In Vitro and In Vivo Characterization of the Pseudomonas aeruginosa Cyclic AMP (cAMP) Phosphodiesterase CpdA, Required for cAMP Homeostasis and Virulence Factor Regulation

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Published in	Journal of Bacteriology Vol. 192; no. 11; pp. 2779 - 2790
Main Authors	FUCHS, Erin L, BRUTINEL, Evan D, KLEM, Erich R, FEHR, Anthony R, YAHR, Timothy L, WOLFGANG, Matthew C
Format	Journal Article
Language	English
Published	Washington, DC American Society for Microbiology 01.06.2010 American Society for Microbiology (ASM)
Subjects	3',5'-Cyclic-AMP Phosphodiesterases - chemistry 3',5'-Cyclic-AMP Phosphodiesterases - genetics 3',5'-Cyclic-AMP Phosphodiesterases - metabolism ADP Ribose Transferases - genetics ADP Ribose Transferases - metabolism Amino Acid Sequence Bacteria Bacterial Proteins - chemistry Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Toxins - genetics Bacterial Toxins - metabolism Bacteriology Biochemistry Biological and medical sciences Blotting, Western Chromatography, Gel Cyclic AMP - metabolism Cyclic AMP Receptor Protein - genetics Cyclic AMP Receptor Protein - metabolism DNA Footprinting Electrophoretic Mobility Shift Assay Eukaryotes Exotoxins - genetics Exotoxins - metabolism Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Regulation, Bacterial - genetics Gene Expression Regulation, Bacterial - physiology Homeostasis Iron - metabolism Microbiology Miscellaneous Molecular Sequence Data Peptide Hydrolases - genetics Peptide Hydrolases - metabolism Prokaryotes Pseudomonas aeruginosa Pseudomonas aeruginosa - enzymology Pseudomonas aeruginosa - genetics Pseudomonas aeruginosa - metabolism Pseudomonas aeruginosa Exotoxin A Sequence Homology, Amino Acid Signal Transduction Virulence Factors - genetics Virulence Factors - metabolism Pseudomonadales Virulence Cyclic AMP Homeostasis Bacteria Pseudomonadaceae Pseudomonas aeruginosa In vitro
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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	Cyclic AMP (cAMP) is an important second messenger signaling molecule that controls a wide variety of eukaryotic and prokaryotic responses to extracellular cues. For cAMP-dependent signaling pathways to be effective, the intracellular cAMP concentration is tightly controlled at the level of synthesis and degradation. In the opportunistic human pathogen Pseudomonas aeruginosa, cAMP is a key regulator of virulence gene expression. To better understand the role of cAMP homeostasis in this organism, we identified and characterized the enzyme CpdA, a putative cAMP phosphodiesterase. We demonstrate that CpdA possesses 3',5'-cAMP phosphodiesterase activity in vitro and that it utilizes an iron-dependent catalytic mechanism. Deletion of cpdA results in the accumulation of intracellular cAMP and altered regulation of P. aeruginosa virulence traits. Further, we demonstrate that the cAMP-dependent transcription factor Vfr directly regulates cpdA expression in response to intracellular cAMP accumulation, thus providing a feedback mechanism for controlling cAMP levels and fine-tuning virulence factor expression. Cyclic AMP (cAMP) is an important second messenger signaling molecule that controls a wide variety of eukaryotic and prokaryotic responses to extracellular cues. For cAMP-dependent signaling pathways to be effective, the intracellular cAMP concentration is tightly controlled at the level of synthesis and degradation. In the opportunistic human pathogen Pseudomonas aeruginosa, cAMP is a key regulator of virulence gene expression. To better understand the role of cAMP homeostasis in this organism, we identified and characterized the enzyme CpdA, a putative cAMP phosphodiesterase. We demonstrate that CpdA possesses 3',5'-cAMP phosphodiesterase activity in vitro and that it utilizes an iron-dependent catalytic mechanism. Deletion of cpdA results in the accumulation of intracellular cAMP and altered regulation of P. aeruginosa virulence traits. Further, we demonstrate that the cAMP-dependent transcription factor Vfr directly regulates cpdA expression in response to intracellular cAMP accumulation, thus providing a feedback mechanism for controlling cAMP levels and fine-tuning virulence factor expression. [PUBLICATION ABSTRACT] Cyclic AMP (cAMP) is an important second messenger signaling molecule that controls a wide variety of eukaryotic and prokaryotic responses to extracellular cues. For cAMP-dependent signaling pathways to be effective, the intracellular cAMP concentration is tightly controlled at the level of synthesis and degradation. In the opportunistic human pathogen Pseudomonas aeruginosa, cAMP is a key regulator of virulence gene