher
  fullname: Fulcher, Nanette B.
  organization: Cystic Fibrosis/Pulmonary Research and Treatment Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599
– sequence: 5
  givenname: Mark L.
  surname: Urbanowski
  fullname: Urbanowski, Mark L.
  organization: Department of Microbiology, University of Iowa, Iowa City, Iowa 52242
– sequence: 6
  givenname: Timothy L.
  surname: Yahr
  fullname: Yahr, Timothy L.
  organization: Department of Microbiology, University of Iowa, Iowa City, Iowa 52242
– sequence: 7
  givenname: Matthew C.
  surname: Wolfgang
  fullname: Wolfgang, Matthew C.
  organization: Cystic Fibrosis/Pulmonary Research and Treatment Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599
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Issue 14
Keywords Pseudomonadales
Virulence
Cyclic AMP
Bacteria
Pseudomonadaceae
Pseudomonas aeruginosa
Mechanism
Language English
License CC BY 4.0
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Present address: Infectious Diseases, Novartis Institutes for BioMedical Research, Cambridge, MA 02139.
E.L.F. and E.D.B. contributed equally to this work.
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SSID ssj0014452
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Vfr is a global regulator of virulence factor expression in the human pathogen Pseudomonas aeruginosa . Although indirect evidence suggests that Vfr activity...
Vfr is a global regulator of virulence factor expression in the human pathogen Pseudomonas aeruginosa. Although indirect evidence suggests that Vfr activity is...
Vfr is a global regulator of virulence factor expression in the human pathogen Pseudomonas aeruginosa . Although indirect evidence suggests that Vfr activity...
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StartPage 3553
SubjectTerms Amino Acid Sequence
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriology
Base Sequence
Biological and medical sciences
Cyclic AMP - metabolism
Cyclic AMP Receptor Protein - genetics
Cyclic AMP Receptor Protein - metabolism
DNA, Bacterial
Fundamental and applied biological sciences. Psychology
Gene Expression Regulation, Bacterial - physiology
Microbiology
Miscellaneous
Molecular Biology of Pathogens
Molecular Sequence Data
Promoter Regions, Genetic
Protein Binding
Pseudomonas aeruginosa
Pseudomonas aeruginosa - genetics
Pseudomonas aeruginosa - metabolism
Virulence Factors - genetics
Virulence Factors - metabolism
Title The Pseudomonas aeruginosa Vfr Regulator Controls Global Virulence Factor Expression through Cyclic AMP-Dependent and -Independent Mechanisms
URI http://jb.asm.org/content/192/14/3553.abstract
https://www.ncbi.nlm.nih.gov/pubmed/20494996
https://www.proquest.com/docview/733457857
https://www.proquest.com/docview/754869475
https://pubmed.ncbi.nlm.nih.gov/PMC2897347
Volume 192
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