expression. To better understand the role of cAMP homeostasis in this organism, we identified and characterized the enzyme CpdA, a putative cAMP phosphodiesterase. We demonstrate that CpdA possesses 3',5'-cAMP phosphodiesterase activity in vitro and that it utilizes an iron-dependent catalytic mechanism. Deletion of cpdA results in the accumulation of intracellular cAMP and altered regulation of P. aeruginosa virulence traits. Further, we demonstrate that the cAMP-dependent transcription factor Vfr directly regulates cpdA expression in response to intracellular cAMP accumulation, thus providing a feedback mechanism for controlling cAMP levels and fine-tuning virulence factor expression.Cyclic AMP (cAMP) is an important second messenger signaling molecule that controls a wide variety of eukaryotic and prokaryotic responses to extracellular cues. For cAMP-dependent signaling pathways to be effective, the intracellular cAMP concentration is tightly controlled at the level of synthesis and degradation. In the opportunistic human pathogen Pseudomonas aeruginosa, cAMP is a key regulator of virulence gene expression. To better understand the role of cAMP homeostasis in this organism, we identified and characterized the enzyme CpdA, a putative cAMP phosphodiesterase. We demonstrate that CpdA possesses 3',5'-cAMP phosphodiesterase activity in vitro and that it utilizes an iron-dependent catalytic mechanism. Deletion of cpdA results in the accumulation of intracellular cAMP and altered regulation of P. aeruginosa virulence traits. Further, we demonstrate that the cAMP-dependent transcription factor Vfr directly regulates cpdA expression in response to intracellular cAMP accumulation, thus providing a feedback mechanism for controlling cAMP levels and fine-tuning virulence factor expression. 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 Cyclic AMP (cAMP) is an important second messenger signaling molecule that controls a wide variety of eukaryotic and prokaryotic responses to extracellular cues. For cAMP-dependent signaling pathways to be effective, the intracellular cAMP concentration is tightly controlled at the level of synthesis and degradation. In the opportunistic human pathogen Pseudomonas aeruginosa , cAMP is a key regulator of virulence gene expression. To better understand the role of cAMP homeostasis in this organism, we identified and characterized the enzyme CpdA, a putative cAMP phosphodiesterase. We demonstrate that CpdA possesses 3′,5′-cAMP phosphodiesterase activity in vitro and that it utilizes an iron-dependent catalytic mechanism. Deletion of cpdA results in the accumulation of intracellular cAMP and altered regulation of P. aeruginosa virulence traits. Further, we demonstrate that the cAMP-dependent transcription factor Vfr directly regulates cpdA expression in response to intracellular cAMP accumulation, thus providing a feedback mechanism for controlling cAMP levels and fine-tuning virulence factor expression.
Author	Erich R. Klem Evan D. Brutinel Anthony R. Fehr Matthew C. Wolfgang Erin L. Fuchs Timothy L. Yahr
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
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SubjectTerms	3',5'-Cyclic-AMP Phosphodiesterases - chemistry 3',5'-Cyclic-AMP Phosphodiesterases - genetics 3',5'-Cyclic-AMP Phosphodiesterases - metabolism ADP Ribose Transferases - genetics ADP Ribose Transferases - metabolism Amino Acid Sequence Bacteria Bacterial Proteins - chemistry Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Toxins - genetics Bacterial Toxins - metabolism Bacteriology Biochemistry Biological and medical sciences Blotting, Western Chromatography, Gel Cyclic AMP - metabolism Cyclic AMP Receptor Protein - genetics Cyclic AMP Receptor Protein - metabolism DNA Footprinting Electrophoretic Mobility Shift Assay Eukaryotes Exotoxins - genetics Exotoxins - metabolism Fundamental and applied biological sciences. Psychology Gene expression Gene Expression Regulation, Bacterial - genetics Gene Expression Regulation, Bacterial - physiology Homeostasis Iron - metabolism Microbiology Miscellaneous Molecular Sequence Data Peptide Hydrolases - genetics Peptide Hydrolases - metabolism Prokaryotes Pseudomonas aeruginosa Pseudomonas aeruginosa - enzymology Pseudomonas aeruginosa - genetics Pseudomonas aeruginosa - metabolism Pseudomonas aeruginosa Exotoxin A Sequence Homology, Amino Acid Signal Transduction Virulence Factors - genetics Virulence Factors - metabolism
Title	In Vitro and In Vivo Characterization of the Pseudomonas aeruginosa Cyclic AMP (cAMP) Phosphodiesterase CpdA, Required for cAMP Homeostasis and Virulence Factor Regulation
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